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Frontiers in Zoology

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Context or arousal? Function of drumming in Mongolian gerbils ( Meriones unguiculatus )

Authors: Yara Silberstein, Janina Büntge, Felix Felmy and Marina Scheumann

Material composition and mechanical properties of the venom-injecting forcipules in centipedes

Authors: Simon Züger, Wencke Krings, Stanislav N. Gorb, Thies H. Büscher and Andy Sombke

Nest site selection and fidelity of European pond turtle ( Emys orbicularis ) population of Babat Valley (Gödöllő, Hungary)

Authors: István Kiss, Gergő Erdélyi and Borbála Szabó

Comparative analysis of optional hunting behavior in Cricetinae hamsters using the data compression approach

Authors: J. Levenets, S. Panteleeva, Zh. Reznikova, A. Gureeva, V. Kupriyanov, N. Feoktistova and A. Surov

De novo assembly of transcriptomes and differential gene expression analysis using short-read data from emerging model organisms – a brief guide

Authors: Daniel J. Jackson, Nicolas Cerveau and Nico Posnien

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Dogs are sensitive to small variations of the Earth’s magnetic field

Authors: Vlastimil Hart, Petra Nováková, Erich Pascal Malkemper, Sabine Begall, Vladimír Hanzal, Miloš Ježek, Tomáš Kušta, Veronika Němcová, Jana Adámková, Kateřina Benediktová, Jaroslav Červený and Hynek Burda

The integrative future of taxonomy

Authors: José M Padial, Aurélien Miralles, Ignacio De la Riva and Miguel Vences

A new versatile primer set targeting a short fragment of the mitochondrial COI region for metabarcoding metazoan diversity: application for characterizing coral reef fish gut contents

Authors: Matthieu Leray, Joy Y Yang, Christopher P Meyer, Suzanne C Mills, Natalia Agudelo, Vincent Ranwez, Joel T Boehm and Ryuji J Machida

The importance of immune gene variability (MHC) in evolutionary ecology and conservation

Authors: Simone Sommer

Fog-basking behaviour and water collection efficiency in Namib Desert Darkling beetles

Authors: Thomas Nørgaard and Marie Dacke

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Now accepting submissions: Establishing methods for gene function studies in emerging model organisms – a brief guide

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Featured blog: Southeast Asian clearwing moths buzz like their model bees

Aims and scope.

Frontiers in Zoology is an open access, peer-reviewed online journal publishing high quality research articles and reviews on all aspects of animal life.

As a biological discipline, zoology has one of the longest histories. Today it occasionally appears as though, due to the rapid expansion of life sciences, zoology has been replaced by more or less independent sub-disciplines amongst which exchange is often sparse. However, the recent advance of molecular methodology into "classical" fields of biology, and the development of theories that can explain phenomena on different levels of organisation, has led to a re-integration of zoological disciplines promoting a broader than usual approach to zoological questions. Zoology has re-emerged as an integrative discipline encompassing the most diverse aspects of animal life, from the level of the gene to the level of the ecosystem.

Frontiers in Zoology is the first open access journal focusing on zoology as a whole. It aims to represent and re-unite the various disciplines that look at animal life from different perspectives and at providing the basis for a comprehensive understanding of zoological phenomena on all levels of analysis. Frontiers in Zoology provides a unique opportunity to publish high quality research and reviews on zoological issues that will be internationally accessible to any reader at no cost.

The journal was initiated and is supported by the Deutsche Zoologische Gesellschaft, one of the largest national zoological societies with more than a century-long tradition in promoting high-level zoological research.

Editors-in-Chief

Jürgen Heinze is currently Professor of Zoology at University of Regensburg, Germany.

"Zoology is an active and colorful biological discipline with a long history and a promising future. The development of new theories and methodology makes this a particularly exciting time for researchers interested in aspects of animal life."

Ulrich Technau is Professor of developmental biology at the University of Vienna, Austria.

"Zoology is addressing some of the most fundamental questions in Biology. It continues to deliver novel insights into the fascinating diversity and biology of animals by taking advantage of a combination of classical concepts and modern methods."

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Deutsche Zoologische Gesellschaft (German Society of Zoology)

Annual Journal Metrics

Citation Impact 2023 Journal Impact Factor: 2.6 5-year Journal Impact Factor: 2.6 Source Normalized Impact per Paper (SNIP): 1.079 SCImago Journal Rank (SJR): 0.917

Speed 2023 Submission to first editorial decision (median days): 4 Submission to acceptance (median days): 124

Usage 2023 Downloads: 601,349 Altmetric mentions: 1,038

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NEW: Bringing fossils back to life

Guest Edited by Marcos D. Ercoli and Jamie A. MacLaren.

Birds and environment

Guest Edited by Ashish Kumar Arya, Archana Bachheti, Kamal Kant Joshi and Vinaya Kumar Sethi 

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Guest Edited by Brock Fenton and Federico Plazzi

Editor's Pick

Giant pandas in captivity undergo short-term adaptation in nerve-related pathways                                   ,                                                   high disparity in repellent gland anatomy across major lineages of stick and leaf insects           .

Morphological and functional trait divergence in endemic fish populations         

Featured blogs, behind the paper: lions & sea lions & bears, oh my.

In his blog, Alexander Okamoto discusses the importance of museum specimens in studying mammalian bone formation outside conventional model systems.

BMC Series: What makes a fighting fish fight?

Kyriacos Kareklas speaks about how his work on Siamese fighting fish challenges traditional models on animal fighting behavior and sheds light on flexible decision-making in contests.

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Assessment of bird diversity and abundance in Mai-Nigus artificial reservoir and surrounding semi-forest in Tigray Region, Northern Ethiopia

Authors: Alembrhan Assefa, Kalayu Mesfin, Weldemariam Tesfahunegny, Birkti Fitsum, Amleset Gaim and Teklay Meles

Topography and morphology of the Eira barbara diaphragm

Authors: Aryane Maximina Melo Silva, Rogério Pereira Silva, Rogério Antônio Ribeiro Rodrigues, Elane Guerreiro Giese, Ana Rita Lima and Érika Branco

Estimation of mammalian wildlife density by REM method in a Mediterranean forest ecosystem ( Pinus brutia ) of Türkiye: how human footprint effects mammal community?

Authors: Yasin İlemin

Biological aspects of the lingual papillae of the Arab Zebu cattle: a new perspicuity of its chad ecological adaptations

Authors: Mohamed Abumandour, Seham Haddad, Foad Farrag, Ramadan Kandyel, Karam Roshdy, Diaa Massoud and Eman Kamal Khalil

Human-De Brazza’s monkey conflict in Kafa Biosphere Reserve, Kafa Zone South West, Ethiopia

Authors: Melaku Haile, Tsegaye Gadisa and Tariku Mekonnen Gutema

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Fishing for iodine: what aquatic foraging by bonobos tells us about human evolution

Authors: Gottfried Hohmann, Sylvia Ortmann, Thomas Remer and Barbara Fruth

Nymphister kronaueri von Beeren & Tishechkin sp. nov., an army ant-associated beetle species (Coleoptera: Histeridae: Haeteriinae) with an exceptional mechanism of phoresy

Authors: Christoph von Beeren and Alexey K. Tishechkin

LemurFaceID: a face recognition system to facilitate individual identification of lemurs

Authors: David Crouse, Rachel L. Jacobs, Zach Richardson, Scott Klum, Anil Jain, Andrea L. Baden and Stacey R. Tecot

White-nose syndrome fungus, Pseudogymnoascus destructans, on bats captured emerging from caves during winter in the southeastern United States

Authors: Riley F. Bernard, Emma V. Willcox, Katy L. Parise, Jeffrey T. Foster and Gary F. McCracken

Micro-CT imaging of live insects using carbon dioxide gas-induced hypoxia as anesthetic with minimal impact on certain subsequent life history traits

Authors: Danny Poinapen, Joanna K. Konopka, Joseph U. Umoh, Chris J. D. Norley, Jeremy N. McNeil and David W. Holdsworth

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Aims and scope

BMC Zoology is an open access, peer-reviewed journal that considers articles on all aspects of zoology, including comparative physiology, mechanistic and functional studies, morphology, life history, animal behavior, signaling and communication, cognition, parasitism, systematics, biogeography and conservation.

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We are delighted to announce the launch of our first joint BMC Ecology and Evolution and BMC Zoology image competition! Bringing together art and science, the competition aims to showcase the beauty of ecology, evolutionary biology and zoological research. Guidelines to enter can be found here .  

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02 September 2024

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22 August 2024

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Citation Impact 2023 Journal Impact Factor: 1.4 5-year Journal Impact Factor: 1.6 Source Normalized Impact per Paper (SNIP): 0.644 SCImago Journal Rank (SJR): 0.498 Speed 2023 Submission to first editorial decision (median days): 19 Submission to acceptance (median days): 179 Usage 2023 Downloads: 236,174 Altmetric mentions: 189

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ISSN: 2056-3132

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Page 1 of 8

Physiological responses of Lizard, Toad and Pigeon during rainy season in tropical savanna climate

This study investigated the adaptation mechanisms of Pigeons, Toads and Lizards during the rainy season in tropical savanna climates. Male Agama Lizards ( Agama agama ), Afep Pigeons ( Columba unicincta ) and Toads (

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Biologically engineered probiotic supplement production containing phytase enzyme for livestock, poultry, and aquaculture consumption

Livestock and aquaculture feed rely heavily on cereals, fish meal, and plant proteins, but these ingredients are not fully utilized by animals, and alternative protein sources are needed due to rising demand, ...

Alteration in butterfly community structure along urban–rural gradient: with insights to conservation management

Ecosystem services rendered by the butterflies are important for the sustenance of community interaction. Butterfly species have also coevolved with the host and nectaring plants. In the adult condition, they ...

Studies on the influence of water quality on community assemblage of immature mosquitoes in different ecosystems along the Vaigai river, Tamil Nadu, South India

Over the last few decades, river ecosystem is highly modified through various anthropogenic activities which are resulted to alter ecosystem functions and services. This modified ecosystem rendering conducive ...

Association between the visceral leishmaniasis vector Lutzomyia longipalpis and tree families in a Brazilian tropical urban area

Visceral leishmaniasis (VL) is a neglected disease endemic to many tropical and subtropical countries. In Brazil, VL is caused by the protozoan parasite Leishmania infantum and is transmitted by the sand fly Lutz...

Pomegranate juice recuperates N ’-Nitrosodiethylamine-induced kidney injury: evidence from biochemical and histological approaches

Pomegranate is considered as one of the oldest elixirs having various properties. Renal fibrosis is a preliminary sign of pathological degradation in most ailments related to kidney. Several efforts have been ...

Molecular study of CYP21 gene polymorphism rs13405728 and CYP11A1 gene polymorphism rs4077582 in polycystic ovarian syndrome patients

PCOS is a serious endocrine-metabolic condition characterized by hyperandrogenemia, anovulation, or oligo-ovulation, and links to obesity, insulin resistance, and an elevated risk of type 2 diabetes mellitus. ...

Microscopic alterations and adaptation in the lungs of the Japanese quail exposed to acute or chronic heat stress

Global warming causes heat stress, a significant bioclimatic factor affecting poultry welfare. The effects of heat stress on the morphology of the Japanese quail lungs were investigated in this study. A total ...

Present status of Papaya Mealybug, Paracoccus marginatus Williams and Granara de Willink, in Assam, India, after a decade of its first invasion

The North Eastern Region (NER) of India is well known for its rich biodiversity and organic cultivation; however, this is one of the least investigated regions owing to its remoteness. A field study on papaya ...

Lowering vector competence in insects: a review

Insects act as disease vectors, spreading disease-causing organisms between plants and animals. There have been studies devoted to determining ways to control these pests. One of the most effective ways to acc...

Assessment of the ecological status of an ancient reservoir using macroinvertebrate assemblage and water quality parameters

Atori Reservoir, located in the heart of southwestern Nigeria, is a tribute to the region's historical significance and natural splendor. Its establishment as a reservoir in 1935 marked a water resource manage...

In vitro molluscicidal activity and biochemical impacts of some thiophene derivatives against the glassy clover snail, Monacha obstructa (Pfeiffer)

The glassy clover snail, Monacha obstructa (Pfeiffer), is considered one of the major agricultural pests that ruin many field crops, vegetables, orchards of fruits, plants of ornament as well as many other planta...

Oxidative stress markers in brain and gonads of rabbit bucks fed herbal supplements

Currently, there is an increase in the usage of phytogenic feed additives to help improve animal welfare and productivity, while less emphasis is now placed on metabolic and oxidative stability of neuronal and...

Growth performance, biochemical outcomes, and testicular histological features in male Japanese quails supplemented with milk thistle seeds

Due to its rich content of active phytochemicals, milk thistle is regarded as a promising nutritional supplement for quails, particularly in regions with limited financial resources. Thus, our study aimed to e...

Analysis of different bioactive compounds in the tissue of the epigeic earthworm, Eisenia fetida

Eisenia fetida is the epigeic earthworm renowned for organic waste management in vermitechnology. The medicinal properties of earthworm biomass is gaining much more importance in extracting various biomolecules. ...

Neurotensin receptor-1 agonist PD 149163 modulates the lipopolysaccharide-induced behavioral disturbances in mice

Neuroendocrine-immune homeostasis is a prerequisite for neurobehavioral performances. Dysregulation of this homeostasis manifested in behavioral dysfunctions and neurodegenerative diseases, including schizophr...

Effects of varying photoperiodic regimens on oviposition behavior of Anopheles subpictus and Culex quinquefasciatus

Environmental factors influence the mosquito behavior, particularly the oviposition behavior. Therefore, understanding the response of mosquitoes to their environmental conditions like photoperiod, humidity, r...

Alternaria alternata as emerging threat for Hoplobatrachus tigerinus and Phrynoderma hexadactylum in southern West Bengal, India

Amphibians are facing a global decline for the last few decades due to habitat loss, pesticide pollution, diseases and some other reasons. Fungal disease called chytridiomycosis has been emerged as one of the ...

Gallic acid counteracts tartrazine-induced testicular dysfunction in rats: biochemical, histopathological and ultrastructural evidences

Tartrazine (Tz) is one of the most commonly used colorants incorporated in the food manufacturing. Its toxicity is derived from metabolic byproducts representing health hazards to consumers. Gallic acid (GA) i...

Probiotics in poultry: a comprehensive review

The increase in global population has elevated the food demand which in turn escalated the food animal production systems, especially poultry industries. For a long time, antibiotics are used worldwide to safe...

Morphologic and phylogenetic investigations revealed size-divergent clades in chelae morphotypes of freshwater prawn Macrobrachium vollenhovenii Herklots (Decapoda: Palaemonidae) in a lake and river system of Southwest Nigeria

The freshwater prawn Macrobrachium vollenhovenii is one of the largest Macrobrachium species, a biological agent against human schistosomiasis, and a cheap protein source in riverine communities in West Africa. H...

Confirmed presence of the enigmatic ant Aphaenogaster gemella (Hymenoptera: Formicidae) in Iberia

While the Iberian Peninsula has been relatively well-studied from a myrmecological standpoint, the true presence of certain ant species has remained obscure for decades. In this context, the case of A. gemella (R...

Ginger ( Zingiber officinale ) attenuates the neurotoxicity in rats induced by organophosphate pesticide

We are exposed to different chemicals in various ways in our daily life, and these can be toxic at minute concentrations. The pesticides used for different purposes are also toxic and may pose threat to life b...

Triazophos toxicity induced histological abnormalities in Heteropneustes fossilis Bloch 1794 (Siluriformes: Heteropneustidae) organs and assessment of recovery response

Agricultural pesticides have toxic effects in the aquatic ecosystem, and their persistence poses a hazard to aquatic life, as seen by fish poisoning, both acute and chronic. Triazophos, a broad-spectrum organo...

The repository of biocontrol agents for Spodoptera frugiperda (Smith, 1797) with emphasis on their mode of action

Spodoptera frugiperda (Smith, 1797) is one of the most destructive pests of Maize plants, causing an estimated 40% crop loss in 2019. It is a native pest of America and difficult to control since it has developed...

A review on the anti-parasitic activity of ruthenium compounds

There are many infectious diseases in the world caused by parasites. Among them, toxoplasmosis, American trypanosomiasis, African trypanosomiasis, leishmaniasis, neosporosis and malaria are more common and con...

Evidences of in vivo cytotoxic and apoptotic potential of anthelmintic phytochemical kaempferol derivative isolated from Lysimachia ramosa (Wall. ex Duby) in Wistar rats

Lysimachia ramosa (Wall. ex Duby) is a traditionally used medicinal plant in Meghalaya, a northeastern state of India. The people use the leaves of the plant to cure gastrointestinal worm infection. Kaempferol de...

A comprehensive examination of camel ( Camelus Dromedaries ) otic prominence through morphological and CT imaging studies

This study explored the morphological anatomy of otic prominences in camels using advanced computed tomography (CT). Nine adult cadaver camel heads underwent CT scanning to generate detailed images of the otic...

Dominance structure and constancy of spiders in the Indian Thar desert

The knowledge about the species of a habitat (both resident and transient/dominant and rare) is a vital step to plan the conservation measures. Being generalist predators, spiders help controlling the populati...

Exochorionic pattern of ten sand fly species (Diptera: Psychodidae: Phlebotominae) from Mexico

Phlebotomine sand flies are of biological importance because of their role as vectors of several pathogens. Morphological identification faces challenges to separate related species; therefore, the study of im...

Effect of dietary seaweed Caulerpa racemosa on growth, biochemical, non-specific immunity, and disease resistance to Pseudomonas aeruginosa in Cirrhinus mrigala

The green seaweed Caulerpa racemosa possesses highly potential elements in animal forages and human use since ancient times. The current study was designed to investigate the antioxidants, phytochemical propertie...

Histological features of the gastrointestinal tract of elongate tigerfish, Hydrocynus forskahlii (Cuvier, 1819), from Lake Albert

The tigerfish ( Hydrocynus forskahlii ) is an important food fish in different regions of Africa. As such, interest in its performance and nutritional requirements as a potential candidate for aquaculture is increa...

Histopathological alterations in the vital organs of Indian major carp Labeo rohita exposed to monosodium glutamate (MSG)

Monosodium glutamate (MSG E621) is one of the most popular flavouring agents of modern times and is widely used in many commercially packed food and even in house hold cooking. Previous studies revealed that e...

Efficacy of combined formulation of bromadiolone and cholecalciferol in reducing rodent population and damage in agricultural crop fields

Field rodents cause significant damage to standing crops in agroecosystems at vulnerable stages. Of all the methods available, chemical rodent control is the most practical and economically feasible. Laborator...

Embryotoxicity of fluconazole on developing chick embryos

Fluconazole is a first-generation triazole used as an antifungal treatment for skin, hair, and nail infections. The study aimed to assess the embryotoxicity and teratological effects of fluconazole on chick em...

The potential of microRNAs in cancer diagnostic and therapeutic strategies: a narrative review

microRNAs (miRNAs/miRs) are endogenous non-coding RNAs that post-transcriptionally regulate gene expression. Altered miRNA expression promotes oncogenesis by changing the expression of genes involved in key bi...

Unveiling polymorphism and protein structure prediction insights in diacylglycerol O-acyltransferase 1 and telethonin genes of Egyptian buffalo

The Egyptian buffalo has a sizable impact on Egypt's agricultural sector and food supply. It is regarded as the main dairy animal and an important source of red meat. This study aimed to detect the polymorphis...

Termite species and functional diversity as determined by vegetation and edaphic characteristics in a savanna ecosystem

Savanna ecosystems support a diversity of biota and are influenced by vegetation and edaphic characteristics, shaping resident communities. This study was carried out at Mlawula nature reserve, a protected sav...

Concentration and risk assessment of Cryptosporidium infection associated with exposure to the Njoro River, Njoro Sub-County, Nakuru, Kenya

Cryptosporidium  is a gastrointestinal pathogen. The oocysts are transmitted through the environment, and drinking contaminated water is one particular route. There is heavy pollution of Cryptosporidium in Njoro R...

Preliminary monosodium glutamate-induced changes in mammary gland receptors and gene expression, water channel, oxidative stress, and some lactogenic biomarkers in lactating rats

Changes induced by monosodium glutamate (MSG) can negatively impact milk production and secretion, among other adverse effects. This study aimed to investigate the effects of MSG consumption on receptor gene e...

Proposal of a mosquito control plan of Smir-Restinga region (north-west of Morocco)

The present study conducted on mosquitoes in the region of Restinga Smir, located in the north-west of Morocco, attempts to provide a scientific platform for an appropriate mosquito control plan for this touri...

Liver and mucous secretion enzymatic biomarkers of Eobania vermiculata treated with some newly synthesized acrylamide derivatives

Acrylamide derivatives have a potential biological activity as well as acting as precursors in many organic syntheses. Moreover, acrylamides and their derivatives cause convulsions and diffused damage to diffe...

Antilithiatic effect of Triticum aestivum against sodium oxalate-induced lithiasis in rat model

The present study pointed to evaluate the role of Triticum aestivum ethanolic extract (TAEE) in prophylactic and curative regimens on sodium oxalate (NaOx)-prompted lithiasis. Forty-eight rats were divided into t...

A novel pyrazole–pyridine derivative (PPD) targets specific biological pathways in the larval stages of the northern house mosquito Culex pipiens Linnaeus (Diptera: Culicidae)

Mosquitoes cause a variety of health problems in humans and pets. So, the control of mosquito larvae is one of the best ways to avoid health problems arising from diseases transmitted by these insects. There a...

Pangenomics of the cichlid species ( Oreochromis niloticus ) reveals genetic admixture ancestry with potential for aquaculture improvement in Kenya

Nile tilapia has a variety of phenotypes suitable for aquaculture farming, yet its entire gene pool with potential for breeding climate ready strains in resource-limited settings remains scanty and poorly docu...

Evaluation of Galleria mellonella immune response as a key step toward plastic degradation

Plastic's remarkable durability presents a significant challenge for our planet, leading to widespread environmental damage. However, some organisms, such as Galleria mellonella larvae, have shown a unique capabi...

Dietary assessment across various life stages of seven-spotted lady beetle Coccinella septempunctata (Coleoptera: Coccinellidae)

Coccinella septempunctata (L.) is an important predator in fighting against aphids on edible crops and vegetables. However, to establish a successful mass-rearing technique, it is crucial to determine the optimal...

The collagen enhancement by Spirulina extract in intrinsic and extrinsic skin aging in albino rat

The aging of the skin is considered a cumulative process that is classed as intrinsic or extrinsic. Environmental factors like sun exposure and air pollution are considered the main cause of extrinsic aging. M...

Proanthocyanidin and sodium butyrate synergistically modulate rat colon carcinogenesis by scavenging free radicals and regulating the COX-2 and APC pathways

The purpose of this study was to explore the effects of sodium butyrate (NaB), grape seed proanthocyanidin extract (GSPE), or their combination against dimethylhydrazine (DMH)-induced aberrant crypt foci (ACF)...

Relationship pattern of enteric bacterial load and assessed micronutrients in the gut of Clarias gariepinus fish sampled in the Ibadan municipal zone

Farmed fish are faced with factors like microflora and micronutrients that could impact their prime health. There is no clear understanding of some specific bacterial flora amidst micronutrients in the gut of ...

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The Journal of Basic and Applied Zoology  is affiliated with the Egyptian Society for Biosciences Advancement (formerly Egyptian German Society for Zoology).

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Citation Impact 2023 Journal Impact Factor: 1.1 5-year Journal Impact Factor: N/A Source Normalized Impact per Paper (SNIP): N/A SCImago Journal Rank (SJR): N/A

Speed 2023 Submission to first editorial decision (median days): 32 Submission to acceptance (median days): 299

Usage 2023 Downloads: 361,833 Altmetric mentions: 26

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• v.43(1); 2022 Jan 18

Zoological Research shines in the East

With the long-term support of every friend and contributor, Zoological Research ( ZR ) has continued to move forward over the past year, with impressive achievements. Notably, ZR attained an impact factor of 4.56 (JCR Q1) and CiteScore of 4.6 in mid-2021, thus ranking in the top five of the 175 SCI journals within the Zoology category. In November 2021, our Citescore reached 5.6, and we expect a higher impact factor in 2022 than in 2021. Although we are not driven by chasing these scores, the increase in these metrics does reflect an elevation in the quality of submissions and publications, as well as the march towards our original aspiration when launching this journal ( Yao et al., 2019 ). The current areas of focus of ZR (i.e., primate and animal models; animal diversity and evolution; conservation & utilization of animal resources) are not only tightly connected to our host – the Kunming Institute of Zoology, which has grown and evolved into “ a comprehensive research institution renowned for its remarkable achievements in evolutionary mechanisms of animal biodiversity, animal resources protection, and sustainable utilization ” ( Yao & Shen, 2019 ) – but also represent the very frontiers of zoology.

Globally, 2020 and 2021 were tough years due to the continuing COVID-19 pandemic. However, with dedicated and focused research from submitting authors, ZR published a variety of important and timely studies over the past two years on a broad range of topics. Several studies on COVID-19, e.g., Yu et al. ( 2020 ) and Gómez-Carballa et al. ( 2020 ), received wide attention in the field and were scored as Hot Papers according to the Web of Science in June 2021. Similarly, another five ZR papers ( Li et al., 2020 ; Tang et al., 2020 ; Wang et al., 2017 ; Xu et al., 2020 ; Yu et al., 2020 ) were featured as Highly Cited Papers by the Web of Science during the same season. ZR also published other high-profile papers in 2021. For instance, Li et al. ( 2021 ) performed a phylogenetic and morphological investigation of an overlooked flying squirrel species (Pteromyini, Rodentia) from the eastern Himalayas and described a new genus; Boubli et al. ( 2021 ) resolved a taxonomic conundrum of pygmy marmosets using ancient DNA of the type specimen; and Ye et al. ( 2021 ) provided an updated annotation of the Chinese tree shrew genome based on large-scale RNA sequencing and long-read isoform sequencing, which will surely become an essential reference for basic and biomedical studies using tree shrews. To list all the important studies published in ZR in 2021 is obviously beyond the scope of this editorial. However, we are proud of our growing reputation among the authors of these papers and their remarkable advances in important research, with many citations in well-regarded journals, such as Nature , Nature Communications , National Science Review , Advanced Science , PNAS , Biological Psychiatry , Molecular Psychiatry , Medicinal Research Reviews , Nature Cell Biology , Cell Research , Molecular Cell, and Nucleic Acids Research .

Excitingly, in 2021, Prof. Le Kang and Prof. Nina Jablonski were elected as international and national members, respectively, of the National Academy of Sciences of the United States. We remain greatly honored to have them as editorial board members of ZR and extend our warmest congratulations to both these outstanding scientists. In addition, to further foster the impact of ZR and strengthen our publishing team, ZR has recruited young and capable researchers to expand our dynamic editorial board. From the beginning of 2022, with continuous support from senior editorial board members, we are honored to welcome a new group of talented and academically diverse members to ZR . While new editors have a more flexible one-year term than senior editorial board members (four-year term), their term can be renewed based on their willingness, devotion, and performance. We believe this new strategy will help younger scientists establish their own academic careers and will help enhance the vitality and creativity of ZR .

When we look back at the evolution of ZR over the past four decades ( Yao & Jiang, 2021 ), we have certainly encountered many challenges, including the initial dip in readership during the conversion from a Chinese to English-only language publication seven years ago, as well as solo publishing without help from renowned platforms such as Springer-Nature, Wiley Press, and Cell Press. Despite these difficulties, ZR has not stopped its march ahead and remains a shining beacon in the East. ZR has always garnered strong support from our many readers and authors. To better serve our contributors, as well as society in general, our growing capacity is not only reflected by the increase in publication quantity, but more importantly, by the academic quality of each paper. ZR always welcomes hot topics within the scope of the journal. If you wish to publish extraordinary research or serve as a guest editor for a special column/issue, please be free to contact us or the Editorial Office.

Finally, but most importantly, we would like to express our deepest appreciation to every ZR supporter. Your interest in ZR is the fuel with which we continue to move forward. We are always proud to publish your research, and we believe that ZR will continue to shine in the East with your enduring faith and support.

Yong-Gang Yao, Editor-in-Chief

Kunming Institute of Zoology , Chinese Academy of Sciences, Kunming, Yunnan 650223, China

Yun Zhang, Executive Editor-in-Chief

Kunming Institute of Zoology, Chinese Academy of Sciences, Kunming Yunnan 650223, China

Zoology - Science topic

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• Published: 09 September 2024

Environmental stress reduces shark residency to coral reefs

• Michael J. Williamson   ORCID: orcid.org/0000-0001-9681-8920 1 , 2 , 3 ,
• Emma J. Tebbs   ORCID: orcid.org/0000-0003-0575-1236 2 ,
• David J. Curnick   ORCID: orcid.org/0000-0002-3093-1282 1 ,
• Francesco Ferretti 4 ,
• Aaron B. Carlisle 5 ,
• Taylor K. Chapple 6 ,
• Robert J. Schallert 7 ,
• David M. Tickler 8 ,
• Barbara A. Block 7 &
• David M. P. Jacoby   ORCID: orcid.org/0000-0003-2729-3811 1 , 9  

Communications Biology volume  7 , Article number:  1018 ( 2024 ) Cite this article

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• Animal behaviour
• Behavioural ecology
• Climate-change ecology

Coral reef ecosystems are highly threatened and can be extremely sensitive to the effects of climate change. Multiple shark species rely on coral reefs as important habitat and, as such, play a number of significant ecological roles in these ecosystems. How environmental stress impacts routine, site-attached reef shark behavior, remains relatively unexplored. Here, we combine 8 years of acoustic tracking data (2013-2020) from grey reef sharks resident to the remote coral reefs of the Chagos Archipelago in the Central Indian Ocean, with a satellite-based index of coral reef environmental stress exposure. We show that on average across the region, increased stress on the reefs significantly reduces grey reef shark residency, promoting more diffuse space use and increasing time away from shallow forereefs. Importantly, this impact has a lagged effect for up to 16 months. This may have important physiological and conservation consequences for reef sharks, as well as broader implications for reef ecosystem functioning. As climate change is predicted to increase environmental stress on coral reef ecosystems, understanding how site-attached predators respond to stress will be crucial for forecasting the functional significance of altering predator behavior and the potential impacts on conservation for both reef sharks and coral reefs themselves.

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Introduction.

Over the past 20 years there has been a significant decline of coral cover across the world’s coral reef ecosystems due to increases in disease, tropical cyclones, and bleaching events 1 , 2 . Coral bleaching can cause increased mortality, reduced coral cover, loss of structural complexity, reduced biodiversity as well as altering species and community composition and ecosystem function 3 , 4 , 5 . Multiple shark species are reliant on coral reefs as important habitat for feeding, breeding and as social refugia 6 , 7 , 8 . Consequently, climate change induced changes in coral reef habitat have the potential to significantly impact the behaviour of predators associated with reef ecosystems, such as reef sharks 9 , 10 . Despite widespread awareness of the perilous state of global shark populations 11 , including reef sharks 12 , 13 , the link between habitat quality, changing environmental drivers, and movement ecology, as well as how these factors interact to impact population vulnerability, remains relatively unexplored 6 .

Reef sharks exhibit routine use of habitats and different ecological landscapes, as they feed, develop and reproduce 14 , 15 . Residency, defined as ‘an individual exhibiting largely uninterrupted occupancy of a limited area for a specified period of time’ 16 , is one aspect of routine animal movement which facilitates crucial ecological processes, and thus is inherently linked to habitat quality, trophic interactions and population persistence 17 , 18 . However, many of the drivers influencing residency in reef shark species, including environmental stress, are not well understood. Changes in reef shark behaviour may have significant implications for ecological processes, such as population dynamics 19 , predator-prey landscapes 20 , nutrient transfer 21 , dispersal 22 , and management and conservation 23 . As such, understanding species responses to disturbance and the longevity or lag in these responses, especially in light of increasing anthropogenic impacts, is becoming ever more important as we face the current biodiversity crisis 24 .

Grey reef sharks ( Carcharhinus amblyrhynchos ) are an Indo-Pacific distributed shark species, commonly associated with coral reefs 7 , 25 and currently listed as Endangered by the International Union for the Conservation of Nature (IUCN) 26 . Grey reef sharks are site-attached, central place foragers which move periodically and predictably from a core area of residency 27 . This behavioural trait make them a good model for evaluating residency, and particularly amenable to acoustic telemetry, where receivers can be located around coral reefs or atolls to monitor long-term space use within core areas and movements within shallow waters 6 , 28 . As reef shark species are increasingly threatened with extinction 12 , long-term data from widely distributed model species, particularly how shark movement is altered with changing environmental conditions on coral reefs, is valuable for informing conservation and management strategies.

Environmental stress can be defined as negative impacts on the growth and health of ecosystems resulting from changes or extremes in environmental variables 29 , 30 . Coral reefs are susceptible to a number of environmental stressors 31 , which in turn may impact reef shark populations. However, there can be significant inter-, and intra-regional variance in how different environmental variables drive stress on these ecosystems 32 , 33 . For example, an environmental stress index, based on satellite remote sensing data that allows assessment of multiple abiotic environmental stressors, recently found that sea surface temperature (SST), current and wind were the primary drivers of environmental stress in the Chagos Archipelago in the Indian Ocean, however depth and SST, and Degree Heating Weeks (DHW), SST, and current, were stronger drivers of stress on coral reefs in the Red Sea and the Gilbert Islands, respectively 32 . Composite indices such as this, therefore, capture interactive variables that may increase, or reduce, environmental stress, providing an opportunity to gain a more holistic understanding of how multiple environmental stressors on coral reefs can impact reef shark movement and residency.

This study aims to investigate how reef shark residency to remote coral reefs is influenced by environmental stress to the reef itself, using an index that balances the following remotely sensed environmental variables: cloud cover, current, depth, salinity, four metrics of SST (SST, DHW, SST anomaly, SST variability), and wind. As reef shark residency is likely to be in part influenced by changes in environmental conditions 15 , 34 , we hypothesise that as environmental stress on coral reefs increases, reef shark residency will decrease. We suggest this is a behavioural response designed to locate more appropriate habitat, enhance resource availability (e.g., prey, physical or thermal refugia), thus decreasing residency to coral reef ecosystems.

Following data preparation and filtering, 714,810 detections from 122 grey reef sharks (81 female, 41 male) from 52 receivers were used for analysis. Grey reef shark lengths ranged from 70–159 cm with mean (SD) = 117.9 cm (19.6) (Supplementary Data  1 ). Residency index for grey reef sharks ranged from 0.03 to 1.00 with mean (SD) = 0.34 (0.33). Environmental Stress Exposure (SE) index values, calculated at the estimated range of each acoustic receiver, varied from 0.03–0.60 with mean (SD) = 0.22 (0.09), on a scale of 0–1 (low to high stress).

Residuals of the global model were free from heteroscedasticity and temporal autocorrelation (Supplementary Fig.  1 ). Following the dredge and nesting of the global model, two candidate models were found with ΔAICc values < 2 (Supplementary Table  1 ). Relative importance values of environmental stress exposure (SE) index, season, sex, and year were all greater than 0, indicating they are important predictors for explaining residency in reef sharks (Table  1 ). Total length had a relative importance of zero and was not deemed an important predictor.

Model averaging of the two candidate models indicated that environmental SE, season, and year were all significant predictors of residency in grey reef sharks in the Chagos Archipelago (Table  1 ). A significant negative relationship between residency and combined environmental SE index was found (estimate = −0.1, z  = −10.48, p  < 0.001, Fig.  1 ), indicating that on average across the reefs of the northern atolls of the archipelago, grey reef sharks became less resident as environmental stress on reefs increased, particularly during strong El Niño conditions, albeit with a delay in these effects during the strong El Niño event. Kernel estimates (KUD) of core (50%), 75% and 95% space use all increased almost immediately during elevated periods of stress exposure, suggesting space use became more diffuse (Fig.  1B ). The variance and standard deviation of the random factors ID and station on the logit scale were 1.90 and 1.38, and 1.58 and 1.26, respectively. Marginal R 2 (R2m) was 0.02 and conditional R 2 (R2c) 0.52, suggesting high variation between stations and individuals. Results from conditional models of the random effects and their standard deviations suggest that 56% (29/52) of receivers had residency significantly different from the intercept, with some showing increased residency (Fig.  2 ). A similar relationship between residency and combined environmental SE index (estimate = −0.07, z  = −4.34, p  < 0.001) (Supplementary Table  2 ) was found even after data from El Niño periods were removed, suggesting persistence of this trend even without extreme climatic events known to cause high environmental stress to coral reefs. The median duration of time spent away from the forereefs were not stochastically equal between times of low and high stress; grey reef sharks were absent for significantly longer when stress was high (Brunner-Munzel; P̂*(1235.9) = −2.8336, p  = 0.0047). The probability that sharks would remain away from the forereef longer during times of stress was 0.4661 (Fig.  3A ).

Temporal trends in combined environmental stress exposure (SE) index experienced by coral reefs in the northern atolls of the Chagos Archipelago during a strong El Niño ‘episode’ and weaker El Niño ‘conditions’ ( A ). Grey reef shark residency (blue trend line) during the same period (Feb 2013–Feb 2021) and temporal changes in area use (km 2 ) measured as the 50% (yellow), 75% (green) and 95% (pink) kernel utilisation estimation (KUD) ( B ).

A Departures of 122 grey reef sharks from the global intercept are plotted with 95% CIs (black bars). Receivers where CIs do not cross zero indicate average residency significantly different than the average. Receivers where grey reef sharks had less than the average residency have negative global intercept values, and those that had more have positive intercept values. B Spatial distribution of acoustic receivers ( n  = 52) coloured by departure from global intercept, where pink is significantly more resident and green significantly less resident (transparent = no change in residency).

A The mean delay in log days, between detections for 122 grey reef sharks leaving the forereef (note: for clarity we represent the mean but test the median using a Brunner-Munzel test to show that the probability that sharks would remain away from the forereef longer during times of stress was 0.466). Box plot represents median mean delay in log days and the interquartile range. Whiskers extend from the hinge to the highest and lowest values within 1.5× the interquartile range. Outliers are not visualised. B The proportion of tagged 122 grey reef sharks falling within each mean residency index bin (0.0–1.0) across 14 sixth monthly periods. Yellow/red indicate El Niño conditions and blue, non-El Niño conditions.

Cross correlations of mean environmental SE index and mean residency index indicated lagged effects (Supplementary Fig.  2 ) with significant negative values at t  − 0 to t  + 16, indicating that ‘current’ environmental stress on coral reefs has a significant persistent negative impact on grey reef shark residency for up to 16 months (Fig.  1 ). Within this time period, correlation coefficient values varied between −0.16 and −0.37. There was also a significant relationship between residency and season, with grey reef sharks in the wet season less resident than during the dry season (Table  1 ) (estimate = −0.40, z  = −21.73, p  < 0.001). Residency behaviour significantly differed in all years, except 2014 and 2018, compared to the baseline year of 2013 (Table  1 ). Sex was not a significant predictor of residency.

Generalised Additive Mixed Modelling (GAMM) results indicated a significant impact of date (Supplementary Fig.  3 ) (edf = 8.9, Ref.df = 9.0, F  = 209.0, p  = <0.001), suggesting that environmental stress varied through time in the region, lowest in March 2013, January 2017 and September 2020 and peaking in May 2015 and May 2016, matching El Niño events in the region (Fig.  1 and Supplementary Fig.  3 ). The adjusted R squared value was 0.28 and deviance explained 27.6%. The proportion of sharks with low residency scores also changed throughout time, with a greater proportion of sharks decreasing residency during periods of high stress also matching these El Niño events (Fig.  3B ). Beta regression and post hoc results indicated significant differences between some atolls within year periods (Supplementary Table  3 ), with receivers at Blenheim reef experiencing significantly less environmental SE than receivers at Salomon and Peros Banhos in 2013, 2014, 2015, and 2016. Receivers at Victory Bank experienced significantly less environmental SE than receivers at Salomon in 2013, 2014, 2015, 2016 and 2018 and Peros Banhos in 2013, 2014, 2015, 2016, 2018 and 2019. Receivers at Benares Shoal experienced significantly more environmental SE than receivers at Victory Bank in 2016.

Climate change is projected to have a strong influence on marine habitats and, as such, is predicted to alter and impact the movement ecology of marine species 9 , 10 . Here, we analysed a multi-year dataset to explore the influence of environmental habitat stress, based on a composite index of nine remotely sensed environmental variables, on the residency behaviour of a site-attached shark species, found in abundance throughout the coral reefs of the Indo-Pacific. We show that increased environmental stress on coral reef habitat reduces residency in grey reef sharks, promoting more diffuse space use and extending periods away from the reef. Additionally, our results suggest that this impact has a lagged effect across the archipelago, with increased environmental stress altering residency for up to 16 months. These findings will likely have important repercussions for trophic interactions and reef ecosystem functioning 7 , 21 with potential alterations in nutrient subsidies to reefs. In addition, these results may also affect conservation and management of both grey reef sharks and coral reef ecosystems, with decreased residency potentially shifting the likelihood of interactions with both commercial and Illegal, Unregulated and Unreported (IUU) fisheries 35 . However, to date, this has yet to be examined. Interestingly, we find that these results are not ubiquitous across the whole area. Some receivers showed significant negative departures, while others showed significant positive departures, from the global mean, suggesting localised factors, such as reef resilience likely also influence residency in grey reef sharks (Fig.  2 ).

Our findings support our hypothesis that, overall, grey reef sharks reduce residency behaviour in the face of increased habitat stress. To respond, large mobile marine ectotherms must balance the behavioural trade-off between moving to escape stress, which requires increased energy expenditure and potentially increased risk, or remaining in the same area, which may become suboptimal but in doing so might conserve energy 36 . Although the energetic implications for these behaviours were not explicitly tested here, we do show an expansion of both core and broader space use, as well as increased periods of absence during times of stress. This might include moving into offshore, deeper and likely cooler waters, and as a result spending more time outside of receiver coverage. For a species well documented to maintain and regularly return to core areas of reef facilitating several important behavioural processes 8 , 27 , these results are a concern. In the short term, our results suggest an immediate ‘avoidance’ response that has implications for this species’ ecology and conservation, but in the longer term, where the benefits of departing suboptimal habitat outweigh the benefits of remaining, there are likely to be implications for the wider reef ecosystem structure (for up to 16 months post peak stress). This study does not aim to tease apart the specific mechanisms driving these short or long-term responses, which are likely different for these two processes. It does, however, offer an exciting research avenue for future studies to explore the different mechanisms influencing space use in response to environmental stress, and at different temporal scales. From a practical perspective, changes in residency may also be due to the influence of changing environmental conditions, such as wind speed, on acoustic detectability 37 , 38 in addition to coral reef health. Range testing was not feasible at this site during the period of study, so this could not be assessed. However, given the long time-series of data obtained, and the wide variation in environmental conditions throughout the study period, the impacts of varying detectability is like to be minimal.

Encouragingly, this negative association between stress and shark residency was not ubiquitous across all monitored locations. Model variance suggests that there is significant variation in residency at each receiver, with sharks more resident in some locations compared to others (Fig.  2 ). This pattern coincided with spatial and temporal variation between atolls in environmental stress exposure in this region 32 , 39 . Receivers in the north and west of Peros Banhos experienced a reduction in residency from the global average, but some receivers in the south of Peros Banhos and west of Salomon Islands experienced an increase in residency (Fig.  2B ). Interestingly, our regional pattern of residency maps with the spatial patterns of rat infestation on the islands of the northern atolls, with receivers with higher residency overlapping with rat absent and rat eradicated islands, and receivers with significantly less residency than the global average overlapping with rat present islands 40 . Although we do not explicitly explore mechanistic drivers within this study, recent research in the Chagos Archipelago has found that seabird nutrients significantly enhance fish biomass on reefs surrounding rat absent or rat eradicated islands compared to islands with rats 41 , 42 . These regional patterns clearly warrant further investigation, but could indicate grey reef shark residency is also influenced by factors that make particular reef habitats more resilient to perturbation, leading to these being more stable areas to occupy as a reef predator.

The spatial variation in residency observed could also be driven by hydrodynamic factors. Coral response to environmental stress, such as bleaching, can be highly variable, even within a reef system, and often is the result of differing fine scale environmental and biological processes 32 , 43 . There is also some congruence between areas of increased residency and areas that are sheltered from wave exposure. Shelter from wave exposure is associated with increased coral cover and quicker recovery from bleaching events 44 , another potentially important factor influencing shark behaviour. The mechanisms driving these results are clearly complex and involve a mixture of variability in shark behaviour as well as heterogeneity in coral reef response to environmental stress, and at different temporal scales.

Results from cross correlations indicate that reduced residency of grey reef sharks on coral reefs in the archipelago persists well into the future, as much as up to 16 months. Time lags in how coral reefs themselves respond to stress can be relatively short, within a few weeks 45 , 46 , or prolonged, over periods of months or even years 47 , 48 . The time lag in response to stress in other reef-reliant species can also vary from months to several years 49 . For example, Halford and Caley 50 found a time lag of 12–18 months between bleaching and change in structure of fish communities on remote reefs of north-west Australia. Declines in the abundance and diversity of coral reef fishes may be apparent more than 3 years after coral depletion in some regions, due to the delay in structural collapse of dead corals 51 . The true mechanisms underlying both the instantaneous reduction in residency and its persistence for months following increased environmental stress seen here are unknown and provide an interesting next step for this research, such as exploration of possible correlation between areas of greater stress and the persistence of reduced residency in reef sharks.

This study did not examine the precise environmental factors driving reductions in residency. Stress on coral reefs is often closely linked to SST, and other temperature metrics, such as DHW and SST variability 32 , 52 , and metrics of SST contributed considerably to the environmental SE index 32 . As such, the reduced residency found in this study could be driven by increases or changes in metrics of SST. Reef sharks are ectotherms and have been seen to exhibit behavioural thermoregulation to regulate their body temperatures and avoid physiological damage from adverse SSTs 15 . Therefore, an influence of different metrics of SST on movement is to be expected. Indeed, links with SST, SST anomalies, and SST variability and movement, residency, and presence/absence of other shark species have been seen elsewhere 53 , 54 . For example Ryan et al. 54 found that low SST anomalies increased white shark ( Carcharodon carcharias ) presence and residency, which increased the chances of attacks on the eastern Australian coast. However, little is known about these relationships in reef sharks 6 , and the few studies that have investigated these relationships have typically found that changing environmental conditions have limited impact. For example, Schlaff et al. 55 found that size and sex were the most important drivers of activity space in Australian blacktip reef sharks Carcharhinus melanopterus , with salinity and water temperature having significant but relatively low impacts, while Heupel and Simpfendorfer 56 found no relationship between activity space and environmental variables in grey reef sharks on the Great Barrier Reef. As such, these results, to our knowledge, provide the some of the first evidence of changing environmental variables impacting the movement and residency of grey reef sharks.

Season was also found to have a significant effect on residency in grey reef sharks, which supports previous research at this site that showed that grey reef sharks spent more time away from reefs during the wet season compared to the dry season 28 . These changes in residency with season could be due to environmental or ecological factors. Shark species have been seen to increase movement and decrease residency during storm events 57 , 58 , which may be increased during the wet season. Alternatively, residency changes may be due to changes in food resources, with historical fisheries known to peak in the wet season in this region 59 , 60 . In addition, our results confirm that year is a variable that should be regularly included as a predictor variable to account for temporal variation when modelling movement ecology of marine species 61 , 62 , which here is most likely linked particularly to the severity of environmental change associated with El Niño events.

As climate change continues to alter oceanic conditions, environmental stress across marine ecosystems, including coral reef habitats, is predicted to increase 63 , 64 . Although reef sharks use coral reef systems as primary habitat, they can spend significant periods of time away from reefs for foraging 28 , 65 , bringing substantial nutrients from deeper pelagic waters that could not be produced by the reefs themselves 21 . Consequently, reduced residency by reef sharks could lead to a reduction of subsidies between pelagic and reef ecosystems, with these cross-ecosystem flows of energy potentially influencing reef resilience during times of high environmental stress. In addition, reduced residency may have trophic implications on particular reefs, with species assemblage reorganisation possible due to loss of large mesopredators 66 , 67 .

As well as ecological impacts to coral reef systems, these results also have implications for the ecology and conservation of reef sharks. Reduced residency may result in increased energetic costs, with subsequent impacts on survival, growth and reproduction 68 , 69 , 70 . In the Chagos Archipelago, and other coral reef systems, grey reef sharks are under threat from Illegal, Unregulated and Unreported (IUU) fishing activity 35 , 71 , 72 , which is believed to be suppressing populations around Peros Banhos and Salomon Islands 73 . Reef shark species that are less resident on coral reef systems are more threatened with extinction risk 12 . Sharks that shift to spending more time in offshore waters may increase their vulnerability to IUU fishing, especially in a large, remote area such as the Chagos Archipelago, as increased movements in some species may increase the encounter rate with IUU vessels 35 , or commercial fisheries, as they spend less time in MPAs. Alternatively, as fishers target where shark are known to aggregate 71 , reduced residency may mean fewer aggregations and reduced impact of fishing on this species as they are less likely to find large numbers of them in one location.

The environmental SE index used in this study was chosen as it includes both reducers and enhancers of stress, therefore providing a balanced metric that helps decipher differences between reefs as well as providing a holistic view of multiple stressors on reef systems, not only those that drive bleaching 32 . Consequently, the results seen here may relate to reef shark response to environmental stress on coral systems, rather than to direct habitat damage. There are now remotely sensed products of coral bleaching available, such as the Allen Coral Atlas ( www.allencoralatlas.org ) but these were not used in this study because the data was only available for 2019 onwards. In addition, it should be noted that the environmental SE index does not contain an exhaustive list of environmental stressors. Environmental variables such as turbidity, chlorophyll- a , pH and ultra-violet light, all known to impact coral habitat quality, are not included in this index, due to a lack of appropriate products or due to low accuracy in shallow areas, such as coral reefs 32 , 74 . Furthermore, some of the variables in the environmental SE index influence habitat quality but can also have direct impacts on reef shark movement behaviour, so it is difficult to disentangle direct and indirect effects using this approach. Future work could address these issues by including additional environmental variables, currently unavailable, into the index, and when satellite-based maps of bleaching become available with sufficient temporal coverage these could be included disentangle these effects.

With climate change predicted to cause bleaching events annually by 2043 75 , changing environmental stress and disturbance on coral reefs has the potential to impact the movement and ecology of reef shark species. Here, we used 714,810 detections from acoustic tagging data for 122 grey reef sharks between 2013 and 2020, combined with satellite remote sensing data to investigate how changing environmental stress on coral reefs can impact the residency of an abundant reef shark species in the Chagos Archipelago. Environmental stress, season and year were all significant predictors of grey reef shark residency. As such, we show that increased environmental stress on coral reef ecosystems reduces grey reef shark residency, expands their space use and extends periods of absence from the reef, patterns that persist more than a year beyond the main period of stress. In addition, there is also some cause for optimism with our finding that residency varies significantly at different reef locations with some areas showing increased residency. As environmental stress on coral reef systems is predicted to increase 76 , 77 , 78 , these changes have important consequences for the ecology and ecosystem functioning of coral reefs in the region, such as altering nutrient subsidies. Furthermore, decreased residency is likely to have conservation impacts on the sharks themselves, potentially altering their interactions with IUU and commercial fishing vessels. Finally, results from the study will enhance predictions about predator responses to climate-related stress into the future.

Materials and methods

Data collection and study site.

The Chagos Archipelago is a large, remote archipelago, at the centre of the British Indian Ocean Territory Marine Protected Area (BIOT MPA) in the Central Indian Ocean. Established in 2010, the reefs are home to multiple resident and transient elasmobranch species 79 , 80 . Following El Niño events in 2015 and 2016, the coral reefs of the Chagos Archipelago experienced widespread bleaching events in response to substantial increases in environmental stress 39 , 79 . A long-term tagging programme of grey reef sharks has been undertaken in the region since 2013 to investigate the efficacy of the MPA for protecting large mobile fishes and for understanding how ecology can inform MPA enforcement 23 , 35 .

Acoustic telemetry data were collected from five atolls (Benares, Blenheim, Peros Banhos, Salomon and Victory Bank) in the Chagos Archipelago between 2013 and 2021 from an acoustic array of 54 receivers 28 (Supplementary Fig.  4 ). All receivers were far enough apart to avoid overlap in their detection range, with mean distance to the next closest receiver being 2.15 km and ranging from 0.55–4.57 km 28 . Although range testing was not undertaken for this array, due to financial and logistical constraints of vessel time in the Chagos Archipelago, other studies conducted around coral atolls in the Indian Ocean using the same or similar equipment have found detection ranges between 300 and 500 m 81 , 82 .

This study utilised tracking data from grey reef sharks carrying 10-year, V16, 69 kHz Innovasea coded acoustic transmitters between 1st March 2013 and the 30th November 2020. In total 122 grey reef (81 female, 41 male) were tagged with sharks being caught from handlines and barbless hooks. Larger animals (>1.5 m) were kept in the water, but all others were brought onto the boat and restrained. A seawater house was used to irrigate the gills, and a wet cloth placed over the eyes. Once restrained, sharks were measured and acoustic tags implanted intraperitoneally through a small incision ( ∼ 2–3 cm) just off the midline of their abdomen 23 . Total handling time was generally less than 5 min per animal. All procedures were approved by the Stanford University Administrative Panel on Laboratory Animal Care (APLAC) under permit APLAC-10765. Tags were configured to transmit an acoustic ‘ping’ containing a unique ID code with a nominal delay of 30–90 s, or 60–180 s for the duration of their battery life (~10 years), providing a long-term time-series of detection data. Differences in transmission delay between tag types were accounted for using the method by Jacoby et al. 35 to ensure that detections between the two delay types were standardised and comparable. Receivers were downloaded and serviced annually at the same time each year (March–May) with the exception of 2017, where for logistical reasons no service expedition took place.

Data preparation

To avoid false detections from unknown tagged animals in our study system, only detections from animals with known ID codes were used for the analyses. To remove the possibility of false positives in the data set three different methods were used. First, animals with a single detection were filtered from the dataset 83 , 84 . Secondly, detection gaps of less than 30 s, under the ping delay of the tags, were also removed from the data by removing the second detection. Finally, transitions (movements between two different receivers) were calculated as per Williamson et al. 28 and removed if the speed of the transition exceeded 10 times the minimum sustainable swimming speeds of 0.69 m/s for grey reef sharks, resulting in a cut-off speed of 6.9 ms −1 28 ,  85 . To reduce any impact of the stress of capture on detected behaviour 86 ,  87 , the first 24 h of data were removed for each individual 88 .

Statistics and reproducibility

There are several equations that can be used for calculating residency from acoustic telemetry 83 . In this study, a local fixed time residency index for each shark was calculated per month at each receiver by counting the number days the shark was present per receiver in that month (minimum 2 days) divided by how many days the receiver was active during that month 83 . This allows for comparisons of residency through both time and space 83 .

To explore environmental stress on the reef habitat of grey reef sharks we used the Reef Environmental Stress Exposure Toolbox (RESET) developed by Williamson et al. 32 ( https://mjw1280.users.earthengine.app/view/reef-environmental-stress-exposure-toolbox ). This study used nine environmental variables (cloud cover, current, depth, salinity, wind, and four SST based metrics), derived from satellite remote sensing and Google Earth engine (GEE), known to have an impact on stress and health of coral reef systems. As the spatial resolution of the nine variables varied (Supplementary Table  4 ), each product was resampled using bilinear interpolation to match the detection range of the receivers (500 m) 89 . These data were combined with ecological and health-based thresholds obtained from the available literature, and fuzzy logic (discontinuous functions), to develop a combined environmental SE index from satellite remote sensing data for monitoring environmental SE on coral reef systems 32 . This index was chosen, as although there are remote sensing datasets available for reef habitat and bleaching (such as the Allen Coral Atlas, https://allencoralatlas.org ), these data were only available for 2019 onwards for the Chagos Archipelago. In addition, the coral reef environmental SE index incorporates several environmental variables that both enhance and reduce stress on the reef. Consequently, the index evaluates environmental stress as a whole, rather than specifically focusing on bleaching, which is one aspect of habitat stress, and can vary spatially and temporally within reef systems 48 , 90 . This index cannot be used to directly quantify the health of coral reefs per se. Rather, it is a temporally explicit monitoring tool (i.e., to compare against various time periods from the same region) to evaluate relative changes in stress exposure on coral reef ecosystems. The environmental SE index is scored between 0–1 with 0 being low environmental SE and 1 being high environmental SE. These index values were then included as an explanatory variable for subsequent analyses. From previous research at this site, RESET scores of 0.3 or higher indicate considerable stress to the reefs in Chagos 32 .

To examine how the environmental SE index changed temporally over the study period, the environmental SE index at each receiver was included as a response variable in a GAMM, with numerical day from 01/01/2014 as an explanatory variable and ‘atoll’ as a random effect, using the ‘gam’ function in the mgcv package 91 . To assess how the environmental stress changed spatially, beta regression with environmental SE index as a response variable was used 92 , 93 , with atoll as a predictor variable, using the ‘betareg’ function in the betareg package 94 . As environmental stress can change between years, year was included as an interaction in the model. Post hoc tests were undertaken between interactions using the ‘emmeans’ function in the emmeans package 95 .

As all receivers were situated greater than 500 m apart 28 , more than the spatial resolution of the index, detections from all receivers were included in the analysis and were not grouped. To limit exploratory analyses, and prevent model overfitting, an a priori selection of additional explanatory variables and interactions based on previous research and theory were included 96 , 97 . Along with the combined environmental SE index, four additional explanatory variables were included in the model. Season was included over month as season is often a more biologically relevant driver of variability in ocean systems 98 . The Chagos Archipelago has two clear seasons (wet—October to March, dry—April to September) which influences ecological processes, such as historical fisheries 59 , 60 . During our study period, El Niño conditions varied, and with different levels of intensity, but driving bleaching events in the region in both 2015 and 2016 39 , 99 . As such, year was also included as an explanatory variable, as a factor, for the global model. As both sex and size have been shown to influence movement patterns in grey reef sharks ‘sex’ and ‘total length’ were also included as explanatory variables. Continuous variables (SE index and total length) were scaled (mean = 0, SD = 1) to aid in model fitting 97 , using the ‘scale’ function from the base package 100 . To prevent pseudoreplication, individual ID and receiver ID were included as independent random factors in the model.

All analyses were conducted in R version 4.2.2 100 . A Generalised Linear Model (GLM) was built to assess the explanatory variables for collinearity. Collinearity was assessed by producing a variance inflation factor (VIF) from the generalised linear model using the ‘check_collinearity’ function in the performance package in R 101 . No evidence of collinearity was found, with all variables having a VIF ≤ 1.05, less than the critical threshold of 5.0 102 , 103 . As such, all a priori selected explanatory variables were included in the global model.

To investigate the drivers of residency, a global model, with all explanatory variables (environmental SE index, season, year, sex, and total length) and individual ID and station as random effects, was created using a Generalised Linear Mixed Model (GLMM) (family = binomial, link = logit) with the ‘glmmTMB’ function from the glmmTMB package. To fit the GLMM with proportion as the response variable, residency index was coded in the model as a fraction (days detected/days per month) and days per month used as the ‘weights’ argument in the model to set the basis of the response proportion 104 . Residuals of the global model were checked for heteroscedasticity, autocorrelation and data were checked for binomial distribution using the functions ‘resid’, ‘fitted’, and ‘acf’ from the stats package 100 .

A model set was subsequently generated from the global model using the ‘dredge’ function, from the MuMIn package 105 , with random effects as fixed terms. Models in the set were ranked by small sample size Akaike Information Criterion (AICc) values 106 , and Akaike weights for each model in the confidence set were calculated 96 , 97 , 107 . To improve inference using AICc the ‘nested’ function from the MuMIn package was used on the model selection table to remove models which were more complex versions of others 96 , 97 . Selected models included those with ΔAICc values < 2 and that were not nested models 107 . If a single parsimonious model remained following selection, this model was fitted to the data. If no single parsimonious model subsequently resulted from the set and the weight of the best model was less than 0.9, model averaging was used 96 , and the relative importance of each predictor variable calculated by summing Akaike weights for all confidence set models containing them. Model averaging was then undertaken on all predictor variables included in the final confidence set 96 , 97 , with parameter estimates indicating the change in probability of residency as the value for continuous predictor variables increased. Categorical predictor variables were compared to the categorical variable level used as the model baseline. Positive estimates indicated an increase in residency in grey reef sharks, negative estimates a decrease in residency. It is important to note that predictors may display a high relative importance but show no significant result in the model averaged estimates, and the relative importance and model averaged estimates should be considered in combination 108 . To test whether the relationship between stress and residency were not exclusively driven by extreme stress events, a secondary analysis removing data from El Niño periods (01/07/2014–30/06/2016 and 01/07/2018–30/06/2019) was undertaken.

The effects of the fixed effects on the model, and the combination of fixed and random effects 109 , 110 , were tested by calculating the marginal R 2 (R 2 m) and conditional R 2 (R 2 c) values using ‘r.squaredGLMM’ in the MuMIn package 105 , 110 , and conditional models of the random effects, and their SDs, extracted from the top model using the ‘ranef ’ function from the lme4 package 111 .

To if there were any lagged responses in residency behaviour as a result of occupying reefs that have undergone long-term stress (in particular during El Niño events) cross correlations were calculated from the mean monthly environmental SE index and mean monthly residency using the ‘ccf’ function from the stats package 100 . These were used to identify time lags in months ( t ) between our predictor (stress) in the present ( t  = 0) and our response (residency) into the future ( t  > 0) based on autocorrelation between the two as we move into the future.

To evaluate if grey reef sharks alter their residency through changes in space and/or time during the study, Kernel Utilisation Density (KUD) estimates as well as the time intervals between consecutive detections were calculated. KUDs at 50, 75 and 95% were generated using the ‘kernelUD’ function from the adehabitatHR package 112 and plotted through time. The median number of days per month between detections across the array were calculated per individual. Median detection differences (i.e., detection gaps) were compared between El- Niño (elevated stress) and non-El Niño periods using the nonparametric Brunner-Munzel test 113 . Finally, residency indices were averaged across individuals for all 6 monthly periods, binned and bubble plots produced to show variation in residency across the population in response to changing stress through time.

Data availability

Raw data supporting the results are available from the Zenodo Digital Repository: https://zenodo.org/records/11653900 114 .

Code availability

The R code used for analyses are available from the Zenodo Digital Repository: https://zenodo.org/records/11639740 115 .

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Acknowledgements

Funding for this project was provided by the Bertarelli Foundation and contributed to the Bertarelli Programme in Marine Science. This work was also supported by the Natural Environment Research Council (Grant No. NE/L002485/1) to M.J.W., as part of the London NERC Doctoral Training Partnership at the Department of Geography, King’s College London and the Institute of Zoology, London. D.J.C. was funded by Research England. All procedures were approved by the Stanford University Administrative Panel on Laboratory Animal Care (APLAC) under permit APLAC-10765. We thank the BIOT Administration for granting us permission to undertake the research. We would like thank S. Vanovac and C. Monk for their help for producing visualisations for this manuscript.

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Institute of Zoology, Zoological Society of London, London, UK

Michael J. Williamson, David J. Curnick & David M. P. Jacoby

Department of Geography, King’s College London, London, UK

Michael J. Williamson & Emma J. Tebbs

Department of Genetics, Evolution and Environment, University College London, London, UK

Michael J. Williamson

Department of Fish and Wildlife Conservation, Virginia Tech, Blacksburg, VA, USA

Francesco Ferretti

School of Marine Science and Policy, University of Delaware, Lewes, DE, USA

Aaron B. Carlisle

Hatfield Marine Science Center, Oregon State University, Newport, OR, USA

Taylor K. Chapple

Hopkins Marine Station, Stanford University, Pacific Grove, CA, USA

Robert J. Schallert & Barbara A. Block

Marine Futures Lab, School of Biological Sciences, University of Western Australia, Perth, WA, Australia

David M. Tickler

Lancaster Environment Centre, Lancaster University, Lancaster, UK

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Michael J. Williamson: conceptualisation (equal); formal analysis (lead); methodology (equal); visualisation (equal); writing—original draft (lead); writing—review & editing (lead). Emma J. Tebbs: supervision (equal); writing—review & editing (supporting). David J. Curnick: funding acquisition (equal); investigation (equal); supervision (supporting); writing—review & editing (supporting). Francesco Ferretti: investigation (equal); writing—review & editing (supporting). Aaron B. Carlisle: investigation (equal); writing—review & editing (supporting). Taylor K. Chapple: investigation (equal); writing—review & editing (supporting). Robert J. Schallert: investigation (equal). David M. Tickler: investigation (equal). Barbara A. Block: funding acquisition (equal); writing—review & editing (supporting). David M. P. Jacoby: conceptualisation (equal); funding acquisition (equal); investigation (equal); methodology (equal); supervision (equal); visualisation (equal); writing—review & editing (supporting).

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Correspondence to Michael J. Williamson or David M. P. Jacoby .

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Williamson, M.J., Tebbs, E.J., Curnick, D.J. et al. Environmental stress reduces shark residency to coral reefs. Commun Biol 7 , 1018 (2024). https://doi.org/10.1038/s42003-024-06707-3

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Received : 12 December 2023

Accepted : 08 August 2024

Published : 09 September 2024

DOI : https://doi.org/10.1038/s42003-024-06707-3

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