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Correction: Using fuzzy logic to compare species distribution models developed on the basis of expert knowledge and sampling records

The original article was published in Frontiers in Zoology 2023 20 :38

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

Many questions in biology benefit greatly from the use of a variety of model systems. High-throughput sequencing methods have been a triumph in the democratization of diverse model systems. They allow for the ...

Paternal care plasticity: males care more for early- than late-developing embryos in an arboreal breeding treefrog

Parental care benefits offspring but comes with costs. To optimize the trade-off of costs and benefits, parents should adjust care based on intrinsic and/or extrinsic conditions. The harm to offspring hypothes...

Segregation of endosymbionts in complex symbiotic system of cicadas providing novel insights into microbial symbioses and evolutionary dynamics of symbiotic organs in sap-feeding insects

The most extraordinary systems of symbiosis in insects are found in the suborder Auchenorrhyncha of Hemiptera, which provide unique perspectives for uncovering complicated insect-microbe symbiosis. We investig...

Metabolism gene expression in worker honey bees after exposure to 50Hz electric field - semi-field analysis

The investigation of the effects of artificial 50 Hz electric field (E-field) frequency on Apis mellifera is a relatively new field of research. Since the current literature focuses mainly on short-term effects, ...

Postembryonic development and lifestyle shift in the commensal ribbon worm

Various morphological adaptations are associated with symbiotic relationships between organisms. One such adaptation is seen in the nemertean genus Malacobdella . All species in the genus are commensals of mollusc...

Sex differences in foraging ecology of a zooplanktivorous little auk Alle alle during the pre-laying period: insights from remote sensing and animal-tracking

Energy and time allocation in seabirds differ between consecutive stages of breeding given various requirements of particular phases of the reproductive period. Theses allocations may also be sex-specific cons...

What frog gill resorption brings: loss of function, cell death, and metabolic reorganization

Anuran metamorphosis, which is driven by thyroid hormone (TH)-mediated processes, orchestrates intricate morphological and functional transformations for the transition from aquatic tadpoles to terrestrial lif...

Fine-grained image classification on bats using VGG16-CBAM: a practical example with 7 horseshoe bats taxa (CHIROPTERA: Rhinolophidae: Rhinolophus ) from Southern China

Rapid identification and classification of bats are critical for practical applications. However, species identification of bats is a typically detrimental and time-consuming manual task that depends on taxono...

Molecular analysis of scats revealed diet and prey choice of grey wolves and Eurasian lynx in the contact zone between the Dinaric Mountains and the Alps

A comprehensive understanding of the dietary habits of carnivores is essential to get ecological insights into their role in the ecosystem, potential competition with other carnivorous species, and their effec...

Updated single cell reference atlas for the starlet anemone Nematostella vectensis

The recent combination of genomics and single cell transcriptomics has allowed to assess a variety of non-conventional model organisms in much more depth. Single cell transcriptomes can uncover hidden cellular...

Obituary: Claus Nielsen 1938–2024

Correction: support for a radiation of free-living flatworms in the african great lakes region and the description of five new  macrostomum  species.

The original article was published in Frontiers in Zoology 2023 20 :31

Rediscovering the unusual, solitary bryozoan Monobryozoon ambulans Remane, 1936: first molecular and new morphological data clarify its phylogenetic position

One of the most peculiar groups of the mostly colonial phylum Bryozoa is the taxon Monobryozoon , whose name already implies non-colonial members of the phylum. Its peculiarity and highly unusual lifestyle as a me...

Fat accumulation in striped hamsters ( Cricetulus barabensis ) reflects the temperature of prior cold acclimation

Proper adjustments of metabolic thermogenesis play an important role in thermoregulation in endotherm to cope with cold and/or warm ambient temperatures, however its roles in energy balance and fat accumulatio...

Differences in spatial niche of terrestrial mammals when facing extreme snowfall: the case in east Asian forests

Recent climate changes have produced extreme climate events. This study focused on extreme snowfall and intended to discuss the vulnerability of temperate mammals against it through interspecies comparisons of...

New insights into mesoderm and endoderm development, and the nature of the onychophoran blastopore

Early during onychophoran development and prior to the formation of the germ band, a posterior tissue thickening forms the posterior pit. Anterior to this thickening forms a groove, the embryonic slit, that...

Wide-spread dispersal in a deep-sea brooding polychaete: the role of natural history collections in assessing the distribution in quill worms (Onuphidae, Annelida)

Modern integrative taxonomy-based annelid species descriptions are detailed combining morphological data and, since the last decades, also molecular information. Historic species descriptions are often compara...

MicroRNA ame-let-7 targets Amdop2 to increase sucrose sensitivity in honey bees ( Apis mellifera )

As an important catecholamine neurotransmitter in invertebrates and vertebrates, dopamine plays multiple roles in the life of the honey bee. Dopamine receptors (DA), which specifically bind to dopamine to acti...

The oral sensory organs in Bathochordaeus stygius (Tunicata Appendicularia) are unique in structure and homologous to the coronal organ

Appendicularia consists of approximately 70 purely marine species that belong to Tunicata the probable sister taxon to Craniota. Therefore, Appendicularia plays a pivotal role for our understanding of chordate...

Frequency jumps and subharmonic components in calls of female Odorrana tormota differentially affect the vocal behaviors of male frogs

Studies have demonstrated that the sounds of animals from many taxa with nonlinear phenomena (NLP)—caused by nonlinear characteristics of vocal organ dynamics that lead to nonlinear vocal phenomena—can influen...

Using fuzzy logic to compare species distribution models developed on the basis of expert knowledge and sampling records

Experts use knowledge to infer the distribution of species based on fuzzy logical assumptions about the relationship between species and the environment. Thus, expert knowledge is amenable to fuzzy logic model...

The Correction to this article has been published in Frontiers in Zoology 2024 21 :18

Holding in the stream: convergent evolution of suckermouth structures in Loricariidae (Siluriformes)

Suckermouth armoured catfish (Loricariidae) are a highly speciose and diverse freshwater fish family, which bear upper and lower lips forming an oral disc. Its hierarchical organisation allows the attachment t...

Despite genetic isolation in sympatry, post-copulatory reproductive barriers have not evolved between bat- and human-associated common bedbugs ( Cimex lectularius L.)

The common bedbug Cimex lectularius is a widespread ectoparasite on humans and bats. Two genetically isolated lineages, parasitizing either human (HL) or bat (BL) hosts, have been suggested to differentiate becau...

Comparative metabolomics analysis reveals high-altitude adaptations in a toad-headed viviparous lizard, Phrynocephalus vlangalii

Extreme environmental conditions at high altitude, such as hypobaric hypoxia, low temperature, and strong UV radiation, pose a great challenge to the survival of animals. Although the mechanisms of adaptation ...

Effects of reduced kinematic and social play experience on affective appraisal of human-rat play in rats

Play is a common and developmentally important behaviour in young mammals. Specifically in Norway rats ( Rattus norvegicus ), reduced opportunity to engage in rough-and-tumble (RT) play has been associated with imp...

Age, brood fate, and territory quality affect nest-site fidelity in white stork Ciconia ciconia

A particular type of site fidelity is faithfulness to the nest site, where birds are not only reoccupying breeding territories but also reusing nests built in previous breeding seasons. Staying faithful to the...

Evolutionary trade-off between innate and acquired immune defences in birds

The development, maintenance, and use of immune defences are costly. Therefore, animals face trade-offs in terms of resource allocation within their immune system and between their immune system and other phys...

Support for a radiation of free-living flatworms in the African Great Lakes region and the description of five new Macrostomum species

The African Great Lakes have long been recognized as an excellent location to study speciation. Most famously, cichlid fishes have radiated in Lake Tanganyika and subsequently spread into Lake Malawi and Lake ...

The Correction to this article has been published in Frontiers in Zoology 2024 21 :6

Food patch use of Japanese quail ( Coturnix japonica ) varies with personality traits

The classic optimal foraging theory (OFT) predicts animals’ food patch use assuming that individuals in a population use the same strategy while foraging. However, due to the existence of animal personality, i...

Minimal resin embedding of SBF-SEM samples reduces charging and facilitates finding a surface-linked region of interest

For decoding the mechanism of how cells and organs function information on their ultrastructure is essential. High-resolution 3D imaging has revolutionized morphology. Serial block face scanning electron micro...

Third-party intervention and post-conflict behaviour in agonistic encounters of pigs ( Sus scrofa )

Third-party interference in agonistic contests entails a deliberate intervention in an ongoing fight by a bystanding individual (third party) and may be followed by post-conflict social behaviour to provide su...

Body mass is associated with hibernation length, body temperature, and heart rate in free-ranging brown bears

Despite centuries of research, debate remains on the scaling of metabolic rate to mass especially for intraspecific cases. The high variation of body mass within brown bears presents a unique opportunity to st...

Terebra steering in chalcidoid wasps

Various chalcidoid wasps can actively steer their terebra (= ovipositor shaft) in diverse directions, despite the lack of terebral intrinsic musculature. To investigate the mechanisms of these bending and rota...

Age-related mating rates among ecologically distinct lineages of bedbugs, Cimex lectularius

Understanding how many mates an animal has in its lifetime is a critical factor in sexual selection. At the same time, differences in an organism's ecology, such as the quantity and quality of food, could be r...

Effects of meteorological conditions on brood care in cooperatively breeding carrion crow and consequences on reproductive success

Meteorological stressors (e.g., temperature and rain shortage) constrain brood provisioning in some bird species, but the consequences on reproductive success have been rarely quantified. Here we show, in a co...

Variations in small-scale movements of, Rousettus aegyptiacus, a Marburg virus reservoir across a seasonal gradient

Bats are increasingly being recognized as important hosts for viruses, some of which are zoonotic and carry the potential for spillover within human and livestock populations. Biosurveillance studies focused o...

First 3-D reconstruction of copulation in Lepidoptera: interaction of genitalia in Tortrix viridana (Tortricidae)

The process of copulation in Lepidoptera is understudied and poorly understood from a functional perspective. The purpose of the present paper is to study the interaction of the male and female genitalia of Tortr...

Proteins from toad’s parotoid macroglands: do they play a role in gland functioning and chemical defence?

Parotoid gland secretion of bufonid toads is a rich source of toxic molecules that are used against predators, parasites and pathogens. Bufadienolides and biogenic amines are the principal compounds responsibl...

Interactions between carnivore species: limited spatiotemporal partitioning between apex predator and smaller carnivores in a Mediterranean protected area

There is need of information on ecological interactions that keystone species such as apex predators establish in ecosystems recently recolonised. Interactions among carnivore species have the potential to inf...

Food availability positively affects the survival and somatic maintenance of hibernating garden dormice ( Eliomys quercinus )

Torpor is an energy saving strategy achieved by substantial reductions of metabolic rate and body temperature that enables animals to survive periods of low resource availability. During hibernation (multiday ...

Southern Europe is becoming climatically favourable for African birds: anticipating the establishment of a new species

The current modification of species distribution ranges, as a response to a warmer climate, constitutes an interesting line of work and a recent challenge for biogeography. This study aimed to determine if the...

Hide or die when the winds bring wings: predator avoidance by activity shift in a mountain snake

Understanding predator–prey relationships is fundamental in many areas of ecology and conservation. In reptiles, basking time often increases the risk of predation and one way to minimise this risk is to reduc...

On latches in biological systems: a comparative morphological and functional study of the retinaculum and the dens lock in Collembola

Springtails have the ability to jump using morphological structures consisting of a catapult, the furca, and a latching system constructed with interaction of the retinaculum and the dens lock. The retinaculum...

A methodological exploration to study 2D arm kinematics in Ophiuroidea (Echinodermata)

Brittle stars, unlike most other echinoderms, do not use their small tube feet for locomotion but instead use their flexible arms to produce a rowing or reverse rowing movement. They are among the fastest-movi...

Appearance of a transparent protrusion containing two pairs of legs on the apodous ring preceding the anamorphic molt in a millipede, Niponia nodulosa

Arthropods gradually change their forms through repeated molting events during postembryonic development. Anamorphosis, i.e., segment addition during postembryonic development, is seen in some arthropod lineag...

The effect of temperature and invasive alien predator on genetic and phenotypic variation in the damselfly Ischnura elegans : cross-latitude comparison

Understanding and predicting how organisms respond to human-caused environmental changes has become a major concern in conservation biology. Here, we linked gene expression and phenotypic data to identify cand...

Offspring thermal demands and parental brooding efficiency differ for precocial birds living in contrasting climates

Chicks of precocial birds hatch well-developed and can search actively for food but their homeothermy develops gradually during growth. This makes them dependent on heat provided by parents (“brooding”), which...

Correction: A protective nesting association with native species counteracts biotic resistance for the spread of an invasive parakeet from urban into rural habitats

The original article was published in Frontiers in Zoology 2020 17 :13

Scorpionfish rapidly change colour in response to their background

To facilitate background matching in heterogenous environments, some animals rapidly change body colouration. Marine predatory fishes might use this ability to hide from predators and prey. Here, we focus on s...

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Null models confirm nest site fidelity by male smallmouth bass, Micropterus dolomieu

Many animals appear to preferentially renest in proximity to a site they previously occupied. Evidence of nest fidelity is often inferred from a right skewed distribution of distances between the nests of indi...

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Integrating phylogenetic, phylogeographic, and morphometric analyses to reveal cryptic lineages within the genus Asaccus (Reptilia: Squamata: Phyllodactylidae) in Iran

The Middle Eastern endemic genus Asaccus comprises Southwest Asian leaf-toed geckos. To date, this genus includes 19 species of leaf-toed geckos (seven in Arabia and 12 in the Zagros Mountains). Despite a recent ...

Biomorphometric and hematobiochemical alterations in the juvenile african catfish Clarias gariepinus exposed to propranolol

Propranolol (PRO) is a beta-blocker drug used for the treatment of anxiety, chest pain, migraine and tremors. The present study investigated whether sublethal concentrations of PRO have effects on the body con...

Lions & sea lions & bears, oh my: utilizing museum specimens to study the ossification sequence of carnivoran taxa

Mammalian skeletons are largely formed before birth. Heterochronic changes in skeletal formation can be investigated by comparing the order of ossification for different elements of the skeleton. Due to the ch...

Daubenton’s bats maintain stereotypical echolocation behaviour and a lombard response during target interception in light

Most bats hunt insects on the wing at night using echolocation as their primary sensory modality, but nevertheless maintain complex eye anatomy and functional vision. This raises the question of how and when i...

Influence of temperature on embryonic development of Pontastacus leptodactylus freshwater crayfish, and characterization of growth and osmoregulation related genes

Narrow clawed crayfish, Pontastacus (Astacus) leptodactylus , represents an ecologically and economically valuable freshwater species. Despite the high importance of artificial breeding for conservation purpose an...

Birds and environment: a multidisciplinary approach to ecological, behavioural and conservation issues

Birds perform significant ecosystem services in the environment. Nevertheless, they have been facing threats to their survival globally. This special collection assembles diverse articles on various aspects of...

Taxonomic reassessment of Rhodnius zeledoni Jurberg, Rocha & Galvão: a morphological and morphometric analysis comparing its taxonomic relationship with Rhodnius domesticus Neiva & Pinto

Rhodnius zeledoni was described from a single specimen. Since its description, doubts have arisen regarding the taxonomic status of this species in relation to Rhodnius domesticus .

Feeding selectivity and a functional trade-off in a benthic fish with a continuous morphological variation: an experimental test

Functional trade-offs through ecological specializations are hypothesized to become causes of adaptive phenotypic divergence under divergent natural selection, where intermediate phenotypes may have the lowest...

Giant pandas in captivity undergo short-term adaptation in nerve-related pathways

Behaviors in captive animals, including changes in appetite, activity level, and social interaction, are often seen as adaptive responses. However, these behaviors may become progressively maladaptive, leading...

Echoes through time: amazing inferences from a fossil bat

Sister to the Chiroptera crown-clade, the 50 million year old Vielasia sigei is suggested to have used laryngeal echolocation based on morphometric analyses. We discuss how Vielasia ’s discovery influences our und...

Forest fragmentation causes an isolated population of the golden takin ( Budorcas taxicolor bedfordi Thomas, 1911) (Artiodactyla: Bovidae) in the Qinling Mountains (China)

Budorcas taxicolor bedfordi is a rare animal uniquely distributed in the Qinling Mountains (China). Human disturbance and habitat fragmentation have directly affected the survival of B. t. bedfordi . It is urgent ...

High disparity in repellent gland anatomy across major lineages of stick and leaf insects (Insecta: Phasmatodea)

Phasmatodea are well known for their ability to disguise themselves by mimicking twigs, leaves, or bark, and are therefore commonly referred to as stick and leaf insects. In addition to this and other defensiv...

Morphological and functional trait divergence in endemic fish populations along the small-scale karstic stream

Organisms with broad distribution ranges, such as fish, often exhibit local ecological specializations based on their utilization of food and habitat. Populations of species that live in different habitat type...

Exploring the morphological dynamics of Nile tilapia ( Oreochromis niloticus Linn. 1758) in Victoria Nile as depicted from geometric morphometrics

Various anthropogenic activities continue to threaten the fish biodiversity of the East African water bodies such as the Victoria Nile. Although the Victoria Nile is a significant source of livelihood for huma...

Diet of Black-backed Jackal ( Canis mesomelas , Schreber, 1775), impacts on livelihood and perceptions of farmers in Konasa Pulasa community conserved forest, omo valley of Ethiopia

Livestock depredation by the black-backed jackal ( Canis mesomelas ) occurs widely across Africa. The study on human-jackal conflict is important for conservation efforts in Ethiopia. The aim of this study was to i...

Rewilding: a requirement for a sustainable future

Nowadays rewilding has received an increasing focus as a sustainable conservation tool for restoring damaged or disturbed habitats. Many types of rewilding initiatives have been implemented all over the globe ...

Acute toxicity of ammonia and nitrite to Siamese fighting fish ( Betta splendens )

The acute toxicity and sublethal effects of ammonia and nitrite on the air-beathing Siamese fighting fish, betta ( Betta splendens ) was studied for 96 h. The LC50 (50% Lethal Concentration) for 96 h for adult bett...

Ecology, behavior and bionomics: functional response of Heterotermes tenuis Hagen (Insecta: Blattaria: Isoptera: Rhinotermitidae) in forests of the Colombian Orinoquía

Land use intensification may affect diversity, abundance, and functional morphological traits (FMT) related to dispersal, food acquisition, digestion, and nesting in some insects, possibly impacting their ecol...

Shifts in energy allocation and reproduction in response to temperature in a small precocial mammal

Species adjust to changes in temperature and the accompanying reduction in resource availability during the annual cycle by shifts in energy allocation. As it gets colder, the priority of energy allocation to ...

Reproductive characteristics of the hermaphroditic four-finger threadfin, Eleutheronema tetradactylum (Shaw, 1804), in tropical coastal waters

This study investigated the reproductive traits of the hermaphroditic four-finger threadfin, Eleutheronema tetradactylum , along the coasts of Thailand during January to December 2021. Fish samples were collected ...

Evaluation of freshwater heavy metals accumulation effect on oxidative stress, Metallothionein biosynthesis and histopathology of Procambarus clarkii (Girard,1985) collected from three locations in the Delta region, Egypt

In this study, the effect of heavy metals accumulation influence was evaluated on adult crayfish Procambarus clarkii (Decapoda, Astacidea) collected from three different Governmental locations (Kafr El-Shaikh, El...

The gametogenic cycle and spawning of the short-necked clam, Paphia undulata Born, 1778 (Bivalvia: Veneridae) from Timsah Lake, Suez Canal, Egypt

Paphia undulata , The Short-Necked Clam, is an edible marine bivalve that is consumed internationally and locally in Egypt. Overfishing and pollution have caused population declines in Egyptian fisheries during th...

Variation in claw morphology among the digits of Bent-toed geckos ( Cyrtodactylus : Gekkota: Gekkonidae)

Ecomorphological studies of lizards have increasingly employed comparison of claw morphology among species in relation to spatial niche use. Typically, such studies focus on digit IV of the autopodia, especial...

Reproductive studies on the carpet clam Paphia textile ( Paratapes textilis ) (Gmelin 1791) (Family: Veneridae): a guide of aquaculture management along the Egyptian coasts of the Red Sea and Suez Canal

Most aquatic biota's reproductive biology and life cycle are essential to the sustainable management and development of coastal ecosystems and aquaculture. The bivalve Paphia textile (Gmelin 1791), also known as

Synergist response of the Peach fruit fly, Bactrocera zonata (Saunders) to some ammonium based proteinaceous food bait attractants

Under the family Tephritidae, Bactrocera zonata (Saunders) is a serious pest, attacking fruits and vegetables causing large quantitative and qualitative damages throughout the world. Fruit flies require proteinac...

Diversity and abundance of birds in dumpsites of Afar region, Ethiopia: implication for conservation

Dumpsites play key role in conservation of birds. A study was conducted to assess the diversity and abundance of birds in dumpsites of Afar region, Ethiopia from August, 2019 to March, 2020, covering both the ...

Morphology of the male reproductive system and sperm ultrastructure of the green lacewing, Chrysopa pallens (Rambur, 1838) (Neuroptera: Chrysopidae)

Chrysopa pallens is one of the most beneficial and effective natural predators, and is famous for its extensive distribution, wide prey spectrum, and excellent reproductive performance. This study examined the an...

Review of the genus Sparasion Latreille, 1802 (Hymenoptera: Platygastroidea: Sparasionidae) of the Oriental region with descriptions of new species from India

The genus  Sparasion , endoparasitoids of Tettigoniidae, occur in the Nearctic, Palearctic, Afrotropical and Oriental regions. It is absent in the Neotropics and Australasia. Of the thirteen species found in the Or...

Effects of morphological traits on body weight and analysis of growth-related genes of Parabramis pekinensis at different ages

Parabramis pekinensis was treated as research object in order to investigate the correlation between morphological traits and body weight. We measured 9 morphological indexes including total length ( X 1 ), body len...

Heart ventricles of the dromedary camel ( Camelus dromedarius ): new insights from sectional anatomy, 3D computed tomography, and morphometry

Dromedary camel heart morphology is a crucial research topic with clinical applications. The study aims to understand the dromedary camel anatomy, morphology, and architecture of the ventricular mass. Results:...

First record of rainbow shrimp, exotic species Mierspenaeopsis sculptilis (Heller, 1862), in the Brazilian coastal amazon, validated by DNA barcode

This is the first record of the alien shrimp Mierspenaeopsis sculptilis in Brazil. The invasion was detected within Marine Extractive Reserves based on eight specimens accidentally caught by local fishermen using...

Comparative study of ovarian development in wild and captive-reared long-whiskered Sperata aor (Hamilton, 1822)

Long-whiskered catfish Sperata aor is a freshwater catfish known for its supreme flesh quality and fast growth, whose captive-reared broodstock denotes a difficult challenge for aquaculture. The reproductive dysf...

New insights into phylogenetic relationships of Rhabdocoela (Platyhelminthes) including members of Mariplanellida

Previous flatworm phylogenetic research has been carried out analysing 18S and 28S DNA markers. Through this methodology, Mariplanellinae subfamily has been recently re-classified as Mariplanellida status novu...

The effects of endogenous FSH and its receptor on oogenesis and folliculogenesis in female Alligator sinensis

The precise mechanisms of hormone action responsible for the full course of events modulating folliculogenesis in crocodilian have not been determined, although histological features have been identified.

The effect of the egg-predator Carcinonemertes conanobrieni on the reproductive performance of the Caribbean spiny lobster Panulirus argus

The Caribbean spiny lobster Panulirus argus is heavily fished throughout its Greater Caribbean and Gulf of Mexico distribution, suggesting a heightened susceptibility to a fisheries collapse. In 2017, a nemertean...

Correction: Mitochondrial phylogeny and taxonomic revision of Italian and slovenian fluvio-lacustrine barbels, Barbus sp. (Cypriniformes, Cyprinidae)

The original article was published in BMC Zoology 2021 6 :8

Human-wildlife interaction: past, present, and future

Human-wildlife interaction is a broad and complex topic. Due to rapid world population growth, there have been greater human impacts on wildlife through agriculture and land fragmentation. In many countries, s...

The phylogenetic relationship among two species of genus Nebo (Scorpiones: Diplocentridae) from Saudi Arabia and Middle East

The genus Nebo has been identified as a medically important scorpion species distributed across Arabia and the Middle East. However, its taxonomic status remains unclear.

Comparison of bird assemblage structures and diversity patterns between seasons among two Ethiopian wetlands

Wetlands are significant habitats for bird populations, and knowledge of the diversity and other ecological aspects of bird species contribute to the management of the ecosystem. The present study was based on...

Correction: Solving a running crab spider puzzle: delimiting Cleocnemis Simon, 1886 with implications on the phylogeny and terminology of genital structures of Philodromidae

The original article was published in BMC Zoology 2022 7 :51

Effects of fine-scale habitat quality on activity, dormancy, habitat use, and survival after reproduction in Rana dybowskii (Chordata, Amphibia)

Amphibians are facing population declines and extinctions, and protecting and supplementing refuges can help species survive. However, the microhabitat requirements of most species are unknown, and artificial ...

Anatomical, histochemical, and immunohistochemical observations on the gastrointestinal tract of Gallinula chloropus (Aves: Rallidae)

Gallinula chloropus (Linnaeus, 1758) is a wild aquatic omnivorous bird characterized by a marked resistance to harsh environmental conditions and a worldwide distribution. In this study, anatomical, morphometrica...

Selection and validation of reference genes for the normalization of quantitative real-time PCR in different muscle tissues of rabbits

In molecular biology studies, the selection of optimal reference genes is of vital importance for accurately quantifying gene expression. The purpose of the present study was to screen the most stable referenc...

Complex strategies: an integrative analysis of contests in Siamese fighting fish

Animals use contests to attain resources and employ strategic decisions to minimise contest costs. These decisions are defined by behavioural response to resource value and competitive ability, but remain poor...

Histamine and gamma-aminobutyric acid in the nervous system of Pygospio elegans (Annelida: Spionidae): structure and recovery during reparative regeneration

In recent two decades, studies of the annelid nervous systems were revolutionized by modern cell labeling techniques and state-of-the-art microscopy techniques. However, there are still huge gaps in our knowle...

Growth, maturity, reproduction, and life expectancy in ex-situ pacific walruses ( Odobenus rosmarus divergens )

Pacific walruses are found in Arctic regions of the Chukchi and Bering Sea where rapid changes in environmental conditions resulting in loss of sea ice are occurring. Therefore, accurate life history data are ...

The ontogenic gonadal transcriptomes provide insights into sex change in the ricefield eel Monopterus albus

The ricefield eel is a freshwater protogynous hermaphrodite fish and has become an important aquaculture species in China. The sex change of ricefield eel is impeding its aquaculture practice, particularly the...

Morphological and morphometric studies on the axial skeleton of the sitatunga ( Tragelaphus spekii gratus )

Anatomical features of the skeleton of wild animals contribute largely to their adaptation. A dearth of information on the skeletal anatomy of the sitatunga ( Tragelaphus spekii gratus ) necessitated this study. Tw...

Disarrangement and reorganization of the hippocampal functional connectivity during the spatial path adjustment of pigeons

The hippocampus plays an important role to support path planning and adjustment in goal-directed spatial navigation. While we still only have limited knowledge about how do the hippocampal neural activities, e...

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Research article Boring life: early colony formation and growth in the endolithic bryozoan genus Penetrantia Silén, 1946 Sebastian H. Decker, Sarah Lemer, Simone Decker, Masato Hirose, Mildred J. Johnson & Thomas Schwaha Published 14 June 2024

Research article Brood success of sex-role-reversed pheasant-tailed jacanas: the effects of social polyandry, seasonality, and male mating order Ya-Fu Lee, Yen-Min Kuo, Bing-Yuan Chuang, Hui-Ching Hsu, Yi-Jun Huang, Yu-Chen Su & Wen-Chen Lee Published 30 April 2024

Research article The more we search, the more we find: discovering and expanding the biodiversity in the ring nematode genus Xenocriconemella De Grisse and Loof, 1965 (Nematoda: Criconematidae) A. Archidona-Yuste, I. Clavero-Camacho, A. N. Ruiz-Cuenca, C. Cantalapiedra-Navarrete, G. Liebanas, P. Castillo & J. E. Palomares-Rius Published 25 March 2024

Research article Starvation resistance in the nematode Pristionchus pacificus requires a conserved supplementary nuclear receptor Tobias Theska, Tess Renahan & Ralf J. Sommer Published 13 March 2024

Research article Correction: Deep-sea ctenostome bryozoans: revision of the family Pachyzoidae, with description of a new genus and three new species from Zealandia Thomas Schwaha & Dennis P. Gordon Published 11 March 2024

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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

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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...

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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 ...

Macroanatomical investigations of the skulls of both genders of Heliosciurus gambianus (Gambian sun squirrel) and Funisciurus anerythrus (Thomas’s rope squirrel)

The skull shape and morphometry have been used by several researchers to differentiate and classify species, breeds and also to age the specimen. This study highlights details of the gross morphometry of the s...

The influence of temporal variation of some limnological parameters on finfish assemblage in Osun River, Nigeria.

Anthropogenic activities is a major factor that determines the condition and sustainability of an environment. The nature and type of activities will determine the health, ecosystem services and general well-b...

Susceptibility of processed and stored cassava, plantain, yam, and cocoyam to coffee bean weevil ( Araecerus fasciculatus De Geer)

Coffee bean weevil ( Araecerus fasciculatus DeGeer) (Coleoptera: Anthribidae) infestation is a major challenge affecting processed, dried, and stored foods globally. However, the growth performance of this insect ...

Effects of dietary supplementation of Parkia biglobosa pulp on growth performance and physiological status of Clarias gariepinus fingerlings

The present study investigated the effect of dietary Parkia biglobosa pulp (PBP) on the growth performance and blood profile of mixed sex Clarias gariepinus . The PBP meal was supplemented with the basal diets at ...

From agricultural waste to chicken feed using insect-based technology

This study investigates the potential of black soldier fly (BSF) larvae to recycle agricultural waste into larval biomass for chicken feed, and was carried out at the University of Dschang, Cameroon in 2020. F...

Anatomical and histological study on the tongue of two different species Ptychadena mascareniensis and Hemidactylus turcicus from the Egyptian environment

The tongue plays definite and important role in simplifying food intake and also, exhibits significant morphological distinctions to acclimatize the environment. This study aimed to investigate the variations ...

Molecular and phenotypic characterization of Hemicriconemoides rosae (Rathour et al., 2003) from mustard rhizosphere in India

Nematodes belonging to Genus Hemicriconemoides , commonly known as sheathoid nematodes, damaged many fruits, vegetables and cash crops, worldwide. A survey has been conducted in the agricultural fields of Bulandsh...

Antiurolithiatic effect of a polyherbal formulation against sodium oxalate-induced urolithiasis in rats

The present study assesses the role of polyherbal formula (LACTN) against sodium oxalate (NaOx)—stimulated urolithiasis prophylactic and curative. Forty-eight rats were separated into the following regimen’s g...

Comparative morphology of sensilla of antennae, maxillary and labial palpi of adult Rhyzopertha dominica (F.) (Coleoptera: Bostrichidae), with specific reference to the typology and possible functions

The lesser grain borer Rhyzopertha dominica (F.) (Coleoptera: Bostrichidae) is a cosmopolitan insect pest of stored cereal grains. In this study, the fine morphology of antennae, maxillary and labial palpi as wel...

Temporal changes in plankton diversity in relation to hydrographical characteristics at Perumal Lake, Cuddalore District, Tamil Nadu, India

The fresh water environment supports the productivity of phyto- and zooplankters and fin and shell fishes. The rate of fish productivity of an aquatic ecosystem solely depends on the rate of plankton productiv...

Effects of potassium bromate on Rattus norvegicus brain antioxidant markers, acetylcholinesterase activity, and DNA fragmentation: investigation of therapeutic effect of Allium cepa

Allium cepa is well-known for its antioxidant capabilities and contains potent antioxidant quercetin (3, 30, 4, 5, 7-pentahydroxyflavone). We investigated the therapeutic effects of aqueous extract of Allium cepa

Seasonal fluctuations of antioxidant enzymes and biochemical compositions of Apis mellifera adansonii L. from three ecological zones of Nigeria

The ability of honeybees to survive and sustain honey production depends on their ability to adapt to their environment. This study evaluated the seasonal fluctuations of antioxidant activities and biochemical...

Stock identification of Congaturi halfbeak ( Hyporhamphus limbatus ): insight into conventional and truss-based morphometrics

Wild fish stocks continuously decline in Bangladeshi rivers and oxbow lakes. Small indigenous fish species management solely depends on their population status and conservation. This study aimed to determine t...

Ameliorating effect of blueberry consumption on energy drink-induced testicular damage in rats: histological and immunohistochemical study

Energy drinks prevent fatigue and increase physical and cognitive performance; however, they also inflict toxic effects on the body. Blueberry (BB) possesses antioxidant and anti-inflammatory properties. The p...

A scoping review of the impact of heat stress on the organs of the Japanese quail ( Coturnix japonica )

Heat stress negatively affects poultry welfare, including the Japanese quail, especially in sub-Saharan African countries. The quail is vital to research and protein food security, which are affected by global...

Hydro-climatic consequences on zooplankton diversity and abundance in perennial Vavuniya reservoir and seasonal Thandikulam reservoir in Vavuniya, Sri Lanka

Zooplankton exhibit strong responses for minute changes in their habitat. Therefore, this study intended to investigate the impacts of hydro-climatic factors and related water quality variables on zooplankton ...

Diversity and species richness of butterfly in soraipung range of Dehing Patkai National Park, Assam, India

The present study deals with the butterfly diversity in Soraipung Range of Dehing Patkai National Park. The site was chosen on the basis that it lies in between Eastern Himalaya and Indo-Burma which is acclaim...

Bioprospective studies of pigmented ink from Sepioteuthis lessoniana and its molecular identification using CO1 gene

The present-day world is teeming with numerous diseases due to the changing environment. The enormous growth of population has overburdened the prevailing resources of drugs; hence, drug manufacturers are in t...

Influence of habitat heterogeneity on avian diversity in the Rajparian Wildlife Sanctuary, Kashmir Himalaya

The value of local and regional landscapes for avian conservation requires a thorough understanding of the diversity and structure of bird communities. Avifauna serves as an important biological indicator in m...

Assessment ameliorative role of fenugreek seeds and germinated fenugreek seeds on pancreatic and testicular gentamicin toxicity of male Swiss albino mice

Gentamicin is one of aminoglycoside antibiotic used for treatment of many infections due to its availability and less cost. The aim of this study aimed to assess the modulation effect of fenugreek seed and its...

Biomarkers as ecological indices in monitoring the status of market fish

Environmental contamination has become a major concern over the past few decades, drawing the attention of numerous researchers from both developed and developing nations. The aquatic system serves as the prim...

Gentiana lutea attenuates hepatotoxicity induced by ketoconazole in rats by fortifying the cellular antioxidant defense system

Ketoconazole (KET) is a broad-spectrum antifungal drug that has been reported to induce hepatotoxicity in humans and animals.

Histopathological and immunohistochemical studies on the influence of orally administration monosodium glutamate, a food additive dependent on time in vivo

Monosodium glutamate is a widely used flavor enhancer/food additive in meat, fish, milk and cheese or vegetable origins. Our present study aimed to assess the effect of utilization monosodium glutamate on the ...

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• Published: 29 October 2019

What’s new from the zoo? An analysis of ten years of zoo-themed research output

• Paul E. Rose   ORCID: orcid.org/0000-0002-5375-8267 1 , 2 ,
• James E. Brereton   ORCID: orcid.org/0000-0002-9104-3975 3 ,
• Lewis J. Rowden 4 ,
• Ricardo Lemos de Figueiredo 5 &
• Lisa M. Riley 6  

Palgrave Communications volume  5 , Article number:  128 ( 2019 ) Cite this article

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The modern zoo’s roles command empirical enquiry to determine the effectiveness of zoos locally and globally. Ten years ago, published work identified the need for empirical research on a diverse range of species beyond charismatic zoo megafauna. We review zoo-based research published in the decade since this original recommendation. We collectively evaluate zoo-themed research papers from those working in zoos and those external to zoos but studying zoo-housed animals. By systematically searching Web of Science © for zoo-based research and performing inductive content analysis to code year, journal, study animal’s taxonomic classification, and research aims and outputs we evaluate trends in zoo-themed research, contrasted with trends in species holding. Significantly more birds and fish are kept compared to mammals, reptiles and amphibians, but mammals are consistently the primary research focus. Whilst output generally rises, only for birds is a steady increase in publications apparent. Husbandry evaluation is a major aim/output, but papers on pure biology, cognition and health also feature. Most publications lead to “specific advancement of knowledge” including validation of methodologies. We show that: (1) trends in species holdings are unrelated to trends in publication; (2) zoo-themed research makes meaningful contributions to science; (3) zoo researchers should diversify their aim/output categories and chosen study species to close the persisting research gaps that we have identified. Finally, we discuss our findings in the context of evident species biases within research outputs across the broader fields of zoology, conservation and ecology.

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Introduction.

Zoos and aquariums have the potential to be excellent locations to develop, implement and complete scientific research. Zoo populations enable hypothesis-driven questions to be answered on species/topics that would be challenging in the wild. This is evidenced by, for example, ground-breaking insights into the reproductive biology of the critically endangered Sumatran rhinoceros, Dicerorhinus sumatrensis (Roth et al., 2004 ) or results on the energetic costs of locomotion in bears, Ursidae (Pagano et al., 2018 ). Zoological databases that hold information on species’ biology can enhance the scientific literature on natural history and ecology (Conde et al., 2019 ); information that also informs animal management practices and species conservation strategies both in-situ and ex-situ. As centres for both pure and applied science, the output from zoological collections not only covers a range of disciplines (Loh et al. 2018 ) but is of increasing value to multiple stakeholders working in all parts of the world with all taxonomic groups.

The four aims of the modern zoo—conservation, education, research and recreation (Mason, 2007 , Fernandez et al., 2009 ) provide a framework for scientific investigation. The importance of research to the modern zoo is reflected in the number of pieces of national zoo legislation that require research activities to be conducted (Hosey et al., 2009 ). Conversely, entertainment is perceived as the least important role of the zoo (Reade and Waran, 1996 ), yet visitation must be maintained as zoos can be reliant on entrance fees for income. This income provides a means for zoos to fulfil their roles in conservation and education, hence zoos must remain attractive destinations to visit (Bueddefeld and Van Winkle, 2018 ). Research into the educational role of the zoo has scrutinised the effectiveness of zoos as learning environments (Marino et al., 2010 , Dawson and Jensen, 2011 , Moss and Esson, 2013 ). Despite an increase in zoo visitor studies over the past decade (Jensen, 2010 , Moss and Esson, 2010 ), there is little evidence that zoos promote understanding or pro-conservation behaviour. The importance of robust experimental design and application of “good science” is also evident in literature (Wagoner and Jensen, 2010 , Moss et al., 2017 ) promoting the need for an evidence-based approach.

Such an evidence-based approach extends to animal husbandry, central to which is researching animal behaviour. A majority of zoo scientific studies has previously been shown to be of a behavioural nature (Hosey, 1997 ). The relevance of behavioural science to conservation outcomes was postulated by Sutherland ( 1998 ) who states the importance of conserving behaviour as part of conservation objectives. A potential fifth aim of the zoo, to promote excellence in animal welfare (Fernandez et al., 2009 ) further supports the need to increase the amount of scientific study and application of such study, into zoo animal management. An increasingly ethically-aware public, who focus on the importance of good welfare and are not just concerned with animal cruelty (Whitham and Wielebnowski, 2013 ) emphasises the need for zoos to manage their populations to ensure a high quality of life can be attained and maintained for all individuals.

As scientific research that collects data to answer an hypothesis-driven question is key to ensuring husbandry regimes are most appropriate, zoos have invested in collaboration with academics (Fernandez and Timberlake, 2008 ), in the development of research methodologies (Plowman, 2003 , Plowman, 2008 ) and in the creation of research-focussed committees and working groups (BIAZA, 2018b ) to increase and develop their scientific output and its uptake by zoological collections. By expanding on how empirical research is applied within zoological collections (e.g., to husbandry routines, visitor engagement and interpretation objectives, or population management goals) the reach, impact and outcome of each of the zoo’s aims is strengthened.

With a new focus on collection planning for population sustainability (Traylor-Holzer et al., 2019 ), a paucity of scientific research for many familiar (i.e., commonly-kept, often-seen-in-the-zoo) species has been apparent (Melfi, 2009 ). This paper (Melfi, 2009 ) shows that researchers study a limited number of individuals of high-profile, charismatic species—a trend previously noted in the wider field of “wildlife research” (Bautista and Pantoja, 2005 ). Species less appealing to the public but housed in greater numbers across more zoological collections have been ignored. Likewise, when considering species responses to captivity, mammals are often focal subjects (Clubb and Mason, 2003 ) and ecological data are used to inform our understanding of their responses to captivity (Mason, 2010 , Kroshko et al., 2016 ). However, for other non-mammalian taxa we consider how they cope with the human-created environment of the zoo less often (Carere et al., 2011 ). Species with a long history of captivity, well-known and recognisable to the visiting public can still challenge us regarding their optimal captive care (Hatt et al., 2005 , Rose, 2018 ) and empirical, structured research programmes can help redress the balance between what a species needs to thrive and what is provided for survival in the zoo. Therefore, to move forward with species-specific Best Practice (husbandry) Guidelines (EAZA, 2019 ) less considered taxa, common but “ignored” species or animals perceived as less charismatic, e.g., reptiles, amphibians, fish and invertebrates, (BIAZA, 2018a ) need to be the focus of future research attention. Melfi ( 2009 ) highlights this lack of research into non-mammals as the cause of anecdote or “rules of thumb” methods of providing captive care.

As such, the aim of our paper was to look retrospectively from 2009 to 2018 to see how much more scientific research has been conducted into the areas identified by Melfi ( 2009 ) as lacking a research focus. Specifically, we collected research papers from five different taxonomic groups, to evaluate the range of taxa now included in scientific publications and we investigated if/how uptake and output of evidence, useful for management, has diversified. We used Melfi ( 2009 )’s Table 1 (page 581) and Fig. 2 (page 582) as a guide to what constitutes “forgotten taxa”—focussing on those animals with large populations but limited scientific investigation. We have added invertebrates, amphibians and fish to our analysis that were excluded or not fully included in the original Melfi paper for reasons outlined below. Melfi ( 2009 )’s Fig. 2 shows the relationship between the number of individuals of specific animal species held by British and Irish association (BIAZA) zoos, as well as the number of zoos that hold each represented species, compared to the number of projects conducted on these species, based on records from the BIAZA research database. A bias towards the study of a small number of charismatic mammalian species, for example chimpanzees (Pan troglyodytes) , bonobos (P. paniscus) , orangutans (Pongo sp.) , elephants (Elephas maximus, Loxodonta africana) , is clear from this figure. Melfi notes that more projects between 1998 and 2008 were conducted on the two species of Pan compared to all projects on birds, reptiles, amphibians, fish and invertebrates in this sample of BIAZA institutions—90 against 84 studies. We aim to see if such a bias exists in a sample of wider zoo output in the ten years from this dataset being published.

Papers were collected using the bibliographic database Web of Science©. Key term searches were carried out by including zoo* combined with either behaviour*/behavior* or welfare or nutrition and research for each type of taxa (mammal, bird, reptile, amphibian, fish), for example “zoo* bird behaviour*. Each author was assigned a specific taxon and asked to scrutinise search results in the same manner, inputting data into a standardised spreadsheet. In January 2019, the lead author searched for remaining papers in 2018 across all taxa and terms to complete the dataset. Papers were categorised by year, species (and later class, genus and order), aim and main output. Aim was defined as the reason why the research was conducted (e.g., to determine the effect of a change of husbandry routine, or the influence of enrichment on behaviour, or to benchmark positive indicators of welfare). Output was defined as the key finding of the study and how this helps to underpin evidence-based zoo management.

Papers that covered more than one species of the same taxa (e.g., free-flight aviaries) were categorised as “multiple mixed”. Papers that covered a range of species from different taxa (e.g., visitor studies research or research into common patterns of stereotypic behaviours) were categorised as “multiple taxa review”. Papers that detailed methodological advances or novel approaches to data collection were categorised as “theory”. Papers that focussed on people including where data could add information on best practice animal care (e.g., influences on collection planning based on visitor perception) were categorised as “visitor”. Only peer-reviewed scientific papers in the Web of Science© search were included. Conference papers were not counted. In total, 1063 papers were categorised from 236 publications.

The impact factor of each publication was recorded from the individual journal website or from www.bioxbio.com if the impact factor was not clear on the journal’s homepage.

Rationalising aims and outputs from each article

Using content analysis, two authors (PER and LMR) coded the description of a paper’s aim and outcome into an aim class and an outcome class and outcome gain (see Table 1 for explanation). Papers were checked at the original source if both reviewing authors (during coding) were unsure of the aims and outcomes of the paper from its abstract. Aims were prioritised based on the paper’s own statement of their original aim and not on subsidiary findings. The aim “Husbandry and training” also includes papers that investigated visitor effects because visitors are provided in the zoo whether the animal wants them or not and therefore they directly impact on daily husbandry and management decisions. For each paper, one author stated their interpretation of aim and outcome code and this was judged using a protocol (Table 1 ) by the second author who also ensured the first aim/outcome was prioritised. Triangulation was not necessary as the two authors agreed on 100% of codes. Codes were created using an inductive approach. If a new aim/outcome was coded or new example were added, all previously papers in that aim class, outcome class or output gain were re-coded to reduce bias.

Specialised journals and global species holding

To compare any trend in publication output seen in the main Web of Science © dataset with two specialist zoo journals that are i) an annual publication without an impact factor and ii) have only incomplete listing on this database, an analysis of the output from the International Zoo Yearbook, IZYB, (published annually since 1960 by the Zoological Society of London) and the new open-access Journal of Zoo and Aquarium Research, JZAR, (published by the European Association of Zoos and Aquaria, EAZA) was conducted in the same manner (assessing the number of publications per taxa between 2009 and 2018). From these two journals, 354 papers were collected.

To provide context to research output gathered from searching for numbers of papers on specific taxa, data on species holdings of all zoos globally, published in the International Zoo Yearbook, were analysed alongside of the research-focussed data. These (unpublished) species holdings data were collected as part of an on-going additional research project (by author JEB) with the annual number of each species of mammal, bird, reptile, amphibian and fish kept at each zoo being recorded.

Invertebrates

Papers on zoo-applicable invertebrate research were sampled alongside of the main dataset. As we were keen to follow Melfi ( 2009 )’s categories of research subjects as closely as possible and because of the high number of papers to review between authors, details collected on invertebrate papers were restricted to: the name of the journal and year, the type of aim of the paper and the study subject. Again, only papers found in Web of Science © were recorded and the same categories for searching across the complete database were used: e.g., “zoo* invertebrate OR cephalopod OR arachnid welfare”. Abstracts of papers were read to ensure there was an application to zoo populations- i.e., the paper was not solely focussed on laboratory experimentation. A total of 17 papers were identified from 2011 to 2018 across 12 different publications.

Total sample size

Overall, 1434 zoo-focussed research papers were collected for analysis and evaluation (from the main dataset, from the IZYB and JZAR dataset, and for the separate search for invertebrate-specific research).

Data analysis

Data were analysed in R studio v. 1.0.136 (R Core Team, 2016 ). Where required, data were checked for collinearity using the “car package” (Fox and Weisberg, 2011 ), with values <2 taken as acceptable. Plots of residuals in R for each model were used to assess the distribution of data before further testing.

To compare differences between total counts of mammalian, avian and fish species held, a two-sample t -test was run. To determine any change in the number of species in each class housed by global zoos over the course of the study, a one-way ANOVA was run for species counts against year.

To compare the number of papers published against the taxonomic class of species held plus year of publication, a general liner model was run in R and post-hoc testing to ascertain differences between predictors was run using the “pbkrtest” and “lsmeans” packages for R studio (Halekoh and Højsgaard, 2014 , Lenth, 2016 ).

Fitted models were also run in R, with associated linear regression plots, for each outcome, gain and taxonomic class per year to identify any significant trend in the number of papers published on that theme.

For those papers with a focus on one taxonomic class only ( n  = 863), a multinomial logistic regression was run in R studio using “multinom” function from the package “nnet” (Venables and Ripley, 2002 ). The “AER” (Kleiber and Zeileis, 2008 ) and “afex” (Singmann et al., 2019 ) packages were used to generate P values of the model fit from ANOVA and Wald’s tests. Post-hoc testing was run using the “lsmeans” package (Lenth, 2016 ) using (model, pairwise ~ factor | object, adjust = “tukey”, mode = “prob”) to generate P values for each pair of factors for each outcome across taxonomic class.

A linear regression was run in R with follow-up ANOVA analysis of the fitted model to determine the significance of predictors (taxonomic class, aim, outcome, gain and year of publication) on journal impact factor.

To remove any chances of Type 1 error, the Benjamini and Hochberg ( 1995 ) method of correcting the level of significance was employed when comparing multiple P values.

Global species holdings and the taxonomic focus of research papers

Figure 1 shows that birds and fish are the most speciose taxa housed in zoos globally, and amphibians comprise the fewest number of species housed. Significantly fewer species of mammal are housed compared to birds ( t  = −21.07; df = 11896; P  < 0.001) and fish ( t  = −8.86; df = 9291; P  < 0.001). For each taxonomic class, there was no significant change in the number of species held by zoos globally between 2009 and 2018 (mammals P  = 0.985; birds P  = 0.809; reptiles P  = 0.488; amphibians P  = 0.559; fish = 0.999).

The mean number of species within each taxonomic class (white dot, no line) housed globally in zoological establishments that provided data to the International Zoo Yearbook from 2009 to 2018 compared to the number of publications (red dot, red line), per year, for that taxonomic class. Overall birds are the most speciose taxonomic class housed by zoos globally and show the biggest increase in research output

There is a significant relationship between the number of papers published on each taxonomic class, the year of publication and the mean number of species in that class held ( F 14,35  = 58.59; r 2  = 0.94; P  < 0.001). Across years the increase in the number of papers published for all taxonomic classes combined was not statistically significant (regression slope = 7.41; P  = 0.338), suggesting that the overall number of papers on all topics identified from this literature search remains similar.

Significant differences are noted for the output for mammals against reptiles (higher number of mammalian papers), for fish against mammals (lower number of fish papers) and for amphibians against mammals (lower number of amphibian papers), Table S1 (supplementary information). When evaluating the interaction between species held and taxonomic class (species_holding*taxonomic_class) there is no significant relationship, showing that the average number of each species (in each taxonomic class) held in zoos is not influencing the number of publications on these taxa (intercept = 1.16, P  = 0.976) even though the relationship between the overall number of papers published and taxonomic class of animal is still significant (F 9,40  = 74.65; r 2  = 93%; P  < 0.001). As there is no significant change in the number of species held over this time period, an increase in the holdings of one class is not causing an increase in research output in that specific class.

Trends in the specific categories and aims of zoo-based papers

Analysis reveals that most of the papers have a husbandry and/or welfare focus (see Table S2, supplementary information), be that in the aim ( n  = 301) of the paper or the overall outcome ( n  = 435). The high number of papers coded as a pure biology outcome ( n  = 271) shows that zoos can be centres for the advancement of “blue sky” science, as well as for applied science. This idea is supported by the proportion of papers (75%) that add to our knowledge of the species or topics being investigated. With only 1.7% of papers having no specific gain (i.e., a need for more research to answer the paper’s aim) zoo-based papers are clearly able to impact on knowledge and practice in this area of science.

Is there a relationship between the question being asked and what type of animal is being studied?

The Analysis of Deviance (type II) tests from the model showed that a paper’s aim (likelihood ratio χ 2  = 81.65; df = 36; P  < 0.001), outcome (likelihood ratio χ 2  = 54.23; df = 20; P  < 0.001) and gain (likelihood ratio χ 2  = 30.13; df = 16; P  = 0.017) are all significant predictors of the taxonomic class of the paper. Year was not a significant predictor but may be trending in that direction (likelihood ratio χ 2  = 49.97; df = 36; P  = 0.06). Post-hoc comparison of outcomes for each taxonomic class identified multiple significant predictors (for example Table S3, supplementary information).

Surveying across single-taxonomic class papers only (for the aim, outcome and gain of each paper) shows differences in the proportion of papers on each specific theme by taxa. For fish, 43% of papers had a husbandry aim, 57% of fish papers had a pure biology outcome and 71% of fish papers were identified as having a gain of a specific advancement in knowledge.

Across those papers on reptiles, 45% had a veterinary medicine and animal health aim, 42% had an animal and ecosystem health outcome, and 52% of papers had a gain of a specific advancement in knowledge. For amphibians, 16% of papers had a behavioural aim and 16% had a veterinary medicine and animal health aim, 29% of amphibian papers had a husbandry outcome and 48% paper were identified as providing a gain by specifically advancing knowledge.

An aim of behaviour was identified for 31% of all papers focussing on birds, 39% of bird papers had a husbandry and welfare outcome and 69% of bird papers provided a gain of a specific advancement in knowledge. For papers on mammals, 32% had a husbandry and training aim, 43% had a pure biology outcome, and 70% provided a gain in the specific advancement of knowledge.

For those wishing to advance an evidence-basis for zoo animal husbandry, 23% of all papers provided a gain of how to advance practice (either species-specific or general) with 78% of these being on mammals. Most papers focussed on adding to our knowledge of the study subject(s). Table S4 (supplementary information) further evidences the popularity of specific taxonomic orders as subjects for zoo-themed research by illustrating the types of question asked and output gained on the different taxonomic classes identified in our dataset. Details are provided for the top five orders from mammals, birds and amphibians, for all three orders of reptiles and for all six orders of fish from the ten-year dataset. Bias in the questions being asked at a taxonomic level is evident for each order and may relate to the accessibility of this animal in a zoo or the expertise of the researcher conducting the science.

Predicting future trends

Assessing the main dataset ( n  = 1063) for increases or decreases in the number of publications per theme or on a particular taxonomic group type of animal identifies key areas where zoo research is growing in output. A significant relationship is found for the number of papers published on captive birds over the ten-year period, +3.5 papers/year ( F 1,8  = 26.99; r 2  = 74.3; P  = 0.001), supporting the trend illustrated by Fig. 1 . Papers with an overall methodology aim also increase, +1.01 papers/year, indicating that zoological research is continuing to publish new ways of assessing the animals within collections ( F 1,8  = 30.23; r 2  = 76.5; P  = 0.001). Papers with an aim of veterinary medicine and animal health also increase (+1.01 articles per year) significantly ( F 1,8  = 8.97; r 2  = 47.0%; P  = 0.017). Figure S1 (supplementary information) illustrates these trends over time.

There are also increases on year for outcome with 1.12 extra papers per year published on animal and ecosystem health ( F 1,8  = 9.69; r 2  = 49.1%; P  = 0.014). Output of papers with a visitor studies aim was not significant ( P  = 0.08, +0.2 papers/year). Husbandry and welfare outcome papers may tend towards a significant increase of +1.7 papers/year ( P  = 0.062). This general trend is supported by Fig. S1, which shows a rise in this outcome category over time (although this is not consistent from one year to the next). Finally, there is a significant increase (+5.8 papers/year) in the number of papers published that specifically advance our knowledge of zoo animals ( F 1,8  = 38.18; r 2  = 80.5%; P  < 0.001).

Conservation and population sustainability papers and those focussing on human behaviour change outcomes appear low overall, when compared to those on pure biology and on husbandry (Fig. S1). Such information highlights areas for research to expand into in the future to ensure output continues to be novel and relevant.

Patterns of publication from an annual and a new scientific journal

To compare with output taken from the impact factor-listed publications in the main dataset, Fig. S2, supplementary information, shows the publication trend for the IZYB and for JZAR. Trends in the IZYB data are harder to predict, even though overall the number of mammal-focussed papers is higher than for other classes (47% overall). However, a notable pattern of mammal-focussed publication is evident in each year of JZAR; since its first publication in 2013, 59% of papers are on mammals. All single-class taxonomic categories aside from mammals can be absent from each of these two publications (Fig. S2). Therefore, consideration for the theme of each volume or the breadth of papers included within may be needed to ensure that a wide-range of species are focussed on per edition.

Assessing impact

Differences are apparent in the spread of journal impact factors for where papers on each class of animal and each type of research topic are published (Fig. 2 ). The top five highest impact factor journals include research on multiple taxonomic classes and papers that provide a general advancement in knowledge (with one species-specific focus (elephants) that provides a specific advancement in knowledge). Of the 1063 papers from 2009–2018, two are published in journals with an impact factor of above 10, with the majority (75%) published in journals with an impact factor of below 2.

Boxplots to show the median impact factor of papers for each type of animal or research aim. Top: taxonomic class (A amphibians, All All classes included, B birds, F fish, M mammals, M+ Mammals plus another taxa, R Reptiles, RA+ Reptiles and amphibians plus another taxa). Middle: Aim category (BEH Behaviour, BPR Breeding programmes, HUS husbandry and training, MTH methods, NUT nutrition, PHY physiology, VET veterinary medicine and animal health, VIS visitor studies, WEL welfare). Bottom: Outcome category (AEH animal and ecosystem health, BCH behaviour change human, CSN conservation and sustainability, HUS husbandry and welfare, PUB pure biology, SCI scientific validity). Papers covering all taxa show the largest range in impact and the highest impact overall

Papers with Husbandry and welfare, Human behaviour change, and Conservation and sustainability outcomes are published in the highest impact journals. Papers with a Welfare, Visitor studies, Methods, and Husbandry aim are also found in these higher-impact publications. It is exciting to see that a wide range of topics can be published and disseminated widely across the breadth of the scientific literature- zoo-focussed research is not restricted to “zoo only” journals.

There is a significant relationship between several predictors and publication in a higher impact factors journal ( F 34, 1028  = 2.59; r 2  = 5%; P  < 0.001). Taxonomic class ( P  < 0.001), aim ( P  < 0.001) and outcome ( P  = 0.009) are all significant predictors of publication in a journal with a higher impact factor. Year of publication ( P  = 0.36) or gain (0.994) show no relationship to a journal’s impact factor. Model estimates for individual GLMs show significantly higher impact factor journals contain papers covering both reptiles and amphibians (estimate = 1.32, P  = 0.007) and papers on birds were more likely to be published in lower impact factor journals compared to other taxonomic groups (estimate = −0.57; P  < 0.001).

For the aim of the paper, those on nutrition (estimate = −0.49; P  = 0.012) and veterinary medicine/animal health (estimate = −0.33; P  = 0.006) were published in lower impact journals, whereas those on visitor studies were significantly more likely to be found in higher impact publications (estimate = 0.52; P  = 0.002). When assessing each paper’s outcomes, those relating to human behaviour change were more likely to be published in journals with higher impact factors (estimate = 0.94; P  < 0.001) compared to other outcome categories.

Comparing the interaction between taxonomic class and the paper’s aim ( F 61,1001  = 1.85; r 2  = 5%; P  < 0.001) shows that higher impact journals are successfully chosen for physiology papers that cover all classes (estimate = 2.36; P  = 0.04) and for methods papers published on reptiles and amphibians (estimate = 3.06; P  = 0.05). A significant interaction is present for papers on reptiles and amphibians with conservation/sustainability outcomes (estimate = 4.47; P  = 0.001), model summary F 39,1023  = 3.003; r 2  = 7%; P  < 0.001. No significant relationship is noted for any interaction between the paper’s gain and the taxonomic class used as the subject, and choice of higher impact journals.

What about invertebrates?

For the 17 relevant papers obtained on invertebrates, the highest number ( n  = 11, 65%) focussed on reviewing or providing commentary on, across taxa, bigger questions relating to welfare (including a paper on enrichment practices that covered other taxa as well invertebrates to determine preferences for a specific type of enrichment provided and a paper on how to design judgement bias tasks, both of which have important welfare connotations). Papers on cephalopods and those covering a review of invertebrate taxa as part of a wider question (e.g., enrichment or welfare assessment) made up several of the articles recorded ( n  = 5, 29%, respectively). Invertebrates articles could cover pure science (i.e., personality studies), as well as be used to inform the management of other taxa in the zoo (i.e., investigating food supplements for invertebrates that are then used as foods for other species). The median impact factor was 1.5, similar to output presented for other taxa in Fig. 2 . Papers published in the top-five impact factor journals were two articles that reviewed welfare (published in journals with an impact factor of 16), a cephalopod welfare paper (published in a journal with an impact factor of 5.23) and paper on cephalopod personality (in a journal with an impact factor of 4.13) and a review paper on welfare (in a journal with an impact factor of 3).

Our results show that zoo-themed researchers are increasing their research output year-on-year; Fig. 1 illustrates that, for bird research at least, the overall trend in output is positive. A bias in the study of large charismatic mammals dominates the overall number of papers published, but zoo-themed researchers are investigating a wide array of topics and increasing their output into areas of knowledge gain, as well as practical application (Fig. S1, supplementary information). This mammal bias appears similar to that noted in the wider field of zoology (Bautista and Pantoja, 2005 ) and the need for a more informed approach (such as our call for more scientific investigation for taxon-specific husbandry guides) is echoed by previous research that highlights a lack of scientific rigour within strategies implemented for habitat and wildlife conservation (Reichhardt, 1999 ).

Zoo-themed research output appears to be aligning with wider conservation messages, for example as emphasised by the One Plan Approach (CBSG, 2015 ), as well as with moves to encourage more direct pro-environmental human behaviour change (Smith et al., 2008 , Spooner et al., 2019 ) and wider usage of ecological evidence for the development of species-specific management plans (EAZA, 2019 ). We demonstrate that zoo-themed research output can cross academic boundaries and answer big questions that extend far beyond the animals housed at the zoo themselves. Increases in the number of papers adding to knowledge of species biology shows the wider relevance of zoos to “blue sky” science and an impact across different fields for all taxa investigated (Fig. 2 ). This expanding and considered research output appears to align with developments noted in other areas of biology too- for example the relative success of conservation initiatives in the United States (Schwartz, 2008 ) even though data to underpin these measures can often be lacking.

The focus on specific taxonomic groups compared to others (Table S1) may be a facet of the particular research interest of individual scientists, the commonality of a particular species in the zoo, or the availability of species in zoos close to the workplace of scientists that are publishing in this field. There are clear trends in the choice of taxonomic order when looking over the aims, outcomes and gains from research published on zoo-housed animals (Table S3), indicating that researchers opt for a particular taxonomic order as a study system when designing how to test an experimental hypothesis. A Husbandry and training aim and a Husbandry and welfare outcome predominates in this dataset (Table S2) showing that zoo research is focussing on key areas of management to improve captive care. This illustrates that the majority of these papers are adding to knowledge to strengthen the aims of the modern zoo, and it is encouraging that only 18 papers provided no firm conclusion to their way. Those researching the zoo are clearly able, in the vast majority of cases, to provide an answer to their question.

Our results identify some interesting trends in how zoo animals are used for research. Notably that reptiles feature more in veterinary and health-related papers than other taxonomic classes, yet whilst mammals are the most commonly studied class (Fig. 1 ), they show the least variation in research aim for across all classes (Table S3), with papers asking either behavioural or husbandry and training related questions. Amphibians are the class with the most diverse array of questions asked—covering breeding, husbandry, nutrition, physiology, behaviour, and veterinary medicine and animal health. This suggests that the conservation relevance of amphibians in zoos (Zippel et al., 2011 ) and the urgency by which captive-naïve populations have had to be created suddenly ex situ (Pavajeau et al., 2008 ) has created niches for variation in research questions more quickly than in mammal populations, for example, that have not been exposed to sudden changes in the novelty of species held.

We identify papers that cover each of the four roles of the modern zoo, demonstrating that zoos are prepared to research how well they are meeting their goals and be scrutinised on the outputs from such research. Given calls for good welfare to be a fifth aim of the modern zoo (Fernandez et al., 2009 ), the high number of papers with a full or in-part welfare outcome (41% of all identified papers) is encouraging. Welfare science is moving quickly, with novel approaches validated (Williams et al., 2018 , Richter and Hintze, 2019 , Yon et al., 2019 ) and an increasing use of natural ecology information as a keystone in determining the relevance of husbandry in the zoo (Rose, 2018 ). Therefore, the application of animal-based welfare assessment to ensure individual welfare is good, rather than a completely resource-based approach is a key area of research for zoos to focus upon (Whitham and Wielebnowski, 2013 ). And as 74% of identified papers that had either a specific or general advancement in practice ( n  = 245) were fully or partly focussed on a welfare outcome, zoos are forging ahead to evaluate many aspects of welfare of the animals they house. Our results indicate this is not confined to a single taxon but relevant to all investigated except reptiles where focus is on health and conservation. This may be because so little of the wild biology is known for many reptilian species that, when in captivity, immediate threats to survival (e.g., disease) must be the primary research concern. Whatever the underlying reason, here there is an identifiable opportunity for future zoo research.

Three key gaps in knowledge of zoo animal management were identified by Melfi ( 2009 ). Firstly, that research tended to investigate indicators of poor rather than positive welfare. Change is evident with research assessing animal-based indicators of a good quality of life now being published (Williams et al., 2018 , Yon et al., 2019 ), and methods for positive welfare assessment for zoo invertebrates, as well as an evidence-basis for captive invertebrate care (Bethell, 2015 , Tonkins et al., 2015 ) can also be found. We demonstrate that targeted research, evidenced by the year-on-year increase in bird research output (for example), with popular aims of husbandry and welfare and with an advancing knowledge outcome, means all aspects of welfare are being considered and investigated.

Secondly that housing and husbandry are historically based on anecdote or tradition. A scientific approach to inform husbandry is noticeable in our dataset, with housing style (Rowden and Rose, 2016 ), daily husbandry regimes (Rose et al., 2016 ), nutrition (Gussek et al., 2018 ), enrichment practices (Costa et al., 2018 ), breeding recommendations (Asa et al., 2011 ) and animal health measures (Greenwell and Montrose, 2017 ) being based on evidence gathered to determine optimal care. The asking of numerous questions (Table S4) with an amphibian model shows that zoo researchers are considering key knowledge gaps at different taxonomic levels when constructing an experimental design. Even within a taxonomic group bias persists as certain species (e.g., Pan spp. in the Primate order) command the evidence-based approach. This is not to say zoos specifically ignore other species as a myriad reasons may explain why the husbandry practices of one species are more science-led than another (for example, the number of individuals kept in zoos). And as Pan sp . studies continue to demonstrate, many research projects are required before an holistic approach to husbandry (and welfare generally) can be achieved. Our paper shows that for many species, zoo research is the start of this evidence-gathering journey.

Thirdly, a lack of species-specific biological data may be inhibiting zoo research output. Well-studied animals, such as Pan sp ., will continue to receive research interest because scientists have a reliable bank of background information to utilise. Consequently, equally important research candidates remain understudied due to this lack of baseline information. Use of ecological information on species’ habitat choices can be used to inform housing (Mason, 2015 , Kroshko et al., 2016 , Mellor et al., 2018 ) and suitability of husbandry can be evaluated via individual preference testing (Mehrkam and Dorey, 2015 , Troxell-Smith et al., 2017a , Troxell-Smith et al., 2017b ). Therefore, constructing “in-zoo” questions based on manipulations that can yield species-specific information means that these poorly understood species can be researched and improvements to their husbandry be made on an evidence-based approach.

We demonstrate that zoo-themed research output is slowly filling in these gaps for more and more species, and we have evaluated how this research can have wider impact across scientific publications with a broader readership (Fig. 2 ). From the output in Melfi ( 2009 ), 89% of the sample concerned mammals (60% of which was primate-focussed), with 8% on birds, 1% on reptiles and 1% on other taxa. Whilst the Melfi ( 2009 ) dataset was restricted to output from only one region (British & Irish facilities), the bias for investigating mammalian species is clear. Within our main Web of Science© dataset, 69% of papers focussed solely on mammals (40% on primates)- therefore highlighting a shift change towards the use of other species as research subjects that is unrelated to the number of species kept of a given taxa.

Inter-disciplinary research also identifies the usefulness of zoo information to big data questions, and such an approach helps further reduce the lack of biological information as identified by Melfi ( 2009 ). Information held in the Zoological Information Management System (ZIMS) database, managed by species360 (species360, 2018 ) has added to the bank of biological information held on non-domestic species (Conde et al., 2019 ) to improve our knowledge and understanding of many important areas of species biology, physiology and life history. To develop this research output, zoos should be increasing the number of scientific studies being published within higher impact journals. Our dataset shows that mammals remain considerably better represented in publications than all other taxonomic groups combined. Indeed, two mammalian Orders, Carnivora (154 papers) and Primates (294 papers), are both better represented in research output than all birds, reptiles, amphibians and fish together (204 papers) for papers covering a single taxonomic class.

Publication output centring on a few species within taxonomic groups that are the focus of research attention is documented (Bautista and Pantoja, 2005 ) and similar reasons are postulated to ones that we cover in our evaluation (i.e., flagship for conservation). These authors also note that fish are an underrepresented group in “wildlife research” and again this echoes our own zoo-focussed findings. Given that aquarium-housed fish can be flagships for conservation research, e.g., McGregor Reid et al. ( 2013 ), there is the potential to build on key traits that make a specific taxa suitable for scientific study to increase its use for research. Increases in species-specific output may be based on active researchers investigating questions on the same taxa because these are considered the most appropriate for that question. However, scientists could consider diversifying the taxa used to ask a similar question. For example, the use of highly-cognitive birds instead of primates for cognition research, facilitating the use of non-mammalian species. Use of cephalopods to determine personality differences (Carere et al., 2015 ) can be a realistic alternative to primate studies given the complex cognition of these invertebrates (Mather and Dickel, 2017 ) that involves both short- and long-term learning and engagement in behaviours such as play.

However, we should also be mindful of the importance of knowledge gaps (e.g., the achievement of optimal welfare) for all captive species, regardless of taxonomic class and therefore zoos should actively engage in directed scientific research to answer key applied questions. A lack of background knowledge on such species, hampering effective evaluation of any results generated, may be causing researchers to choose more familiar species as study models. When considering zoo-specific and open access publications (Fig. S2, Supplementary information) there is an overall predominance of mammalian-research noted, even when annual volumes are themed around a particular taxa, such as freshwater fish (McGregor Reid, 2013 ), or area of work, such as reintroduction and translocation practice (Gilbert and Soorae, 2017 ).

The continuing decline in biodiversity is resulting in zoos providing care for species with a limited to non-existent captive history. Science has a role to play in informing practice for these species if species conservation initiatives are to be successful. Zoos and aquariums are unique in their capacity to provide direct conservation action to threatened species across the globe (Michaels et al., 2014 , Biega et al., 2019 ), and it is encouraging to see that many zoo research projects already focus on conservation breeding and the wider role of animals in ecosystem health. Zoo studies currently are used to better inform conservation projects for animals in situ (da Silva et al., 2019 , Lacy, 2019 ) and this trend is likely to continue into the future. The success of in-situ conservation initiatives can be hindered by a lack of evidence (Reichhardt, 1999 , Schwartz, 2008 ) and therefore decisions that influence population management, breeding recommendations and similar measures to conserve biological diversity ex situ must have an evidence basis to them.

The Convention on Biological Diversity (2020) is currently developing a post-2020 global biodiversity framework, which will aim to address the key drivers of extinction (CBD, 2019 ). A key area for future focus is the relatively poor representation of amphibians, both in zoo collection plans, and also in the research output. Zoos appear to be housing relatively few species of amphibians. In relation to biodiversity and conservation, there are over 7900 amphibian species, and roughly 40% of these species are threatened with extinction (IUCN, 2019 ). While some animal collections have produced excellent conservation education strategies centred around amphibians (Pavajeau et al., 2008 ), it is clear there is room for development of collection plans for these species. It may be difficult for visitors to appreciate the diversity of threatened amphibians if few are represented in captivity (Michaels et al., 2014 b).

Because zoological collections have the responsibility of maintaining populations of highly endangered species, prioritising research into areas of population sustainability, educational initiatives and human behaviour change, can help inform the overall conservation plan for species at the brink of extinction. Whilst our results show that current conservation and ecosystem health output appears low, there is evidence that the quantity of research output is growing. This range of publications has value for those engaged in direct conservation action, as well as to educators disseminating information to zoo visitors and beyond.

It is interesting to note that the best represented animals in our dataset also appear to be some of the favourite animals of zoo visitors (Carr 2016 ). Primates, carnivores and elephants are well-represented in the public’s top ten favourite animals (Courchamp et al., 2018 ) and whilst it is beyond the scope of this paper to determine why these animals appear to feature in both public interest and in zoo literature, we do suggest that public interest could act as a driver for research focus on this species (i.e., to better inform practice and scrutinise the extent to which species are presented to visitors). We do not suggest “less primates” in the output from zoos but more focus on other taxa, as well as the continuation of high levels of research on traditional study species. We would encourage researchers to consider their choice of study population carefully and think about other benefits to their research. It might be intriguing to study chimpanzees but is there more added conservation, education and recreational value if the waxy monkey frog (Phyllomedusa sauvagii) was studied instead…?

In conclusion, our results demonstrate that, globally, zoo-themed researchers have an impressive scientific output and are investigating a range of empirical, hypothesis-driven questions that relate to all the modern zoo’s key roles. Between 2009 and 2018, considerable progress has been made regarding the number of zoo-based publications, especially papers focussed on welfare assessment or improvement. Our results show that there remains a mismatch between the number of species within a taxonomic class held in captivity and the representation of this class in the peer-reviewed literature. Whilst it is relevant that some charismatic species are receiving considerable publication interest, further focus on species that are less represented in literature would help the zoological community to develop welfare indicators and evidence-based husbandry more rapidly for a wider range of taxa. The research output of zoological collections is worthwhile, not only for those working within the industry, but also for those working in other capacities with wild animals and in related disciplines (e.g., academia). As such, progress in increasing the number of questions being posed and output of answering such questions, both within and beyond the zoo, has value to people and animals worldwide.

Data availability

The dataset on publications gathered from scientific databases is available at Open Research Exeter: https://ore.exeter.ac.uk/repository/handle/10871/39092 . The dataset generated on species holdings are not publicly available due to this project still be researched but are available from author James E. Brereton upon reasonable request.

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Acknowledgements

We thank A. Loader for her help with compiling data from JZAR and the IZYB. We thank S. Bereton for assistance with the global species holdings dataset. The open access publication charge was covered by the University of Exeter’s Institutional APC Fund.

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Rose, P.E., Brereton, J.E., Rowden, L.J. et al. What’s new from the zoo? An analysis of ten years of zoo-themed research output. Palgrave Commun 5 , 128 (2019). https://doi.org/10.1057/s41599-019-0345-3

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DOI : https://doi.org/10.1057/s41599-019-0345-3

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Zoology is the branch of science dealing with the study of animals and their structure, behavior, and evolutionary relationships. Zoologists play a key role in understanding the behavior and physiology of animals, as well as the impact of humans on the environment. Zoologists use their knowledge to help conserve biodiversity, develop sustainable management practices for species and habitats, and study disease epidemiology and transmission dynamics in domestic and wild animals. Zoologists also apply their knowledge to the development of medical treatments, such as antibiotics and vaccines. Zoology is increasingly becoming important due to the rapid decline of animal species due to human activities such as overfishing, habitat destruction, pollution, climate change and more. By understanding the structure, behavior, and biology of animals, zoologists can make a contribution to the conservation of the environment, and to the wellbeing of human health.

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