Explosive vocal activity for attracting human attention is related to domestication in silver fox

Domestication affects behavioral and vocal responses, involved in communication with humans; in particular, those that attract human attention. In this study, we found that silver foxes of Tame strain, experimentally domesticated for a few tenses of generation, displayed bursts of vocal activity during the first minute after appearance of an unfamiliar human, that faded quickly during the remaining time of the test, when the experimenter stayed passively before the cage. Distinctively, foxes of Aggressive strain, artificially selected for tenses of generation for aggressive behavior toward humans, and the control group of Unselected for behavior silver foxes kept steady levels of vocal activity for the duration of the tests. We found also that Aggressive foxes vocalized for a larger proportion of time than Unselected foxes for all 5 min of the test. We discuss the obtained data in relation to proposal effects of domestication on mechanisms directed to involving people into human-animal interactions and structural similarity between human laughter and vocalization of Tame foxes.     

Vocalization toward conspecifics in silver foxes (Vulpes vulpes) selected for tame or aggressive behavior toward humans

We examined the production of different vocalizations in three strains of silver fox (unselected, aggressive, and tame) attending three kinds of behavior (aggressive, affiliative, and neutral) in response to their same-strain conspecifics. This is a follow-up to previous experiments which demonstrated that in the presence of humans, tame foxes produced cackles and pants but never coughed or snorted, whilst aggressive foxes produced coughs and snorts but never cackled or panted. Thus, cackle/pant and cough/snort were indicative of the tame and aggressive fox strains respectively toward humans. Wild-type unselected foxes produced cough and snort toward humans similarly to aggressive foxes. Here, we found that vocal responses to conspecifics were similar in tame, aggressive and unselected fox strains. Both cackle/pant and cough/snort occurred in foxes of all strains. The difference in the use of cackle/pant and cough/snort among these strains toward humans and toward conspecifics suggest that silver foxes do not perceive humans as their conspecifics. We speculate that these vocalizations are produced in response to a triggering internal state, affiliative or aggressive, that is suppressed by default in these fox strains toward humans as a result of their strict selection for tame or aggressive behavior, whilst still remaining flexible toward conspecifics.     

Kind granddaughters of angry grandmothers: The effect of domestication on vocalization in cross-bred silver foxes

The genetic basis of the effects of domestication has previously been examined in relation to morphological, physiological and behavioural traits, but not for vocalizations. According to Belyaev [Belyaev, D.K., 1979. Destabilizing selection as a factor in domestication. J. Hered. 70, 301-308], directional selection for tame behaviour toward humans resulted in domestication. This hypothesis has been confirmed experimentally on the farm-bred silver fox Vulpes vulpes population that has undergone 45 years of artificial selection for tameness and 35 years of selection for aggressiveness. These foxes, with their precisely known attitudes toward people, provide a means of examining vocal indicators of tameness and aggressiveness to establish the genetic basis for vocal production in canids. We examined vocalizations toward people in foxes selected for tameness and aggressiveness compared to those of three kinds of crosses: Hybrids (Tame × Aggressive), A-Backcrosses (Aggressive × Hybrid) and T-Backcrosses (Tame × Hybrid). We report the effects of selection for tameness on usage and structure of different vocalizations and suggest that vocal indicators for tameness and aggressiveness toward people are discrete phenotypic traits in silver foxes.     

The function of nonlinear phenomena in meerkat alarm calls

Nonlinear vocal phenomena are a ubiquitous feature of human and non-human animal vocalizations. Although we understand how these complex acoustic intrusions are generated, it is not clear whether they function adaptively for the animals producing them. One explanation is that nonlinearities make calls more unpredictable, increasing behavioural responses and ultimately reducing the chances of habituation to these call types. Meerkats (Suricata suricatta) exhibit nonlinear subharmonics in their predator alarm calls. We specifically tested the ‘unpredictability hypothesis’ by playing back naturally occurring nonlinear and linear medium-urgency alarm call bouts. Results indicate that subjects responded more strongly and foraged less after hearing nonlinear alarm calls. We argue that these findings support the unpredictability hypothesis and suggest this is the first study in animals or humans to show that nonlinear vocal phenomena function adaptively.     

Long-term effects of different handling procedures on behavioural, physiological, and production-related parameters in silver foxes

Fifty-one silver fox vixens, subjected to three different handling treatments as cubs (no-handling, gentle or forced handling), were studied for long-term effects on behavioural, physiological and production-related parameters in a one and a half year period following the last handling session. As juveniles, the animals were exposed to three different behavioural tests at 18, 22, 28, and 32 weeks of age. Both forcibly and gently handled animals showed reduced fear responses compared with nonhandled controls in test situations involving close contact with humans (P < 0.05). The foxes were tested again as adults at 10, 13, 15, and 18 months of age with the same behavioural tests. It was revealed that forcibly handled animals persistently showed reduced fear responses compared with control animals, both in close contact with humans and when exposed to a novel object, whereas gently handled animals only differed from control animals in one of the tests involving some human contact and when exposed to a novel object (P < 0.05). Significant differences between adult gently handled and forcibly handled animals were found in the “confront’ test involving close human contact. In this test more flight responses were observed in the gently handled group than in the forcibly handled group (P < 0.01). Control animals had significantly larger adrenal weights compared with both forcibly handled animals and gently handled animals at 22 months of age (total mean adrenal weight: controls, 0.62 g; gentle, 0.54 g; forced, 0.54 g, P < 0.05, general linear models). Other physiological measures and production-related parameters such as body weight, body size, gastric ulceration and pelt qualities did not differ between treatments (P > 0.05). Early post-weaning handling made foxes less fearful towards humans. Forced handling seemed somewhat superior to gentle handling as a means to produce animals which, in the long term, adapted better to the farm environment both behaviourally and physiologically. Non-handled control animals suffered from long-term stress as reflected by high levels of fear responses and enlarged adrenals. Thus post-weaning handling may be beneficial in the long term for the wellbeing of farmed foxes. When applied as a management routine, handling had no significant influence on later production-related parameters and was not considered an economic risk.     

Reflecting on ethical and legal issues in wildlife disease

Disease in wildlife raises a number of issues that have not been widely considered in the bioethical literature. However, wildlife disease has major implications for human welfare. The majority of emerging human infectious diseases are zoonotic: that is, they occur in humans by cross‐species transmission from animal hosts. Managing these diseases often involves balancing concerns with human health against animal welfare and conservation concerns. Many infectious diseases of domestic animals are shared with wild animals, although it is often unclear whether the infection spills over from wild animals to domestic animals or vice versa. Culling is the standard means of managing such diseases, bringing economic considerations, animal welfare and conservation into conflict. Infectious diseases are also major threatening processes in conservation biology and their appropriate management by culling, vaccination or treatment raises substantial animal ethics issues. One particular issue of great significance in Australia is an ongoing research program to develop genetically modified pathogens to control vertebrate pests including rabbits, foxes and house mice. Release of any self‐replicating GMO vertebrate pathogen gives rise to a whole series of ethical questions. We briefly review current Australian legal responses to these problems. Finally, we present two unresolved problems of general importance that are exemplified by wildlife disease. First, to what extent can or should ‘bioethics’ be broadened beyond direct concerns with human welfare to animal welfare and environmental welfare? Second, how should the irreducible uncertainty of ecological systems be accounted for in ethical decision making?     

Correspondence between evoked vocal responses and auditory thresholds in Pleurodema thaul (Amphibia; Leptodactylidae)

Thresholds for evoked vocal responses and thresholds of multiunit midbrain auditory responses to pure tones and synthetic calls were investigated in males of Pleurodema thaul, as behavioral thresholds well above auditory sensitivity have been reported for other anurans. Thresholds for evoked vocal responses to synthetic advertisement calls played back at increasing intensity averaged 43 dB RMS SPL (range 31–52 dB RMS SPL), measured at the subjects’ position. Number of pulses increased with stimulus intensities, reaching a plateau at about 18–39 dB above threshold and decreased at higher intensities. Latency to call followed inverse trends relative to number of pulses. Neural audiograms yielded an average best threshold in the high frequency range of 46.6 dB RMS SPL (range 41–51 dB RMS SPL) and a center frequency of 1.9 kHz (range 1.7–2.6 kHz). Auditory thresholds for a synthetic call having a carrier frequency of 2.1 kHz averaged 44 dB RMS SPL (range 39–47 dB RMS SPL). The similarity between thresholds for advertisement calling and auditory thresholds for the advertisement call indicates that male P. thaul use the full extent of their auditory sensitivity in acoustic interactions, likely an evolutionary adaptation allowing chorusing activity in low-density aggregations.     

Feeding responses of the red fox (<Emphasis Type="Italic">Vulpes vulpes</Emphasis>) to different wild rabbit (<Emphasis Type="Italic">Oryctolagus cuniculus</Emphasis>) densities: a regional approach

We investigate the feeding responses of the red fox (Vulpes vulpes) at a regional scale to different densities of European wild rabbit (Oryctolagus cuniculus) in central–southern Spain. Rabbit abundance indices were obtained in 86 localities during summer 2002. The diet of the fox was studied by analysis of 114 scats collected in 47 of these localities. The feeding response of the fox was examined by a representation of the dry weight percent of rabbit in the diet as a function of the abundance of rabbits; this used data only from those localities where at least 3 scats were collected (70 fox scats from 18 localities). We evaluated the relationship between rabbit abundance and the diversity of the diet of the fox. The feeding patterns of red foxes approximated to Holling’s type III functional response, typical of opportunistic predators. There was a negative relationship between the diversity of the fox’s diet and the abundance of rabbits. Therefore, the fox apparently behaves as a facultative predator, feeding on rabbits when they are abundant and shifting to other prey (and hence a more diverse diet) when rabbits are scarce. These findings are the first step towards understanding the potential role of red foxes in regulating rabbit populations in central–southern Spain.     

Ecology and welfare of aquatic animals in wild capture fisheries

The expansion of commercial aquaculture production has raised awareness of issues relating to the welfare of aquatic animals. The “Five Freedoms” approach to animal welfare was originally devised for farmed terrestrial animals, and has been applied in some countries to aquatic animals reared in aquaculture due to several commonalities inherent within food production systems. There are now moves towards assessing and addressing aquatic animal welfare issues that may arise in wild capture fisheries. However, all “five freedoms” are regularly contradicted in the natural environment, meaning this concept is inappropriate when considering the welfare of aquatic animals in their natural environments. The feelings-based approach to welfare relies on a suffering centered view that, when applied to the natural aquatic environment, requires use of value judgements, cannot encompass scientific uncertainty regarding awareness in fish, elasmobranchs and invertebrates (despite their unquestioned welfare needs), and cannot resolve the welfare conundrums posed by predator–prey interactions or anthropocentrically mediated environmental degradation. For these reasons, the feelings-based approach to welfare is inadequate, inappropriate and must be rejected if applied to aquatic animals in wild capture fisheries, because it demonstrably ignores empirical evidence and several realities apparent within the natural aquatic environment. Furthermore, application of the feelings-based approach is counterproductive as it can alienate key fisheries stakeholders, many of whom are working to address environmental issues of critical importance to the welfare, management and conservation of aquatic animal populations in their natural environment. In contrast, the function-based and nature-based approaches for defining animal welfare appear appropriate for application to the broad range of welfare issues (including emerging environmental issues such as endocrine disruption) that affect aquatic animals in their natural environment, without the need to selectively ignore groups such as elasmobranchs and invertebrates. We consider that the welfare needs of aquatic animals are inextricably entwined with the need for conservation of their populations, communities and their environment, an approach that is entirely consistent with the concept of ecosystem-based management.     

Gnawing bones as enrichment for farmed blue foxes ( Vulpes lagopus)

According to present acts and regulations, farmed foxes shall have a gnawing or other enrichment object in their cages. However, research on the welfare effects of gnawing objects has been scarce. We assessed physiology and health, that is weight development, urinary cortisol-creatinine ratio, serum cortisol level after adrenocorticotropic hormone administration, internal organ masses and incidence of gastric ulcerations as well as dental and overall oral health, in pair-housed juvenile blue foxes that were housed either with or without a possibility to interact with bones (cattle femur) during their growing season (July to December). The results show that the physiological effects of the possibility to interact with bones were either non-significant or suggested that competition for bones may jeopardize the welfare of subordinate individuals. However, the results clearly show that gnawing bones are beneficial for the dental health of farmed foxes.     

Pulses of movement across the sea ice: population connectivity and temporal genetic structure in the arctic fox

Lemmings are involved in several important functions in the Arctic ecosystem. The Arctic fox (Vulpes lagopus) can be divided into two discrete ecotypes: “lemming foxes” and “coastal foxes”. Crashes in lemming abundance can result in pulses of “lemming fox” movement across the Arctic sea ice and immigration into coastal habitats in search for food. These pulses can influence the genetic structure of the receiving population. We have tested the impact of immigration on the genetic structure of the “coastal fox” population in Svalbard by recording microsatellite variation in seven loci for 162 Arctic foxes sampled during the summer and winter over a 5-year period. Genetic heterogeneity and temporal genetic shifts, as inferred by STRUCTURE simulations and deviations from Hardy–Weinberg proportions, respectively, were recorded. Maximum likelihood estimates of movement as well as STRUCTURE simulations suggested that both immigration and genetic mixture are higher in Svalbard than in the neighbouring “lemming fox” populations. The STRUCTURE simulations and AMOVA revealed there are differences in genetic composition of the population between summer and winter seasons, indicating that immigrants are not present in the reproductive portion of the Svalbard population. Based on these results, we conclude that Arctic fox population structure varies with time and is influenced by immigration from neighbouring populations. The lemming cycle is likely an important factor shaping Arctic fox movement across sea ice and the subsequent population genetic structure, but is also likely to influence local adaptation to the coastal habitat and the prevalence of diseases.     

Development of Auditory-Vocal Perceptual Skills in Songbirds

Songbirds are one of the few groups of animals that learn the sounds used for vocal communication during development. Like humans, songbirds memorize vocal sounds based on auditory experience with vocalizations of adult “tutors”, and then use auditory feedback of self-produced vocalizations to gradually match their motor output to the memory of tutor sounds. In humans, investigations of early vocal learning have focused mainly on perceptual skills of infants, whereas studies of songbirds have focused on measures of vocal production. In order to fully exploit songbirds as a model for human speech, understand the neural basis of learned vocal behavior, and investigate links between vocal perception and production, studies of songbirds must examine both behavioral measures of perception and neural measures of discrimination during development. Here we used behavioral and electrophysiological assays of the ability of songbirds to distinguish vocal calls of varying frequencies at different stages of vocal learning. The results show that neural tuning in auditory cortex mirrors behavioral improvements in the ability to make perceptual distinctions of vocal calls as birds are engaged in vocal learning. Thus, separate measures of neural discrimination and behavioral perception yielded highly similar trends during the course of vocal development. The timing of this improvement in the ability to distinguish vocal sounds correlates with our previous work showing substantial refinement of axonal connectivity in cortico-basal ganglia pathways necessary for vocal learning.     

Genotyping of Enterocytozoon bieneusi in Farmed Blue Foxes (Alopex lagopus) and Raccoon Dogs (Nyctereutes procyonoides) in China

Enterocytozoon bieneusi is the most common species of microsporidia found both in humans and animals. Farmed animals, particularly closely associated to humans, may play an important role of zoonotic reservoir in transmitting this disease to humans. The fur industry is a major economic component in some parts of China. To understand the prevalence, genotype variety and zoonotic risk of E. bieneusi in farmed foxes and raccoon dogs, two species of fur animals, fecal specimens of 110 blue foxes and 49 raccoon dogs from Heilongjiang and Jilin provinces in China were examined by internal transcribed spacer (ITS)-based PCR. E. bieneusi was detected in 16.4% (18/110) blue foxes and 4.1% (2/49) raccoon dogs. Altogether, four genotypes of E. bieneusi were identified, including two known genotypes D (n = 13) and EbpC (n = 5), and two novel genotypes named as CHN-F1 (n = 1) in a fox and CHN-R1 (n = 1) in a raccoon dog. Phylogenetic analysis revealed that all the four genotypes were the members of zoonotic group 1. Genotypes D and EbpC were found in humans previously. The findings of zoonotic genotypes of E. bieneusi in the foxes and raccoon dogs suggest these animals infected with E. bieneusi may pose a threat to human health.     

Effects of selection for behavior, human approach mode and sex on vocalization in silver fox

This study presents a first direct comparison of vocal type, call rate and time spent vocalizing among Unselected, Tame and Aggressive strains of silver fox (Vulpes vulpes) in three modes of human approach (Provoking, Approach–Retreat, and Static). Also, it provides a first comparison of male and female vocal output in the Provoking test. Vocal types were found strain-specific irrespective of the fox sex or the test. Males had higher call rates and spent shorter times vocalizing than females. These results support the evidence of genetic-based emotional states, triggering vocal behavior in silver fox strains, and suggest sex dimorphism in vocal activity toward humans.     

Great tits take greater risk toward humans and sparrowhawks in urban habitats than in forests

Urban animals often take more risk toward humans than their non‐urban conspecifics do, but it is unclear how urbanization affects behavior toward non‐human predators. Responses to humans and non‐human predators may covary due to common mechanisms enforcing a phenotypic correlation. However, while increased tolerance toward humans may be advantageous for urban animals, reduced vigilance toward non‐human predators that can pose actual threat may be costly. Therefore, urban animals may benefit from showing specific responses to different threat levels, such as humans versus non‐human predators, or hostile versus non‐hostile humans. To test these alternatives, we compared responses (latencies to return to nest) of urban and forest‐breeding great tits (Parus major) to familiar hostile and unfamiliar humans as well as one of their common predators, the sparrowhawk (Accipiter nisus). We found that urban birds were more risk‐taking toward both humans and sparrowhawk than forest birds. However, responses to sparrowhawk did not correlate with responses to humans either within or across habitats. This suggests that higher risk‐taking of urban compared to forest‐dwelling great tits toward sparrowhawk may be threat‐specific response to lower predation risk rather than a spillover effect of increased tolerance to humans. Furthermore, birds responded similarly to unfamiliar and familiar (potentially dangerous) humans in both habitats, suggesting that great tits may not adjust their risk‐taking to the threat represented by individual humans. These findings indicate that urban birds may flexibly adjust their risk‐taking to certain, but not all, types of threat.     

The variation in reliability of individual vocal signature throughout ontogenesis in the red-crowned crane Grus japonensis

Distinctiveness of chicks’ calls may arise in ontogenesis when parents can confuse their own and alien chicks, leaving their nests and forming crèches or flocks. It is unknown, however, whether the individual vocal signature retains further in ontogenesis or relaxes when the necessity in the parental care disappears. In this paper, we study the inter- and intra-individual variations of the acoustic parameters in chicks’ calls in the red-crowned crane Grus japonensis, the species with prolonged development enveloping three stages: territorial under parental care, in flocks under parental care and in flocks self-independently. We found, that discriminability of chicks’ calls increased significantly to the second stage, characterized by the maximum risk for parents to confuse the own and alien chicks, and significantly decreased to the third stage, when the needs in the parent–chick vocal recognition disappeared. Our data agree with a hypothesis that the individual distinctiveness decreases in the absence of necessity in accuracy of parent–chick recognition.     

Cognitive ability and sentience: which aquatic animals should be protected?

It is of scientific and practical interest to consider the levels of cognitive ability in animals, which animals are sentient, which animals have feelings such as pain and which animals should be protected. A sentient being is one that has some ability to evaluate the actions of others in relation to itself and third parties, to remember some of its own actions and their consequences, to assess risk, to have some feelings and to have some degree of awareness. These abilities can be taken into account when evaluating welfare. There is evidence from some species of fish, cephalopods and decapod crustaceans of substantial perceptual ability, pain and adrenal systems, emotional responses, long- and short-term memory, complex cognition, individual differences, deception, tool use, and social learning. The case for protecting these animals would appear to be substantial. A range of causes of poor welfare in farmed aquatic animals is summarised.     

Subharmonics increase the auditory impact of female koala rejection calls

Although non‐linear phenomena are common in human and non‐human animal vocalisations, their functional relevance remains poorly understood. One theory posits that non‐linear phenomena generate unpredictability in vocalisations, which increases the auditory impact of vocal signals, and makes animals less likely to habituate to call repetition. Female koalas (Phascolarctos cinereus) produce vocal signals when they reject male copulation attempts that contain relatively high levels of non‐linear phenomena, and thus may function as attention grabbing vocal signals during the breeding season. To test this hypothesis, we used playback experiments: firstly, to determine whether female rejection calls induce heightened behavioural responses in free‐ranging male koalas during the breeding season, and secondly, to examine how the relative amount of non‐linear phenomena in rejection calls influences male behavioural response. The results show that male koalas look for longer towards speakers broadcasting playback sequences of male bellows followed by a series of female rejection calls than those broadcasting only male bellows. In addition, female rejection call sequences with more subharmonics, higher harmonics‐to‐noise ratios, and less biphonation produced the greatest male looking responses. Our findings support the hypothesis that female koala rejection calls function to grab male attention during the breeding season, and indicate that subharmonics are the main acoustic feature that increases the auditory impact of these vocal signals.     

Effect of lesion of nucleus robustus archistriatalis on call in bramble finch ( Fringilla montifringilla )

The lesion of nucleus robustus archistriatalis (RA) has no effect on normal short calls in the bramble finch, but affects significantly the temporal and acoustic features of learned long calls. It causes the principal frequency of basic sound in monotone long calls to increase 500 cents, and to lose two upper partials. The lesion of RA not only results in the increased sound length of loud-sound and shortened coda of variable-tone long calls by 13.4%–22.1% and 21.2%–24.2% on average, respectively, but also makes the frequency rising coefficient (FRC) of even order partial tone in loud-sound drop 18.5%–25.8% on an average, and the step-up rate decrease 22.7% –24.0% on an average with the increase of frequencies. These results show that the control of temporal and frequency features of learned calls by RA matches to each other. Moreover, the lesion of bilateral RA can confuse the vocal pattern, and the produced long call has the character of both the mono- and variable-tone long calls. The prelude shows rising frequency, and the loud sound is monotone sound.