Abstract View

Bo Zhao, Teng Li, Richard Shine, and Wei-Guo Du
Turtle embryos move to optimal thermal environments within the egg
Biol. Lett. August 23, 2013 9 4 20130337; doi:10.1098/rsbl.2013.0337 1744-957X

A recent study demonstrated that the embryos of soft-shelled turtles can reposition themselves within their eggs to exploit locally warm conditions. In this paper, we ask whether turtle embryos actively seek out optimal thermal environments for their development, as do post-hatching individuals. Specifically, (i) do reptile embryos move away from dangerously high temperatures as well as towards warm temperatures? and (ii) is such embryonic movement due to active thermoregulation, or (more simply) to passive embryonic repositioning caused by local heat-induced changes in viscosity of fluids within the egg? Our experiments with an emydid turtle (Chinemys reevesii) show that embryos avoid dangerously high temperatures by moving to cooler regions of the egg. The repositioning of embryos is an active rather than passive process: live embryos move towards a heat source, whereas dead ones do not. Overall, our results suggest that behavioural thermoregulation by turtle embryos is genuinely analogous to the thermoregulatory behaviour exhibited by post-hatching ectotherms.

Tengfei Li, Baoping Ren, Dayong Li, Pingfen Zhu, Ming Li
Mothering Style and Infant Behavioral Development in Yunnan Snub-Nosed Monkeys (Rhinopithecus bieti) in China
International Journal of Primatology, June 2013

Considerable variation in mothering styles is found among primate species, which may be directly related to species-typical differences in social structure, dominance style, patterns of infant development, and rates of intragroup aggression. We predicted that, as egalitarian Asian colobines, mothers of Yunnan snub-nosed monkeys (Rhinopithecus bieti) would adopt a mothering style characterized by low restrictiveness and low rejection. We followed six mother–infant dyads in a provisioned group of Rhinopithecus bieti inhabiting the Baimaxueshan National Nature Reserve, Yunnan, China, and collected 717.2 h of observational data on maternal care and infant development. In the first month after birth, infants were completely dependent on their mothers for nutrition and movement. They began to locomote clumsily during their second month of life. Mothers restricted the movements of their infants only during their first 2 mo of life. Maternal rejection occurred infrequently and never exceeded a mean of two events per hour for a given infant over any 1-mo period. Most rejections were mild, and did not result in a cessation of nursing. Infants were not weaned when they were 12 mo old. Our study offers support for the contention that females of Rhinopithecus bieti adopt a relaxed mothering style in caring for offspring during their first year of life.

Robert Maslak, Agnieszka Sergiel, Sonya P. Hill, Some aspects of locomotory stereotypies in spectacled bears (Tremarctos ornatus) and changes in behavior after relocation and dental treatment, Journal of Veterinary Behavior: Clinical Applications and Research, Available online 15 June 2013, ISSN 1558-7878, http://dx.doi.org/10.1016/j.jveb.2013.05.004.
The behavior of 2 spectacled bears (Tremarctos ornatus) was studied at Wroclaw Zoo (Poland), where they were housed in a very small outdoor enclosure, and then in a separate study after transfer to a large naturalistic exhibit at Chester Zoo (CZ; United Kingdom). The studies combine to form an opportunistic “experiment” on the effects of transfer on zoo animals. This situation provided a unique opportunity for a closer investigation of known behavior problems and their causation. In part 1 of the study, at Wroclaw Zoo, the median amount of time devoted to stereotypical movements was 57 min/h. After the move to CZ, immediate changes in behavior were reported in 1 individual, for whom the stereotypy was eradicated. The other bear continued performing repetitive behavior of high intensity and only used a small area of the large enclosure. Signs of dental problems were subsequently observed in both bears, and so a dental examination was carried out, resulting in multiple extractions. After treatment, the amount of time that the bear with ongoing behavior problems spent stereotyping reduced significantly, and foraging increased. Our data suggest the bears‘ stereotypic behavior occurred not only in response to an understimulating environment in their old enclosure but also perhaps in association with medical conditions in one of the bears. Although other factors could have contributed to the observed reduction in stereotypy, it is clear that further investigation is needed into the effects of pain and physical condition on stereotypy in animals.

Côté, S. D., Hamel, S., St-Louis, A. and Mainguy, J. (2013)
Do mountain goats habituate to helicopter disturbance?
The Journal of Wildlife Management. doi: 10.1002/jwmg.565

Helicopter flights may affect wildlife, but habituation to disturbance is possible. We tested the hypothesis that mountain goats in a population exposed to helicopter flights for over 40 years have habituated to helicopter traffic. We contrasted behavioral responses of marked mountain goats to helicopter flights during 2 time periods (1995 vs. 2005–2009). The proportions of helicopter flights resulting in no/light, moderate, or strong disturbance were similar in 1995 and 2005–2009. Horizontal distance was the main factor determining mountain goat responses to helicopter flights; goats had a very high probability (>0.8) of being moderately and strongly disturbed (moderate: moved 10–100 m, alert for 2–10 min; strong: ran >100 m, alert for >10 min) when they were approached within 500 m by helicopters. We found that mountain goats only very slightly habituated to helicopter flights during a period of 10–15 years of repeated helicopter traffic. Because disturbance from helicopter flights has remained high, and in view of the continuous increase of helicopter traffic in mountainous habitat, we recommend helicopter flights do not approach closer than 1,500 m from mountain goat groups.

Britton, Adam R. C., Britton, Erin K., and McMahon, Clive R. (2013) Impact of a toxic invasive species on freshwater crocodile (Crocodylus johnstoni) populations in upstream escarpments. Wildlife Research ,

Spread of the invasive cane toad (Rhinella marina) across northern Australia is of concern. Predator species, including the freshwater crocodile (Crocodylus johnstoni), are susceptible to cane toad toxins when ingested. Upstream populations of freshwater crocodiles are smaller than downstream counterparts because of limited resources. We measured the impact of cane toad arrival on densities of these upstream populations.
Our aim was to determine whether the influx of cane toads had a negative impact on populations of upstream ‘stunted’ freshwater crocodiles.
Population surveys for crocodiles were conducted in three upstream creek systems, using day- and night-based survey methods, before the arrival of cane toads in the area. These surveys were repeated under similar conditions following the arrival of cane toads, to compare the distribution and densities of freshwater crocodiles and, hence, measure the impact of cane toads.
There were significant declines in crocodile density at two survey sites following the arrival of cane toads, and we found dead crocodiles and cane toad carcasses with crocodile bite marks. The third site showed no change in density. There was a decline in mean density across all sites from 3.0 crocodiles km–1 to 1.1 crocodiles km–1 following the arrival of cane toads.
There was an overall decrease in crocodile densities and a reduction in distribution following the arrival of cane toads into the survey area. Dead crocodiles and evidence of their having eaten cane toads strongly suggest that these declines were caused directly by the arrival of cane toads into the area. One site showed no apparent change other than an increase in wariness, which may reflect the distribution of available feeding and shelter resources among the three sites.
These results suggest that upstream freshwater crocodile populations are highly susceptible to cane toad toxins, and that impacts on their population can include local extirpation. Considering their morphological and possibly genetic distinctiveness, the loss of these unique populations is of conservation concern.

Lowther, A. D., Harcourt, R. G., and Goldsworthy, S. D. (2013) Regional variation in trophic ecology of adult female Australian sea lions inferred from stable isotopes in whiskers. Wildlife Research ,

The primary selective forces responsible for shaping life-history traits come from the physical and biological environment in which a species resides. Consequently, the limits of a species range may provide a useful measure of adaptive potential to environmental change. The proximity of foraging grounds to terrestrial nursing habitat constrains central-place foragers such as otariid seals in selecting breeding locations. The Australian sea lion (Neophoca cinerea) is an endangered otariid endemic to Australia, whose northern-range extent occurs at a temperate–tropical transition zone on the western coast of Western Australia (WA).
Currently, there is a complete absence of data on the foraging ecology of Australian sea lions in WA. We sought to address this critical knowledge gap and provide data on the foraging ecology of adult female Australian sea lions at three isolated breeding colonies in western WA.
We used stable-isotope ratios of carbon (δ13C) and nitrogen (δ15N) in the whiskers of pups as proxies to characterise feeding behaviour of 10–28% of all adult female Australian sea lions at each colony. We then compared these geographic data to (1) conspecifics at similar latitude in South Australia (SA) and (2) isotopic data collated from other studies on seabirds that inhabit the region, to place foraging behaviour of adult female Australian sea lions into context.
At the southernmost colonies in WA, individual animals were members of one of two distinct isotopic clusters that could be described by differences in δ15N and δ13C values. Individuals at the northernmost colony displayed δ15N values similar to those of seabirds in the same region. Across the study, isotope ratios of adult female Australian sea lions in western WA were between 3‰ and 5‰ lower than those observed at a colony at similar latitude in SA.
Gross differences in the physical oceanography between WA and SA may in part explain the differences in isotope ratios of individuals between the regions, with lower δ15N and δ13C values in WA probably reflecting the relatively depauperate conditions of the Leeuwin Current.
Potential regional differences in trophic structure should be considered when developing appropriate management plans for Australian sea lions and regional variation in the diet of Australian sea lion warrants further investigation.

Carter AW, DuRant SE, Hepp GR, Hopkins WA. 2013. Thermal challenge severity differentially influences wound healing in Wood Duck (Aix sponsa) ducklings. J. Exp. Zool. 9999:000–000.
Environmental conditions during early development can profoundly influence an individual’s phenotype. Development requires simultaneous maturation and orchestration of multiple physiological systems creating the potential for interaction among key systems and requiring substantial resources. We investigated the influence of thermoregulation on immunocompetence in Wood Duck ducklings (Aix sponsa). At both 1 and 2 days post hatch (dph) we evaluated ducklings‘ abilities to thermoregulate during a thermal challenge at one of four temperatures (36 [thermoneutral controls], 20, 10, or 5°C). At 3 dph, ducklings received a superficial wound, which was monitored until full recovery to quantify wound healing ability, an ecologically relevant, integrative measure of immune function. We demonstrated that duckling body temperature decreased with increasing thermal challenge severity, thermoregulatory ability increased with age, and thermoregulation had temperature-dependent effects on the immune system. Specifically, a more severe thermal challenge (5°C) resulted in decreased immune performance when compared to a mild challenge (20°C). We conclude that early thermoregulatory experiences are influential in shaping immune responses early in development. Furthermore, our results emphasize that future studies of environmental stressors need to consider multiple physiological endpoints since interaction among systems can result in competing physiological demands.

WATTS, D. P. and AMSLER, S. J. (2013), ChimpanzeeRed Colobus Encounter Rates Show a Red Colobus Population Decline Associated With Predation by Chimpanzees at Ngogo. Am. J. Primatol.. doi: 10.1002/ajp.22157
Chimpanzees (Pan troglodytes) hunt various primates, but concentrate on red colobus monkeys (Piliocolobus spp.) wherever the two species are sympatric. The extraordinarily large Ngogo chimpanzee community in Kibale National Park, Uganda, preys heavily on the local population of red colobus (P. tephrosceles). Census data showed a steep decline in this population in the center of the chimpanzees‘ home range between 1975 and 2007 [Lwanga et al., 2011; Teelen, 2007b]. Given no obvious change in food availability, predation by chimpanzees was the most likely cause [ibid.; Teelen, 2008]. However, census data from other parts of the home range raised the possibility that the decline was restricted to this central area [Teelen, 2007a] We present data from 1998 to 2012 on the rate of encounters between chimpanzees and red colobus that provide a chimpanzee-centered estimate of red colobus density, thus of predation opportunities, throughout the home range. These corroborate census data by showing a long-term decline in encounters near the center. They also show that encounters become relatively more common at increasing distances from the center, but encounter rates have decreased even in peripheral areas and, by implication, the red colobus population has declined throughout the study area. These data corroborate Teelen’s [2008] conclusion that chimpanzee predation on red colobus during the 1990s and early 2000s was unsustainable. Hunting rates and prey offtake rates have also declined markedly; whether this will allow the red colobus population to recover is unknown. In contrast, rates at which chimpanzees encountered redtail monkeys (Cercopithecus ascanius) and grey-cheeked mangabeys (Lophocebus albigena) did not decrease. Neither did they increase, however, contrary to long-term census data from the center of the study area [Lwanga et al., 2011].

Taeko Miyazaki
Retinal ganglion cell topography in juvenile Pacific bluefin tuna Thunnus orientalis (Temminck and Schlegel)
Fish Physiology and Biochemistry, June 2013

The retinal ganglion cell distribution, which is known to reflect fish feeding behavior, was investigated in juvenile Pacific bluefin tuna Thunnus orientalis. During the course of examination, regularly arrayed cells with a distinctive larger soma, which may be regarded as motion-sensitive cells, were found. The topographical distribution of ordinary-sized ganglion cells, which is usually utilized to estimate fish visual axis and/or visual field characteristics, showed that the highest-density area, termed the area centralis, was localized in the ventral-temporal retina. The retinal topography of ordinary-sized ganglion cells seems to reflect the bluefin tuna’s foraging behavior; while cruising, cells in the area centralis may signal potential prey, such as small schooling pelagic fishes or squids, that are present in the upward-forward direction. Judging from morphological characteristics, the large ganglion cells localized in the small temporal retinal area seem to be equivalent to physiologically categorized off-center Y-cells of cat, which are stimulated by a transient dark spot in a bright visual field. It was inferred that presumed large off-center cells in the temporal retina detect movements of agile prey animals escaping from bluefin tuna as a silhouette against environmental light.

Harriet T. Davies-Mostert, Michael G. L. Mills, David W. Macdonald
Hard Boundaries Influence African Wild Dogs’ Diet and Prey Selection
Journal of Applied Ecology 2013
DOI: 10.1111/1365-2664.12129

Human-mediated changes in habitat structure may disturb predator–prey relationships.We investigated the influence of perimeter fences on the diet of a reintroduced population of African wild dogs Lycaon pictus Temminck 1820 in a 316 km2, fenced reserve in South Africa, by tracking radio-collared individuals during hunting periods to determine dietary composition from observed kills.Nutritional status of impala Aepyceros melampus and kudu Tragelaphus strepsiceros prey, as measured by the percentage of femur marrow fat, was significantly lower than that of unselectively culled individuals. This supports the hypothesis that wild dog predation is at least partially compensatory.Fence-impeded kills (those for which escape was deemed to be compromised by the fence) comprised 40.5% of kills (n=316), and 54.1% of all edible biomass consumed. Compared to fence-unimpeded kills, fence-impeded kills comprised larger species (32.9 kg vs. 25.0 kg, W= 25667.0, P<<0.001), older age classes for one prey category (female kudu: Fisher's Exact Test, P=0.02, n=65), and animals in better condition for adult impala males(Mann-Whitney, W=111.0, P=0.012, n=28).Fence-impeded kills also provided greater catch per unit hunting effort (27.3 kg km−1 vs. 12.2 kg km−1; χ2 = 7.89, P = 0.005), resulting in longer inter-kill intervals. Movement of the pack towards the fence at the start of each hunting period suggested a decision to exploit the advantage that fences conferred for capturing prey.Synthesis and applications. By enabling coursing predators to capture prey that would otherwise have escaped, fences may reduce the compensatory nature of predation, causing shifts in predator–prey dynamics that could influence the ability of small reserves to support such predators. The establishment of larger conservation areas to reduce perimeter-to-area ratios should be encouraged to limit the undesired effects of fences on predator–prey dynamics. Michael J. Beran, Theodore A. Evans, Fabio Paglieri, Joseph M. McIntyre, Elsa Addessi, William D. Hopkins
Chimpanzees (Pan troglodytes) can wait, when they choose to: a study with the hybrid delay task
Animal Cognition June 2013

Self-control has been studied in nonhuman animals using a variety of tasks. The inter-temporal choice (ITC) task presents choices between smaller–sooner (SS) and larger–later (LL) options. Using food amounts as rewards, this presents two problems: (a) choices of the LL option could either reflect self-control or instead result from animals’ difficulty with pointing to smaller amounts of food; (b) there is no way to verify whether the subjects would not revert their choice for the LL option, if given the opportunity to do so during the ensuing delay. To address these problems, we have recently introduced a new protocol, the hybrid delay task, which combines an initial ITC with a subsequent accumulation phase in which selection of the SS option leads to its immediate delivery, but choice of the LL option then leads to one-by-one presentation of those items that continues only as long as the subject does not eat any of the accumulated items. The choice of the LL option therefore only reflects self-control when the number of items obtained from LL choices during the accumulation phase is higher than what could be received in the SS option. Previous research with capuchin monkeys demonstrated that their apparent self-control responses in the ITC task may have overestimated their general self-control abilities, given their poor performance in the hybrid delay task. Here, chimpanzees instead demonstrated that their choices for the LL option in the ITC phase of the hybrid delay task were confirmed by their ability to sustain long delays during accumulation of LL rewards.

Harun Albayrak, Emre Ozan, Abdullah Cavunt
A serological survey of selected pathogens in wild boar (Sus scrofa) in northern Turkey
European Journal of Wildlife Research June 2013

During the hunting season in March 2012, a total of 93 blood samples were collected from wild boars (Sus scrofa) shot in the area of northern Turkey (Samsun and Gumushane provinces). These blood samples were examined by enzyme immunoassay (ELISA) for the presence of antibodies to classical swine fever virus (CSFV), Aujeszky’s disease virus (ADV), porcine reproductive and respiratory syndrome virus (PRRSV), porcine respiratory coronavirus (PRCV), swine influenza virus (SIV), porcine parvovirus (PPV), swine vesicular disease virus (SVDV), hepatitis E virus (HEV), African swine fever virus (ASFV), porcine rotavirus (PRV), transmissible gastroenteritis virus (TGEV) and bovine viral diarrhoea virus (BVDV). Out of 93 serum samples examined, 65 (69.9 %) were positive for PRV, 22 (23.7 %) were positive for ADV, 5 (5.4 %) were positive for BVDV, 4 (4.3 %) were positive for PPV and 2 (2.2 %) were positive for PRRSV. All sera were negative for ASFV, SVDV, HEV, SIV, PRCV, TGEV and CSFV. The results, recorded for the first time in Turkey, supported the hypothesis that wild boar act as a potential reservoir of selected viruses and thus have a role in the epidemiology of these diseases.

Keith A. Hobson, Steven L. Van Wilgenburg, Yves Ferrand, François Gossman, Claudine Bastat
A stable isotope (δ 2H) approach to deriving origins of harvested woodcock (Scolopax rusticola) taken in France
European Journal of Wildlife Research June 2013

A crucial but elusive aspect of the effective conservation and management of migratory birds is the determination of which regions or habitats contribute to the recruitment of juvenile birds into the adult breeding population or, in the case of hunted species, the annual harvest. Although ring recoveries have provided important information for several game species, limitations of this approach include the bias to only marked populations and the tremendous scale of effort required to recover enough individuals. Here, we explored the use of an intrinsic marker, the stable hydrogen isotope composition of feathers (δ2Hf) of juvenile woodcock (Scolopax rusticola), as a means of assigning birds to natal origin using a woodcock-specific δ2Hf isoscape. We applied this approach to 987 juvenile woodcock during the winters of 2005–2006 and 2006–2007, and 1875 juvenile woodcock sampled during autumn migration of 2005 and 2006. We used a likelihood-based assignment approach to determine origins from four regions. Considering only the feather isotope data, the majority (50 %) were assigned to origins in the Baltic—Western European Russia region (including western Russia) and 44 % assigned to central European origins. Few (6 %) were considered residents in France and <1 % were assigned to northern Fennoscandia and northern European Russia. Using the amount of forest cover available within zones as a prior resulted in greater emphasis on origins in the Baltic and western European Russia (62 %) and less emphasis (29 %) on central Europe as a potential origin. We also depicted origins of birds on a continuous isoscape surface which emphasised more extant forests of central and eastern Europe and western Russia. were relatively similar regardless of whether we considered samples collected during migration versus those collected during the wintering period. Spatial assignment of 51 woodcock sampled in Switzerland was consistent with the Baltic and central Europe. Our results are in general agreement with ring-recovery data and emphasise the utility of an isotope approach to assignment of gamebirds to origin. Mariguela, T. C., Alexandrou, M. A., Foresti, F. and Oliveira, C. (2013), Historical biogeography and cryptic diversity in the Callichthyinae (Siluriformes, Callichthyidae). Journal of Zoological Systematics and Evolutionary Research. doi: 10.1111/jzs.12029
The family Callichthyidae, divided into the subfamilies Corydoradinae and Callichthyinae, contains more than 200 species of armoured catfishes distributed throughout the Neotropics, as well as fossil species dating from the Palaeocene. Both subfamilies are very widely distributed throughout the continent, with some species ranges extending across multiple hypothesized biogeographical barriers. Species with such vast geographical ranges could be made up of multiple cryptic populations that are genetically distinct and have diverged over time. Although relationships among Callichthyinae genera have been thoroughly investigated, the historical biogeography of the Callichthyinae and the presence of species complexes have yet to be examined. Furthermore, there is a lack of fossil-calibrated molecular phylogenies providing a time frame for the evolution of the Callichthyinae. Here, we present a novel molecular data set for all Callichthyinae genera composed of partial sequences of mitochondrial and nuclear markers. These data were used to construct a fossil-calibrated tree for the Callichthyinae and to reconstruct patterns of spatiotemporal evolution. All phylogenetic analyses [Bayesian, maximum likelihood and maximum parsimony (MP)] resulted in a single fully resolved and well-supported hypothesis for the Callichthyinae, where Dianema is the sister group of all the remaining genera. suggest that the ancestry of most Callichthyinae genera originated in the Amazonas basin, with a number of subsequent ancestral dispersal events between adjacent basins. High divergences in sequences and time were observed for several samples of Hoplosternum littorale, Megalechis picta and Callichthys callichthys, suggesting that these species may contain cryptic diversity. The results highlight the need for a taxonomic revision of species complexes within the Callichthyinae, which may reveal more diversity within this relatively species-poor lineage.

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