Journal of Zoology

Cover image for Vol. 299 Issue 3

Early View (Online Version of Record published before inclusion in an issue)

Edited By: Nigel Bennett (Editor-in-Chief), Matt Hayward, Andrew Kitchener, Mark-Oliver Roedel, Jean-Nicolas Volff, Gabriele Uhl. Reviews Editor: Trish Fleming

Impact Factor: 1.819

ISI Journal Citation Reports © Ranking: 2015: 33/160 (Zoology)

Online ISSN: 1469-7998

Associated Title(s): Animal Conservation, International Zoo Yearbook, Remote Sensing in Ecology and Conservation

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  1. Original Articles

    1. Predation risk between cannibalistic aeshnid dragonflies influences their functional response on a larval salamander prey

      T. L. Anderson

      Version of Record online: 25 JUL 2016 | DOI: 10.1111/jzo.12376

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      Non-consumptive effects among predators influence both predator and prey populations. I evaluated how such effects impact predator functional response among cannibalistic larval dragonflies foraging on salamander prey. Dragonflies exhibited a Type II functional response, but in the presence of a larger conspecific, foraging rates were depressed at higher prey densities.

    2. Health assessment of grey mullet Mugil cephalus based on interrelationship between parasite co-infections and relative condition factor

      A. Özer, E. Çankaya and D. Yılmaz Kırca

      Version of Record online: 25 JUL 2016 | DOI: 10.1111/jzo.12371

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      We here addressed the question of whether co-infections by multiple pathogenic parasites alter the well-being of a commercially important mugilid species, M. cephalus, using the relative condition factor as a measure. Distinctively from the early studies which have largely focused on the parasite fauna identification, ecology or individual parasitic effects, this study here first attempts to evaluate interspecific differences in infection levels and seasonal patterns of co-infections by taking prevalences, mean intensities and log-ratios of relative abundances into account. Results showed that the majority of ectoparasites were positively correlated with the condition, their interraction with endoparasites however caused alteration in the health status of M. cephalus, revealing some specific interrelationship of these two parasite categories.

    3. Energetic consequences of time-activity budgets for a breeding seabird

      P. M. Collins, L. G. Halsey, J. P. Y. Arnould, P. J. A. Shaw, S. Dodd and J. A. Green

      Version of Record online: 25 JUL 2016 | DOI: 10.1111/jzo.12370

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      We deployed accelerometers on breeding kittiwakes to investigate how they allocate time to different behaviours and what the energetic consequences of variation in time allocation to behaviour might be. We provide evidence for higher energy expenditure in chick-rearing birds when compared to incubating birds, as well as evidence of behavioural compensation to limit overall energy expenditure.

    4. Baiting for carnivores might negatively affect capture rates of prey species in camera-trap studies

      D. G. Rocha, E. E. Ramalho and W. E. Magnusson

      Version of Record online: 19 JUL 2016 | DOI: 10.1111/jzo.12372

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      Baits have been used to increase carnivore capture rates in many camera-trap surveys as low capture rates can preclude detailed analyses. Here, we test the effect of one carnivore bait type on the capture rates of carnivores and prey species in a camera-trap survey in the Central Brazilian Amazon. We also test if the quality of records of naturally marked felids for individual identification is enhanced by the use of bait. We found that the bait had no apparent effect on the carnivore capture rates, but it might have repelled some prey species. Moreover, the use of baits did not result in practical advantages for felid individual identification.

    5. Effect of natural brood size variability on growth and survival of thornbird nestlings

      M. J. Saravia-Pietropaolo, D. E. Manzoli, L. R. Antoniazzi, M. A. Quiroga and P. M. Beldomenico

      Version of Record online: 19 JUL 2016 | DOI: 10.1111/jzo.12368

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      This study showed the natural strategy of two thornbirds species regarding brood size, and therefore, the effect of natural variability in this trait on the development and survival of nestlings. Several factors that were considered potential confounders or effect modifiers were recorded and included in the statistical analysis. We found a positive effect of brood size on growth, and a negative effect on survival. Both of these effects appeared to depend on the context. Our results suggest that the brood size of thornbirds that inhabit central Argentina in part reflects the aptitude of the parents to embark on breeding. In the populations studied, it is advantageous to have brood size variability to anticipate the unpredictable circumstances that will prevail along the breeding season.

    6. Heterochronic neuromuscular junction development in an Australian marsupial (Macropus fuliginosus)

      S. J. Etherington, I. H. K. Hong, C. J. W. Wong, N. Stephens and N. M. Warburton

      Version of Record online: 26 JUN 2016 | DOI: 10.1111/jzo.12367

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      The present work documents the mature form of the neuromuscular junction (NMJ) in the western gray kangaroo and demonstrates that NMJ formation in the forelimbs of kangaroos precedes that in hindlimbs by several weeks. Forelimb and hindlimb NMJs reach a similar level of development by the end of the first postnatal month, an outcome that results from accelerated hindlimb development in the early postnatal period together with a more unexpected stagnation or even regression of forelimb NMJ maturity over the same period.

    7. Decrease in tooth count in melon-headed whales

      N. Kurihara, M. Amano and T. K. Yamada

      Version of Record online: 26 JUN 2016 | DOI: 10.1111/jzo.12363

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      A total of 62 skulls from two herds of melon-headed whales stranded on Japanese coasts were examined. Although they originally have around 22 teeth in each tooth row, older specimens (30–35 years old) possessed only an average of 9.2 teeth on each side of the upper jaw. The ontogenetic decrease in tooth count coincides with the tendency of evolutionary tooth number reduction in odontocetes at two particular points, the secondary reduction from polyodontia and the more progressed decrease in teeth in the upper jaw than in the lower jaw. Therefore, the evolutionary tooth count reduction seems to be repeated in the lifetime of the melon-headed whale.

    8. Clarifying habitat niche width using broad-scale, hierarchical occupancy models: a case study with a recovering mesocarnivore

      R. J. Moll, K. Kilshaw, R. A. Montgomery, L. Abade, R. D. Campbell, L. A. Harrington, J. J. Millspaugh, J. D. S. Birks and D. W. Macdonald

      Version of Record online: 26 JUN 2016 | DOI: 10.1111/jzo.12369

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      Evaluations of wide-ranging species’ habitat niche width require broad-scale, quantitatively rigorous approaches, but these are often lacking, especially for species of lesser conservation concern. We present a case study of how a broad-scale, hierarchical occupancy model, based on data collected across Scotland from 526 camera traps, can be used to update the habitat niche width of a recovering mesocarnivore. Given the dual ubiquity of camera trapping and hierarchical modeling, our approach could be applied in a variety of settings to accurately position species on the generalist–specialist continuum, which in turn can guide conservation action.

    9. Toxic hydrogen sulphide shapes brain anatomy: a comparative study of sulphide-adapted ecotypes in the Poecilia mexicana complex

      T. Schulz-Mirbach, C. Eifert, R. Riesch, M. S. Farnworth, C. Zimmer, D. Bierbach, S. Klaus, M. Tobler, B. Streit, J. R. Indy, L. Arias-Rodriguez and M. Plath

      Version of Record online: 22 JUN 2016 | DOI: 10.1111/jzo.12366

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      The teleost brain is an energetically costly organ. This raises the questions of how brain anatomy is shaped by divergent ecological factors in contrasting (extreme/resource-limited vs. benign) environments, and how shared (‘convergent’) anatomical changes of the teleost brain are reflected in species that transitioned several times along a replicated, natural toxicity gradient. We therefore compared ecotypes in the P. mexicana species complex that have independently evolved increased tolerance to hydrogen sulphide (H2S) in three river drainages in southern Mexico. We found shared and unique patterns of brain size variation; habitat type, and to a lesser degree drainage system of origin and sexual dimorphism, affected the size of the brain, the brain regions and eye diameter. Turbidity and toxicity in sulphidic habitats may explain patterns of brain size divergence. Nonetheless, some unique patterns of brain differentiation suggest as yet unidentified differences in selection regimes between different sulphidic springs.

    10. Anthropogenic food resources foster the coexistence of distinct life history strategies: year-round sedentary and migratory brown bears

      G. Cozzi, M. Chynoweth, J. Kusak, E. Çoban, A. Çoban, A. Ozgul and Ç. H. Şekercioğlu

      Version of Record online: 22 JUN 2016 | DOI: 10.1111/jzo.12365

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      To cope with novel and constantly changing environments, cognitively complex species may develop plastic strategies, which can result in the establishment of distinct alternative behaviors and life history strategies within a population. We identified two remarkably distinct behavioral types: bears that regularly visited a garbage dump and remained sedentary year-round and bears that never visited the dump and migrated 165.7 ± 20.1 km prior to hibernation to search for food. Our study shows that anthropogenic food resources can influence food habits, which can have cascading effects on movement patterns and hence habitat selection, ultimately resulting in the establishment of distinct behavioral types within a population. Identification and consideration of observed variation in behavioral types is fundamental for the correct implementation of evidence-based conservation strategies. Failures to detect such differences could result in the erroneous allocation of limited conservation resources, such as setting aside portions of land characterized by landscape features that are critical to only particular behavioral types.

    11. Cellular basis of anti-predator adaptation in a lizard with autotomizable blue tail against specific predators with different colour vision

      T. Kuriyama, G. Morimoto, K. Miyaji and M. Hasegawa

      Version of Record online: 19 JUN 2016 | DOI: 10.1111/jzo.12361

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      The shades of blue colour in the tails of juvenile lizards, which likely serve to deflect predator attacks toward the autotomizable tail rather than the lizard's body, vary across populations, most notably among those island populations with different predator assemblages. Lizard tails with vivid blue reflectance evolved in communities with either weasel or snake predators, which have the ability to detect blue wavelengths. However, a cryptic brown tail evolved independently on the islands where birds are the primary lizard predator. We also determined through TEM that thickness of light reflecting platelets in iridophores, and densities of iridophores and xanthophores, predicted the wavelengths and intensity of light reflected by the lizard tail.

    12. Biogeography of polymorphic phenotypes: Mapping and ecological modelling of coat colour variants in an elusive Neotropical cat, the jaguarundi (Puma yagouaroundi)

      L. G. da Silva, T. G. de Oliveira, C. B. Kasper, J. J. Cherem, E. A. Moraes Jr, A. Paviolo and E. Eizirik

      Version of Record online: 16 JUN 2016 | DOI: 10.1111/jzo.12358

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      The jaguarundi Puma yagouaroundi is a small Neotropical cat that presents two main coloration phenotypes (grey/dark vs. reddish), whose exact geographic distribution has never been mapped. Based on 566 location records encompassing the entire historical range of the species, we mapped and produced a habitat suitability model for each of these phenotypes. The frequency of grey/dark jaguarundis was c. 80%, while that of reddish animals was c. 20%. The spatial distribution of grey/dark animals was approximately random, whereas that of the reddish form was significantly non-random. Grey/dark animals were significantly associated with moist and dense forests, while reddish forms were associated with dry and open areas. Furthermore, there were clear spatial differences between the suitability models of these phenotypes. We observed that environmental predictors related to moisture were especially influential on the differences between the models. These results support an effect of natural selection on the distribution of coloration traits.

  2. Reviews

    1. The need for new categorizations of dietary specialism incorporating spatio-temporal variability of individual diet specialization

      E. Pagani-Núñez, C. A. Barnett, H. Gu and E. Goodale

      Version of Record online: 13 JUN 2016 | DOI: 10.1111/jzo.12364

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      Recently, the use of the terms generalism and specialism have been under debate. In this review, we show that this categorization cannot capture the complexity found in nature using two avian species, great and blue tits, as models. We argue that diet specialization varies geographically and temporally. Moreover, we suggest that great tits can be considered generalists at the species level and specialists at the individual level, while blue tits can be considered generalists at both the species and the individual level. Therefore, we propose that label ‘generalists’ should distinguish between facultative generalists, which can develop new specializations, and obligate generalists, which have a limited capacity to develop novel specializations.

  3. Original Articles

    1. The moon cycle effect on the activity patterns of ocelots and their prey

      L. P. Pratas-Santiago, A. L. S. Gonçalves, A. M. V. da Maia Soares and W. R. Spironello

      Version of Record online: 9 JUN 2016 | DOI: 10.1111/jzo.12359

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      We assessed the temporal activity patterns of ocelots and their prey. We found that the activity of ocelots greatly overlapped that of their nocturnal prey and that the overlap was even higher than with diurnal prey during full moon. We therefore suggest that during full moon, ocelots have greater hunting efficiency and they switch the type of their prey (i.e. nocturnal), and that the foraging benefits outweigh the risk of being exposed to larger competitors in brighter nights.

    2. Thermal constraints and the influence of reproduction on thermoregulation in a high-altitude gecko (Quedenfeldtia trachyblepharus)

      A. Bouazza, T. Slimani, H. El Mouden, G. Blouin-Demers and O. Lourdais

      Version of Record online: 9 JUN 2016 | DOI: 10.1111/jzo.12353

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      Cold climates are particularly challenging for ectothermic animals because thermal conditions constrain physiological performance and activity. The Atlas Day Gecko, Q. trachyblepharus, is the only Mediterranean gecko specialized in high mountain habitats. We demonstrated that this species has high thermal preferences and that gravid females thermoregulate more precisely compared to males and non-gravid females.

    3. Non-random accumulation of LINE1-like sequences on differentiated snake W chromosomes

      M. Mezzasalma, V. Visone, A. Petraccioli, G. Odierna, T. Capriglione and F. M. Guarino

      Version of Record online: 5 JUN 2016 | DOI: 10.1111/jzo.12355

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      This study provides evidence of the scarce presence and the recent origin of LINE1 sequences in squamate genomes, and evidence a non-random, preferential accumulation of these sequences in highly heterochromatic W sex chromosomes. Our data also highlight a similar, convergent, distribution pattern of L1 retroposons on vertebrate sex chromosomes when their differentiation takes place through heterochromatinization events.

    4. Territory selection in the city: can birds reliably judge territory quality in a novel urban environment?

      P. Minias and T. Janiszewski

      Version of Record online: 3 JUN 2016 | DOI: 10.1111/jzo.12362

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      We found convincing evidence that territory choice of Eurasian coots from a newly established urban population was adaptive, as birds preferred territories which maximized their reproductive success. In contrast, coots were not able to reliably assess food availability in a novel urban environment due to either poor temporal predictability of anthropogenic food resources or due to disregarding anthropogenic food during territory selection because of its novelty.

    5. Ontogenetic bite-force modeling of Alligator mississippiensis: implications for dietary transitions in a large-bodied vertebrate and the evolution of crocodylian feeding

      P. M. Gignac and G. M. Erickson

      Version of Record online: 31 MAY 2016 | DOI: 10.1111/jzo.12349

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      On the basis of performance measurements, gross dissection and musculoskeletal modeling of the crocodylian jaw adductor system, we found that the anatomy of bite-force generation in the American alligator is broadly applicable to crown Crocodylia and reflects an important, but often overlooked, aspect of the crocodylian feeding ecomorphology: littoral, sit-and-wait predation is enhanced by posteroventrally displaced, exceptionally large and forceful ventral pterygoideus muscles, in particular.

    6. Comparative assessment of metrics for monitoring the body condition of polar bears in western Hudson Bay

      L. Sciullo, G. W. Thiemann and N. J. Lunn

      Version of Record online: 25 MAY 2016 | DOI: 10.1111/jzo.12354

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      We assessed multiple metrics of body condition in polar bears Ursus maritimus in western Hudson Bay with particular focus on bioelectrical impedance analysis (BIA) and its feasibility in the field. We also monitored body condition across a broad temporal scale (2004–2013) in conjunction with sea ice breakup and freeze-up date. Although BIA found similar patterns across age and sex class as other established metrics, this method had several limitations when used in the field and may not be as efficient as other modelled metrics that require only morphological measurements (i.e., energy density). We also found body condition to decline across a broad temporal scale in adult and subadult males and females, suggesting a potential link to fluctuations in sea ice habitat. This highlights the importance of continuous monitoring of polar bear body condition and allows for better understanding of the interaction between environmental change and species response in the Arctic.

    7. Small, rare and trendy: traits and biogeography of lizards described in the 21st century

      S. Meiri

      Version of Record online: 24 MAY 2016 | DOI: 10.1111/jzo.12356

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      New lizard species are described with greater pace than ever before. In this study, I examine the traits of newly described lizard taxa, and compare them to those of species described earlier, to predict where new species will be found, what traits they have, and whether they are likely to be more extinction-prone than well-known species. I showed that newly described lizards are more likely smaller, tropical and more threatened than previously described species. This work contributes to predicting what types of species are likely to be found in future and where.

    8. Unleashing the Kraken: on the maximum length in giant squid (Architeuthis sp.)

      C. G. M. Paxton

      Version of Record online: 17 MAY 2016 | DOI: 10.1111/jzo.12347

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      Statistical investigation of various measures of body length and beak size in Architeuthis suggests that giant squid of at least 2.69 m (99.9% prediction interval: 1.60–3.83 m) mantle length (ML) may be handled by large bull sperm whales but perhaps not females. Given the relationship of squid ML to standard (from tip of mantle to end of arms) and total (from tip of mantle to end of tentacles) length, the observed spread of individual lengths, along with a longest reliably measured ML of 2.79 m, purported squid of 10 m standard length and even 20 m total length are eminently plausible.

    9. Morphology of the nucho-dorsal glands and related defensive displays in three species of Asian natricine snakes

      A. Mori, T. Jono, H. Takeuchi, L. Ding, A. de Silva, D. Mahaulpatha and Y. Tang

      Version of Record online: 16 MAY 2016 | DOI: 10.1111/jzo.12357

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      We describe the detailed morphological features of unique defensive organs, called mucho-dorsal glands, in three species of Asian natricine snakes, Rhabdophis nuchalis, R. pentasupralabialis and Macropisthodon plumbicolor. We also report a novel display, body lift, which is considered to enhance the defensive function of the glands. Correlated evolution of these morphological and behavioural traits are discussed.

    10. Reevaluating geographic variation in life-history traits of a widespread Nearctic amphibian

      J. M. Davenport and B. R. Hossack

      Version of Record online: 13 MAY 2016 | DOI: 10.1111/jzo.12352

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      Body size can vary across climatic gradients and this variation can have implications for reproduction. We found that wood frog adult size and egg size decrease as latitude increases and mean annual temperature decreases. This implies that a limit to adaptation may exist for some populations which is important as accelerating climate change will expose populations to novel environmental conditions.

    11. Virtual plaster cast: digital 3D modelling of lion paws and tracks using close-range photogrammetry

      A. F. J. Marchal, P. Lejeune and P. J. N. de Bruyn

      Version of Record online: 5 MAY 2016 | DOI: 10.1111/jzo.12342

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      The ecological monitoring of threatened species is vital for their survival as it provides the baseline for conservation, research and management strategies. Wildlife studies using tracks are controversial mainly due to unreliable recording techniques limited to two dimensions (2D). We assess close-range photogrammetry as a low-cost, rapid, practical and reliable field technique for the digital three-dimensional (3D) modelling of lion Panthera leo paws and tracks.

    12. Evolutionary history and conservation significance of the Javan leopard Panthera pardus melas

      A. Wilting, R. Patel, H. Pfestorf, C. Kern, K. Sultan, A. Ario, F. Peñaloza, S. Kramer-Schadt, V. Radchuk, D. W. Foerster and J. Fickel

      Version of Record online: 3 MAY 2016 | DOI: 10.1111/jzo.12348

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      The leopard Panthera pardus is widely distributed across Africa and Asia; however, there is a gap in its natural distribution in Southeast Asia, where it occurs on the mainland and on Java but not on the interjacent island of Sumatra. We used mtDNA sequences and Pleistocene distribution modelling of leopards to gain further insights into the evolutionary history of leopards in Southeast Asia. Our data confirmed that Javan leopards are evolutionarily distinct from other Asian leopards, and that they have been present on Java since the Middle Pleistocene. Our study therefore emphasizes the need for greater conservation efforts for this critically endangered leopard subspecies, as its extinction would greatly reduce the natural diversity of leopards.

    13. Experiments on ostrich decomposition and opisthotonus with implications for theropod dinosaurs

      T. Lingham-Soliar

      Version of Record online: 3 MAY 2016 | DOI: 10.1111/jzo.12345

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      To investigate decomposition and the opisthotonic posture in fossils, ostrich cadavers were allowed to decompose in a natural environment over 120 h with fly maggots – the primary agent of decay. In two of the severely degraded cadavers, considerable retraction of the neck occurred although not classic opisthotonus. In the cadaver partially submerged in a natural pool of water, classic opisthotonus occurred. The study has implications for the famous small Chinese theropod dinosaur, Sinosauropteryx (so-called ‘feathered dinosaur’).

    14. Polyploid unisexual salamanders have higher tissue regeneration rates than diploid sexual relatives

      M. J. Saccucci, R. D. Denton, M. L. Holding and H. L. Gibbs

      Version of Record online: 28 APR 2016 | DOI: 10.1111/jzo.12339

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      Understanding phenotypic differences between polyploid and diploid competitors can help illuminate the drivers of coexistence within these communities. We compare a biologically relevant trait (tail regeneration rate) between an all-female polyploid lineage of salamander and a closely related diploid species. Similar to other polyploid taxa, polyploid salamanders regenerate tail tissue at approximately twice the rate of a sympatric diploid species.

    15. Incubation temperature affects development order of morphological features and staging criteria in turtle embryos

      J. Dormer, J. M. Old, J. U. Van Dyke and R.-J. Spencer

      Version of Record online: 27 APR 2016 | DOI: 10.1111/jzo.12346

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      We tested the effects of temperature on embryological development in a turtle. We found that incubation temperature impacts the order of development of morphological features. This has potential to complicate the use of published embryological staging series.

    16. Sticklebacks show consistent prey share hierarchies within but not between patchy and sequential prey distributions

      D. E. F. Taylor, D. Cownden and M. M. Webster

      Version of Record online: 25 APR 2016 | DOI: 10.1111/jzo.12350

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      If the outcome of prey competition under different conditions is dependent upon different sets of attributes, then we may expect to see domain-specific prey share hierarchies emerge. Here, we report that within shoals of sticklebacks Gasterosteus aculeatus individual prey share was correlated across pairs of patch- and pairs of drift-foraging trials, but not between the two conditions, suggesting that separate repeatable but independent prey share hierarchies do indeed arise for each type of prey distribution.

    17. Sexual dimorphism and physiological correlates of horn length in a South African isopod crustacean

      D. S. Glazier, S. Clusella-Trullas and J. S. Terblanche

      Version of Record online: 20 MAR 2016 | DOI: 10.1111/jzo.12338

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      The dorsal horns of the South African horned isopod Deto echinata are significantly longer and scale with body size more steeply in adult males than in adult females and juveniles. Body-length adjusted correlations of male horn length with body condition and resting metabolic rate are consistent with the hypothesis that the sexual dimorphism of horn length in D. echinata is the result of sexual selection and that horn length is a reliable indicator of the ability of a male to acquire and process resources, which in turn may be critical to female mate choice and (or) male-male competition for mates. However, this hypothesis requires further testing based on direct observations of female mate choice and male-male behavioral interactions, which have not yet been carried out.

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