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Primate Serenades: Call Variation, Species Diversity, and Adaptation in Nocturnal Strepsirhines
Abstract
Interspecific divergence in acoustic signaling systems is a major focus of biodiversity and evolutionary research, but empirical data for primates are rare. Our research team compared communication calls of four cryptic, genetically defined mouse lemur (Microcebus) species uttered in comparable social situations. We found that calls vary interspecifically to different extents depending on the context. The acoustic pattern of calls given in the startle context was conserved across species, whereas calls given in agonistic and mating contexts showed significant interspecific variation. Uniformity in the acoustic pattern of calls across species can be explained by similar physiological and environmental constraints; and divergences have been explained by several hypotheses including natural and sexual selection. Because of remarkable species-specific differences in frequency contours, advertisement calls are the most useful diagnostic tools for noninvasive species and subspecies identification.
... Acoustic signals may inform receivers about the sender's specific and individual identity, sex, social group, age class or physical abilities ('static' information; see Hopp et al. 1998;Charlton et al. 2009a;Zimmermann 2013). They may also give information about the sender's location, its motivation (such as in aggressive, territorial or courtship signals) and its emotional state ('dynamic' information; see Briefer 2012;Zimmermann 2013;Guerra KEYWORDS coding; vocalization; signal analysis; vocal signature; individual identity; mammals; sheep amplitude modulation) is thus required if we wish to fully understand the coding system of individual signature in lamb bleat. ...
... Acoustic signals may inform receivers about the sender's specific and individual identity, sex, social group, age class or physical abilities ('static' information; see Hopp et al. 1998;Charlton et al. 2009a;Zimmermann 2013). They may also give information about the sender's location, its motivation (such as in aggressive, territorial or courtship signals) and its emotional state ('dynamic' information; see Briefer 2012;Zimmermann 2013;Guerra KEYWORDS coding; vocalization; signal analysis; vocal signature; individual identity; mammals; sheep amplitude modulation) is thus required if we wish to fully understand the coding system of individual signature in lamb bleat. ...
... The fact that amplitude modulation is so strongly involved in the vocal individual signature of the lamb is interesting since few studies have demonstrated that this acoustic feature can be a highly individualized component of mammalian vocalizations (Charrier et al. 2003;Charrier and Harcourt 2006;Charlton et al. 2009Charlton et al. , 2009bCharrier et al. 2009;Pitcher et al. 2012;Aubin et al. 2015). Conversely, temporal parameter, as the amplitude modulation is classically considered as a 'labile' parameter, susceptible to variation induced by, e.g. the emotional state of the emitter, and it is usually not considered as a good candidate for bearing individuality (Briefer 2012;Zimmermann 2013). ...
The source-filter theory of vocal production supports the idea that acoustic signatures are preferentially coded by the fundamental frequency (source-induced variability) and the distribution of energy among the frequency spectrum (filter-induced variability). By investigating the acoustic parameters supporting individuality in lamb bleats, a vocalization which mediates recognition by ewes, here we show that amplitude modulation – an acoustic feature largely independent of the shape of the acoustic tract – can also be an important cue defining an individual vocal signature. Female sheep (Ovis aries) show an acoustic preference for their own lamb. Although playback experiments have shown that this preference is established soon after birth and relies on a unique vocal signature contained in the bleats of the lamb, the physical parameters that encode this individual identity remained poorly identified. We recorded 152 bleats from 13 fifteen-day-old lambs and analyzed their acoustic structure with four complementary statistical methods (ANOVA, potential for individual identity coding PIC, entropy calculation 2Hs, discriminant function analysis DFA). Although there were slight differences in the acoustic parameters identified by the four methods, it remains that the individual signature relies on both the temporal and frequency domains. The coding of the identity is thus multi-parametric and integrates modulation of amplitude and energy parameters. Specifically, the contribution of the amplitude modulation is important, together with the fundamental frequency F0 and the distribution of energy in the frequency spectrum.
... She became particularly interested in the role of advertisement calls in speciation (Zimmermann, 1992(Zimmermann, , 2017(Zimmermann, , 2018Zimmermann et al., 2000a). By comparing advertisement calls of different closely related species, she noticed that bioacoustics is a powerful tool for discriminating cryptic species (Zimmermann, 2013(Zimmermann, , 2016 and used this tool to investigate speciation in the cryptic mouse lemurs (Microcebus spp.;Braune et al., 2008;Hasiniaina et al., 2020;Zimmermann, 2013Zimmermann, , 2016Zimmermann et al., 2000b). One of her last papers showed that similarities in agonistic calls match phylogenetic proximity (Hasiniaina et al., 2020). ...
... She became particularly interested in the role of advertisement calls in speciation (Zimmermann, 1992(Zimmermann, , 2017(Zimmermann, , 2018Zimmermann et al., 2000a). By comparing advertisement calls of different closely related species, she noticed that bioacoustics is a powerful tool for discriminating cryptic species (Zimmermann, 2013(Zimmermann, , 2016 and used this tool to investigate speciation in the cryptic mouse lemurs (Microcebus spp.;Braune et al., 2008;Hasiniaina et al., 2020;Zimmermann, 2013Zimmermann, , 2016Zimmermann et al., 2000b). One of her last papers showed that similarities in agonistic calls match phylogenetic proximity (Hasiniaina et al., 2020). ...
... It defines species as sexually reproducing populations that share a system of fertilization mechanisms (Paterson 1985(Paterson , 1993. In particular, specific-mate recognition signals that enable assortative mating are species diagnostic because species define their own boundaries, maintained by stabilizing selection (Ambrose 2003;Bearder et al. 1995;Braune et al. 2008;1996;Masters 1991Masters , 1993Nietsch and Kopp 1998;Pozzi et al. 2019;Zimmermann 1990Zimmermann , 2013Zimmermann et al. 2000). The recognition concept is an exclusive alternative to the most extreme phylogenetic species concept, the universal species concept, which regards lineage separation as both a necessary and sufficient condition for speciation (de Queiroz 2007;Mendelson and Shaw 2012;Sullivan 2009). ...
... The newly recognized species diversity of cryptic nocturnal strepsirrhines was established on the basis of such slight morphological differences (e.g., Groves 2000;Masters and Couette 2015;Rasoloarison et al. 2000), molecular sequence variation, allopatric distributions (e.g., Lei et al. 2017;Olivieri et al. 2007;Pozzi et al. 2019Pozzi et al. , 2020Schüßler et al. 2020;Yoder et al. 2000), as well as distinct vocalizations (e.g., Ambrose 2003;Bearder et al. 1995Bearder et al. , 1996Braune et al. 2008;Masters 1991Masters , 1993Nietsch and Kopp 1998;Pozzi et al. 2019;Zimmermann 1990Zimmermann , 2013Zimmermann et al. 2000). This pluralistic approach based on different species concepts was advocated by many authors (Mayr 1996;Mendelson and Shaw 2012;Sullivan 2009;Tattersall 2013) but often leads to discrepancies, explored in this contribution, focussing on the Paragalago zanzibaricus complex. ...
Cryptic animal species are often distinguishable by nonvisual communication signals used in specific-mate recognition. The three cryptic taxa comprising the Paragalago zanzibaricus species complex use distinct loud calls that do not obviously reflect molecular phylogenetic relationships. Paragalago granti and P. cocos both have incremental calls but are not sister taxa; P. cocos is the sister taxon to P. zanzibaricus, which has a rolling (trilling) call like that of P. rondoensis, one of the outliers to the complex. To test current hypotheses of species delimitation, I conducted 378 playback trials, using conspecific and heterospecific loud calls and recording both vocal responses and movement toward the speaker. To investigate the sensory drive hypothesis (acoustic adaptation), I measured reverberation duration of 215 short “yap” mobbing calls and examined 282 sonotopes (local soundscapes). I tested the hypothesis that different species’ ear lengths allow the animals to filter out interfering frequencies in local background noise. On Zanzibar Island, P. zanzibaricus responded solely to conspecific calls (23/32). In South Africa, P. granti individuals responded to conspecific calls (12/22) but also sometimes to P. cocos calls (9/22). In Kenya, P. cocos individuals responded to conspecific calls (34/40) but also sometimes to P. zanzibaricus calls (8/40). The three habitats showed differences in reverberation duration, and soundscapes differed in background orthopteran frequencies. Incremental calls probably evolved in the ancestor of the complex, in response to high levels of reverberation and a continuous backdrop of katydid stridulation in dry forest. Secondary evolution of trilling and decreased ear size probably evolved as result of decreased reverberation and higher frequency katydid interference in the P. cocos–P. zanzibaricus ancestor. A loss of short units in P. zanzibaricus probably occurred as result of decreased reverberation in thicket. The study validates the three species of the complex and provides information supporting speciation by sensory drive.
... Intraspecific differences in call structure also occur among populations of robust chimpanzees (Pan troglodytes) [Mitani et al., 1999;Crockford et al., 2004], silvery gibbons (Hylobates moloch) [Dallmann and Geissmann, 2001] and pygmy marmosets (Callithrix pygmaea) [De La Torre and Snowdon, 2009]. In strepsirhines, comparison of the spectral parameters of the loud call is the most useful diagnostic tool for subspecies identification [Zimmermann, 2012]. ...
Vocal repertoires and call structure can provide insights into the behaviour and evolution of species, as well as aid in taxonomic classification. Nocturnal primates have large vocal repertoires. This suggests that acoustic communication plays an important role in their life histories. Little is known about the behavioural context or the intraspecific variation of their vocalisations. We used autonomous recording units and manual recorders to investigate the vocal behaviour and structure of loud calls of the small-eared greater galago (Otolemur garnettii)in Kenya and Tanzania. We describe the vocal repertoire, temporal calling patterns and structure of 2 loud calls of 2 subspecies: O. g. panganiensis and O. g. kikuyuensis. We found considerable intraspecific structural differences in both loud calls. These are congruent with the current subspecies classification. Differences in vocalisations among populations are not consistent with the “acoustic adaptation hypothesis,” rather they are likely a result of geographic variation due to isolation caused by vegetational barriers in southern Kenya.
... Predators are nocturnal viverrids, domestic cats and dogs, raptors and owls, as well as snakes. As in other nocturnal primates, acoustic and olfactory signals are of the utmost importance for governing predator avoidance as well as spacing between and cohesion within social groups Braune et al. , 2005Braune et al. , , 2008Scheumann et al. , 2007 ;Sündermann et al ., 2008 ;Zimmermann 2010Zimmermann , 2013Kappel et al. , 2011 ;Hohenbrink et al. , 2012Hohenbrink et al. , , 2013Kessler et al. , 2012 ). Due to their small body size, mouse lemurs can be maintained and bred cost-effi ciently under controlled experimental conditions in captivity Bons et al. , 2006 ;Lacreuse and Herndon, 2009 ;Fischer and Austad, 2011 ;Finch and Austad, 2012 ;Languille et al. , 2012 ) and currently three captive research colonies of more than 100 mouse lemurs exist worldwide (Brunoy and Montpellier, France, for M. murinus and Hannover, Germany, for M. murinus and M. lehilahytsara ). ...
... Predators are nocturnal viverrids, domestic cats and dogs, raptors and owls, as well as snakes. As in other nocturnal primates, acoustic and olfactory signals are of the utmost importance for governing predator avoidance as well as spacing between and cohesion within social groups Braune et al. , 2005Braune et al. , , 2008Scheumann et al. , 2007 ;Sündermann et al ., 2008 ;Zimmermann 2010Zimmermann , 2013Kappel et al. , 2011 ;Hohenbrink et al. , 2012Hohenbrink et al. , , 2013Kessler et al. , 2012 ). Due to their small body size, mouse lemurs can be maintained and bred cost-effi ciently under controlled experimental conditions in captivity Bons et al. , 2006 ;Lacreuse and Herndon, 2009 ;Fischer and Austad, 2011 ;Finch and Austad, 2012 ;Languille et al. , 2012 ) and currently three captive research colonies of more than 100 mouse lemurs exist worldwide (Brunoy and Montpellier, France, for M. murinus and Hannover, Germany, for M. murinus and M. lehilahytsara ). ...
... Predators are nocturnal viverrids, domestic cats and dogs, raptors and owls, as well as snakes. As in other nocturnal primates, acoustic and olfactory signals are of the utmost importance for governing predator avoidance as well as spacing between and cohesion within social groups Braune et al. , 2005Braune et al. , , 2008Scheumann et al. , 2007 ;Sündermann et al ., 2008 ;Zimmermann 2010Zimmermann , 2013Kappel et al. , 2011 ;Hohenbrink et al. , 2012Hohenbrink et al. , , 2013Kessler et al. , 2012 ). Due to their small body size, mouse lemurs can be maintained and bred cost-effi ciently under controlled experimental conditions in captivity Bons et al. , 2006 ;Lacreuse and Herndon, 2009 ;Fischer and Austad, 2011 ;Finch and Austad, 2012 ;Languille et al. , 2012 ) and currently three captive research colonies of more than 100 mouse lemurs exist worldwide (Brunoy and Montpellier, France, for M. murinus and Hannover, Germany, for M. murinus and M. lehilahytsara ). ...
The dwarf and mouse lemurs of Madagascar are two very species-rich lemur genera, yet there is a relative paucity of information on this primate family in published literature. In this first ever treatment of the Cheirogaleidae, international experts are brought together to review and integrate our current knowledge of the behaviour, physiology, ecology, genetics and biogeography of these species. A wide range of direct and indirect research methods that are currently used to study these cryptic nocturnal solitary foragers are described. By uniting often disparate research on captive and free-ranging taxa and synthesising recent methodological advances, this book provides new insights that will encourage further studies of this fascinating primate family. This synthesis will provide an incentive for more integrative studies of the Cheirogaleidae in captivity and in the wild, enabling the impacts of deforestation and other factors to be identified and directions for future conservation efforts to be established.
... Predators are nocturnal viverrids, domestic cats and dogs, raptors and owls, as well as snakes. As in other nocturnal primates, acoustic and olfactory signals are of the utmost importance for governing predator avoidance as well as spacing between and cohesion within social groups Braune et al. , 2005Braune et al. , , 2008Scheumann et al. , 2007 ;Sündermann et al ., 2008 ;Zimmermann 2010Zimmermann , 2013Kappel et al. , 2011 ;Hohenbrink et al. , 2012Hohenbrink et al. , , 2013Kessler et al. , 2012 ). Due to their small body size, mouse lemurs can be maintained and bred cost-effi ciently under controlled experimental conditions in captivity Bons et al. , 2006 ;Lacreuse and Herndon, 2009 ;Fischer and Austad, 2011 ;Finch and Austad, 2012 ;Languille et al. , 2012 ) and currently three captive research colonies of more than 100 mouse lemurs exist worldwide (Brunoy and Montpellier, France, for M. murinus and Hannover, Germany, for M. murinus and M. lehilahytsara ). ...
... Some controversy exists over the taxonomic validity over the newly named species, associated in large part with problems of sample size and geographic coverage, and diffi culty in distinguishing clinal variation from distinct phylogenetic species (Tattersall, 2007 ;Markolf et al ., 2011 ). Although cryptic species are often differentiated solely on the basis of genetics (Pastorini et al ., 2001 ;Olivieri et al ., 2007 ;Horvath et al ., 2008 ;Groeneveld et al ., 2009 ;Weisrock et al ., 2012 ), integrative studies of primate taxonomy have recently used diet, social system, communication signals, sleeping site ecology, and reproductive behavior to delineate species boundaries (Kamilar, 2006 ;Radespiel et al ., 2006 ;Zimmermann, 2013 ;Zimmermann and Radespiel, 2014 ). Such studies have demonstrated that sympatric species of Microcebus coexist in several regions of Madagascar (Yoder et al ., 2005 ;Weisrock et al ., 2010 ;Rasoloarison et al ., 2013 ). ...
The dwarf and mouse lemurs of Madagascar are two very species-rich lemur genera, yet there is a relative paucity of information on this primate family in published literature. In this first ever treatment of the Cheirogaleidae, international experts are brought together to review and integrate our current knowledge of the behaviour, physiology, ecology, genetics and biogeography of these species. A wide range of direct and indirect research methods that are currently used to study these cryptic nocturnal solitary foragers are described. By uniting often disparate research on captive and free-ranging taxa and synthesising recent methodological advances, this book provides new insights that will encourage further studies of this fascinating primate family. This synthesis will provide an incentive for more integrative studies of the Cheirogaleidae in captivity and in the wild, enabling the impacts of deforestation and other factors to be identified and directions for future conservation efforts to be established.
... Soft vocalizations (e.g., hums in indris; grumbles calls in sifakas) are described regulating contact with other group members at short distances (Pollock, 1975;Petter and Charles-Dominique, 1979;Macedonia and Stanger, 1994;Maretti et al., 2010;Patel and Owren, 2012). Nocturnal lemurs which form permanent sleeping groups, but forage solitarily during the night, such as mouse lemurs, use acoustic signals in the context of mating, intra-group cohesion (mother2infant, sleeping group reunions) and group coordination (Hafen et al., 1998;Braune et al., 2005;Scheumann and Zimmermann, 2007b), as well as during conflicts with con-and heterospecifics (Zimmermann, 2010(Zimmermann, , 2013Zimmermann et al., 2013). Olfactory mechanisms seem to be important for regulating the distribution of groups in space (Braune et al., 2005) and avoiding predators (S€ undermann et al., 2008;Kappel et al., 2011). ...
Objectives:
How social groups govern their distribution in time and space is a central question in socioecology. The aim of this study is to explore the role of acoustic signaling for spacing and cohesiveness in a nocturnal, cohesive, pair-living strepsirrhine.
Material and methods:
The study was conducted in northwestern Madagascar. Six pairs of Avahi occidentalis were radio-collared and home range usage, vocalizations and call-associated behavior recorded using GPS-based focal animal sampling. Home range size was analyzed using ArcView GIS 3.3. Calls were characterized by a multiparametric sound analysis.
Results:
Three frequently used, acoustically distinct call types were identified: the avahee call, the whistle call, and the growling call, the latter is a soft; the two others are loud calls. Call types are given by both sexes and convey individually-specific signatures. Call types are used primarily in the locomotion context in the non-core-area of home ranges. The least common avahee call is responded by the avahee call from farther away. The more common whistle call, given when partners become visually isolated, and the growling call emitted at close distances, were answered by the whistle and the growling call. Results suggest a spacing function for the avahee call and group coordination functions for the other call types.
Discussion:
Our study provides first empirical evidence for a nocturnal, cohesive pair-living strepsirrhine that vocal signaling represents an important mechanism for spacing, group coordination and decision making. Findings contribute to a better understanding of the evolutionary roots of primate vocal communication. Am J Phys Anthropol, 2015. © 2015 Wiley Periodicals, Inc.
... 15 Our subsequent integrative work has shown, however, that they also differ genetically, 16,17 as well as in their sleeping-site ecology, 18 habitat preferences, 18 feeding ecology, 18 reproduction, 18 geographical distribution, 17,18 social system, 18 and acoustic communication. 19,20 By applying bioacoustic methods, we provided the first evidence of the specific relevance of social calls to speciation in primates. 19 Our findings on the acoustic divergence of advertisement calls of the two sympatric morphs supported the hypothesis that specific differences in signaling and recognition systems can represent an efficient premating isolation mechanism that contributes to morph cohesiveness in sympatry. ...
... 15 Our subsequent integrative work has shown, however, that they also differ genetically, 16,17 as well as in their sleeping-site ecology, 18 habitat preferences, 18 feeding ecology, 18 reproduction, 18 geographical distribution, 17,18 social system, 18 and acoustic communication. 19,20 By applying bioacoustic methods, we provided the first evidence of the specific relevance of social calls to speciation in primates. 19 Our findings on the acoustic divergence of advertisement calls of the two sympatric morphs supported the hypothesis that specific differences in signaling and recognition systems can represent an efficient premating isolation mechanism that contributes to morph cohesiveness in sympatry. ...
Humans primarily rely on vision when categorizing the world. If you just look at the same-sized but strikingly differently colored Neotropical poison-dart frogs such as strawberry frogs (Fig. ), you would be convinced that they must belong to different species. However, this is an excellent example of a polymorphic species, meaning that although these frogs look quite different, mating decisions are made based on their conspicuous and species-specific advertisements calls, which are not primarily linked to specific color pattern. The situation is quite different among nocturnal primates living in dense forest environments, such as the tiny nocturnal Malagasy mouse lemurs. In this case, even geographically isolated, well-accepted species look superficially quite similar and are therefore often termed cryptic species (Fig. ). Some morphs are a bit larger than others or show minor phenotypic differences, but morph-specific differences are difficult to detect in living subjects. This phenomenon explains why, until the end of the last century, species diversity in mouse lemurs was assumed to be low, with only two morphologically distinct species. Over the last two decades, several international working groups, including our own, undertook a massive island-wide sampling effort, including DNA sequencing and phylogenetic analyses of mouse lemurs. These revealed a 10-fold higher species diversity, with 21 currently described species. Are these new species, mostly defined based on the phylogenetic species concept (sensu Cracraft), or independent evolutionary lineages or, perhaps, only artifacts of taxonomic inflation? What is a species? How can we identify primate species? How and why do species emerge during evolution?
Information on primate vocalisations can be applied in several ways, including: improving captive welfare, as a census tool for cryptic species, or to investigate the impacts of anthropogenic disturbance on species’ behaviour (Delgado and van Shaik, 2000; Konrad and Geissman, 2006; Jacobsen et al., 2010). Vocalisations can be used as a taxonomic tool, and structural differences between calls have been used to compare a wide variety of taxa, including species of gibbon (Hylobatidae spp., Ruppell, 2010), marmosets (Callithrix spp., Mendes et al., 2009), owls (Strigidae spp., Flint et al., 2015), wolves (Canis spp., Kershenbaum et al., 2016), and galagos (Galagidae spp., Svensson et al., 2017). Additionally, differences in voca- lisations across taxonomic groups can be used to help determine genetic distances between species or investigate why vocal behaviours evolved (Blumstein and Armitage, 1998; Ord and Garcia-Porta, 2012).
Bioacoustic analyses of animal vocalizations are predominantly accomplished through manual scanning, a highly subjective and time-consuming process. Thus, validated automated analyses are needed that are usable for a variety of animal species and easy to handle by non-programing specialists. This study tested and validated whether DeepSqueak, a user-friendly software, developed for rodent ultrasonic vocalizations, can be generalized to automate the detection/segmentation, clustering and classification of high-frequency/ultrasonic vocalizations of a primate species. Our validation procedure showed that the trained detectors for vocalizations of the gray mouse lemur ( Microcebus murinus ) can deal with different call types, individual variation and different recording quality. Implementing additional filters drastically reduced noise signals (4225 events) and call fragments (637 events), resulting in 91% correct detections (N total = 3040). Additionally, the detectors could be used to detect the vocalizations of an evolutionary closely related species, the Goodman’s mouse lemur ( M. lehilahytsara ). An integrated supervised classifier classified 93% of the 2683 calls correctly to the respective call type, and the unsupervised clustering model grouped the calls into clusters matching the published human-made categories. This study shows that DeepSqueak can be successfully utilized to detect, cluster and classify high-frequency/ultrasonic vocalizations of other taxa than rodents, and suggests a validation procedure usable to evaluate further bioacoustics software.
The dwarf and mouse lemurs of Madagascar are two very species-rich lemur genera, yet there is a relative paucity of information on this primate family in published literature. In this first ever treatment of the Cheirogaleidae, international experts are brought together to review and integrate our current knowledge of the behaviour, physiology, ecology, genetics and biogeography of these species. A wide range of direct and indirect research methods that are currently used to study these cryptic nocturnal solitary foragers are described. By uniting often disparate research on captive and free-ranging taxa and synthesising recent methodological advances, this book provides new insights that will encourage further studies of this fascinating primate family. This synthesis will provide an incentive for more integrative studies of the Cheirogaleidae in captivity and in the wild, enabling the impacts of deforestation and other factors to be identified and directions for future conservation efforts to be established.
Studies of animal behavior often assume that all members of a species exhibit the same behavior. Geographic Variation in Behavior shows that, on the contrary, there is substantional variation within species across a wide range of taxa. Including work from pioneers in the field, this volume provides a balanced overview of research on behavioral characteristics that vary geographically. The authors explore the mechanisms by which behavioral differences evolve and examine related methodological issues. Taken together, the work collected here demonstrates that genetically based geographic variation may be far more widespread than previously suspected. The book also shows how variation in behavior can illuminate both behavioral evolution and general evolutionary patterns. Unique among books on behavior in its emphasis on geographic variation, this volume is a valuable new resource for students and researchers in animal behavior and evolutionary biology.
This chapter discusses species concepts, and the particular applicability of the Recognition Concept to nocturnal primates.
There is a bewildering diversity of signals, sensory systems, and signaling behavior. A consideration of how these traits affect each other's evolution explains some of this diversity. Natural selection favors signals, receptors, and signaling behavior that maximize the received signals relative to background noise and minimize signal degradation. Properties of sensory systems bias the direction of evolution of the signals that they receive. For example, females may prefer males whose signals they can perceive more easily, and this will lead to the spread of more easily perceived male traits. Environmental conditions during signal transmission and detection also affect signal perception. Specific environmental conditions will bias the evolutionary direction of behavior, which affects the time and place of signaling as well as microhabitat preferences. Increased specialization of microhabitats and signaling behavior may lead to biased evolution of the sensory systems to work more efficiently. Thus, sensory systems, signals, signaling behavior, and habitat choice are evolutionarily coupled. These suites of traits should coevolve in predictable directions, determined by environmental biophysics, neurobiology, and the genetics of the suites of traits--hence the term "sensory drive." Because conditions vary in space and time, diversity will be generated
Scientists often posit an intimate connection between form and function, a conceptual approach that plays a central role in evolutionary anthropology. Functional morphologists and paleontologists, for example, routinely connect structure and function in exploring how skeletal features of fossils reflect adaptations to particular motor demands. Archeologists' reconstructions of early hominid life-ways are guided by functional interpretations of material remains, while both primatologists and human ecologists use structural properties of the environment to understand important aspects of social organization. Although comparisons to human language were characteristic of early work on nonhuman primate vocal behavior as well, during the last two or more decades they also have become dominent in the anthropological subfield of acoustic primatology. This strategy has paid dividends by, for example, generating widespread interest in primate signaling and catalyzing a variety of fruitful empirical studies. However, it also creates conceptual worries, particularly in the teleology inherent in using complex linguistic phenomena from humans as models for simpler vocal processes in nonhumans.
Recent work on human vocal production demonstrates that certain irregular phenomena seen in human pathological voices and baby crying result from nonlinearities in the vocal production system. Equivalent phenomena are quite common in nonhuman mammal vocal repertoires. In particular, bifurcations and chaos are ubiquitous aspects of the normal adult repertoire in many primate species. Here we argue that these phenomena result from properties inherent in the peripheral production mechanism, which allows individuals to generate highly complex and unpredictable vocalizations without requiring equivalently complex neural control mechanisms. We provide examples from the vocal repertoire of rhesus macaques, Macaca mulatta, and other species illustrating the different classes of nonlinear phenomena, and review the concepts from nonlinear dynamics that explicate these calls. Finally, we discuss the evolutionary significance of nonlinear vocal phenomena. We suggest that nonlinear phenomena may subserve individual recognition and the estimation of size or fluctuating asymmetry from vocalizations. Furthermore, neurally ‘cheap’ unpredictability may serve the valuable adaptive function of making chaotic calls difficult to predict and ignore. While noting that nonlinear phenomena are in some cases probably nonadaptive by-products of the physics of the sound-generating mechanism, we suggest that these functional hypotheses provide at least a partial explanation for the ubiquity of nonlinear calls in nonhuman vocal repertoires.
Geographic variation in primate vocalizations has been described at two levels. First, at the level of acoustic variation within the same call type between populations and, second, at the level of presence or absence of certain call types in different populations. Acoustic variation is of interest because there are several factors that can explain this variation, such as gene flow, ecological factors and population density. Here we focus on the first level in a Southeast Asian primate, the Thomas langur. We recorded male loud calls in four populations that differed in their geographic distances from each other and had varying geographic barriers in between them, such as rivers and mountain ranges. The presence of these barriers leads to expectations of loud call variation under the gene flow model, which are examined here. We conducted a principal components analysis to condense the number of acoustic variables. With a subsequent discriminant function analysis on the six principal component scores, we found that the percentage of loud calls that were correctly assigned to a population was relatively high (50.0-76.2%) when three randomly selected loud calls from each male were used. Using the discriminant functions from this analysis to predict population membership of the remainder of the loud calls yielded lower, but still relatively high correct assignment percentages (26.2-66.7%). Analyses to examine the influence of barriers on similarities between populations confirm our expectations. We discuss that differences in loud calls are probably most parsimoniously explained by gene flow (or the lack thereof) between the populations and that future studies of genetic differences are crucial to test this hypothesis.
A central question in evolutionary biology is how cryptic species maintain species cohesiveness in an area of sympatry. The coexistence of sympatrically living cryptic species requires the evolution of species-specific signalling and recognition systems. In nocturnal, dispersed living species, specific vocalisations have been suggested to act as an ideal premating isolation mechanism. We studied the structure and perception of male advertisement calls of three nocturnal, dispersed living mouse lemur species, the grey mouse lemur (Microcebus murinus), the golden brown mouse lemur (M. ravelobensis) and the Goodman's mouse lemur (M. lehilahytsara). The first two species occur sympatrically, the latter lives allopatrically to them.
A multi-parameter sound analysis revealed prominent differences in the frequency contour and in the duration of advertisement calls. To test whether mouse lemurs respond specifically to calls of the different species, we conducted a playback experiment with M. murinus from the field using advertisement calls and alarm whistle calls of all three species. Individuals responded significantly stronger to conspecific than to heterospecific advertisement calls but there were no differences in response behaviour towards statistically similar whistle calls of the three species. Furthermore, sympatric calls evoked weaker interest than allopatric advertisement calls.
Our results provide the first evidence for a specific relevance of social calls for speciation in cryptic primates. They furthermore support that specific differences in signalling and recognition systems represent an efficient premating isolation mechanism contributing to species cohesiveness in sympatrically living species.
Sir Charles Lyell opened his first notebook on “the species question” in 1855 (Wilson, 1970). A hundred years later, Mayr (1957) edited a volume entitled The Species Problem. Now, 34 years on, Eldredge has opened this volume with a title that emphasizes, once again, that crucial step in understanding natural organization: “What, if Anything, Is a Species?” In recognition of this probing tradition, I have constructed this chapter around a series of questions and possible answers relating to the application of species concepts, particularly to primates. I should point out that while Eldredge has tended to deal with the ontological side of the question—what we think species really are—this contribution is directed more toward epistemological issues—how do we identify the kinds of species that we believe to exist?
This paper describes a concept, not altogether new but largely neglected, that should lead to a greater understanding of the information contained in certain classes of vocal communication signals of birds and mammals. The concept is based on empirical data, first pointed out by Collias (1960, p. 382), showing that natural selection has resulted in the structural convergence of many animal sounds used in "hostile" and "friendly" contexts. Simply stated, birds and mammals use harsh, relatively low-frequency sounds when hostile and higherfrequency, more pure tonelike sounds when frightened, appeasing, or approaching in a friendly manner. Thus, there appears to be a general relationship between the physical structures of sounds and the motivation underlying their use. I hope to develop the idea that this relationship has had a far greater influence on the evolution of animal communication systems than has hitherto been discussed. I will discuss the idea that there exist motivation-structural rules (MS) governing the physical structure of close contact sounds in animal communication systems. The greatest value of the MS concept is that it provides the opportunity to compare the evolution of vocal communication in any species against an abstract concept. The adaptive nature of communication systems against varying backgrounds of environment, social system, and competition will appear in clear relief.
The adult vocal repertoire of T. belangeri consists of 8 distinct sounds which are organized into a graded system. Within the repertoire 4 basic acoustic structures have been distinguished which can be associated with one of the following functional categories: contact, aggression, defence, attention and alarm; Elements repeated continually at short regular intercall intervals showing narrow frequency band spectra occur during courtship and mating in males; Elements of short duration with harmonic spectra, low fundamentals and often low frequency noise components signal alarm which consequently focuses other individuals' attention on the sender or the external stimulus; Elements of irregular repetition rate showing broadband harmonic spectra of highly variable duration and frequency modulation are associated with the vocalizers defensive behavior; Elements with noisy spectra over a wide frequency range parallel aggressive behavior by the vocalizer which is often intensified with visual threat display. The findings of the present study are compared and discussed with data from literature referring to tupaia vocalizations. A comparison with the call system of insectivores and prosimians revealed similarities as well as divergencies. Presence of many similarities regarding the basic structural patterning of contact, aggressive and defensive vocalizations in the three orders indicates a certain conservatism in these sounds. Propagation of alarm calls in tree shrews which lacks in insectivores appears to be a more recent evolutionary development in mammals with the highest degree of elaboration in primates.
Vocalizations and concurrent behaviours of adult slow loris kept in small groups under seminatural conditions were recorded during their nocturnal activity period. According to structural criteria 8 fairly distinct call types were determined which could be related to one of the two functionally defined sound categories, ‘contact and contact-seeking’ and ‘aggressive and defensive calls’. Comparison with other bioacoustic studies of the family Lorisidae revealed general trends in the evolution of call systems in two subfamilies Lorisinae and Galaginae.Copyright © 1985 S. Karger AG, Basel
Acoustic structures, situations and proposed messages of vocalisations used by the nocturnal arboreal prosimian species Galago senegalensis senegalensis are described. Eighteen different sounds are identified which could be related to one of the following functional categories: contact, aggressive and defensive and attention and alarm behaviour. The call types within these behavioural categories show striking similarities in their acoustic structures. Vocalisations used during inter- and intragroup contact situations demonstrate harmonic spectra with low frequency fundamentals and formants and slight frequency modulations. Noisy spectra as well as an irregular repetition rate characterize sounds uttered by the aggressor during agonistic encounters. They can be intensified by visual threat displays. Harmonic spectra, high frequency fundamentals and formants, and rapid frequency modulations are typical for calls given by submissives during aggressive intraspecific interactions. Sounds which indicate social or external disturbance factors show noisy and harmonic spectra with broad dominant frequency range as well as a regular repetition rate. Factors that might have favoured the evolution of this call system are discussed.
Relatively few data exist on population differences in the vocal behavior of mammals. Geographic variation in calls is of special interest because of the implications for resolving evolutionary and behavioral questions. For example, information on geographic variation in vocalizations complements morphological and molecular data used to infer phylogenetic relationships and provides evidence for the mechanisms underlying call development. A quantitative acoustic analysis of orangutan long calls was undertaken, comparing flanged adult males from four geographically distinct sites across Borneo and Sumatra, revealing consistent differences among the calls of individuals. Long calls produced by orangutans from the four sites in Borneo and Sumatra differ in quantitative acoustic measures. Discriminant function analysis reveals that acoustic variables can be used in combination to assign calls to the correct individual, site and island at rates higher than that expected by chance. Specifically, four acoustic parameters proved reliable for distinguishing among the individuals, between sites, and across the two islands that arguably represent populations from separate species or subspecies. Although Bornean and Sumatran long calls share a repetitive structure and show similar call rates (0.100–0.500 LCs/h) and maximum frequency bands (0.400–1.500 kHz), they differ significantly in the number of pulses per call, call speed, call duration, bandwidth, pulse duration, and dominant frequency. Strong consistency in these acoustic parameters is also seen among males within sites and the observed variation may allow for individual recognition. Individual identification by call structure presumably benefits dispersed orangutans, where individuals characteristically forage independently and both encounters and interactions with signaling males are highly variable and largely dependent on context. Acoustic recognition of callers facilitates the choice of which males to join or avoid, thus allowing receivers to manipulate potential costs and benefits of association.
During the breeding season sexually active male mouse lemurs produce a trill call used for advertising. The trill call displays a variable, high pitched, complex frequency and amplitude modulated acoustical structure and is given with a high sound intensity. The different sources of its variation in structure and usage have to be determined to understand its complex acoustical design and function. We investigated the vocal morphology of the trill call of males with known age and weight as well as the behavioral context, in order to evaluate sources of its variation. Cluster and discriminant analyses revealed that the structure of trill calls showed a high degree of individual stereotypy in contrast to a high interindividual variability. A set of three distinct variables (fundamental frequency of call onset, bandwidth of 3rd frequency modulation and end frequency of 7th modulation) was sufficient to identify individual senders with almost 90% probability. The structure of the trill call of adult males was independent of age, weight and context and was stable over at least one breeding season. Its individually distinct call structure and use in relation to social status provide the potential for individual recognition and for assessing the “quality” of a male.
This chapter discusses the evolution, function, and meaning of marmot alarm communication. Alarm calls are a system in which one can study the dynamics of altruism. Calls can contain potentially referential information about the specific type of predator and information about the degree of risk that the caller faces while calling. Moreover, alarm‐calling systems may offer some unique insights into the adaptive significance of individuality. The chapter focuses on alarm communication; marmots obtain other information about risk acoustically. Many species respond to the sounds that their predators make. A phylogenetic reconstruction of the ability to respond to the sound of predators predicts that yellow‐bellied marmots should respond to predators. Recent experiment suggests that marmots have an innate ability to respond to the sounds of locally extinct predators. Future work can focus on the specific acoustic cues that marmots use, which enable them to respond to novel predators.
In order to remain stable, dispersed social groups have to solve two fundamental problems: the coordination of movement and cohesiveness within a group and the spacing between the groups. Here, we investigate mechanisms involved in intra-group coordination and inter-group spacing using the golden brown mouse lemur, Microcebus ravelobensis, as a model for a nocturnal, solitary foraging mammal with a dispersed social system. By means of radiotelemetry and bioacoustics we studied the olfactory and vocal behaviour during nocturnal dispersal and reunion of five sleeping groups.
All groups used 3–17 sleeping sites exclusively, suggesting a sleeping site-related territoriality and competition for them. The occurrence of olfactory and vocal behaviour showed an asymmetrical temporal distribution. Whereas marking behaviour was observed exclusively during dispersal, a particular call type, the trill, was used by all groups during reunions. Interestingly, these trills carried group-specific signatures.
Our findings provide the first empirical evidence for nocturnal primates in a natural environment that olfactory signals represent an important mechanism to regulate the distribution of different groups in space, whereas acoustic signals control intra-group cohesion and coordination.
The grey mouse lemur (Microcebus murinus) has a dispersed social structure, within which female sleeping associations are common. These sleeping associations have been hypothesised to confer anti-predatory and thermoregulatory benefits, especially when rearing offspring. The genetic composition of these associations was determined using microsatellite markers to test predictions derived from kin selection theory. 161 (99 males, 62 females) individual M. murinus belonging to a free-living population in Ampijoroa, north-western Madagascar, were genotyped and observed over a total of 13 months distributed over the dry seasons of 3 successive years (1995-1997). Kin selection theory predicts that these female associations should consist of closely related members, and that female philopatry and male natal dispersal should characterise the dispersal pattern within this species. These predictions were confirmed by the data. Five out of six female sleeping groups consisted of one or more closely related dyads. Females that slept alone did not have close female kin in the vicinity or within the population at all. Closely related female dyads lived in significantly closer proximity than closely related male dyads and closely related male-female dyads showed intermediate proximity. In combination with the result that females possessed significantly more relatives within the population than males, these findings support the behavioural hypotheses of female philopatry and male natal dispersal. Matrilinear grouping patterns and sex-biased dispersal are therefore genetically established in a dispersed primate social organisation for the first time. The results further indicate that several generations of mouse lemurs live together within a given area, implying both an effective mechanism of kin recognition to avoid father-daughter incest and the potential for social learning to ensure individual recognition.
This chapter reviews our current knowledge on vocal expression of emotional states in a prosimian primate group, the mouse lemurs, by applying a cross-taxa concept of emotion. In this concept, emotions are defined based on their adaptive significance. Using standardized ethological protocols, we were able to predictably induce changes in vocal expression of mouse lemurs by manipulating defined stimuli or situations. Whereas infants produced context-specific vocalizations linked to the external environment, adults additionally linked vocal features to the respective interaction partner. In a courtship paradigm, mouse lemur males showed dynamic changes in vocal expression paralleling the intensity of arousal evoked by the condition of females and their behavior. In contrast to rodents, neither vomeronasalectomy nor bulbectomy affected vocal production. Castration led to a decrease in vocal rate of a specific vocal expression. The emission of the latter, however, was not related to plasma testosterone in intact males. Altogether, the findings suggested that vocal control was more linked to individual social experience than to olfactory input or gonadal androgens. A comparison of three context-specific acoustically distinct vocal expressions across different mouse lemur species indicated that comparable vocal features were used across species to convey a particular individualized context, and thereby a specific appetitive or aversive state.The findings support the hypothesis that vocalizations of mouse lemurs express the emotional state of a signaler reliably when linked to the respective individualized context.
Predation represents an important selective force shaping the evolution of primate behavior. Primates confronted with predators
have evolved various strategies to minimize the probability of being eaten. Predation risk and hunting styles of predators
should have selected for communicative and cognitive abilities linked to socioecology and life history. As studies on several
socially cohesive mammals indicate, the study of anti-predator behavior represents an important tool for gaining insight into
cognition, e.g., to understand how animals classify objects and events in the world around them (e.g., marmots: Blumstein, 1999; vervet monkeys: Seyfarth et al., 1980; Diana monkeys: Zuberbühler, 2000; suricates: Manser et al., 2002).
In mammals individual distinctiveness in vocalizations provides the basis for individual recognition and thus plays an important role in social behavior. In this study, first evidence is provided for a nocturnal primate that variation in individual distinctiveness across the vocal repertoire is to some extent determined by the context and the acoustic structure of the call types. Individual distinctiveness was investigated across call types in the gray mouse lemur, a nocturnal primate, living in a dispersed multi-male multi-female social system. To explore to what degree context and acoustic structure predict variations in individual distinctiveness, four major call types were examined (grunts, tsaks, short whistles, and trills). Call types differed in context and acoustic structure and were recorded under controlled experimental conditions. A discriminant function analysis revealed that all call types are individually distinct, but not to the same degree. The findings suggest that variations in individual distinctiveness can to some extent be explained by the context and the acoustic structure of the call types.
Male primates have evolved particular displays to advertise male fitness. In nocturnal prosimians it was assumed that such displays (vocal advertisement, marking behaviour) are hormonally dependent and influenced by olfactory cues of a receptive female. To test this assumption mouse lemur males of different gonadal status (males castrated as adults, normal males), or of varying olfactory input (males vomeronasalectomized or bulbectomized as adults) were paired with intact "stimulus" preoestrous females and vocalization, vocal rates, and marking behaviours were monitored. The vocal rate of only one particular vocalization, the "trill" advertisement call, was sexually dimorphic and changed depending on gonadal status. Vocalization rate declined significantly in sexually experienced, castrated males as did their marking behaviour. There was however no significant correlation between either calling rate or marking behaviour and plasma testosterone levels in gonadally intact males. Neither vomeronasalectomy nor bulbectomy had a significant effect on trill calling rate or marking behaviour. Results imply that testicular hormones have a greater impact on advertisement calling and marking motivation than olfactory information of preoestrous females. In contrast to rodents, ultrasonic calling rate seems to be not only dependent on gonadal status, but also on social experience.
Sexual advertisement calls of male mouse lemurs from two neighbouring demes in a dry deciduous forest of western Madagascar were recorded during the breeding season. Demes were located about 1.5 km apart with no geographic barrier between them. They were characterised morphometrically and genotyped by RAPD fingerprinting. According to univariate and multivariate statistical analysis, demes differed neither in body measurements, nor in the banding patterns produced by RAPD fingerprinting. The acoustic pattern of the advertisement call, however, showed significant differences: Six variables of the frequency and time domain differed between the demes. Discriminant function analysis revealed that one variable, total call duration, was sufficient to classify more than 89% of the calls correctly to the corresponding deme. We postulate that these differences are comparable to dialects in birds, because demes were morphologically and genetically indistinguishable and no barrier prevented genetic exchange between them. Possible explanations for the emergence of dialects in a prosimian species are outlined.
Cheirogaleidae currently comprises five genera whose relationships remain contentious. The taxonomic status and phylogenetic position of both Mirza coquereli and Allocebus trichotis are still unclear. The taxonomic status of the recently discovered Microcebus ravelobensis (a sympatric sibling species of Microcebus murinus) and its phylogenetic position also require further examination. A approximately 2.4-kb mitochondrial DNA sequence including part of the COIII gene, complete ND3, ND4L, and ND4 genes, and 5 tRNAs was used to clarify relationships among cheirogaleids. Mirza and Microcebus form a clade representing the sister group of Allocebus, with a clade containing Cheirogaleus major and Cheirogaleus medius diverging first. M. ravelobensis and Microcebus rufus form a subclade within Microcebus, with M. murinus as its sister group. The molecular data support the generic status of Mirza coquereli and species-level divergence of M. ravelobensis. Furthermore, "M. rufus" may well represent more than one species.
Our study provides the first data on the social organization of the golden brown mouse lemur, a nocturnal primate discovered in northwestern Madagascar in 1994. The study was carried out in two 6-month field periods during the dry season, covering time before and during the mating season. The spatial and temporal distributions of the sexes in the population were investigated by mark/recapture and radiotelemetry. Focal observations and the determination of sleeping associations provided further insights into the sociality of this solitary forager. High intra- and intersexual home-range overlaps occurred throughout the study. In general, individuals of both sexes had spatial access to more than one conspecific of the same and the opposite sex. We found no indication for spatial monopolization of females by certain males. These results suggest a dispersed multimale/multifemale system with a promiscuous mating pattern. Individuals showed temporal stability in their home range locations and interacted regularly with conspecifics. Five sleeping groups were identified during the study period: one female group and four mixed-sex groups. Even though sleeping sites were changed frequently, sleeping-group compositions remained stable over time. Thermoregulatory constraints are the most likely explanation for sleeping-group composition with members of both sexes in this species. Mixed-sex sleeping groups can be described as the basic social unit within this dispersed multimale/multifemale society.
Female mate choice can be hypothesised in most nocturnal primates, since females show a higher investment in their offspring than males. The aim of this experimental study was to investigate if female grey mouse lemurs perform mate choice and whether age, relatedness (to the male), or male advertisement call activity systematically influence their decisions. A two-way mate choice design was developed in which females could choose between two males. Mate choice was deduced from the time spent in proximity to the males and from mating behaviour. During oestrus 12 of 17 females participated actively in the experiment and all of them showed either a significant spatial (n = 11) or behavioural (n = 1) preference for one male. In four cases copulations were observed. The influence of age on female mate choice was not statistically significant. In the cases with copulations, however, females mostly preferred the older male. This might indicate a preference for older age as an indicator of experience, fitness, and/or status. The influence of relatedness on female mate choice could not be definitely clarified. However, results imply a mechanism of kin recognition on the basis of familiarity. In the majority of choices, females preferred the male with higher trill call activity. Since trill call activity correlates with the relative dominance status of males, these results suggest an importance of the male dominance status for female mate choice in grey mouse lemurs. Altogether our findings indicate that females use a complex of different cues to choose their mates.
Mouse lemurs (Microcebus spp.) are the world's smallest primates and endemic to Madagascar. Several recent taxonomic revisions resulted in an extraordinary increase of recognized species. What still was considered as being two species at the beginning of the 20th century is currently recognized as 12 taxa. Based on fur coloration pattern, they can be divided into grayish and reddish forms. Two major models have been proposed to explain the extensive speciation events in the Malagasy fauna. The best known suggests that major rivers and mountains combine to act as effective barriers to gene flow and thereby facilitate allopatric speciation processes. A more recent model used an analysis of watersheds in the context of Quaternary climatic shifts to explain the process of explosive speciation on the island. We tested these two models by covering the areas between all major rivers (n=8) in northwestern and northern Madagascar. Mouse lemurs were systematically caught, sampled and morphometrically characterized in 25 sites (with 2-49 individuals per site and species). A complete phylogeny was constructed on the basis of the sequences of three mitochondrial loci (in total 1296 bp). The phylogenetic data revealed a previously unknown biodiversity with three new mouse lemur species among the reddish forms, each having a very small distribution, i.e., being restricted to only one Inter-River-System (IRS). Morphometric analyses underlined their distinctiveness and a brief formal species description is provided. In contrast to the reddish forms, grayish forms have a very low species diversity coupled with broad distributions that cover more than one IRS. These differences among the species are discussed as outcome of divergent colonization scenarios. Elements of both biogeographic models are combined in a new hypothesis that aims to explain the speciation process leading to the present distribution of mouse lemurs in Madagascar.
Despite the considerable amount of interest in phylogeny reconstruction, patterns of homoplasy in morphological and behavioral data have received only limited attention to date, whereas the patterns of homoplasy in molecular data are relatively well understood. First, because the number of alternative molecular character states is strictly limited (particularly for nucleotide sequence data), higher rates of substitution generate higher levels of homoplasy. Second, depending on the relative proportions of constrained and unconstrained sites, each molecular data set has a time frame of applicability outside of which resolution becomes ambiguous. There is good evidence to suggest that numbers of alternative character states for morphological and even behavioral data may be similarly limited and that higher rates of evolution are often linked to higher rates of homoplasy. Like molecular data sets, morphological and behavioral data sets contain rapidly evolving characters as well as more conservative elements. Morphologies and behaviors related to sexual recognition and reproduction show low levels of intraspecific variation, but high levels of lability between species, making them crucial for species identification but often poor as markers of relationship at greater time depths. The organization theory of speciation derived by Carson is a model based on genome dynamics, and it predicts exactly this window of applicability for characters related to sexual reproduction. Nonsexual characters related to environmental adaptation should be applicable at greater phylogenetic depths. A better understanding of patterns of homoplasy enables a more sophisticated approach to the assessment of the relative reliabilities of alternative tree topologies.
The presence of context-specific communication sounds, structurally different call types related to particular situations and potentially expressing distinct emotions of the caller, were not systematically studied in infants of strepsirrhine primates. We exposed suckling's of gray mouse lemurs (Microcebus murinus) in an infant separation paradigm to three distinct contexts (isolation, threat-induced, grooming). An audio-videographic analysis of sound-correlated infant behaviors and a simultaneous multiparametric sound analysis revealed context-specific calls. Peak frequency predicted their acoustic classification best. Findings provided first evidence for a strepsirrhine primate that infant communication sounds may express distinct contexts and thereby infant's need reliably.
Interspecific affinities among guenons as deduced from vocalizations (eds) A primate radiation: evolutionary biology of the African guenons
- J-P Gautier
Predation, communication and cognition in lemurs
- M Scheumann
- A Rabesandratana
- E Zimmermann
Scheumann M, Rabesandratana A, Zimmermann E (2007a) Predation, communication and cognition in lemurs. In: Gursky SL, Nekaris KAI (eds) Primate anti-predator strategies. Springer,
New York, pp 100-126
Artendiversitaet bei Mausmakis: die Bedeutung der akustischen Kommunikation
- V Zietemann
Zietemann V (2000) Artendiversitaet bei Mausmakis: die Bedeutung der akustischen
Kommunikation. Unpubl. PhDthesis, University of Hannover, Hannover
Morphology, behavior and molecular evolution of giant mouse lemurs
- Pm Kappeler
- Rm Rasoloarison
- L Razafimanantsoa
- L Walter
- C Roos
Vocal expression of emotion in a nocturnal prosimian group, mouse lemurs Handbook of mammalian vocalization
- E Zimmermann