Stability of acoustic individuality in the alarm calls of wild yellow ground squirrels Spermophilus fulvus and contrasting calls from trapped and free-ranging callers

The questions of individuality and stability of cues to identity in vocal signals are of considerable importance from theoretical and conservation perspectives. While individuality in alarm calls has been reported for many sciurids, it is not well-documented that the vocal identity encoded in the alarm calls is stable between different encounters with predators. Previous studies of two obligate hibernating rodents, speckled ground squirrels Spermophilus suslicus, and yellow ground squirrels Spermophilus fulvus demonstrated that, after hibernation, most individuals could not be identified reliably by their alarm calls. Moreover, in most speckled ground squirrels, individual patterns of alarm calls changed progressively over as little as 2 weeks. However, these previous data have been obtained using the collection of alarm calls from trapped animals. Here, we examined ten free-ranging dye-marked yellow ground squirrels to determine whether their alarm calls retain the cues to individuality between two encounters of surrogate predators (humans), separated on average by 3 days. Discriminant function analysis showed that the alarm calls of individual yellow ground squirrels were very similar within a recording session, providing very high individual distinctiveness. However, in six of the ten animals, the alarm calls were unstable between recording sessions. Also, we examined ten dye-marked individuals for consistency of acoustic characteristics of their alarm calls between the encounters of humans, differing in techniques of call collection, from free-ranging vs trapped animals. We found differences only in two variables, both related to sound degradation in the environment. Data are discussed in relation to hypotheses explaining the adaptive utility of acoustic individuality in alarm calls.     

Speed of call delivery is related to context and caller identity in Campbell’s monkey males

Call rate can be a salient feature in animal communication. Depending on the species, different psychological variables appear to influence call rates but the exact nature of these relationships remains poorly explored. Here, we demonstrate for free-ranging Campbell’s monkeys that the call rates of four different alarm series (termed H, K, K₊, and B series) vary systematically as a function of context, associated behaviour, and identity of the caller. K₊ series were given more rapidly to predation than non-predation events, K₊ and K series more rapidly to visual than auditory predator detection, and H series more rapidly while counterattacking an eagle than staying put. Finally, there were individual differences in B series, suggesting that call rate potentially provides listeners with cues about the caller’s anti-predator behaviour, event type experienced, and his identity.     

Mourning dove (Zenaida macroura) wing-whistles may contain threat-related information for con- and hetero-specifics

Distinct acoustic whistles are associated with the wing-beats of many doves, and are especially noticeable when doves ascend from the ground when startled. I thus hypothesized that these sounds may be used by flock-mates as cues of potential danger. To test this hypothesis, I compared the responses of mourning doves (Zenaida macroura), northern cardinals (Cardinalis cardinalis), and house sparrows (Passer domesticus) to audio playbacks of dove ‘startle wing-whistles’, cardinal alarm calls, dove ‘nonstartle wing-whistles’, and sparrow ‘social chatter’. Following playbacks of startle wing-whistles and alarm calls, conspecifics and heterospecifics startled and increased vigilance more than after playbacks of other sounds. Also, the latency to return to feeding was greater following playbacks of startle wing-whistles and alarm calls than following playbacks of other sounds. These results suggest that both conspecifics and heterospecifics may attend to dove wing-whistles in decisions related to antipredator behaviors. Whether the sounds of dove wing-whistles are intentionally produced signals warrants further testing.     

Two sympatric species of passerine birds imitate the same raptor calls in alarm contexts

While some avian mimics appear to select sounds randomly, other species preferentially imitate sounds such as predator calls that are associated with danger. Previous work has shown that the Greater Racket-tailed Drongo (Dicrurus paradiseus) incorporates predator calls and heterospecific alarm calls into its own species-typical alarm vocalizations. Here, we show that another passerine species, the Sri Lanka Magpie (Urocissa ornata), which inhabits the same Sri Lankan rainforest, imitates three of the same predator calls that drongos do. For two of these call types, there is evidence that magpies also use them in alarm contexts. Our results support the hypothesis that imitated predator calls can serve as signals of alarm to multiple species.     

Delayed onset of vocal recognition in Australian sea lion pups (Neophoca cinerea)

In pinnipeds, maternal care strategies and colony density may influence a species’ individual recognition system. We examined the onset of vocal recognition of mothers by Australian sea lion pups (Neophoca cinerea). At 2 months of age, pups responded significantly more to the calls of their own mothers than alien female calls demonstrating a finely tuned recognition system. However, newborn pups did not respond differentially to the calls of their mother from alien female calls suggesting that vocal recognition had not yet developed or is not yet expressed. These findings are in stark contrast to other otariid species where pups learn their mother’s voice before their first separation. Variance in colony density, pup movements, and natal site fidelity may have reduced selective pressures on call recognition in young sea lions, or alternatively, another sensory system may be used for recognition in the early stage of life.     

The mimetic repertoire of the spotted bowerbird <Emphasis Type="Italic">Ptilonorhynchus maculatus</Emphasis>

Although vocal mimicry in songbirds is well documented, little is known about the function of such mimicry. One possibility is that the mimic produces the vocalisations of predatory or aggressive species to deter potential predators or competitors. Alternatively, these sounds may be learned in error as a result of their acoustic properties such as structural simplicity. We determined the mimetic repertoires of a population of male spotted bowerbirds Ptilonorhynchus maculatus, a species that mimics predatory and aggressive species. Although male mimetic repertoires contained an overabundance of vocalisations produced by species that were generally aggressive, there was also a marked prevalence of mimicry of sounds that are associated with alarm such as predator calls, alarm calls and mobbing calls, irrespective of whether the species being mimicked was aggressive or not. We propose that it may be the alarming context in which these sounds are first heard that may lead both to their acquisition and to their later reproduction. We suggest that enhanced learning capability during acute stress may explain vocal mimicry in many species that mimic sounds associated with alarm.     

Echolocation calls of Poey’s flower bat (<Emphasis Type="Italic">Phyllonycteris poeyi</Emphasis>) unlike those of other phyllostomids

Unlike any other foraging phyllostomid bat studied to date, Poey’s flower bats (Phyllonycteris poeyi-Phyllostomidae) emit relatively long (up to 7.2 ms), intense, single-harmonic echolocation calls. These calls are readily detectable at distances of at least 15 m. Furthermore, the echolocation calls contain only the first harmonic, which is usually filtered out in the vocal tract of phyllostomids. The foraging echolocation calls of P. poeyi are more like search-phase echolocation calls of sympatric aerial-feeding bats (Molossidae, Vespertilionidae, Mormoopidae). Intense, long, narrowband, single-harmonic echolocation calls focus acoustic energy maximizing range and favoring detection, which may be particularly important for cruising bats, like P. poeyi, when flying in the open. Flying in enclosed spaces, P. poeyi emit short, low-intensity, frequency-modulated, multiharmonic echolocation calls typical of other phyllostomids. This is the first report of a phyllostomid species emitting long, intense, single-harmonic echolocation calls with most energy in the first harmonic.     

A cost of alarm pheromone production in cotton aphids, Aphis gossypii

The sesquiterpene, (E)--farnesene, is used by many aphid species as an alarm pheromone to warn related individuals of predation. Disturbed cotton aphids, Aphis gossypii Glover, released (E)--farnesene into the air as detected by solid phase microextraction and gas chromatography mass spectrometry (GC–MS). Solvent extracts of cotton aphids of various life stages and weights also were analyzed by GC–MS for sums of ions 69 and 93, which discriminated (E)--farnesene from coeluting compounds. Aphids of all life stages and sizes reared on cotton plants in both an environmental chamber and glasshouse contained (E)--farnesene in amounts ranging from 0.1 to 1.5 ng per individual. The quantities of (E)--farnesene in aphids increased in relation to increasing body weight, and variation in individual weights explained about 82% of the variation in alarm pheromone. However, the concentrations (ng/mg fresh weight) declined exponentially with increasing body weight. These findings indicate that aphid nymphs try to compensate for their smaller size by producing relatively more pheromone per weight than adults but still cannot approach an evolutionary optimal load, as assumed in adults with the greatest total amounts. This suggests that young aphids need to balance costs of growth and maturation with costs of producing the alarm pheromone.     

Altai pika (<Emphasis Type="Italic">Ochotona alpina</Emphasis>) alarm calls: individual acoustic variation and the phenomenon of call-synchronous ear folding behavior

Non-hibernating pikas collect winter food reserves and store them in hay piles. Individualization of alarm calls might allow discrimination between colony members and conspecifics trying to steal food items from a colony pile. We investigated vocal posture, vocal tract length, and individual acoustic variation of alarm calls, emitted by wild-living Altai pikas Ochotona alpina toward a researcher. Recording started when a pika started calling and lasted as long as possible. The alarm call series of 442 individual callers from different colonies consisted of discrete short (0.073–0.157 s), high-frequency (7.31–15.46 kHz), and frequency-modulated calls separated by irregular intervals. Analysis of 442 discrete calls, the second of each series, revealed that 44.34% calls lacked nonlinear phenomena, in 7.02% nonlinear phenomena covered less than half of call duration, and in 48.64% nonlinear phenomena covered more than half of call duration. Peak frequencies varied among individuals but always fitted one of three maxima corresponding to the vocal tract resonance frequencies (formants) calculated for an estimated 45-mm oral vocal tract. Discriminant analysis using variables of 8 calls per series of 36 different callers, each from a different colony, correctly assigned over 90% of the calls to individuals. Consequently, Altai pika alarm calls are individualistic and nonlinear phenomena might further increase this acoustic individualization. Additionally, video analysis revealed a call-synchronous, very fast (0.13–0.23 s) folding, depression, and subsequent re-expansion of the pinna confirming an earlier report of this behavior that apparently contributes to protecting the hearing apparatus from damage by the self-generated high-intensity alarm calls.     

Explanative power of variables used in species distribution modelling: an issue of general model transferability or niche shift in the invasive Greenhouse frog (Eleutherodactylus planirostris)

The use of species distribution models (SDMs) to predict potential distributions of species is steadily increasing. A necessary assumption when projecting models throughout space or time is that climatic niches are conservative, but recent findings of niche shifts during biological invasion of particular plant and animal species have indicated that this assumption is not categorically valid. One reason for observed shifts may relate to variable selection for modelling. In this study, we assess differences in climatic niches in the native and invasive ranges of the Greenhouse frog (Eleutherodactylus planirostris). We analyze which variables are more ‘conserved’ in comparison to more ‘relaxed’ variables (i.e. subject to niche shift) and how they influence transferability of SDMs developed with Maxent on the basis of ten bioclimatic layers best describing the climatic requirements of the target species. We focus on degrees of niche similarity and conservatism using Schoener's index and Hellinger distance. Significance of results are tested with null models. Results indicate that the degrees of niche similarity and conservatism vary greatly among the predictive variables. Some shifts can be attributed to active habitat selection, whereas others apparently reflect variation in the availability of climate conditions or biotic interactions between the frogs' native and invasive ranges. Patterns suggesting active habitat selection also vary among variables. Our findings evoke considerable implications on the transferability of SDMs over space and time, which is strongly affected by the choice and number of predictors. The incorporation of ‘relaxed’ predictors not or only indirectly correlated with biologically meaningful predictors may lead to erroneous predictions when projecting SDMs. We recommend thorough assessments of invasive species' ecology for the identification biologically meaningful predictors facilitating transferability.     

Reversed sex change by widowed males in polygynous and protogynous fishes: female removal experiments in the field

Sex change, either protogyny (female to male) or protandry (male to female), is well known among fishes, but evidence of bidirectional sex change or reversed sex change in natural populations is still very limited. This is the first report on female removal experiments for polygnous and protogynous fish species to induce reversed sex change in the widowed males in the field. We removed all of the females and juveniles from the territories of dominant males in the cleaner wrasse Labroides dimidiatus (Labridae) and the rusty angelfish Centropyge ferrugata (Pomacanthidae) on the coral reefs of Okinawa. In both species, if new females or juveniles did not immigrate into the territories of the widowed males, some of them emigrated to form male–male pairs. When a male–male pair formed, the smaller, subordinate partner began to perform female sexual behaviours (n = 4 in L. dimidiatus; n = 2 in C. ferrugata) and, finally, released eggs (n = 1, respectively). Thus, the reversed sex change occurred in the widowed males according to the change of their social status. These results suggest that such female removal experiments will contribute to the discovery of reversed sex change in the field also in other polygnous and protogynous species.     

Dancing to different tunes: heterospecific deciphering of the honeybee waggle dance

Although the structure of the dance language is very similar among species of honeybees, communication of the distance component of the message varies both intraspecifically and interspecifically. However, it is not known whether different honeybee species would attend interspecific waggle dances and, if so, whether they can decipher such dances. Using mixed-species colonies of Apis cerana and Apis mellifera, we show that, despite internal differences in the structure of the waggle dances of foragers, both species attend, and act on the information encoded in each other’s waggle dances but with limited accuracy. These observations indicate that direction and distance communication pre-date speciation in honeybees.     

Form and nature of precopulatory sexual selection in both sexes of a moth

Sexual selection is a process that operates through intrasexual competition and intersexual choice for reproduction in both sexes. Here, we report our work on a polygamous moth, Ephestia kuehniella Zeller (Lepidoptera: Pyralidae), aiming to infer the form and nature of precopulatory sexual selection in males and females. We show that, although a number of traits measured in each sex are correlated with mating success, the primary selection trait in females appears to be abdominal thickness and that in males is aedeagus length. As the female’s abdominal thickness is a reliable signal about the number and developmental stage of eggs, males who select females with thicker abdomens for mating will gain reproductive benefit, i.e., fertilizing more mature eggs. For females, earlier maturation of their eggs makes the females more likely to achieve mating earlier in an uncertain world where there is no guarantee that they will find more males in the future. Sexual selection appears to be the important force behind the evolution of fast egg maturation in females. We show that, under a male-biased sex ratio, more than 20% of mating fails within a few minutes after the aedeagus has penetrated into the female’s genitalia, suggesting that females can assess the features of the male aedeagus before allowing insemination to occur. Dissection and examination of both sexes suggest that a longer aedeagus enhances mating and fertilization efficiency in this species, supporting the notion that sexual selection is a primary force in the evolution of genital variance.     

Eunuchs as better fighters?

Male–male competition for females can significantly affect a male’s reproductive success and hence his fitness. Game theory predicts that an individual should avoid fighting when its future reproductive potential is high, but should fight forcefully when its future reproductive potential is insignificant. When mates are scarce, extreme competition and fatal fighting is expected. We recently showed that Nephilengys malabarensis eunuchs, i.e. sterile spider males that lost their genitals during copulation, become more aggressive during male–male contests. Here, we add crucial comparative data by exploring eunuch fighting behaviour in Nephilengys livida from Madagascar, specifically by testing the ‘better fighter hypotheses’ in a laboratory setting. Similar to N. malabarensis, N. livida copulations resulted in total male castration with the severed palp plugging the female genitals in 70.83% cases, which mostly (63.63%) prevented subsequent copulations. Unexpectedly, however, N. livida eunuchs exhibited lower aggressiveness than virgin males. We interpret these results in the light of different mating biology between the so far studied species known for the eunuch phenomenon, which might reflect differing plug effectiveness due to variation in genital anatomy in N. livida, N. malabarensis and Herennia multipuncta. However, detected differences in aggressive behaviour of N. livida versus N. malabarensis eunuchs might also be explained by the species’ ecology, with lower population densities resulting in a relaxed male–male competition making excessive aggression and mate guarding redundant. This study thus questions the generality of overt aggressiveness in mated males with no reproductive value, and highlights the importance of understanding the natural history of species in the question.     

Avoiding incidental predation by mammalian herbivores: accurate detection and efficient response in aphids

Mammalian herbivores eat plants that may also provide food and shelter for insects. The direct trophic effect of the browsing and grazing of mammalian herbivory on insects, which is probably prevalent in terrestrial ecosystems, has been mostly neglected by ecologists. We examined how the aphid Uroleucon sonchi L. deals with the danger of incidental predation by mammalian herbivores. We found that most (76%) of the aphids in a colony survive the ingestion of the plant by a feeding herbivore. They do so by sensing the combination of heat and humidity in the herbivore’s breath and immediately dropping off the plant in large numbers. Their ability to sense the herbivore’s breath or their tendency to drop off the plant weakens as ambient temperature rises. This could indicate a limitation of the aphids’ sensory system or an adaptation that enables them to avoid the hostile conditions on a hot ground. Once on the ground, U. sonchi is highly mobile and capable of locating a new host plant by advancing in a pattern that differs significantly from random movement. The accurate and efficient defense mechanism of U. sonchi emphasizes the significance of incidental predation as a danger to plant-dwelling invertebrates.     

Women infected with parasite Toxoplasma have more sons

The boy-to-girl ratio at birth (secondary sex ratio) is around 0.51 in most populations. The sex ratio varies between societies and may be influenced by many factors, such as stress and immunosuppression, age, primiparity, the sex of the preceding siblings and the socioeconomic status of the parents. As parasite infection affects many immunological and physiological parameters of the host, we analyzed the effect of latent toxoplasmosis on sex ratios in humans. Clinical records of 1,803 infants born from 1996 to 2004 contained information regarding the mother’s age, concentration of anti-Toxoplasma antibodies, previous deliveries and abortions and the sex of the newborn. The results of our retrospective cohort study suggest that the presence of one of the most common parasites (with a worldwide prevalence from 20 to 80%), Toxoplasma gondii, can influence the secondary sex ratio in humans. Depending on the antibody concentration, the probability of the birth of a boy can increase up to a value of 0.72, C.I.₉₅ = (0.636, 0.805), which means that for every 260 boys born, 100 girls are born to women with the highest concentration of anti-Toxoplasma antibodies. The toxoplasmosis associated with immunosuppression or immunomodulation might be responsible for the enhanced survival of male embryos. In light of the high prevalence of latent toxoplasmosis in most countries, the impact of toxoplasmosis on the human population might be considerable.     

Queue up, please! Spermathecal filling in the rove beetle Drusilla canaliculata (Coleoptera, Staphylinidae)

Most studies on insect sperm motility have been conducted in vitro using artificial environments outside the animal’s body. Only little is known about the function of motile insect sperm at different sites within the male or female genital tracts. We dissected genital tracts of female rove beetles (Drusilla canaliculata) to show that spermatozoa use their own motility to migrate from the spermatophore into the spermatheca. Our dissection method allowed direct observation and filming of the spermathecal filling process inside the female’s genital tract. Spermatozoa were found to enter the spermatheca individually, sometimes in groups of two or three. Although exhibiting only weak motility and no progressive motion in buffer solution, the spermatozoa inside the female show vigorous lashing and reach an average velocity of 47.5 μm s⁻¹. To gain mobility and speed, the spermatozoa likely utilize the relatively small diameter of the spermathecal duct to push themselves off the duct walls, rather than swimming freely in seminal fluid. The spermatozoa (approximately 1,250 μm) are considerably longer than the distance they have to travel along the spermathecal duct (approximately 800 μm). Our study provides the first direct observation of active sperm migration within the female of an insect stressing the importance of the genital tract as a prerequisite for functional sperm motility.     

The Triassic dicynodont Kombuisia (Synapsida, Anomodontia) from Antarctica, a refuge from the terrestrial Permian-Triassic mass extinction

Fossils from the central Transantarctic Mountains in Antarctica are referred to a new species of the Triassic genus Kombuisia, one of four dicynodont lineages known to survive the end-Permian mass extinction. The specimens show a unique combination of characters only present in this genus, but the new species can be distinguished from the type species of the genus, Kombuisia frerensis, by the presence of a reduced but slit-like pineal foramen and the lack of contact between the postorbitals. Although incomplete, the Antarctic specimens are significant because Kombuisia was previously known only from the South African Karoo Basin and the new specimens extend the taxon’s biogeographic range to a wider portion of southern Pangaea. In addition, the new finds extend the known stratigraphic range of Kombuisia from the Middle Triassic subzone B of the Cynognathus Assemblage Zone into rocks that are equivalent in age to the Lower Triassic Lystrosaurus Assemblage Zone, shortening the proposed ghost lineage of this taxon. Most importantly, the occurrence of Kombuisia and Lystrosaurus mccaigi in the Lower Triassic of Antarctica suggests that this area served as a refuge from some of the effects of the end-Permian extinction. The composition of the lower Fremouw Formation fauna implies a community structure similar to that of the ecologically anomalous Lystrosaurus Assemblage Zone of South Africa, providing additional evidence for widespread ecological disturbance in the extinction’s aftermath.