Foraging Ecology in the Mehely's Horseshoe Bat

Foraging Ecology in the Mehely’s Horseshoe Bat: from Resource Preferences to Competitive Interactions Egoitz Salsamendi Pagola PhD Thesis Leioa, Basque Country, 2010

 

DOKTORE GRADUKO AKTA DOGTORE TESIAREN DENFENTSAKO AKTA DOKTOREGAIA: Egoitz Salsamendi Pagola TESIAREN IZENA: Foraging Ecology in the Mehely’s Horseshoe Bat: from Resource Preferences to Competitive Interactions UPV/EHUko Doktorego Azpibatzordeak epaimahaia izendatu zuen goian adierazitako doktore tesia epaitzeko. Epaimahai hori behean aipatzen den egunean bildu da, eta doktoregaiak defentsa burututa, eta aurkeztu zaizkion eragozpen edota proposamenei erantzuna eman ondoren, epaimahaiak, _______________________, honako kalifikazio hau eman dio:

Leioan, 2010eko _____________aren ___a EPAIMAHAIKO BURUA,

IDAZKARIA,

Izpta.: _______________

Izpta.:________________

1. EPAIMAHAIKIDEA

2. EPAIMAHAIKIDEA

3. EPAIMAHAIKIDEA

Izpta.:_______________

Izpta.:______________

Izpta.: _______________

Doktoregaia, Egoitz Salsamendi Pagola

Izpta.:_________________

TESIAREN ZUZENDARIAREN BAIMENA TESIA AURKEZTEKO

Joxerra Aihartza Azurtza jaunak, 15958697-D I.F.Z. zenbakia duenak Foraging Ecology in the Mehely’s Horseshoe Bat: from Resource Preferences to Competitive Interactions izenburua duen doktorego-tesiaren zuzendari naizenak, tesia aurkezteko baimena ematen dut, defendatua izateko baldintzak betetzen dituelako. Egoitz Salsamendi Pagola doktoregai jaunak egin du aipaturiko tesia, Zoologia eta Animali Zelulen Biologia sailean.

Leioan, 2009ko Abenduaren 9a

TESIAREN ZUZENDARIA

Iz.: Joxerra Aihartza Azurtza

TESIAREN ZUZENDARIAREN BAIMENA TESIA AURKEZTEKO

Inazio Garin Atorrasagati jaunak, 15988367-D I.F.Z. zenbakia duenak Foraging Ecology in the Mehely’s Horseshoe Bat: from Resource Preferences to Competitive Interactions izenburua duen doktorego-tesiaren zuzendari naizenak, tesia aurkezteko baimena ematen dut, defendatua izateko baldintzak betetzen dituelako. Egoitz Salsamendi Pagola doktoregai jaunak egin du aipaturiko tesia, Zoologia eta Animalia Zelulen Biologia sailean.

Leioan, 2009ko Abenduaren 9a

TESIAREN ZUZENDARIA

Iz.: Inazio Garin Atorrasagati

SAILAREN ADOSTASUNA

Zoologia eta Animalia Zelulen Biologia Saileko Kontseiluak, 2009ko irailaren 25eko bileran, Foraging Ecology in the Mehely’s Horseshoe Bat: from Resource Requirements to Competitive Interactions izenburua duen doktorego-tesia aurkeztearen alde dagoela adierazi du. Joxerra Aihartza Azurtza eta Inazio Garin Atorrasagasti jaunen zuzendaritzapean egin den tesi hori Egoitz Salsamendi Pagola jaunak aurkeztu du sail honetan.

Leioan, 2009ko abenduaren 9a

O. E. SAILEKO ZUZENDARIA

Iz.: Juan Carlos Iturrondobeitia Bilbao

SAILEKO IDAZKARIA

Iz.: Miren P. Cajaraville Bereziartua

Foraging Ecology in the Mehely’s Horseshoe Bat: from Resource Preferences to Competitive Interactions

A thesis submitted by Egoitz Salsamendi Pagola to the University of the Basque Country for the degree of Doctor of Philosophy, under the supervision of Dr. Inazio Garin Atorrasagasti and Dr. Joxerra Aihartza Azurtza Leioa, Basque Country, 2010

Iñakiri, aurkitu duzu etxerako bidea

Contents

CONTENTS

ESKER ONAK – ACKNOWLEDGEMENTS SUMMARY GENERAL INTRODUCTION FORAGING ECOLOGY IN ANIMALS FORAGING ECOLOGY IN INSECTIVOROUS BATS HORSESHOE BATS AS MODEL-SPECIES THESIS BACKGROUND AND STRUCTURE MAIN OBJECTIVES References

v   vii  1 1 2 3 5 7 7

CHAPTER I: Echolocation and wing morphology in the Mehely’s (Rhinolophus mehelyi) and the Mediterranean (R. euryale) horseshoe bats: implications for resource partitioning Laburpena Introduction Methods STUDY COLONY DATA COLLECTION AND ANALYSIS Results Discussion RESOURCE PARTITIONING Reference

13 15 16 17 17 18 19 20 20 21

CHAPTER II: Diet and prey selection in Mehely’s horseshoe bat Rhinolophus mehelyi (Chiroptera, Rhinolophidae) in the south-western Iberian Peninsula

25

i

Egoitz Salsamendi Pagola

Laburpena Introduction Methods STUDY AREAS DATA COLLECTION SELECTION ANALYSES Results DIET PREY SELECTION Discussion References

27 28 29 29 30 31 32 32 33 33 36

CHAPTER III: Does wing morphology and echolocation signal structure constrain foraging decisions by bats? Laburpena Introduction Methods BAT TRAPPING AND TRACKING STATISTICAL AMALYSES Results CART MODELS Discussion VARIABLES INFLUENCING FORAGING DECISIONS PLASTICITY IN FORAGING DECISIONS ACCORDING TO AVAILABILITY IMPLICATIONS FOR CONSERVATION AND CONCLUSIONS References

39 41 42 44 44 46 49 49 51 51 53 54 54

CHAPTER IV: Fine-grained foraging habitat preferences mediate niche differentiation in sympatric sibling rhinolophids Laburpena Introduction Methods STUDY SITE AND BAT CAPTURE MORPHOLOGY AND ECHOLOCATION DIET AND PREY ABUNDANCE RADIO-TRACKING AND HABITAT USE NICHE BREADTH AND OVERLAP Results MORPHOLOGY AND ECHOLOCATION DIET AND PREY ABUNDANCE NICHE BREADTH AND OVERLAP HUNTING BEHAVIOUR SPACE AND HABITAT USE

59 61 62 64 64 65 65 66 68 69 69 69 70 71 71

ii

Contents

Discussion FORAGING HABITAT PREFERENCES FORAGING RANGE DIET AND PREY SIZE WHAT UNDERLIES NICHE SEGREGATION? CONCLUSIONS References

73 73 76 76 78 79 80

CONCLUDING REMARKS

85

APPENDIX

89

iii


iv

Esker onak – Acknowledgements

ESKER ONAK – ACKNOWLEDGEMENTS

P

ERTSONA askok modu askotara hartu du parte lan honen garapenean, zuei guztioi nere eskerrik beroenak – Many people have been involved in many ways in the development of this thesis, my warmest gratitude to all of you:

Joxerrari eta Inaziori, bion artean zuendari ezin hobea osatu baituzue, eta askoz gehiago! Segi horrela! Urtziri, Davidi eta Mariari, taldekide bikainak izateagatik, mendiko lanak merezi izan du zuekin. Zenbat gaupasa! Batzuk onak, besteak hobeak! Mendiko lanean lagundu duzuen gainerakoak ahaztu gabe: Domingo Trujillo, Manuel Mercadal, Aritz Aranzabal, Maider Guiu, Sergio Couto eta Toni Castelló. Many thanks to John O’Brien who kindly edited all the chapters and improved the English style. Go raibbh mile agat John! I would like to thank Elisabeth Kalko, Marco Tschapka and all the people in Ulm for taking so good care of me during my stay in there. A Bea por haber realizado un magnífico trabajo procurándome un poco de vida social y sobre todo con las ilustraciones (sin rencores, ein!). Borja Ruizek hainbat aldiz argitu ditu lan hau garatzen joan den heinean GIS analisiekin sortu diren hainbat zalantza. Mila esker txo! Inma Arostegik ere, hainbat eta hainbat aldiz argitu ditu lan hau garatzen joan den heinenan sortu diren hainbat eta hainbat zalantza estatistiko. Eskerrak eman edo barkamena eskatu? Mila esker eta barkatu eragozpenak! Eskerrik asko ere, nola ez, Aitor Larrañagari bere laguntza estatistikoagatik. Muchas gracias a Godfried Schreur y Ana Cordero por compartir su conocimiento sobre la fauna murcielaguera de Extremadura. Agradezco de verdad el enorme trabajo desarrollado y la ayuda ofrecida por Oscar de Paz durante la coordinación del proyecto LIFE de Extremadura. This thesis has been funded by the LIFE project LIFE00/NAT/E/7337 coordinated by Carlos Ibañez (EBD, CSIC) and co-funded by the Conselleria de Territori i Habitatge of the Regional Council of Valencia and the European Commission, and the LIFE project

v


LIFE04/NAT/E/000043 coordinated by Oscar de Paz (SECEM) and co-funded by the Consejería de Agricultura y Medio Ambiente of the Regional Council of Extremadura and the European Commission. It was also funded by the University of the Basque Country (Project GUI04/01) and the Basque Government (Project IT-385-07). Eskerrik asko etxekoei, Ixiarri eta Leireri animoengatik. Neskurri ere, iganderoko interrogatorioagatik eta animoengatik eta amonari bere kroketengatik!

vi

Summary

SUMMARY

T

HE Mehely’s (Rhinolophus mehelyi) and Mediterranean (R. euryale) horseshoe bats are two cave-dwelling, vulnerable species. Both are morphologically very similar, medium-sized sibling species whose distributions overlap extensively in the Mediterranean basin. These two rhinolophids often co-exist within the same areas and their maternity colonies often roost together, forming mixed clusters. In accordance with the ecomorphological paradigm, similarities in the characteristics of wing morphology and echolocation signal between bat species should be reflected in ecological similarities. However, according to the competitive exclusion principle the co-existence of these species should be associated with a mechanism of resource partitioning. Since basic knowledge on prey and habitat selection in allopatric R. mehelyi populations remained unknown, we carried out some basic behavioural studies of this species prior to focussing on examining what happens in sympatric rhinolophids,. We studied diet and prey selection in R. mehelyi during breeding season in four colonies. We collected faecal pellets from individuals and identified prey fragments to family or order level, where possible. We assessed prey abundance using Malaise traps. The bulk of the diet of R. mehelyi consisted of moths, representing more than the 80% of the average volume, and more than 90% of the average occurrence. Lacewings and crane flies were locally abundant. Males and females did not differ in consumed prey categories, whereas juveniles consumed fewer moths than adults. As expected, moths were the preferred prey category, followed by lacewings and crane flies. Therefore, R. mehelyi can be considered a moth specialist. Juveniles may acquire this strategy while gaining hunting experience. R. mehelyi is adapted to forage in structurally-complex and highly-cluttered environments due to its wing morphology and echolocation signal design. Therefore, to study foraging habitat preferences in R. mehelyi, we characterised the landscape according to variables related with these ecomorphological constraints, and investigated if those are the main factors determining foraging habitat selection in R. mehelyi. Foraging activity was analysed by means of radio-tracking in two contrasting landscapes with allopatric R. mehelyi

vii


populations. R. mehelyi mainly foraged in structurally-complex and highly-cluttered environments (riparian and broadleaved woodlands, including eucalyptus plantations), particularly when close to water sources. The species showed a high plasticity and also foraged in more open, savannah-like environments (the dehesa), but always close to water sources. No foraging activity was recorded in open environments (pastures). Structural complexity of foraging sites together with prey abundance seems to determine habitat selection in R. mehelyi. We modelled the foraging behaviour of R. mehelyi and R. euryale using echolocation signal and wing morphology parameters and, assuming that resource partitioning occurs between the two species, we explored how it is shaped by these factors. Resting frequency of echolocation signals was recorded and weight, forearm length, wing loading, aspect ratio and wing tip shape were measured in a colony where populations of the two species co-exist. R. mehelyi showed a higher resting frequency than R. euryale. Body mass, forearm length, aspect ratio, and wing loading were also higher in R. mehelyi. However, a high degree of overlap occurred between species in all these parameters. Differences in resting frequency are deemed insufficient for segregation of dietary features and they may compete for trophic resources in sympatry. Nevertheless, differences in wing morphology are probably large enough to permit spatial resource partitioning. The predictions of this model were then evaluated using empirical data. We simultaneously analysed wing morphology, echolocation, foraging habitat use and diet in a new study area with sympatric populations of R. mehelyi and R. euryale. Resting frequency in R. mehelyi was again higher than in R. euryale. Aspect ratio and wing loading were also higher in R. mehelyi. A high degree of overlap occurred between both species in all the parameters. Moths represented more than the 85% of the average volume for both species and moth body lengths did not differ between species (R. mehelyi = 14.1 ± 2.1 mm; R. euryale = 12.7 ± 2.1 mm). Foraging habitats were spatially segregated and also differed structurally. According to the model, R. mehelyi preferred structurally less-complex foraging sites than R. euryale. Finescale differences in foraging habitat preferences appeared to be the principal mechanism mediating resource partitioning between R. mehelyi and R. euryale. Therefore, we verified that even fine-scale resource partitioning mechanisms may be adequately predicted with refined ecomorphological and echolocation studies. Nevertheless, we stress the importance of behavioural processes minimising competition.

viii

General introduction

GENERAL INTRODUCTION

FORAGING ECOLOGY IN ANIMALS

F

Krebs 1986). Additionally, this objective has become particularly important in conservation ecology. Provided such studies relate to the auto-ecology of species, results may assist in identifying the key resource requirements of threatened species and, thus, conservationists may propose specific conservation strategies (Garshelis 2000).

Basic knowledge about the foraging ecology of a given species emerges from analyses of the resource types it consumes, and where those resources are consumed. Elucidating prey and habitat selection is, therefore, one of the main objectives in studies of foraging ecology (Stephens &

Resources may become even more crucial, particularly when consumption by one species affects what is available to other species. Inter-specific competition occurs when individuals of one species reduce the fecundity, survival or growth of individuals of another species, for example as a consequence of exploitation of shared resources. Thus, competition is most likely to arise when two (or more) species with very similar requirements obtain their resources from a limited supply (Leibold 1995). Even so, the stable coexistence of similar species may be facilitated if their respective niches differ sufficiently (Levine & HilleRisLambers 2009). Although the importance of niche differentiation is easy to conceptualise as a consequence of interspecific competition, it is difficult to prove, since the demonstration of niche differentiation per se does not necessarily

ORAGING ecology is central to animal ecology, since animals generally spend most of their time searching for and consuming food resources. Foraging ecology addresses fundamental aspects of the interactions between consumers and their resources (food and habitats), from predatorprey interactions to inter-specific competition (Begon, Harper & Townsend 1986). From the consumer’s perspective, food resources are important prerequisites that must be acquired. Therefore, animals live in a resource regime that constantly varies both spatially and temporally and thus, foraging individuals need to make decisions on where to position themselves in order to optimise food acquisition and ultimately maximise their fitness (Berstein, Kacelnik & Krebs 1988; Moody, Houston & McNamara 1996).

 

1


indicate anything about the role played by competition in contributing to it. Removal or demographic response experiments, if adequately designed, may demonstrate a cause-effect relationship between niche differentiation and interspecific competition (Suding 2001; Díaz et al. 2003). However, such experiments are inappropriate for rare, elusive, K-selected and/or endangered animals (e.g. bats) and thus, non-disruptive and more inductive approaches are currently the only practical alternatives. These approaches usually compare the morphology, physiology, behaviour and ecology of two (or more) species under sympatric and allopatric conditions, and assume that the observed niche shift (if any) is directly due to the presence/absence of the competitor species. The aim of such approaches is to investigate species’ realised and fundamental niches, the realised niche of one species being a constrained subset of its fundamental niche, truncated by interactions with a second (competitor) species (Hutchinson 1957). Pairs of similar, sympatric species offer opportunities to understand niche differentiation, and ultimately species coexistence. Among pairs of sympatric species, those that are sibling species not only provide opportunities for understanding niche differentiation, but also allow investigation of the evolutionary processes beyond niche differentiation (Mayr 1976). Additionally, understanding the resource preferences of these species offers valuable information on how to effectively manage habitats for their conservation (Sachot, Perrin & Neet 2003). Similarly, knowledge of the ecological processes ruling species coexistence may lead to greater understanding of the effect of human disturbances on biological diversity. FORAGING ECOLOGY IN INSECTIVOROUS BATS 2

 

Bats (order Chiroptera) are the only mammals capable of powered flight. This, together with the ability of some to orient with ultrasounds, opened up an entirely new and enigmatic niche to bats, i.e. the dark sky. Bats evolved rapidly through adaptive radiation to become today, the second most speciose (after rodents), and probably the most ecologically diverse, mammalian order, with more than 1100 species currently recognised (Wison & Reeder 2005). Their ability to fly and echolocate is certainly responsible for the global success, species richness and diverse ecology of bats (Jones & Teeling 2006). As flying mammals, bats depend entirely on flight as their principal means of locomotion and so their wing morphology greatly influences their foraging ecology (Swartz, Freemam & Stockwell 2003). Short and broad wings facilitate manoeuvrability in restricted environments and are typical of forest species. In contrast, bats with large and narrow wings typically forage in open environments (Norberg & Rayner 1987). Conventional aerodynamic theories provided a starting point from which to generate hypotheses about the functional significance of the diversity of bat wing morphologies; largely due to a lack of more appropriate approaches. However, bat wings are functionally more complex than those of conventional aircrafts (Swartz, Bishop & Aguirre 2006). Even so, characterisation of wing morphology using conventional measures, namely aspect ratio and wing loading, may facilitate inferences on the use of foraging habitats by bats (Aldridge & Rautenbach 1987). Bats use ultrasounds to orient in space and to get information about their prey. The accuracy of the information they receive largely depends on the design of the echolocation signal; such as its signal shape, frequency, intensity and duration (Schnitzler,


Moss & Denzinger 2003). Wing morphology and echolocation signal design are interrelated elements of the same adaptive complex and may severely constrain the foraging ecology of insectivorous bats (Aldridge & Rautenbach 1987; Norberg 1994; Kingston et al. 2000; Schnitzler et al. 2003). Bats foraging in different types of environments have to deal with environmentspecific constraints, ranging from open and uncluttered spaces to complex and semi- or highly-cluttered spaces near to vegetation (Schnitzler & Kalko 2001). Bats that forage in open space face the problem that prey are widely distributed and may, therefore, be difficult to detect. These bats emit narrow-band, frequency-modulated (FM) signals of long duration optimised to long-range detection, and tend to have narrow and pointed wings. Conversely, aerial/trawling foragers adapted to semicluttered habitats have to localize prey near echo-producing clutter backgrounds. These bats generally emit step FM signals of rather short duration optimised to determine prey position in relation to the background. They have broader and more rounded wings compared to open space foragers. Foragers in highly cluttered habitat capture prey from surfaces (gleaning) or very close to it. Gleaning foragers generally use preygenerated sounds to detect and localize prey and have wing morphologies adapted to hover around their prey. Narrow-space flutter-detecting foragers face the problem that prey position is masked by the clutterecho overlap zone and is, therefore, extremely difficult to detect. These bats emit constant frequency (CF) signals and have a specialised hearing system to recognise modulated echoes from fluttering prey among unmodulated background echoes. These bats have broad and rounded wings to manoeuvre very close to or within vegetation (Norberg & Rayner 1987; Schnitzler et al. 2003).

 

HORSESHOE BATS AS MODEL-SPECIES Horseshoe bats (Rhinolophidae Gray, 1825) are classified within the guild of narrow-space, flutter-detecting foragers based on their flight performance, wing morphology and echolocation signal structure. Rhinolophids consist of a single genus Rhinolophus with 77 recognised species worldwide (Simmons 2005). These bats have a single characteristic that distinguishes them from other bat families: they posses a synapomorphic solid thoracic ring formed by the fusion of the presternum, the first two ribs, and the last cervical and first two thoracic vertebrae (Csorba et al. 2003). This characteristic thoracic ring is associated with a capability to emit echolocation signals whilst stationary (i.e. perch hunting). These bats have the ability to emit ultrasound signals through the nostrils and thus, nose-leaves aid focussing of the emitted sounds (Pedersen 1993). Echolocation signals are characterised by a high and strong CF component, usually with brief initial and terminal FM components, with maximum energy concentrated in the second harmonic (Schnitzler & Kalko 2001). Rhinolophids have highly specialised auditory systems that can exploit Doppler-shift echoes and can emit and receive echolocation signals simultaneously. These bats recognise modulated echoes from the beating wings of fluttering insects among unmodulated background echoes. The flutter-modulated echoes provide information that facilitates categorisation and identification of prey according to their wing beat patterns (von der Emde & Schnitzler 1990). The wings of horseshoe bats are short and broad, with rounded ends, endowing butterfly-like fluttering or hovering flight. Rhinolophids have two main hunting strategies: 1) hunting for insects on the wing very close to or within vegetation, and 2) using feeding perches from which the bat ambushes prey, flying out to 3


capture prey as it flies past (i.e. perch hunting; Norberg & Rayner 1987). Rhinolophids have peculiar and complex expansions of the skin around the rhinarium, called ‘nose-leaves’, that are constituted of three main parts. The lower part, the ‘horseshoe’, partly or fully covers the upper lip and surrounds the nostrils. The upper part, the ‘lancet’, is a pointed, erect and anteroposteriorly flattened appendage attached at its base to the rhinarium. Located between the horseshoe and the lancet is a second perpendicular appendage, the ‘sella’, which is laterally flattened. The shape and arrangement of the nose-leaves varies from species to species and, thus, are useful characteristics for species identification. The ears are moderate to large and lack a tragus. The tail is well-developed and is completely enclosed in the tail membrane. Besides the two functional nipples on the chest and located slightly above and to the sides of the genital opening, there are two additional nonfunctional ‘false nipples’ that are not connected to mammary glands, which develop during the first pregnancy. Horseshoe bat pups grasp these false-nipples in the first days after parturition (Nowak 1994; Csorba et al. 2003). Rhinolophids are distributed exclusively in the Old World, occurring throughout the temperate and tropical areas of the African, Australian, Indomalayan, Oceanian and Paleartic bio-regions (Csorba, Ujhelyi & Thomas 2003). Recent molecular phylogenetic analyses suggest that the putative origin of rhinolophids was situated in the Asian tropical rainforest during the Eocene (Stoffberg et al. 2010). From this early origin many forms evolved in the context of climate change and tectonic events, into the second most speciose bat genus (Janis 1993; Guillen, Francis & Ricklefs 2003). Although species diverse, the morphological uniformity of the group when 4

 

compared to other bat families is quite striking (Bogdanowicz 1992; Bogdanowicz & Owen 1992). This uniformity is mirrored in the numerous morphologically-similar and frequently confused pairs of sympatric species (Csorba et al. 2003; Stoffberg et al. 2010). The Mehely’s (Rhinolophus mehelyi) and Mediterranean (R. euryale) horseshoe bats are two sibling circum-Mediterranean species that overlap over much of their distribution area and often co-roost in maternity colonies (Benzal & de Paz 1991; Benda et al. 2003). Both species are listed as Vulnerable in the IUCN Red List and they feature in the Second and Fourth Annexes of the European Directive (Council Directive 92/43/EEC on the conservation of natural habitats and of wild flora and fauna; Temple & Terry 2007). R. mehelyi is a thermophile, largely restricted to the Mediterranean climatic region. It has a discontinuous distribution in the north of Africa; from Morocco to Egypt and through Asia Minor to Iran. In Europe it occurs discontinuously; ranging from Portugal to Turkey, predominantly in the Mediterranean peninsulas. It also occurs on some of the biggest islands in the Mediterranean Sea (Rodrigues & Palmeirim 1999; Csorba et al. 2003). It is a mediumsized rhinolophid with a forearm length of 47-55 mm, a weight range of 10-18 g and emits echolocation signal frequencies around 107 kHz (Heller & von Helversen 1989: Russo et al. 2001, 2007; Salsamendi et al. 2005). Currently, populations of R. mehelyi show declining trends in all areas of its range where data are available, and it is though to be extinct or seriously threatened in some European countries (Rodrigues & Palmeirim 1999; Hutson, Mickleburgh & Racey 2001; Almenar, Alcocer & Monsalve 2007). Disturbance, loss of roosts and changes in foraging habitats have been proposed as the main causes of decline in this species,


although the causes are not fully understood since crucial information for effective conservation strategies, such as knowledge of spatial and trophic ecology, is scarce. R. euryale is also mainly distributed in the Mediterranean climatic region. In the North of Africa it occurs in Morocco, Algeria, Tunisia and possibly Egypt, and through the Middle East to Turkmenistan. In Europe, it ranges from Portugal to Turkey, but also ranges northwards into the Oceanic climatic region of central France and southern Slovakia. The species also occurs on some large Mediterranean islands (Ibañez 1999; Csorba et al. 2003). R. euryale is also a medium-sized rhinolophid with a forearm length of 44-51 mm, a weight range of 7-16 g and emits echolocation signal frequencies around 104 kHz (Schnitzler 1968; Heller & von Helversen 1989: Russo et al. 2001, 2007; Salsamendi et al. 2005). It has been in this Oceanic climatic region where the species has suffered the most dramatic declines (Brosset et al. 1988; Aihartza 2004); though local extinctions have also been reported from Mediterranean regions (Goiti & Aihartza 2007). Roost disturbances and losses, especially of maternity colonies, and degradation and loss of foraging habitats are the main causes of the declining trends in this species (Goiti & Aihartza 2007). The foraging behaviour of R. euryale is welldocumented. This species shows preference for semi- and highly-cluttered environments such as broadleaved woodlands in both the Mediterranean and Oceanic climatic regions and preys predominantly and selectively on moths although, seasonally, other prey may also play important roles (Russo et al. 2002, 2005; Aihartza et al. 2003; Goiti et al. 2004, 2006, 2008). This thesis has two main motivations. The first stems from the scarcity of basic knowledge on the foraging ecology of R. mehelyi. For the purpose of this work,

 

foraging refers to any process and behaviour related to the search, detection, selection and consumption of food resources, from analyses of echolocation signal structure to investigations of foraging habitat preferences. Therefore, the data obtained here will facilitate a better understanding of the resource requirements of R. mehelyi and, ultimately, aid the formulation of specific management and conservation strategies for the species. Moreover, competitive interactions with R. euryale have also been proposed as one of the factors causing the decline of R. mehelyi (Russo et al. 2005). Understanding the resource preferences of these species may, therefore, offer valuable information on how to manage areas effectively for the conservation of both species (Sachot, Perrin & Neet 2003). The second motivation stems from examining one of the main mechanisms that structures ecological communities, i.e. species competition and coexistence. R. mehelyi and R. euryale constitute particularly suitable model-species to investigate how environmental and ecomorphological variables determine foraging site selection in animals since, as insectivorous bats that rely on echolocation to detect, classify and localize prey, wing morphology, echolocation system and spatio-temporal variability in prey abundance may impose severe limitations on their foraging behaviour (Norberg 1994; Vaughan, Jones & Harris 1996). Segregation in space, habitat use, and diet have been proposed as the main mechanisms of coexistence among sympatric bat species (e.g. Saunders & Barclay 1992; Kalko 1995; Arlettaz 1999). However, no detailed ecological and behavioural studies have been published on resource partitioning mechanisms between sibling horseshoe bats. THESIS BACKGROUND AND STRUCTURE

5


The proposal for this thesis arose from preliminary research carried out in the Natural Park of Sierra Norte de Sevilla, in the south-western Iberian Peninsula as part of the LIFE project (LIFE00NAT/E/7337) coordinated by Carlos Ibañez (Estación Biológica de Doñana, CSIC) and co-funded by the Conseleria de Territori i Habitatge of the Generalitat Valenciana and the European Commission. The aims of our research were, 1) to generate, for the first time, data about the foraging habitat preferences of R. mehelyi, 2) to further our understanding about the foraging habitat preferences of R. euryale, and 3) to examine the likely competitive interactions between both species (Russo et al. 2005). This work presented the first information about foraging habitat preferences in R. mehelyi but, primarily, provided findings on niche segregation between R. mehelyi and R. euryale under sympatric conditions, indicating that both species have converging, although not identical, foraging habitat preferences. Nevertheless, the limited number of radiotracked individuals (only seven R. mehelyi and five R. euryale were successfully radiotracked), together with the limited time tracked per species (107.7 minutes for R. mehelyi and 162.8 for R. euryale) and the coarseness of location accuracy (fixes were obtained by triangulation), advise caution against generalising these preliminary results. In order to clarify the likely competition between both species, we arranged similar research to the above in a new area where both species coexist in abundance. This research was established as part of another LIFE project (LIFE04/NAT/E/000043) supervised by Oscar de Paz (Sociedad Española para la Conservación y Estudio de los Murciélagos) and co-funded by the Consejería de Agricultura y Medio Ambiente of the Council of Extremadura and the European Commission. However, prior to clarifying the ecological and behavioural 6

 

processes that might mediate niche segregation between R. mehelyi and R. euryale, we realised that basic knowledge on the ecology of R. mehelyi was lacking: questions like ‘what kind of prey or foraging habitat does R. mehelyi select?’ remained unsolved. Thus, we concluded that knowledge of the trophic and spatial ecology of R. mehelyi under allopatric conditions was a necessary prerequisite as a ‘control’ of an experimental design. This thesis is structured as a compendium of four main chapters, each one representing an autonomous work with complete introduction, methods, results, discussion and reference sections. Therefore, underlying background and theoretical concepts are incorporated into each chapter where necessary and, as a result, some sections of the chapter introductions and methods are repeated throughout the thesis. We have structured this thesis in accordance with the chronological order of the investigations as they were completed and the results published. The first chapter (echolocation and morphology in rhinolophids) derived from the investigations carried out within the first LIFE project. This chapter predicted a niche partitioning model under sympatric conditions based on the differences and similarities of wing morphology and echolocation signal design between R. mehelyi and R. euryale and aimed to contrast the model with species-specific foraging habitat preferences. Since the model could not be verified completely, it remained valuable for subsequent investigations. The second chapter (prey selection in R. mehelyi) presents the diet and prey selection data from four maternity colonies of R. mehelyi. The value of this chapters lies in that it is the first work that displays results on the diet and prey selection of R. mehelyi in Europe; prerequisites for adequate conservation policy formation and understanding the species


foraging behaviour. The third chapter (foraging decisions by bats) relates to habitat selection, another prerequisite for the formulation of conservation strategies. Although it is essentially devoted to elucidating foraging habitat selection in R. mehelyi, it also attempts to identify what are the variables determining the selection of foraging sites in bats in general, using R. mehelyi as a model-species. This chapter compares the relative importance of environmental and ecomorphological constraints on decisions regarding foraging site selection by bats, using an innovative multivariate method that hierarchically ranks variables according to their influence on site selection. The fourth chapter (niche differentiation in sibling rhinolophids) examines niche partitioning by contrasting the hypothesised scenario based on knowledge from the species in allopatry with empirical data on foraging habitat preferences for both species in sympatry. Again, wing morphology and echolocation signal frequencies are investigated in R. mehelyi and R. euryale, together with foraging habitat selection and diet to elucidate the degree, if any, of niche partitioning. Finally, the thesis concludes with some remarks that briefly encompass all the main conclusions of this work. The first and second chapters have already been published. The third chapter has recently been submitted and the fourth one is in preparation.

1) To provide a novel and complete data set on wing morphology and echolocation signal structure in R. mehelyi and R. euryale and to infer a niche partitioning scenario under sympatric conditions, based on the similarities and differences of these parameters. 2) To describe the diet of R. mehelyi and to determine whether the species forages selectively or randomly on different prey categories. 3) To compare diet composition among R. mehelyi individuals of different classes (based on sex and age) and among individuals of different localities. 4) To determine foraging habitat requirements in R. mehelyi from a multivariate perspective, characterising the landscape according to variables related with bat ecomorphology and prey abundance. 5) To ascertain how, and in which hierarchical order, ecomorphological and environmental variables constrain foraging behaviour in bats using R. mehelyi as a model-species. 6) To study the diet and foraging habitat preference in R. mehelyi and R. euryale in sympatry, and therefore, to verify or refute the results obtained from previous studies.

MAIN OBJECTIVES

References

Prior to this thesis, knowledge on the spatial and trophic ecology of R. mehelyi was limited. Results realised by Russo et al. (2005) precluded any firm conclusions on habitat preferences and available dietary analyses were merely descriptive (Sharifi & Hemmati 2001, 2004). Therefore, the main aims of this thesis were:

AIHARTZA, J.R. 2004. Quirópteros de Araba, Bizkaia y Gipuzkoa: distribución, ecología y conservación. Euskal Herriko Unibertsiateta, Bilbo. AIHARTZA, J.R., GARIN, I., GOITI, U., ZABALA, J. & ZUBEROGOITIA, I. 2003. Spring habitat selection by the Mediterranean horseshoe bat (Rhinolophus euryale) in the Urdaibai

 

7


Biosphere Reserve (Basque Country). Mammalia, 67: 25-32. ALDRIDGE, H.D.J.N. & RAUTENBACH, I.L 1987. Morphology, echolocation and resource partitioning in insectivorous bats. Journal of Animal Ecology, 56:763-778. ALMENAR, D., ALCOCER, A. & MONSALVE, Á. 2007. Rhinolophus mehelyi Matschie, 1901. In: Palomo, L.J., Gisbert, J. & Blanco, J.C. (eds). Atlas y Libro Rojo de los Mamíferos Terrestres de España. Dirección General para la BiodiversidadSECEM-SECEMU, Madrid, pp. 148-152. ALTRINGHAM, J.D. 1996. Bats. Biology and Behaviour. Oxford University Press, Oxford. ARLETTAZ, R. 1999. Habitat selection as a major resource partitioning mechanism between two sympatric sibling bat species Myotis myotis and Myotis blythii. Journal of Animal Ecology, 68: 460-471. BEGON, M., HARPER, J.L. & TOWNSEND, C.R. 1986. Ecology: individuals, populations and communities. Blackwell Scientific Publications, Oxford. BENDA, P., IVANOVA, T., HORÁČEK, I., HANÁK, V., ČERVENÝ, J., GAISLER, J., GUERGUIEVA, A., PETROV, B. & VOHRALÍK, V. 2003. Bats (Mammalia: Chiroptera) of the Eastern Mediterranean. Part 3. Review of bat distribution in Bulgaria. Acta Societatis Zoologica Bohemicae, 67: 245–357. BENZAL, J. & DE PAZ, O. 1991. Los Murciélagos de España y Portugal. Icona, Madrid. BERNSTEIN, C., KACELNIK, A. & KREBS, J.R. 1988. Individual decisions and the distribution of predators in a patchy environment. Journal of Animal Ecology, 57: 1007-1025. BOGDANOWICZ, W. 1992. Phenetic relationships among bats of the family Rhinolophidae. Acta Theriologica, 37: 213-240. BOGDANOWICZ, W. & OWEN, R.D. 1992. Phylogenetic analyses of the bat family 8

 

Rhinolophidae. Zeitschrift für Zoologische Systematik und Evolutionsforschung, 30: 142-160. BROSSET, A., BARBE, L., BEAUCOURNU, J.C., FAUGIER, C. SALVAYRE, H. & TUPINIER, Y. 1988. La raréfaction du rhinolophe euryale (Rhinolophus euryale Blasius) en France. Recherche d’une explication. Mammalia, 52: 101-122. CSORBA, G., UJHELYI, P. & THOMAS, N. 2003. Horseshoe Bats of the World. Alana Book, Shropshire. DÍAZ, S., SYMTAD, A.J., CHAPIN III, F.S., WARDLE, D.A. & HUENNEKE, L.F. 2003. Functional diversity revealed by removal experiments. Trends in Ecology and Evolution, 18: 140-146. GARSHELIS, D.L. 2000. Delusions in habitat evaluation: measuring use, selection, and importance. In: Boitani, L. & Fuller, T.K. (eds). Research Techniques in Animal Ecology: controversies and consequences. Columbia University Press, New York, pp. 111-164. GOITI, U. & AIHARTZA, J. 2007. Rhinolophus euryale Blasius, 1853. In: Palomo, L.J., Gisbert, J. & Blanco, J.C. (eds). Atlas y Libro Rojo de los Mamíferos Terrestres de España. Dirección General para la Biodiversidad-SECEM-SECEMU, Madrid, pp. 144-147. GOITI, U., AIHARTZA, J.R. & GARIN I. 2004. Diet and prey selection in the Mediterranean horseshoe bat Rhinolophus euryale (Chiroptera, Rhinolophidae) during the pre-breeding season. Mammalia, 68: 397-402. GOITI, U., AIHARTZA, J.R., ALMENAR, D., SALSAMENDI, E. & GARIN, I. 2006. Seasonal foraging by Rhinolophus euryale (Rhinolphidae) in an Atlantic rural landscape in northern Iberian Peninsula. Acta Chiropterologica, 8: 141-156. GOITI, U., GARIN, I., ALMENAR, D., SALSAMENDI, E. & AIHARTZA, J. 2008. Foraging by Mediterranean horseshoe bats (Rhinolophus euryale) in relation to prey


distribution and edge habitat. Journal of Mammalogy, 89: 493-502. GUILLÉN. A., FRANCIS, C.M. & RICKLEFS, R.E. 2003. Phylogeny and biogeography of the horseshoe bats. In: Csorba, G., Ujhelyi, P. & Thomas, N. (eds). Horseshoe Bats of the World. Alana Books, Shropshire, pp. xii-xxiv. HELLER, K.G. & VON HELVERSEN, O. 1989. Resource partitioning of sonar frequency bands in rhinolophid bats. Oecologia, 80: 178-186. HUTCHINSON, G.E. 1957. Concluding remarks. Cold Spring Harbour Symposium on Quantitative Biology, 22: 415-427. HUTSON, A.M., MICKLEBURGH, S.P. & RACEY, P.A. 2001. Microchiropteran bats: global status survey and conservation action plan. IUCN/SSC Chiroptera Specialist Group, IUCN, Gland. IBAÑEZ, C. 1999. Rhinolophus euryale Blasius, 1853. In: Mitchell-Jones, A.J., Amori, G., Bogdanowicz, W., Kryštufek, B., Reijnders, P.J.H., Spitzenberger, F., Stubbe, M., Thissen, J.B.M., Vohralík, V. & Zima, J. (eds). The Atlas of European mammals. T & AD Poyser, London, pp. 92–93. JANIS, C.M. 1993. Tertiary mammal evolution in the context of changing climates, vegetation, and tectonic events. Annual Review in Ecology and Systematics, 24: 467-500. JONES, G. & TEELING, E.C. 2006. The evolution of echolocation in bats. Trends in Ecology and Evolution, 21: 149-156. KALKO, E.K.V. 1995. Echolocation signal design, foraging habitats and guild structure in six Neotropical sheath-tailed bats (Emballonuridae). Symposium of the Zoological Society of London, 67: 259273. KINGSTON, T., JONES, G., ZUBAID, A. & KUNZ, T.H. 2000. Resource partitioning in rhinolophoid bats revisited. Oecologia, 124: 332-342.

 

LEIBOLD, M.A. 1995. The niche concept revisited: mechanistic models and community context. Ecology, 76: 13711382. LEVINE, J.M. & HILLERISLAMBERS, J. 2009. The importance of niches for the maintenance of species diversity. Nature, 461: 254-257. MAYR, E. 1976. Evolution and the Diversity of Life. Harvard University Press, Cambridge. MOODY, A.L., HOUSTON, A.I. & MCNAMARA J.M. 1996. Ideal free distribution under predation risk. Behavioural Ecology and Sociobiology, 38: 131-143. NORBERG, U.M. 1994. Wing design, flight performance, and habitat use in bats. In: Wainwriht, P.C. and Reilly, S.M. (eds). Ecological Morphology: integrative organismal biology. The University of Chicago Press, Chicago, pp. 205-239. NORBERG, U.M. & RAYNER, J.M.V. 1987. Ecological morphology and flight in bats (Mammalia; Chiroptera): wing adaptations, flight performance, foraging strategy and echolocation. Philosophical Transactions of the Royal Society of London, 316: 335-427. NOWAK, R.M. 1994. Walker’s Bats of the World. The Johns Hopkins University Press, Baltimore. PEDERSEN, S.C. 1993. Cephalomatic correlates of echolocation in the Chiroptera. Journal of Morphology, 218: 85-98. RUSSO, D., JONES, G. & MUCEDDA, M. 2001. Influence of age, sex and body size on echolocation calls of Mediterranean and Mehely’s horseshoe bats, Rhinolophus euryale and R. mehelyi (Chiroptera: Rhinolophidae). Mammalia, 65: 429-436. RUSSO, D., JONES, G. & MIGLIOZZI, A. 2002. Habitat selection by the Mediterranean horseshoe bat, Rhinolophus euryale (Chiroptera: Rhinolophidae) in a rural area of southern Italy and implications for conservation. Biological Conervation, 9


107: 71-81. RUSSO, D., ALMENAR, D., AIHARTZA, J., GOITI, U., SALSAMENDI, E. & GARIN, I. 2005. Habitat selection in sympatric Rhinolophus mehelyi and R. euryale. (Mammalia: Chiroptera). Journal of Zoology, London, 266: 327-332. RUSSO, D., MUCEDDA, M., BELLO, M., BISCARDI, S., PIDINCHELDA, E. & JONES, G. 2007. Divergent echolocation call frequencies in insular rhinolophids (Chiroptera): a case of character displacement? Journal of Biogeography, 34: 2129-2138. RODRIGUES, L. & J.M. PALMEIRIM. 1999. Rhinolophus mehelyi Matschie, 1901. In: Mitchell-Jones, A.J., Amori, G., Bogdanowicz, W., Kryštufek, B., Reijnders, P.J.H., Spitzenberger, F., Stubbe, M., Thissen, J.B.M., Vohralík, V. & Zima, J. (eds). The Atlas of European mammals. T & AD Poyser, London, pp. 98–99. SACHOT, S., PERRIN, N. & NEET, C. 2003. Winter habitat selection by two sympatric forest grouses in western Switzerland: implications for conservation. Biological Conservation, 112: 373–382. SALSAMENDI, E., AIHARTZA, J., GOITI, U., ALMENAR, D. & GARIN, I. 2005. Echolocation calls and morphology in the Mehelyi’s (Rhinolophus mehelyi) and Mediterranean (R. euryale) horseshoe bats: implications for resource partitioning. Hystrix, 16: 149-158. SAUNDERS, M.B. & BARCLAY, R.M.R. 1992. Ecomorphology of insectivorous bats: a test of predictions using two morphologically similar species. Ecology, 73: 1335-1345. SCHNITZLER, H.U. 1968. Die UltraschallOrtungslaute der Hufeisen-Fledermäuse (Chiroptera-Rhinolophidae) in Verschiedenen Orientierungssituationen. Zeitschrift für Vergleichende Physiologie, 57: 376-408. 10

 

SCHNITZLER, H.-U. & KALKO, E.K.V. 2001. Echolocation by insect eating bats. Bioscience, 51: 557-569. SCHNITZLER, H.-U., MOSS, C.F. & DENZINGER, A. 2003. From spatial orientation to food acquisition in echolocating bats. Trends in Ecology and Evolution, 18: 386-394. SHARIFI, M. & HEMMATI, Z. 2001. Food of Mehely’s horseshoe bat Rhinolophus mehelyi in a maternity colony in western Iran. Myotis, 39: 17–20. SHARIFI, M. & HEMMATI, Z. 2004. Variation in the diet of Mehely’s horseshoe bat, Rhinolophus mehelyi, in three contrasting environments in western Iran. Zoology in the Middle East, 33: 65–72. SIMMONS, N.B. 2005. Order Chiroptera. In: Wilson, D.E. & Reeder. D.M. (eds). Mammal Species of the World: A Taxonomic and Geographic Reference. Johns Hopkins University Press, Baltimore. STEPHENS, D.W. & KREBS, J.R. 1986. Foraging theory. Princeton University Press, New Jersey. STOFFBERG, S., JACOBS, D.S., MACKIE, I.J. & MATTHEE, C.A. 2010. Molecular phylogenetics and historical biogeography of Rhinolophus bats. Molecular Phylogenetics and Evolution, 54: 1-9. SUDING, K.N. 2001. The effects of gap creation on competitive interactions: separating changes in overall intensity from relative rankings. Oikos, 94: 219227. SWARTZ, S.M., FREEMAN, P.W. & STOCKWELL, E.F. 2003. Ecomorphology of bats: comparative and experimental approaches relating structural design to ecology. In: Kunz, T.H. & Fenton, M.B. (eds). Bat Ecology. The University of Chicago Press, Chicago, pp. 257-300. SWARTZ, S.M., BISHOP, K. & AGUIRRE, M.-F. I. 2006. Dynamic complexity of wing form in bats: implications for flight performance. In: Zubaid, A., McCracken


G.F. & Kunz, T.H. (eds). Functional and Evolutionary Ecology of Bats. Oxford University Press, Oxford, pp. 110-130. TEMPLE, H.J. & TERRY, A. 2007. The Status and Distribution of European Mammals. Office for Official Publications of the European Communities, Luxembourg. VON DER EMDE, G. & SCHNITZLER, H.-U. 1990. Classification of insects by echolocating greater horseshoe bats. Journal of Comparative Physisology A, 167: 423-430. VAUGHAN, N., JONES, G. & HARRIS, S. 1996. Effects of sewage effluent on the activity of bats (Chiroptera, Vespertilionidae) foraging along rivers. Biological Conservation, 78: 337-343. WILSON, D.E. & REEDER. D.M. 2005. Mammal Species of the World: A Taxonomic and Geographic Reference. Johns Hopkins University Press, Baltimore.

 

11


12

 

Chapter I: Echolocation and morphology in rhinolophids

CHAPTER I ECHOLOCATION AND WING MORPHOLOGY IN THE MEHELY’S (Rhinolophus mehelyi) AND MEDITERRANEAN (R. euryale) HORSESHOE BATS: IMPLICATIONS FOR RESOURCE PARTITIONING1

1

Salsamendi, E., Aihartza,, J., Goiti, U., Almenar, D. & Garin, I. 2005. Echolocation calls and morphology in the Mehelyi’s (Rhinolophus mehelyi) and Mediterranean (R. euryale) horseshoe bats: implications for resource partitioning. Hystrix, 16: 149-158.

13

Egoitz salsamendi Pagola

Previous page: horseshoe bats focus their echolocation signals toward the prey with the aid of nose-leaves.

14

Chapter I: Echolocation and morphology in rhinolophids

Ekokokapena eta hegal-morphologia Mehely ferra-saguzarrean (Rhinolophus mehelyi) eta ferra-saguzar Mediterranearrean (R. euryale): inplikazioak baliabideen banaketan Laburpena Rhinolophus euryale eta R. mehelyi espezieak oso antzekoak dira morfologikoki eta beraien banaketak gainezarri egiten dira Mediterranear itsasoaren bueltan. Bi espezieen bazka-portaera modelizatu genuen ekokokapen-hotsen eta hegomorfologiaren bitartez eta beraien artean nitxoen banaketa gertatzen dela ontzat hartuz, faktore hauek bazka-portaeran duten eragina aztertu genuen. Ekokokapenhotsen atseden-frekuentziak grabatu ziren eta pisua, besagainaren luzera, hegozama, itxura-ratioa eta hego-muturraren formaren indizea neurtu ziren. R. mehelyi espezieak R. euryale-k baino esangarriki atseden-frekuentzia garaiagoa erakutsi zuen, baina desberdintasunak ez ziruditen behar bezain handiak nitxo trofikoaren banaketa eragiteko. Pisua eta besagainaren luzera esangarriki handiagoak izan ziren R. mehelyi espeziean. Itxura-ratioan eta hego-zaman balio handiagoak izateak eta hego-muturraren formaren indizean balio baxuagoa izateak, hegakeran maniobrabilitatea eragozten diote R. mehelyi espezieari. Beraz, hegan egiteko gaitasuna murriztu egiten da R. mehelyi-n habitataren konplexutasuna areagotzen den bezala. Hau guztia kontutan hartuz, baliabideen banaketarako mekanismo nagusia habitat desberdinen erabilpenean dagoela dirudi, hegoen morfologia izanik banaketa honen giltzarri.

15

Egoitz salsamendi Pagola

I. ECHOLOCATION AND WING MORPHOLOGY IN THE MEHELY’S (Rhinolophus mehelyi) AND MEDITERRANEAN (R. euryale) HORSESHOE BATS: IMPLICATIONS FOR RESOURCE PARTITIONING

Introduction

G

IVEN the substantial energy demands of flight, bats must optimise energy-expenditure by adapting to ecological factors such as the habitat type or food resources that they exploit. This optimisation is reflected in different ecomorphological patterns that are based on body mass and wing morphology, which condition both flight speed and performance (e.g. Norberg and Rayner 1987). Short and broad wings facilitate manoeuvrability in restricted spaces and are typical of forest species. In contrast, animals with large and narrow wings typically fly in open areas or above the forest canopy. Large volant animals need comparatively more wing surface area than small ones since with increasing volume, body mass is cubed whereas the wing surface area that supports this mass is only squared. Additionally, assuming similar wing shapes, heavier animals need to fly faster in order to remain airborne (de Juana 1992). Since wing morphology in bats influences flight style and performance, its characterisation can facilitate inferences on habitat use. 16

Bats use echolocation to move in threedimensional space and to get information from their environment and hunting targets. The accuracy of the information they receive depends on the ultrasound system of each species. Higher frequency echolocation signals provide better resolution of target detail, so bats with higher frequency signals are better suited to the detection of smaller targets (Schnitzler 1968; Fenton 1999: Jones 1999). Additionally, higher frequency signals have higher echo attenuation due to atmospheric absorption and thus, they have a shorter range detection (Hartley 1989). Morphology and echolocation signals are inter-related elements of the adaptive complex that determines foraging strategies in bats (Aldridge & Rautenbach 1987; Kingston et al. 2000). For example, bats with narrow and pointed wings are fast and openair flyers and therefore, tend to have low frequency echolocation signals to discriminate prey-items from long distances. On the other hand, bats with broad and rounded wings exhibit slow and manoeuvrable flight, and tend to have high frequency echolocation signals to forage in

Chapter I: Echolocation and morphology in rhinolophids Table 1.1. Morphological measurements of R. euryale and R. mehelyi. Sample size in brackets and italics; standard deviation in parentheses. Mann-Whitney’s U test comparing morphological measurements and p values are shown for both species. Asterisks indicate significance (NS = not significant; ** = p Brachycera >>> other insects >>> Nematocera but Tipulidae (categories preceding ‘>’ are preferred to those following it; ‘>>>’ denotes a significant difference between categories). Results from the Chi-square test showed that moths, Myrmeleontidae, Chrysopidae, and Tipulidae were positively selected (i.e., they were consumed more than expected by chance; χ2=14.06, d.f.=7, p