Phonic Types Research Articles

Habitat Use of Constant Frequency Echolocating Bats in North-West Madagascar with Acoustic Evidence for a Possible New Species

Bioacoustics can be a non-invasive, cost-effective way of studying echolocating bats, and is especially useful for detecting and identifying rare or cryptic species. The insectivorous bats of Madagascar are understudied in comparison to the rest of the island's fauna, and very little is known about their habitat use. Here, we used a remote bioacoustic surveying technique in a bat survey of the Sahamalaza-Îles Radama National Park, northwest Madagascar, to study constant frequency echolocating bats (Hipposideridae and Rhinonycteridae). We used two passive acoustic monitoring units to automatically record bat activity from dusk until dawn in a range of habitat types that are characteristic of the region. Analysis of call acoustic parameters revealed three distinct constant-frequency phonic types within the national park, which we identified as Commerson's leaf-nosed bat (Macronycteris commersoni), the red trident bat (Triaenops menamena) and an unknown phonic type of ca. 78 kHz. We found significant differences in the habitat usage of these three species, suggesting species-specific habitat preferences among Madagascar's bats. Our statistical analyses revealed significant differences between the acoustic echolocation calls of these three phonic types. The 78 kHz calls do not match any of the other constant frequency-calling bat species currently described for Madagascar, indicating either acoustic divergence among bat sub-populations or the possible existence of a new undescribed species. These results highlight the need for increased survey efforts to gain an understanding of species-specific geographic distributions and habitat usage among Malagasy bats and to disentangle their cryptic species complexes.

Cryptic Diversity in Common Mustached BatsPteronotuscf.parnellii(Mormoopidae) in French Guiana and Brazilian Amapa

The common mustached bat (Pteronotus parnellii) is a mormoopid bat living in caves in lowland rainforests throughout the north and eastern Neotropics, including several Caribbean islands. Recent studies have shown that this taxon is certainly a composite of several cryptic species, especially in the western part of the Guianan Shield, where molecular reconstructions and bioacoustics point to the presence of at least two cryptic species that may not be related to genuine P. parnellii, native to Jamaica. We examined here over 200 bioacoustically identified individuals to show that two phonic types live in sympatry in French Guiana with no overlap in frequencies of echolocation calls. Morphological variation in some skull characters showed consistent and significant differences between the two phonic types, whereas external measurements alone were unable to discriminate between groups. Two mitochondrial markers analyzed in a selection of each of these phonic types were further used to evidence that they represent two genetically discrete groups, and to assign them to the existing molecular clades described elsewhere. Molecular comparisons with reference specimens sampled near the type localities of P. parnellii and P. rubiginosus further suggest that the 53 kHz phonic type found in French Guiana and Amapa (Brazil) should be assigned to the later species, while the 59 kHz phonic type represents an undescribed species.

Sibling species in South Indian populations of the rufous horse-shoe bat Rhinolophus rouxii

Cryptic species are difficult to identify using morphological identification tools. They represent hitherto unknown biodiversity and their discovery helps formulate more efficient conservation management policies. In this study we assess intraspecific diversity of Rhinolophus rouxii and investigate the presence of cryptic lineages. We characterize acoustic, morphological and genetic differences between allopatric populations of this species in Southern India. Our results reveal the presence of two distinct acoustic lineages (80 and 90 kHz phonic types). Forearm length also differs significantly between the two phonic types. They share a sister taxa relationship and the average genetic distance between them is over 8 %. Phylogenetic reconstruction and the associated divergence time suggest an evolutionary history that correlates with a middle Miocene separation. We propose that these two phonic types be called sibling species and evolutionarily significant units (ESU) within the subgenus Indorhinolophus. We recommend a new name, R. indorouxii for the species representing the 90 kHz phonic type. This study reiterates our lack of accurate taxonomic knowledge of bats, and highlights the value in combining genetics with behavioral (phonic characterization) and morphological measurements in the discovery of cryptic species.

A Taxonomic Review of theHipposideros bicolorSpecies Complex andH. pomona(Chiroptera: Hipposideridae) in Thailand

Following extensive field work in Thailand (2006–2008), this paper reviews the taxonomic status of the three species of the Hipposideros bicolor group. Based on morphometric characters and acoustic data, the two phonic types, H. bicolor (131 kHz) and H. bicolor (142 kHz) are treated as distinct species. Hipposideros bicolor (131 kHz) is designated as H. bicolor; H. bicolor (142 kHz) is provisionally designated as H. atrox. The morphometric characters, acoustic data, and geographical distribution of H. pomona are also reviewed. The diagnostic characters of these frequently confused taxa are discussed, with a detailed study of the external, cranio-dental, and bacular morphology, and acoustic features. New data on the conservation status, distribution and ecology of these three species are included.

Insectivorous Bat Activity at Cenotes in the Yucatan Peninsula, Mexico

The behaviour and habitat associations of aerial insectivorous bats are poorly understood despite constituting up to 65% of bat species in the Neotropics. In 2003, 2004 and 2005 we quantified the activity of insectivorous bats and their insect prey at pastureland and forest sites with and without cenotes (water-filled sinkholes) in the Yucatan Peninsula, Mexico. We used a time-expansion bat detector to survey each habitat for 24 nights and analysed 2,880 one-minute recorded sequences to determine bat activity. We identified 14 species and five phonic types belonging to four families. Bat activity and the average number of bat species acoustically sampled each night were significantly greater in habitats with cenotes than in those without. Pteronotus personatus and an unidentified molossid were recorded exclusively at cenotes. Peropteryx macrotis showed the highest activity of all bat species. In all habitats insects were more abundant during the rainy season but only in pastureland was bat activity significantly greater during the rainy season. Insect abundance was correlated with bat activity only at cenotes in pastureland. Cenotes are important foraging habitats for insectivorous bats as 16 species, 84% of those revealed by this study, were recorded feeding in these habitats and the number of feeding buzzes was higher in comparison to habitats without cenotes. Protection of cenotes and their surrounding vegetation should be a management priority in order to conserve the high diversity of insectivorous bats associated with these distinctive habitats.

A taxonomic review of Rhinolophus stheno and R. malayanus (Chiroptera: Rhinolophidae) from continental Southeast Asia: an evaluation of echolocation call frequency in discriminating between cryptic species

The taxon Rhinolophus microglobosus is elevated to specific rank on the basis of clearly defined morphometric and acoustic characters which differentiate it from Rhinolophus stheno. It is recorded from Cambodia for the first time. Rhinolophus malayanus exhibits considerable geographical variation in echolocation calls, with apparently two phonic types: a northern population with lower frequency calls and a predominantly southern population with higher frequencies. However, this acoustic divergence is not reflected in any morphometric divergence, and the taxonomic status of the two phonic populations remains unclear. Discriminating characters of all three species are given, together with distribution data and short ecological summaries. The value of echolocation as an indicator of cryptic species and the zoogeographical implications of the study are briefly discussed.

What you see is not what you get: the role of ultrasonic detectors in increasing inventory completeness in Neotropical bat assemblages

Summary 1. Microchiropteran bats have the potential to be important biodiversity indicator species as they are distributed globally and are important in ecosystem functioning. Survey and monitoring protocols for bats are often ineffective as sampling techniques vary in their efficacy depending on the species involved and habitats surveyed. Acoustic sampling using bat detectors may prove an alternative or complementary technique to capture methods but is largely untested in the tropics. 2. To compare the efficacy of bat detectors and capture methods in surveys, we used ground mist nets, sub-canopy mist nets and harp traps to sample bats while simultaneously recording the echolocation calls of insectivorous bats in a diversity of habitats in the Yucatan, Mexico. We described echolocation calls, analysed call characteristics to identify species, and compared species inventories derived from traditional capture methods with those derived from acoustic sampling. 3. A total of 2819 bats representing 26 species and six families were captured; 83% were captured in ground nets, 13% in sub-canopy nets and 4% in harp traps. Fourteen species and five phonic types were identified based on five echolocation call characteristics. Discriminant function analysis showed a high level of correct classification of the calls (84·1%), indicating that identification of species by their echolocation calls is feasible. 4. In all habitats, acoustic sampling and capture methods sampled significantly more species each night than capture methods alone. Capture methods failed to sample 30% of the bat fauna, and aerial insectivores were sampled only by bat detectors. 5. Synthesis and applications . Given the importance of bats in ecosystem functioning, and their potential as indicator species, developing effective methodologies to survey and monitor bats is important for sustainable forest management and biodiversity conservation. Acoustic sampling should be used with capture methods to increase inventory completeness in bat assemblage studies, and could form part of a single standardized monitoring protocol that can be used globally in tropical forests, as this method detects aerial insectivores not sampled by capture methods.

Genetic divergence and echolocation call frequency in cryptic species of Hipposideros larvatus s.l. (Chiroptera: Hipposideridae) from the Indo-Malayan region

The intermediate leaf-nosed bat (Hipposideros larvatus) is a medium-sized bat distributed throughout the Indo-Malay region. In north-east India, bats identified as H. larvatus captured at a single cave emitted echolocation calls with a bimodal distribution of peak frequencies, around either 85 kHz or 98 kHz. Individuals echolocating at 85 kHz had larger ears and longer forearms than those echolocating at 98 kHz, although no differences were detected in either wing morphology or diet, suggesting limited resource partitioning. A comparison of mitochondrial control region haplotypes of the two phonic types with individuals sampled from across the Indo-Malay range supports the hypothesis that, in India, two cryptic species are present. The Indian 98-kHz phonic bats formed a monophyletic clade with bats from all other regional populations sampled, to the exclusion of the Indian 85-kHz bats. In India, the two forms showed 12–13% sequence divergence and we propose that the name Hipposideros khasiana for bats of the 85-kHz phonic type. Bats of the 98-kHz phonic type formed a monophyletic group with bats from Myanmar, and corresponded to Hipposideros grandis, which is suggested to be a species distinct from Hipposideros larvatus. Differences in echolocation call frequency among populations did not reflect phylogenetic relationships, indicating that call frequency is a poor indicator of evolutionary history. Instead, divergence in call frequency probably occurs in allopatry, possibly augmented by character displacement on secondary contact to facilitate intraspecific communication.

CRYPTIC SPECIES IN AN INSECTIVOROUS BAT, SCOTOPHILUS DINGANII

In recent years many cryptic bat species have been unmasked by differences in their echolocation calls. The yellow house bat (Scotophilus dinganii) is 1 of 3 species of Scotophilus currently described in southern Africa and is distinguished from the other 2 species by its size and yellow venter. Here we use genetic, morphological, and echolocation call data to show the existence of a cryptic species. We found that S. dinganii consists of 2 forms, one that uses a peak echolocation frequency of 44 kHz and the other a peak frequency of 33 kHz. Both forms have yellow venters. The 44-kHz phonic type is up to 15% smaller than the 33-kHz phonic type and differed genetically by an average cytochrome-b (Cytb) sequence divergence of 3.3%. Furthermore, combined phylogenetic analyses of Cytb and control region sequences indicate that the 2 phonic types are reciprocally monophyletic, suggesting that they are sibling species.

Molecular architecture of Pipistrellus pipistrellus/Pipistrellus pygmaeus complex (Chiroptera: Vespertilionidae): further cryptic species and Mediterranean origin of the divergence

Previous genetic analyses have demonstrated that two phonic types of one of the most common European bats, the Common pipistrelle, belong to distinct species, although they are almost identical morphologically (45kHz Pipistrellus pipistrellus and 55kHz Pipistrellus pygmaeus). To reconstruct the history of the species complex and explain the codistribution of both forms in Europe and the Mediterranean, we performed phylogenetic analysis based on a 402-bp portion of the cytochrome b gene. Particular attention was paid to the eastern and southern parts of the range where no data were available. We found further distinctive allopatric haplotypes from Libya and Morocco. The difference of about 6–7% described in the Libyan population suggests the occurrence of a new species in the southern Mediterranean. The species status of Moroccan population is also discussed. The phylogeographic patterns obtained and analysis of fossil records support the hypothesis of expansion of both species into Europe from the Mediterranean region during the Holocene. The allopatric speciation model fits our data best. The paleobiographic scenario envisaged is corroborated also by molecular clock estimations and correlations with Late Neogene environmental changes in the Mediterranean region which ended with the Messinian salinity crisis.

Acoustic divergence in two cryptic Hipposideros species: a role for social selection?

We present evidence that a relatively widespread and common bat from South East Asia comprises two morphologically cryptic but acoustically divergent species. A population of the bicoloured leaf-nosed bat (Hipposideros bicolor) from Peninsular Malaysia exhibits a bimodal distribution of echolocation call frequencies, with peaks in the frequency of maximum energy at ca. 131 and 142 kHz. The two phonic types are genetically distinct, with a cytochrome b sequence divergence of just under 7%. We consider the mechanisms by which acoustic divergence in these species might arise. Differences in call frequency are not likely to effect resource partitioning by detectable prey size or functional range. However, ecological segregation may be achieved by differences in microhabitat use; the 131kHz H. bicolor is characterized by significantly longer forearms, lower wing loading, a lower aspect ratio and a more rounded wingtip, features that are associated with greater manoeuvrability in flight that may enable it to forage in more cluttered environments relative to the 142 kHz phonic type. We suggest that acoustic divergence in these species is a consequence of social selection for a clear communication channel, which is mediated by the close link between the acoustic signal and receptor systems imposed by the highly specialized nature of the hipposiderid and rhinolophid echolocation system.

The social calls of Kuhl's pipistrelles Pipistrellus kuhlii (Kuhl, 1819): structure and variation (Chiroptera: Vespertilionidae)

AbstractThe aim of this study was to describe the structure of social calls produced by Kuhl's pipistrelles Pipistrellus kuhlii. Bats foraging around street lamps in the Campania region, Southern Italy, were recorded. Calls were produced by bats during chases and, similarly to those of Pipistrellus pipistrellus, were probably used to repel conspecifics from hunting sites. Calls often had three components, lasted on average 34 ms and contained most energy at about 17 kHz. A positive correlation was found between the frequencies of maximum amplitude of echolocation and social calls. Social calls from two adjacent populations differed in their peak frequencies, and possible hypotheses for this variation are given. The structure of P. kuhlii social calls was compared with those of the 45 and 55 kHz P. pipistrellus phonic types. Kuhl's pipistrelle calls lasted longer and showed lower values of minimum and peak frequencies. These differences can help to discriminate between field recordings of P. kuhlii and P. pipistrellus where the two species occur sympatrically.

Habitat around maternity roosts of the 55 kHz phonic type of pipistrelle bats (Pipistrellus pipistrellus)

AbstractWe quantified the percentage cover of habitats and the extent of linear features within 2 km of 11 maternity roosts of the 55 kHz phonic type of pipistelles Pipistrellus pipistrellus in south‐west England, and compared these with habitats around random points. The dominant habitats around both roosts and random points were improved grassland and built‐up areas. There was significantly more water (especially water edge habitat with woodland or hedgerow on the banks), and continuous hedgerow with emergent trees, around roosts. Preference for freshwater habitats around roosts was shown in comparisons of single habitats, and in compositional analyses with and without the inclusion of urbanized random points. These habitats may be preferred by 55 kHz pipistrelles: riparian habitats support large numbers of flying insects of the types eaten by 55 kHz pipistrelles, and hedgerows may be important linear features used by bats. The conservation of continuous hedgerows and watercourses close to maternity roosts would appear to be very important for 55 kHz pipistrelles.

The diets of two phonic types of the bat Pipistrellus pipistrellus in Britain

The pipistrelle (Pipistrellus pipistrellus) occurs as two phonic types in the British Isles, termed the 45 kHz phonic type and the 55 kHz phonic type. The two types are probably sibling species and therefore may have different diets. The aim of this study was to investigate differences in the diets of the two phonic types by using faecal analysis. Droppings were collected from three roosts of the 45 kHz phonic type and three roosts of the 55 kHz phonic type in three standardized time‐periods during June and July 1994. Prey remains were identified in each sample as far as possible to the class, order, or family level, and the Percentage Items of each prey group in the diet of each phonic type was calculated. Analyses of variance were carried out to investigate the effects of time‐period and roost on dietary composition, and to determine differences in the diets of the two phonic types for the main prey groups found. Both phonic types ate mostly the dipteran suborder Nematocera, and there was no difference between the phonic types in dietary breadth. The main prey groups in the diet of bats of the 45 kHz phonic type were the families Psychodidae, Anisopodidae and Muscidae, whereas the main prey groups of bats of the 55 kHz phonic type were the families Chironomidae and Ceratopogonidae. Differences in the diets of the two phonic types are discussed with respect to differences in habitat use by, and differences in echolocation call frequencies of, the two phonic types. The reported dietary differences support the hypothesis that the two phonic types are sibling species.

Habitat Use by Bats (Chiroptera) Assessed by Means of a Broad-Band Acoustic Method

1. Bat foraging activity was quantified by using a broad-band acoustic method on transects in 10 land use types in south-west England. From multivariate analysis of parameters of bat echolocation calls, 83% of bat passes could be identified to species level with quantified degrees of certainty. The remaining 17% could be identified to species group. 2. Total bat activity was positively correlated with air temperature, and once adjusted for temperature, was significantly higher over rivers and lakes than over other land use types. 3. Bats that use frequency-modulated echolocation calls (mainly Myotis spp., but some Plecotus auritus) were recorded in nine of 10 land use types, but never in villages. Rivers and lakes supported high levels of activity of these species. Bats classified as 45 kHz and 55 kHz phonic types of Pipistrellus pipistrellus had different habitat requirements; 45 kHz P. pipistrellus fed in many habitats, while 55 kHz P. pipistrellus fed mainly over rivers and lakes. Bats classified as Nyctalus noctula, Nyctalus leisleri and Eptesicus serotinus were most active in open habitats and over rivers and lakes. 4. Total bat activity was equally high in woodland interiors and along woodland edges, but bats were relatively more active in sheltered sections of transects than in exposed sections. 5. Plans for land management should take into account the habitat needs of bats. For most bat species in Britain, rivers and lakes are of primary importance. Management plans should aim to maintain physical diversity and features used by insects in freshwater habitats, woodlands and pasture.

Function of pipistrelle social calls: field data and a playback experiment

The study aimed to determine whether the so-called social calls that are produced by foraging bats of two phonic types ofPipistrellus pipistrellusserve a social function. First, the relationship between insect availability and the rate of production of social calls was measured at a foraging site of both phonic types. Second, playback experiments of social calls of the two phonic types were conducted in the field to determine the response of foraging bats to these calls, and to determine whether the calls are used in communication within or between phonic types. Two hypotheses are suggested for the function of social calls: that they may be used either to attract other bats to a food patch, or in agonistic interactions between bats in defence of a food patch. At relatively low insect densities, the rate of social call production of both phonic types increased significantly as insect density decreased. When social calls of each phonic type were broadcast, there was a significant reduction in bat activity of the same phonic type. In contrast, playbacks of social calls resulted in no change in activity of the other phonic type. The results supported the food patch defence hypothesis, that social calls are used to warn off other bats of the same phonic type when insects are scarce. The results also supported the hypothesis that the two phonic types are sibling species. Social calls were shown to serve a social function in intraspecific communication, but there was no communication between phonic types. 1997 The Association for the Study of Animal Behaviour

Differences in songflight calls and social calls between two phonic types of the vespertilionid bat Pipistrellus pipistrellus

The pipistrelle (Pipistrellus pipistrellus) occurs as two phonic types in Britain, its echolocation calls falling into two distinct frequency bands, with mean frequencies of maximum energy at 55 kHz and 46 kHz. These are termed the 55 kHz and 45 kHz phonic types here for simplicity. Songflight calls produced by males in the mating season, probably to attract females, differed between the two phonic types in the number of components in the calls and the call parameters measured. Songflight calls of the 55 kHz phonic type, which generally consisted of three components, were of higher frequencies than those of the 45 kHz phonic type, usually of four components. There were also significant differences in call parameters among individuals. A discriminant analysis of songflight calls classified 100% of individuals to the correct phonic type. The relationships between echolocation call frequency and songflight call frequency differed significantly between phonic types. Social calls produced during flight also differed between phonic types, in the number of components and call parameters measured. Social calls were compared to songflight calls of each phonic type. Social calls of the 55 kHz phonic type did not differ significantly from songflight calls; there were small but significant differences between the two types of calls of the 45 kHz phonic type. The study provides support for the hypothesis that the phonic types should be treated as sibling species. If songflight calls are used for mate choice, the differences may allow reproductive isolation between the two phonic types. The functions of songflight calls and social calls need to be investigated through experimental studies to explain the implications of the differences between phonic types.

Effects of sewage effluent on the activity of bats (Chiroptera: Vespertilionidae) foraging along rivers

In order to investigate how a decline in river water quality might affect the foraging behaviour of bats in riparian habitats, bat activity and feeding rates were measured at sites upstream and downstream from 19 sewage outputs. Paired sampling was used to control for variation in bat activity due to environmental parameters. Bat activity (bat passes) and attempted prey captures (terminal buzzes) recorded from broad band bat detectors were counted at each site, and bat species groups could be distinguished. Overall bat activity and foraging activity were reduced downstream from sewage outputs, by 11% (total reduction in passes) and 28% (total reduction in buzzes). Both phonic types of Pipistrellus pipistrellus were less active at downstream sites than at upstream sites (total reduction in activity was 55% for the 45 kHz phonic type and 51% for the 55 kHz phonic type). The 45 kHz phonic type of P. pipistrellus concentrated its foraging effort at upstream sites (total reduction in counts of buzzes was 87%), while Myotis spp. foraged at higher rates downstream from outputs than upstream (total increase in foraging rate was 112%). For the conservation of P. pipistrellus, the maintenance of high standards of water quality may be important. Myotis daubentonii may be able to benefit from eutrophication.

Assortative roosting in the two phonic types ofPipistrellus pipistrellusduring the mating season

The European pipistrelle, Pipistrellus pipistrellus, consists of two phonic types that echolocate with frequencies of maximum energy (FMAXE) averaging 46 kHz and 55 kHz (named the 45 kHz and 55 kHz phonic types for simplicity). These two phonic types occur in sympatry over much of Britain. Between 1993 and 1995 mating groups of P. pipistrellus were located in bat boxes between August and October, the main mating period for these bats. Mating groups comprised a single male and up to three females. Broadband, time-expanded recordings of search-phase echolocation calls were made from bats immediately after release. The average FMAXE of each bat was calculated: bats with an FMAXE less than 49 kHz were classed as 45 kHz phonic types and bats with an FMAXE greater than 52 kHz were classed as 55 kHz phonic types. A total of 16, 45 kHz groups and ten 55 kHz groups were located. No mating group ever contained more than one phonic type, although both types were known to be present at several of the study sites. Males emitted calls of higher frequency than females for both phonic types. The study suggests that the two phonic types are reproductively isolated and supports the hypothesis that P. pipistrellus should be considered as two cryptic sibling species.

Bimodal echolocation in pipistrelle bats: are cryptic species present?

The pipistrelle bat Pipistrellus pipistrellus is the most widespread in Europe, and is often the most abundant bat species in northern and central Europe. P. pipistrellus has traditionally been considered as one species throughout Europe. Here we show that: (i) the echolocation calls of pipistrelles fall into two distinct frequency bands in Britain, with frequencies containing most energy averaging 46 kHz and 55 kHz; (ii) roosts consist of bats which use only one form of echolocation; (iii) small but significant differences in average gross morphology exist between the phonic types; and (iv) the two phonic types occur in sympatry over much of Britain. Recordings made from European populations show that bimodal echolocation is also typical of continental pipistrelles, with only one phonic type found in some areas, two types in sympatry in others. The sympatric occurrence of two phonic types, the lack of mixing of types between colonies, and the morphological divergence between phonic types suggests that P. pipistrellus may actually consist of at least two cryptic sibling species. The evolution of bimodal echolocation in bats is discussed, and a model involving disruptive selection is presented to show how sympatric speciation may occur.