Does Interspecific Eavesdropping Promote Aerial Aggregations in European Pipistrelle Bats During Autumn?

Eavesdropping is a widespread strategy to optimize decision‐making. Bats are interesting models for investigating acoustic information transfer, as they possess a broad vocalization repertoire of echolocation and social calls. Yet, the knowledge of the extent to which eavesdropping plays a role in bat communication is scarce. Here, we examined the vocal and spatial activity patterns of three congeneric bat species (Pipistrellus pipistrellus, P. pygmaeus, P. nathusii, hereafter called pipistrelles) during autumn – their migration and mating season. We hypothesized that pipistrelles utilize information of conspecifics and congenerics to localize stopover sites for mating or other information purposes during migration. We found that bats formed small multispecies aggregations on the wing, suggesting interspecific eavesdropping on feeding buzzes and/or courtship calls could occur among these species. Pipistrelles produced similar proportions of feeding buzzes and social calls at aggregation sites. To test whether pipistrelles respond to the courtship vocalizations of conspecifics and congenerics, we conducted a playback experiment with P. pipistrellus where we presented courtship vocalizations of the three pipistrelle species and as a control, a motif of the noctule bat's song (Nyctalus noctula). Pipistrellus pipistrellus decreased the rate of social calls in response to the broadcast of songs of P. nathusii, yet they tended to increase the rate in response to the playback of their own species. We conclude that interspecific eavesdropping occurs at least between P. pipistrellus and P. nathusii and might thus favour the formation of multispecies aggregations. Our findings provide novel insights into the social behaviour and interspecific communication of a bat community during the season of migration and mating.     

Multiplex panels of polymorphic microsatellite loci for two cryptic bat species of the genus Pipistrellus,developed by cross‐species amplification within the family Vespertilionidae

The paper presents multiplex panels of polymorphic microsatellites for two closely related cryptic species Pipistrellus pipistrellus and Pipistrellus pygmaeus. We tested the cross‐species amplification of 34 microsatellite loci, originally developed for five vespertilionid bat species. Ten and nine polymorphic loci in P. pipistrellus (mean number of alleles per locus = 10.5) and P. pygmaeus (8.1), respectively, in three multiplex polymerase chain reactions per species were amplified. All loci can be analysed in a single fragment analysis and can be used as markers to the study of evolution and the ecology of structured populations of socially living bats.     

Interspecific responses to distress calls in bats (Chiroptera: Vespertilionidae): a function for convergence in call design?

Distress calls were recorded from three sympatric species of pipistrelle bat (Pipistrellus nathusii, P. pipistrellus and P. pygmaeus) in England and Northern Ireland. At foraging sites, we conducted playback experiments, consisting of experimental distress call sequences from each species and control sequences of random noise and sound recorded with no bats present. We measured response by simultaneously recording ultrasound during playbacks and counting the echolocation pulses above a predetermined threshold which were then identified to species. All three species responded to each other's calls. The number of recorded echolocation pulses of all species increased eight-fold, on average, during the playback of distress call sequences compared with the playback of ultrasonic noise, and four-fold compared with the playback of silence. In a separate playback experiment, the number of echolocation pulses of P. pygmaeus increased 14-fold during the playback of distress calls of four endemic species of bat from Madagascar (Emballonura atrata, Myotis goudoti, Miniopterus majori and M. manavi) compared with the playback of silence. This increased response might have been caused by the high calling rates of the Malagasy species. Distress calls of P. nathusii, P. pipistrellus and P. pygmaeus were structurally convergent, consisting of a series of downward-sweeping, frequency-modulated elements of short duration and high intensity with a relatively strong harmonic content. Selection may favour convergence in the structure of distress calls among bat species, if attracting heterospecifics increases the chance of repelling predators by mobbing.     

An appetite for pests: Synanthropic insectivorous bats exploit cotton pest irruptions and consume various deleterious arthropods

Conservation biological control (CBC) seeks to minimize the deleterious effects of agricultural pests by enhancing the efficiency of natural enemies. Despite the documented potential of insectivorous bats to consume pests, many synanthropic bat species are still underappreciated as beneficial species. We investigated the diet of Kuhl's pipistrelle (Pipistrellus kuhlii), a common synanthropic insectivorous bat that forages in urban and agricultural areas, to determine whether it may function as a natural enemy in CBC. Faecal samples of P. kuhlii were collected throughout the cotton‐growing season from five roost sites near cotton fields located in a Mediterranean agroecosystem, Israel, and analyzed using DNA metabarcoding. Additionally, data on estimated abundance of major cotton pests were collected. We found that the diet of P. kuhlii significantly varied according to sites and dates and comprised 27 species of agricultural pests that were found in 77.2% of the samples, including pests of key economic concern. The dominant prey was the widespread cotton pest, the pink bollworm, Pectinophora gossypiella, found in 31% of the samples and in all the roosts. Pink bollworm abundance was positively correlated with its occurrence in the bat diet. Furthermore, the bats’ dietary breadth narrowed, while temporal dietary overlap increased, in relation to increasing frequencies of pink bollworms in the diet. This suggests that P. kuhlii exploits pink bollworm irruptions by opportunistic feeding. We suggest that synanthropic bats provide important pest suppression services, may function as CBC agents of cotton pests and potentially contribute to suppress additional deleterious arthropods found in their diet in high frequencies.     

Phenotypic integration and the evolution of signal repertoires: A case study of treefrog acoustic communication

Animal signals are inherently complex phenotypes with many interacting parts combining to elicit responses from receivers. The pattern of interrelationships between signal components reflects the extent to which each component is expressed, and responds to selection, either in concert with or independently of others. Furthermore, many species have complex repertoires consisting of multiple signal types used in different contexts, and common morphological and physiological constraints may result in interrelationships extending across the multiple signals in species’ repertoires. The evolutionary significance of interrelationships between signal traits can be explored within the framework of phenotypic integration, which offers a suite of quantitative techniques to characterize complex phenotypes. In particular, these techniques allow for the assessment of modularity and integration, which describe, respectively, the extent to which sets of traits covary either independently or jointly. Although signal and repertoire complexity are thought to be major drivers of diversification and social evolution, few studies have explicitly measured the phenotypic integration of signals to investigate the evolution of diverse communication systems. We applied methods from phenotypic integration studies to quantify integration in the two primary vocalization types (advertisement and aggressive calls) in the treefrogs Hyla versicolor, Hyla cinerea, and Dendropsophus ebraccatus. We recorded male calls and calculated standardized phenotypic variance–covariance ( P ) matrices for characteristics within and across call types. We found significant integration across call types, but the strength of integration varied by species and corresponded with the acoustic similarity of the call types within each species. H. versicolor had the most modular advertisement and aggressive calls and the least acoustically similar call types. Additionally, P was robust to changing social competition levels in H. versicolor. Our findings suggest new directions in animal communication research in which the complex relationships among the traits of multiple signals are a key consideration for understanding signal evolution.     

Echolocation calls produced by Kuhl's pipistrelles in different flight situations

Flexibility in the echolocation call structure of bats can improve their performances, because, in some situations, some signal designs are better than others. Hence, at least some bats should adjust their echolocation calls according to the setting in which they are operating but also to the specific task at hand, that is their behavioral intention. We studied variation in the echolocation calls of Pipistrellus kuhlii emitted during four flight situations that were similar in setting but differed in behavioral context: emergence from a roost, commuting to and from foraging sites, foraging and returning to a roost. Echolocation calls produced by P. kuhlii differed significantly according to the flight situation. Call types differed most distinctly between foraging and commuting. We also found a high variance in the emergence calls we recorded, perhaps reflecting pre- and post-takeoff calls. Discriminant function analysis on calls emitted while foraging, commuting or returning to the roost classified the calls to the correct group 73.3% of the time. The differences between bats' echolocation calls in different flight situations might indicate an intrinsic change in the bat's behavior. Recognizing these differences could be crucial when using call variables to identify bat species.     

Genetic variability analyses of the somatic embryogenesis induction process in Olea spp. using nuclear microsatellites

The crop species Olea europaea L. (olive tree) is of great economic importance in the Mediterranean region. Hence, many efforts have been done in the last decades to propagate this commercially valuable species by in vitro methods. On the other hand, the lesser known Olea maderensis (Lowe) Rivas Mart. & Del Arco which is a native species of the Madeira Archipelago has only been the subject of micropropagation from nodal stem cuttings. Therefore, in this work we analysed the stability of ten nuclear simple sequence repeat (SSR) markers at successive stages of the somatic embryogenesis process in two adult trees belonging to these two species from the Madeira Archipelago. For the induction of somatic embryogenesis, petiole and leaf explants were cultivated on solid Murashige and Skoog medium (MS) with 12.25 μM indole-3-butyric acid (IBA) and 4.56 μM of zeatin, in the dark. After 3 months, different callus tissues (non-embryogenic, pre-embryogenic and embryogenic) developed from leaf explants and petioles were later transferred to MS medium without growth regulators in the dark. All ten SSR markers were able to distinguish between species. However, no mutations were found at the SSR loci at any of the successive developmental stages from PEMs (pre-embryogenic masses) to somatic embryos. This genetic uniformity was observed within material derived from each genotype/species and its respective donor plant. Therefore, we conclude that the genomic integrities of both O. europaea and O. maderensis were maintained throughout the stages of the embryogenic processes in study suggesting the absence of somaclonal variation.     

Can pipistrelles, Pipistrellus pipistrellus (Schreber, 1774) and Pipistrellus pygmaeus (Leach, 1825), foraging in a group, change parameters of their signals?

Echolocation behaviour and the structure of calls of Pipistrellus pygmaeus and Pipistrellus pipistrellus were studied by using a time expansion bat detector. Echolocation signals were recorded in the field in south-eastern Moravia and northern Bohemia (Czech Republic) and in an ad hoc experimental laboratory. For each of the species, multivariate analysis of variance (MANOVA) indicated significant differences in calls produced inside the experimental room and in the open. Paired t -tests and MANOVA were also used to reveal influences of interindividual contacts in each of the cryptic species on the spectral patterns of call variables. Differences were found in the spectral variables of echolocation calls of an individual flying in the room alone and in a group of conspecifics. The possibility that bats use their flexibility to avoid mutual disturbances of echolocation calls was tested. We found that bats flying in a group modify the parameters of their echolocation signals according to the presence of other individuals of the same species. These differences can indicate jamming avoidance and recognition of own echoes. However, they did not change the parameters if individuals of another species were present. Social calls are more numerous when bats fly in a mixed-species group than in a monospecific group.     

Managing anthropogenic driven range expansion behaviourally: Mediterranean bats in desert ecosystems

Bat abundance and activity in deserts is affected by the distribution of water sources. Kuhl’s pipistrelle (Pipistrellus kuhlii) is one of several bat species that penetrated the Negev desert from Mediterranean habitats following anthropogenic development, and potentially competes with desert dwelling bats of the same guild. Pipistrellus kuhlii is an obligate drinker requiring a clear ‘swoop zone’ to drink. Thus, to reduce the competitive load that P. kuhlii has on desert dwelling species, we tested the effectiveness of obstructions above water surfaces, which we hypothesised would reduce the drinking ability of P. kuhlii, thus providing desert species a competitive edge. We obstructed the water surface of a swimming pool and successfully prevented P. kuhlii from drinking. Next, we manipulated natural water sources used by bats for foraging. This was done on two spatial and temporal scales: on 11 adjacent ephemeral water pools in Nahal Zin where each treatment was applied for several nights and on eight isolated natural pools in the Negev where treatments were alternated every 20 min. Manipulation of adjacent pools had no effect on activity levels of bats, but in isolated pools, the obstruction reduced the proportion of P. kuhlii activity by up to 15%. Although this tool cannot be used for management without further examination of its long-term effects on other bats and wildlife, this study does demonstrate its feasibility. Conservation schemes aiming to mitigate effects of undesirable species can be designed by identifying ecological differences between competing species, and manipulating the environment accordingly.     

Syntax manipulation changes perception of mobbing call sequences across passerine species

Many species approach predators to harass them and drive them away. Both the intensity of this antipredator strategy and its success are positively related to the size of the group that carries out this mobbing. To recruit individuals to the mob, members of prey species produce mobbing calls. In some songbirds—the Japanese tit, Parus minor, and the southern pied babbler, Turdoides bicolor—mobbing calls are structurally complex and it has been suggested that they convey information by means of compositional syntax, when meaningful items are combined into larger units. These two species combine alert and recruitment calls into an alert and recruitment sequence when attracting conspecifics to cooperate in mobbing a predator. Whether this rudimentary, two‐call, compositional structure is used by other bird species in mobbing calls and how it can alter the ability of heterospecifics to adequately recognize mobbing calls is not well understood. Heterospecifics’ responses to mobs are critical to the success of the mobbing strategy, so it is of great importance to understand whether and how syntax influences these responses. To address these questions, we conducted two playback experiments. Firstly, we investigated whether the great tit, Parus major, extracts different meanings from different individual motifs (i.e., component calls), and from combined motifs in both natural and artificially reversed order. We found that great tits extract different meanings from the two motifs involved in mobbing calls and that they also discriminate for motif order reversal in the mobbing call sequence. Secondly, we investigated whether heterospecifics (the coal tit, Periparus ater, and the common chaffinch, Fringilla coelebs) are sensitive to syntax alteration of great tit mobbing calls. While chaffinches did not respond to great tit mobbing calls, coal tits were sensitive to mobbing call sequence reversal although they did not react in the same way as conspecific subjects. Overall, whereas our results indicate that tits are sensitive to call reversal, this is not to say that tits actually use compositional syntax to increase the information content.     

An investigation of the cochlear microphonic response of two species of echolocating bats:Rousettus aegyptiacus (geoffroy) andPipistrellus pipistrellus (Schreber)

Summary The cochlear microphonic (CM) responses of two species of echolocating bats:Rousettus aegyptiacus andPipistrellus pipistrellus have been investigated (Figs. 1 and 3) and the responses have been shown to have a single major peak corresponding with the lower range of frequencies produced in echolocation.My thanks are due to Professor Don R. Arthur for providing laboratory facilities for this work and Dr. J. D. Pye for advice during this study and for much valuable unpublished information on calls produced by the bats in this study, and also to Dr. P. Racey for the pipistrelles. This research was made possible by a Science Research Council grant and was sponsored in part by the Air Force Office of Scientific Research under contract number AF61(052)-876 to Dr. Pye. The author was a Harold Row student of King's College.     

Tillage and herbicide reduction mitigate the gap between conventional and organic farming effects on foraging activity of insectivorous bats

The increased use of pesticides and tillage intensification is known to negatively affect biodiversity. Changes in these agricultural practices such as herbicide and tillage reduction have variable effects among taxa, especially at the top of the trophic network including insectivorous bats. Very few studies compared the effects of agricultural practices on such taxa, and overall, only as a comparison of conventional versus organic farming without accurately accounting for underlying practices, especially in conventional where many alternatives exist. Divergent results founded in these previous studies could be driven by this lack of clarification about some unconsidered practices inside both conventional and organic systems. We simultaneously compared, over whole nights, bat activity on contiguous wheat fields of one organic and three conventional farming systems located in an intensive agricultural landscape. The studied organic fields (OT) used tillage (i.e., inversion of soil) without chemical inputs. In studied conventional fields, differences consisted of the following: tillage using few herbicides (T), conservation tillage (i.e., no inversion of soil) using few herbicides (CT), and conservation tillage using more herbicide (CTH), to control weeds. Using 64 recording sites (OT = 12; T = 21; CT = 13; CTH = 18), we sampled several sites per system placed inside the fields each night. We showed that bat activity was always higher in OT than in T systems for two (Pipistrellus kuhlii and Pipistrellus pipistrellus) of three species and for one (Pipistrellus spp.) of two genera, as well as greater species richness. The same results were found for the CT versus T system comparison. CTH system showed higher activity than T for only one genus (Pipistrellus spp.). We did not detect any differences between OT and CT systems, and CT showed higher activity than CTH system for only one species (Pipistrellus kuhlii). Activity in OT of Pipistrellus spp. was overall 3.6 and 9.3 times higher than CTH and T systems, respectively, and 6.9 times higher in CT than T systems. Our results highlight an important benefit of organic farming and contrasted effects in conventional farming. That there were no differences detected between the organic and one conventional system is a major result. This demonstrates that even if organic farming is presently difficult to implement and requires a change of economic context for farmers, considerable and easy improvements in conventional farming are attainable, while maintaining yields and approaching the ecological benefits of organic methods.     

Habitat usage of Daubenton's bat (Myotis daubentonii), common pipistrelle (Pipistrellus pipistrellus), and soprano pipistrelle (Pipistrellus pygmaeus) in a North Wales upland river catchment

Distributions of Daubenton's bat (Myotis daubentonii), common pipistrelle, (Pipistrellus pipistrellus), and soprano pipistrelle (Pipistrellus pygmaeus) were investigated along and altitudinal gradient of the Lledr River, Conwy, North Wales, and presence assessed in relation to the water surface condition, presence/absence of bank‐side trees, and elevation. Ultrasound recordings of bats made on timed transects in summer 1999 were used to quantify habitat usage. All species significantly preferred smooth water sections of the river with trees on either one or both banks; P. pygmaeus also preferred smooth water with no trees. Bats avoided rough and cluttered water areas, as rapids may generate high‐frequency echolocation‐interfering noise and cluttered areas present obstacles to flight. In lower river regions, detections of bats reflected the proportion of suitable habitat available. At higher elevations, sufficient habitat was available; however, bats were likely restricted due to other factors such as a less predictable food source. This study emphasizes the importance of riparian habitat, bank‐side trees, and smooth water as foraging habitat for bats in marginal upland areas until a certain elevation, beyond which bats in these areas likely cease to forage. These small‐scale altitudinal differences in habitat selection should be factored in when designing future bat distribution studies and taken into consideration by conservation planners when reviewing habitat requirements of these species in Welsh river valleys, and elsewhere within the United Kingdom.     

Diet and prey selection in Kuhl’s pipistrellePipistrellus kuhlii (Chiroptera: Vespertilionidae) in south-western Europe

The trophic ecology of Kuhl’s pipistrellePipistrellus kuhlii (Kuhl, 1817) was investigated monthly from May to October 1999. Nine insect and two arachnid orders were identified in faeces and classified in 24 different categories. The most frequently occurring prey categories were Culicidae, Lepidoptera, Chironomidae/Ceratopogonidae, Hymenoptera, unidentified Brachycera, Tipulidae and unidentified Coleoptera in decreasing order. Other categories exhibited seasonal importance, such as the coleopteranRhizotrogus sp. Prey availability was evaluated monthly using Malaise traps in known feeding areas. Bats preyed selectively through a temporarily changing pattern. Some taxa constituted an important part of the diet and were positively selected either monthly or in most of the months. Many of them were the largest prey featuring in the diet and changes of their relative profitability across time would determine their selection index. The small size of some prey categories as well asP.kuhlii’s morphofunctional constraints relative to flight and echolocation could explain their underexploitation or rejection. Our results suggest thatP. kuhlii could be regarded as a ‘selective opportunist’ species.     

Isolation and characterization of microsatellite loci in the Japanese pipistrelle (Pipistrellus abramus)

We describe the first set of ten microsatellite markers isolated in Pipistrellus abramus. The number of alleles per locus ranged from 7 to 13. The observed and expected heterozygosities values ranged from 0.486 to 0.971 and from 0.752 to 0.876, respectively. Three loci revealed significant departure from Hardy–Weinberg equilibrium and no linkage disequilibrium was found between loci pairs. These informative microsatellite markers will be a powerful molecular tool for studying the population genetic structure of P. abramus, as well as other species of this genus.     

日本伏翼的翼型、回声定位信号及出飞时间特征

对日本伏翼的翼型、回声定位信号及晚间出飞时间进行研究。结果表明,日本伏翼的翼型具有高翼载、低翼展比和中等偏高的翼型特征。日本伏翼发出具有1 - 2 个谐波结构的调频型(FM)回声定位信号叫声,其叫声时程、主频率的平均值分别为3.26 ms 和56. 27 kHz,所有叫声特征参数,个体间变异系数CVb 比个体内变 异系数CVw 大。日本伏翼的晚间出飞时间具有明显月变化,与当地日落时间、气温呈现显著相关。通过与文献比较,发现日本伏翼的回声定位信号特征与录音状态、飞行生境有关;此外,晚间出飞时间存在一定的地理差异。本研究结果将为蝙蝠回声定位信号特征的种属特异性及其生境选择的进一步研究提供有用的信息。     

Temporal and spatial differences in the emission of calls by pipistrelle bats<Emphasis Type="Italic">Pipistrellus pipistrellus</Emphasis> and<Emphasis Type="Italic">P. pygmaeus</Emphasis>

The number of orientation, feeding and social calls emitted by pipistrelle batsPipistrellus pipistrellus Schreber, 1774 andP. pygmaeus Leach, 1825 was recorded throughout the night at eight different sites. Social calls were unaffected by weather variables, whereas orientation calls and feeding buzzes were both significantly affected by cloud and temperature conditions. The number of emissions of each call type was significantly different between sites, indicating that the bats used different sites for different activities. Significant positive correlations between all three combinations of call types occurred only during the middle of the night, corresponding with the nadir of flying insects. This suggests that bats were engaged in activities other than feeding at this time, such as territory protection or mate attraction.     

Phenotypic diversification and island evolution of pipistrelle bats (Pipistrellus pipistrellus group) in the Mediterranean region inferred from geometric morphometrics and molecular phylogenetics

Aim The Mediterranean Basin is a centre of radiation for numerous species groups. To increase our understanding of the mechanisms underlying speciation and radiation events in this region, we assessed the phenotypic variability within the Pipistrellus pipistrellus–pygmaeus–hanaki species complex. Although bats form the second largest mammalian order, studies of insular evolution in this group are scarce. We approached this problem from a microevolutionary perspective and tested for the recurrence of the insular syndrome. Location The Mediterranean Basin, with a special focus on isolated populations from Corsica, the Maghreb, Cyprus, Cyrenaica and Crete. Methods Phenotypic variability was assessed by cranial morphometrics using the coordinates of 41 3D landmarks and associated geometric‐morphometric methods. We analysed 125 specimens representing all of the lineages in the species complex. Differences between taxa and between insular and continental populations in cranial size, shape, form and allometries were tested using analyses of variance and visualized using boxplots and canonical variate analysis. Relationships between molecular data from a previous study (cytochrome b sequences) and morphometric data were tested with co‐inertia analyses (RV test) and multivariate regressions. Results The three species were relatively well differentiated in cranial size and shape, and each species showed a significant amount of inter‐population variability. Comparisons of pairs of insular versus continental populations revealed heterogeneities in cranial patterns among island phenotypes, suggesting no recurrent insular syndrome. Molecular and phenotypic traits were correlated, except for molecular and lateral cranium shape. Main conclusions The Pipistrellus pipistrellus – pygmaeus – hanaki species complex exhibits phenotypic variability as a result of the fragmentation of its distribution (especially on islands), its phylogenetic and phylogeographic history and, most probably, other evolutionary factors that were not investigated in this study. We found no recurrent pattern of evolution on islands, indicating that site‐specific factors play a prevailing role on Mediterranean islands. The correlation between molecular and phenotypic data is incomplete, suggesting that factors other than phylogenetic relationships, potentially connected with feeding ecology, have played a role in shaping cranial morphology in this species complex.