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Animal Husbandry

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Animal Husbandry is commonly defined as a branch of agriculture dealing with the domestication, breeding, and rearing of animals for various purposes including labor (as in the case of large animals), a food source, protection, and companionship (as with dogs, primarily), and a source of material goods such as hides and bones, used for clothing and tools.

The domestication of animals is dated to the First Agricultural Revolution of c. 10,000 BCE, though probably began much earlier, and significantly changed how people lived. Prior to the domestication of animals, human communities revolved around the hunter-gatherer paradigm in which wild animals were hunted and plant life gathered; afterwards, domesticated animals and plants encouraged the establishment of permanent settlements with resources at hand for the needs of the people.

The first animals domesticated were dogs, used for hunting, protection, and companionship, with sheep and goats probably next and then other animals such as chickens. Larger animals, like horses and oxen, were likely domesticated after smaller ones. Herbivores were chosen because they could live off the land, and it is for this reason that scholars maintain domestication of plant life must have preceded that of animals - there needed to be a reliable food source in order for the animal population to thrive – though this claim has been challenged.

Once established, animal husbandry is understood to have benefited humans in many ways but also to have raised the standard of living of animals who were now protected and cared for. Beginning in the 18th and 19th century (though there are earlier examples), this claim was challenged by animal rights activists, who argue that animal husbandry benefits humans to the detriment of animals and the environment, it has come to be driven by profit without regard for the welfare of animals, and continued commercial animal husbandry in the modern age is ultimately unsustainable.

Pathways to Domestication

The English word 'domestication' comes from the Latin domesticus referring to the home ("belonging to the house") while husbandry means "to care for" or "manage prudently," and, applied to animals, is the care for, breeding, and management of formerly wild species of animals by human beings. It is thought that the domestication of animals was encouraged by climate change following the last Ice Age c. 21,000 years ago which dispersed game and forced people to travel greater distances to hunt and forage for food. Seeds dropped from plant life they foraged, it is thought, were observed to sprout, encouraging the intentional planting of such seeds and the beginning of agriculture.

Dogs are thought to have already been domesticated in Europe by this time as their dates have been determined at roughly 32,000-18,800 years ago, with the earlier time period favored. Dogs are thought to have developed from the Asian wolf and the European grey wolf, and while which was domesticated first continues to be debated, it is likely that the Asian wolf was first and was then transported to Europe where these now-domesticated animals might have encouraged the European wolves to trust and draw near to human communities – though this claim is speculative and has been challenged.

It is impossible to know for certain how the first animals were domesticated, but geneticists and scholars have developed various theories which have been accepted as reasonably sound. Scholar Melinda A. Zeder, for example, in her Pathways to Animal Domestication , outlines the three routes taken in the domestication of animals which is widely accepted by the academic community:

• Commensal Pathway: Habituation – Partnership – Directed Breeding
• Prey Pathway: Prey – Game Management – Herd Management – Breeding
• Directed Pathway: Competitor – Prey – Control – Directed Breeding

In the Commensal Pathway, the animal becomes used to humans by association. Wolves, for example, were most likely domesticated through their attraction to the bones or offal of a community's garbage pit or, perhaps, by scraps thrown to them. In time, the wolves were habituated to humans, entered into a mutually beneficial partnership, and were then directly bred for different purposes. Cats would have followed this same pathway to domestication.

Prey Pathway refers to animals such as horses, cattle, sheep, and goats which were initially human prey. These animals would have been domesticated individually, eventually becoming managed as herds and, again, subject to directed breeding according to human needs. The former prey, after domestication, becomes a partner in the human community and, again, is understood as benefitting as much from the relationship as humans.

Directed Pathway concerns animals who were formerly competitors for prey or were prey themselves (such as horses, donkeys, camels, and elephants, among others) who are brought under human control and then bred for specific purposes. In the case of the elephant, this would have been for labor, hunting, warfare , or entertainment as evidenced by their use in the arenas of ancient Rome . Zeder comments:

This fast-track to domestication begins when humans use knowledge gained from the management of already domesticated animals to domesticate a wild species that possesses a resource or a set of resources that humans see as desirable. (246)

It is thought that, after the domestication of the dog, humans used the same kinds of approaches in attracting and domesticating other animals.

Ancient Domestication

As Zeder notes, the path to domestication neither did always proceed quickly nor was the sedentary, agrarian lifestyle instantly embraced by hunter-gatherer communities. The evolution from nomadic hunters to sedentary farmers and animal breeders was a slow process. Scholar Marc van de Mieroop comments:

There was not a sudden change from hunting-gathering to farming, but rather a slow process during which people increased their reliance on resources they managed directly, but still supplemented their diets by hunting wild animals. Agriculture enabled an increase in continuous settlement by people. (12)

In Mesopotamia , the domestication of plants and animals was already established by c. 10,000 BCE. Excavations of refuse dumps outside of Mesopotamian towns and cities have shown a gradual decline in the number of wild gazelle bones after 7000 BCE (which, it has been suggested, shows a depletion of wild game) while the number of domesticated sheep and goat bones grows in number. Scholars have determined that these sheep and goats were domesticated, and not wild, based upon the condition of the bones and, of course, on inscriptions and artwork.

It is thought likely that wild sheep and goats came to graze around human settlements in an attempt to escape from natural predators who would have avoided contact with humans. In time, these animals grew increasingly tame and became an easily accessible source of food, following the route of Zeder's Prey Pathway. Wheat was domesticated and in wide use in Mesopotamia by 7700 BCE, goats by 7000 BCE, sheep by 6700 BCE, and pigs by 6500 BCE. By the time of the establishment of the city of Eridu in 5400 BCE, animal husbandry was widely practiced, and domesticated animals were used in the workforce (such as in plowing), as pets, and as a food source. Horses were tamed by 4000 BCE and, in time, became an important component in warfare.

This same basic pattern has been determined in the regions of the Indus Valley Civilization , Egypt , and China . In the Indus Valley , plants and animals were domesticated by the time of the pre-Harappan period (c. 7000 to c. 5500 BCE), and domestication was established prior to the Predynastic Period in Egypt (c. 6000 to c. 3150 BCE) and prior to the foundation of Banpo Village in China (c. 4500-3750 BCE) where they kept domesticated dogs and pigs.

At roughly the same time, humans in other parts of the world were engaged in the same practice. In the Americas, during the Archaic Stage (8000-1000 BCE) permanent settlements were established as plants and animals were domesticated. The Caral-Supe civilization , the oldest in the Americas (in modern-day Peru), was already cultivating the 'three sisters' of squash, beans, and corn, as well as other vegetables, and had domesticated the llama as a pack animal prior to 3000 BCE. The Olmec civilization , the Maya , the Aztec Empire , and others followed the same model as did those to the north of them who established the great cultural centers such as Cahokia and Poverty Point .

Domestication of plants and animals produced a dramatic change in the way people lived. Civilizations that had relied on hunting and gathering as a means of subsistence now built permanent settlements and engaged in a pastoral existence relying on their cattle and crops. The Agricultural Revolution, in fact, is considered the starting point for civilization as it enabled the five aspects which define that concept:

• surplus food
• division of labor
• urbanization
• a writing system

Further, once people realized that animals could be tamed, the creatures became incorporated into the most basic and widespread rituals of the culture , notably in religious rites as sacrificial offerings or as representatives of the gods and the concept of order.

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Domestication & Order

In Mesopotamia, Egypt, and other civilizations, the gods were associated with the establishment of order. In time, the domestication of animals seems to have acquired the same meaning. Humans, as co-workers with the gods in maintaining the ordered world, were doing their part in taming that which had been wild and bringing it under their control.

Worship of animals in Egypt is well known, most notably their reverence for the cat, associated with the goddess of the hearth and home, Bastet , but many ancient cultures incorporated animal imagery into their religious icons and practices. Wild animals came to represent untamed forces in the universe (such as the lions of the goddess Inanna in Mesopotamia), while domesticated creatures symbolized comfort and security (for example, the dog in Greece and Rome). In India , according to scholar Will Durant:

There was no real gap between animals and men; animals as well as men had souls and souls were perpetually passing from men into animals and back again; all these species were woven into one infinite web of karma and reincarnation. The elephant, for example, became the god Ganesha , and was recognized as Shiva 's son; he personified man's animal nature and, at the same time, his image served as a charm against evil fortune. (509)

Hinduism , Jainism , and Buddhism all taught the concept of reincarnation and encouraged the belief, as Durant notes, that the souls of animals were of the same eternal substance as those that animated humans. In domesticating animals, people were drawing them from a perilous world of uncertainty to the safety of the human community. The people of the Indus Valley Civilization are thought to have worshipped a Mother Goddess whose male consort is depicted in the company of wild animals, possibly a reference to the gods' approval of their domestication or of the gods offering protection against elements beyond human control. The domesticated animal came to symbolize order as opposed to the chaos of the untamed world.

Animal husbandry, as defined specifically as care for animals, reached its height in the ancient world in Egypt where cats and dogs were cared for as though they were part of the human family in which they lived. Mummies of cats and dogs have been discovered in tombs in Egypt, and so deeply did the Egyptians feel for their cats, Herodotus notes, that they would shave their eyebrows and form a funeral procession of mourning upon the death of one of these pets. Other animals were also mourned as fully as any family member, and this practice was later observed in Greece and Rome where monuments to departed pets were erected.

Once domesticated, animals became a part of the human story, and just as people labored in the service of the gods, so animals served people. Scholar Stephen Bertman comments:

In ancient Mesopotamia, the most important domesticated animals were oxen and donkeys, on the one hand, and sheep and cattle on the other. The former served as draught animals; the latter were raised for their milk and for hides and wool that could be converted into clothing…Farmyards also included ducks and geese raised for their eggs and meat…and there is evidence that the ancient Mesopotamians raised pigs. (246)

Animals were bred to serve these and many other purposes in ancient Mesopotamia but were also directly linked with divinity just as they may have been in the Indus Valley. Gula , the Sumerian goddess of healing, is routinely depicted in the company of a dog, and they often appear as amulets for protection. This same paradigm holds for Mesoamerica where animals were associated with the divine, especially dogs who were thought to be able to safely conduct the souls of the dead to paradise.

At the same time that dogs, and other animals, were associated with divinity, they were kept as a food source and understood primarily as utilities in the service of humanity. An interesting observation to come from the field of genomic archaeology is how selective breeding of domesticated animals changed the various species. The floppy ears of rabbits, sheep, and certain breeds of dogs are the result of directed breeding by humans through which floppy ears came to be a sign of submission. Spots or other defining markings on animals including cats, cows, dogs, goats, horses, and rabbits seem to be an inadvertent consequence of directed breeding.

Animals were bred to retain favorable characteristics (such as attention-seeking and adaptability to changes in the environment) and eliminate unfavorable ones (including difficulty in adapting and wariness of humans). Zeder notes how "in all domesticated animals, the single most important behavioral response to domestication is reduced wariness and low reactivity to external stimuli" (232). This reduction in wariness seems to correspond to a reduction in brain size as Zeder observes that domesticated animals experienced a significant reduction in brain mass when compared to those in the wild and how silver foxes, bred for tameness, "experienced a reduction in cranial height and width, and by inference in brain size, after only 40 years of intensive breeding" (233).

In the 18th and 19th centuries, there was a reaction against the practice of breeding and keeping domesticated animals, focusing on the claim that animals had the right to live their own lives naturally and should not be made to serve humanity. British philosopher Jeremy Bentham (l. 1748-1832) rejected the domestication of animals as unethical in that it led to their suffering and deprived them of the kind of life they were supposed to live. This claim is echoed by animal rights activists of the present day such as Peter Singer, Liz White, and guitarist Brian May, among many others.

At this point, it seems unlikely the paradigm is going to change, and so many modern activists advocate not for the abolition of keeping domesticated animals but for the more humane and ethical treatment of them in businesses such as commercial factory farming. These activists, and others not directly associated with animal rights per se, note that present policies directing the use of domesticated animals contribute directly to climate change – most notably those concerning cattle – and are unsustainable for humans, the environment, and the animals themselves.

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Bibliography

• Bertman, S. Handbook to Life in Ancient Mesopotamia. Oxford University Press, 2005.
• Dogs first domesticated in Europe, study says | CNN , accessed 22 Oct 2022.
• Durant, W. Our Oriental Heritage. Simon & Schuster, 2010.
• Leick, G. The A to Z of Mesopotamia. Scarecrow Press, 2010.
• Scarre, C. & Fagan, B.F. Ancient Civilizations. Pearson, 2010.
• Singer, P. Ethics Into Action. Rowman & Littlefield Publishers, 2000.
• Van De Mieroop, M. A History of the Ancient Near East, ca. 3000-323 BC. Wiley-Blackwell, 2015.
• Zeder, M. A. "Pathways to Animal Domestication." Biodiversity in Agriculture , 2012, pp. 229-259.

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Mark, J. J. (2022, October 26). Animal Husbandry . World History Encyclopedia . Retrieved from https://www.worldhistory.org/Animal_Husbandry/

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Mark, Joshua J.. " Animal Husbandry ." World History Encyclopedia . Last modified October 26, 2022. https://www.worldhistory.org/Animal_Husbandry/.

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Article Contents

Introduction, how husbandry variables can impact study outcome, husbandry-related cycles, in-house transport, physicochemical environment, material-related issues, social aspects, conclusions.

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Animal Husbandry and Experimental Design

Timo Nevalainen, DVM, MS, PhD is an Emeritus Professor in the Laboratory Animal Center of the University of Eastern Finland, Kuopio Campus, Finland.

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Timo Nevalainen, Animal Husbandry and Experimental Design, ILAR Journal , Volume 55, Issue 3, 2014, Pages 392–398, https://doi.org/10.1093/ilar/ilu035

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If the scientist needs to contact the animal facility after any study to inquire about husbandry details, this represents a lost opportunity, which can ultimately interfere with the study results and their interpretation. There is a clear tendency for authors to describe methodological procedures down to the smallest detail, but at the same time to provide minimal information on animals and their husbandry. Controlling all major variables as far as possible is the key issue when establishing an experimental design. The other common mechanism affecting study results is a change in the variation. Factors causing bias or variation changes are also detectable within husbandry. Our lives and the lives of animals are governed by cycles: the seasons, the reproductive cycle, the weekend-working days, the cage change/room sanitation cycle, and the diurnal rhythm. Some of these may be attributable to routine husbandry, and the rest are cycles, which may be affected by husbandry procedures. Other issues to be considered are consequences of in-house transport, restrictions caused by caging, randomization of cage location, the physical environment inside the cage, the acoustic environment audible to animals, olfactory environment, materials in the cage, cage complexity, feeding regimens, kinship, and humans. Laboratory animal husbandry issues are an integral but underappreciated part of investigators' experimental design, which if ignored can cause major interference with the results. All researchers should familiarize themselves with the current routine animal care of the facility serving them, including their capabilities for the monitoring of biological and physicochemical environment.

If the scientist needs to contact the animal facility after the study is completed and inquire about husbandry details to be included in the manuscript, it is obvious that there has not been proper emphasis placed on animal husbandry-related issues in the experimental design. Unless agreed otherwise, all facilities follow their own animal care routines, which may not be suitable or include the best choices for individual studies. It may be possible to obtain information on this routine care afterwards, but study-specific details, e.g., when the cages were changed, the location of cages in the rack, and any aberrations in environment may no longer be available. This is an opportunity lost and can ultimately interfere with the study results and their interpretation. Contacts with the animal facility personnel to include and plan husbandry-related aspects should be established well ahead of the study.

An original article communicates results to the scientific community; therefore, it is absolutely necessary that the article contains a complete description of the study under comparable conditions, preferably following ARRIVE guidelines ( Kilkenny et al. 2010 ) to help fellow scientists design future investigations. An article not revealing all the essential pieces of information becomes impossible to repeat with the same results, yet repeatability is one of the key qualities that all scientists seek. There is a clear tendency for researchers to describe procedures, chemicals, reagents, and statistics down to the smallest detail, yet at the same time provide minimal information on animals and their husbandry ( Alfaro 2005 ; Everitt and Foster 2004 ; Gerdin et al. 2012 ).

The most common animal study type deals with interference with the natural order of events and carefully observing the consequences. The importance stems from the quest for inference, i.e., what is produced, contributed to, or caused without ambiguity. In the end, the authors must be able to rule out all possible alternate causes for the results they have obtained. Husbandry issues should be included as essential parts of this process.

There are several recent guidelines available to describe animals and their husbandry ( Alfaro 2005 ; Brattelid and Smith 2000 ; Hooijmans et al. 2010 ; Kilkenny et al. 2010 ; National Research Council (US) Institute for Laboratory Animal Research 2011 ). Some are based on surveys of the existing situation, while others provide reasons or lists of items to be described. A closer look at the surveys assessing the quality of design reveals that there are common deficiencies in design, such as lack of description of randomization and bias ( Kilkenny et al. 2009 ; McCance 1995 ; Perel et al. 2007 ). Although the primary focus of randomization is on random allocation of the animals to the groups, it is feasible to assume that the same deficiencies are true for husbandry-related experimental design items.

Controlling all major variables as far as possible is the key issue when establishing an experimental design, i.e., the only difference between the study and control groups is the procedure and nothing else. Any remaining variation can be controlled by randomizing the treatments to the animals. This applies to all aspects of the design, e.g., procedures under study and everything influencing the lives of the animals and to what they are exposed.

Bias is any systematic difference between the groups in addition to the procedure in the study design. No one would purposely incorporate bias into their design, yet it may be introduced because several aspects have not been properly considered or understood or the possibility has been totally ignored. A simple example of a bias is a study examining the effects of ethanol on animals through offering 10% ethanol in the drinking water. In reality, this design evaluates the combined effects of ethanol, eating less, and drinking less; the latter because animals tend to drink less fluid and ethanol provides a considerable amount of calories and eating is calorie guided.

The other common mechanism affecting study results is a change in variation; sources of variation in animal study in relation to husbandry and beyond have been analyzed by Howard (2002) . An increase in the background noise makes statistical significance more difficult to attain or it may require more animals. Consequently, a decrease in variation will have the opposite effect. Husbandry-related variation effects are traceable to disturbances in animals' lives, such as disease, transportation or cage change, or simply exposure to a fluctuating or changing physicochemical environment. In principle, a change in variation can be caused by any husbandry variable, though some are more likely candidates than others. While establishing an experimental design for an experiment, it is important to invest adequate time for the identification of such factors and building up effective strategies to cope with them. The aim of this paper is to elucidate selected animal housing and care-related items with examples and discuss their potential to interfere with the experimental design.

Animal life follows many different cycles, including the seasonal cycle, reproductive cycle, weekend-working days cycle, cage change /room sanitation cycle, and diurnal cycle. Some of these are actually established by the routine husbandry, and the rest are cycles that are sensitive to husbandry procedures.

Seasonal Cycle

Animals are capable of sensing the season even when housed in windowless rooms with programmed photoperiods and with a tightly regulated physicochemical environment. For example, there are reports of seasonal variation of immunoreactivity in models of septic shock and immunosuppression induced by chronic stress in 2 strains of mice. Kiank et al. (2007) showed that mice living with a 12:12-hour photoperiod had an enhanced risk to die of peritonitis in the summer or autumn compared with the other seasons. This is a situation where a control group may offer a solution to this problem. Theoretically, there is no other way to counteract seasonal variation other than to always carry out the study during the same season, yet even seasons are not alike and this approach as such may not be practical.

Reproductive Cycle

In rodents, the female reproductive cycle is sensitive to the pheromones present in male urine. Classical examples of this are the Whitten effect; male pheromones synchronizing estrus in females, the Lee–Boot effect; suppression or prolongation of estrous cycles of mature females when they are housed in groups and isolated from male mice, and the Bruce effect, which refers to the tendency for female rodents to terminate their pregnancies following exposure to the scent of an unfamiliar male.

Controlling spread of odors within a room, if not to the whole facility, is problematic; this is possible only if ventilation of the test enclosure is separated from the rest of the animals. In other situations, all persons visiting animal rooms should wash their hands with unscented soap and change protective clothing between the rooms ( Wersinger and Martin 2009 ).

Weekend-Working Days Cycle

During the weekend, fewer people are present in the animal facility; there is less human activity and hence a reduced acoustic environment audible to animals in the animal rooms. This change does not go unnoticed by the animals. Whether this represents a better time window for sampling and recording is a study-specific question.

For instance, this cycle causes change in blood pressure, which is a parameter commonly recorded in research. By using telemetric methods, which allow continuous recording of freely moving animals, it has been shown that spontaneous locomotor activity and blood pressure in the working days in rats are higher than during weekends. Apart from the increased locomotor activity (33%, p < 0.001), the daytime blood pressure differences were small (3.7–4.2 mmHg, p < 0.05) yet large enough to complicate the interpretation of study results ( Schreuder et al. 2007 ).

In most animal facilities, sound levels are low during the weekends, suggesting that human activities are a very important source of sound ( Milligan et al. 1993 ). Every facility has its own weekend environment, and all weekends are not exact replicas of the previous ones. For the purposes of experimental design, this possible confounding effect has to be discussed with the facility personnel to decide whether to conduct samplings all through 7 days a week, or to use either working days or weekends, keeping in mind that there may be other disturbing factors that one may prefer to avoid.

Cage Change and Room Sanitation Cycle

Cage changes and room sanitation represent major exposures for laboratory animals. The key question here is how long the animals are disturbed and what is the magnitude and nature of the disturbance, starting from preparations and in particular after the cage change, when the animals are not suitable for sampling or recording. Another solution is to find and use appropriate husbandry procedures to replicate the previous physiological state.

Rats housed in their home cages display increased locomotive activity, bedding manipulation, and defecation in both the mornings and afternoons of cage change days. This behavioral effect is greater than that of time of day and lasts for several hours after the cage change ( Saibaba et al. 1996 ). Likewise in rats, the cage change results in elevations in heart rate and mean arterial pressure levels lasting for up to 5 hours after the procedure. The reactions observed after cage change were significantly greater than those observed after simple handling, handling being part of the cage change process ( Meller et al. 2011 ).

In mice, postcleaning activity also includes aggression, which can cause serious injuries ( Van Loo et al. 2004 ). In C57BL6/NTac mice, the cage change increased systolic blood pressure, heart rate, and locomotor activity; in females, these changes lasted about 100 minutes, while in males the effect duration was about 20 to 25% shorter, irrespective of change frequency (weekly vs . fortnightly) ( Gerdin et al. 2012 ). It seems safe to recommend that no manipulation, dosing, sampling, or recording of animals should be done during the cage change day or the following day. For sensitive behavioral experiments, an even longer timescale may be necessary.

In studies on social behavior, the routine frequency of cage cleaning can be deleterious by disrupting its environment, including scent marks (pheromones), nests, and hoarded food. Cage cleaning and sanitation processes can also alter a rodent's normal production of pheromones and thus may affect behavior. To prevent pheromonal interference and stress-induced pheromonal release in their research subjects, experimenters should assess their current laboratory protocols regarding cage cleaning processes, housing designs, and behavioral assays. The lowest possible frequency would avoid unnecessary stress to animals ( Wersinger and Martin 2009 ).

There is evidence that transfer of specific olfactory cues during cage cleaning and the provision of nesting material can decrease aggression and stress in group-housed male mice ( Van Loo et al. 2004 ). Removing only the wet soiled bedding from a dirty cage, returning the nest or a portion of soiled bedding, some familiar complexity item, or food hopper with diet to the clean cage might be better options for the animals and the study design ( Bind et al. 2013 ; Meller et al. 2011 ; Wersinger and Martin 2009 ).

Diurnal Cycle

Diurnal rhythm influences many aspects of animal life, and changes seen are more than minute “physiologic” variations around a 24-hour mean. The rhythm has an endogenous nature but is affected by husbandry-related factors such as food, light, stress, and even tinted cage walls, and it also influences in vivo results such as melatonin, total fatty acids, glucose, lactic acid, corticosterone, insulin, and leptin in rats ( Wren et al. 2014 ). In animal care and housing, one should avoid anything that could disrupt the diurnal rhythm, such as malfunctioning or changing photoperiods or practicing common types of restricted feeding ( Chacon et al. 2005 ).

Ideally, samples and recordings should be obtained from freely moving animals, so that they are not aware of the procedure. In most cases, this simply is not possible; hence, samples are ‘contaminated’ with human presence in the room and the handling and sampling method. Moving the animals to another space gives them more time to react compared with the same procedure done in the animal room. For example, when cages of group-housed mice were transported to another room on a wheeled trolley and stored on a mobile ventilated rack during testing, this had no effect on blood glucose, but body temperature increased significantly when compared with nontransported controls. It required one hour of acclimatization for temperature to be restored ( Gerdin et al. 2012 ). Because there are more and less sensitive parameters to be assessed in each study, the study group has to evaluate the optimal location to conduct the procedures.

Current caging systems have been designed primarily with disease control in mind, i.e., materials should be easy to sanitize and sterilize. Complexity items came later; some of them are intended only for single use, some can be used to transfer specific olfactory cues during cage cleaning. Any disease, whether overt or subclinical, can interfere with the investigation in an unpredictable way. Health monitoring is practiced to detect the presence of an animal pathogen as quickly as possible. Depending on the caging system, this may require measures ranging from decontamination of the entire facility to a few cages.

Protection of the animals against pathogenic organisms is crucial to animals, animal center personnel, and investigators. The facility has rules to be followed and obeyed, e.g., restricted access of both animals and humans into the facility, acceptable working practices when inside, and requirements for cleaning of research equipment, instruments, and biological materials, and these must be adhered to while establishing the experimental design.

The investigators should allocate the animals at random into the study groups, and then cages should be placed into the cage rack also at random. An alternative is to incorporate blocking, which would not involve an increase in the number of animals but might provide additional information on analysis. Cages in different locations experience temperature, humidity, and lighting gradients based on cage level, distance to ventilation inlets and exhausts, lighting, and even sound sources. If cages are assigned to cage racks in a systematic manner, these external factors can introduce bias into the statistical analyses. These kinds of effects have been reported, but it is likely that most of these biased results have gone unnoticed ( Herzberg and Lagakos 1992 ).

Animal technicians should be told that cage locations are being randomized and be given the master key to the locations. Unless this is done, the location may accidentally change. There are claims that cage locations should be continuously changed, e.g., at each cage change and that would achieve the same goal as permanent random order. Unfortunately, this is not the case; instead, continuous place change leads to increased variation in parameters sensitive to gradients in the room.

Temperature Humidity and Illumination

All holding and caging systems do not provide similar environments to the animals. In some cages, the physical environment is close to the one in the room, whereas in others the changes can be considerable. As an example, a study by Memarzadeh et al. (2004) compared environmental conditions inside mice cages with 4 different mechanical ventilation designs and a static isolator cage. The static isolator cages were found to have lower air velocity, higher relative humidity, higher NH 3 and CO 2 levels, lower body weight gain, and lower water consumption compared with the mechanically ventilated cages ( Memarzadeh et al. 2004 ). In mice, temperature and humidity variation can affect the age of puberty, i.e., low temperatures and extremely low humidity levels have been shown to delay sexual maturation ( Drickamer 1990 ).

Illumination has been shown to affect the estrous cycle in both in albino and normally pigmented mice. When 2 light intensities (15–20 and 220–290 lux) were used, the estrous cycle of both types of mice was shorter, and the proportion of albino mice from which embryos were recovered was significantly smaller than the proportion from black mice at the lower intensity ( Donnelly and Saibaba 1993 ).

Acoustic Environment

Noise sources are facility specific and include environmental control systems, maintenance and husbandry procedures, cleaning equipment, and other equipment used near to the animals. The sounds cover a wide frequency range, including the ultrasonic ( >20 kHz) frequency that animals but not humans hear. It seems likely that the levels reported can have a negative effect on animal physiology or behavior ( Sales et al. 1999 ). It is rather rare for the facilities to monitor the acoustic environment, especially ultrasounds beyond the range of human hearing. Although background sound levels in undisturbed situations are generally low, marked increases in sound levels often occur during the working days. It is clear that the acoustic environment of laboratory animals is an uncontrolled variable with the potential to interfere with behavioral and physiological experiments ( Milligan et al. 1993 ).

Investigators cannot avoid noise created by HVAC machinery in the facility, but they can try to make best of it. A good starting point is to find out whether the facility has assessed the sounds audible to animals all the time and those created by machinery used intermittently, such as cage and rack washers and autoclaves. Avoiding cage manipulations such as cage change, addition of diet to the cage lid and topping off water bottles ( Voipio et al. 2006 ), all sanitation processes, the presence of other experimenters in the same space, and conducting tests during the weekends are all things to be considered. If there are building construction activities causing noise or vibrations going on nearby, it may be best to avoid any studies at all.

Laboratory animals have a much better developed sense of smell than humans. Therefore, it is no surprise that the olfactory environment is important and any disruption to it carries wide range of consequences to the animals and hence to the study results. For example, changing the cage bedding and/or nesting material at various prescribed intervals results in delayed puberty as compared with nondisrupted control mice ( Drickamer 1990 ). Open-top cages allow the odors to spread from one room to the next unless animals are housed in special conditions, e.g., in an IVC-system or isolators with separate inlet and exhaust air ducts.

Cage Material

Traditionally, the polymers used as cage materials have been considered as being inert. The most common clear material, polycarbonate, has been shown to leach Bisphenol A, a monomer with estrogenic activity. Howdeshell et al. (2003) have shown that this compound becomes a problem once polycarbonate equipment is exposed to high temperatures and alkaline conditions, common procedures in sterilization and washing, and the amount of leaching increases as a function of use. Bisphenol A exposure as a result of being housed in used polycarbonate cages produced a 16% increase in uterine weight in prepubertal female mice relative to females housed in used polypropylene cages; however, it has to be noted that this difference was not statistically significant ( Howdeshell et al. 2003 ). This should be taken as a warning sign; the animals in old cages with bottles or even complexity items made of polycarbonate may be exposed to varying amounts of Bisphenol A, which may interfere with any estrogen-sensitive parameters. The only effective solution is to avoid using polycarbonate cages; other polymer materials are less prone to leaching of this chemical.

Bedding is the material with which the animals have continuous contact. The original observation that softwood bedding contains α- and β-pinene, which are compounds with liver microsomal enzyme induction properties, is quite old but so far it has not been widely implemented ( Vesell 1967 ). This is not the only effect of bedding; several other interfering properties have subsequently been discovered, e.g., measurable amounts of endotoxin and (1– >3)-beta- d -glucan are present in different bedding materials; after 5 weeks' exposure, this evoked moderate inflammatory reactions in the lung of the animals ( Ewaldsson et al. 2002 ).

To exclude bedding interference, one can assay residues in a batch, keep to one batch whenever possible, and, if using softwood bedding, then it is advisable to standardize heat treatments both at the manufacturer's plant and the facility, because heat treatment can decrease the levels of the compounds responsible for enzyme induction ( Nevalainen and Vartiainen 1996 ).

Complexity Items

Adding items and materials into the cage increases the complexity of the intimate environment of the animals. Complexity becomes environmental enrichment once it has been verified to confer a welfare outcome on the animals. However, despite many studies on complexity, there are still major gaps in our understanding, e.g., because of variety of item combinations, lack of applicability beyond one strain or stock of animals, and inappropriate controls.

For the scientist, the most important aspect of complexity is consistency; the added items must be present all of the time and they have to be the same for all animals. In group-housed animals, social hierarchies may influence the use of complexity items. Both the facility and the scientists need to understand that complexity is not an inert object in the cage but a potential variable in the study. Changing the intimate environment of animals has effects on brain structure, physiology, and behavior as well as an influence on which genes are expressed in various organs ( Benefiel et al. 2005 ). It has to be understood that minor complexity changes meant to improve animal welfare may alter the physiology and development of the animals in an unpredictable way. Moreover, there is also the possibility that the complexity preferred by the animals may not enhance laboratory animal welfare and may even interfere with the study ( Benefiel et al. 2005 ; Wersinger and Martin 2009 ). It is important to consider the potential effects of any complexity on welfare of the animal strain in use and, even more importantly, more studies need to be done to obtain more accurate data.

Variability between diet brands is to be expected, but there may be considerable variation between batches of the same diet brand. Consequently, the study parameters will also vary. Keeping to one batch in an experiment is advisable, but in subsequent studies, this may not be possible, and then analysis of at least the critical components affecting the study may be helpful. Because the food deteriorates during storage, the analysis may also be necessary if the duration of the experiment is prolonged.

It is widely known that eating too much is unhealthy, but this is what we routinely offer to our research animals. The drawbacks of ad libitum feeding include an increased variation in food intake and consequently an increased variation in body weight and other variables and increased mortality and shorter lifespan. It is not surprising that ad libitum feeding has been called the least controlled variable in rodent bioassays ( Keenan et al. 1998 ).

Dietary restriction is the solution to these problems, but this can lead to other problems. Dietary restriction in rodents requires single housing in order to provide them with a meal once a day, often during the daytime; this disrupts physiological and behavioral diurnal rhythms and would exert a confounding effect on the investigation ( Chacon et al. 2005 ; Damiola et al. 2000 ; Forestell et al. 2001 ; Nelson 1988 ). For example, in studies with dietary restriction, it is unclear whether the differences observed are due to caloric intake per se or altered diurnal rhythms.

The diet board offers the possibility of combining dietary restriction with group-housing and normal eating rhythms ( Kasanen et al. 2009a , 2009b ). From the point of view of scientific quality, the combination of undisturbed diurnal rhythm and restricted caloric intake in rodents would be a valuable achievement. In rats fed with the diet board, serum ghrelin, blood glucose, and fecal corticosterone and immunoglobulin A have been shown to follow a diurnal rhythm ( Kasanen et al. 2010 ).

Scientists are well aware that with large laboratory animals, family relationship such as sisters and brothers must be evenly distributed to all groups in the study. The same allocation principle is not practiced with small laboratory animals, such as rodents. Although rats and mice look alike and litter data is usually lost at weaning, when the sexes are separated and cages filled to predetermined cage occupancy, nonetheless this may not be the best practice.

Good laboratory practice-guidelines emphasize that the study design should take account of kinship in large animals, but not for rodents. Safety studies with small animals typically include hundreds of animals, whereas in studies with large animals, the numbers are comparable with the numbers of small animals used in basic biomedical research. Rather than tacitly accepting the difference in scale of experimental design, it is worth noticing that it is often logically inconsistent. Indeed, this a question of animal numbers, not of species.

In outbred and other undefined animals, litter effects are large and ignoring them can make replication of the studies difficult, if not impossible. As an example, a recent literature review of the valproic acid model of autism showed that only 9% (3/34) of studies correctly determined that the experimental unit was the litter and therefore had made valid statistical inferences. In fact, litter effects accounted for up to 61% ( p < 0.001) of the variation in behavioral outcomes, a much larger percentage than the treatment effects ( Lazic and Essioux 2013 ).

The need to recognize kinship is clear with outbred animals, but it should not be ignored in inbred and defined animals. Prager et al. (2010) showed that in young outbred rats, maternal care and litter size exerted a profound effect on immune-related parameters. Although inbred animals are genetically identical, their embryonic development and maternal care may not be the same, and hence kinship is an issue to be considered with defined strains of laboratory animals.

Accounting for kinship in rodents becomes a reality only once litter codes are available. In the case of in-house breeding, this should not be too difficult. With major breeders, this must be possible but ordering has to be done earlier than usual. The expected higher cost of animals can be offset by a reduction in the numbers of animals needed and thus less labor. When kinship data are available, animals should be divided into the study groups as evenly as possible following a random block design as presented by Festing et al . (2002) .

Animal technicians, not only the scientists, should be considered as key individuals in the studies. The technicians see and observe the animals at least on a daily basis and consequently have a good understanding of what is normal in these animals and in particular what is not. They are also in charge of daily routines, and the way they deal with the animals can make a profound difference.

There is anecdotal evidence that if rats are moved to a new cage by lifting from the base of the tail, they become aggressive, and that this does not happen if they are lifted by holding the body. Lifting by the base of tail has traditionally been the preferred method for mice, and these animals have been considered aggressive and they do not habituate to handling. A recent article by Hurst and West (2010) has challenged this view using 2 strains and a stock of mice. If the mice were transferred to a new cage in cupped hands or in a transparent tunnel kept in the cage, then their anxiety decreased already after one such transfer. The animals were more tame when receiving administrations using the traditional means of immobilization ( Hurst and West 2010 ).

It was concluded that there is no need to consider handling-induced anxiety in mice, in essence representing an animal model of anxiety ( Hurst and West 2010 ). Investigators are urged to find out the advice provided by the facility on how to handle animals during routine care. Furthermore, they may apply this approach themselves and see the outcome.

Laboratory animal husbandry issues are an integral but underappreciated part of experimental design, which if ignored can cause major interference with the results. All study groups should familiarize themselves with the current routine animal care of the facility serving them and their monitoring capabilities on biological and physicochemical environment. With respect to husbandry issues, it is often easier to say what should not be done rather than what to do, but the final decisions are left to the group and depend largely on specific requirements of the study. While defining the experimental design for an experiment, it is important to invest adequate time in the identification of such issues and to devise effective strategies to deal with them.

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• Table Of Contents

In modern civilizations, most people rely on meat , milk , and eggs as major sources of numerous nutrients . To satisfy this demand, sheep , goats , cattle , water buffalo , swine, chickens , ducks , geese , and turkeys are produced on farms all over the world. To understand how agricultural animals convert feedstuffs into the food and other commodities consumers demand, animal scientists have undertaken broad investigations using highly sophisticated techniques. The animal sciences comprise applied animal physiology, nutrition, breeding and genetics, ecology and ethology , and livestock and poultry management. In addition, diseases of food animals are the focus of many veterinary scientists.

Animal nutrition research was well-established in several centres around the world by the turn of the 20th century, and it began to flourish during the second quarter of the 1900s. Many discoveries have been made about animal metabolism and consequent nutrient requirements; the usefulness of hundreds of feedstuffs as sources of essential amino acids , vitamins , and minerals, as well as lipids and carbohydrates ; the proper balance of available nutrients in the diet; nutrient supplements and feed-processing technologies; and metabolite-partitioning and growth-promoting compounds . These fundamental findings have been applied widely since 1950, bringing about improved animal feeding and the rise of feedlots and intensive animal farming . Studies of life processes in farm animals have helped in developing the optimal nutriment for each animal, and human nutrition has benefited enormously from the knowledge that has come from these investigations.

The notion that “like begets like” was already current in biblical times. Long before the science of animal genetics developed, all species of agricultural animals were subjected to selective breeding to some extent. Modifying livestock and poultry to meet consumer demands requires the application of scientific principles to the selection of superior breeding animals and planned matings. For example, consumers have come to prefer more lean tissue and less fat in meat, and so the meat-type hog was developed in two decades of intensive selection and crossbreeding starting in the 1950s. Swine now yield more lean pork, grow faster, and require less feed to reach market weight than before. By the 1980s, a laying hen of any popular genetic strain, if managed properly, could be expected to produce more than 250 eggs annually, while special meat-producing strains of chickens gain body weight at a rate of 1 : 2 in ratio with feed intake.

Some of the most significant research in animal breeding has been done with dairy cattle and has established the proved sire system, in which bulls are ranked according to the performance of their offspring. The use of sires proved in this way together with artificial insemination has enabled dairy farmers to improve their herds by greatly expanding the influence of genetically superior bulls. Along with increased emphasis on performance testing, efforts have been made to predict at a young age whether an individual animal will be an efficient meat, milk, or egg producer. Such success has made for earlier culling and for herds and flocks of higher genetic merit.

Animals represent renewable agricultural resources because they reproduce, and animal scientists have studied animal reproduction assiduously since the 1930s. These investigations began in the United Kingdom but were soon joined by scientists in the United States , where the work blossomed. Basic discoveries have been put to use quickly in the animal industries. Elucidation of reproductive structures and mechanisms made it possible to refine reproductive management in the 1940s, and artificial insemination made possible the widespread use of proved sires in the 1950s. Additional basic knowledge and later technological developments made practical the control of the estrous cycle and of parturition by exogenous hormones and the serial harvesting and transplantation of embryos from donor females of high merit. The result of these changes has been an increase in the reproductive rate and efficiency of all species of farm animals.

Animal ecology and ethology are relatively young branches of the animal sciences. Around the middle of the 20th century, environmental physiologists in the United States and the United Kingdom began to study agricultural animals’ relations with their environment , including temperature, air, light, and diet. Interactions among environmental temperature, diet, and the animals’ genetic makeup have been characterized, and great strides have been made in improving thermal-environmental management on farms. Lighting management is now essential to profitable poultry production, and the light environment is being controlled in livestock houses as well. Since the 1970s emphasis has shifted to include the behavioral adaptability of animals to their surroundings and the effects of environmental stress on the immune status of livestock and poultry. Farmers have widely adopted intensive systems of animal production, and these systems continue to present opportunities and problems to animal scientists concerned with discovering and accommodating the environmental and ethological needs of food animals.

Animal health is essential to the efficient production of wholesome animal products. An example of the economic effect of animal-disease research conducted by veterinary scientists is the control of Marek’s disease , a highly contagious disease affecting the nerves and visceral organs of chickens, which resulted in a loss of more than $200,000,000 annually to the U.S. poultry industry alone. The disease was studied for more than 30 years before it was learned that it is caused by a herpes virus . Within three years of this discovery, a vaccine was developed that reduced the frequency of Marek’s disease and the resultant meat condemnations in vaccinated chickens by 90 percent and increased egg production by 4 percent. In the first quarter of the 21st century, outbreaks of avian flu outbreaks, often transmitted from wild migrating birds to farm animals, have necessitated the culling of millions of poultry animals, highlighting the continued need for effective vaccines. Veterinary scientists also investigate the chronic infectious diseases associated with high morbidity rates and various metabolic disorders.

A group of sciences and technologies underlie the processing, storage, distribution, and marketing of agricultural commodities and by-products. Modern post-harvest technology helps provide inexpensive and various food supplies for consumers, meets the demands of a variety of industrial users, and even creates replacements for fossil fuels .

Research having particular significance to post-harvest technology includes genetic engineering techniques that increase the efficiency of various chemical and biological processes and fermentations for converting biomass to feedstock and for use in producing chemicals (including alcohols) that can replace petroleum-based products. Among the expected outcomes are the manufacture of new products from reconstituted ones and the recovery of by-products that would otherwise be considered waste.

Agricultural engineering includes appropriate areas of mechanical , electrical, environmental , and civil engineering , construction technology, hydraulics , and soil mechanics .

The use of mechanized power and machinery on the farm has increased greatly throughout the world, fourfold in the United States since 1930. Research in energy use, fluid power , machinery development, laser and microprocessor control for maintaining grain quality, and farm structures is expected to result in further gains in the efficiency with which food and fibre are produced and processed.

Agricultural production presents many engineering problems and opportunities. Agricultural operations—soil conservation and preparation; crop cultivation and harvesting; animal production; and commodities transportation, processing, packaging, and storage—are precision operations involving large tonnages, heavy power, and critical factors of time and place. Facilities designed to aid farm operations help farm workers to minimize the time and energy requirements of routine jobs.

Four primary branches have developed within agricultural engineering, based on the problems encountered . Farm power and machinery engineering is concerned with advances in farm mechanization—tractors, field machinery, and other mechanical equipment. Farm structures engineering studies the problems of providing shelter for animals and human beings, crop storage, and other special-purpose facilities. Soil and water control engineering deals with soil drainage, irrigation , conservation, hydrology , and flood control. Electric power and processing engineering is concerned with the distribution of electric power on the farm and its application to a variety of uses, such as lighting to control plant growth and certain animal production operations.

The field of agricultural economics includes agricultural finance, policy , marketing , farm and agribusiness management, rural sociology , and agricultural law. The idea that the individual farm enterprise forms a unit—affected by location, production techniques, and market factors—originated during the 19th century. It was later supplemented by the theory of optimum utilization of production factors by the selection of production lines. Further refinement came about through applications of modern accounting methods. Research into farm and agribusiness management led to mathematical planning systems and statistical computation of farm-enterprise data, and interest has been drawn to decision-making behaviour studies of farm managers.

Agricultural policy is concerned with the relations between agriculture, economics , and society. Land ownership and the structure of farm enterprises were traditionally regarded as primarily social problems. The growth of agricultural production in the 20th century, accompanied by a decline in size of the rural population, however, gave impetus to research in agricultural policy. In the capitalist countries, this policy has concentrated on the influence of prices and market mechanisms; in the centrally planned countries, emphasis has been placed on artificially created market structures.

Research in agricultural marketing was originally limited to the problem of supply and demand , but the crises of the Great Depression in the 1930s brought new analytical studies. In Europe the growth of the cooperative movement—begun in Germany in the 19th century as a response to capital shortage and farm indebtedness—brought satisfactory solutions to problems of distribution of products from farmer to processor. Consequently, little interest in market research developed in Europe until the mid-20th century. Today, agricultural marketing studies focus on statistical computations of past market trends to supply data for forecasting.

Agricultural law concentrates on legal issues of both theoretical and practical significance to agriculture such as land tenure , land tenancy, farm labour, farm management , and taxation . From its beginnings at the University of Illinois in the 1940s, modern agricultural law has evolved to become a distinct field of law practice and scholarship.

Rural sociology, a young discipline , involves a variety of research methods, including behaviour study developed from studies in decision making in farm management.

Animal Husbandry - Science topic

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REVIEW article

Integrating animal husbandry with crops and trees.

• Carbon Management and Sequestration Center, The Ohio State University, Columbus, OH, United States

Per capita intake of animal protein is expected to increase globally through 2050, and the rate of increase will be more in developing or emerging economies than in developed countries. Global meat consumption between 1980 and 2050 is projected to increase from 133 million to 452 million tons, and 86% (279 million tons) of the increase will occur in developing countries. Animal-based agricultural systems occupy 45% of the global land area and contribute a large proportion of agricultural emissions. In addition to being a major source of nitrous oxide (N 2 O), methane (CH 4 ), and other greenhouse gases (GHGs), livestock also use 8% of the global water withdrawal. The animal sector is dominated by resource-poor and small landholders of developing countries. Adverse effects of livestock on the environment are caused by the way animal husbandry is practiced, in no small part because animals are not integrated with other agricultural and forestry-based practices. Thus, improving and sustaining the livestock sector is critical to advancing the Sustainable Development Goals (SDGs) of the United Nations, especially SDG #1 (No Poverty), SDG #2 (Zero Hunger), SDG #6 (Clean Water and Sanitation), and SDG #13 (Climate Action). Separating raising of livestock from cultivating seasonal crops and perennial trees has decoupled the biogeochemical/biogeophysical cycling of carbon (C), water (H 2 O), nitrogen (N), phosphorus (P), and sulfur (S). This decoupling is a causative factor of the increase in emissions of N 2 O and CH 4 , eutrophication and contamination of water resources, degradation of rangelands, and decline in its biodiversity. Therefore, identifying and adopting systems that integrate livestock with crops and trees are critical for reducing the environmental footprint of animal-based dietary products. Incorporating pastures/forages in the rotation cycle along with controlled grazing, called ley farming, and agroforestry, such as alley cropping, are examples of integrated farming systems. Other strategies of reducing the environmental footprint comprise the following: reducing enteric fermentation by precision feeding and matching dietary protein to animal need, processing CH 4 and N 2 O emissions for other uses, and managing manure and other animal waste prudently. Other important considerations are adopting multiple GHG perspectives and minimizing gas swapping, reducing wastage of animal products, decreasing the use of antibiotics, and restoring rangeland for sequestration of atmospheric CO 2 as soil organic matter.

Introduction

The domestication of animals, which started as early as the 12th millennium circa BP ( Zeder, 2008 ), began with dogs and was followed by that of ruminants (i.e., goats, sheep, cattle). Chickens were domesticated about 10,000 years ago, followed by oxen and horses as beasts of burden for plowing and transportation ( Rutledge and McDaniel, 2011 ). Over millennia, the cultivation of crops was closely integrated with that of raising livestock. Since the mid-twentieth century, however, the separation of raising livestock from the growing of crops has caused environmental issues such as the degradation of soil health, eutrophication of water, emission of greenhouse gases (GHGs) into the atmosphere, and loss of biodiversity ( Peyraud et al., 2014 ).

Raising livestock separately may not be a sustainable option ( Broom et al., 2013 ) economically, pedologically or ecologically. In view of the numerous demands of the growing and increasingly affluent human population, achieving food and nutritional security is seemingly at odds with the necessity of reducing the negative environmental footprint of agriculture. An important cause of this dilemma may be the simplification of agro-ecosystems, and the attendant decline in diversity of farming systems at the soil scape, landscape, and the farm scale ( Lemaire et al., 2014 ). The adverse effects of livestock on the environment are attributed to the way in which the animals are raised, and such issues can be addressed ( Dalibard, 1995 ). In some climates and landscapes, separating livestock from crops and trees is an important cause of the decline in diversity at the farm scale, with the attendant adverse impacts on the environment. Such a simplification and loss of biodiversity also leads to decoupling of the cycling of carbon (C) from those of water (H 2 O), nitrogen (N), phosphorus (P), and sulfur (S) ( Lal, 2010 ). Cycles of N and C, closely connected to livestock's role in land use and land use change ( Steinfeld et al., 2006 ), may be decoupled by this simplification of the farming system. Emission of GHGs (i.e., CH 4 ) is exacerbated when ruminants are concentrated, which tends to uncouple the C and N cycle by releasing the digestible C as CO 2 and CH 4 and digestible N in waste as N 2 O ( Soussana and Lemaire, 2014 ). The risks of uncoupling, which has severe implications to climate change because CH 4 and N 2 O have a high global warming potential (GWP), can be minimized by integrating livestock with crops and trees. Practices such as establishing vegetation buffers on agricultural fields to enhance biodiversity and conserve soil and water (i.e., agroforestry or alley cropping), can also reduce the environmental footprint of livestock raised on the same land unit ( Goldstein et al., 2012 ).

The objectives of this article are to discuss: (1) the potential and challenges of increasing food and nutrition for the growing human population by raising livestock, (2) the livestock sector and the Sustainable Development Goals (SDGs) of the United Nations, (3) the conceptual basis of integrating livestock with crops and trees to increase the biodiversity of farming systems, (4) the options for sustainable management of grasslands for food and climate security, (5) the potential of integration of livestock with crops and trees to sequester carbon and reduce gaseous emissions, and (6) improved management of livestock in the tropics.

The Potential and Challenges of Increasing Food and Nutrition for the Growing Human Population by Raising Livestock

Fears of widespread famine were aggravated by the rapid population growth during the 1950s and 1960s ( Ehrlich, 1968 ). The human population of 2.56 billion (B) in 1950 increased to 3.04 B in 1960, 3.71 B in 1970, and 4.34 B in 1980 at the 10-year growth rate of 18.9, 22.0, and 20.2%, respectively. The fears of widespread famine were averted by the spectacular increase in yields of cereal crops, achieved through the Green Revolution during the 1960s ( Pingali, 2012 ). However, the world population has increased to 7.8 B in 2020 and is projected to be 9.8 B by 2050 and 11.2 B by 2100 ( UN, 2019b ). Whereas 820 million people are prone to undernourishment ( FAO, 2017 ), about 2 B are suffering from malnourishment because of deficiencies in protein, micronutrients, and vitamins ( Ritchie and Roser, 2019 ). However, the livestock sector can play an important role in eliminating hunger and malnourishment.

Since the 1960s, large parts of natural lands have been converted into agro-ecosystems to feed the growing world population. In addition to reducing biodiversity, conversion of natural ecosystems at a larger scale has also depleted and contaminated water resources, polluted air, and exacerbated the emission of GHGs into the atmosphere. There has also been a growing interest in increasing animal products to address malnourishment. The global population of livestock (i.e., cattle, sheep, goats, pigs, poultry) has increased drastically since the 1950s. This increase in both populations (i.e., human and animals) has also led to a growing concern whether the biosphere has the capacity to support such large populations of domesticated livestock and people.

The human population has increased from about 10–20 million at the dawn of settled agriculture to about 7.8 B (~10,000 times) in 2020 ( UN, 2019a ), and there is an equally alarming growth of the population of domesticated livestock. While the cattle population has declined from a of high of 1.4 B in 2011, it still remains at ~1 B in 2019 ( The Economist, 2011 ; Shahbandeh, 2019 ). The global average stock of chicken is estimated at 19 B, and that of sheep and pigs at about 1 B. Global demand for animal-based produce is projected to double by 2050 ( Herrero et al., 2009 ) because of the increasing affluence and the change in dietary preferences ( Rojas-Downing et al., 2017 ). The global population of bovines is projected to increase from 1.9 B in 2010 to 2.4 B in 2030, 2.6 B in 2040, and 2.64 B in 2050 ( Rosegrant et al., 2009 ; Thornton, 2010 ). The human population is increasing at an average global annual rate of 1.2%, but the population of domesticated livestock is increasing at an annual rate of 2.4%. The geographical distributions of livestock population also vary widely depending on biophysical, socio-economic, and cultural factors ( Gilbert et al., 2018 ).

Along with the livestock population, the amount of livestock produce is also growing rapidly. Between 2000 and 2050, global production is projected to increase from 229 to 465 million tons of meat and 580 to 1043 million tons of milk ( FAO, 2006 ; Steinfeld et al., 2006 ). More than 60 B land animals are used worldwide for meat, egg, and dairy production, and the global population of livestock may exceed 100 B by 2050 ( Yitbarek, 2019 ), when the world's meat production is projected to double ( FAO, 2019 ). All trends from 1980 to 2002 indicate that meat consumption increased from 47 million to 132 million tons in developing countries ( NAS, 2015 ). All trends from 1980 to 2050 indicate that meat consumption is projected to increase from 86 million to 120 million tons in developed countries and 47 million to 326 million tons in developing countries ( NAS, 2015 ). By 2050, the increase in meat production may be 290% for pig meat, 200% for sheep and goats, 180% for beef and buffalo meat, 180% for milk, 700% for poultry meat, and 90% for egg ( Yitbarek, 2019 ). Similar to meat products, production of milk is also increasing globally. With a current average milk consumption of 100 kg per person per year ( Reay and Reay, 2019 ), the projected increase in population will increase milk production as well. Each liter of fresh milk is equivalent to 3 kg of GHG emissions ( Reay and Reay, 2019 ).

The strong nexus between livestock and anthropogenic climate change can neither be denied nor ignored. Indeed, livestock impact climate change, and the rapidly changing climate is also impacting livestock. It is precisely in this context that integrating livestock with crops and trees can play an important role in re-greening of the planet ( Janzen, 2011 ). Harnessing the positive effects of livestock-based farming systems (e.g., nutritious food, eliminating hunger and hidden hunger) can lead to sustainable management of crops and trees and reduce the environmental footprint of farming ( Herrero et al., 2009 ). In addition, sustainable management of rangelands by adopting ecologically based principles of animal husbandry can strengthen the provisioning of ecosystem services (ESs) from these fragile and ecologically-sensitive but economically important ecoregions ( Havstad et al., 2007 ).

Livestock Sector and Sustainable Development Goals of the United Nations

The highly dynamic livestock sector is rapidly changing in response to the ever-increasing demands of the growing population, especially in developing countries. Thus, judicious management and eco-intensification of livestock-based systems can also address the daunting challenge of advancing the SDGs of the United Nations ( Figure 1 ) because site-specific integration of crops with livestock is critical to advancing several SDGs. Specifically, prudent management of livestock can advance SDG #1 (No Poverty) by improving income of small landholders as well as that of commercial farmers. For small landholders in developing countries, livestock are not only a source of nourishment, they are also a source of renewable energy through draft animals, use of dung as household fuel, and also a source of manure as an amendment for crops. In addition to addressing the vulnerability of 820 million under-nourished people, most of them concentrated in South Asia and Sub-Saharan Africa ( FAO, 2017 ), judicious production and use of animal-based diet can also alleviate malnutrition (hidden hunger) affecting 2 B people globally. Thus, livestock are critical to advancing SDG #2 (Zero Hunger).

Figure 1 . Eco-intensification of livestock-based systems to advance the Sustainable Development Goals of the United Nations.

The livestock industry, which consumes 8% of the global water supply ( Schlink et al., 2010 ), has a strong impact on SDG #6 (Clean Water and Sanitation). Livestock production involves the use of both blue and green water ( Falkenmark, 2003 ). Nearly one-third of the total water footprint of agriculture in the world is related to animal products ( Mekonnen and Hoekstra, 2012 ), and beef has a larger water footprint than poultry and pork ( Gerbens-Leenes et al., 2013 ). Therefore, reducing the water footprint of livestock, an important consideration of eco-intensification of livestock-based systems ( Doreau et al., 2012 ), can advance SDG #6. Judicious management of livestock and rangelands is critical to improving the quality and renewability of water through buildup of soil organic matter content that can enhance soil water storage and denature and filter pollutants.

In addition to water, reducing emissions of GHGs from the livestock sector is pertinent to advancing SDG #13 (Climate Action). Because of its importance, the interaction between climate change and the livestock sector is now widely recognized ( Thornton et al., 2009 ). Livestock are responsible for a large part of agricultural emissions ( Gill et al., 2010 ; Havlík et al., 2014 ). Agriculture contributes about 10–12% of the current anthropogenic emissions. Some estimate that direct livestock non-carbon dioxide emissions caused about 19% of the total modeled warming of 0.81 O C from all anthropogenic emissions in 2010 ( Reisinger and Clark, 2018 ). GHG emission per unit of livestock product is more in ruminants than that in monogastric animals ( Gill et al., 2010 ). Because of the high global warming potential (GWP) of CH 4 and N 2 O, it is appropriate to combine the cumulative effect of all GHGs into CO 2 -equivalent ( Pitesky et al., 2009 ).

Conceptual Basis of Integrating Livestock with Crops and Trees

Livestock use 30% of the Earth's entire land surface as permanent pastures; 33% of arable land is used to produce feed for the livestock ( FAO, 2006 ), and thus livestock have a large environmental footprint ( Smith et al., 2013 ). Pelletier and Tyedmers (2010) projected that the livestock sector will even more strongly impact the environment by 2050 with regards to three issues: (i) climate change, (ii) reactive nitrogen mobilization, and (iii) appropriation of plant biomass at a global scale. Pelletier and Tyedmers also predicted that the livestock sector alone may overshoot humanity's “safe operating space” by 2050 in each of these three domains. While ( FAO, 2006 ) estimates in the report “Livestock's Long Shadow” have been strongly debated ( Maday, 2019 ), emissions of GHGs from the livestock sector, especially that of CH 4 and N 2 O, can be reduced and managed by adapting the integrated systems presented herein. It is also pertinent to carefully choose site-specific sustainable livestock production to reduce or mitigate emissions, and to develop policies that promote climate change adaptation and mitigation options ( Rojas-Downing et al., 2017 ). Some concerns about the impacts of animal-based diet ( Pitesky et al., 2009 ; Gerber et al., 2013b ; Eshel et al., 2014 ; Hedenus et al., 2014 ) can be addressed through a judicious integration of crops with livestock. The latter can lead to an increase in the quantity and quality of food production and economic returns while also reducing pressure on land and water resources ( Franzluebbers, 2007 ; Provenza et al., 2019 ).

Most emissions from the livestock sector occur in commodity (meat, milk) production or the supply-side. However, gaseous emissions are also affected by the demand-side, or the consumer population, which is not only growing in numbers but is also undergoing a nutrition transition in favor of the animal-based diet. Therefore, several studies have suggested that merely addressing the supply-side emissions from the livestock sector may be insufficient to limit the temperature rise to <2°C, and addressing the demand-side is also necessary ( Kiff et al., 2016 ; Scherer and Verburg, 2017 ). Indeed, demand-side mitigation measures—including preferences for a plant-based diet, along with eating more poultry and fish than red meat, or grass-fed rather than grain-fed meat – have a greater potential to reduce emissions (1.5–15.6 Gt CO 2 -eq /yr) (1 Gt = gigaton = billion ton) than do supply-side measures (1.5–4.3 Gt CO 2 -eq/yr) ( Smith et al., 2013 ). An integrated and judicious management of crops and livestock may mitigate some of the negative environmental impacts on the supply-side when crops are grown separately from that of raising the livestock ( Herrero and Thornton, 2013 ).

Ruminant production systems are under pressure for several reasons: (i) methane emission, (ii) inefficient use of land, (iii) feed-food competition, and (iv) weakening of key ecosystems services through large-scale conversion of grasslands to crop production for livestock. However, livestock can produce human food of high nutritional quality from marginal lands that are mostly unsuitable for crop production. Thus, a viable strategy may involve the following: (i) raising animals from feed that is non-edible for humans, (ii) grazing livestock on land not suitable for crop production, and (iii) reducing emissions of GHGs (CH 4 , N 2 O). Some site-specific grassland-based ruminant production systems are much more efficient than concentrate-based systems for producing protein ( Peyraud and Peeters, 2016 ). The challenge lies in developing sustainable systems of forage production that also lead to positive responses to societal demands for consuming more natural products ( Peyraud and Peeters, 2016 ).

Site-specific options for integrated crop-livestock systems can also achieve synergies between agricultural production and environmental quality ( Lemaire et al., 2014 ). Table 1 outlines examples of sustainable intensification of livestock-based systems, involving judicious combinations of sod/forages with crops and trees, which address some concerns of ruminant production systems. The term “sod” refers to the soil surface when covered with grass, sward, or turf. By using grassland-based ruminant-livestock systems (GRLS) models of African Guinea Savanna, Bateki et al. (2019) observed that sustainable intensification of livestock, integrated with crops and trees, could increase food security of the growing African population.

Table 1 . Examples of integrated livestock systems with crops and trees (Compiled from Kang et al., 1990 ; Leakey, 1996 ; McCown, 1996 ; Bajracharya et al., 1998 ; Garrett et al., 2004 ; Fike et al., 2016 ; Jose and Dollinger, 2019 ; Munsell and Chamberlain, 2019 ; USDA-NRCS, 2020 ).

Agroforestry is a set of technologies in which trees are sequentially or simultaneously integrated with crops and/or livestock in a wide range of integrated systems ( Leakey, 1996 ). Alley cropping is a system of planting trees on the contour at a wide spacing (4–10 m apart) with a food crop grown in the alley ways between the rows of trees. Planting several rows of trees and shrubs, which can also be used as forage, is a system that integrates livestock with both crops and trees. Trees can also be harvested as a source of fuel wood. Such a complex system is an example of an agro-silvopastorial system ( Okali and Sumberg, 1985 ; Kang et al., 1990 ). In temperate alley cropping systems, tree species may include hard wood veneer or lumber species; softwood species for fiber production, or fruits and nuts for food ( USDA, 2020 ). Trees grown on the contour can also be used as filter strip and for contour farming in strip cropping ( USDA-NRCS, 2020 ). Grain crops (i.e., corn, soybean, cowpeas) are grown when the trees are young. When the ground is shaded, forages can be harvested and cattle grazed, and the prunings can also be used as green manure for cereals (i.e., corn). Leguminous trees serve as a source of nitrogen to enhance soil fertility.

Models are needed for simultaneous quantification of C and N flows and how they are affected by different livestock-crop-tree management systems. Several whole-farm based models have tried to estimate gaseous emissions ( Snow et al., 2014 ; Bateki et al., 2019 ), but there is a need for more data on nutrient and C flows at the field level ( Snow et al., 2014 ).

Options for Sustainable Management of Grasslands for Food and Climate Security

Site-specific options are needed for sustainable intensification of livestock systems in diverse socio-economic and biophysical regions prone to climate change. For example, livestock-based systems occupy 45% of the global land area; grasslands/savannas suitable for grazing cover 37% of Earth's surface area ( NAS, 2015 ). These ecosystems are highly diverse and occur within the seasonally dry tropical to sub-tropical equatorial regions ( Whitley et al., 2017 ). Savanna ecoregions, open-canopy and fire-dependent biomes, are also prone to climate change that may alter phenology, root-water access and fire dynamics ( Whitley et al., 2017 ). Principal environmental drivers affecting biomass/feedstock productivity in savanna regions are water and nutrient availability, vapor pressure deficit, solar radiation and fire ( Devi Kanniah et al., 2010 ). Therefore, understanding these controls and their management through eco- intensification is critical for enhancing net primary productivity (NPP) under the changing global environment ( Kanniah et al., 2013 ). Important controls include restoring soil functions, conserving water to minimize the risks of drought, and adopting improved species of forages and meat of better nutritional quality ( Herrero and Thornton, 2013 ; Provenza et al., 2019 ).

Climate change is already adversely impacting agro-pastoral production in Africa ( Stige et al., 2006 ; O'Mara, 2012 ). Under these conditions, Teague et al. (2011) observed that multi-paddock (MP) grazing may be an option for sustainable intensification. Teague and colleagues reported that MP grazing at a high stocking rate increased SOC content and cation exchange capacity of soil compared with light continuous and heavy continuous grazing. Similarly, Kleppel (2019) reported that microbial biomass in MP grazed soils was higher, more diverse, and contained relatively more fungal than bacterial biomass than did conventional management and hay field. A 2-year study in South Africa by Chaplot et al. (2016) showed that topsoil SOC stocks were significantly increased in soil with either livestock exclosure and NPK fertilization or high density and short duration grazing compared with annual burning, livestock exclosure and livestock exclosure with topsoil tillage. This was accomplished by high intensity, short duration grazing (HDSD, 1200 cows per ha for only 3 days per year) followed by complete exclosure for the remainng 362 days each year ( Chaplot et al., 2016 ). On the basis of a global assessment of holistic planned grazing, however, Hawkins (2017) concluded that only rangelands with higher precipitation have the resources to support MP grazing at a high stocking rate.

The Potential for Integrating Livestock with Crops and Trees to Sequester Carbon and Reduce Gaseous Emissions

Restoration and sustainable management of grasslands can play an important role in adaptation and mitigation of climate change ( Lal, 2008 ). Technical potential of C sequestration in global savannas, through land restoration and integrated management of livestock with crops and trees, can be as much as 2.55 Gt C/y ( Table 2 ). Pertinent animal feeding strategies (e.g, use of flax seeds, protein-intensive forages) can reduce enteric CH 4 and NH 3 emissions ( Yáñez-Ruiz et al., 2018 ). Above all, carbon sequestration in grass—by planting species with high biomass production and biological nitrogen fixation, such as trees like Acacia albida and Leucaena leucocephala in west Africa ( Kang et al., 1990 ; Pieri and Gething, 1992 ; Soussana et al., 2010 )—is an important option to reduce net emissions from the livestock sector. In addition, recycling of livestock manure in a whole-farm perspective ( Petersen et al., 2007 ) can reduce the input of fertilizers in croplands.

Table 2 . Global land area under grasslands and the estimates of C sequestration (Adapted from Grace et al., 2006 ; Lal, 2008 ).

Adaptation and mitigation of climate change in the livestock sector requires translating of science into action by policy interventions that remove barriers to implementing proven technologies ( Smith et al., 2007 ). Appropriate policy interventions are especially important in developing countries for achieving sustainable management of rangeland because of ecologically fragile and climatologically harsh environments. In India, for example, total annual CH 4 emissions, estimated at 9–10 Tg (Tg = teragram = 1 million ton) from enteric fermentation and animal waste ( Sirohi and Michaelowa, 2007 ), can be reduced by appropriate policy interventions such as payments for provisioning of ecosystem services.

The goal of enhancing and sustaining agricultural production for meeting the needs of the growing population while reducing the environmental footprint of agriculture necessitates local and site-specific integration of cropping with livestock systems. Soil C sequestration and decrease in gaseous emissions are in accord with SDG #13 of the U.N. Therefore, site-specific technologies for integrating livestock with crops and trees ( Table 1 ) are needed to: (i) better moderate coupled biogeochemical cycles and reduce fluxes of pollutants into the atmosphere and the hydrosphere, (ii) create a more diversified and structured landscape mosaic that supports diverse habitats, and (iii) enhance capacity of the system to adapt to extreme events associated with climate change and alterations in the socio-economic and human dimensions ( Lemaire et al., 2014 ). It is precisely in this context that management of grasslands can strengthen the coupled cycling of carbon (C) with those of H 2 O, N, P, and S within vegetation, soil organic matter (SOM) stock and soil biota in general, but the soil microbial biomass in particular ( Lemaire et al., 2014 ).

The schematic in Figure 2 depicts the pathways of decreasing the environmental footprint of livestock products. Conceptually, choosing a livestock product with a lower emission footprint for a diet would reduce the overall negative impact on climate and the environment. The environmental footprint of a dietary product can be expressed in three ways ( de Vries and de Boer, 2010 ): (i) per kg of product, (ii) per kg of protein, and (iii) per kg of average daily intake of each livestock product. Based on the lifecycle analysis (LCA) of 16 studies conducted in OECD (Organization for Economic Cooperation and Development) countries, de Vries and de Boer (2010) determined that the land and energy use and the GWP for 1 kg of product followed the order of beef > pork > poultry. This order was based on differences in feed efficiency, enteric CH 4 emission, and reproduction rates. Similar trends were reported by ( Eshel et al., 2014 ).

Figure 2 . A flow chart depicting the integration of livestock with arable land use for decreasing the number of livestock required (SOC, soil organic carbon; GHGs, greenhouse gases).

Emissions of all gases (CO 2 , CH 4 , N 2 O) are used to compute CO 2 equivalents ( Lal, 2004 ). Direct emissions of CH 4 and N 2 O in the livestock sector must be reduced. In this context, a multiple GHG perspective must be adopted ( Figure 3 ) because CH 4 has a GWP of 21 and N 2 O of 310. Because of the high GWP of CH 4 in both confined and grazing systems, steps must be taken to develop credible methods of measuring CH 4 emission by ruminants ( Hill et al., 2016 ), and to reduce enteric fermentation by ruminants ( Grossi et al., 2018 ). Precision feeding, matching feed intake with the need of the animal ( Gerber et al., 2013a ), and the choice of forages can also reduce the gaseous footprint. For example, the combination of highly digestible forages ( Haque, 2018 ; van Gastelen et al., 2019 ) that contain secondary compounds such as tannins ( Roca-Fernández et al., 2020 ) can also reuce methane emissions. The multiple GHG perspective is an important strategy that can address the potential pollution swapping—a reduction in one gas can lead to emission of another ( Gerber et al., 2013a ). Thus, a full accounting of all GHGs is required ( Soussana et al., 2007 ).

Figure 3 . Measures to reduce emissions of greenhouse gases (GHGs) from the livestock sector (SOC, soil organic carbon).

Improved Management of Livestock in the Tropics

Livestock are an important component of agroecosystems in the tropics and adopting innovative livestock/farming approaches can enhance production and reduce environmental footprints. Judiciously combining crops with livestock within the same landscape has numerous co-benefits ( Gil et al., 2015 ). For example, ley farming ( Carberry et al., 1996 ; McCown, 1996 ), involving light grazing of legumes grown in rotation with crops, is a pertinent strategy for integrating crops and livestock. Built on the concept of ley farming, pasture cropping is a farmer-initiated concept of sowing a winter-active cereal into a summer-active native perennial pasture ( Millar and Badgery, 2009 ). Self-regenerating annual legume pastures ( Puckridge and French, 1983 ) can enhance soil fertility and increase cereal yield, along with more forage for sheep and cattle production. Ley farming, developed in Southern Australia since the 1930s, is also relevant to similar regions in Sub-Saharan Africa, South/Central Asia, and the Caribbean. However, soil/site specific choices of legumes and grazing patterns/intensity must be identified.

The numerous benefits of ley farming include ( Bell et al., 2010 ): (i) enhancing soil N for the next crop, (ii) sequestering SOC and off-setting emissions, (iii) controlling weeds and other pests, (iv) minimizing risks of runoff, soil erosion, and deep drainage, (v) increasing livestock production, and (vi) sustaining crop yield. However, several challenges exist. Successfully implementing ley farming includes a critical appraisal of the following ( Bell et al., 2010 ): (i) addressing difficulties with pasture establishment, (ii) suppressing/removing pasture plants before seeding crops, and (iii) reducing competition for water and some plant nutrients. Site-specific choice of pasture species is critical.

Integrating livestock with cropland and forestland can also be a prudent complimentary strategy. For example, growing Acacia albida ( Faidherbia albida ) as a permanent tree crop on farmlands (cereals, vegetables, and livestock) is a traditional agroforestry system in Sub-Saharan Africa ( Poschen, 1986 ; Weil and Mughogho, 1993 ; Wanyancha et al., 1994 ). Faidherbia sp. has been widely used for enhancing soil fertility and as a source of shade and shelter for livestock in Sub-Saharan Africa ( Pieri and Gething, 1992 ).

Widespread adoption of integrated systems can reduce the risks of rangeland degradation, as seen in China ( Hou et al., 2008 ). India provides an example of how integrated systems can reduce land area under pasture. With 2.3% of the global land area, India supports 18% of the human and 11% of the world's livestock population: the latter consists of 536 million animals and 740 million poultry in 2019, which are raised on only 12.3 M ha of land under permanent pastures and grazing land ( TAAS, 2019 ).

Successfully integrating crops with livestock has numerous economic, ecological, and other benefits ( Figure 4 ), especially in developing countries of the tropics ( Herrero et al., 2013 ). Important among these are: (i) creating another income stream for farmers and alleviating rural poverty ( De Haan et al., 2001 ), (ii) developing a safety net for the poor and especially women farmers, (iii) enhancing assets for farmers, and (iv) alleviating malnourishment ( Figure 4 ). However, livestock need additional land, water, nutrients, and forage resources. Therefore, judicious management of the growth of this sector is critical, especially for reducing environmental footprints. These technical dimensions must be objectively considered within the context of institutional support (market) and the human dimensions ( Tarawali et al., 2011 ).

Figure 4 . Ecological and socio-economic benefits of integrating livestock with crops and trees.

Conclusions

Intensive farming, which is designed to produce large amounts of economic food to meet the demands of the growing and increasingly affluent human population by using high inputs on small areas, has its merits and demerits. Intensification of crops and livestock systems have drastically increased per capita food production since the 1960s. However, the environmental footprint of livestock sector must be reduced by decreasing soil degradation, increasing water and nutrient use efficiency, reducing eutrophication of water, decreasing pollution of air, and minimizing the risks to global warming. Despite the successes in food production, there are 820 M people vulnerable to undernourishment and more than 2 B to malnourishment caused by the deficiency of protein, micro-nutrients and vitamins. The proportion of vulnerable population may increase as a result of the COVID-19 pandemic. Thus, the objective of sustainable agriculture is to adopt technologies that increase production, reduce the environmental footprint of food production systems ( IPBES, 2019 ; IPCC, 2019 ; UNEP, 2019 ), and also minimize any risks of diseases and infections through intensive livestock farming ( Sigsgaard and Balmes, 2017 ; Smit and Heederik, 2017 ).

A feasible option to produce the required amount of nutritious food while restoring and sustaining the environment is through site-specific integration of livestock with crops and trees. Such an approach of eco-intensification would simultaneously achieve several overlapping and interconnected SDGs including #2 (Zero Hunger), #3 (Good Health and Wellbeing), #6 (Clean Water and Sanitation), #13 (Climate Action) and #15 (Life on Land). Ignoring such an option would aggravate risks of environmental pollution, exacerbate perpetuation of natural ecosystems, increase harmful interactions between humans and the wildlife, and even aggravate the frequency and intensity of tragedies such as the COVID-19 pandemic ( Lal, 2020b ). Some recommendations of the Conference of Parties (COP) of the United Nations Framework Convention to Combat Climate Change (UNFCCC) are also in accord with the strategies of integrating livestock with crops and trees. Examples of these are the “4 Per 1,000” initiative launched at COP21 in Paris in 2015 and “Adapting African Agriculture“of COP 22 in Marrakech ( Lal, 2019 , 2020a ). The scientific community and land managers should seize the opportunity to adopt innovative options such as those outlined in this article and promote sustainable agricultural practices which reconcile the need for producing more and nutritious food with the absolute necessity of improving the environment. Integrating livestock with crops and trees can reduce direct non-CO 2 emissions and achieve the COP21 mitigation goal of limiting global warming to 2°C.

These efforts can be enhanced through research priorities identified by The Committee on Consideration for the Future of Animal Science Research ( NAS, 2015 ). They include: (1) identifying appropriate mixes of intensification and extensification required to simultaneously increase production and reduce environmental footprints in different regions throughout the world, (2) enhancing sustainability of medium- and smaller-scale producers, (3) developing policy interventions to optimize demand for animal products, and (4) evaluating environmental impacts of diverse livestock-based production systems.

Author Contributions

The author confirms being the sole contributor of this work and has approved it for publication.

Conflict of Interest

The author declares that the research was conducted in the absence of any commercial or financial relationships that could be construed as a potential conflict of interest.

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Keywords: gaseous emissions, food security, ecological footprint, sustainable development goals, waste management, farming systems

Citation: Lal R (2020) Integrating Animal Husbandry With Crops and Trees. Front. Sustain. Food Syst. 4:113. doi: 10.3389/fsufs.2020.00113

Received: 17 March 2020; Accepted: 23 June 2020; Published: 29 July 2020.

Reviewed by:

Copyright © 2020 Lal. This is an open-access article distributed under the terms of the Creative Commons Attribution License (CC BY) . The use, distribution or reproduction in other forums is permitted, provided the original author(s) and the copyright owner(s) are credited and that the original publication in this journal is cited, in accordance with accepted academic practice. No use, distribution or reproduction is permitted which does not comply with these terms.

*Correspondence: Rattan Lal, lal.1@osu.edu

Disclaimer: All claims expressed in this article are solely those of the authors and do not necessarily represent those of their affiliated organizations, or those of the publisher, the editors and the reviewers. Any product that may be evaluated in this article or claim that may be made by its manufacturer is not guaranteed or endorsed by the publisher.

Research on Coordinated Development Between Animal Husbandry and Ecological Environment Protection in Australia

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• Yiming Zhu 17 &
• Shasha Li 17  

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Australia is one of the countries whose scientific level of using grassland resources and animal husbandry development level is very high and the way to coordinate Australia’s animal husbandry and ecological environment protection is worth using for reference. This study focuses on facilities about the Australian government’s controlling and protecting of ecological environment in the process of development of animal husbandry, and combines with the current problems in the process of China’s animal husbandry development, in order to explore a suitable path for implementing the animal husbandry sustainable development in China.

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• Ecological environment
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1 Introduction

The animal husbandry in Australia is rather developed where sheep and cattle are the main livestock. In addition, the number of sheep in Australia is the top in the world, and Australia is known as “riding on the sheep’s back country”. In the early, the development model of Australia’s animal husbandry tended to rough grazing. Since the early 19th century, European settlers’ increasing investment in science and technology, introducing high quality forage grass and implementing policies and measures are conducive to the development of animal husbandry. Especially after the Second World War, the number of Australia’s livestock breeding stock and livestock production increased significantly. In 1972, compared with 1950, the number of cattle and sheep breeding stock increased by 87 % and 44 % respectively and wool production grew by 89 % in comparison to the average output from 1947 to 1949. In addition, compared with 1955, the beef and egg production increased by 86 % and 95 % respectively [ 1 ]. During this period, there are mainly three points about the cause of the rapid development of animal husbandry in Australia. The first point is that during the post-war, world economy began to recover and the demand for animal products increased at home and abroad. Developing animal husbandry can not only meet the domestic demand, can increase income through export animal products. So animal husbandry industry had more obvious competitive advantage than other industry. The second point is that the Australia government ordered the Italian prisoners of war to engage in livestock production, which increased the required labor input during the process of livestock production from 1941 to 1947. The third point is that combined with the domestic and international market demand, the Australia government guided the livestock farmers to adopt the latest Science and Technology and farming equipment, what is more, the government implemented financial support and policy inclination to development the animal husbandry. Considering the scarcity of resources and the protection of ecological environment and basing on the conditions of natural resources and markets all over the world, the Australian government continuously adjusted the animal husbandry development policy in order to realize the coordinated development of animal husbandry and ecological environment protection.

Since the reform and opening, with the aid of the push of market economy, government policy support and irregular factors, China’s animal husbandry were integrated and were in the transition period from extensive to intensive little by little. Extensive development pattern makes natural environment deteriorating surrounding China’s pastoral areas, which make the protection of natural resources face great challenge. This study summarizes the current development situation, the characteristics of the development of animal husbandry in Australia and the policy support and emphasis on the measures to protect the ecological environment in the process of sustainable development of animal husbandry. Analysis of Australian animal husbandry development can guide to seek a suitable way for China to coordinate animal husbandry development and ecological environment protection.

2 Current Development Situation of Graziery Industry in Australia

Australia’s land area is about 7.68 million km 2 , and the number of population is about 23.71 million people of which 80 % distribute in the eastern coastal areas. Most area of Australia is plain region, the climate is relatively dry and seasonal temperature difference is inconspicuous. The unique climate conditions in Australia forms a perennial natural pasture grazing. 55 % of the land area is used to develop animal husbandry whose output value accounted for about 80 % of the agricultural output in 2014. Animal husbandry in Australia occupies an irreplaceable position in the agricultural and even the entire national economy. In Australia, over average, everyone owned 5.00 sheep and 5.00 cowsin 2011. However, compared with the Australia, the Chinese person just has the number of sheep and cattle less than a quarter [ 2 ].

Australia’s sheep and goat breeding stock is the largest, followed by chicken and beef. From 1993 to 2013, Australia mainly livestock breeding stock is on the decline on the whole. From Fig.  1 , we can see that the sheep and goats breeding stock decline relatively obvious, down from 1.40 million in 1993 to 2013 in 0.71 million, dropping about 49.28 %. The number change of beef cattle and pig breeding stock is not obvious, of which the former increased but pig breeding stock has a downward trend.

Main livestock number of Australia from 1993 to 2013

From 2006 to 2011, the number of beef, mutton and red meat production decline year by year (Table  1 ). Combined with Fig.  1 , it can be seen that the Australian animal husbandry is in the transition to a new development model. There are two possible reasons: the first one is that animal products exports accounts for a large proportion of total output in Australian [ 3 ]. With the rapid development of animal husbandry in emerging countries, the international market for Australia’s livestock reliance declines, resulting in the decrease of breeding stock. The second one is that with the all-round development of economy, the international market increases demand for some of the agricultural economic crops, such as soybean and rapeseed, so planting economic crops has more competitive advantage than raising livestock, which makes laborer to increase the crop planting area in parts of Australia animal husbandry area.

According to above analysis, the Australian animal husbandry is transforming from a single animal husbandry to planting-culture combined animal husbandry development model gradually.

3 The Characteristics of Harmonious Development Between Graziery and Ecology Environment in Australia

Since the idiographic climate in Australia, natural pasture is the main food of animal composite feed. After more than 200 years of development, animal husbandry in Australia has completed transformation and upgrading and the ecological environment is protected simultaneously in the process of animal husbandry industry in Australia. In extensive development phase, the utilization of grassland resource in Australia also experienced overgrazing, pasture degradation and desertification process. In the early 20th century, the grassland in Australia has reached the ceiling of the bearing capacity and the deterioration of ecological environment has endangered the healthy development of animal husbandry. The stockholders took positive and effective cooperation to prohibit overgrazing behavior and improved ecological environment finally.

3.1 Seeding to Revive Ranch, Formulating Appropriate Grazing Capacity

According to soil conditions and climatic environment, planning different varieties of forage can not only balance the year’s yield, but also helps to improve the quality of soil and increase the yield and to optimize the quality. Grassland yield of forage planting is five times as much as natural grassland [ 4 ]. Grassland yield and regeneration ability determine the grassland grazing capacity. The Australian government boosted grassland ecological construction and decided appropriate grazing capacity according to the production capacity of grassland and grassland recovery ability to prevent the grassland desertification caused by overgrazing grassland. Each family determines reasonable scale of breeding according to suitable grazing capacity to avoid the behavior of grassland overgrazing.

3.2 Rotation Grazing on an Area Basis and Grazing off Season

According to the different growth stages of herds, combining with the carrying capacity of grassland, the herdsman adjusts grazing stages scientifically and manages grassland pasture to guarantee the sustainable utilization of grassland resources. In addition, Australian government divided grazing area all over the country into four different types of the grassland animal husbandry according to the precipitation, temperature, and soil conditions such as low density livestock grazing district, natural grassland grazing area, mixed farming zone and high density grazing area [ 5 ]. In the same zone, livestock farmers divided family farm into several small areas of which 20 % of the pastoral areas of grazing to protect other pasture grass growing in order to maximize the grassland biomass.

3.3 Grazing in Accordance with the Law and Utilizing the Water Resource Rationally

The Australian government had strict rules on grassland construction, the development of environmental protection, water conservancy etc. The government would impose severe penalties on violators, which ensured the coordinated development between animal husbandry and ecological environment protection and cultivated the ecological environment protection consciousness of farmers and herdsmen at the same time. The weather of Australian outback is drought where the average annual rainfall is less than 200 mm. In order to protect the grassland yield, it is indispensable to exploit and utilize water resources. In Australia, livestock farmers built small water storage low dam, reservoir and other water engineering project generally. Storage of water resources ensures livestock drinking water and grassland irrigation.

4 Australian Animal Husbandry Development Model for China’s Enlightenment

As people living standard rising, for Chinese people, demand for animal products is on the rise. What’s more, the price of domestic beef and mutton market is higher, which causes part of the pastoral areas overgrazing phenomenon, resulting in bearing pressure increasing and grassland ecological environment destructed [ 6 ]. In recent years, in order to maintain sustainable use of grassland, the Chinese government is strengthening the construction of grassland ecology and intensifying the efforts on ecological protection, such as returning farmland to grassland project and ecological compensation mechanism. However, support on the investment of pastoral animal husbandry development still has a lot of space [ 7 ]. At the same time, livestock farmers list livestock production as the first goal at the current stage and lack the protection environment consciousness about grassland ecological [ 8 ]. Although there are some difference about the basis of existing on the animal husbandry between Australia and China, China can combine their own development period of animal husbandry and existing problems to explore a sustainable development way to coordinate animal husbandry development and ecological environment protection.

4.1 Planning and Constructing Regional and Special Pastoral Areas

According to the climatic conditions all over China and the annual average precipitation, China should divide and construct pastoral area and set up the appropriate grazing way to achieve balanced development in breeding according to the local territory characteristics to protect grassland resources and ecological environment eventually. Referring to ecological grassland division from Ren [ 9 ], we can divide Chinese grassland animal husbandry into the following areas, such as north desert scrub area, qinghai-tibetalpine region, onobrychisuiciaefolia, the northeast forest district, southwest karst mountain thickets grassland ecological economic zone and southeast evergreen broad leaved forest area. Planning and constructing regional and special pastoral areas is beneficial to promote the development of animal husbandry and ecological environment protection.

4.2 Planting Grass and Improving Pastures

To alleviate the prairie excessive load problem, Australia government promoted to cultivate grass artificially. This move can not only guarantee the supply of grass feed and improve the soil but accelerates the sustainable development. One of the methods to improve pasture construction is cultivating artificial grassland in the pastoral areas of China. In different area, herdsman should cultivate and plant suitable grass according to local climate and soil conditions. At the same time, the aid of soil testing and fertilizer technology on the shortage of trace elements in soilcan promote the growth of grass. In addition, the same pastoral areas should be divided into different farming area and the shepherd also should delimit the pasture use ratio to ensure the rest of the time grazing plot of grass growing.

4.3 Conducting Water Conservancy Facilities Construction

Water resources is the necessary means of production in the process of herbage growth, in pastoral areas with less precipitation, effective supply of water resources is a necessary condition for the sustainable development of animal husbandry. According to pasture area and grazing capacity, the farm family can select suitable water conservancy project, such as the construction of reservoirs, small reservoirs, deep well and so on. If the condition is appropriate, the government can also construct large water conservancy facilities.

4.4 Strengthening the Grassland Ecological Protection Ability and Passing Relevant Laws and Regulations for the Protection of Grassland Ecological Environment

The protection of the ecological environment is dependent on the government’s support and guidance. The Chinese government should be on the basis of the existing ecological construction projects, strengthen ecological environmental protection, return grazing land to grassland continually, moderate grazing capacity and implement the effective governance of desertification and sandstorm. In recent years, the Chinese government issued some laws and regulations about ecological environment protection and the construction of grassland, which has obtained the good effect. These measures played a significant role in promoting transformation of animal husbandry and ecological breeding. However, under the comprehensive effect of the inherent mode of production and the external economic environment, ecological protection consciousness of farmers still need to be further improved. The Chinese government should draw lessons from the Australian government’s relevant measures, such as strengthening the professional training of herdsmen, intensifying the communication and collaboration between different pastoral areas, etc.

5 Conclusions

This study argues that the animal husbandry of China should be based on the long-term view, pay attention to ecological environment protection in the process of animal husbandry and implement sustainable development strategy. Through summarizing the measures to coordinate the animal husbandry and ecological environment protection in Australian, combining with the current problems in the development of animal husbandry in China, this paper puts forward the planning and construction of regionalization and specialization, the construction of cultivated grassland in pastoral area and improvement of grassland, promoting water conservancy facilities construction, strengthening the protection of grassland ecology and introducing relevant laws and regulations for the protection of grassland ecological environment policy suggestions, meanwhile, should develop modern animal husbandry and improve the ecological environment to promote the sustainable development of animal husbandry in China ultimately.

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Acknowledgment

Funds for this research was provided by the Modern Agricultural Industry Technology System of China (CARS-41-K26) and China’s Livestock and Poultry Industry Research Project during the 13th Five-Year Plan.

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Zhu, Y., Li, S. (2016). Research on Coordinated Development Between Animal Husbandry and Ecological Environment Protection in Australia. In: Li, D., Li, Z. (eds) Computer and Computing Technologies in Agriculture IX. CCTA 2015. IFIP Advances in Information and Communication Technology, vol 478. Springer, Cham. https://doi.org/10.1007/978-3-319-48357-3_28

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Beyond3Rs   >  Research   >  Housing and Husbandry

Housing and Husbandry

We can go Beyond3Rs by focusing on how an animal is housed and cared for.

Laboratory animals spend the vast majority of their lives within their enclosures, rather than in experimental procedures. Aspects of housing and husbandry can profoundly affect both animal well-being and the quality of scientific data produced. Much progress has been made in recent decades, but there are opportunities to continue improving:

• The housing environment at minimum should meet all of the physical needs of an animal, allowing them the space to pursue species-specific behaviors.
• Environmental enrichment should be provided to give animals the opportunity to demonstrate behavioral agency (i.e., make choices and engage with their environment) and experience improved psychological well-being.
• Many animals find handling stressful, and handling stress can have substantial impacts on animal behavior and physiology. Care should be taken to use non-aversive methods whenever possible.
• Several aspects of life in a laboratory facility can impact the animals living there. For example, these might include room temperature, smells, vibrations from equipment, exposure to light, loud noises, cage cleaning, and being disturbed while sleeping. Some of these aspects might go unnoticed by humans, but can have profound impacts on animals.
• Inadequate housing environments or chronic stress can result in poor well-being, which may impact the validity of scientific outcomes. We are working to further establish how housing and husbandry practices may affect reproducibility and translation.

Refining housing and husbandry not only improves the humaneness of animal research, but mitigates confounding factors which can impact the reliability of results and the validity of animal models. To achieve refinements in housing and husbandry, it is important to promote a culture where we always strive to improve (e.g., by performing regular assessments of programs, and changing practices when presented with new evidence of better methods).

Prioritizing refinements to housing and husbandry takes us Beyond3Rs.

Research: Housing and Husbandry

Stressed out: providing laboratory animals with behavioral control to reduce the physiological effects of stress.

Brianna N Gaskill, Joseph P Garner (2017), Lab Animal

Laboratory animals experience a large amount of environmental stress. Chronic uncontrollable stress is widely acknowledged for its negative alterations to physiology. However, there is a lack in the understanding of how the laboratory environment affects animal physiology and behavior, particularly as it relates to characteristics of the human disease being modeled. Given the evidence on how stressors affect physiology, it is clear that efforts to model human physiology in animal models must consider animal stress as a confounding factor. We present evidence illustrating that providing captive animals with control or predictability is the best way to reduce the negative physiological effects of these difficult-to-manage stressors.

Read more >

Conventional laboratory housing increases morbidity and mortality in research rodents: results of a meta-analysis

Jessica Cait, Alissa Cait, R. Wilder Scott, Charlotte B. Winder & Georgia J. Mason (2022), BMC Biology

Over 120 million mice and rats are used annually in research, conventionally housed in shoebox-sized cages that restrict natural behaviours. This can reduce physical fitness, impair thermoregulation and reduce welfare. In humans, chronic stress has biological costs, increasing disease risks and potentially shortening life. This meta-analysis therefore tested the hypothesis that, compared to rodents in ‘enriched’ housing that better meets their needs, conventional housing increases stress-related morbidity and all-cause mortality. The hypothesis was supported: conventional housing significantly exacerbated disease severity (cancer, stroke, depression, cardiovascular disease, signs of anxiety) with medium to large effect sizes. Conventional housing appears sufficiently distressing to compromise rodent health, raising ethical and scientific concerns.

Nest Building as an Indicator of Health and Welfare in Laboratory Mice

Brianna N. Gaskill, Alicia Z. Karas, Joseph P. Garner, Kathleen R. Pritchett-Corning (2013), JOVE

The minimization and alleviation of suffering has moral and scientific implications. In order to mitigate this negative experience one must be able to identify when an animal is actually in distress. Pain, illness, or distress cannot be managed if unrecognized. The observation of nesting behavior shows promise as the basis of a species appropriate cage-side assessment tool for recognizing distress in mice. Here we demonstrate the utility of nest building behavior in laboratory mice as an ethologically relevant indicator of welfare. The methods presented can be successfully used to identify thermal stressors, aggressive cages, sickness, and pain. Observation of nest building behavior in mouse colonies provides a refinement to health and well-being assessment on a day to day basis.

Optimising reliability of mouse performance in behavioural testing: the major role of non-aversive handling

Kelly Gouveia, Jane L Hurst (2017), Scientific Reports

Picking up mice by the tail is aversive, stimulating stress and anxiety. Handling stress can be reduced substantially by using a handling tunnel, or cupping mice without restraint on the open hand. Here the authors use a habituation-dishabituation paradigm in which animals discriminate between two stimuli in successive trials. Tail-handled mice showed little willingness to explore and investigate test stimuli, leading to poor test performance that was only slightly improved by prior familiarisation. Mice handled by tunnel explored readily and showed robust responses to test stimuli regardless of prior familiarisation or stimulus location, though responses were more variable for cup handling. This study shows that non-aversive tunnel handling can substantially improve mouse performance in behavioural tests compared to traditional tail handling.

The critical issue for well-being and model quality is control, not of the animal, but by the animal. Through over-engineering animal housing we take away an animal's control of its environment, which in turn makes it fundamentally abnormal.

From "Introducing Therioepistomology"

Effects of Cage Enrichment on Behavior, Welfare and Outcome Variability in Female Mice

Jeremy D. Bailoo, Eimear Murphy, Maria Boada-Saña, Justin A. Varholick, Sara Hintze, Caroline Baussière, Kerstin C. Hahn, Christine Göpfert, Rupert Palme, Bernhard Voelkl, Hanno Würbel (2018), Frontiers in Behavioral Neuroscience

In mice, common laboratory housing conditions are associated with indicators of impaired welfare. Due to concerns that more complex environmental conditions might increase variation in experimental results, there has been considerable resistance to the implementation of environmental enrichment beyond the provision of nesting material. Here,  the authors systematically varied environmental enrichment across four levels: (1) bedding alone; (2) bedding + nesting material; (3) deeper bedding + nesting material + shelter + increased vertical space; and (4) semi-naturalistic conditions, including weekly changes of enrichment items. The greatest benefit was observed in animals housed with the greatest degree of enrichment: stereotypic behavior, anxiety, growth and stress physiology varied in a manner consistent with improved animal welfare compared to the other housing conditions with less enrichment. There was no indication that environmental enrichment increased variation in experimental results.

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Embracing Variability

Harmonizing animal and human research, spontaneous disease models, and biomarkers

Reproducibility and Translation

Experimental design, animal-to-human translation, and "the science of doing science"

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National Research Council (US) Committee for the Update of the Guide for the Care and Use of Laboratory Animals. Guide for the Care and Use of Laboratory Animals. 8th edition. Washington (DC): National Academies Press (US); 2011.

Guide for the Care and Use of Laboratory Animals. 8th edition.

• Hardcopy Version at National Academies Press

3 Environment, Housing, and Management

This chapter provides guidelines for the environment, housing, and management of laboratory animals used or produced for research, testing, and teaching. These guidelines are applicable across species and are relatively general; additional information should be sought about how to apply them to meet the specific needs of any species, strain, or use (see Appendix A for references). The chapter is divided into recommendations for terrestrial (page 42) and aquatic animals (page 77), as there are fundamental differences in their environmental requirements as well as animal husbandry, housing, and care needs. Although formulated specifically for vertebrate species, the general principles of humane animal care as set out in the Guide may also apply to invertebrate species.

The design of animal facilities combined with appropriate animal housing and management are essential contributors to animal well-being, the quality of animal research and production, teaching or testing programs involving animals, and the health and safety of personnel. An appropriate Program (see Chapter 2 ) provides environments, housing, and management that are well suited for the species or strains of animals maintained and takes into account their physical, physiologic, and behavioral needs, allowing them to grow, mature, and reproduce normally while providing for their health and well-being.

Fish, amphibians, and reptiles are poikilothermic animals: their core temperature varies with environmental conditions and they have limited ability (compared with birds and mammals) to metabolically maintain core temperature. The majority of poikilothermic laboratory animals are aquatic species—for example, fish and most amphibians—although some, such as reptiles and certain amphibian species, are terrestrial. Personnel working with aquatic animals should be familiar with management implications, e.g., the importance of providing appropriate temperature ranges for basic physiologic function.

• TERRESTRIAL ANIMALS

Terrestrial Environment

Microenvironment and macroenvironment.

The microenvironment of a terrestrial animal is the physical environment immediately surrounding it; that is, the primary enclosure such as the cage, pen, or stall. It contains all the resources with which the animals come directly in contact and also provides the limits of the animals’ immediate environment. The microenvironment is characterized by many factors, including illumination, noise, vibration, temperature, humidity, and gaseous and particulate composition of the air. The physical environment of the secondary enclosure, such as a room, a barn, or an outdoor habitat, constitutes the macroenvironment .

Microenvironment: The immediate physical environment surrounding the animal (i.e., the environment in the primary enclosure such as the cage, pen, or stall).

Although the microenvironment and the macroenvironment are generally related, the microenvironment can be appreciably different and affected by several factors, including the design of the primary enclosure and macroenvironmental conditions.

Macroenvironment: The physical environment of the secondary enclosure (e.g., a room, a barn, or an outdoor habitat).

Evaluation of the microenvironment of small enclosures can be difficult. Available data indicate that temperature, humidity, and concentrations of gases and particulate matter are often higher in the animal microenvironment than in the macroenvironment ( Besch 1980 ; Hasenau et al. 1993 ; Perkins and Lipman 1995 ; E. Smith et al. 2004 ), while light levels are usually lower. Microenvironmental conditions can directly affect physiologic processes and behavior and may alter disease susceptibility ( Baer et al. 1997 ; Broderson et al. 1976 ; Memarzadeh et al. 2004 ; Schoeb et al. 1982 ; Vesell et al. 1976 ).

Temperature and Humidity

Maintenance of body temperature within normal circadian variation is necessary for animal well-being. Animals should be housed within temperature and humidity ranges appropriate for the species, to which they can adapt with minimal stress and physiologic alteration.

The ambient temperature range in which thermoregulation occurs without the need to increase metabolic heat production or activate evaporative heat loss mechanisms is called the thermoneutral zone (TNZ) and is bounded by the lower and upper critical temperatures (LCTs and UCTs; Gordon 2005 ). To maintain body temperature under a given environmental temperature animals adjust physiologically (including their metabolism) and behaviorally (including their activity level and resource use). For example, the TNZ of mice ranges between 26°C and 34°C ( Gordon 1993 ); at lower temperatures, building nests and huddling for resting and sleeping allow them to thermoregulate by behaviorally controlling their microclimate. Although mice choose temperatures below their LCT of 26°C during activity periods, they strongly prefer temperatures above their LCT for maintenance and resting behaviors ( Gaskill et al. 2009 ; Gordon 2004 ; Gordon et al. 1998 ). Similar LCT values are found in the literature for other rodents, varying between 26–30°C for rats and 28–32°C for gerbils ( Gordon 1993 ). The LCTs of rabbits (15–20°C; Gonzalez et al. 1971 ) and cats and dogs (20–25°C) are slightly lower, while those of nonhuman primates and farm animals vary depending on the species. In general, dry-bulb temperatures in animal rooms should be set below the animals’ LCT to avoid heat stress. This, in turn, means that animals should be provided with adequate resources for thermoregulation (nesting material, shelter) to avoid cold stress. Adequate resources for thermoregulation are particularly important for newborn animals whose LCT is normally considerably higher than that of their adult conspecifics.

Environmental temperature and relative humidity can be affected by husbandry and housing design and can differ considerably between primary and secondary enclosures as well as within primary enclosures. Factors that contribute to variation in temperature and humidity between and within enclosures include housing design; construction material; enrichment devices such as shelters and nesting material; use of filter tops; number, age, type, and size of the animals in each enclosure; forced ventilation of enclosures; and the type and frequency of contact bedding changes ( Besch 1980 ).

Exposure to wide temperature and humidity fluctuations or extremes may result in behavioral, physiologic, and morphologic changes, which might negatively affect animal well-being and research performance as well as outcomes of research protocols ( Garrard et al. 1974 ; Gordon 1990 , 1993 ; Pennycuik 1967 ). These effects can be multigenerational ( Barnett 1965 , 1973 ).

The dry-bulb temperatures listed in Table 3.1 are broad and generally reflect tolerable limits for common adult laboratory animal species, provided they are housed with adequate resources for behavioral thermoregulation; temperatures should normally be selected and maintained with minimal fluctuation near the middle of these ranges. Depending on the specific housing system employed, the selection of appropriate macro- and microenvironmental temperatures will differ based on a variety of factors, including but not limited to the species or strain, age, numbers of animals in the enclosure, size and construction of the primary enclosure, and husbandry conditions (e.g., use/provision of contact bedding, nesting material and/or shelter, individually ventilated cages). Poikilotherms and young birds of some species generally require a thermal gradient in their primary enclosure to meet basic physiological processes. The temperature ranges shown may not apply to captive wild animals, wild animals maintained in their natural environment, or animals in outdoor enclosures that have the opportunity to adapt by being exposed to seasonal changes in ambient conditions.

Recommended Dry-Bulb Macroenvironmental Temperatures for Common Laboratory Animals.

Some conditions require increased environmental temperatures for housing (e.g., postoperative recovery, neonatal animals, rodents with hairless phenotypes, reptiles and amphibians at certain stages of reproduction). The magnitude of the temperature increase depends on housing details; sometimes raising the temperature in the microenvironment alone (e.g., by using heating pads for postoperative recovery or radiant heat sources for reptiles) rather than raising the temperature of the macroenvironment is sufficient and preferable.

Relative humidity should also be controlled, but not nearly as narrowly as temperature for many mammals; the acceptable range of relative humidity is considered to be 30% to 70% for most mammalian species. Microenvironmental relative humidity may be of greater importance for animals housed in a primary enclosure in which the environmental conditions differ greatly from those of the macroenvironment (e.g., in static filter-top [isolator] cages).

Some species may require conditions with high relative humidity (e.g., selected species of nonhuman primates, tropical reptiles, and amphibians; Olson and Palotay 1983 ). In mice, both abnormally high and low humidity may increase preweaning mortality ( Clough 1982 ). In rats, low relative humidity, especially in combination with temperature extremes, may lead to ringtail, a condition involving ischemic necrosis of the tail and sometimes toes ( Crippa et al. 2000 ; Njaa et al. 1957 ; Totten 1958 ). For some species, elevated relative humidity may affect an animal’s ability to cope with thermal extremes. Elevated microenvironmental relative humidity in rodent isolator cages may also lead to high intracage ammonia concentrations ( Corning and Lipman 1991 ; Hasenau et al. 1993 ), which can be irritating to the nasal passages and alter some biologic responses ( Gordon et al. 1980 ; Manninen et al. 1998 ). In climates where it is difficult to provide a sufficient level of environmental relative humidity, animals should be closely monitored for negative effects such as excessively flaky skin, ecdysis (molting) difficulties in reptiles, and desiccation stress in semiaquatic amphibians.

Ventilation and Air Quality

The primary purpose of ventilation is to provide appropriate air quality and a stable environment. Specifically, ventilation provides an adequate oxygen supply; removes thermal loads caused by the animals, personnel, lights, and equipment; dilutes gaseous and particulate contaminants including allergens and airborne pathogens; adjusts the moisture content and temperature of room air; and, where appropriate, creates air pressure differentials (directional air flow) between adjoining spaces. Importantly, ventilating the room (i.e., the macroenvironment) does not necessarily ensure adequate ventilation of an animal’s primary enclosure (i.e., the microenvironment), that is, the air to which the animal is actually exposed. The type of primary enclosure may considerably influence the differences between these two environments—for example, differences may be negligible when animals are housed in open caging or pens, whereas they can be significant when static isolator cages are used.

The volume and physical characteristics of the air supplied to a room and its diffusion pattern influence the ventilation of an animal’s primary enclosure and are important determinants of the animal’s microenvironment. The type and location of supply air diffusers and exhaust registers in relation to the number, arrangement, location, and type of primary and secondary enclosures affect how well the microenvironments are ventilated and should therefore be considered. The use of computer modeling for assessing those factors in relation to heat loading, air diffusion patterns, and particulate movement may be helpful in optimizing ventilation of micro- and macroenvironments ( Hughes and Reynolds 1995 ).

Direct exposure of animals to air moving at high velocity (drafts) should be avoided as the speed of air to which animals are exposed affects the rate at which heat and moisture are removed from an animal. For example, air at 20°C moving at 60 linear feet per minute (18.3 m/min) has a cooling effect of approximately 7°C ( Weihe 1971 ). Drafts can be particularly problematic for neonatal homeotherms (which may be hairless and have poorly developed mechanisms for thermoregulatory control), for mutants lacking fur, and for semiaquatic amphibians that can desiccate.

Provision of 10 to 15 fresh air changes per hour in animal housing rooms is an acceptable guideline to maintain macroenvironmental air quality by constant volume systems and may also ensure microenvironmental air quality. Although this range is effective in many animal housing settings, it does not take into account the range of possible heat loads; the species, size, and number of animals involved; the type of primary enclosure and bedding; the frequency of cage changing; the room dimensions; or the efficiency of air distribution both in the macroenvironment and between the macro- and microenvironments. In some situations, the use of such a broad guideline might overventilate a macroenvironment containing few animals, thereby wasting energy, or underventilate a microenvironment containing many animals, allowing heat, moisture, and pollutants to accumulate.

Modern heating, ventilation, and air conditioning (HVAC) systems (e.g., variable air volume, or VAV, systems) allow ventilation rates to be set in accordance with heat load and other variables. These systems offer considerable advantages with respect to flexibility and energy conservation, but should always provide a minimum amount of air exchange, as recommended for general use laboratories ( Bell 2008 ; DiBerardinis et al. 2009 ).

Individually ventilated cages (IVCs) and other types of specialized primary enclosures, that either directly ventilate the enclosure using filtered room air or are ventilated independently of the room, can effectively address animals’ ventilation requirements without the need to increase macroenvironmental ventilation. However, cautions mentioned above regarding high-velocity air should be considered ( Baumans et al. 2002 ; Krohn et al. 2003 ). Nevertheless, the macroenvironment should be ventilated sufficiently to address heat loads, particulates, odors, and waste gases released from primary enclosures ( Lipman 1993 ).

If ventilated primary enclosures have adequate filtration to address contamination risks, air exhausted from the microenvironment may be returned to the room in which animals are housed, although it is generally preferable to exhaust these systems directly into the building’s exhaust system to reduce heat load and macroenvironmental contamination.

Static isolation caging (without forced ventilation), such as that used in some types of rodent housing, restricts ventilation ( Keller et al. 1989 ). To compensate, it may be necessary to adjust husbandry practices, including sanitation and cage change frequency, selection of contact bedding, placement of cages in a secondary enclosure, animal densities in cages, and/or decrease in macroenvironmental relative humidity to improve the microenvironment and heat dissipation.

The use of recycled air to ventilate animal rooms may save energy but entails risks. Because many animal pathogens can be airborne or travel on fomites (e.g., dust), exhaust air recycled into HVAC systems that serve multiple rooms presents a risk of cross contamination. Recycling air from nonanimal use areas (e.g., some human occupancy areas and food, bedding, and supply storage areas) may require less intensive filtration or conditioning and pose less risk of infection. The risks in some situations, however, might be too great to consider recycling (e.g., in the case of non-human primates and biohazard areas). The exhaust air to be recycled should be filtered, at minimum, with 85–95% ASHRAE efficient filters to remove airborne particles before it is recycled ( NAFA 1996 ). Depending on the air source, composition, and proportion of recycled air used (e.g., ammonia and other gases emitted from excrement in recirculating air from animal rooms), consideration should also be given to filtering volatile substances. In areas that require filtration to ensure personnel and/or animal safety (e.g., hazardous containment holding), filter efficiency, loading, and integrity should be assessed.

The successful operation of any HVAC system requires regular preventive maintenance and evaluation, including measurement of its function at the level of the secondary enclosure. Such measurements should include supply and exhaust air volumes, fluctuation in temperature and relative humidity, and air pressure differentials between spaces as well as critical mechanical operating parameters.

Illumination

Light can affect the physiology, morphology, and behavior of various animals ( Azar et al. 2008 ; Brainard et al. 1986 ; Erkert and Grober 1986 ; Newbold et al. 1991 ; Tucker et al. 1984 ). Potential photostressors include inappropriate photoperiod, photointensity, and spectral quality of the light ( Stoskopf 1983 ).

Numerous factors can affect animals’ needs for light and should be considered when an appropriate illumination level is being established for an animal holding room. These include light intensity and wavelength as well as the duration of the animal’s current and prior exposure to light, and the animal’s pigmentation, circadian rhythm, body temperature, hormonal status, age, species, sex, and stock or strain ( Brainard 1989 ; Duncan and O’Steen 1985 ; O’Steen 1980 ; Saltarelli and Coppola 1979 ; Semple-Row-land and Dawson 1987 ; Wax 1977 ). More recent studies in rodents and primates have shown the importance of intrinsically photosensitive retinal ganglion cells (distinct from rods and cones) for neuroendocrine, circadian, and neurobehavioral regulation ( Berson et al. 2002 ; Hanifin and Brainard 2007 ). These cells can respond to light wavelengths that may differ from other photoreceptors and may influence the type of lighting, light intensity, and wavelength selected for certain types of research.

In general, lighting should be diffused throughout an animal holding area and provide sufficient illumination for the animals’ well-being while permitting good housekeeping practices, adequate animal inspection including for the bottom-most cages in racks, and safe working conditions for personnel. Light in animal holding rooms should provide for both adequate vision and neuroendocrine regulation of diurnal and circadian cycles ( Brainard 1989 ).

Photoperiod is a critical regulator of reproductive behavior in many animal species ( Brainard et al. 1986 ; Cherry 1987 ), so inadvertent light exposure during the dark cycle should be minimized or avoided. Because some species, such as chickens ( Apeldoorn et al. 1999 ), will not eat in low light or darkness, such illumination schedules should be limited to a duration that will not compromise their well-being. A time-controlled lighting system should be used to ensure a regular diurnal cycle, and system performance should be checked regularly to ensure proper cycling.

Most commonly used laboratory rodents are nocturnal. Because albino rodents are more susceptible to phototoxic retinopathy than other animals ( Beaumont 2002 ), they have been used as a basis for establishing room illumination levels ( Lanum 1979 ). Data for room light intensities for other animals, based on scientific studies, are not available. Light levels of about 325 lux (30-ft candles) approximately 1 m (3.3 ft) above the floor appear to be sufficient for animal care and do not cause clinical signs of phototoxic retinopathy in albino rats ( Bellhorn 1980 ). Levels up to 400 lux (37-ft candles) as measured in an empty room 1 m from the floor have been found to be satisfactory for rodents if management practices are used to prevent retinal damage in albinos ( Clough 1982 ). However, the light experience of an individual animal can affect its sensitivity to phototoxicity; light of 130–270 lux above the light intensity under which it was raised has been reported to be near the threshold of retinal damage in some individual albino rats according to histologic, morphometric, and electrophysiologic evidence ( Semple-Rowland and Dawson 1987 ). Some guidelines recommend a light intensity as low as 40 lux at the position of the animal in midcage ( NASA 1988 ). Rats and mice generally prefer cages with low light intensity ( Blom et al. 1996 ), and albino rats prefer areas with a light intensity of less than 25 lux ( Schlingmann et al. 1993a ). Young mice prefer much lower illumination than adults ( Wax 1977 ). For animals that have been shown to be susceptible to phototoxic retinopathy, light should be between 130 and 325 lux in the room at cage level.

Light intensity decreases with the square of the distance from its source. Thus the location of a cage on a rack affects the intensity of light to which the animals within are exposed. Light intensity may differ as much as 80-fold in transparent cages from the top to the bottom of a rack, and differences up to 20-fold have been recorded within a cage ( Schlingmann et al. 1993a , b ). Management practices, such as rotating cage position relative to the light source ( Greenman et al. 1982 ) or providing animals with ways to control their own light exposure by behavioral means (e.g., nesting or bedding material adequate for tunneling), can reduce inappropriate light stimulation. Variable-intensity lights are often used to accommodate the needs of research protocols, certain animal species, and energy conservation. However, such a system should also provide for the observation and care of the animals. Caution should be exercised as increases in daytime room illumination for maintenance purposes have been shown to change photoreceptor physiology and can alter circadian regulation ( NRC 1996 ; Reme et al. 1991 ; Terman et al. 1991 ).

Noise and Vibration

Noise produced by animals and animal care activities is inherent in the operation of an animal facility ( Pfaff and Stecker 1976 ) and noise control should be considered in facility design and operation ( Pekrul 1991 ). Assessment of the potential effects of noise on an animal warrants consideration of the intensity, frequency, rapidity of onset, duration, and vibration potential of the sound and the hearing range, noise exposure history, and sound effect susceptibility of the species, stock, or strain. Similarly, occupational exposure to animal or animal care practices that generate noise may be of concern for personnel and, if of sufficient intensity, may warrant hearing protection.

Separation of human and animal areas minimizes disturbances to both human and animal occupants of the facility. Noisy animals, such as dogs, swine, goats, nonhuman primates, and some birds (e.g., zebra finches), should be housed away from quieter animals, such as rodents, rabbits, and cats. Environments should be designed to accommodate animals that make noise rather than resorting to methods of noise reduction. Exposure to sound louder than 85 dB can have both auditory and nonauditory effects ( Fletcher 1976 ; Peterson 1980 )—for example, eosinopenia, increased adrenal gland weights, and reduced fertility in rodents ( Geber et al. 1966 ; Nayfield and Besch 1981 ; Rasmussen et al. 2009 ), and increased blood pressure in nonhuman primates ( Peterson et al. 1981 )—and may necessitate hearing protection for personnel ( OSHA 1998 ). Many species can hear sound frequencies inaudible to humans ( Brown and Pye 1975 ; Heffner and Heffner 2007 ); rodents, for example, are very sensitive to ultrasound ( Olivier et al. 1994 ). The potential effects of equipment (such as video display terminals; Sales 1991 ; Sales et al. 1999 ) and materials that produce noise in the hearing range of nearby animals can thus become an uncontrolled variable for research experiments and should therefore be carefully considered ( Turner et al. 2007 ; Willott 2007 ). To the greatest extent possible, activities that generate noise should be conducted in rooms or areas separate from those used for animal housing.

Because changes in patterns of sound exposure have different effects on different animals ( Armario et al. 1985 ; Clough 1982 ), personnel should try to minimize the production of unnecessary noise. Excessive and intermittent noise can be minimized by training personnel in alternatives to noisy practices, the use of cushioned casters and bumpers on carts, trucks, and racks, and proper equipment maintenance (e.g., castor lubrication). Radios, alarms, and other sound generators should not be used in animal rooms unless they are part of an approved protocol or enrichment program. Any radios or sound generators used should be switched off at the end of the working day to minimize associated adverse physiologic changes ( Baldwin 2007 ).

While some vibration is inherent to every facility and animal housing condition, excessive vibration has been associated with biochemical and reproductive changes in laboratory animals ( Briese et al. 1984 ; Carman et al. 2007 ) and can become an uncontrolled variable for research experiments. The source of vibrations may be located within or outside the animal facility. In the latter case, groundborne vibration may affect both the structure and its contents, including animal racks and cages. Housing systems with moving components, such as ventilated caging system blowers, may create vibrations that could affect the animals housed within, especially if not functioning properly. Like noise, vibration varies with intensity, frequency, and duration. A variety of techniques may be used to isolate groundborne (see Chapter 5 ) and equipment-generated vibration ( Carman et al. 2007 ). Attempts should be made to minimize the generation of vibration, including from humans, and excessive vibration should be avoided.

Terrestrial Housing

Microenvironment (primary enclosure).

All animals should be housed under conditions that provide sufficient space as well as supplementary structures and resources required to meet physical, physiologic, and behavioral needs. Environments that fail to meet the animals’ needs may result in abnormal brain development, physiologic dysfunction, and behavioral disorders ( Garner 2005 ; van Praag et al. 2000 ; Würbel 2001 ) that may compromise both animal well-being and scientific validity. The primary enclosure or space may need to be enriched to prevent such effects (see also section on Environmental Enrichment).

An appropriate housing space or enclosure should also account for the animals’ social needs. Social animals should be housed in stable pairs or groups of compatible individuals unless they must be housed alone for experimental reasons or because of social incompatibility (see also section on Behavioral and Social Management). Structural adjustments are frequently required for social housing (e.g., perches, visual barriers, refuges), and important resources (e.g., food, water, and shelter) should be provided in such a way that they cannot be monopolized by dominant animals (see also section on Environmental Enrichment).

The primary enclosure should provide a secure environment that does not permit animal escape and should be made of durable, nontoxic materials that resist corrosion, withstand the rigors of cleaning and regular handling, and are not detrimental to the health and research use of the animals. The enclosure should be designed and manufactured to prevent accidental entrapment of animals or their appendages and should be free of sharp edges or projections that could cause injury to the animals or personnel. It should have smooth, impervious surfaces with minimal ledges, angles, corners, and overlapping surfaces so that accumulation of dirt, debris, and moisture is minimized and cleaning and disinfecting are not impaired. All enclosures should be kept in good repair to prevent escape of or injury to animals, promote physical comfort, and facilitate sanitation and servicing. Rusting or oxidized equipment, which threatens the health or safety of animals, needs to be repaired or replaced. Less durable materials, such as wood, may be appropriate in select situations, such as outdoor corrals, perches, climbing structures, resting areas, and perimeter fences for primary enclosures. Wooden items may need to be replaced periodically because of damage or difficulties with sanitation. Painting or sealing wood surfaces with nontoxic materials may improve durability in many instances.

Flooring should be solid, perforated, or slatted with a slip-resistant surface. In the case of perforated or slatted floors, the holes and slats should have smooth edges. Their size and spacing need to be commensurate with the size of the housed animal to minimize injury and the development of foot lesions. If wire-mesh flooring is used, a solid resting area may be beneficial, as this floor type can induce foot lesions in rodents and rabbits ( Drescher 1993 ; Fullerton and Gilliatt 1967 ; Rommers and Meijerhof 1996 ). The size and weight of the animal as well as the duration of housing on wire-mesh floors may also play a role in the development of this condition ( Peace et al. 2001 ). When given the choice, rodents prefer solid floors (with bedding) to grid or wire-mesh flooring ( Blom et al. 1996 ; Manser et al. 1995 , 1996 ).

Animals should have adequate bedding substrate and/or structures for resting and sleeping. For many animals (e.g., rodents) contact bedding expands the opportunities for species-typical behavior such as foraging, digging, burrowing, and nest building ( Armstrong et al. 1998 ; Ivy et al. 2008 ). Moreover, it absorbs urine and feces to facilitate cleaning and sanitation. If provided in sufficient quantity to allow nest building or burrowing, bedding also facilitates thermoregulation ( Gordon 2004 ). Breeding animals should have adequate nesting materials and/or substitute structures based on species-specific requirements (mice: Sherwin 2002 ; rats: Lawlor 2002 ; gerbils: Waiblinger 2002 ).

Specialized housing systems (e.g., isolation-type cages, IVCs, and gnotobiotic 1 isolators) are available for rodents and certain species. These systems, designed to minimize the spread of airborne particles between cages or groups of cages, may require different husbandry practices, such as alterations in the frequency of bedding change, the use of aseptic handling techniques, and specialized cleaning, disinfecting, or sterilization regimens to prevent microbial transmission by other than airborne routes.

Appropriate housing strategies for a particular species should be developed and implemented by the animal care management, in consultation with the animal user and veterinarian, and reviewed by the IACUC. Housing should provide for the animals’ health and well-being while being consistent with the intended objectives of animal use. Expert advice should be sought when new species are housed or when there are special requirements associated with the animals or their intended use (e.g., genetically modified animals, invasive procedures, or hazardous agents). Objective assessments should be made to substantiate the adequacy of the animal’s environment, housing, and management. Whenever possible, routine procedures for maintaining animals should be documented to ensure consistency of management and care.

Environmental Enrichment

The primary aim of environmental enrichment is to enhance animal well-being by providing animals with sensory and motor stimulation, through structures and resources that facilitate the expression of species-typical behaviors and promote psychological well-being through physical exercise, manipulative activities, and cognitive challenges according to species-specific characteristics ( NRC 1998a ; Young 2003 ). Examples of enrichment include structural additions such as perches and visual barriers for nonhuman primates ( Novak et al. 2007 ); elevated shelves for cats ( Overall and Dyer 2005 ; van den Bos and de Cock Buning 1994 ) and rabbits ( Stauffacher 1992 ); and shelters for guinea pigs ( Baumans 2005 ), as well as manipulable resources such as novel objects and foraging devices for nonhuman primates; manipulable toys for nonhuman primates, dogs, cats, and swine; wooden chew sticks for some rodent species; and nesting material for mice ( Gaskill et al. 2009 ; Hess et al. 2008 ; Hubrecht 1993 ; Lutz and Novak 2005 ; Olsson and Dahlborn 2002 ). Novelty of enrichment through rotation or replacement of items should be a consideration; however, changing animals’ environment too frequently may be stressful.

Well-conceived enrichment provides animals with choices and a degree of control over their environment, which allows them to better cope with environmental stressors ( Newberry 1995 ). For example, visual barriers allow nonhuman primates to avoid social conflict; elevated shelves for rabbits and shelters for rodents allow them to retreat in case of disturbances ( Baumans 1997 ; Chmiel and Noonan 1996 ; Stauffacher 1992 ); and nesting material and deep bedding allow mice to control their temperature and avoid cold stress during resting and sleeping ( Gaskill et al. 2009 ; Gordon 1993 , 2004 ).

Not every item added to the animals’ environment benefits their well-being. For example, marbles are used as a stressor in mouse anxiety studies ( De Boer and Koolhaas 2003 ), indicating that some items may be detrimental to well-being. For nonhuman primates, novel objects can increase the risk of disease transmission ( Bayne et al. 1993 ); foraging devices can lead to increased body weight ( Brent 1995 ); shavings can lead to allergies and skin rashes in some individuals; and some objects can result in injury from foreign material in the intestine ( Hahn et al. 2000 ). In some strains of mice, cage dividers and shelters have induced overt aggression in groups of males, resulting in social stress and injury (e.g., Bergmann et al. 1994 ; Haemisch et al. 1994 ). Social stress was most likely to occur when resources were monopolized by dominant animals ( Bergmann et al. 1994 ).

Enrichment programs should be reviewed by the IACUC, researchers, and veterinarian on a regular basis to ensure that they are beneficial to animal well-being and consistent with the goals of animal use. They should be updated as needed to ensure that they reflect current knowledge. Personnel responsible for animal care and husbandry should receive training in the behavioral biology of the species they work with to appropriately monitor the effects of enrichment as well as identify the development of adverse or abnormal behaviors.

Like other environmental factors (such as space, light, noise, temperature, and animal care procedures), enrichment affects animal phenotype and may affect the experimental outcome. It should therefore be considered an independent variable and appropriately controlled.

Some scientists have raised concerns that environmental enrichment may compromise experimental standardization by introducing variability, adding not only diversity to the animals’ behavioral repertoire but also variation to their responses to experimental treatments (e.g., Bayne 2005 ; Eskola et al. 1999 ; Gärtner 1999 ; Tsai et al. 2003 ). A systematic study in mice did not find evidence to support this viewpoint ( Wolfer et al. 2004 ), indicating that housing conditions can be enriched without compromising the precision or reproducibility of experimental results. Further research in other species may be needed to confirm this conclusion. However, it has been shown that conditions resulting in higher-stress reactivity increase variation in experimental data (e.g., Macrì et al. 2007 ). Because adequate environmental enrichment may reduce anxiety and stress reactivity ( Chapillon et al. 1999 ), it may also contribute to higher test sensitivity and reduced animal use ( Baumans 1997 ).

Sheltered or Outdoor Housing

Sheltered or outdoor housing (e.g., barns, corrals, pastures, islands) is a primary housing method for some species and is acceptable in many situations. Animals maintained in outdoor runs, pens, or other large enclosures must have protection from extremes in temperature or other harsh weather conditions and adequate opportunities for retreat (for subordinate animals). These goals can normally be achieved by providing windbreaks, species-appropriate shelters, shaded areas, areas with forced ventilation, heat-radiating structures, and/or means of retreat to conditioned spaces, such as an indoor portion of a run. Shelters should be large enough to accommodate all animals housed in the enclosure, be accessible at all times to all animals, have sufficient ventilation, and be designed to prevent buildup of waste materials and excessive moisture. Houses, dens, boxes, shelves, perches, and other furnishings should be constructed in a manner and made of materials that allow cleaning or replacement in accord with generally accepted husbandry practices.

Floors or ground-level surfaces of outdoor housing facilities may be covered with dirt, absorbent bedding, sand, gravel, grass, or similar material that can be removed or replaced when needed to ensure appropriate sanitation. Excessive buildup of animal waste and stagnant water should be avoided by, for example, using contoured or drained surfaces. Other surfaces should be able to withstand the elements and be easily maintained.

Successful management of outdoor housing relies on stable social groups of compatible animals; sufficient and species-appropriate feeding and resting places; an adequate acclimation period in advance of seasonal changes when animals are first introduced to outdoor housing; training of animals to cooperate with veterinary and investigative personnel (e.g., to enter chutes or cages for restraint or transport); and adequate security via a perimeter fence or other means.

Naturalistic Environments

Areas such as pastures and islands may provide a suitable environment for maintaining or producing animals and for some types of research. Their use results in the loss of some control over nutrition, health care and surveillance, and pedigree management. These limitations should be balanced against the benefits of having the animals live in more natural conditions. Animals should be added to, removed from, and returned to social groups in this setting with appropriate consideration of the effects on the individual animals and on the group. Adequate supplies of food, fresh water, and natural or constructed shelter should be ensured.

General Considerations for All Animals An animal’s space needs are complex and consideration of only the animal’s body weight or surface area may be inadequate. Important considerations for determining space needs include the age and sex of the animal(s), the number of animals to be cohoused and the duration of the accommodation, the use for which the animals are intended (e.g., production vs. experimentation), and any special needs they may have (e.g., vertical space for arboreal species or thermal gradient for poikilotherms). In many cases, for example, adolescent animals, which usually weigh less than adults but are more active, may require more space relative to body weight ( Ikemoto and Panksepp 1992 ). Group-housed, social animals can share space such that the amount of space required per animal may decrease with increasing group size; thus larger groups may be housed at slightly higher stocking densities than smaller groups or individual animals. Socially housed animals should have sufficient space and structural complexity to allow them to escape aggression or hide from other animals in the pair or group. Breeding animals will require more space, particularly if neonatal animals will be raised together with their mother or as a breeding group until weaning age. Space quality also affects its usability. Enclosures that are complex and environmentally enriched may increase activity and facilitate the expression of species-specific behaviors, thereby increasing space needs. Thus there is no ideal formula for calculating an animal’s space needs based only on body size or weight and readers should take the performance indices discussed in this section into consideration when utilizing the species-specific guidelines presented in the following pages.

Consideration of floor area alone may not be sufficient in determining adequate cage size; with some species, cage volume and spatial arrangement may be of greater importance. In this regard, the Guide may differ from the US Animal Welfare Regulations (AWRs) or other guidelines. The height of an enclosure can be important to allow for expression of species-specific behaviors and postural adjustments. Cage height should take into account the animal’s typical posture and provide adequate clearance for the animal from cage structures, such as feeders and water devices. Some species—for example, nonhuman primates, cats, and arboreal animals—use the vertical dimensions of the cage to a greater extent than the floor. For these animals, the ability to stand or to perch with adequate vertical space to keep their body, including their tail, above the cage floor can improve their well-being ( Clarence et al. 2006 ; MacLean et al. 2009 ).

Space allocations should be assessed, reviewed, and modified as necessary by the IACUC considering the performance indices (e.g., health, reproduction, growth, behavior, activity, and use of space) and special needs determined by the characteristics of the animal strain or species (e.g., obese, hyperactive, or arboreal animals) and experimental use (e.g., animals in long-term studies may require greater and more complex space). At a minimum, animals must have enough space to express their natural postures and postural adjustments without touching the enclosure walls or ceiling, be able to turn around, and have ready access to food and water. In addition, there must be sufficient space to comfortably rest away from areas soiled by urine and feces. Floor space taken up by food bowls, water containers, litter boxes, and enrichment devices (e.g., novel objects, toys, foraging devices) should not be considered part of the floor space.

The space recommendations presented here are based on professional judgment and experience. They should be considered the minimum for animals housed under conditions commonly found in laboratory animal housing facilities. Adjustments to the amount and arrangement of space recommended in the following tables should be reviewed and approved by the IACUC and should be based on performance indices related to animal well-being and research quality as described in the preceding paragraphs, with due consideration of the AWRs and PHS Policy and other applicable regulations and standards.

It is not within the scope of the Guide to discuss the housing requirements of all species used in research. For species not specifically indicated, advice should be sought from the scientific literature and from species-relevant experts.

Laboratory Rodents Table 3.2 lists recommended minimum space for commonly used laboratory rodents housed in groups. If they are housed singly or in small groups or exceed the weights in the table, more space per animal may be required, while larger groups may be housed at slightly higher densities.

Recommended Minimum Space for Commonly Used Laboratory Rodents Housed in Groups.

Studies have recently evaluated space needs and the effects of social housing, group size, and density ( Andrade and Guimaraes 2003 ; Bartolomucci et al. 2002 , 2003 ; Georgsson et al. 2001 ; Gonder and Laber 2007 ; Perez et al. 1997 ; A.L. Smith et al. 2004 ), age ( Arakawa 2005 ; Davidson et al. 2007 ; Yildiz et al. 2007 ), and housing conditions ( Gordon et al. 1998 ; Van Loo et al. 2004 ) for many different species and strains of rodents, and have reported varying effects on behavior (such as aggression) and experimental outcomes ( Karolewicz and Paul 2001 ; Laber et al. 2008 ; McGlone et al. 2001 ; Rock et al. 1997 ; Smith et al. 2005 ; Van Loo et al. 2001 ). However, it is difficult to compare these studies due to the study design and experimental variables that have been measured. For example, variables that may affect the animals’ response to different cage sizes and housing densities include, but are not limited to, species, strain (and social behavior of the strain), phenotype, age, gender, quality of the space (e.g., vertical access), and structures placed in the cage. These issues remain complex and should be carefully considered when housing rodents.

Other Common Laboratory Animals Tables 3.3 and 3.4 list recommended minimum space for other common laboratory animals and for avian species. These allocations are based, in general, on the needs of pair- or group-housed animals. Space allocations should be reevaluated to provide for enrichment or to accommodate animals that exceed the weights in the tables, and should be based on species characteristics, behavior, compatibility of the animals, number of animals, and goals of the housing situation ( Held et al. 1995 ; Lupo et al. 2000 ; Raje 1997 ; Turner et al. 1997 ). Singly housed animals may require more space per animal than that recommended for group-housed animals, while larger groups may be housed at slightly higher densities. For cats, dogs, and some rabbits, housing enclosures that allow greater freedom of movement and less restricted vertical space are preferred (e.g., kennels, runs, or pens instead of cages). Dogs and cats, especially when housed individually or in smaller enclosures ( Bayne 2002 ), should be allowed to exercise and provided with positive human interaction. Species-specific plans for housing and management should be developed. Such plans should also include strategies for environmental enrichment.

Recommended Minimum Space for Rabbits, Cats, and Dogs Housed in Pairs or Groups.

Recommended Minimum Space for Avian Species Housed in Pairs or Groups.

Nonhuman Primates The recommended minimum space for nonhuman primates detailed in Table 3.5 is based on the needs of pair- or group-housed animals. Like all social animals, nonhuman primates should normally have social housing (i.e., in compatible pairs or in larger groups of compatible animals) ( Hotchkiss and Paule 2003 ; NRC 1998a ; Weed and Watson 1998 ; Wolfensohn 2004 ). Group composition is critical and numerous species-specific factors such as age, behavioral repertoire, sex, natural social organization, breeding requirements, and health status should be taken into consideration when forming a group. In addition, due to conformational differences of animals within groups, more space or height may be required to meet the animals’ physical and behavioral needs. Therefore, determination of the appropriate cage size is not based on body weight alone, and professional judgment is paramount in making such determinations ( Kaufman et al. 2004 ; Williams et al. 2000 ).

Recommended Minimum Space for Nonhuman Primates Housed in Pairs or Groups.

If it is necessary to house animals singly—for example, when justified for experimental purposes, for provision of veterinary care, or for incompatible animals—this arrangement should be for the shortest duration possible. If single animals are housed in small enclosures, an opportunity for periodic release into larger enclosures with additional enrichment items should be considered, particularly for animals housed singly for extended periods of time. Singly housed animals may require more space per animal than recommended for pair- or group-housed animals, while larger groups may be housed at slightly higher densities. Because of the many physical and behavioral characteristics of nonhuman primate species and the many factors to consider when using these animals in a biomedical research setting, species-specific plans for housing and management should be developed. Such plans should include strategies for environmental and psychological enrichment.

Agricultural Animals Table 3.6 lists recommended minimum space for agricultural animals commonly used in a laboratory setting. As social animals, they should be housed in compatible pairs or larger groups of compatible animals. When animals exceed the weights in the table, more space is required. For larger animals (particularly swine) it is important that the configuration of the space allow the animals to turn around and move freely ( Becker et al. 1989 ; Bracke et al. 2002 ). Food troughs and water devices should be provided in sufficient numbers to allow ready access for all animals. Singly housed animals may require more space than recommended in the table to enable them to turn around and move freely without touching food or water troughs, have ready access to food and water, and have sufficient space to comfortably rest away from areas soiled by urine and feces.

Recommended Minimum Space for Agricultural Animals.

Terrestrial Management

Behavioral and social management.

Activity Animal Activity typically implies motor activity but also includes cognitive activity and social interaction. Animals’ natural behavior and activity profile should be considered during evaluation of suitable housing or behavioral assessment.

Animals maintained in a laboratory environment are generally restricted in their activities compared to free-ranging animals. Forced activity for reasons other than attempts to meet therapeutic or approved protocol objectives should be avoided. High levels of repetitive, unvarying behavior (stereotypies, compulsive behaviors) may reflect disruptions of normal behavioral control mechanisms due to housing conditions or management practices ( Garner 2005 ; NRC 1998a ).

Dogs, cats, rabbits, and many other animals benefit from positive human interaction ( Augustsson et al. 2002 ; Bayne et al. 1993 ; McCune 1997 ; Poole 1998 ; Rennie and Buchanan-Smith 2006 ; Rollin 1990 ). Dogs can be given additional opportunities for activity by being walked on a leash, having access to a run, or being moved into areas for social contact, play, or exploration ( Wolff and Rupert 1991 ). Loafing areas, exercise lots, and pastures are suitable for large farm animals, such as sheep, horses, and cattle.

Social Environment Appropriate social interactions among members of the same species (conspecifics) are essential to normal development and well-being ( Bayne et al. 1995 ; Hall 1998 ; Novak et al. 2006 ). When selecting a suitable social environment, attention should be given to whether the animals are naturally territorial or communal and whether they should be housed singly, in pairs, or in groups. An understanding of species-typical natural social behavior (e.g., natural social composition, population density, ability to disperse, familiarity, and social ranking) is key to successful social housing.

Not all members of a social species are necessarily socially compatible. Social housing of incompatible animals can induce chronic stress, injury, and even death. In some species, social incompatibility may be sex biased; for example, male mice are generally more prone to aggression than female mice, and female hamsters are generally more aggressive than male hamsters. Risks of social incompatibility are greatly reduced if the animals to be grouped are raised together from a young age, if group composition remains stable, and if the design of the animals’ enclosure and their environmental enrichment facilitate the avoidance of social conflicts. Social stability should be carefully monitored; in cases of severe or prolonged aggression, incompatible individuals need to be separated.

For some species, developing a stable social hierarchy will entail antagonistic interactions between pair or group members, particularly for animals introduced as adults. Animals may have to be introduced to each other over a period of time and should be monitored closely during this introductory period and thereafter to ensure compatibility.

Single housing of social species should be the exception and justified based on experimental requirements or veterinary-related concerns about animal well-being. In these cases, it should be limited to the minimum period necessary, and where possible, visual, auditory, olfactory, and tactile contact with compatible conspecifics should be provided. In the absence of other animals, enrichment should be offered such as positive interaction with the animal care staff and additional enrichment items or addition of a companion animal in the room or housing area. The need for single housing should be reviewed on a regular basis by the IACUC and veterinarian.

Procedural Habituation and Training of Animals Habituating animals to routine husbandry or experimental procedures should be encouraged whenever possible as it may assist the animal to better cope with a captive environment by reducing stress associated with novel procedures or people. The type and duration of habituation needed will be determined by the complexity of the procedure. In most cases, principles of operant conditioning may be employed during training sessions, using progressive behavioral shaping, to induce voluntary cooperation with procedures ( Bloomsmith et al. 1998 ; Laule et al. 2003 ; NRC 2006a ; Reinhardt 1997 ).

Food Animals should be fed palatable, uncontaminated diets that meet their nutritional and behavioral needs at least daily, or according to their particular requirements, unless the protocol in which they are being used requires otherwise. Subcommittees of the National Research Council Committee on Animal Nutrition have prepared comprehensive reports of the nutrient requirements of laboratory animals ( NRC 1977 , 1982 , 1993 , 1994 , 1995a , 1998b , 2000 , 2001 , 2003a , 2006b , 2007 ); these publications consider issues of quality assurance, freedom from chemical or microbial contaminants and natural toxicants in feedstuffs, bioavailability of nutrients in feeds, and palatability.

There are several types of diets classified by the degree of refinement of their ingredients. Natural-ingredient diets are formulated with agricultural products and byproducts and are commercially available for all species commonly used in the laboratory. Although not a significant factor in most instances, the nutrient composition of ingredients varies, and natural ingredients may contain low levels of naturally occurring or artificial contaminants ( Ames et al. 1993 ; Knapka 1983 ; Newberne 1975 ; NRC 1996 ; Thigpen et al. 1999 , 2004 ). Contaminants such as pesticide residues, heavy metals, toxins, carcinogens, and phytoestrogens may be at levels that induce few or no health sequelae yet may have subtle effects on experimental results ( Thigpen et al. 2004 ). Certified diets that have been assayed for contaminants are commercially available for use in select studies, such as preclinical toxicology, conducted in compliance with FDA Good Laboratory Practice standards ( CFR 2009 ). Purified diets are refined such that each ingredient contains a single nutrient or nutrient class; they have less nutrient concentration variability and the potential for chemical contamination is lower. Chemically defined diets contain the most elemental ingredients available, such as individual amino acids and specific sugars ( NRC 1996 ). The latter two types of diet are more likely to be used for specific types of studies in rodents but are not commonly used because of cost, lower palatability, and a reduced shelf life.

Animal colony managers should be judicious when purchasing, transporting, storing, and handling food to minimize the introduction of diseases, parasites, potential disease vectors (e.g., insects and other vermin), and chemical contaminants in animal colonies. Purchasers are encouraged to consider manufacturers’ and suppliers’ procedures and practices (e.g., storage, vermin control, and handling) for protecting and ensuring diet quality. Institutions should urge feed vendors to periodically provide data from laboratory-based feed analyses for critical nutrients. The user should know the date of manufacture and other factors that affect the food’s shelf life. Stale food or food transported and stored inappropriately can become deficient in nutrients. Upon receipt, bags of feed should be examined to ensure that they are intact and unstained to help ensure that their contents have not been potentially exposed to vermin, penetrated by liquids, or contaminated. Careful attention should be paid to quantities received in each shipment, and stock should be rotated so that the oldest food is used first.

Areas in which diets and diet ingredients are processed or stored should be kept clean and enclosed to prevent the entry of pests. Food stocks should be stored off the floor on pallets, racks, or carts in a manner that facilitates sanitation. Opened bags of food should be stored in vermin-proof containers to minimize contamination and to avoid the potential spread of pathogens. Exposure to elevated storage room temperatures, extremes in relative humidity, unsanitary conditions, and insects and other vermin hastens food deterioration. Storage of natural-ingredient diets at less than 21°C (70°F) and below 50% relative humidity is recommended. Precautions should be taken if perishable items—such as meats, fruits, and vegetables and some specialty diets (e.g., select medicated or high-fat diets)—are fed, because storage conditions may lead to variation in food quality.

Most natural-ingredient, dry laboratory animal diets stored properly can be used up to 6 months after manufacture. Nonstabilized vitamin C in manufactured feeds generally has a shelf life of only 3 months, but commonly used stabilized forms can extend the shelf life of feed. Refrigeration preserves nutritional quality and lengthens shelf life, but food storage time should be reduced to the lowest practical period and the manufacturers’ recommendations considered. Purified and chemically defined diets are often less stable than natural-ingredient diets and their shelf life is usually less than 6 months ( Fullerton et al. 1982 ); they should be stored at 4°C (39°F) or lower.

Irradiated and fortified autoclavable diets are commercially available and are commonly used for axenic and microbiologically defined rodents, and immunodeficient animals ( NRC 1996 ). The use of commercially fortified autoclavable diets ensures that labile vitamin content is not compromised by steam and/or heat ( Caulfield et al. 2008 ; NRC 1996 ). But consideration should be given to the impact of autoclaving on pellets as it may affect their hardness and thus palatability and also lead to chemical alteration of ingredients ( Thigpen et al. 2004 ; Twaddle et al. 2004 ). The date of sterilization should be recorded and the diet used quickly.

Feeders should be designed and placed to allow easy access to food and to minimize contamination with urine and feces, and maintained in good condition. When animals are housed in groups, there should be enough space and enough feeding points to minimize competition for food and ensure access to food for all animals, especially if feed is restricted as part of the protocol or management routine. Food storage containers should not be transferred between areas that pose different risks of contamination without appropriate treatment, and they should be cleaned and sanitized regularly.

Management of caloric intake is an accepted practice for long-term housing of some species, such as some rodents, rabbits, and nonhuman primates, and as an adjunct to some clinical, experimental, and surgical procedures (afor more discussion of food and fluid regulation as an experimental tool see Chapter 2 and NRC 2003a ). Benefits of moderate caloric restriction in some species may include increased longevity and reproduction, and decreased obesity, cancer rates, and neurogenerative disorders ( Ames et al. 1993 ; Colman et al. 2009 ; Keenan et al. 1994 , 1996 ; Lawler et al. 2008 ; Weindruch and Walford 1988 ).

Under standard housing conditions, changes in biologic needs commensurate with aging should be taken into consideration. For example, there is good evidence that mice and rats with continuous access to food can become obese, with attendant metabolic and cardiovascular changes such as insulin resistance and higher blood pressure ( Martin et al. 2010 ). These and other changes along with a more sedentary lifestyle and lack of exercise increase the risk of premature death (ibid.). Caloric management, which may affect physiologic adaptations and alter metabolic responses in a species-specific manner ( Leveille and Hanson 1966 ), can be achieved by reducing food intake or by stimulating exercise.

In some species (e.g., nonhuman primates) and on some occasions, varying nutritionally balanced diets and providing “treats,” including fresh fruit and vegetables, can be appropriate and improve well-being. Scattering food in the bedding or presenting part of the diet in ways that require the animals to work for it (e.g., puzzle feeders for nonhuman primates) gives the animals the opportunity to forage, which, in nature, normally accounts for a large proportion of their daily activity. A diet should be nutritionally balanced; it is well documented that many animals offered a choice of unbalanced or balanced foods do not select a balanced diet and become malnourished or obese through selection of high-energy, low-protein foods ( Moore 1987 ). Abrupt changes in diet, which can be difficult to avoid at weaning, should be minimized because they can lead to digestive and metabolic disturbances; these changes occur in omnivores and carnivores, but herbivores ( Eadie and Mann 1970 ) are especially sensitive.

Water Animals should have access to potable, uncontaminated drinking water according to their particular requirements. Water quality and the definition of potable water can vary with locality ( Homberger et al. 1993 ). Periodic monitoring for pH, hardness, and microbial or chemical contamination may be necessary to ensure that water quality is acceptable, particularly for use in studies in which normal components of water in a given locality can influence the results. Water can be treated or purified to minimize or eliminate contamination when protocols require highly purified water. The selection of water treatments should be carefully considered because many forms of water treatment have the potential to cause physiologic alterations, reduction in water consumption, changes in microflora, or effects on experimental results ( Fidler 1977 ; Hall et al. 1980 ; Hermann et al. 1982 ; Homberger et al. 1993 ; NRC 1996 ).

Watering devices, such as drinking tubes and automated water delivery systems, should be checked frequently to ensure appropriate maintenance, cleanliness, and operation. Animals sometimes have to be trained to use automated watering devices and should be observed regularly until regular usage has been established to prevent dehydration. It is better to replace water bottles than to refill them, because of the potential for microbiologic cross contamination; if bottles are refilled, care should be taken to return each bottle to the cage from which it was removed. Automated watering distribution systems should be flushed or disinfected regularly. Animals housed in outdoor facilities may have access to water in addition to that provided in watering devices, such as that available in streams or in puddles after a heavy rainfall. Care should be taken to ensure that such accessory sources of water do not constitute a hazard, but their availability need not routinely be prevented. In cold weather, steps should be taken to prevent freezing of outdoor water sources.

Bedding and Nesting Materials Animal bedding and nesting materials are controllable environmental factors that can influence experimental data and improve animal well-being in most terrestrial species. Bedding is used to absorb moisture, minimize the growth of microorganisms, and dilute and limit animals’ contact with excreta, and specific bedding materials have been shown to reduce the accumulation of intracage ammonia ( Perkins and Lipman 1995 ; E. Smith et al. 2004 ). Various materials are used as both contact and noncontact bedding; the desirable characteristics and methods of evaluating bedding have been described ( Gibson et al. 1987 ; Jones 1977 ; Kraft 1980 ; Thigpen et al. 1989 ; Weichbrod et al. 1986 ). The veterinarian or facility manager, in consultation with investigators, should select the most appropriate bedding and nesting materials. A number of species, most notably rodents, exhibit a clear preference for specific materials ( Blom et al. 1996 ; Manser et al. 1997 , 1998 ; Ras et al. 2002 ), and mice provided with appropriate nesting material build better nests ( Hess et al. 2008 ). Bedding that enables burrowing is encouraged for some species, such as mice and hamsters.

No type of bedding is ideal for all species under all management and experimental conditions. For example, in nude or hairless mice that lack eyelashes, some forms of paper bedding with fines (i.e., very small particles found in certain types of bedding) can result in periorbital abscesses ( White et al. 2008 ), while cotton nestlets may lead to conjunctivitis ( Bazille et al. 2001 ). Bedding can also influence mucosal immunity ( Sanford et al. 2002 ) and endocytosis ( Buddaraju and Van Dyke 2003 ).

Softwood beddings have been used, but the use of untreated softwood shavings and chips is contraindicated for some protocols because they can affect metabolism ( Vesell 1967 ; Vesell et al. 1973 , 1976 ). Cedar shavings are not recommended because they emit aromatic hydrocarbons that induce hepatic microsomal enzymes and cytotoxicity ( Torronen et al. 1989 ; Weichbrod et al. 1986 , 1988 ) and have been reported to increase the incidence of cancer ( Jacobs and Dieter 1978 ; Vlahakis 1977 ). Prior treatment with high heat (kiln drying or autoclaving) may, depending on the material and the concentration of aromatic hydrocarbon constituents, reduce the concentration of volatile organic compounds, but the amounts remaining may be sufficient to affect specific protocols ( Cunliffe-Beamer et al. 1981 ; Nevalainen and Vartiainen 1996 ).

The purchase of bedding products should take into consideration vendors’ manufacturing, monitoring, and storage methods. Bedding may be contaminated with toxins and other substances, bacteria, fungi, and vermin. It should be transported and stored off the floor on pallets, racks, or carts in a fashion consistent with maintenance of quality and avoidance of contamination. Bags should be stored sufficiently away from walls to facilitate cleaning. During autoclaving, bedding can absorb moisture and as a result lose absorbency and support the growth of microorganisms. Therefore, appropriate drying times and storage conditions should be used or, alternatively, gamma-irradiated materials if sterile bedding is indicated.

Bedding should be used in amounts sufficient to keep animals dry between cage changes, and, in the case of small laboratory animals, it should be kept from coming into contact with sipper tubes as such contact could cause leakage of water into the cage.

Sanitation Sanitation —the maintenance of environmental conditions conducive to health and well-being—involves bedding change (as appropriate), cleaning, and disinfection. Cleaning removes excessive amounts of excrement, dirt, and debris, and disinfection reduces or eliminates unacceptable concentrations of microorganisms. The goal of any sanitation program is to maintain sufficiently clean and dry bedding, adequate air quality, and clean cage surfaces and accessories.

The frequency and intensity of cleaning and disinfection should depend on what is necessary to provide a healthy environment for an animal. Methods and frequencies of sanitation will vary with many factors, including the normal physiologic and behavioral characteristics of the animals; the type, physical characteristics, and size of the enclosure; the type, number, size, age, and reproductive status of the animals; the use and type of bedding materials; temperature and relative humidity; the nature of the materials that create the need for sanitation; and the rate of soiling of the surfaces of the enclosure. Some housing systems or experimental protocols may require specific husbandry techniques, such as aseptic handling or modification in the frequency of bedding change.

Agents designed to mask animal odors should not be used in animal housing facilities. They cannot substitute for good sanitation practices or for the provision of adequate ventilation, and they expose animals to volatile compounds that might alter basic physiologic and metabolic processes.

Bedding/Substrate Change Soiled bedding should be removed and replaced with fresh materials as often as necessary to keep the animals clean and dry and to keep pollutants, such as ammonia, at a concentration below levels irritating to mucous membranes. The frequency of bedding change depends on multiple factors, such as species, number, and size of the animals in the primary enclosure; type and size of the enclosure; macro- and microenvironmental temperature, relative humidity, and direct ventilation of the enclosure; urinary and fecal output and the appearance and wetness of bedding; and experimental conditions, such as those of surgery or debilitation, that might limit an animal’s movement or access to clean bedding. There is no absolute minimal frequency of bedding changes; the choice is a matter of professional judgment and consultation between the investigator and animal care personnel. It typically varies from daily to weekly. In some instances frequent bedding changes are contraindicated; examples include portions of the pre- or postpartum period, research objectives that will be affected, and species in which scent marking is critical and successful reproduction is pheromone dependent.

Cleaning and Disinfection of the Microenvironment The frequency of sanitation of cages, cage racks, and associated equipment (e.g., feeders and watering devices) is governed to some extent by the types of caging and husbandry practices used, including the use of regularly changed contact or noncontact bedding, regular flushing of suspended catch pans, and the use of wire-bottom or perforated-bottom cages. In general, enclosures and accessories, such as tops, should be sanitized at least once every 2 weeks. Solid-bottom caging, bottles, and sipper tubes usually require sanitation at least once a week. Some types of cages and housing systems may require less frequent cleaning or disinfection; such housing may include large cages with very low animal density and frequent bedding changes, cages containing animals in gnotobiotic conditions with frequent bedding changes, individually ventilated cages, and cages used for special situations. Other circumstances, such as filter-topped cages without forced-air ventilation, animals that urinate excessively (e.g., diabetic or renal patients), or densely populated enclosures, may require more frequent sanitation.

The increased use of individually ventilated cages (IVCs) for rodents has led to investigations of the maintenance of a suitable microenvironment with extended cage sanitation intervals and/or increased housing densities ( Carissimi et al. 2000 ; Reeb-Whitaker et al. 2001 ; Schondelmeyer et al. 2006 ). By design, ventilated caging systems provide direct continuous exchange of air, compared to static caging systems that depend on passive ventilation from the macroenvironment. As noted above, decreased sanitation frequency may be justified if the microenvironment in the cages, under the conditions of use (e.g., cage type and manufacturer, bedding, species, strain, age, sex, density, and experimental considerations), is not compromised ( Reeb et al. 1998 ). Verification of microenvironmental conditions may include measurement of pollutants such as ammonia and CO 2 , microbiologic load, observation of the animals’ behavior and appearance, and the condition of bedding and cage surfaces.

Primary enclosures can be disinfected with chemicals, hot water, or a combination of both. 2 Washing times and conditions and postwashing processing procedures (e.g., sterilization) should be sufficient to reduce levels or eliminate vegetative forms of opportunistic and pathogenic bacteria, adventitious viruses, and other organisms that are presumed to be controllable by the sanitation program. Disinfection from the use of hot water alone is the result of the combined effect of the temperature and the length of time that a given temperature (cumulative heat factor) is applied to the surface of the item. The same cumulative heat factor can be obtained by exposing organisms either to very high temperatures for short periods or to lower temperatures for longer periods ( Wardrip et al. 1994 , 2000 ). Effective disinfection can be achieved with wash and rinse water at 143–180°F or more. The traditional 82.2°C (180°F) temperature requirement for rinse water refers to the water in the tank or in the sprayer manifold. Detergents and chemical disinfectants enhance the effectiveness of hot water but should be thoroughly rinsed from surfaces before reuse of the equipment. Their use may be contraindicated for some aquatic species, as residue may be highly deleterious. Mechanical washers (e.g., cage and rack, tunnel, and bottle washers) are recommended for cleaning quantities of caging and movable equipment.

Sanitation of cages and equipment by hand with hot water and detergents or disinfectants can also be effective but requires considerable attention to detail. It is particularly important to ensure that surfaces are rinsed free of residual chemicals and that personnel have appropriate equipment to protect themselves from exposure to hot water or chemical agents used in the process.

Water bottles, sipper tubes, stoppers, feeders, and other small pieces of equipment should be washed with detergents and/or hot water and, where appropriate, chemical agents to destroy microorganisms. Cleaning with ultrasound may be a useful method for small pieces of equipment.

If automated watering systems are used, some mechanism to ensure that microorganisms and debris do not build up in the watering devices is recommended ( Meier et al. 2008 ); the mechanism can be periodic flushing with large volumes of water or appropriate chemical agents followed by a thorough rinsing. Constant recirculation loops that use properly maintained filters, ultraviolet lights, or other devices to disinfect recirculated water are also effective. Attention should be given to the routine sanitation of automatic water delivery valves (i.e., lixits) during primary enclosure cleaning.

Conventional methods of cleaning and disinfection are adequate for most animal care equipment. However, it may be necessary to also sterilize caging and associated equipment to ensure that pathogenic or opportunistic microorganisms are not introduced into specific-pathogen-free or immuno-compromised animals, or that experimental biologic hazards are destroyed before cleaning. Sterilizers should be regularly evaluated and monitored to ensure their safety and effectiveness.

For pens or runs, frequent flushing with water and periodic use of detergents or disinfectants are usually appropriate to maintain sufficiently clean surfaces. If animal waste is to be removed by flushing, this will need to be done at least once a day. During flushing, animals should be kept dry. The timing of pen or run cleaning should take into account the normal behavioral and physiologic processes of the animals; for example, the gastrocolic reflex in meal-fed animals results in defecation shortly after food consumption.

Cleaning and Disinfection of the Macroenvironment All components of the animal facility, including animal rooms and support spaces (e.g., storage areas, cage-washing facilities, corridors, and procedure rooms) should be regularly cleaned and disinfected as appropriate to the circumstances and at a frequency based on the use of the area and the nature of likely contamination. Vaporized hydrogen peroxide or chlorine dioxide are effective compounds for room decontamination, particularly following completion of studies with highly infectious agents ( Krause et al. 2001 ) or contamination with adventitious microbial agents.

Cleaning implements should be made of materials that resist corrosion and withstand regular sanitation. They should be assigned to specific areas and should not be transported between areas with different risks of contamination without prior disinfection. Worn items should be replaced regularly. The implements should be stored in a neat, organized fashion that facilitates drying and minimizes contamination or harborage of vermin.

Assessing the Effectiveness of Sanitation Monitoring of sanitation practices should fit the process and materials being cleaned and may include visual inspection and microbiologic and water temperature monitoring ( Compton et al. 2004a , b ; Ednie et al. 1998 ; Parker et al. 2003 ). The intensity of animal odors, particularly that of ammonia, should not be used as the sole means of assessing the effectiveness of the sanitation program. A decision to alter the frequency of cage bedding changes or cage washing should be based on such factors as ammonia concentration, bedding condition, appearance of the cage and animals, and the number and size of animals housed in the cage.

Mechanical washer function should be evaluated regularly and include examination of mechanical components such as spray arms and moving headers as well as spray nozzles to ensure that they are functioning appropriately. If sanitation is temperature dependent, the use of temperature-sensing devices (e.g., thermometers, probes, or temperature-sensitive indicator strips) is recommended to ensure that the equipment being sanitized is exposed to the desired conditions.

Whether the sanitation process is automated or manual, regular evaluation of sanitation effectiveness is recommended. This can be performed by evaluating processed materials by microbiologic culture or the use of organic material detection systems (e.g., adenosine triphosphate [ATP] bioluminescence) and/or by confirming the removal of artificial soil applied to equipment surfaces before washing.

Waste Disposal Conventional, biologic, and hazardous waste should be removed and disposed of regularly and safely ( Hill 1999 ). There are several options for effective waste disposal. Contracts with licensed commercial waste disposal firms usually provide some assurance of regulatory compliance and safety. On-site incineration should comply with all federal, state, and local regulations ( Nadelkov 1996 ).

Adequate numbers of properly labeled waste receptacles should be strategically placed throughout the facility. Waste containers should be leak-proof and equipped with tight-fitting lids. It is good practice to use disposable liners and to wash containers and implements regularly. There should be a dedicated waste storage area that can be kept free of insects and other vermin. If cold storage is used to hold material before disposal, a properly labeled, dedicated refrigerator, freezer, or cold room should be used that is readily sanitized.

Hazardous wastes must be rendered safe by sterilization, containment, or other appropriate means before their removal from the facility ( DHHS 2009 or most recent edition; NRC 1989 , 1995b ). Radioactive wastes should be kept in properly labeled containers and their disposal closely coordinated with radiation safety specialists in accord with federal and state regulations; the federal government and most states and municipalities have regulations controlling disposal of hazardous wastes. Compliance with regulations concerning hazardous-agent use (see Chapter 2 ) and disposal is an institutional responsibility.

Infectious animal carcasses can be incinerated on site or collected by a licensed contractor. Use of chemical digesters (alkaline hydrolysis treatment) may be considered in some situations ( Kaye et al. 1998 ; Murphy et al. 2009 ). Procedures for on-site packaging, labeling, transportation, and storage of these wastes should be integrated into occupational health and safety policies ( Richmond et al. 2003 ).

Hazardous wastes that are toxic, carcinogenic, flammable, corrosive, reactive, or otherwise unstable should be placed in properly labeled containers and disposed of as recommended by occupational health and safety specialists. In some circumstances, these wastes can be consolidated or blended. Sharps and glass should be disposed of in a manner that will prevent injury to waste handlers.

Pest Control Programs designed to prevent, control, or eliminate the presence of or infestation by pests are essential in an animal environment. A regularly scheduled and documented program of control and monitoring should be implemented. The ideal program prevents the entry of vermin and eliminates their harborage in the facility ( Anadon et al. 2009 ; Easterbrook et al. 2008 ). For animals in outdoor facilities, consideration should be given to eliminating or minimizing the potential risk associated with pests and predators.

Pesticides can induce toxic effects on research animals and interfere with experimental procedures ( Gunasekara et al. 2008 ). They should be used in animal areas only when necessary and investigators whose animals may be exposed to them should be consulted beforehand. Use of pesticides should be recorded and coordinated with the animal care management staff and be in compliance with federal, state, or local regulations. Whenever possible, nontoxic means of pest control, such as insect growth regulators ( Donahue et al. 1989 ; Garg and Donahue 1989 ; King and Bennett 1989 ; Verma 2002 ) and nontoxic substances (e.g., amorphous silica gel), should be used. If traps are used, methods should be humane; traps that catch pests alive require frequent observation and humane euthanasia after capture ( Mason and Littin 2003 ; Meerburg et al. 2008 ).

Emergency, Weekend, and Holiday Care Animals should be cared for by qualified personnel every day, including weekends and holidays, both to safeguard their well-being and to satisfy research requirements. Emergency veterinary care must be available after work hours, on weekends, and on holidays.

In the event of an emergency, institutional security personnel and fire or police officials should be able to reach people responsible for the animals. Notification can be enhanced by prominently posting emergency procedures, names, or telephone numbers in animal facilities or by placing them in the security department or telephone center. Emergency procedures for handling special facilities or operations should be prominently posted and personnel trained in emergency procedures for these areas. A disaster plan that takes into account both personnel and animals should be prepared as part of the overall safety plan for the animal facility. The colony manager or veterinarian responsible for the animals should be a member of the appropriate safety committee at the institution, an “official responder” in the institution, and a participant in the response to a disaster ( Vogelweid 1998 ).

Population Management

Identification Animal records are useful and variable, ranging from limited information on identification cards to detailed computerized records for individual animals ( Field et al. 2007 ). Means of animal identification include room, rack, pen, stall, and cage cards with written, bar-coded, or radio frequency identification (RFID) information. Identification cards should include the source of the animal, the strain or stock, names and contact information for the responsible investigator(s), pertinent dates (e.g., arrival date, birth date, etc.), and protocol number when applicable. Genotype information, when applicable, should also be included, and consistent, unambiguous abbreviations should be used when the full genotype nomenclature (see below) is too lengthy.

In addition, the animals may wear collars, bands, plates, or tabs or be marked by colored stains, ear notches/punches and tags, tattoos, subcutaneous transponders, and freeze brands. As a method of identification of small rodents, toe-clipping should be used only when no other individual identification method is feasible. It may be the preferred method for neonatal mice up to 7 days of age as it appears to have few adverse effects on behavior and well-being at this age ( Castelhano-Carlos et al. 2010 ; Schaefer et al. 2010 ), especially if toe clipping and genotyping can be combined. Under all circumstances aseptic practices should be followed. Use of anesthesia or analgesia should be commensurate with the age of the animals ( Hankenson et al. 2008 ).

Recordkeeping Records containing basic descriptive information are essential for management of colonies of large long-lived animals and should be maintained for each animal ( Dyke 1993 ; Field et al. 2007 ; NRC 1979a ). These records often include species, animal identifier, sire and/or dam identifier, sex, birth or acquisition date, source, exit date, and final disposition. Such animal records are essential for genetic management and historical assessments of colonies. Records of rearing and housing histories, mating histories, and behavioral profiles are useful for the management of many species, especially nonhuman primates ( NRC 1979a ). Relevant recorded information should be provided when animals are transferred between institutions.

Medical records for individual animals can also be valuable, especially for dogs, cats, nonhuman primates, and agricultural animals ( Suckow and Doerning 2007 ). They should include pertinent clinical and diagnostic information, date of inoculations, history of surgical procedures and postoperative care, information on experimental use, and necropsy findings where applicable.

Basic demographic information and clinical histories enhance the value of individual animals for both breeding and research and should be readily accessible to investigators, veterinary staff, and animal care staff.

Breeding, Genetics, and Nomenclature Genetic characteristics are important with regard to the selection and management of animals for use in breeding colonies and in biomedical research (see Appendix A ). Pedigree information allows appropriate selection of breeding pairs and of experimental animals that are unrelated or of known relatedness.

Outbred animals are widely used in biomedical research. Founding populations should be large enough to ensure the long-term genetic heterogeneity of breeding colonies. To facilitate direct comparison of research data derived from outbred animals, genetic management techniques should be used to maintain genetic variability and equalize founder representations ( Hartl 2000 ; Lacy 1989 ; Poiley 1960 ; Williams-Blangero 1991 ). Genetic variability can be monitored with computer simulations, biochemical markers, DNA markers and sequencing, immunologic markers, or quantitative genetic analyses of physiologic variables ( MacCluer et al. 1986 ; Williams-Blangero 1993 ).

Inbred strains of various species, especially rodents, have been developed to address specific research needs ( Festing 1979 ; Gill 1980 ). When inbred animals or their F1 progeny are used, it is important to periodically monitor genetic authenticity ( Festing 1982 ; Hedrich 1990 ); several methods of monitoring have been developed that use immunologic, biochemical, and molecular techniques ( Cramer 1983 ; Festing 2002 ; Groen 1977 ; Hoffman et al. 1980 ; Russell et al. 1993 ). Appropriate management systems ( Green 1981 ; Kempthorne 1957 ) should be designed to minimize genetic contamination resulting from mutation and mismating.

Genetically modified animals (GMAs) represent an increasingly large proportion of animals used in research and require special consideration in their population management. Integrated or altered genes can interact with species or strain-specific genes, other genetic manipulations, and environmental factors, in part as a function of site of integration, so each GMA line can be considered a unique resource. Care should be taken to preserve such resources through standard genetic management procedures, including maintenance of detailed pedigree records and genetic monitoring to verify the presence and zygosity of transgenes and other genetic modifications ( Conner 2005 ). Cryopreservation of fertilized embryos, ova, ovaries, or spermatozoa should also be considered as a safeguard against alterations in transgenes over time or accidental loss of GMA lines ( Conner 2002 ; Liu et al. 2009 ).

Generation of animals with multiple genetic alterations often involves crossing different GMA lines and can lead to the production of offspring with genotypes that are not of interest to the researcher (either as experimental or control animals) as well as unexpected phenotypes. Carefully designed breeding strategies and accurate genotype assessment can help to minimize the generation of animals with unwanted genotypes ( Linder 2003 ). Newly generated genotypes should be carefully monitored and new phenotypes that negatively affect well-being should be reported to the IACUC and managed in a manner to ensure the animals’ health and well-being.

Accurate recording, with standardized nomenclature when available, of both the strain and substrain or of the genetic background of animals used in a research project is important ( NRC 1979b ). Several publications provide rules developed by international committees for standardized nomenclature of outbred rodents and rabbits ( Festing et al. 1972 ), inbred rats, inbred mice, and transgenic animals ( FELASA 2007 ; Linder 2003 ). In addition, the International Committee on Standardized Genetic Nomenclature for Mice and the Rat Genome and Nomenclature Committee maintain online guidelines for these species ( MGI 2009 ).

• AQUATIC ANIMALS

The variety of needs for fish and aquatic or semiaquatic reptiles and amphibians is as diverse as the number of species considered. This section is intended to provide facility managers, veterinarians, and IACUCs with basic information related to the management of aquatic animal systems ( Alworth and Harvey 2007 ; Alworth and Vazquez 2009 ; Browne et al. 2007 ; Browne and Zippel 2007 ; Denardo 1995 ; DeTolla et al. 1995 ; Koerber and Kalishman 2009 ; Lawrence 2007 ; Matthews et al. 2002 ; Pough 2007 ). Specific recommendations are available in texts and journal reviews, and it will be necessary to review other literature and consult with experienced caregivers for further detail on caring for aquatic species (see Appendix A ).

Aquatic Environment

As with terrestrial systems, the microenvironment of an aquatic animal is the physical environment immediately surrounding it—the primary enclosure such as the tank, raceway, or pond. It contains all the resources with which the animals are in direct contact and also provides the limits of the animals’ immediate environment. The microenvironment is characterized by many factors, including water quality, illumination, noise, vibration, and temperature. The physical environment of the secondary enclosure, such as a room, constitutes the macroenvironment .

Water Quality

The composition of the water ( water quality ) is essential to aquatic animal well-being, although other factors that affect terrestrial microenvironments are also relevant. Water quality parameters and life support systems for aquatic animals will vary with the species, life stage, the total biomass supported, and the animals’ intended use ( Blaustein et al. 1999 ; Fisher 2000 ; Gresens 2004 ; Overstreet et al. 2000 ; Schultz and Dawson 2003 ). The success and adequacy of the system depend on its ability to match the laboratory habitat to the natural history of the species ( Godfrey and Sanders 2004 ; Green 2002 ; Lawrence 2007 ; Spence et al. 2008 ).

Characteristics of the water that may affect its appropriateness include temperature, pH, alkalinity, nitrogen waste products (ammonia, nitrite, and nitrate), phosphorus, chlorine/bromine, oxidation-reduction potential, conductivity/salinity, hardness (osmolality/dissolved minerals), dissolved oxygen, total gas pressure, ion and metal content, and the established microbial ecology of the tank. Water quality parameters can directly affect animal well-being; different classes, species, and ages in a species may have different water quality needs and sensitivities to changes in water quality parameters.

Routine measurement of various water characteristics (water quality testing) is essential for stable husbandry. Standards for acceptable water quality, appropriate parameters to test, and testing frequency should be identified at the institutional level and/or in individual animal use protocols depending on the size of the aquatic program. Staff managing aquatic systems need to be trained in biologically relevant aspects of water chemistry, how water quality parameters may affect animal health and well-being, how to monitor water quality results, and how water quality may affect life support system function (e.g., biologic filtration).

The specific parameters and frequency of testing vary widely (depending on the species, life stage, system, and other factors), from continuous monitoring to infrequent spot checks. Recently established systems and/or populations, or changes in husbandry procedures, may require more frequent assessment as the system ecology stabilizes; stable environments may require less frequent testing. Toxins from system components, particularly in newly constructed systems, may require special consideration such as leaching of chemicals from construction materials, concrete, joint compounds, and sealants ( DeTolla et al. 1995 ; Nickum et al. 2004 ). Chlorine and chloramines used to disinfect water for human consumption or to disinfect equipment are toxic to fish and amphibians and must be removed or neutralized before use in aquatic systems ( Tompkins and Tsai 1976 ; Wedemeyer 2000 ).

Life Support System

The phrase life support system refers to the physical structure used to contain the water and the animals as well as the ancillary equipment used to move and/or treat the water. Life support systems may be simple (e.g., a container to hold the animal and water) or extremely complex (e.g., a fully automated recirculating system). The type of life support system used depends on several factors including the natural habitat of the species, age/size of the species, number of animals maintained, availability and characteristics of the water required, and the type of research.

Life support systems typically fall into three general categories: recirculating systems where water (all or part) is moved around a system, flow-through systems where water is constantly replaced, or static systems where water is stationary and periodically replenished or replaced. The water may be fresh, brackish, or salt and is maintained at specific temperatures depending on the species’ needs.

The source of water for these systems typically falls into four general categories: treated wastewater (e.g., municipal tap water), surface water (e.g., rivers, lakes, or oceans), protected water (e.g., well or aquifer water), or artificial water (e.g., reverse osmosis or distilled water). Artificial saltwater may be created by adding appropriate salt to freshwater sources. Source water selection should be based on the provision of a consistent or constant supply, incoming biosecurity level requirements, water volumes needed, species selection, and research considerations.

Recirculating systems are common in indoor research settings where high-density housing systems are often needed. Most recirculating systems are designed to exchange a specific volume of water per unit time and periodically introduce fresh water into the system. These systems are the most mechanically advanced, containing biologic filters ( biofilters ) that promote conversion of ammonia to nitrite and nitrate via nitrifying bacteria, protein skimmers (foam fractionators) and particulate filters to remove undissolved and dissolved proteins and particulate matter, carbon filters to remove dissolved chemicals, and ultraviolet or ozone units to disinfect the water. The systems generally contain components to aerate and degas the water (to prevent gas oversaturation) and to heat or cool it, as well as automated dosing systems to maintain appropriate pH and conductivity. Not all elements are present in all systems and some components may accomplish multiple functions. Recirculating systems may be designed so that multiple individual tanks are supplied with treated water from a single source, as is the case with “rack” systems used for zebrafish ( Danio rerio ) and Xenopus laevis and X. tropicalis, as examples ( Fisher 2000 ; Koerber and Kalishman 2009 ; Schultz and Dawson 2003 ).

The development and maintenance of the biofilter is critical for limiting ammonia and nitrite accumulation in recirculating systems. The biofilter must be of sufficient size (i.e., contain a sufficient quantity of bacteria) to be capable of processing the bioload (level of nitrogenous waste) entering the system. The microorganisms supported by the biofilter require certain water quality parameters. Alterations in the aquatic environment (e.g., rapid changes in salinity, temperature, and pH) as well as the addition of chemicals or antimicrobials may significantly affect the microbial ecology of the system and therefore water quality and animal well-being. If damaged, biofilter recovery may take weeks ( Fisher 2000 ). Changes in water quality parameters (e.g., pH, ammonia, and nitrite) may negatively affect animal health and the efficiency of the biofilter, so species sensitive to change in water quality outside of a narrow range require more frequent monitoring.

Continuous or timed flow-through systems can be used where suitable water is available to support the species to be housed (e.g., in aquaculture facilities). These systems may use extremely large volumes of water as it is not reused. The water may be used “as is” or processed before use, for example by removing sediments, excessive dissolved gases, chlorine, or chloramines, and by disinfecting with UV or ozone ( Fisher 2000 ; Overstreet et al. 2000 ). Static systems vary in size from small tanks to large inground ponds, and may use mechanical devices to move and aerate water.

Temperature, Humidity, and Ventilation

The general concepts discussed in the Terrestrial Animals section also apply to the aquatic setting. Most aquatic or semiaquatic species (fish, amphibians, and reptiles) used in research are poikilotherms, which depend, for the most part, on the temperature of their environment to sustain physiologic processes, such as metabolism, reproduction, and feeding behavior ( Browne and Edwards 2003 ; Fraile et al. 1989 ; Maniero and Carey 1997 ; Pough 1991 ). Temperature requirements are based on the natural history of the species and can vary depending on life stage ( Green 2002 ; Pough 1991 ; Schultz and Dawson 2003 ). Water temperature may be controlled at its source, within the life support system, or by controlling the macroenvironment. Some semiopen systems (e.g., raceways by a river) depend on source water temperature and thus enclosure water temperature will vary with that of the source water.

The volume of water contained in a room can affect room temperature, temperature stability, and relative humidity. Likewise the thermal load produced by chiller/heater systems can affect the stability of the macroenvironmental temperature. Air handling systems need to be designed to compensate for these thermal and moisture loads. Macroenvironmental relative humidity levels are generally defined by safety issues and staff comfort, since room humidity is not critical for aquatic species; however, excessive moisture may result in condensation on walls, ceilings, and tank lids, which may support microbial growth and serve as a source of contamination or create a conducive environment for metal corrosion. In a dry environment (e.g., indoor heating during cold weather or outdoor housing in some climates/seasons), evaporation rates may be higher, potentially requiring the addition of large quantities of water to the system and monitoring for increases in salinity/conductivity, contaminants, or other water quality aberrations. Some amphibians and reptiles may need elevated microenvironmental humidity (in excess of 50–70% relative humidity), which may require maintaining elevated macroenvironmental humidity levels ( Pough 1991 ; St. Claire et al. 2005 ).

Room air exchange rates are typically governed by thermal and moisture loads. For fish and some aquatic amphibians, the microenvironmental air quality may affect water quality (i.e., gas exchange), but appropriate life support system design may reduce its importance. Airborne particulates and compounds (e.g., volatile organic compounds and ammonia) may dissolve in tank water and affect animal health ( Koerber and Kalishman 2009 ). As the aerosolization of water can lead to the spread of aquatic animal pathogens (e.g., protozoa, bacteria) within or throughout an aquatic animal facility, this process should be minimized as much as possible ( Roberts-Thomson et al. 2006 ; Wooster and Bowser 2007 ; Yanong 2003 ).

Aquatic and semiaquatic species are often sensitive to changes in photoperiod, light intensity, and wavelength ( Brenner and Brenner 1969 ). Lighting characteristics will vary by species, their natural history, and the research being conducted. Gradual changes in room light intensity are recommended, as rapid changes in light intensity can elicit a startle response in fish and may result in trauma. Some aquatic and semiaquatic species may need full-spectrum lighting and/or heat lamps to provide supplemental heating to facilitate adequate physiological function (e.g., aquatic turtles provided with a basking area; Pough 1991 ).

General concepts discussed in the Terrestrial Animals section apply to aquatic animals. These animals may be sensitive to noise and vibration, which are readily transmitted through water. Species vary in their response and many fish species acclimate to noise and vibration, although these may cause subclinical effects ( Smith et al. 2007 ). Vibration through floors can be reduced by using isolation pads under aquaria racks. Some facilities elect to place major components of the life support system (e.g., filters, pumps, and biofilters) outside the animal rooms to reduce vibration and noise.

Aquatic Housing

The primary enclosure (a tank, raceway, pond, or pen holding water and the animal) defines the limits of an animal’s immediate environment. In research settings, acceptable primary enclosures

• allow for the normal physiological and behavioral needs of the animals, including excretory function, control and maintenance of body temperature, normal movement and postural adjustments, and, where indicated, reproduction. In some poikilothermic reptiles and amphibians, microenvironmental temperature gradients may be needed for certain physiologic functions such as feeding and digestion.
• allow conspecific social interactions (e.g., schooling in fish species).
• provide a balanced, stable environment that supports the animal’s physiologic needs.
• provide the appropriate water quality and characteristics, and permit monitoring, filling, refilling, and changing of water.
• allow access to adequate food and removal of food waste.
• restrict escape or accidental entrapment of animals or their appendages.
• are free of sharp edges and/or projections that could cause injury.
• allow for observation of the animals with minimal disturbance.
• are constructed of nontoxic materials that do not leach toxicants or chemicals into the aquatic environment.
• do not present electrical hazards directly or indirectly.

Environmental Enrichment and Social Housing

Environmental enrichment strategies for many aquatic species are not well established. The implications of a barren versus an enriched environment on well-being, general research, growth, and development are unknown or poorly defined, as is true of individual versus group (social) housing for many species. When used, enrichment should elicit species-appropriate behaviors and be evaluated for safety and utility.

Generally, schooling fish species are housed with conspecifics, and many amphibians, especially anuran species, may be group housed. Aggression in aquatic animals does occur ( van de Nieuwegiessen et al. 2008 ; Speedie and Gerlai 2008 ) and, as for terrestrial animals, appropriate monitoring and intervention may be necessary ( Matthews et al. 2002 ; Torreilles and Green 2007 ). Some species need appropriate substrate (e.g., gravel) to reproduce or need substrate variety to express basic behaviors and maintain health ( Overstreet et al. 2000 ). Improved breeding success in enriched environments has been reported but further research in this area is needed ( Carfagnini et al. 2009 ). For many species (including, e.g., X. laevis ), visual barriers, hides, and shading are appropriate ( Alworth and Vasquez 2009 ; Torreilles and Green 2007 ). Most semiaquatic reptiles spend some time on land (basking, feeding, digesting, and ovipositing) and terrestrial areas should be provided as appropriate.

Sheltered, Outdoor, and Naturalistic Housing

Animals used in aquaculture are often housed in situations that mimic agricultural rearing and may be in outdoor and/or sheltered raceways, ponds, or pens with high population densities. In these settings, where natural predation and mortalities occur, it may be appropriate to measure animal “numbers” by using standard aquaculture techniques such as final production biomass ( Borski and Hodson 2003 ).

Space recommendations and housing density vary extensively with the species, age/size of the animals, life support system, and type of research ( Browne et al. 2003 ; Green 2009 ; Gresens 2004 ; Hilken et al. 1995 ; Matthews et al. 2002 ). In the United States, for example, adult zebrafish ( Danio rerio ) in typical biomedical research settings are generally housed 5 adult fish per liter of water ( Matthews et al. 2002 ), but this housing density varies when breeding and for housing younger animals ( Matthews et al. 2002 ). This guidance is not necessarily relevant for other species of fish, and may change as research advances ( Lawrence 2007 ). X. laevis adults may be housed at 2 liters of water per frog ( NRC 1974 ), but a wide variety of housing systems are currently used in research settings ( Green 2009 ). Institutions, investigators, and IACUC members should evaluate the appropriate needs of each species during program evaluations and facility inspections and continue to review ongoing research in these areas.

Aquatic Management

Behavior and social management.

Visual evaluations of aquatic and semiaquatic animals are typically used for monitoring. To avoid damage to the protective mucus layers of the skin and negative effects on immune function ( De Veer et al. 2007 ; Subramanian et al. 2007 ; Tsutsui et al. 2005 ), handling of these species should be kept to the minimum required ( Bly et al. 1997 ). Appropriate handling techniques vary widely depending on the species, age/size, holding system, and specific research need ( Fisher 2000 ; Matthews et al. 2002 ; Overstreet et al. 2000 ); they should be identified at the facility or individual protocol level.

Latex gloves have been associated with toxicity in some amphibians ( Gutleb et al. 2001 ). The use of appropriate nets by well-trained personnel can reduce skin damage and thus stress. Nets should be cleaned and disinfected appropriately when used in different systems and should be dedicated to animals of similar health status whenever possible.

Exercise and activity levels for aquatic species are minimally described but informed decisions may be extrapolated from studies of behavior of the same or similar species in the wild ( Spence et al. 2008 ). Some aquatic species do not rest and constantly swim; others may rest all or a significant portion of the day. Water flow rates and the provision of hides or terrestrial resting platforms (e.g., for some reptiles and amphibians) need to be appropriate for species and life stage.

Food The general principles relating to feeding of terrestrial animals are applicable to aquatic animals. Food should be stored in a type-appropriate manner to preserve nutritional content, minimize contamination, and prevent entry of pests. Food delivery methods should ensure that all animals are able to access food for a sufficient period of time while minimizing feeding aggression and nutrient loss. Feeding methods and frequency vary widely depending on the species, age/size of species, and type of life support system. Many aquatic or semiaquatic species are not provided with food ad libitum in the tank, and in some cases may not be fed daily.

Commercial diets (e.g., pellets, flakes) are available for certain species and storage time should be based on manufacturer recommendations or follow commonly accepted practices. In aquatic systems, particularly in fish rearing or when maintaining some amphibian and reptile species, the use of live foods (e.g., Artemia sp. larva, crickets, or mealworm beetle larvae) is common. Live food sources need to be maintained and managed to ensure a steady supply and the health and suitability of the organism as a food. Care should be taken to feed a complete diet to avoid nutritional deficiencies.

Water (see also section on Water Quality) Aquatic animals need access to appropriately conditioned water. Fully aquatic animals obtain water in their habitat or absorb it across their gills or skin. Some semiaquatic amphibians and reptiles may need “bowls” of water for soaking and drinking, and water quality should be appropriate (see Terrestrial Animals section). Chlorine or chloramines may be present in tap water at levels that could be toxic to some species.

Substrate Substrates can provide enrichment for aquatic animals by promoting species-appropriate behavior such as burrowing, foraging, or enhanced spawning ( Fisher 2000 ; Matthews et al. 2002 ; Overstreet et al. 2000 ). They may be an integral and essential component of the life support system by providing increased surface area for denitrifying bacteria (e.g., systems with undergravel filtration), and need routine siphoning (i.e., hydrocleaning) to remove organic debris. System design and species needs should be evaluated to determine the amount, type, and presentation of substrate.

Sanitation Sanitation of the aquatic environment in recirculating systems is provided through an appropriately designed and maintained life support system, regular removal of solid waste materials from the enclosure bottom, and periodic water changes. The basic concept of sanitation (i.e., to provide conditions conducive to animal health and welfare) is the same for terrestrial and aquatic systems. However, sanitation measures in aquatic systems differ from those for terrestrial systems because much of the nitrogenous waste (feces and urine) and respiratory output (carbon dioxide) is dissolved in the water.

A properly functioning life support system, designed to process the bioload, will maintain nitrogenous wastes within an acceptable range. Solids may be removed in a variety of ways, depending on the design of the system; generally they are removed by siphoning (hydrocleaning) and/or filtration. Depending on the type, filters need routine cleaning or replacement or, if self-cleaning, proper maintenance; in saltwater systems dissolved proteins may be removed by protein skimmers. Reducing organic solids limits the quantities of nitrogen and phosphorus that need to be removed from the system, both of which can accumulate to levels that are toxic to fish and amphibians. The biologic filter (denitrifying bacteria) typically removes ammonia and nitrite, potential toxins, from aquatic systems. Nitrate, the end product of this process, is less toxic to aquatic animals but at high levels can be problematic; it is generally removed through water changes, although large systems may have a specialized denitrification unit to reduce levels.

Disinfection is usually accomplished through water treatment (e.g., filtration and application of UV light or ozone) and/or water changes. Chlorine and most chemical disinfectants are inappropriate for aquatic systems containing animals as they are toxic at low concentrations; when used to disinfect an entire system or system components, extreme care must be taken to ensure that residual chlorine, chemical, and reactive byproducts are neutralized or removed. The type of monitoring and frequency varies depending on the disinfection method, the system, and the animals.

Algal growth is common in aquatic systems and increases with the presence of nitrogen and phosphorus, particularly in the presence of light. Excessive growth may be an indication of elevated nitrogen or phosphorus levels. Algal species seen with recirculating systems are generally nontoxic, although species capable of producing toxins exist. Algae are typically removed using mechanical methods (i.e., scrubbing or scraping). Limiting algal growth is important to allow viewing of the animals in the enclosure. Cyanobacteria (commonly called blue-green algae) growth is also possible and may be common in freshwater aquaculture. The same factors that promote algae growth also promote cyanobacteria growth. As with algae, while most species are harmless, some species can produce clinically relevant toxic compounds ( Smith et al. 2008 ).

Tank (cage) changing and disinfection are conducted at frequencies using methods that often differ from terrestrial systems. Because waste is dissolved in the water and/or removed as solids by siphoning or filtration, regular changing of tanks is not integral to maintaining adequate hygiene in typical aquatic systems. The frequency of cleaning and disinfection should be determined by water quality, which should permit adequate viewing of the animals, and animal health monitoring. System components such as lids on fish tanks, which may accumulate feed, may require sanitation as often as weekly depending on the frequency and type of feed and the system’s design.

Cleaning and Disinfection of the Macroenvironment As with terrestrial systems, all components of the animal facility, including animal rooms and support spaces (e.g., storage areas, cage-washing facilities, corridors, and procedure rooms), should be regularly cleaned and disinfected as appropriate to the circumstances and at a frequency determined by the use of the area and the nature of likely contamination. Cleaning agents should be chosen and used with care to ensure there is no secondary contamination of the aquatic systems.

Waste Disposal Wastewater treatment and disposal may be necessary in some facilities depending on water volume, quality, and chemical constituents. Local regulations may limit or control the release of wastewater.

Pest Control Terrestrial animal pest control principles apply to aquatic systems but, due to transcutaneous absorption, aquatic and semiaquatic species may be more sensitive to commonly used pest control agents than terrestrial animals. Before use, an appropriate review of chemicals and methods of application is necessary.

Emergency, Weekend, and Holiday Care As with terrestrial species, aquatic animals should receive daily care from qualified personnel who have a sufficient understanding of the housing system to identify malfunctions and, if they are unable to address a system failure of such magnitude that it requires resolution before the next workday, access to staff who can respond to the problem. Automated monitoring systems are available and may be appropriate depending on system size and complexity. Appropriate emergency response plans should be developed to address major system failures.

Identification Identification principles are similar to those for terrestrial animals. Identification criteria are based on the species and housing system. Identification methods available for use in aquatic species include fin clipping, genetic testing ( Matthews et al. 2002 ; Nickum et al. 2004 ), identification tags, subcutaneous injections of elastomeric or other materials ( Nickum et al. 2004 ), individual transponder tags (in animals of sufficient size), and, as applicable, external features such as individual color patterns. Because it can be difficult to individually identify some small aquatic animals throughout their life, group identification may be more appropriate in some situations ( Koerber and Kalishman 2009 ; Matthews et al. 2002 ).

Aquatic Animal Recordkeeping Adequate recordkeeping is necessary in aquatic system management. In general, the same standards used for terrestrial animals apply to aquatic and semiaquatic species, although modifications may be necessary to account for species or system variations ( Koerber and Kalishman 2009 ).

Although many aquatic animals are maintained using group (vs. individual) identification, detailed animal records are still necessary. Animal information that may routinely be captured, particularly in biomedical research with fish, includes species; genetic information (parental stock identification, genetic composition); stock source; stock numbers in system; tank identification; system life support information; breeding; deaths; illnesses; animal transfers within and out of the facility; and fertilization/hatching information ( Koerber and Kalishman 2009 ; Matthews et al. 2002 ). Records should be kept concerning feeding information (e.g., food offered, acceptance), nonexpired food supplies to ensure sustenance of nutritional profile, and any live cultures (e.g., hatch rates and information to ensure suppliers’ recommendations are being met; Matthews et al. 2002 ).

Records of water quality testing for system and source water and maintenance activities of the life support system components are important for tracking and ensuring water quality. The exact water quality parameters tested and testing frequency should be clearly established and will vary with such factors as the type of life support system, animals, and research, as discussed under Water Quality. Detailed tracking of animal numbers in aquatic systems is often possible with accurate records of transfers, breeding, and mortalities ( Matthews et al. 2002 ). In some cases where animals are housed in large groups (e.g., some Xenopus colonies) periodic censuses may be undertaken to obtain an exact count. In large-scale aquaculture research it may be more appropriate to measure biomass of the system versus actual numbers of animals ( Borski and Hodson 2003 ).

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Gnotobiotic: germ-free animals or formerly germ-free animals in which the composition of any associated microbial flora, if present, is fully defined (Stedman’s Electronic Medical Dictionary 2006. Lippincott Williams & Wilkins).

Rabbits and some rodents, such as guinea pigs and hamsters, produce urine with high concentrations of proteins and minerals. These compounds often adhere to cage surfaces and necessitate treatment with acid solutions before and/or during washing.

• Cite this Page National Research Council (US) Committee for the Update of the Guide for the Care and Use of Laboratory Animals. Guide for the Care and Use of Laboratory Animals. 8th edition. Washington (DC): National Academies Press (US); 2011. 3, Environment, Housing, and Management.
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Essays articulate a specific perspective on a topic of broad interest to scientists.

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Leveraging social media and other online data to study animal behavior

Roles Conceptualization, Data curation, Visualization, Writing – original draft, Writing – review & editing

* E-mail: [email protected]

Affiliations School of Geography and the Environment, University of Oxford, Oxford, United Kingdom, WildCRU, Recanati-Kaplan Centre, Department of Zoology, Oxford University, Oxford, United Kingdom, School of Zoology, Tel Aviv University, Tel Aviv, Israel

Roles Conceptualization, Data curation, Writing – review & editing

Affiliations CEABN, Centro de Ecologia Aplicada Prof. Baeta Neves, InBIO Laboratório Associado, Instituto Superior de Agronomia, Universidade de Lisboa, Lisboa, Portugal, Helsinki Lab of Interdisciplinary Conservation Science (HELICS), Department of Geosciences and Geography, University of Helsinki, Helsinki, Finland

Affiliations Department of Anatomy, Cell Biology and Zoology, Faculty of Sciences, University of Extremadura, Badajoz, Spain, Ecology in the Anthropocene, Associated Unit CSIC-UEX, Faculty of Sciences, University of Extremadura, Badajoz, Spain

Roles Data curation, Writing – review & editing

Affiliation Poznań University of Life Sciences, Department of Zoology, Poznań, Poland

Affiliation Institute of Evolutionary Biology, Faculty of Biology, Biological and Chemical Research Centre, University of Warsaw, Warsaw, Poland

Affiliations Faculty of Environmental Sciences, Czech University of Life Sciences Prague, Prague, Czech Republic, TUM School of Life Sciences, Ecoclimatology, Technical University of Munich, Freising, Germany, Institute for Advanced Study, Technical University of Munich, Garching, Germany

Affiliation Mitrani Department of Desert Ecology, Jacob Blaustein Institutes of Desert Research, Ben-Gurion University of the Negev, Ben-Gurion, Israel

Affiliation Department of Ecology and Evolutionary Biology, University of California, Los Angeles, California, United States of America

Roles Data curation, Visualization, Writing – review & editing

Affiliations Université Paris-Saclay, CNRS, AgroParisTech, Ecologie Systématique Evolution, Gif sur Yvette, France, Biology Centre of the Czech Academy of Sciences, Institute of Hydrobiology, České Budějovice, Czech Republic

Roles Conceptualization, Data curation, Visualization, Writing – review & editing

Affiliation Department of Marine Renewable Resources, Institute of Marine Science (ICM-CSIC), Barcelona, Spain

• Reut Vardi, 
• Andrea Soriano-Redondo, 
• Jorge S. Gutiérrez, 
• Łukasz Dylewski, 
• Zuzanna Jagiello, 
• Peter Mikula, 
• Oded Berger-Tal, 
• Daniel T. Blumstein, 
• Ivan Jarić, 
• Valerio Sbragaglia

Published: August 29, 2024

• https://doi.org/10.1371/journal.pbio.3002793
• Reader Comments

This is an uncorrected proof.

The widespread sharing of information on the Internet has given rise to ecological studies that use data from digital sources including digitized museum records and social media posts. Most of these studies have focused on understanding species occurrences and distributions. In this essay, we argue that data from digital sources also offer many opportunities to study animal behavior including long-term and large-scale comparisons within and between species. Following Nikko Tinbergen’s classical roadmap for behavioral investigation, we show how using videos, photos, text, and audio posted on social media and other digital platforms can shed new light on known behaviors, particularly in a changing world, and lead to the discovery of new ones.

Citation: Vardi R, Soriano-Redondo A, Gutiérrez JS, Dylewski Ł, Jagiello Z, Mikula P, et al. (2024) Leveraging social media and other online data to study animal behavior. PLoS Biol 22(8): e3002793. https://doi.org/10.1371/journal.pbio.3002793

Copyright: © 2024 Vardi et al. This is an open access article distributed under the terms of the Creative Commons Attribution License , which permits unrestricted use, distribution, and reproduction in any medium, provided the original author and source are credited.

Funding: R.V. was partly funded by the Alexander and Eva Lester post-doctoral fellowship. A.S-R. was supported by grant 2022.01951.CEECIND from the Portuguese Foundation for Science and Technology. P.M. was supported by the Faculty of Environmental Sciences CZU Prague within the framework of the Research Excellence in Environmental Sciences (REES 003) and by IAS TUM – Hans Fisher Senior Fellowship. I.J. was supported by grant no. 23-07278S from the Czech Science Foundation. V.S. is supported by a Ramón y Cajal research fellowship (RYC2021-033065-I) granted by the Spanish Ministry of Science and Innovation and he also acknowledges the Spanish government through the ‘Severo Ochoa Centre of Excellence’ accreditation (CEX2019-000928-S). Funders played no rule in the study design, data collection and analysis, decision to publish, or preparation of the manuscript.

Competing interests: The authors have declared that no competing interests exist.

Introduction

Rapidly accumulating digital data offer numerous opportunities for science. With more than half of the world’s population online ( https://www.itu.int/en/ITU-D/Statistics/Pages/stat/default.aspx ), billions of people are generating online digital data in the form of text, images, videos, and audio uploaded to social media platforms and other websites ( Box 1 ). Furthermore, field notes, printed books, and old news media are being increasingly digitized and made available online [ 1 ]. These vast digital knowledge repositories can provide meaningful insights into the natural world. Indeed, several emerging fields have been developed for that purpose; conservation culturomics uses digital data to inform conservation science and human–nature interactions [ 2 ], while iEcology (or passive crowdsourcing [ 3 ]) uses such data to study ecological patterns [ 4 ]. Indeed, geotagged data from multiple digital sources can complement other data to monitor distributions and occurrences of species, particularly of charismatic ones, or in and around human-dominated landscapes such as urban habitats or areas subjected to high human visitation [ 5 , 6 ].

Box 1. Categories of digital data

While using the term digital data, we distinguish between 3 major categories:

• Digitized scientific databases, such as digitized museum records, and audio or video online libraries, that have usually been collected by researchers.
• Citizen/community science data sets where members of the public record their nature sightings for scientific use, either for general data repositories or for specific research projects (e.g., iNaturalist and eBird).
• Social media platforms—such as X (formerly known as Twitter), Instagram, or Google Images—where individuals upload content generated for various purposes typically not with the intention to address scientific questions yet may, nevertheless, be relevant to research.

Data from the 3 categories can differ in their collection protocols, reliability, accuracy, accompanied metadata, and data-sharing rights. While we consider the importance of data use from all 3 categories, given the novelty, extent, and challenges associated with using data from social media platforms, we focus primarily on the potential and limitations of such digital data sources.

Digital data can also be used to characterize animal behavior [ 7 ]. For example, Jagiello and colleagues [ 8 ] used YouTube videos to compare the occurrence of various behaviors of Eurasian red squirrels and invasive gray squirrels ( Sciurus vulgaris and S . carolinensis ) between 2 habitats. They found that calling and aggressive behaviors were more frequent in forests than in urban habitats ( Fig 1 ). Similarly, Boydston and colleagues [ 9 ] analyzed YouTube videos to understand the structure and putative function of coyote–dog ( Canis latrans – C . familiaris ) interactions. They found evidence of intricate social behavior between the 2 species. However, YouTube is not the only platform that offers data that, while collected for other purposes, can be meaningful for behavioral ecology. Other sources may include various social media platforms (X (formerly Twitter), Facebook, Instagram, etc.), digitized scientific records, and citizen science databases (see Box 1 ). Such alternative sources of information may help fill important gaps in our understanding of animal behavior and shed light on how animal behavior may be influenced by humans’ actions.

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(A) Digital data (inner circle; photos, videos, and audio) can complement experimental and observational approaches aiming to characterize several aspects of animal behavior, such as social interactions and biological rhythms (middle circle). Applications of digital data are particularly interesting for characterizing behavioral and ecological patterns addressing several research fields (e.g., urban ecology and biological invasions) as well as tackling conservation issues (outer circle). ( B–D) Representative examples of studies that used digital data to characterize animal behavior. ( B ) Percentage of recorded behavior in forest and urban ecosystems for the European red squirrel ( Sciurus vulgaris ) based on YouTube videos (right; adapted from [ 8 ]); photo of a red squirrel (photo credit: Peter Mikula); ( C ) Density maps showing the distribution of bat predation records by diurnal birds based on published literature (left map) and online records such as Google images, Flickr, and YouTube (right map; adapted from [ 10 ], countries borders map taken from https://public.opendatasoft.com/explore/dataset/ne_10m_admin_0_countries/map/ ). Example photo of a European bee-eater ( Merops apiaster ) trying to swallow a Kuhl’s pipistrelle bat ( Pipistrellus kuhlii ; photo credit: Shuki Cheled). ( D ) Wilson’s phalarope ( Phalaropus tricolor ) spinning (counterclockwise) in tight circles to upwell small prey and feed upon them as revealed by freely available videos on YouTube, Vimeo, and Flickr (photo credit: Miroslav Šálek). Nearest neighbors are more likely to spin in the same direction, thus reducing interference with each other (adapted from [ 11 ]).

https://doi.org/10.1371/journal.pbio.3002793.g001

In the mid-20th century, Nikko Tinbergen created a foundational framework for the integrative study of animal behavior [ 12 , 13 ] by posing 4 interlinked questions regarding the 4 main axes of behavior: causation , the mechanistic basis of behavior; ontogeny , its development throughout an individual’s lifetime; evolution , its changes over an evolutionary time scale; and function , its adaptive value and current utility. Answering Tinbergen’s questions can be hindered by many research challenges including, but not restricted to, limited funds, time, accessibility, and sample sizes. In such cases, readily available data from various online platforms such as citizen science databases or social media platforms (for example, YouTube, Facebook, or Flickr) can prove to be a powerful and complementary tool to traditional methods involving observations and experiments ( Fig 2 ) [ 4 , 7 ]. Furthermore, social media platforms, similar to citizen science platforms, can also provide bridges between scientists and nature enthusiasts (as well as the general public) that can be harnessed to help create and review large data sets. This, in turn, can also encourage people to reconnect with nature and promote biodiversity conservation [ 14 ].

Traditionally, animal behavior has been studied mostly with empirical approaches and literature surveys. The addition of digital data enables us to explore ecological patterns (iEcology) and human–nature interactions (conservation culturomics). All of these approaches can help address Tinbergen’s questions of behavior. In return, Tinbergen’s questions help direct and shape research questions, experimental setups, and data collection. Conservation culturomics infers human behavior related to nature and is thus represented with a dashed arrow. Icons taken from https://openclipart.org/ .

https://doi.org/10.1371/journal.pbio.3002793.g002

Here, we propose that digital data, especially from social media platforms, can be used to answer questions beyond species distribution and occurrence to advance the field of animal behavior ( Fig 2 ). While keeping in mind that Tinbergen’s questions are interlinked and complementary to each other, we explore each question separately, highlighting both opportunities and challenges in using digital data to answer them. We further highlight the increased relevance of Tinbergen’s questions to biodiversity conservation. We showcase instances where digital data has already been used to study animal behavior ( Fig 1 and S1 Table ) and suggest possible avenues for further research incorporating digital data to address fundamental and applied behavioral issues.

Studies dealing with causation try to understand what causes a behavior to be performed. When combined with remotely sensed, freely available data, digital data sources can be used to explore the external mechanisms underlying a behavioral trait. For example, Cabello-Vergel and colleagues [ 15 ] combined data on the thermoregulatory behavior of individual storks (Ciconiidae) from georeferenced images and videos found at the Macaulay Library repository ( https://www.macaulaylibrary.org ) with remotely sensed microclimate data. They investigated the determinants of “urohidrosis” (excreting onto the legs as a form of evaporative cooling) in 19 stork species. They found that high heat loads (high temperature, humidity, and solar radiation, and low wind speed) promoted the use of urohidrosis and thus evaporative heat loss. In the face of global climate change, exploring shifts in mechanisms of control with microclimate data can inform us about mechanisms of adaptation to changing environments and provide profound insights facilitating future conservation efforts.

The study of social learning and the emergence of novel and innovative behaviors in relation to environmental conditions could particularly benefit from digital data sources because people often record surprising or unexpected animal behaviors [ 7 ]. For example, data from multiple digital data sources revealed that 10 out of the 16 world’s terrestrial hermit crab species ( Coenobitidae ) widely use artificial shells, predominantly plastic caps, but also pieces of glass or metal [ 16 ]. This novel behavior may be driven by decreased availability of gastropod shells, sexual signaling, lightness of artificial shells, odor cues, and/or camouflage in a polluted environment. Together with controlled preferences experiments and/or records of pollution levels and other environmental conditions, we can address the underlying mechanisms of this behavior, which may ultimately influence the evolutionary trajectory of the species. Other examples include YouTube videos that have been used to describe horses opening doors and gate mechanisms [ 17 ] or investigate death-related behavioral responses in Asian elephants ( Elephas maximus ) such as carrying dead calves [ 18 ]. Understanding why and when these rare behaviors occur may not be possible without such online records.

In 2022, Møller and Xia [ 19 ] showed that bird species recorded on YouTube videos feeding directly from people’s hands also presented more innovative behaviors, had a higher rate of introduction success, and greater urban tolerance than species not recorded displaying such behavior. This demonstrates the connections between Tinbergen’s questions and highlights that an individual’s (or species) ability to respond behaviorally to external conditions may also rely on its evolutionary history and affects its chances of survival. It further shows that the fields of urban ecology and invasion biology can greatly benefit from integrating these novel digital data sources. For example, with most of the global human population living in cities and the omnipresence of online social platforms, digital data can make global multi-city comparisons of urbanization effects on species behavior feasible. Moreover, human activity can be easily tracked using mobility reports provided by Google ( https://www.google.com/covid19/mobility/ ) and Apple ( https://covid19.apple.com/mobility ). These can provide a high-resolution understanding of where and when humans are active and how they can play an important role in shaping animal behavior. Such knowledge can help enhance studies of antipredator behavior and wildlife tolerance, as it was used to study the consequences of the COVID-19 pandemic lockdowns [ 20 , 21 ]. Likewise, documenting first arrivals and monitoring the spread of invasive species, their behavior, and interactions with native species can become more efficient by incorporating digital data from online repositories [ 22 ].

We acknowledge that digital sources alone cannot offer many insights into internal mechanisms of behavior, such as hunger state or past experience (exceptions may include behaviors that are influenced by temperature, which may be inferred if the data are georeferenced and time stamped). Studying proximate physiological mechanisms often requires extensive field and laboratory experiments. However, addressing what mechanisms drive behavior in terms of changes in the external stimulus (social and physical environment) could greatly benefit from the copious number of available images and videos online. This is particularly true considering current and future global environmental challenges.

Digital data in the forms of images, audio, videos, and live-streaming videos can also be used to study and quantify different behavioral shifts in individuals over their lifetimes. For example, using online-sourced photographs, Naude and colleagues [ 23 ] showed that adult martial eagles ( Polemaetus bellicosus ) preyed more on birds than juveniles and subadults, which preferred less agile reptiles and mammals. They attributed this pattern to an improvement in hunting skills with age. Another study found evidence for “ontogenetic deepening”—the phenomenon that older and larger fish are found in deeper water, whereas younger and smaller fish stay in shallower water—in dusky groupers ( Epinephelus marginatus ) using YouTube videos of recreational fishers [ 24 ]. Exploring videos over several years, they further showed that fishing depth did not change over time and thus suggested that this ontogenetic deepening may not be solely driven by changes in harvesting pressure. Combining acoustic recordings from various sources (field recordings, a museum sound library, and citizen science records), Riós-Chelén and colleagues [ 25 ] found that birds can adapt their songs to environmental acoustic conditions. The fact that songbirds (known as oscines), who learn their songs, showed stronger associations between environmental noise and song modifications than other closely related bird species with innate songs (suboscines) indicates the involvement of ontogenetic processes in this adjustment.

Other studies can use similar approaches to further explore ontogenetic changes in different species’ hunting skills, aggressiveness, mating rituals, and parental care, with or without complementing intensive fieldwork (see S1 Table ). Exploring such changes in behavior in response to anthropogenic environmental changes worldwide can be of great importance for conservation science, urban ecology, and agroecology. For example, live-streaming videos of bird nests—which have become very common for many species and sites (e.g., https://camstreamer.com/blog/streaming-birds-with-an-eagle-eye and https://www.viewbirds.com/ )—can provide rich information to study the development of nestling vocal signals, the learning of songs, or the establishment of siblings relationships, as well as differences in such behaviors as a function of the distance to urban areas, human disturbance level, or levels of noise or light pollution [ 26 ]. Nonetheless, similar to exploring causation mechanisms, answering questions related to ontogeny cannot solely rely on digital data sources since ontogenetic processes often involve studying individuals over time. Furthermore, developing a deep understanding of external factors affecting the development of behavior may also require well-designed controlled experiments, which can be more challenging to accomplish with the available digital databases.

With images and videos from around the world spanning several decades available online, it is now possible to use digital data to explore intra- and interspecific traits and behaviors, as well as study their evolution in the light of anthropogenic environmental changes. For example, using crowd-sourced images and videos, Mikula and colleagues [ 10 ] showed that predator–prey interactions between diurnal birds and bats, which were previously thought to be rare, have been commonly reported around the world ( Fig 1 ). This indicates that diurnal bird predation might act as one of the drivers of the evolution of bat nocturnality. Similarly, using social media videos and phylogenetic modeling, Bastos and colleagues [ 27 ] showed that tool-using behavior in parrots is far more common than previously thought and that these new sources of data can be used to better understand the origin, evolution, and drivers of rare behaviors. In another example, Pearse and colleagues [ 28 ] were able to explore evolutionary patterns in bird song at a broad scale (in terms of pitch and complexity) using a large citizen science digital repository, combined with scientific data on bird biology, life history, and geographical distribution, and advanced machine learning techniques. Surprisingly, they showed that suboscine and oscine birds have similar song complexity. They further noted that using Artificial intelligence (AI) tools to help analyze citizen science data can further facilitate research on bird song evolution. However, such tools may also have limitations and need to be routinely validated and assessed.

The fact that digital repositories can potentially hold decades-old data allows retrospective explorations of data collected long before the research has commenced. For example, the COVID-19 pandemic highlighted the importance and usefulness of citizen science data sets, as past records could be compared with records under the novel environmental settings created by the pandemic [ 21 ]. Similar data sets may be obtained from various social media platforms that are far more popular than citizen science platforms, both in volume and in geographic coverage. For example, there are 3 million iNaturalist users ( https://www.inaturalist.org/stats ) compared with 300 million X (formerly Twitter) users ( https://www.statista.com/statistics/303681/twitter-users-worldwide/ ). While most of the content on X would probably be irrelevant for ecology and conservation, the potential to reach and engage new audiences, and access diverse data could be valuable. Using these novel data sources can further facilitate large spatial scale explorations of evolutionary changes in animal behavior. It may also help researchers to better plan and choose field sites before embarking on intensive fieldwork.

Many aspects of the evolution of animal behavior are challenging to document directly because numerous phenotypic traits co-evolve over large spatial and phylogenetic scales, making comparative studies useful. For example, body coloration may be an important factor in answering fundamental questions in behavioral ecology that provides insights into local behavioral adaptations [ 29 , 30 ]. Online image repositories have already been used to document geographical and phylogenetic variation in color patterns in birds and mammals, including color polymorphism [ 31 ], mutations [ 32 ], and variation in the morphology of color strips and patches [ 33 ]. In addition to readily available data, people can be encouraged to upload their images, videos, and sound recordings for specific studies through citizen science platforms [ 34 ] or social media platforms [ 35 ]. Spatial data on the phenotypic distributions are often collected via field observations and inspection of voucher specimens.

We envision that online images, videos, and acoustic recordings may provide a rich resource of information on large-scale variation in many phenotypic traits closely linked to animal behavior, such as nest morphology in fish and birds, or the size and shape of ornaments and armaments (e.g., antlers in deer or bony spurs in birds). Yet, we must acknowledge the limitations of using digital data to answer questions of an evolutionary nature that require some genomic knowledge. Still, the sheer volume of digital data and the ability to compare data of many species and populations inhabiting different areas and environments can provide valuable information for the processes and mechanisms involved in evolutionary adaptation and speciation.

Answering function-related questions—how a behavior increases one’s fitness through survival and reproduction—can also gain much from using digital data. With the ubiquity of the Internet, we can explore external drivers of current utility and sexual selection regarding behavioral contributions to overall fitness. These may include intra- and interspecific interactions, migratory patterns, predation risk, and mating rituals. For example, using live-streaming underwater cameras, Coleman and Burge [ 36 ] showed a higher association between sand tiger sharks ( Carcharias taurus ) and round scads ( Decapterus punctatus ) in the presence of scad mesopredators, which enhances foraging opportunities for sand tiger sharks and reduces predation risk for the scads. Such behaviorally mediated indirect interactions may have far-reaching implications for trophic interactions, including predator and prey strategies. Studies like this highlight the potential of these novel data and technologies in ecological research.

Digital data can be further used to study the timing of biological processes (i.e., phenology) in animals and how these are being affected by external cues such as climate change, land use changes, or human disturbance. For example, using Wikipedia page views, Mittermeier and colleagues [ 37 ] tracked seasonal migration patterns in sockeye salmon ( Oncorhynchus nerka ) and Atlantic salmon ( Salmo salar ). Atsumi and Koizumi [ 38 ] used X (formerly Twitter) and Google Images to explore spatial variations in breeding timing in Japanese dace fish ( Tribolodon hakonensis ) and how they may have been affected by climate change. Combined with data on breeding success or the costs of not adjusting breeding timing, these studies could greatly advance function-related research. Given the ongoing global environmental change, such explorations can be invaluable to understanding how these changes impact various species in terms of range shifts and/or expansions. Again, digital data has limits, and complementing it with traditional methods may be required to accurately assess the fitness value of a behavior.

The challenges and limitations of using digital data to study animal behavior

Addressing questions related to any of Tinbergen’s 4 levels of analysis is challenging. While digital data and approaches can greatly advance the fields of behavioral ecology and conservation behavior, these data sources and tools currently cannot replace empirical work and field studies. We acknowledge the limitations of digital data, particularly in answering questions related to internal mechanisms such as endocrine or neural control of behavior. Available digital data may not provide reliable information on an individual’s physiological state, its developmental history, or its reproductive state. Nonetheless, digital data sources can provide new opportunities to explore many aspects of Tinbergen’s 4 questions in a noninvasive and without manipulation of free-living animals, thus solving underlying ethical and welfare issues associated with the use of animals in research [ 39 ]. It is important to note, however, that digital data research also raises ethical questions and should follow rules to avoid disruption to the focal animal(s), the animals’ population, or the wider ecosystem. Viewing digital data as complementary to more traditional sources of data may be very useful. Moreover, in some areas traditional data sources are lacking, and so adequately reliable digital data may be the best source of behavioral data available. Nevertheless, we must consider the biases, technical challenges, and ethical concerns associated with digital data.

First, data sets obtained from online platforms—particularly ones provided by the general public—have an inherited bias linked to Internet coverage and use such that different regions of the world are not equally represented in digital records. Similarly, different sectors of society based on, for example, ethnicity, language, socioeconomic status, and education level, are currently not equally represented in the digital realm, complicating research on human–nature interactions using digital data.

Second, only a fraction of the global biodiversity is digitally recorded and has an online presence [ 1 , 40 ]. This limits the number of species that can be explored using digital data sets and leads to an uneven sampling effort across different taxa and clades. Such biases, for example, towards charismatic or larger-bodied species, are widespread and well known from more traditional approaches of scientific research [ 41 ], but may be exacerbated using data from social media. Furthermore, this limitation of unequal human interest goes beyond which species are predominantly documented, but also to which behaviors are recorded. Such human preferences and biases, and how they may differ across cultures, may compromise analyses and conclusions if not properly accounted for [ 42 ]. Furthermore, search algorithms of search engines like Google or platform-internal ones may also introduce biases affecting the results returned.

The lack of rigorous collection protocols across various digital platforms, especially in light of the complexity and variety of animal behavior, makes applying digital data sources in behavioral ecology research even more challenging. For example, in exploring bird plumage color aberrations using various digital sources (Google Images and several local platforms devoted to bird watching and photography), Zbyryt and colleagues [ 32 ] highlighted how digital sources and public participation can advance our understanding of less-studied natural phenomena. They showed that color aberrations are more prevalent in urban, larger, and sedentary birds. However, the nature of the input data prevented them from concluding whether these patterns were biologically driven or resulted from inherent biases in their data set that people more easily spot and report large sedentary birds in human settlements. Thus, it is essential to address these and other biases and limitations to understand when and where it is appropriate to use various digital data sources. As a start, combining data from novel digital sources—such as various social media platforms and Google Images—with more rigorous scientific data sets, dedicated fieldwork, or literature surveys, can help validate digital sources and ensure meaningful results. Another approach is creating well-designed question-first citizen science data sets in which researchers recruit and train citizen scientists to collect dedicated data to answer specific questions [ 43 ].

When exploring user-generated content—for example, videos uploaded on social media platforms—we must also consider legal and ethical aspects such as data protection and privacy [ 44 ]. In order to minimize the risk of misusing sensitive data (e.g., IP address, localization details, or user name), we advocate for establishing and following protocols for data protection [ 44 ]. It is also important to note that many social media recordings may be associated with unintentional or even intentional disturbances and harmful actions towards the animal being recorded [ 5 , 45 ], raising ethical concerns as well as questions of interpretation and relevance. Even if individuals are not directly harmed, the context under which data were recorded (e.g., Were domestic animals like dogs present? Did the humans feed the animals before filming?) is not always known, and this may have substantial impacts on the recorded behavior [ 17 ]. Such human disturbances, combined with partial recording and suboptimal recording quality, necessitate extensive filtering processes and the implementing of clear protocols for the inclusion of records. Furthermore, it may limit the use of digital data sources in certain explorations [ 7 ]. While we encourage people to share their nature observations online, we discourage harmful human–nature interactions to obtain these observations. By contrast, recording people’s negative interactions with nature can potentially be helpful for both legal and conservation interventions, as well as for related research.

Finally, while these readily available data sets are relatively easy to obtain, using them requires programming skills, computational power, and storage capacity, among other things [ 46 ]. Accessing various platforms may further require data-sharing agreements, proprietary companies opening their data sets for researchers, and consistency in how data is managed [ 47 ]. Once obtained, data filtering and cleaning processes and analysis would further require advanced technological tools, such as machine learning methods and machine vision models. Such filtering process should also consider for example AI-generated content and ensure only reliable data are used. Post-analysis challenges may include repeatability and reproducibility [ 4 , 48 ] as data may not be archived on different platforms, and downloading and sharing all records may face legal issues (copyrights), as well as storage space limitations. While some of these aspects are beyond our control, keeping clear records of protocols, versions, and codes, as well as publishing metadata and when possible raw data, could increase transparency and help address some limitations [ 4 ].

Conclusions and future outlook

The use of digital data in ecological and evolutionary research on animal behavior has emerged as a promising approach to enhance traditional data sources and overcome several constraints such as lack of time, accessibility, and financial resources. Digital data enables researchers to conduct retrospective analysis and comparisons across various temporal, spatial, and taxonomic scales, providing a potentially vast data set to explore. Moreover, as Internet use continues to grow and new digital platforms emerge, more data will become available, offering further opportunities to advance both basic and applied studies in behavioral ecology. The use of digital data in behavioral ecology is rapidly increasing and will potentially unveil larger data sets and larger audiences than existing citizen science platforms [ 35 , 49 ]. These new databases will enable researchers to ask basic and novel questions and study animal behavior with greater depth and scope. Furthermore, by leveraging social media data created by individuals, researchers can advance knowledge on animal (including human) behavior, promote public engagement with nature, and enhance present and future conservation efforts.

In addition to using data already uploaded to the Internet, scientists can encourage people to upload data containing species or areas of interest for their study. Researchers can also recruit people to help filter, score, or tag data collected online as on the Zooniverse platform ( https://www.zooniverse.org/ ), with the ultimate goal of involving the public in biodiversity conservation and science and facilitating the processing of big data. With advances in AI models, such collection and classification of data can be made automatically (fully or semi), based on taxonomic group or the location where the observation was recorded. This will enhance the ability of researchers to incorporate publicly available data in their studies. For example, using machine learning approaches, Pardo and Wittemyer [ 50 ] were able to find a name-like calling behavior in African savannah elephants ( Loxodonta africana ). However, limited by their sample size, they were not able to isolate and encode specific “name” sounds. Social media recording of tourists in those areas could potentially help in future research.

With the increasing global environmental challenges linked to biodiversity loss and climate change, digital resources are invaluable sources of data, especially in time-sensitive cases. Behavioral aspects such as interspecific interactions or behavioral flexibility are missing from many large-scale analyses and predictions of future species responses to human-driven environmental changes [ 51 , 52 ]. Digital data can greatly improve our ability to successfully integrate such behavioral dimensions into spatial modeling of abiotic changes and help us produce more realistic estimates of future risks and potential species distributions [ 52 ]. Taken together, such studies can help us develop a rich understanding of behavior based on the Tinbergen framework.

From an applied perspective, the field of conservation behavior [ 53 ] can benefit substantially from digital data sources too. Online images and video repositories can help conservation scientists and managers better understand anthropogenic impacts on animal behavior, identify behavioral indicators of changes to the species’ environment, highlight potential human–wildlife conflicts, and design and implement behavior-sensitive management [ 54 ]. With the great advancements in AI and machine learning and the increased availability of big data, we expect that more behavioral ecologists and conservation scientists will start incorporating digital-based data sources and approaches alongside their field and empirical work.

Supporting information

S1 table. examples of publications utilizing digital data for behavioral ecology divided into their potential contribution to understanding animal behavior according to tinbergen’s 4 questions..

https://doi.org/10.1371/journal.pbio.3002793.s001

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Domesticating horses had a huge impact on human society − new science rewrites where and when it first happened

Assistant Professor and Curator of Archaeology, University of Colorado Boulder

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Across human history, no single animal has had a deeper impact on human societies than the horse. But when and how people domesticated horses has been an ongoing scientific mystery.

Half a million years ago or more, early human ancestors hunted horses with wooden spears, the very first weapons , and used their bones for early tools . During the late Paleolithic era, as far back as 30,000 years ago or more, ancient artists chose wild horses as their muse: Horses are the most commonly depicted animal in Eurasian cave art .

Following their first domestication, horses became the foundation of herding life in the grasslands of Inner Asia , and key leaps forward in technology such as the chariot , saddle and stirrup helped make horses the primary means of locomotion for travel, communication, agriculture and warfare across much of the ancient world. With the aid of ocean voyages, these animals eventually reached the shores of every major landmass – even Antarctica, briefly.

As they spread, horses reshaped ecology, social structures and economies at a never-before-seen scale. Ultimately, only industrial mechanization supplanted their near-universal role in society.

Because of their tremendous impact in shaping our collective human story, figuring out when, why and how horses became domesticated is a key step toward understanding the world we live in now.

Doing so has proven to be surprisingly challenging. In my new book, “ Hoof Beats: How Horses Shaped Human History ,” I draw together new archaeological evidence that is revising what scientists like me thought we knew about this story.

A horse domestication hypothesis

Over the years, almost every time and place on Earth has been suggested as a possible origin point for horse domestication, from Europe tens of thousands of years ago to places such as Saudi Arabia, Anatolia, China or even the Americas.

By far the most dominant model for horse domestication, though, has been the Indo-European hypothesis, also known as the “Kurgan hypothesis.” It argues that, sometime in the fourth millennium BCE or before, residents of the steppes of western Asia and the Black Sea known as the Yamnaya, who built large burial mounds called kurgans, hopped astride horses. The newfound mobility of these early riders, the story goes , helped catalyze huge migrations across the continent, distributing ancestral Indo-European languages and cultures across Eurasia.

But what’s the actual evidence supporting the Kurgan hypothesis for the first horse domestication? Many of the most important clues come from the bones and teeth of ancient animals, via a discipline known as archaeozoology . Over the past 20 years, archaeozoological data seemed to converge on the idea that horses were first domesticated in sites of the Botai culture in Kazakhstan, where scientists found large quantities of horse bones at sites dating to the fourth millennium BCE.

Other kinds of compelling circumstantial evidence started to pile up. Archaeologists discovered evidence of what looked like fence post holes that could have been part of ancient corrals. They also found ceramic fragments with fatty horse residues that, based on isotope measurements, seem to have been deposited in the summer months, a time when milk could be collected from domestic horses.

The scientific smoking gun for early horse domestication, though, was a set of changes found on some Botai horse teeth and jawbones. Like the teeth of many modern and ancient ridden horses, the Botai horse teeth appeared to have been worn down by a bridle mouthpiece, or bit.

Together, the data pointed strongly to the idea of horse domestication in northern Kazakhstan around 3500 BCE – not quite the Yamnaya homeland, but close enough geographically to keep the basic Kurgan hypothesis intact.

There were some aspects of the Botai story, though, that never quite lined up. From the outset, several studies showed that the mix of horse remains found at Botai were unlike those found in most later pastoral cultures: Botai is evenly split between male and female horses, mostly of a healthy reproductive age. Killing off healthy, breeding-age animals like this on a regular basis would devastate a breeding herd. But this demographic blend is common among animals that have been hunted. Some Botai horses even have projectile points embedded in their ribs, showing that they died through hunting rather than a controlled slaughter.

These unresolved loose ends loomed over a basic consensus linking the Botai culture to horse domestication.

New scientific tools raise more questions

In recent years, as archaeological and scientific tools have rapidly improved, key assumptions about the cultures of Botai, Yamnaya and the early chapters of the human-horse story have been overturned.

First, improved biomolecular tools show that whatever happened at Botai, it had little to do with the domestication of the horses that live today. In 2018, nuclear genomic sequencing revealed that Botai horses were not the ancestors of domestic horses but of Przewalski’s horse , a wild relative and denizen of the steppe that has never been domesticated, at least in recorded history.

Next, when my colleagues and I reconsidered skeletal features linked to horse riding at Botai, we saw that similar issues are also visible in ice age wild horses from North America, which had certainly never been ridden. Even though horse riding can cause recognizable changes to the teeth and bones of the jaw, we argued that the small issues seen on Botai horses can reasonably be linked to natural variation or life history.

This finding reopened the question: Was there horse transport at Botai at all?

Leaving the Kurgan hypothesis in the past

Over the past few years, trying to make sense of the archaeological record around horse domestication has become an ever more contradictory affair.

For example, in 2023, archaeologists noted that human hip and leg skeletal problems found in Yamnaya and early eastern European burials looked a lot like problems found in mounted riders, consistent with the Kurgan hypothesis. But problems like these can be caused by other kinds of animal transport, including the cattle carts found in Yamnaya-era sites .

So how should archaeologists make sense of these conflicting signals?

A clearer picture may be closer than we think. A detailed genomic study of early Eurasian horses, published in June 2024 in the journal Nature , shows that Yamnaya horses were not ancestors of the first domestic horses, known as the DOM2 lineage. And Yamnaya horses showed no genetic evidence of close control over reproduction, such as changes linked with inbreeding.

Instead, the first DOM2 horses appear just before 2000 BCE, long after the Yamnaya migrations and just before the first burials of horses and chariots also show up in the archaeological record.

For now, all lines of evidence seem to converge on the idea that horse domestication probably did take place in the Black Sea steppes, but much later than the Kurgan hypothesis requires. Instead, human control of horses took off just prior to the explosive spread of horses and chariots across Eurasia during the early second millennium BCE.

There’s still more to be settled, of course. In the latest study, the authors point to some funny patterns in the Botai data, especially fluctuations in genetic estimates for generation time – essentially, how long it takes on average for a population of animals to produce offspring. Might these suggest that Botai people still raised those wild Przewalski’s horses in captivity, but only for meat, without a role in transportation? Perhaps. Future research will let us know for sure.

Either way, out of these conflicting signals, one consideration has become clear: The earliest chapters of the human-horse story are ready for a retelling.

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Impact of operating scale on factor inputs in grassland animal husbandry—intermediary effects based on market risk, 1. introduction, 2. theoretical analysis, 2.1. operating scale and bias in the input of production factors, 2.2. the mediating role of market risk, 3. methodology and data, 3.1. study area, 3.2. methods, 3.2.1. cost contribution model, 3.2.2. cobb–douglas production function model, 3.2.3. multiple linear regression model, 3.2.4. mediation effect model, 4. empirical study, 4.1. analysis of the cost contribution, 4.2. analysis of the bias of production factors input from the economic optimal result, 4.3. analysis of the impact of operating scale on the bias of production factors, 4.3.1. regression results analysis, 4.3.2. mediation effect analysis, 5. conclusions and prospects, 5.1. conclusions, 5.2. policy implications, 5.3. prospects, author contributions, institutional review board statement, informed consent statement, data availability statement, conflicts of interest.

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Xue, C.; Du, F.; Yong, M. Impact of Operating Scale on Factor Inputs in Grassland Animal Husbandry—Intermediary Effects Based on Market Risk. Sustainability 2024 , 16 , 7540. https://doi.org/10.3390/su16177540

Xue C, Du F, Yong M. Impact of Operating Scale on Factor Inputs in Grassland Animal Husbandry—Intermediary Effects Based on Market Risk. Sustainability . 2024; 16(17):7540. https://doi.org/10.3390/su16177540

Xue, Chen, Fulin Du, and Mei Yong. 2024. "Impact of Operating Scale on Factor Inputs in Grassland Animal Husbandry—Intermediary Effects Based on Market Risk" Sustainability 16, no. 17: 7540. https://doi.org/10.3390/su16177540

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