Females that experience threat are better teachers

Superb fairy-wren (Malurus cyaneus) females use an incubation call to teach their embryos a vocal password to solicit parental feeding care after hatching. We previously showed that high call rate by the female was correlated with high call similarity in fairy-wren chicks, but not in cuckoo chicks, and that parent birds more often fed chicks with high call similarity. Hosts should be selected to increase their defence behaviour when the risk of brood parasitism is highest, such as when cuckoos are present in the area. Therefore, we experimentally test whether hosts increase call rate to embryos in the presence of a singing Horsfield''s bronze-cuckoo (Chalcites basalis). Female fairy-wrens increased incubation call rate when we experimentally broadcast cuckoo song near the nest. Embryos had higher call similarity when females had higher incubation call rate. We interpret the findings of increased call rate as increased teaching effort in response to a signal of threat.     

Alarm substance from adult zebrafish alters early embryonic development in offspring

Alarm substances elicit behavioural responses in a wide range of animals but effects on early embryonic development are virtually unknown. Here we investigated whether skin injury-induced alarm substances caused physiological responses in embryos produced by two Danio species (Danio rerio and Danio albolineatus). Both species showed more rapid physiological development in the presence of alarm substance, although there were subtle differences between them: D. rerio had advanced muscle contraction and heart function, whereas D. albolineatus had advanced heart function only. Hence, alarm cues from injured or dying fish may be of benefit to their offspring, inducing physiological responses and potentially increasing their inclusive fitness.     

Song discrimination by nestling collared flycatchers during early development

Pre-zygotic isolation is often maintained by species-specific signals and preferences. However, in species where signals are learnt, as in songbirds, learning errors can lead to costly hybridization. Song discrimination expressed during early developmental stages may ensure selective learning later in life but can be difficult to demonstrate before behavioural responses are obvious. Here, we use a novel method, measuring changes in metabolic rate, to detect song perception and discrimination in collared flycatcher embryos and nestlings. We found that nestlings as early as 7 days old respond to song with increased metabolic rate, and, by 9 days old, have increased metabolic rate when listening to conspecific when compared with heterospecific song. This early discrimination between songs probably leads to fewer heterospecific matings, and thus higher fitness of collared flycatchers living in sympatry with closely related species.     

Alarm calls elicit predator-specific physiological responses

Glucocorticoids regulate glucose concentrations and responses to unpredictable events, while also modulating cognition. Juvenile Belding''s ground squirrels (Urocitellus beldingi) learn to respond to whistle and trill alarm calls, warning of aerial and terrestrial predators, respectively, shortly after emerging from natal burrows at one month of age. Alarm calls can cause physiological reactions and arousal, and this arousal, coupled with watching adult responses, might help juveniles learn associations between calls and behavioural responses. I studied whether young show differential cortisol responses to alarm and non-alarm calls, using playbacks of U. beldingi whistles, trills, squeals (a conspecific control vocalization) and silent controls. Trills elicited very high cortisol responses, and, using an individual''s response to the silent control as baseline, only their response to a trill was significantly higher than baseline. This cortisol increase would provide glucose for extended vigilance and escape efforts, which is appropriate for evading terrestrial predators which hunt for long periods. Although whistles do not elicit a cortisol response, previous research has shown that they do result in bradycardia, which enhances attention and information processing. This is a novel demonstration of two physiological responses to two alarm calls, each appropriate to the threats represented by the calls.     

Parent–offspring and inter-offspring responses to conspecific versus heterospecific distress calls in 2 sympatric birds

Distress calls, as a type of alarm call, play important roles in expressing bodily condition and conveying information concerning predation threats. In this study, we examined the communication via distress calls in parent–offspring and inter-offspring interactions. First, we used playback of chick distress calls of 2 sympatric breeders, the vinous-throated parrotbill Sinosuthora webbiana and the oriental reed warbler Acrocephalus orientalis, to the adults/chicks of these 2 species, respectively, and measured the responses of conspecifics or heterospecifics. The playback-to-chicks experiment showed that both species of chicks reduced the number of begging calls and begging duration time as a response to conspecific/heterospecific distress calls compared with natural begging and background noise controls. However, reed warbler chicks also reduced beak opening frequency in the response to conspecific distress calls compared with other playback stimuli. Second, the results of the playback-to-adults experiment showed that reed warbler adults could eavesdrop on distress calls of conspecific neighbors and sympatric heterospecifics. Furthermore, the nest-leaving behavior of reed warblers did not differ significantly when they heard the distress calls of conspecifics or parrotbills. Finally, reed warbler adults responded to heterospecific distress calls more quickly than to conspecific distress calls, and parrotbill adults presented the same response. Our results supported the warn-kin hypothesis and show that chick distress calls play an important role in conveying risk and the condition of chicks to enhance individual fitness. In addition, we also found that eavesdropping on distress calls is a congenital behavior that begins in the chick stage.     

Operant conditioning of small birds for acoustic discrimination

Standard operant conditioning techniques have been successfully applied to the problem of call discrimination in small birds. Budgerigars (Melopsittacus undulatus) and canaries (Serinus canarius) were trained with a GO/NOGO procedure using positive reinforcement to discriminate between both conspecific contact calls and contact calls of the other species. Budgerigars showed equal facility at each task. By contrast, canaries learned the task involving conspecific contact calls but failed, as a group, to discriminate between budgerigar contact calls. These results show that conditioning techniques can be used to study perceptual learning of species typical calls in small birds.     

Why do shrews twitter? Communication or simple echo-based orientation

Shrews are very vocal animals. We tested behaviourally whether the high-pitched laryngeal ‘twittering’ calls of as-yet unclear function serve for communication or echo-based orientation. We used a representative species from each of the two largest phylogenetic groups of shrews. In both species, experimental manipulation of substrate density, but not of the likelihood of conspecific presence, affected the shrews'' call rate when exploring an unknown environment. This adaptation of call rate to the degree of habitat clutter parallels bat echolocation and suggests that shrews may use the echoes and reverberations of their calls for identifying routes through their habitat or for probing habitat type. To assess the acoustic feasibility of shrew echo orientation, we ensonified shrew habitats in the field with an ‘artificial shrew’ (small speaker mounted close to a sensitive microphone). The data showed that shrew-like calls can indeed yield echo scenes useful for habitat assessment at close range, but beyond the range of the shrews'' vibrissae.     

Effect of conspecific alarm calls in the parental behaviour of nesting southern house wrens

Alarm calls are usually used to signal the presence of a threat to members of the same species and have been studied broadly in social foraging species. We analysed the effects of conspecific alarm calls on the parental behaviour of a territorial species, the southern house wrens (Troglodytes aedon musculus), during nestling stage. We compared the parental response of adults feeding 9–11-day-old nestlings when faced with conspecific alarm calls and with a control non-sympatric species’ song broadcast from a neighbouring territory. We measured the time required by parents to return to the nest (latency) when exposed to the stimuli and estimated parent’s nest visitation rate and mean visit duration. Parents took longer to resume parental activities when we broadcast a conspecific alarm call, but they did not modify their nest visitation rate or the mean visit duration. Heterospecific songs did not seem to affect parental behaviour. Our results suggest that nesting southern house wrens can use alarm calls uttered from neighbouring territories to assess the presence of a threat and adjust their parental behaviour accordingly.     

Female Sexual Preferences Toward Conspecific and Hybrid Male Mating Calls in Two Species of Polygynous Deer, <Emphasis Type="Italic">Cervus elaphu</Emphasis>s and <Emphasis Type="Italic">C. nippon</Emphasis>

The behavioral processes at the basis of hybridization and introgression are understudied in terrestrial mammals. We use a unique model to test the role of sexual signals as a reproductive barrier to introgression by investigating behavioral responses to male sexual calls in estrous females of two naturally allopatric but reproductively compatible deer species, red deer and sika deer. Previous studies demonstrated asymmetries in acoustic species discrimination between these species: most but not all female red deer prefer conspecific over sika deer male calls while female sika deer exhibit no preference differences. Here, we extend this examination of acoustic species discrimination to the role of male sexual calls in introgression between parent species and hybrids. Using two-speaker playback experiments, we compared the preference responses of estrous female red and sika deer to male sexual calls from conspecifics versus red × sika hybrids. These playbacks simulate early secondary contact between previously allopatric species after hybridization has occurred. Based on previous conspecific versus heterospecific playbacks, we predicted that most female red deer would prefer conspecific calls while female sika deer would show no difference in their preference behaviors toward conspecific and hybrid calls. However, results show that previous asymmetries did not persist as neither species exhibited more preferences for conspecific over hybrid calls. Thus, vocal behavior is not likely to deter introgression between these species during the early stages of sympatry. On a wider scale, weak discrimination against hybrid sexual signals could substantially contribute to this important evolutionary process in mammals and other taxa.     

No pre-existing biases for heterospecific call traits in the frog Physalaemus enesefae

Previous phonotaxis studies with two species of the Physalaemuspustulosus species group indicated that female preferences for several heterospecific call traits resulted from sensory biases inherited from a common ancestor. In phonotaxis experiments, we determined whether Physalaemus enesefae, a distant relative of the P. pustulosus group, showed similar preferences for call traits not present in conspecific males. We presented females with a choice between the typical conspecific advertisement call and the same call to which we digitally appended a chuck from P. pustulosus, a squawk from P. freibergi, and an amplitude-modulated prefix from P. pustulatus. In addition we presented the advertisement call in doublets, a trait peculiar to P. coloradorum. We also analysed male vocal behaviour evoked in response to the same suite of stimuli. Physalaemus enesefae females did not prefer the calls of their own males with appended heterospecific traits over unmodified calls, nor conspecific calls in doublets over single calls. The lack of preference among females was not the result of a behavioural polymorphism. Female responses to repeated presentations of the same stimulus pair were not consistent. Males also did not show an enhanced vocal response to altered calls relative to the typical conspecific call. Consequently, there are no pre-existing biases for these heterospecific call traits in P. enesefae; pre-existing preferences in the P. pustulosus group could have been inherited from an ancestor not shared with P. enesefae, but data from other closely related species are needed to confirm this conclusion. Copyright 2002 The Association for the Study of Animal Behaviour. Published by Elsevier Science Ltd. All rights reserved.     

The adaptive significance of avian mobbing. III. Cultural transmission of enemy recognition in blackbirds: Cross-species tutoring and properties of learning

Taped conspecific and alien species mobbing calls suffice to transmit enemy recognition of a conditioned object CS to European blackbirds (Turdus merula), though their reinforcing effect is probably less than that of a real blackbird mobber. Blackbirds habituated to the CS learn to mob it in the latter case without impairment, but fail completely if taped conspecific mobbing calls serve as the reinforcer. Mobbing performance of the learner during learning peaks significantly later with a weak CS than with a strong CS. A general mobbing motivation, as measured by mobbing performance over many episodes, is typical for each individual: i.e. responses correlate intra-individually over a wide range of different compound stimuli. A more specific motivation accompanying enemy stimulus learning weakens these inter-response relationships and enhances performance of the learned response; the learned response correlates more strongly with the response during learning than with any other preceding response. This suggests that a specific motivation during engram formation has reinforcing properties. As revealed by multiple regression analysis, all three mobbing elements scored exert their learning-enhancing effect by a strictly intra-element facilitation.     

Marine algal symbionts benefit benthic invertebrate embryos deposited in gelatinous egg masses

Algae colonize the gelatinous egg masses of marine invertebrates. This study demonstrates a symbiotic relationship between marine algae and the invertebrate embryos in gelatinous egg masses found in Indian River Lagoon, FL, USA. The benefits to the embryos in this association differ among host species investigated. The embryos of the polychaete Axiothella mucosa graze on the diatom assemblage in their egg masses and the fitness of the crawl-away juveniles is improved by this food source. The tenuous egg masses of the polychaete Arenicola cristata and the mollusk Haminoea succinea are negatively buoyant when spawned and become buoyant when symbiotic algae are present. In addition to increased dispersal of their lecithotrophic larvae, the potential of the egg masses of A. cristata and H. succinea to float may reduce predation on the embryos by benthic predators such as the gastropod Nassarius vibex. Photosynthetically derived oxygen from the algae may benefit the embryos of the opisthobranch Haminoea elegans by increasing oxygen supply when crawl-away juveniles emerge from the egg mass. However, when mostly earlier stage larvae are hatched from egg masses of H. elegans, the additional oxygen supplied by the algae does not provide a substantial advantage. Algae were absent in the gelatinous egg mass core of only one of the five species examined, Haminoea antillarum. H. antillarum has both a short embryonic development time and denser egg mass gel than the other four species tested. What is not understood is whether invertebrate egg masses are an opportunistic space for algae to colonize or whether only a few microalgal species can exploit the gelatinous substrate.     

Conspecific discrimination in an object-choice task in African grey parrots (Psittacus erithacus)

Living in social groups presents the opportunity to use information provided by other individuals. Several animal species emit specific vocalizations when they find food. Here, we investigate whether African grey parrots (Psittacus erithacus) use vocal and non-vocal information provided by a conspecific in order to find a hidden food source. One subject was attracted by the presence or the vocalizations of a subordinate conspecific, but not of a dominant, which brings us to hypothesize that parrots could be capable of individual vocal discrimination.     

Presence of a conspecific causes divergent changes in resting metabolism,depending on its relative size

It is well established that the average metabolism of many species of fish varies with group size. However, it is not clear whether all individuals respond in the same way. Here, we use a newly calibrated method of measuring the metabolic rate of fish from opercular (ventilatory) movements that allows for the first-time estimation of changes in resting metabolic rate (RMR) of each individual within different social groups and when alone. The presence of a conspecific had divergent effects on the RMR of juvenile Atlantic salmon Salmo salar, depending on its relative body size: the presence of a smaller fish caused a 40 per cent reduction, whereas the presence of a slightly larger fish approximately doubled RMR. These effects occurred in the absence of activity and were sustained at lower magnitude in the case of the relatively smaller conspecific even if a transparent barrier prevented any physical interactions between fish. Changes in RMR were mirrored by changes in eye colour that indicate they were linked to stress levels. These contrasting and strong responses show that even the nearby presence of a conspecific can have profound and variable effects on an individual''s energy budget; they also highlight the complex trade-offs involved in social interactions.     

Do allopatric male Calopteryx virgo damselflies learn species recognition?

There is a growing amount of empirical evidence that premating reproductive isolation of two closely related species can be reinforced by natural selection arising from avoidance of maladaptive hybridization. However, as an alternative for this popular reinforcement theory, it has been suggested that learning to prefer conspecifics or to discriminate heterospecifics could cause a similar pattern of reinforced premating isolation, but this possibility is much less studied. Here, we report results of a field experiment in which we examined (i) whether allopatric Calopteryx virgo damselfly males that have not encountered heterospecific females of the congener C. splendens initially show discrimination, and (ii) whether C. virgo males learn to discriminate heterospecifics or learn to associate with conspecifics during repeated experimental presentation of females. Our experiment revealed that there was a statistically nonsignificant tendency for C. virgo males to show initial discrimination against heterospecific females but because we did not use sexually naïve individuals in our experiment, we were not able to separate the effect of innate or associative learning. More importantly, however, our study revealed that species discrimination might be further strengthened by learning, especially so that C. virgo males increase their association with conspecific females during repeated presentation trials. The role of learning to discriminate C. splendens females was less clear. We conclude that learning might play a role in species recognition also when individuals are not naïve but have already encountered potential conspecific mates.     

Mating and Sexual Communication by Steinernema carpocapsae (Nemata: Steinernematidae)

Entomopathogenic nematodes are lethal insect parasites that reproduce exclusively inside their hosts in nature. Infection decisions made by the free-living infective-stage juveniles have an impact on reproductive success, but it is likely that mating decisions are made by adults while inside their host. We investigated sexual communication between male and female adult stages of Steinernema carpocapsae (Rhabditida: Steinernematidae) to assess whether mating is chemically mediated during the adult stage or results from incidental encounters between adults inside the insect host. To assess chemical communication, we measured the behavioral response of adult male S. carpocapsae to several different potential sources of chemical information. Male S. carpocapsae responded to virgin females only and were not influenced by mated conspecific females, conspecific males, or heterospecific females. These results show that species-specific communication takes place between adult entomopathogenic nematodes within the host cadaver just prior to mating.     

Distress call alternation in peking ducklings (Anas platyrhynchos)

Peking ducklings (Anas platyrhynchos) were found to alternate their distress calls with those of conspecifics. This alternation response consisted of two components: a strong tendency to suppress vocalizing during the conspecific's calls and a weaker tendency to increase vocalizing (above the level given by birds tested in auditory isolation) following those calls. Similar results were obtained whether pairs of ducklings were tested or whether individual ducklings were tested with tape-recorded calls. Further, visual contact with the conspecific, or a mirror image, although not necessary for eliciting an alternation response, did have a significant facilitative effect on this response. This latter effect may have been due to the general arousal-reducing properties of the visual stimulus. Finally, in contrast to the strong response of ducklings to conspecific distress calls, they displayed a much weaker tendency to alternate their calls with (a) clicking sounds and 7.0-kHz tones with the same temporal patterning and intensity as the taped distress calls, (b) 3.8-kHz tones that additionally matched the dominant frequency of the taped calls, and (c) synthetic distress calls that also approximated the frequency modulation of the taped calls. These results indicate that the distress call alternation response is not simply an artifact of a more general orienting response in which ducklings inhibit their own vocalizations whenever they hear any salient auditory stimulus. Rather, the response appears to be quite specifically triggered by the sound of the sibling calls. The present results stand in contrast to the common assertion that young birds largely ignore the distress calls of siblings. These results are, however, consistent with recent literature emphasizing the importance of sibling interactions in the analysis of mallard early social attachments.     

Vocal communication in a neotropical treefrog, Hyla ebraccata: Advertisement calls

We studied the vocal communication of Hyla ebraccata in central Panama. The advertisement call of this species consists of a pulsed buzz-like primary note which may be given alone or followed by 1–4 secondary click notes. Primary notes are highly stereotyped, showing little variation within or0 among individuals in dominant frequency, duration, pulse repetition rate or rise time. Males calling in isolation give mostly single-note calls. They respond to playbacks of conspecific calls by increasing calling rates and the proportion of multi-note calls, and by giving synchronized calls 140–200 ms after the stimulus begins. Responses to conspecific advertisement calls are usually given immediately after the primary note of the leading call, but the primary note of the response often overlaps with the click notes of the leading call. Experiments with synthetic signals showed that males synchronize to any type of sound of the appropriate frequency (3 kHz), regardless of the fine structure of the stimulus. Playbacks of synthetic calls of variable duration showed that males do not synchronize well to calls less than 150 ms long, but they do to longer calls (200–600 ms). The variance in response latency increased with increasing stimulus duration, but modal response times remained at around 140–200 ms. Similar results were obtained in experiments withsynthetic calls having a variable number of click notes. Males showed no tendency to increase the number of click notes in their calls in response to increasing stimulus duration or increasing number of clicks in the stimulus. Females preferred three-note to one-note calls in two-choice playback experiments, whether these were presented in alternation, or with the one-note call leading and the three-note call following. Females showed no preference for leader or follower calls when both were one-note. When two-note calls were presented with the primary note of the follower overlapping the click note of the leader, females went to calls in which click notes were not obscured. Our results indicate that male H. ebraccata respond to other males in a chorus in ways which enhance their ability to attract mates.     

Learned mate recognition and reproductive isolation in guppies

Research on learned species discrimination has focused on the consequences of early experience. However, in species where parental care is limited or absent, including most fish, juveniles have fewer opportunities to learn from adult conspecifics. We examined male mate recognition in Trinidadian guppies, Poecilia reticulata, and in their sister species, the swamp guppy, P. picta. Choice tests revealed that males from localities where their species is the only poeciliid present initially mated with conspecific and heterospecific females at random. In contrast, P. reticulata and P. picta found in sympatry preferred their own females. We then investigated the acquisition of mating discrimination by wild P. reticulata males from two allopatric populations. Males that were allowed to interact with females of both species learned within 4 days to distinguish conspecific partners, and within a week their species discrimination matched that of sympatric populations. This study confirms that learning is important in the acquisition of adult mating preferences and shows why learned mate preferences can be important in the last stages of speciation.