Cognitie, Creier, Comportament / Cognition, Brain, Behavior Vol. IX(3), 479-496, 2005 ©Romanian Association of Cognitive Sciences

STUDYING COMMUNICATION IN BATS Dina K. N. DECHMANN*, Kamran SAFI Zoologisches Institut, Universität Zürich

ABSTRACT Only a handful of publications exist on social communication in bats, despite the high numbers of species and ecological diversity in this order. Historically methodological limitations for the study of these nocturnal and evasive animals were largely responsible for the lack of investigations of bat communication. However, nowadays, modern technologies and methods are being used on other groups of animals and would also be suitable for the study of bats. In this paper we review the literature on bat communication, mentioning work from other fields of research such as ecology, if the methods could potentially be used for the investigation of communication. We focus on olfactory communication because this is the field where most information is available beside acoustic communication. In addition there is great potential for the design of experiments here that would yield relevant results not only for the better understanding of bats, but of mammals or even sociality in general. KEY-WORDS: Chiroptera, olfaction, interspecific, intraspecific, echolocation, eavesdropping, social behaviour

INTRODUCTION The study of communication by animals with each other and their environment has received an increase in interest and effort over the recent years. Bats, although the second largest mammalian order, are strongly underrepresented in comparison. Only a small percentage of studies on bat behaviour deal with communication and most of them focus on the acoustic exchange of information. We conducted a quick literature search to illustrate this (ISI Web of Science searched on 26. Mai 2005): the keywords “bats” and “echolocation” yielded 572 results, the keywords “bats” and “communication” yielded only 54 papers, 47 of which deal with acoustic communication (see also Altringham & Fenton, 2003). Bats are a very large order and unusually diverse in terms of ecological *

Corresponding address: Dina K. N. Dechmann, Zoologisches Institut, Universität Zürich, Winterthurerstrasse 190, CH-8057 Zürich E-mail: [email protected]

Cognitie, Creier, Comportament / Cognition, Brain, Behavior Vol. IX(3), 497-510, 2005 ©Romanian Association of Cognitive Sciences

adaptations. This diversity is also reflected in the variety of their social systems, most species being social at least during part of the year (Bradbury, 1977b; McCracken & Wilkinson, 2000). Sociality requires a minimum degree of communication between group members; but how this is achieved in bats is largely unknown. In addition to the ecological and behavioural diversity, the combination of bats’ ability to fly and, in the large majority of species, to echolocate is unique among mammals. This allows researchers to address questions that cannot be studied in other taxa. Historically, the investigation of bats, which are crepuscular/nocturnal and often have a highly cryptic lifestyle, was limited by a lack of methods and numerous, especially experimental approaches remain difficult to date. Nonetheless, recent developments in equipment allow studying many unknown aspects of bat biology. Newly available technologies include recording and playback equipment, infrared videography, thermosensitive cameras as well as laboratory methods such as odour-, hormone-, or DNA-analysis. Bats use the same cues as humans and communicate by the same senses, mainly olfaction, hearing, vision, and touch all of which are important (Smith, 1977). For example, there is strong evidence that odours play a prominent role in the social lives of bats (Bloss, Acree, Bloss, Hood, & Kunz, 2002; Bouchard, 2001; Safi & Kerth, 2003; Voigt & von Helversen, 1999). It has also been shown that frugivorous bats use smell when foraging (Acharya, Roy, & Krishna, 1998; Kalko & Condon, 1998; Luft, Curio, & Tacud, 2003). Most studies on the acoustic behaviour of bats investigated the role of echolocation during foraging and orientation in space (Schnitzler & Kalko, 2001; Schnitzler, Moss, & Denzinger, 2003), while in other groups of mammals the majority of studies dealt with social communication by sound (see also chapter xx of this volume). The importance of bats’ social calls, which often are produced at relatively low frequencies, has been long known, although poorly investigated (e.g. Balcombe & McCracken, 1992; Barlow & Jones, 1997; Wilkinson & Boughman, 1998). However, a few recent publications have also emphasized the role of echolocation for passive communication, so-called “eavesdropping” (Balcombe & Fenton, 1988; Barclay, 1982; Fenton, 2003; Nieh, Barreto, Contrera, & Imperatriz-Fonseca, 2004). Striking is the almost complete lack of studies on other types of communication. For instance vision, although the eyes of bats are well developed and important for the animals in contrast to widespread belief. Olfaction and hearing are the senses that have been studied most intensively in bats. This is largely due to the fact that they are the most reliable senses in the absence of light, sound providing short-term and smell providing long-term cues. This is well known for mammals in general (Brown & Macdonald, 1985). A large number of publications deal with the use of echolocation for orientation and foraging and many of them describe the methods in detail. The methods for studying acoustic communication in bats would largely be the same. Consequently, we outline some major methods used in studies of olfactory communication in bats instead, using the most important publications as examples. Finally, we also speculate a bit about possibilities that remain unexploited in spite 480 Septembrie 2005 • Cogniţie, Creier, Comportament

Cognitie, Creier, Comportament / Cognition, Brain, Behavior Vol. IX(3), 497-510, 2005 ©Romanian Association of Cognitive Sciences

of today’s technologies and knowledge.

OLFACTORY COMMUNICATION As mentioned above, nocturnal lifestyle and olfaction are closely connected and thus probably play a major role in the social communication of bats, especially among colony members (Brown & Macdonald, 1985). Bats possess a large and diverse number of physiological structures connected to the production and perception of smell. For example, the cranial integument of European vespertilionid bats contains large glandular complexes with storage chambers as well as structures for storage and application of sebum (Haffner, 1989, 1998, 2000). The size and position of these glands, which are located in a highly sensitive zone between the eye and the nose, suggest that they may be used for communication (Figure 1). But glands are also very common everywhere else on the body of most bat species (Scully, Fenton, & Saleuddin, 2000). Several other morphological adaptations (Figure 1) of bats are closely linked to olfactory communication, e.g. the wing sacs in the genus Saccopteryx (e.g. Voigt, 2002; Voigt & von Helversen, 1999), the subaxillary region and inguinal pockets of Noctilio leporinus (Brooke & Decker, 1996; Studier & Lavoie, 1984), or the buccal glands in Nyctalus noctula (Seine, 1988). The importance of olfaction is also reflected by the relative size of the main olfactory bulb, a brain region processing most information related to smell (Barton, Purvis, & Harvey, 1995; Hutcheon, Kirsch, & Garland, 2002; Safi & Dechmann, 2005).

Figure 1. Morphological features in bats are closely linked with scent production and application. a) The osmeotrichia on the head of male Chaerophon pumilus are normally folded back and invisible (below), but are erectable (above). They are only present in the male, b) facial glands of Myotis myotis between eye and nose are present in both sexes, secretion is released with the help of special muscles, c) the wing sac of male Saccopteryx bilineata (above), can be opened with the help of muscles to release odour during mating Septembrie 2005 • Cogniţie, Creier, Comportament

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displays in front of the females (below).

Olfaction is also a very important interspecific (e.g. bat-plant) communication channel. This has been shown for bats from both frugivorous families the Phyllostomidae (Kalko & Condon, 1998; Thies, E.K.V., & Schnitzler, 1998; von Helversen, Winkler, & Bestmann, 2000) and the Pteropodidae (Luft et al., 2003). Phytophagous species use olfactory cues for detecting the ripeness and location of fruits and flowers and their main olfactory bulb is larger than in animal eating species (Hutcheon et al., 2002; Safi & Dechmann, 2005). Chemical analyses suggest that olfactory cues co-evolved with the preferences of their mammalian pollinators (Korine, Kalko, & Herre, 2000; von Helversen et al., 2000; Winkler, 1998). Finally, the Pteropodidae seem to use their sense of smell not only for the detection of food but also for orientation in increasingly complex habitats (Safi & Dechmann, 2005). The few field studies dealing with olfactory communication in bats, revealed the use of odour for social interactions emphasizing the general importance of this communication channel (Bouchard, 2001; Brooke & Decker, 1996; De Fanis & Jones, 1995; Safi & Kerth, 2003; Voigt, 2002; Voigt & von Helversen, 1999). Choice experiments in the laboratory have demonstrated that adult females can distinguish roost mates by scent (Pipistrellus pipistrellus; De Fanis & Jones, 1995; Mops condylurus; Bouchard, 2001; Eptesicus fuscus, Bloss et al., 2002). Olfactory cues are also used for individual recognition, e.g. between mothers and their offspring (De Fanis & Jones, 1996; Gustin & McCracken, 1987; McCracken & Gustin, 1991). Finally, olfaction can play an important role in sexual selection, i.e. mate choice and mate attraction (Voigt & von Helversen, 1999; Voigt, von Helversen, Michener, & Kunz, 2001). Methods applied in the study of olfactory communication Approaches and methods of analysis used in biochemistry and organic chemistry are often applied to the study of olfactory communication. These approaches require a well-equipped chemistry laboratory. Substantial experience with the methods and an adaptation to the specific aim and question are necessary. We point out some aspects, which should be considered during each step of only the most common experimental and analytical procedures as providing details on all them would suffice to fill an entire volume. Bioassays: The biological use and behavioural context of an odour must be verified before collecting samples and determining their chemical compounds (Figure 2). This is especially important, considering the amount of technical and financial effort involved in odour analysis and the great potential for failure. Choice experiments are a useful tool for testing the ability of animals to distinguish between olfactory cues and for the determination of scent detection threshold levels. They were developed for rodents and insects but can be applied to a range of animals. These experiments can either be conducted in Y-mazes where individuals have to decide between two cues or in choice arenas where individuals choose between several cues (Bloss et al., 2002; Cloe, Woodley, Waters, Zhou, & 482 Septembrie 2005 • Cogniţie, Creier, Comportament

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Baum, 2004; Lester, 1968; Stolberg & Grigoryan, 1992). Also important are habituation/ dishabituation experiments where behavioural changes according to presented stimuli are observed (Baum & Keverne, 2002; Deiss, Feron, & Baudoin, 1999; Mayeaux & Johnston, 2002; Schellinck, West, & Brown, 1992; Todrank, Heth, & Johnston, 1998, 1999). In all of these approaches, the number of animals choosing a cue, as well as the number of animals whose cues are presented should be large enough to avoid pseudoreplication (i.e. for statistical reasons >5). In addition, the standardized sampling and presentation of olfactory cues has to be planned and carried out carefully. Differences in the presented amount of secretion may lead to biologically irrelevant choices. This problem can be partially avoided through the constant airflow created by an olfactometer (Bodyak & Slotnick, 1999; Clanton, Nicolai, & Larson, 1999; Cortada, Valor, & Uribarri, 1997; Fox & Thiessen, 1984; Gralapp, Powers, & Bundy, 2001; Joly, Michel, Figure 2. Steps in the study of olfactory communication. Deputte, & Verdier, 2004; Kraemer & Apfelbach, 2004; Pfaffmann, Goff, & Bare, 1958; Turlings, Davison, & Tamo, 2004). But the environments and samples must be standardized even when olfactometers are being used. Thus many experiments can only be conducted under semi-natural or artificial conditions, and are not possible with free-ranging bats. Experimental setup: After determining the biological relevance of an olfactory cue with the help of bioassays, the procedure is usually the following a) analysis of samples, b) identification of potentially informative compounds, c) synthesis of compounds and finally d) experimental proof of the role of these compounds in communication (=second bioassay, Figure 2). No single study on bats contains data that was obtained by applying all of these steps. Instead, odour differences at individual, family-, hierarchical and/or other levels are usually determined in the laboratory without further identification of the specific molecules (Safi & Kerth, 2003). The weakness of such an approach is that differences at a statistical level do not prove that animals perceive and use these differences (Gralapp et al., 2001). Similarly, the inability to detect differences by chemical analysis does not imply the inability of the animal to distinguish between scents in natural circumstances (Kazial, Burnett, & Masters, 2001; Kazial & Masters, 2004). Both scenarios again emphasize the importance of bioassays. Collection, storage and preparation of secretions: Whenever possible several samples from the same individual should be obtained. For example, 53 Septembrie 2005 • Cogniţie, Creier, Comportament

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females from four different colonies were sampled two to four times each in a study of colony member recognition in Myotis bechsteinii (Safi & Kerth, 2003). While a lower total number of animals may theoretically suffice, more samples per individual would strengthen statistical estimates of individual variation. Changes in the composition of secretions of individuals or groups of individuals due to internal (e.g. physiology, diet, condition) and external conditions can be considerable (Brown, Schellinck, & West, 1996; Buesching, Waterhouse, & Macdonald, 2002; Schellinck et al., 1992) but can be accounted for by statistical procedures. However, depending on the aim of the study it may be interesting to consider how components covary with behavioural and/or physiological attributes (Heth, Nevo, & Todrank, 1996; Heth, Todrank, Busquet, & Baudoin, 2001; Mayeaux & Johnston, 2002; Osada et al., 2003; Schellinck et al., 1992; Todrank et al., 1998, 1999; Willis & Poulin, 2000; Woodley & Baum, 2003). It is also important to know the nature and origin of a smell to plan collecting and analysing it. For example, recent evidence confirms that the bacterial fauna on the skin of bats affects scent production. In addition, the smell of each bat can be influenced by physical contact and exchange of bacteria with conspecifics (Studier & Lavoie, 1984). Carefully standardized collection and storage procedures are essential. Due to the high sensitivity of some analytical methods, even small differences caused by collection and storage may change the composition of the collected samples. Depending on their chemical nature, time and temperature during storage may also change the composition of samples. Many substrates used for collecting scent samples (i.e. medicinal cotton) must be washed before use, because they contain chemicals that may differ between packages or brands. Similarly, vials and tubes used for storing samples can contain chemicals (usually polymer plasticizer) that will appear in the analysis and may mask biologically relevant information. Consequently, it is best to use glass vials. Sterile equipment including fresh powder-free gloves for every sampled individual must be used to avoid cross contamination. Control samples can be generated by going through the motions but not actually collecting the sample and putting the empty collecting substrate (e. g. cotton swabs) into a blank storage container. This should be done at least once at the beginning and once at the end of the collection of a series of samples. Blanks should also be inserted at regular intervals when collecting large series of samples. For the sample collection itself various methods can be used. Secretions can rarely be collected from bats directly with a pipette or syringe as it is normally done in larger mammals. Instead, cotton swabs or microscopic slides are commonly used (Bouchard, 2001; Safi & Kerth, 2003). Sometimes secretion needs to be squeezed out carefully before it can be accessed. If odours other than secretions from glands such as the content of wing pouches (Voigt & von Helversen, 1999) are being investigated more specific collecting methods may be necessary. In cases where small quantities of secretion are produced or the odour source is not clearly defined, direct collection from the animal with headspace analysis (see box) may be advisable. When planning sampling regimes it is important to consider the fact 484 Septembrie 2005 • Cogniţie, Creier, Comportament

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that scents may only occur seasonally or may be affected by the emotional state of animals including stress caused by handling. For the latter reason, animals should be processed quickly and odour collection should be carried out before obtaining other data such as weight or morphological measurements. Samples should be analyzed as soon as possible after collection, but all samples should be stored for similar amounts of time. To slow down degradation samples should be stored on ice immediately after collection and transferred to storage at–20°C as soon as possible. GC/MS: Gaschromatography/Masspectrometry allows separating chemical compounds of secretions according to their specific retention time in the gaschromatography column. Later the molecular mass of these separated chemical compounds can be determined with masspectrometry. This method allows the detection of very small amounts of chemical components. Headspace GC/MS: The physical removal of secretions and transferring them into a solvent may change the nature of the sample. In order to avoid an influence of the sampling, technique headspace analysis is often used in studies of olfactory communication. The volatile compounds are collected by air suction either directly from the animal or from the collecting device such as a cotton swab. They can then be analysed with GC or GC/MS. This method is very sensitive to contamination and careful experimental controls are required to obtain interpretable results. The advantage of this method is that the number of chemicals is usually lower than in the analysis of entire secretions. In addition, superposition of different chemicals is less likely. As the volatile compounds are also the ones that play a role in olfactory communication, this method is most likely to yield data on biologically relevant information conveyed by the odour .

The preparation of samples for analysis depends on the method, but some rules generally apply. Every sample must be prepared for analysis in the same way. The samples should be prepared immediately before analysis. If it is necessary to transfer the sample into a solvent (see also box) this should be done on ice or even at lower temperatures and the same temperature must be used for all samples. As during sample collection, avoid the use of vials and other containers that may contaminate the samples in the laboratory (see above). The substrate used for collecting samples should also be analyzed “empty” as a control. Ensure regularly that the equipment used for chemical analysis produces clean and repeatable results, especially when the same instruments are used simultaneously for different studies. When choosing the appropriate method various factors ranging from financial costs, or amount of secretion available per animal, to the selection of the appropriate solvents must be taken into account. With most classic methods in chemical analysis components are separated by using different retention times e.g. in a column with a specific matrix. Chemical compounds are thus sorted according to size, hydrophily, electron load etc. See the box for a short description of the most common methods. Very difficult to measure non-invasively is the amount of secretion produced by an animal at a given time. The onset and offset of secretion production as well as the amount of secretion are often tightly linked to the natural history of animals and thus biologically relevant. Male Nyctalus noctula, for example, Septembrie 2005 • Cogniţie, Creier, Comportament

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produce the largest amounts of secretion during the mating season when they are establishing and defending mating roosts (Seine, 1988). It is assumed that the scents play an important role in the mating system of this species. Assessing the absolute amount of secretions or compounds is often not feasible due to variation caused by the sampling procedure. As a result, amounts of single compounds are commonly given in proportion to the total amount of eluted secretion (= sum of all compounds). This allows inferring changes in relative amount of each compound. While this procedure corrects for sampling and analysis biases, it generates interdependent compositional data that needs specific statistical analysis (Aitchinson, 1982). Here, compositional data analysis, multivariate approaches such as principal component analysis or, pattern recognition approaches are most useful (Aebischer, Robertson, & Kenward, 1993; Aitchinson, 1982; Service, Brereton, & Harris, 2001). Conclusion and outlook on olfactory communication The study of chemical communication, if carried out thoroughly, can help to provide a basis for the study of the costs of signalling (Gosling, Roberts, Thornton, & Andrew, 2000), the evolution of communication (Bininda-Emonds, Decker-Flum, & Gittleman, 2001) and other interesting aspects of chemical communication and sexual selection that are poorly investigated in bats (Brown & Macdonald, 1985; Burger, 2005; Emes, Beatson, Ponting, & Goodstadt, 2004; Fisher, Swaisgood, & Fitch-Snyder, 2003a, 2003b; Humphries, Robertson, Beynon, & Hurst, 1999; Hurst & Beynon, 2004; Milinski & Wedekind, 2001; Nieh et al., 2004; Platek, Burch, & Gallup, 2001; Singh & Bronstad, 2001; Voigt & von Helversen, 1999; von Helversen et al., 2000; Wedekind & Furi, 1997; Willis & Poulin, 2000). Odours play an important role for individual recognition or colony mate recognition. Such intraspecific signals are thought to be prerequisites for sociality and cooperation in animals (Crowley et al., 1996). The investigation of the role and nature of such signals is crucial for the understanding of sociality in bats. But olfactory communication is also commonly involved in mate choice and species recognition (Bininda-Emonds et al., 2001; Heth et al., 2001; Munclinger & Frynta, 1997). In bats the use of olfactory cues for mate choice and sexual selection has only been studied thoroughly in one species though commonly presumed important (Voigt, 2002; Voigt & von Helversen, 1999; Voigt et al., 2001). But, as studies such as those on the scent production of bat-pollinated plants have shown, odours can play an important role even beyond signalling within and between bat species (von Helversen et al., 2000). The role of olfactory communication for the co-evolution of plant-pollinator signal systems provides large opportunity for future projects. Many methods are available today, which have not yet been applied to bats. Such methods include modern approaches such as the study of MHC that are known to be important in kin and mate recognition processes (Beauchamp, Curran, & Yamazaki, 2000; Eggert, Muller-Ruchholtz, & Ferstl, 1998; Ehman & Scott, 486 Septembrie 2005 • Cogniţie, Creier, Comportament

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2001; Singer, Beauchamp, & Yamazaki, 1997; Wedekind, Seebeck, Bettens, & Paepke, 1995; Yamazaki, Singer, & Beauchamp, 1998). Also the new and promising field of the study of the role of major urinary proteins (MUPs) as carriers of olfactory signals that were detected and are being studied intensely in rodents and which, once investigated, may contribute to the understanding of bat communication (Cavaggioni & Mucignat-Caretta, 2000; Humphries et al., 1999; Hurst & Beynon, 2004; Hurst, Thom, Nevison, Humphries, & Beynon, 2005; Mucignat-Caretta & Caretta, 1999; Mucignat-Caretta, Cavaggioni, & Caretta, 2004). The study of olfactory communication in bats is only in its beginnings and it should be rewarding to relate new knowledge to the large and diverse amount of knowledge on the neurobiology and ecology of this order (Bloss, 1999).

OTHER SENSES OF BATS Acoustic communication Bats produce two main types of vocalizations or calls. One type, echolocation calls, is mainly used for orientation and foraging (Schnitzler & Kalko, 2001). This is the context in which these calls have been investigated most thoroughly. Only recently, researchers have developed an interest in the use of echolocation calls for active and passive communication in bats (Balcombe & Fenton, 1988; Barclay, 1982; Fenton, 2003). The other type of call is social calls, which often but not always are produced at lower frequencies and within the hearing range of humans (Andrews & Andrews, 2003; Barlow & Jones, 1997; Fenton, 1977, 2003; Pfalzer & Kusch, 2003; Russo & Jones, 1999; Wilkinson & Boughman, 1998). Their phonic structure is entirely different from that of foraging or orientation calls produced at ultrasound frequencies. Social calls are used for recognition of conspecifics, group members, the coordination of foraging, motheroffspring communication and probably in many other currently unknown social contexts (Pfalzer & Kusch, 2003). For example, on a species level, playback of conspecific calls caused Pipistrellus sp. to avoid an area. In this case social calls probably help to avoid competition when the insects these bats feed on are scarce (Barlow & Jones, 1997). The role of social calls for the recognition of group members is illustrated by the studies of Wilkinson and Boughman (J. W. Boughman, 1997; J. W. Boughman & Wilkinson, 1998; Wilkinson & Boughman, 1998), who showed that screech calls allow female Phyllostomus hastatus to fly in groups during the season when food e.g. fruit occurs in clumps. Screech calls were also emitted more often during the fruiting season. Playback experiments with captive Tadarida brasiliensis showed that mothers in this species recognize their pups, but pups do not recognize mothers (Balcombe, 1990; Balcombe & McCracken, 1992). The range of echolocation calls and some social calls lies above the hearing range of most humans, i.e. above 20 kHz, and researchers studying acoustic behaviour of bats face two challenges: a) to record, analyze and Septembrie 2005 • Cogniţie, Creier, Comportament

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(if required) play back the calls and b) to design experiments or observation schemes for the study of communication. Technical limitations in conjunction with expensive devices limited the study of acoustic communication for a long time. However, data acquisition boards that can be attached directly to a computer now allow recording and playback of sound up at to several hundred kilohertz. In combination with tools such as infrared videography and thermosensitive cameras it is now possible to observe behaviour while recording and playing back calls with a reasonable financial effort. The knowledge about echolocation calls from other contexts provides a solid theoretical and methodological background. Almost all aspects of social communication in bats remain largely uninvestigated. Another example is the use of echolocation for communication. The echolocation calls of foraging bats seem to be used as acoustic cues by conspecific as well as heterospecific bats (Balcombe & Fenton, 1988; Barclay, 1982; Fenton, 2003). Acoustic information probably also plays an important role in mate choice and sexual selection as is known from many other groups of animals such as insects (Klappert & Reinhold, 2003), amphibians (Ryan, 1991), birds (Gentner & Hulse, 2000), or other mammals (McElligott & Hayden, 2000). Serenading behaviour has been described in male Saccopteryx bilineata (Behr & von Helversen, 2004) and is also known from other species such as European pipistrelle bats, even if the structure and exact role of the calls remain unclear (e.g. Gerelllundberg & Gerell, 1994). Finally, even the areas where a few studies exist, namely those investigating acoustic recognition of species, individuals, group members, and relatives (J. W. Boughman, 1997; Kazial & Masters, 2004; McCracken & Gustin, 1991; Obrist, 1995; Pfalzer & Kusch, 2003) require more indepth study of a larger number of species in order to unravel the many uses of acoustic information in the social lives of bats. For example, vigilance and warning behaviour in bats has not been assessed, although bats caught in nets emit distress calls that attract conspecific and heterospecific individuals (personal observations), a phenomenon that is reminiscent of mobbing behaviour in other taxa (Hass & Valenzuela, 2002). Vision Only a handful of studies investigated the role of vision in bats for orientation (Davis & Barbour, 1965), navigation (Serra-Cobo, Lopez-Roig, Marques-Bonet, & Lahuerta, 2000; Williams, Williams, & Griffin, 1966), and finding prey (Eklöf & Jones, 2003; Eklöf, Svensson, & Rydell, 2002; Rydell & Eklöf, 2003; Winter, Lopez, & von Helversen, 2003); reviewed in (Mueller, 1968). None of them investigated the subject of visual communication. Generally, because bats are nocturnal and many of them are capable of echolocation, vision is assumed to be of lesser importance. However, bats, as flying animals with an energetically costly surface to volume ratio are under high-pressure to minimize weight and energy expenditure (Berger & Hart, 1974; McNab, 1983; Winter & von Helversen, 1998). For example, the selective pressure on energetic optimization probably lead 488 Septembrie 2005 • Cogniţie, Creier, Comportament

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to a significant secondary brain size decrease in some species (Safi, Seid, & Dechmann, 2005). One would expect that the eyes of bats would also have been reduced similar to cave dwelling fish or amphibians if they were superfluous. In contrast, bats do have eyes, which function like typical mammalian eyes (Figure 3, reviewed in Eklöf, 2003).

Figure 3. Bats possess eyes and a fully functional sense of vision. The differences in the relative size of eyes indicate that species may rely on vision to different degrees. However, the role of vision for social communication has not been studies, a) Pteronotus parnellii (Mormoopidae), b) Noctilio leporinus (Noctilionidae), c) Epomophorus wahlbergii (Pteropodidae), d) Lambronycteris brachyotis (Phyllostomidae).

The results of the few studies investigating the role of vision indicate that visual information can overrule auditory information. For example, Plecotus auritus is more successful at finding meal worms in Petri dishes when both, acoustic and visual information is available, and visual information is more important although echolocation is also used throughout experiments (Eklöf & Jones, 2003). Similarly, Eptesicus nilssonii was able to find experimentally presented moths in the clutter overlap zone, where detection by echolocation is difficult and white moths where removed more successfully than black ones, again indicating the use and importance of vision for foraging (Eklöf et al., 2002). Sexual Septembrie 2005 • Cogniţie, Creier, Comportament

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dimorphisms in behaviour and/or external appearance indicate that vision may also play a role in communication. However, such dimorphisms are often connected to acoustic (such as the large rostrum of Hypsignathus monstrosus, used for singing in leks; (Bradbury, 1977a), or olfactory communication (such as the hovering displays of Saccopteryx bilineata used for the fanning of scents towards females; Voigt & von Helversen, 1999) Primarily, methods need to be established for the study of visual communication in bats. Careful planning of experiments will be necessary to distinguish between the role of visual from acoustic, olfactory, and other cues. This sensory channel thus represents a whole new challenge, whether in the context of communication or orientation and foraging.

REFERENCES Acharya, K. K., Roy, A., & Krishna, A. (1998). Relative role of olfactory cues and certain non-olfactory factors in foraging of fruit-eating bats. Behavioural Processes, 44(1), 59-64. Aebischer, N. J., Robertson, P. A., & Kenward, R. E. (1993). Compositional analysis of habitat use from animal radio-tracking data. Ecology, 74(5), 1313-1325. Aitchinson, J. (1982). Statistical analysis of compositional data. Journal of the Royal Statistical Society Series B, 44, 139-177. Altringham, J. D., & Fenton, M. B. (2003). Sensory Ecology and Communication in the Chiroptera. In T. H. Kunz & M. B. Fenton (Eds.), Bat Ecology (pp. 90-118). Chicago: The University of Chicago Press. Andrews, M. M., & Andrews, P. T. (2003). Ultrasound social calls made by greater horseshoe bats (Rhinolophus ferrumequinum) in a nursery roost. Acta Chiropterologica, 5(2), 221-234. Balcombe, J. P. (1990). Vocal Recognition of Pups By Mother Mexican Free-Tailed Bats, Tadarida-Brasiliensis-Mexicana. Animal Behaviour, 39, 960-966. Balcombe, J. P., & Fenton, M. B. (1988). Eavesdropping by Bats - the Influence of Echolocation Call Design and Foraging Strategy. Ethology, 79(2), 158-166. Balcombe, J. P., & McCracken, G. F. (1992). Vocal Recognition in Mexican Free-Tailed Bats - Do Pups Recognize Mothers. Animal Behaviour, 43(1), 79-87. Barclay, R. M. R. (1982). Interindividual Use of Echolocation Calls - Eavesdropping by Bats. Behavioral Ecology and Sociobiology, 10(4), 271-275. Barlow, K. E., & Jones, G. (1997). Function of pipistrelle social calls: Field data and a playback experiment. Animal Behaviour, 53(5), 991-999. Barton, R. A., Purvis, A., & Harvey, P. H. (1995). Evolutionary radiation of visual and olfactory brain systems in primates, bats and insectivores. Philosophical Transactions of the Royal Society of London Series B-Biological Sciences, 348(1326), 381-392. Baum, M. J., & Keverne, E. B. (2002). Sex difference in attraction thresholds for volatile odors from male and estrous female mouse urine. Hormones and Behavior, 41(2), 213-219. Beauchamp, G. K., Curran, M., & Yamazaki, K. (2000). MHC-mediated fetal odourtypes expressed by pregnant females influence male associative behaviour. Animal Behaviour, 60, 289-295. 490 Septembrie 2005 • Cogniţie, Creier, Comportament

Cognitie, Creier, Comportament / Cognition, Brain, Behavior Vol. IX(3), 497-510, 2005 ©Romanian Association of Cognitive Sciences

Behr, O., & von Helversen, O. (2004). Bat serenades - complex courtship songs of the sacwinged bat (Saccopteryx bilineata). Behavioral Ecology and Sociobiology, 56(2), 106-115. Berger, M., & Hart, J. S. (1974). Physiology and energetics of flight. In D. S. Farner & J. R. King (Eds.), Avian Biology IV (Vol. IV, pp. 260-415). New York: Academic Press. Bininda-Emonds, O. R. P., Decker-Flum, D. M., & Gittleman, J. L. (2001). The utility of chemical signals as phylogenetic characters: an example from the Felidae. Biological Journal of the Linnean Society, 72(1), 1-15. Bloss, J. (1999). Olfaction and the use of chemical signals in bats. Acta Chiropterologica, 1(1), 31-45. Bloss, J., Acree, T. E., Bloss, J. M., Hood, W. R., & Kunz, T. H. (2002). Potential use of chemical cues for colony-mate recognition in the big brown bat, Eptesicus fuscus. Journal of Chemical Ecology, 28(4), 819-834. Bodyak, N., & Slotnick, B. (1999). Performance of mice in an automated olfactometer: Odor detection, discrimination and odor memory. Chemical Senses, 24(6), 637-645. Bouchard, S. (2001). Sex discrimination and roostmate recognition by olfactory cues in the African bats, Mops condylurus and Chaerephon pumilus (Chiroptera : Molossidae). Journal of Zoology, 254, 109-117. Boughman, J. W. (1997). Greater spear-nosed bats give group-distinctive calls. Behavioral Ecology and Sociobiology, 40(1), 61-70. Boughman, J. W., & Wilkinson, G. S. (1998). Greater spear-nosed bats discriminate group mates by vocalizations. Animal Behaviour, 55(6), 1717-1732. Bradbury, J. W. (1977a). Lek mating-behavior in hammer-headed bats. Zeitschrift Fur Tierpsychologie-Journal of Comparative Ethology, 45(3), 225-255. Bradbury, J. W. (1977b). Social Organization and Communication. In W. A. Wimsatt (Ed.), Biology of Bats (Vol. 3, pp. 2-72). New York: Academic Press. Brooke, A. P., & Decker, D. M. (1996). Lipid compounds in secretions of fishing bat, Noctilio leporinus (Chiroptera: Noctilionidae). Journal of Chemical Ecology, 22(8), 1411-1428. Brown, R. E., & Macdonald, D. W. (1985). Social odours in Mammals. Oxford: Clarendon Press. Brown, R. E., Schellinck, H. M., & West, A. M. (1996). The influence of dietary and genetic cues on the ability of rats to discriminate between the urinary odors of MHC-congenic mice. Physiology & Behavior, 60(2), 365-372. Buesching, C. D., Waterhouse, J. S., & Macdonald, D. W. (2002). Gas-chromatographic analyses of the subcaudal gland secretion of the European badger (Meles meles) Part II: Time-related variation in the individual-specific composition. Journal of Chemical Ecology, 28(1), 57-69. Burger, B. V. (2005). Mammalian semiochemicals. In Chemistry of Pheromones and Other Semiochemicals Ii (Vol. 240, pp. 231-278). Berlin: Springer-Verlag Berlin. Cavaggioni, A., & Mucignat-Caretta, C. (2000). Major urinary proteins, alpha(2u)globulins and aphrodisin. Biochimica Et Biophysica Acta-Protein Structure and Molecular Enzymology, 1482(1-2), 218-228. Clanton, C. J., Nicolai, R. E., & Larson, V. J. (1999). Dynamic olfactometer airflow variation in determining odor dilutions-to-threshold. Transactions of the Asae, 42(6), 1847-1852. Cloe, A. L., Woodley, S. K., Waters, P., Zhou, H., & Baum, M. J. (2004). Contribution of anal scent gland and urinary odorants to mate recognition in the ferret. Physiology & Behavior, 82(5), 871-875. Septembrie 2005 • Cogniţie, Creier, Comportament

491

Cognitie, Creier, Comportament / Cognition, Brain, Behavior Vol. IX(3), 497-510, 2005 ©Romanian Association of Cognitive Sciences

Cortada, C., Valor, I., & Uribarri, E. (1997). The olfactometry as an analytical method for quantification of odours. Quimica Analitica, 16(3), 205-209. Crowley, P. H., Provencher, L., Sloane, S., Dugatkin, L. A., Sophn, B., Rogers, L., et al. (1996). Evolving cooperation: The role of individual recognition. Biosystems, 37(12), 49-66. Davis, W. H., & Barbour, R. W. (1965). Use of vision in flight by bat Myotis sodalis. American Midland Naturalist, 74(2), 497-&. De Fanis, E., & Jones, G. (1995). The role of odour in the discrimination of conspecifics by pipistrelle bats. Animal Behaviour, 49(3), 835-839. De Fanis, E., & Jones, G. (1996). Allomaternal care and recognition between mothers and young in pipistrelle bats (Pipistrellus pipistrellus). Journal of Zoology, 240, 781787. Deiss, V., Feron, C., & Baudoin, C. (1999). Discrimination of olfactory sexual cues in staggerer mutant male mice. Physiology & Behavior, 67(5), 631-634. Eggert, F., Muller-Ruchholtz, W., & Ferstl, R. (1998). Olfactory cues associated with the major histocompatibility complex. Genetica, 104(3), 191-197. Ehman, K. D., & Scott, M. E. (2001). Urinary odour preferences of MHC congenic female mice, Mus domesticus: implications for kin recognition and detection of parasitized males. Animal Behaviour, 62, 781-789. Eklöf, J. (2003). Vision in echolocating bats. Unpublished Dissertation, University of Göteborg, Göteborg. Eklöf, J., & Jones, G. (2003). Use of vision in prey detection by brown long-eared bats, Plecotus auritus. Animal Behaviour, 66, 949-953. Eklöf, J., Svensson, A. M., & Rydell, J. (2002). Northern bats, Eptesicus nilssonii, use vision but not flutter-detection when searching for prey in clutter. Oikos, 99(2), 347351. Emes, R. D., Beatson, S. A., Ponting, C. P., & Goodstadt, L. (2004). Evolution and comparative genomics of odorant-and pheromone-associated genes in rodents. Genome Research, 14(4), 591-602. Fenton, M. B. (1977). Variation in social calls of little brown Bats (Myotis lucifugus). Canadian Journal of Zoology-Revue Canadienne De Zoologie, 55(7), 1151-1157. Fenton, M. B. (2003). Eavesdropping on the echolocation and social calls of bats. Mammal Review, 33(3-4), 193-204. Fisher, H. S., Swaisgood, R. R., & Fitch-Snyder, H. (2003a). Countermarking by male pygmy lorises (Nycticebus pygmaeus): do females use odor cues to select mates with high competitive ability? Behavioral Ecology and Sociobiology, 53(2), 123-130. Fisher, H. S., Swaisgood, R. R., & Fitch-Snyder, H. (2003b). Odor familiarity and female preferences for males in a threatened primate, the pygmy loris Nycticebus pygmaeus: applications for genetic management of small populations. Naturwissenschaften, 90(11), 509-512. Fox, J. H., & Thiessen, D. D. (1984). An Olfactometer for Small Rodents. Behavior Research Methods Instruments & Computers, 16(5), 415-419. Gentner, T. Q., & Hulse, S. H. (2000). Female European starling preference and choice for variation in conspecific male song. Animal Behaviour, 59, 443-458. Gerelllundberg, K., & Gerell, R. (1994). The mating-behavior of the pipistrelle and the Nathusius pipistrelle (Chiroptera) - a comparison. Folia Zoologica, 43(4), 315-324. Gosling, L. M., Roberts, S. C., Thornton, E. A., & Andrew, M. J. (2000). Life history costs of olfactory status signalling in mice. Behavioral Ecology and Sociobiology, 48(4), 328-332. 492 Septembrie 2005 • Cogniţie, Creier, Comportament

Cognitie, Creier, Comportament / Cognition, Brain, Behavior Vol. IX(3), 497-510, 2005 ©Romanian Association of Cognitive Sciences

Gralapp, A. K., Powers, W. J., & Bundy, D. S. (2001). Comparison of olfactometry, gas chromatography, and electronic nose technology for measurement of indoor air from swine facilities. Transactions of the Asae, 44(5), 1283-1290. Gustin, M. K., & McCracken, G. F. (1987). Scent recognition between females and pups in the bat Tadarida brasiliensis-mexicana. Animal Behaviour, 35, 13-19. Haffner, M. (1989). Tasthaare als diagnostisches Merkmal bei mitteleuropäischen Vespertilionidae (Mammalia, Chiroptera). Unpublished PhD, Zurich, Zurich. Haffner, M. (1998). The size of sebaceous glands in relation to the size of hair follicles on the heads of some small mammals (Insectivora, Chiroptera, Rodentia). Annals of Anatomy-Anatomischer Anzeiger, 180(2), 165-171. Haffner, M. (2000). Structure and function of pilosebaceous units on the heads of small mammals (Insectivora, Chiroptera, Rodentia). Acta Zoologica, 81(3), 195-203. Hass, C. C., & Valenzuela, D. (2002). Anti-predator benefits of group living in white-nosed coatis (Nasua narica). Behavioral Ecology and Sociobiology, 51(6), 570-578. Heth, G., Nevo, E., & Todrank, J. (1996). Seasonal changes in urinary odors and in responses to them by blind subterranean mole rats. Physiology & Behavior, 60(3), 963-968. Heth, G., Todrank, J., Busquet, N., & Baudoin, C. (2001). Odour-genes covariance and differential investigation of individual odours in the Mus species complex. Biological Journal of the Linnean Society, 73(2), 213-220. Humphries, R. E., Robertson, D. H. L., Beynon, R. J., & Hurst, J. L. (1999). Unravelling the chemical basis of competitive scent marking in house mice. Animal Behaviour, 58, 1177-1190. Hurst, J. L., & Beynon, R. J. (2004). Scent wars: the chemobiology of competitive signalling in mice. Bioessays, 26(12), 1288-1298. Hurst, J. L., Thom, M. D., Nevison, C. M., Humphries, R. E., & Beynon, R. J. (2005). MHC odours are not required or sufficient for recognition of individual scent owners. Proceedings of the Royal Society of London Series B-Biological Sciences, 272(1564), 715-724. Hutcheon, J. M., Kirsch, J. W., & Garland, T. (2002). A comparative analysis of brain size in relation to foraging ecology and phylogeny in the chiroptera. Brain Behavior and Evolution, 60(3), 165-180. Joly, M., Michel, B., Deputte, B., & Verdier, J. M. (2004). Odor discrimination assessment with an automated olfactometric method in a prosimian primate, Microcebus murinus. Physiology & Behavior, 82(2-3), 325-329. Kalko, E. K. V., & Condon, M. A. (1998). Echolocation, olfaction and fruit display: How bats find fruit of flagellichorous cucurbits. Functional Ecology, 12(3), 364-372. Kazial, K. A., Burnett, S. C., & Masters, W. M. (2001). Individual and group variation in echolocation calls of big brown bats, Eptesicus fuscus (Chiroptera : Vespertilionidae). Journal of Mammalogy, 82(2), 339-351. Kazial, K. A., & Masters, W. M. (2004). Female big brown bats, Eptesicus fuscus, recognize sex from a caller's echolocation signals. Animal Behaviour, 67, 855-863. Klappert, K., & Reinhold, K. (2003). Acoustic preference functions and sexual selection on the male calling song in the grasshopper Chorthippus biguttulus. Animal Behaviour, 65, 225-233. Korine, C., Kalko, E. K. V., & Herre, E. A. (2000). Fruit characteristics and factors affecting fruit removal in a Panamanian community of strangler figs. Oecologia, 123(4), 560-568. Kraemer, S., & Apfelbach, R. (2004). Olfactory sensitivity, learning and cognition in young Septembrie 2005 • Cogniţie, Creier, Comportament

493

Cognitie, Creier, Comportament / Cognition, Brain, Behavior Vol. IX(3), 497-510, 2005 ©Romanian Association of Cognitive Sciences

adult and aged male Wistar rats. Physiology & Behavior, 81(3), 435-442. Lester, D. (1968). Effects of olfactory stimuli on Y-maze exploration of rats. Psychonomic Science, 12(3), 97-&. Luft, S., Curio, E., & Tacud, B. (2003). The use of olfaction in the foraging behaviour of the golden- mantled flying fox, Pteropus pumilus, and the greater musky fruit bat, Ptenochirus jagori (Megachiroptera : Pteropodidae). Naturwissenschaften, 90(2), 84-87. Mayeaux, D. J., & Johnston, R. E. (2002). Discrimination of individual odours by hamsters (Mesocricetus auratus) varies with the location of those odours. Animal Behaviour, 64, 269-281. McCracken, G. F., & Gustin, M. K. (1991). Nursing behavior in mexican free-tailed bat maternity colonies. Ethology, 89(4), 305-321. McCracken, G. F., & Wilkinson, G. S. (2000). Bat Mating Systems. In E. G. Crichton & P. H. Krutzsch (Eds.), Reproductive Biology of Bats (pp. 321-362). San Diego: Academic Press. McElligott, A. G., & Hayden, T. J. (2000). Lifetime mating success, sexual selection and life history of fallow bucks (Dama dama). Behavioral Ecology and Sociobiology, 48(3), 203-210. McNab, B. K. (1983). Energetics, Body Size, and the Limits to Endothermy. Journal of Zoology, 199(JAN), 1-29. Milinski, M., & Wedekind, C. (2001). Evidence for MHC-correlated perfume preferences in humans. Behavioral Ecology, 12(2), 140-149. Mucignat-Caretta, C., & Caretta, A. (1999). Chemical signals in male house mice urine: Protein-bound molecules modulate interactions between sexes. Behaviour, 136, 331343. Mucignat-Caretta, C., Cavaggioni, A., & Caretta, A. (2004). Male urinary chemosignals differentially affect aggressive behavior in male mice. Journal of Chemical Ecology, 30(4), 777-791. Mueller, H. C. (1968). Role of vision in vespertilionid bats. American Midland Naturalist, 79(2), 524-&. Munclinger, P., & Frynta, D. (1997). Relations between distant populations of Mus musculus sensu lato: Is there any odour-based discrimination? Folia Zoologica, 46(3), 193-199. Nieh, J. C., Barreto, L. S., Contrera, F. A. L., & Imperatriz-Fonseca, V. L. (2004). Olfactory eavesdropping by a competitively foraging stingless bee, Trigona spinipes. Proceedings of the Royal Society of London Series B-Biological Sciences, 271(1548), 1633-1640. Obrist, M. K. (1995). Flexible bat echolocation - the influence of individual, habitat and conspecifics on sonar signal-design. Behavioral Ecology and Sociobiology, 36(3), 207-219. Osada, K., Yamazaki, K., Curran, M., Bard, J., Smith, B. P. C., & Beauchamp, G. K. (2003). The scent of age. Proceedings of the Royal Society of London Series BBiological Sciences, 270(1518), 929-933. Pfaffmann, C., Goff, W. R., & Bare, J. K. (1958). Olfactometer for the Rat. Science, 128(3330), 1007-1008. Pfalzer, G., & Kusch, J. (2003). Structure and variability of bat social calls: implications for specificity and individual recognition. Journal of Zoology, 261, 21-33. Platek, S. M., Burch, R. L., & Gallup, G. G. (2001). Sex differences in olfactory selfrecognition. Physiology & Behavior, 73(4), 635-640. 494 Septembrie 2005 • Cogniţie, Creier, Comportament

Cognitie, Creier, Comportament / Cognition, Brain, Behavior Vol. IX(3), 497-510, 2005 ©Romanian Association of Cognitive Sciences

Russo, D., & Jones, G. (1999). The social calls of Kuhl's pipistrelles Pipistrellus kuhlii (Kuhl, 1819): structure and variation (Chiroptera : Vespertilionidae). Journal of Zoology, 249, 476-481. Ryan, M. J. (1991). Sexual Selection and Communication in Frogs. Trends in Ecology & Evolution, 6(11), 351-355. Rydell, J., & Eklöf, J. (2003). Vision complements echolocation in an aerial-hawking bat. Naturwissenschaften, 90(10), 481-483. Safi, K., & Dechmann, D. K. N. (2005). Adaptation of brain regions to habitat complexity: a comparative analysis in bats (Chiroptera). Proceedings of the Royal Society of London Series B-Biological Sciences, 272, 179-186. Safi, K., & Kerth, G. (2003). Secretions of the interaural gland contain information about individuality and colony membership in the Bechstein's bat. Animal Behaviour, 65, 363-369. Safi, K., Seid, M., & Dechmann, D. K. N. (2005). Bigger is not always better: when brains become smaller. Biology Letters, online. Schellinck, H. M., West, A. M., & Brown, R. E. (1992). Rats can discriminate between the urine odors of genetically identical mice maintained on different diets. Physiology & Behavior, 51(5), 1079-1082. Schnitzler, H. U., & Kalko, E. K. V. (2001). Echolocation by insect-eating bats. Bioscience, 51(7), 557-569. Schnitzler, H. U., Moss, C. F., & Denzinger, A. (2003). From spatial orientation to food acquisition in echolocating bats. Trends in Ecology & Evolution, 18(8), 386-394. Scully, W. M. R., Fenton, M. B., & Saleuddin, A. S. M. (2000). A histological examination of the holding sacs and glandular scent organs of some bat species (Emballonuridae, Hipposideridae, Phyllostomidae, Vespertilionidae, and Molossidae). Canadian Journal of Zoology-Revue Canadienne De Zoologie, 78(4), 613-623. Seine, R. (1988). Die Buccaldrüse beim Grossen Abendsegler, Nyctalus noctula Schreber, 1774: Morphologie und Gaschromatographische Analyse des Sekrets. Unpublished Diplomarbeit, Rheinischen Friedrich-Wilhelms Universität Bonn, Bonn. Serra-Cobo, J., Lopez-Roig, M., Marques-Bonet, T., & Lahuerta, E. (2000). Rivers as possible landmarks in the orientation flight of Miniopterus schreibersii. Acta Theriologica, 45(3), 347-352. Service, K. M., Brereton, R. G., & Harris, S. (2001). Analysis of badger urine volatiles using gas chromatography-mass spectrometry and pattern recognition techniques. Analyst, 126(5), 615-623. Singer, A. G., Beauchamp, G. K., & Yamazaki, K. (1997). Volatile signals of the major histocompatibility complex in male mouse urine. Proceedings of the National Academy of Sciences of the United States of America, 94(6), 2210-2214. Singh, D., & Bronstad, P. M. (2001). Female body odour is a potential cue to ovulation. Proceedings of the Royal Society of London Series B-Biological Sciences, 268(1469), 797-801. Smith, W. J. (1977). The behavior of communicating. Cambridge, Mass.: Harvard University Press. Stolberg, A. M., & Grigoryan, G. E. (1992). Olfactory Orientation of White-Rats in the YMaze. Zhurnal Vysshei Nervnoi Deyatelnosti Imeni I P Pavlova, 42(4), 797-799. Studier, E. H., & Lavoie, K. H. (1984). Microbial involvement in scent production in noctilionid bats. Journal of Mammalogy, 65(4), 711-714. Thies, W., E.K.V., K., & Schnitzler, H.-U. (1998). The roles of echolocation and olfaction in two Neotropical fruit-eating bats, Carollia perspicillata and C. castanea, feeding Septembrie 2005 • Cogniţie, Creier, Comportament

495

Cognitie, Creier, Comportament / Cognition, Brain, Behavior Vol. IX(3), 497-510, 2005 ©Romanian Association of Cognitive Sciences

on Piper. Behavioral Ecology and Sociobiology, 42(6), 397-409. Todrank, J., Heth, G., & Johnston, R. E. (1998). Kin recognition in golden hamsters: evidence for kinship odours. Animal Behaviour, 55, 377-386. Todrank, J., Heth, G., & Johnston, R. E. (1999). Social interaction is necessary for discrimination between and memory for odours of close relatives in golden hamsters. Ethology, 105(9), 771-782. Turlings, T. C. J., Davison, A. C., & Tamo, C. (2004). A six-arm olfactometer permitting simultaneous observation of insect attraction and odour trapping. Physiological Entomology, 29(1), 45-55. Voigt, C. C. (2002). Individual variation in perfume blending in male greater sac- winged bats. Animal Behaviour, 63, 907-913. Voigt, C. C., & von Helversen, O. (1999). Storage and display of odour by male Saccopteryx bilineata (Chiroptera, Emballonuridae). Behavioral Ecology and Sociobiology, 47(1-2), 29-40. Voigt, C. C., von Helversen, O., Michener, R., & Kunz, T. H. (2001). The economics of harem maintenance in the sac-winged bat, Saccopteryx bilineata (Emballonuridae). Behavioral Ecology and Sociobiology, 50(1), 31-36. von Helversen, O., Winkler, L., & Bestmann, H. J. (2000). Sulphur-containing "perfumes" attract flower-visiting bats. Journal of Comparative Physiology a-Sensory Neural and Behavioral Physiology, 186(2), 143-153. Wedekind, C., & Furi, S. (1997). Body odour preferences in men and women: do they aim for specific MHC combinations or simply heterozygosity? Proceedings of the Royal Society of London Series B-Biological Sciences, 264(1387), 1471-1479. Wedekind, C., Seebeck, T., Bettens, F., & Paepke, A. J. (1995). Mhc-dependent mate preferences in humans. Proceedings of the Royal Society of London Series BBiological Sciences, 260(1359), 245-249. Wilkinson, G. S., & Boughman, J. W. (1998). Social calls coordinate foraging in greater spear-nosed bats. Animal Behaviour, 55, 337-350. Williams, T. C., Williams, J. M., & Griffin, D. R. (1966). Homing ability of Neotropical bat Phyllostomus hastatus with evidence for visual orientation. Animal Behaviour, 14(4), 468-&. Willis, C., & Poulin, R. (2000). Preference of female rats for the odours of non-parasitised males: the smell of good genes? Folia Parasitologica, 47(1), 6-10. Winkler, L. (1998). Fledermausbestäubte Pflanzen. Unpublished Dissertation, FriedrichAlexander-Universität Erlangen-Nürnberg, Erlangen. Winter, Y., Lopez, J., & von Helversen, O. (2003). Ultraviolet vision in a bat. Nature, 425, 612-614. Winter, Y., & von Helversen, O. (1998). The energy cost of flight: do small bats fly more cheaply than birds? Journal of Comparative Physiology B-Biochemical Systemic and Environmental Physiology, 168(2), 105-111. Woodley, S. K., & Baum, M. J. (2003). Effects of sex hormones and gender on attraction thresholds for volatile anal scent gland odors in ferrets. Hormones and Behavior, 44(2), 110-118. Yamazaki, K., Singer, A., & Beauchamp, G. K. (1998). Origin, functions and chemistry of H-2 regulated odorants. Genetica, 104(3), 235-240.

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