Do echolocation calls of wild colony-living Bechstein's bats (Myotis bechsteinii) provide individual-specific signatures?

Social animals often use vocal communication signals that contain individual signatures. As bats emit echolocation calls several times per second to orient in space, these might seem ideal candidates for conveying the caller's individual identity as a free by-product. From a proximate perspective, however, coding of caller identity is hampered by the simple acoustic structure of echolocation signals, by their task-specific design and by propagation loss. We investigated the occurrence of individual signatures in echolocation calls in individually marked, free-living Bechstein's bats (Myotis bechsteinii) in a situation with defined social context in the field. The bats belonged to two different colonies, for both of which genetic data on relatedness structure was available. While our data clearly demonstrate situation specificity of call structure, the evidence for individual-specific signatures was relatively weak. We could not identify a robust and simple parameter that would convey the caller's identity despite the situation-specific call variability. Discriminant function analysis assigned calls to call sequences with good performance, but worsened drastically when tested with other sequences from the same bats. Therefore, we caution against concluding from a satisfactory discrimination performance with identical training and test sequences that individual bats can reliably be told apart by echolocation calls. At least the information contained in a single call sequence seems not to be sufficient for that purpose. Starting frequencies did give the best discrimination between individuals, and it was also this parameter that was correlated with genetic relatedness in one of our two study colonies. Echolocation calls could serve as an additional source of information for individual recognition in Bechstein's bats societies, while it is unlikely that a large number of individuals could be reliably identified in different situations based on echolocation alone.     

Mean colony relatedness is a poor predictor of colony structure and female philopatry in the communally breeding Bechstein's bat (Myotis bechsteinii)

In order to understand why animals are social and how group members interact with each other it is important to know their relatedness. However, few studies have investigated the genealogy in complete social groups of free-living animals with low reproductive skew. This holds particularly true for bats. Although almost all bat species are social, their sociobiology is not well understood. Because they are volant, nocturnal and have a rather cryptic life-style, bats are difficult to observe in the wild. Furthermore females are generally gregarious making genetic parent-offspring assignment a challenging task. We used genetic markers in combination with knowledge about age and colony membership of individually marked bats to construct pedigrees in completely sampled maternity colonies of Bechstein's bats (Myotis bechsteinii). Despite considerable fluctuations in population size, no immigration occurred over 5 years in four colonies living in close proximity. Additionally, confrontation tests showed that females of one maternity colony were able to detect and attempted to prevent the intrusion of foreign females into a roost they occupy. Although colonies were absolutely closed, and 75% of the colony members lived together with close relatives (rS=0.25), mean colony relatedness was nearly zero (0.02). Average relatedness therefore is a poor estimator for the potential of kin selection in Bechstein's bat colonies and may be misleading when attempting to understand the social structure of animals living in groups where many members breed. Based on our results we discuss the potential adaptive value of living in closed societies with low reproductive skew.     

Differences in sensory ecology contribute to resource partitioning in the bats Myotis bechsteinii and Myotis nattereri (Chiroptera: Vespertilionidae)

Coexisting animal species frequently differ in resource use in at least one niche dimension and thus avoid competition. While a range of morphological differences that lead to differentiation in animals' mechanical access to food have been identified, the role of sensory differences in within-guild niche differentiation has received less attention. We tested the hypothesis that differences in sensory access to prey contribute to resource partitioning between potentially competing species using two sympatric, similar-sized, congeneric bat species as a model system. Nursery colonies of Natterer's bat (Myotis nattereri) and Bechstein's bat (Myotis bechsteinii) roost in bat boxes in the same orchard and forage in forests and orchards nearby. In observations and behavioural experiments with freshly captured M. bechsteinii, we showed that individuals are able to hunt using prey-generated sound alone. In contrast, M. nattereri rarely uses prey-generated sound, but instead is able to find prey by echolocation very close to vegetation. In accordance with these behavioural data, we showed that M. bechsteinii has significantly larger ears than M. nattereri, providing it with superior detection and localization abilities for relatively low-frequency prey rustling sounds. We hypothesized that these differences in sensory ecology of the two syntopic, congeneric species would contribute to resource partitioning, so that M. bechsteinii would find more noisy prey taxa, possibly hidden in vegetation, by listening for prey sounds, while M. nattereri would have better access to still prey using echolocation or associative learning. Analysis of faecal samples collected on the same nights from bat boxes occupied by each species corroborated this prediction. The diets of the two species differed significantly, reflecting their different prey perception techniques and thereby supporting the hypothesis that differences in sensory ecology contribute to niche differentiation. Electronic supplementary material Supplementary material is available for this article at and accessible for authorised users. B.M. Siemers and S.M. Swift contributed equally to this work.     

Foraging areas and foraging behavior in the notch-eared bat,Myotis emarginatus (Vespertilionidae)

Summary Field observations in a maternity colony of Myotis emarginatus (Vespertilionidae) were made during the summers of 1986 and 1987 in southern Germany. The nursery colony consisted of about 90 adult and 30 juvenile bats which roosted in a dimly lit and relatively cool church attic. Telemetry data from six adult M. emarginatus disclosed that some individuals also use secondary day roosts in trees or small buildings located close to their foraging areas. During the night, radiotagged individuals spent most of the time on the wing in forested areas (Fig. 2). Stationary bouts lasted no longer than 63 min. Individual bats returned to the same foraging areas on consecutive nights. All major foraging areas were situated in or at the fringes of forests, at distances as far as 10 km from the nursery roost. During commuting flights to the forests, M. emarginatus avoided open fields and preferred flight paths which offered cover such as orchards, hedges, overhanging foliage along creeks, etc. On the way to the forests, the bats started to forage within buildings, in open spaces where aggregations of insects were present, and around or within the foliage of various types of trees at the level of tree tops or the upper third of the foliage. At these transient foraging areas close to the maternity roost, M. emarginatus displayed flexible foraging strategies: (1) They gleaned prey (mainly flies and spiders) from the substrate, (2) seized insects in aerial pursuit, and (3) occasionally hovered in front of foliage and walls.Our observations confirm the conclusion from morphometric data on the wings that M. emarginatus is a predominantly gleaning bat and contradict the suggestion that it makes only brief flights of short distances. On the contrary, our field data suggest that M. emarginatus spends most of the night on the wing and commutes over distances of at least 10 km. Offprint requests to: D. Krull     

Oceanic residents, neritic migrants: a possible mechanism underlying foraging dichotomy in adult female loggerhead turtles (Caretta caretta)

To reveal the mechanism underlying intrapopulation variation in the use of feeding habitats (oceanic vs. neritic) by adult female loggerhead turtles (Caretta caretta), we compared telomere length in the epidermis (a proxy for age) between oceanic- and neritic-foraging recruits (first-time nesters). Based on egg-yolk stable isotope ratios, recruits at Yakushima Island, Japan, were clearly divided into small oceanic planktivores and large neritic benthivores. There were no significant differences in telomere length between oceanic and neritic foragers, suggesting that they start reproduction at similar ages. Turtles that experienced faster growing conditions during their oceanic early lives may achieve sexual maturity there, while others may move from oceanic areas into neritic habitats, switching diets from nutrient-poor macroplankton to nutrient-rich benthic fauna in order to compensate for their earlier slow growth rate and continue their sexual development, reaching maturity in neritic waters.     

The role of internal and external information in foraging decisions of Melipona workers (Hymenoptera: Meliponinae)

Social insect foragers have to make foraging decisions based on information that may come from two different sources: information learned and memorised through their own experience (“internal” information) and information communicated by nest mates or directly obtained from their environment (“external” information). The role of these sources of information in decision-making by foragers was studied observationally and experimentally in stingless bees of the genus Melipona. Once a Melipona forager had started its food-collecting career, its decisions to initiate, continue or stop its daily collecting activity were mainly based upon previous experience (activity on previous days, the time at which foraging was initiated the day(s) before, and, during the day, the success of the last foraging flights) and mediated through direct interaction with the food source (load size harvested and time to collect a load). External information provided by returning foragers advanced the start of foraging of experienced bees. Most inexperienced bees initiated their foraging day after successful foragers had returned to the hive. The start of foraging by other inexperienced bees was stimulated by high waste-removal activity of nest mates. By experimentally controlling the entries of foragers (hence external information input) it was shown that very low levels of external information input had large effect on the departure of experienced foragers. After the return of a single successful forager, or five foragers together, the rate of forager exits increased dramatically for 15 min. Only the first and second entry events had large effect; later entries influenced forager exit patterns only slightly. The results show that Melipona foragers make decisions based upon their own experience and that communication stimulates these foragers if it concerns the previously visited source. We discuss the organisation of individual foraging in Melipona and Apis mellifera and are led to the conclusion that these species behave very similarly and that an information-integration model (derived from Fig. 1) could be a starting point for future research on social insect foraging. Received: 16 April 1997 / Accepted after revision: 30 August 1997     

Assured fitness returns favor sociality in a mass-provisioning sweat bee,Megalopta genalis (Hymenoptera: Halictidae)

Assured fitness returns models for the evolution of sociality emphasize the selective value of ensuring that offspring receive adequate parental care to reach maturity. If a member of a social group dies, it can accrue returns on investment in offspring through the efforts of surviving social partners. We provide evidence that in the mass-provisioning, facultatively social sweat bee Megalopta genalis, adult presence in the nest throughout brood development provides protection from ant predation. Nests with adults present were well protected, and brood in nests with adults removed suffered higher predation. Females in observation nests showed effective defensive behavior against experimentally introduced ants, and bees in natural nests repulsed naturally occurring ant raids. Megalopta nest architecture and behavior are such that the brood of several cooperating females can be defended with little additional cost relative to solitary nesting. The benefits of cooperative defense may favor group living in mass provisioning bees. Our observations and experiments suggest that parental care throughout brood development can be adaptive in mass provisioning species, supporting the predictions of assured fitness returns models.     

The benefits of multiple mating to female seaweed flies, Coelopa frigida (Diptera: Coelpidae)

Female seaweed flies, Coelopa frigida, have the potential to benefit from mating more than once. Single matings result in low fertility so females may benefit directly from multiple copulations by sperm replenishment. A chromosomal inversion associated with larval fitness, with heterokaryotypic larvae having higher viability than homokaryotypes, means that polyandrous homokaryotypic females have a higher probability of producing genetically fit offspring than monandrous homokaryotypic females. We allowed females to mate only once, repeatedly four times to the same male, or polyandrously four times to four different males. Multiply mated and polyandrous females laid more eggs and produced more offspring than singly mated and monandrous females, respectively. Polyandrous females laid more eggs, had higher egg-to-adult survival rates and produced more offspring than repeatedly mated females. Fertility rates did not differ between treatments. The observed fitness patterns therefore resulted from increased oviposition through multiple mating per se, and a further increase in oviposition coupled with higher egg-to-adult offspring survival benefits to polyandry. Daily monitoring of individual females over their entire life spans showed that multiple copulations induced early oviposition, with polyandrous females ovipositing earlier than repeatedly mated females. Singly mated and polyandrous females incurred a longevity cost independent of egg production, whereas repeatedly mated females did not. This suggests that repeatedly mating with the same male may counteract a general cost of mating. Longevity, however, was not correlated with overall female fitness. Our data are discussed in the overall context of the seaweed fly mating system.Communicated by G. Wilkinson     

Parasitic flies (Diptera: Phoridae) influence foraging rhythms and caste division of labor in the leaf-cutter ant,Atta cephalotes (Hymenoptera: Formicidae)

Summary Three lines of evidence, including interspecific comparisons, temporal division of foraging between size castes, and experimental manipulations, suggest that the diurnal parasitoid Neodohrniphora curvinervis (Diptera: Phoridae) influences both the caste sizes and numbers of leaf-cutter ants (Atta cephalotes) that leave their underground nests to collect leaves. At Parque Nacional Corcovado in Costa Rica, A. cephalotes was attacked by Neodohrniphora during the daytime, and foraged less during the day than at night; a closely related ant at the same site, A. colombica, had no phorid parasites and foraged exclusively during the day. Most daytime foragers of A. cephalotes were smaller than the lower size threshold for attack by Neodohrniphora, while nocturnal foragers, active when parasitoids were absent, were both larger than this threshold and within the energetically optimal size range for foraging. When I supplied artificial lighting to allow phorids to hunt at A. cephalotes colonies past dusk, ants foraged less than when light was provided but flies were removed. The influence of Neodohrniphora on the foraging activity of A. cephalotes may explain why investigations focusing on abiotic factors have largely failed to discover what drives this ant's daily foraging cycles, and suggests that forager sizes are influenced not only by energetic efficiency, but also by the threat of parasitism.     

Sperm transfer,displacement and precedence in Ischnura graellsii (Odonata : Coenagrionidae)

Summary Copulation in Ischnura graellsii may be divided into three stages, according to the movements and position of the male's abdomen. We measured sperm volumes in males and females interrupted at different phases of copulation in laboratory-reared and field specimens. The results showed that males remove sperm from the female during stage I, and do not transfer sperm until stage Il of the copulation. In the field females interrupted during stage I of copulation had less sperm than postcopula females, and the volume of sperm in laboratory females mated once or twice was similar. These results suggest that males can remove most of the sperm during stage I of copulation. Preparations of in-copula specimens showed the horns of the penis (used to remove sperm) inside the bursa copulatoox and the spermatheca. Therefore males can remove sperm from both organs, in contrast to the other Ischnura species so far studied, where males can empty only the bursa. The length of these horns is positively correlated with male body length, and there are significant differences in length between the left and right horns of individual males. This suggests great variability in the male's ability to remove sperm. On the other hand, ejaculate volume is positively related to male and female size, and negatively to male age. Males are likely to be able to detect the presence of sperm in females: if the effect of population density and time of start of copulation are taken into account, copulations are longer with mated than with virgin females. Using genetic markers, sperm precedence was studied by rearing the female offspring of 6 females mated with two males of different genotype. In 5 out of 6 crosses, the second male fertilized all the eggs laid by the female in her first clutch. On average, the following clutches were progressively more fertilized by the first male, but there were striking differences between crosses. These differences are probably due to the variability in the amount of sperm transferred and/or removed. Offprint requests to: A. Cordero     

Development and expression of sexual maturity in femaleCalanus pacificus (Copepoda: Calanoida) in relation to food quality

Dinoflagellates, which comprise an important part of the phytoplankton in the neritic region of the Southern California Bight, are known to be grazed byCalanus pacificus; rates of ingestion, development and survival of nauplii are influenced by the food quality of dinoflagellates. We have examined the effects of dinoflagellate food quality on reproduction ofC. pacificus females sampled in La Jolly Bay (32°N; 117°W) between 6 April and 4 May 1988. Four sets of experiments were conducted in which copepods were fed five different species:Gymnodinium splendens, Gyrodinium resplendens., G. dorsum, Exuviella mariae lebourae andGymnodinium simplex. These species were selected on the criterion of their success in supporting the growth of nauplii in previous rearing experiments. The experimental culture concentration was maintained at 100µg C 1^–1, near that of the natural seston. As indices of successful reproduction, we measured the percentage of spawning females and the number of eggs laid per female per day. Laboratory results were compared to stages of ovarian maturation of wild females. Four stages of maturation were determined using histological and microscopic observations.Gymnodinium splendens, Exuviella mariae lebourae, andG. simplex yielded clearly inferior results: few females were able to lay eggs repetitively over the first few days of confinement.Gyrodinium resplendens and, above all,G. dorsum yielded the best results. The stage of sexual maturation in situ appears to influence the rhythmicity of egg-laying events. In the presence of high-quality food, females are able to maintain high reproductive rates by sustaining the maturation of successive batches of eggs; good food quality appears to assure this secondary vitellogenesis and the rapid turnover of ovocytes.     

Mating expenditures reduced via female sex pheromone modulation in the primitively eusocial halictine bee, Lasioglossum (Evylaeus) malachurum (Hymenoptera: Halictidae)

The present paper reports on behavioral experiments and gas chromatographic analysis of chemical communication in the mating biology of the primitively eusocial sweat bee Lasioglossum (Evylaeus) malachurum. In a dual-choice experiment, a female made odorless was significantly less attractive than an untreated one. Attraction in L. (Evylaeus) malachurum is therefore mediated by a female-produced sex pheromone. Further bioassays showed that unmated gynes are more attractive to males than mated ones. Males are able to differentiate between the two groups of females as little as 3 h after mating. Biotests with different samples obtained from attractive gynes showed surface extracts to be most attractive. Behavioral tests with synthetic copies of the compounds identified as cuticular constituents of virgin gynes were highly attractive to males; the volatile bouquets consisting of n-alkanes, n-alkenes and iso- pentenyl esters of unsaturated fatty acids were the most attractive samples. Isopentenyl esters of unsaturated fatty acids were the key compounds in inducing male inspections as well as stimulating pounces and copulatory attempts. Virgin and nesting gynes differed clearly in the relative and absolute amounts of the volatiles on the cuticle. The total amount of volatiles was significantly higher in virgin gynes and decreased in breeding queens. Hydrocarbons were the dominant group of compounds in both groups of females. The relative amounts of the wax-type ester, hexadecyl oleate, iso- pentenyl esters, and a hitherto unidentified steroid were higher in attractive virgin gynes, while the relative proportions of hydrocarbons and lactones dominated in nesting queens. The site of sex pheromone production in attractive young L. (Evylaeus) malachurum gynes remains unknown. Head glands or Dufour's gland secretions may be involved. Another possible source of the `active principle' found among the cuticular lipids could be glandular cells of the epidermis. The significance of modulation of female sex pheromone composition is discussed in terms of a reduction in mating expenditures. Received: 30 April 1998 / Accepted after revision: 24 July 1998