The role of facial pattern variation for species recognition in red-fronted lemurs (Eulemur rufifrons)
© The Author(s). 2018
Received: 28 June 2017
Accepted: 16 January 2018
Published: 13 February 2018
Species recognition, i.e., the ability to distinguish conspecifics from heterospecifics, plays an essential role in reproduction. The role of facial cues for species recognition has been investigated in several non-human primate species except for lemurs. We therefore investigated the role of facial cues for species recognition in wild red-fronted lemurs (Eulemur rufifrons) at Kirindy Forest. We presented adult red-fronted lemurs pictures of male faces from five species including red-fronted lemurs, three closely related species, white-fronted lemurs (E. albifrons), brown lemurs (E. fulvus), rufous brown lemurs (E. rufus), and genetically more distant red-bellied lemurs (E. rubriventer), occurring in allopatry with the study population. We predicted that red-fronted lemurs respond stronger to conspecific than to heterospecific pictures and that females show stronger responses than males. In addition, if genetic drift has played a role in the evolution of facial color patterns in the members of this genus, we predicted that responses of red-fronted lemurs correlate negatively with the genetic distance to the different species stimuli.
Red-fronted lemurs looked significantly longer at pictures of their own species than at those of heterospecifics. Females spent less time looking at pictures of white-fronted, brown and red-bellied lemurs than males did, but not to pictures of red-bellied lemurs and a control stimulus. Individuals also exhibited sniffing behavior while looking at visual stimuli, and the time spent sniffing was significantly longer for pictures of conspecifics compared to those of heterospecifics. Moreover, the time spent looking and sniffing towards the pictures correlated negatively with the genetic distance between their own species and the species presented as stimulus.
We conclude that red-fronted lemurs have the ability for species recognition using visual facial cues, which may allow them to avoid costly interbreeding. If so, sexual selection might have influenced the evolution of facial patterns in eulemurs. Since responses also correlated with genetic distance, our findings suggest a potential role of genetic drift as well as sexual selection in influencing the evolution of facial variation in eulemurs. Because study subjects looked and sniffed towards the presented pictures, red-fronted lemurs might have the ability for multi-modal species recognition.
The ability to differentiate conspecifics from heterospecifics plays an important role in reproduction [1–6]. Since females usually experience higher costs during reproduction than males, heterospecific mating is more costly for females [7–9]. Females should therefore be selected to recognize and discriminate against heterospecific males to avoid costly interbreeding . Indeed, the ability for species recognition has been demonstrated in several taxa, such as bats using olfactory signals , fish using olfactory or visual signals [10, 11] and frogs, birds and mammals using acoustic signals [12–15].
Visual cues have been suggested to be important for several animal taxa as they can be used for individual as well as species recognition [11, 16–18]. In addition, facial color patterns are among the phenotypic traits that play a communicative role in many social interactions of primates [19–24]. Facial cues can contain visual information such as shape and colors that differ across individuals or species [25–28], and they can provide information about social status, condition and identity of an individual [22, 23, 29, 30]. Several studies have demonstrated the ability of non-human primates to differentiate individuals of their own kin/group from strangers and also to discriminate between conspecifics and heterospecifics based on visual cues [2, 21, 31–35]. For example, chimpanzees (Pan troglodytes) and rhesus macaques (Macaca mulatta) used facial cues in black-and-white photographs presented on a computer screen to discriminate between different individuals . Chimpanzees are also able to discriminate kin by means of black-and-white photographs of mothers and their offspring, matching mother-son dyads but not mother-daughter ones . Finally, Tonkean macaques (Macaca tonkeana) and brown capuchin monkeys (Cebus apella) were able to discriminate between pictures of conspecific and heterospecific individuals, as inferred by their longer looking time towards pictures of conspecifics .
The lemurs of Madagascar also exhibit highly diverse facial color patterns [37, 38], which may have a communicative function in social interactions as well as in species recognition. So far only a few studies have investigated the potential use of visual signals for individual or species recognition in lemurs, however. For example, brown and black lemurs (Eulemur macaco) were able to differentiate between familiar and unfamiliar individuals by using facial cues , and females of seven eulemur species differentiated colorful from non-colorful conspecific male photographs , suggesting a potential ability for visual species recognition as well. In contrast to visual signals, olfactory signals are used by some species to discriminate conspecifics from heterospecifics [41–43], whereas acoustic signals, especially long-distance calls, appear to be used in mouse lemurs (Microcebus murinus) to distinguish conspecifics from heterospecifics .
Among lemurs, eulemurs are the only taxon with sexual dichromatism, as males are particularly colorful and show considerably more variation in facial patterns than females [24, 38]. Eulemurs have dichromatic color vision, except for some females that exhibit polymorphic trichromacy [45–49], suggesting that variation in facial coloration can be perceived by them (see also ). Additional visual information used in this context may include variation in patterns, shape and contrasts.
Genetic distance and description of facial color patterns for the different species (species are listed according to their genetic distance between red-fronted lemurs and the respective species)
Dark red crown, black muzzle, golden-red cheek beard, creamy-white patches above the eyes.
Rufous brown lemurs
Genetic distance: 0.35
Allopatric heterospecific and very similar to red-fronted lemurs in facial color patterns: brick-red crown, golden-red cheek beard, black muzzle and black midfacial stripe extending from crown to nose.
Genetic distance: 0.72
Occurs in allopatry with red-fronted lemurs and facial color variation differs strongly from red-fronted lemurs. Black muzzle and white beard, cheeks and crown.
Genetic distance: 0.72
Occurs in allopatry with red-fronted lemurs and is slightly different in facial color patterns. Dark-brown to almost black muzzle and crown, light grey beard and variable patches of light fur above the eyes.
Genetic distance: 4.57
Occurs in sympatry with red-fronted lemurs in the eastern parts of Madagascar but not at the study site in the West and is very different in facial color patterns. Black muzzle, face shading to black; patches of white skin form characteristic “tear-drops” beneath the eyes, no bushy beard.
If variation in facial color patterns is used for species recognition in eulemurs, we predicted that red-fronted lemurs should respond stronger to pictures of faces of their own species than to pictures of faces of heterospecifics. Additionally, if sexual selection has played a role in the evolution of facial color pattern variation, we predicted that females should show stronger responses than males. Finally, as the species used as stimuli differ in phylogenetic distance to the test species, we predicted that if genetic drift has played a role in the evolution of facial color patterns in eulemurs, the response of red-fronted lemurs should correlate negatively with their respective genetic distance to the different species used as stimuli.
Time spent looking towards the picture
Parameter estimated for the Linear Mixed Models (LMM) on the influence of (a) the species of the presented picture and (b) the genetic distance between species on the percentage of time spent looking towards the pictures. The influence (c) of species of the presented picture and (d) the genetic distance between species on the percentage of time spent sniffing the pictures
Percentage of time spent looking towards the pictures
rufous brown lemurs
rufous brown lemurs-sex male
brown lemurs- sex male
white-fronted lemurs-sex male
red-bellied lemurs-sex male
Percentage of time spent looking towards the pictures
Percentage of time spent of sniffing events
rufous brown lemurs
Percentage of time of sniffing events
Duration of sniffing
This study provides the first investigation of wild lemurs’ ability to discriminate between photographs of their own and closely related species. Our results indicate that red-fronted lemurs can use facial cues to discriminate between conspecifics and heterospecifics. Interestingly, test subjects also spent more time sniffing during presentation of conspecific pictures, indicating that they also may use olfactory cues in this context. Hence, they might simultaneously process olfactory and visual information to differentiate conspecifics from heterospecifics, suggesting that multi-modal communication might play a role in species recognition in these animals. Moreover, males and females differed in time spent looking towards the pictures of some heterospecifics, which may suggest a potential role of sexual selection in the evolution of facial variation in this species. Since the time spent looking as well as sniffing at the pictures were negatively correlated with genetic distances between red-fronted lemurs and the stimuli species, genetic drift may have also influenced the evolution of facial color patterns in this species. Finally, our study showed that the experimental use of photographs is feasible to test the ability of wild non-human primates for species recognition, which has been so far studied only in captive settings [2, 22, 34, 36, 39]. We discuss these key results in more detail below.
The variation in time spent looking at the pictures indicates that red-fronted lemurs are able to discriminate between the pictures of conspecifics and heterospecifics. Looking duration also appeared to correspond to the similarity of facial patterns between red-fronted lemurs and the other species: rufous brown lemurs are very similar in facial appearance to red-fronted lemurs, and these two species are also difficult for humans to distinguish (Fig. 1, Table 1), whereas white-fronted, brown and red-bellied lemurs are gradually more different in facial appearance. In addition, females spent less time looking towards pictures of white-fronted, brown and red-bellied lemurs than males, thus exhibiting a more pronounced differentiated response. Since we adjusted the size of the pictures to the average head size of the respective species, we cannot completely rule out the possibility that the responses of red-fronted lemurs were influenced by the slight differences in size of the pictures. However, if the size of the stimulus per se has influenced their responses, they should have responded more strongly to the control, which was adjusted to the average size of all stimuli, but they looked only briefly at this stimulus.
As interbreeding can occur in non-human primates (e.g. in macaques , eulemurs [50–55], sexual selection may act on species to avoid potentially costly heterospecific mating. Pronounced sexual dichromatism and striking differences in male patterning and coloration may provide a substrate for species recognition in the context of mate choice, and our experiments indicate that females perceive and respond to this variation. For example, red-bellied lemurs occur in sympatry with red-fronted, brown and white-fronted lemurs in the east of Madagascar . Because these three species are visually very different from its sympatric congener, facial color variation might have played a role in creating reproductive barriers among these species during their recent divergence . Because some eulemur species hybridize in their natural contact zones, future experiments in hybrid zones could investigate whether individuals in these zones discriminate potential mates based on variation in facial patterns.
Sex differences in responses towards the pictures might also reflect differences in color vision between sexes. Females can have polymorphic trichromacy or be dichromatic, whereas males are all dichromatic. Hence, eulemur females exhibiting a polymorphic trichromacy have the ability to perceive red and orange colors , and may therefore have shown a more pronounced differentiated response than males. However, the genetic tests required to test this assumption have not been performed. Interestingly, males payed more attention to stimuli of white-fronted, brown and red-bellied lemurs than females. Indeed, facial colors of these three species are dominated by a dark face with light (white or light gray) patches (Fig. 1). As red-fronted lemur males exhibit only dichromatic color vision [24, 62], contrasting dark and light areas might be more salient stimuli to them than to potentially trichromatic females.
The degree of phenotypic differences between red-fronted lemurs and white-fronted, brown, rufous brown and red-bellied lemurs also corresponds both to the genetic distance between them, as well as to the time red-fronted lemurs spent looking at the various stimuli. Similarly, the looking duration of macaques towards pictures of several heterospecific species also correlated with their morphological similarity in facial patterns as well as the genetic distance between them [2, 34]. Genetic differentiation as a result of drift during and following recent speciation events may therefore also have played a role in the evolution of facial color pattern in eulemurs.
Finally, multiple studies demonstrated that animals can process and use signals of different modalities for species recognition [63–65]. For example, male blackcaps (Sylvia atricapilla) are able to associate acoustic and visual sensory modalities in matching species-specific songs and species-specific plumage to distinguish their own species from sympatric heterospecifics (Sylvia borin) during playback experiments presented in combination with stuffed models of conspecifics and heterospecifics . In non-human primates, for instance, tufted capuchin monkeys (Cebus apella), rhesus macaques (Macaca mulatta) as well as Japanese macaques (Macaca fuscata) are able to use visual and acoustic sensory modalities (voice-face matching) to distinguish between conspecifics and heterospecifics [66–68]. Moreover, ringtailed lemurs (Lemur catta) are capable of multi-modal (olfactory-auditory matching) individual recognition , and the use of olfactory signals for species recognition in some eulemurs has been already shown [41, 43]. Whether red-fronted lemurs are capable of multi-modal species recognition was not explicitly tested in this study. However, our results showed that while red-fronted lemurs processed visual cues during the experiment, they also sniffed at the stimuli. Thus, red-fronted lemurs might be able to use two different sensory modalities (olfactory-visual matching) at the same time to discriminate individuals of their own species from heterospecifics. However, explicit experiments with signals of two different modalities are required to confirm our preliminary conclusion that red-fronted lemurs dispose of multi-modal species recognition abilities.
This study revealed the importance of facial cues as visual signals for species recognition in wild red-fronted lemurs. Females of red-fronted lemurs may also be better at differentiating conspecifics from heterospecifics due to sex difference in color vision abilities. Our findings suggest a potential role for sexual selection as well as genetic drift in influencing the evolution of facial variation in eulemurs. Moreover, this study revealed evidence for visual species recognition abilities in wild red-fronted lemurs and also suggested a potential for multi-modal species recognition. However, it remains unclear which specific components of the facial cues are used for species recognition, requiring further investigations to identify the essential cue(s), such as colors, patterns or a combination of both, used by eulemurs to discriminate their own from different species as well as among individuals.
Experiments were conducted with red-fronted lemurs in Kirindy Forest, western Madagascar (Fig. 1). Study subjects are individually marked as part of a long-term study and are well habituated to human observers [56, 57]. We studied eight adult females and seven adult males in four different groups (2–5 subjects per group).
Responses of experimental subjects were recorded with a SONY digital video camera from briefly before until 60 s after the onset of each experiment. The camera was placed in front of the focal animal, aligned with the picture frame so that looking direction could be clearly recorded. Based on these video-recordings, we measured the time each subject spent looking towards the picture after the onset (looking direction within a 45° angle of the direct line of sight towards the picture), and calculated the percentage of time spent looking towards the picture from the total time spent looking around. In addition, during the experiments, we observed sniffing behaviors of focal individuals while conducting the experiments. We therefore measured also the time individuals spent sniffing (inhaling a short and distinct breath through the nose combined with very small movements of the snout) towards each picture after the onset and calculated the percentage of time spent sniffing (see Additional file 1). Videos were analyzed frame-by-frame with a resolution of 30 frames/s, using Adobe Premiere Elements (12.0). All experiments were rated by HR, and 10% were rated again by a second observer naïve to the research question. We used R to calculate the intra-class correlation coefficient (ICC) to test for inter-observer reliability. The resulting ICC was 0.95 indicating strong agreement between raters.
Sample video showing an individual of red-fronted lemurs looking at the picture with sniffing behavior. (MP4 3840 Kb)
We used linear mixed models (LMM) to test for differences in the percentage of time red-fronted lemurs spent looking towards the pictures as well as the percentage of time spent sniffing at the pictures in response to different stimuli using LmerTest package in R . Percentage of time looking towards the pictures and percentage of time sniffing in the direction of the pictures were arcsine-square root transformed and fitted as responses. Species and sex were fitted as fixed factors and individual identity as a random factor to control for repeated measurements. Because the genetic distance correlates with the categories of the species, we fitted a second LMM in order to examine whether the percentage of time red-fronted lemurs spent looking and sniffing towards the pictures was influenced by the genetic distances between red-fronted lemurs and the species providing the stimuli. The percentage of time spent looking or sniffing towards the pictures were fitted as response, genetic distance and sex were fitted as fixed factors and individual identity as random factor. All analyses were conducted in R version 3.1.3.
We thank the Malagasy Ministère de l’Environnement et des Eaux et Forêts, the Departement de Biologie Ecologie et Conservation Animale de l’Université d’Antananarivo, the Centre National de Formation, d’Etudes et de Recherche en Environnement et Foresterie de Morondava, Madagascar National Parks and the Centre ValBio Ranomafana for allowing and supporting research in Kirindy Forest and Ranomafana National Park. We are grateful to Daniela Fuchs for helping with the video analyses, as well as Stephen Nash for the illustrations of Eulemur faces and Matthias Markolf for the photographs. We thank the German Academic Exchange Service (DAAD) for supporting and funding this study. PMK was a Fellow at the Wissenschaftskolleg zu Berlin while writing this manuscript.
This study was financially supported by the German Primate Center in Göttingen Germany, the University of Göttingen (Georg-August-Universität Göttingen) and the German Academic Exchange Service (DAAD).
Availability of data and materials
The data will be made available in a public database (dryad.org) prior to publication.
HR, PMK, CF conceived the study and wrote the manuscript. HR collected and analyzed the data. All authors read and approved the final manuscript.
This study was conducted in accordance with the German and Malagasy (Commission Tripartite CAFF) legal and ethical requirements of appropriate animal procedures. Research protocols and experimental procedures were approved by the Ministry for the Environment, Water and Forests of Madagascar (MINEEF).
Consent for publication
The authors declare that they have no competing interests.
Springer Nature remains neutral with regard to jurisdictional claims in published maps and institutional affiliations.
Open AccessThis article is distributed under the terms of the Creative Commons Attribution 4.0 International License (http://creativecommons.org/licenses/by/4.0/), which permits unrestricted use, distribution, and reproduction in any medium, provided you give appropriate credit to the original author(s) and the source, provide a link to the Creative Commons license, and indicate if changes were made. The Creative Commons Public Domain Dedication waiver (http://creativecommons.org/publicdomain/zero/1.0/) applies to the data made available in this article, unless otherwise stated.
- Ratcliffe LM, Grant PR. Species recognition in Darwin’s finches (Geospiza, Gould) I. Discrimination by morphological cues. Anim Behav. 1983;31(4):1139–53.View ArticleGoogle Scholar
- Fujita K. Species recognition by five macaque monkeys. Primates. 1987;28(3):353–66.View ArticleGoogle Scholar
- Ryan MJ, Rand AS. Species recognition and sexual selection as a unitary problem in animal communication. Evolution. 1993;47:647–57.View ArticlePubMedGoogle Scholar
- Boake CR, DeAngelis MP, Andreadis DK. Is sexual selection and species recognition a continuum? Mating behavior of the stalk-eyed fly Drosophila heteroneura. Proc Natl Acad Sci. 1997;94(23):12442–5.View ArticlePubMedPubMed CentralGoogle Scholar
- Baugh AT, Akre KL, Ryan MJ. Categorical perception of a natural, multivariate signal: mating call recognition in túngara frogs. Proc Natl Acad Sci. 2008;105(26):8985–8.View ArticlePubMedPubMed CentralGoogle Scholar
- Caspers BA, Schroeder FC, Franke S, Streich WJ, Voigt CC. Odour-based species recognition in two sympatric species of sac-winged bats (Saccopteryx bilineata, S. leptura): combining chemical analyses, behavioural observations and odour preference tests. Behav Ecol Sociobiol. 2009;63(5):741–9.View ArticleGoogle Scholar
- Trivers RL. Parental investment and sexual selection. In: Sexual selection & the descent of man. New York: Aldine de Gruyter; 1972. p. 136–79.Google Scholar
- Clutton-Brock TH, Parker GA. Potential reproductive rates and the operation of sexual selection. Q Rev Biol. 1992;67:437–56.View ArticleGoogle Scholar
- Kappeler PM. Mate choice. In: Mitani JC, Call J, Kappeler PM, Palombit RA, Silk JB, editors. The evolution of primate societies. Chicago and London: University of Chicago Press; 2012. p. 343–66.Google Scholar
- McLennan DA, Ryan MJ. Responses to conspecific and heterospecific olfactory cues in the swordtail Xiphophorus cortezi. Anim Behav. 1997;54:1077–88.View ArticlePubMedGoogle Scholar
- Seehausen O, Terai Y, Magalhaes IS, Carleton KL, Mrosso HDJ, Miyagi R, et al. Speciation through sensory drive in cichlid fish. Behav Ecol Sociobiol. 2008;42:1–8.View ArticleGoogle Scholar
- Höbel G, Gerhardt H. Reproductive character displacement in the acoustic communication system of green tree frogs (Hyla cinerea). Evolution. 2003;57(4):894–904.View ArticlePubMedGoogle Scholar
- Boul KE, Funk WC, Darst CR, Cannatella DC, Ryan MJ. Sexual selection drives speciation in an Amazonian frog. Proc R Soc Lond B. 2007;274:399–406.View ArticleGoogle Scholar
- Curé C, Mathevon N, Mundry R, Aubin T. Acoustic cues used for species recognition can differ between sexes and sibling species: evidence in shearwaters. Anim Behav. 2012;84:239–50.View ArticleGoogle Scholar
- Raemaekers JJ, Raemaekers PM. Field playback of loud calls to gibbons (Hylobates lar): territorial, sex-specific and species-specific responses. Anim Behav. 1985;33:481–91.View ArticleGoogle Scholar
- Lank DB, Dale J. Visual signals for individual identification: the silent “song” of ruffs. Auk. 2001;118(3):759–65.Google Scholar
- Tibbetts EA. Complex social behaviour can select for variability in visual features: a case study in Polistes wasps. Proc R Soc B. 2004;271(1551):1955–60.View ArticlePubMedPubMed CentralGoogle Scholar
- Tibbetts EA, Dale J. Individual recognition: it is good to be different. Trends Ecol Evol. 2007;22(10):529–37.View ArticlePubMedGoogle Scholar
- Nahm FK, Perret A, Amaral DG, Albright TD. How do monkeys look at faces? J Cogn Neurosci. 1997;9(5):611–23.View ArticlePubMedGoogle Scholar
- Parr LA, Dove T, Hopkins WD. Why faces may be special: evidence of the inversion effect in chimpanzees. J Cogn Neurosci. 1998;10(5):615–22.View ArticlePubMedGoogle Scholar
- Pascalis O, Bachevalier J. Face recognition in primates: a cross-species study. Behav Process. 1998;43(1):87–96.View ArticleGoogle Scholar
- Parr LA, Winslow JT, Hopkins WD, de Waal FB. Recognizing facial cues: individual discrimination by chimpanzees (Pan troglodytes) and rhesus monkeys (Macaca mulatta). J Comp Psychol. 2000;114(1):47–60.View ArticlePubMedPubMed CentralGoogle Scholar
- Setchell JM, Wickings EJ, Knapp LA. Signal content of red facial coloration in female mandrills (Mandrillus sphinx). Proc R Soc Lond B. 2006;273(1599):2395–400.View ArticleGoogle Scholar
- Bradley BJ, Mundy NI. The primate palette: the evolution of primate coloration. Evol Anthr. 2008;17(2):97–111.View ArticleGoogle Scholar
- Dufour V, Pascalis O, Petit O. Face processing limitation to own species in primates: a comparative study in brown capuchins, Tonkean macaques and humans. Behav Process. 2006;73(1):107–13.View ArticleGoogle Scholar
- Burrows AM. The facial expression musculature in primates and its evolutionary significance. BioEssays. 2008;30(3):212–25.View ArticlePubMedGoogle Scholar
- Santana SE, Alfaro JL, Alfaro ME. Adaptive evolution of facial colour patterns in neotropical primates. Proc R Soc Lond B. 2012;279:2204–11.View ArticleGoogle Scholar
- Santana SE, Alfaro JL, Noonan A, Alfaro ME. Adaptive response to sociality and ecology drives the diversification of facial colour patterns in catarrhines. Nat Commun. 2013;4:1–7.View ArticleGoogle Scholar
- Setchell JM. Do female mandrills prefer brightly colored males? Int J Primatol. 2005;26(4):715–35.View ArticleGoogle Scholar
- Marty JS, Higham JP, Gadsby EL, Ross C. Dominance, coloration, and social and sexual behavior in male drills Mandrillus leucophaeus. Int J Primatol. 2009;30(6):807–23.View ArticleGoogle Scholar
- Gauthier I, Logothetis NK. Is face recognition not so unique after all? Cogn Neurosci. 2000;17(1–3):125–42.Google Scholar
- Bruce C. Face recognition by monkeys: absence of an inversion effect. Neuropsychologia. 1982;20(5):515–21.View ArticlePubMedGoogle Scholar
- Dittrich W. How monkeys see others: discrimination and recognition of monkeys’ shape. Behav Process. 1994;33:139–54.View ArticleGoogle Scholar
- Fujita K, Watanabe K, Widarto TH, Suryobroto B. Discrimination of macaques by macaques: the case of Sulawesi species. Primates. 1997;38(3):233–45.View ArticleGoogle Scholar
- Allen WL, Higham JP. Assessing the potential information content of multicomponent visual signals: a machine learning approach. Proc R Soc Lond B. 2015;282(1802):20142284.Google Scholar
- Parr LA, de Waal FB. Visual kin recognition in chimpanzees. Nature. 1999;399(6737):647–8.View ArticlePubMedGoogle Scholar
- Mittermeier RA, Louis EE Jr, Richardson M, Schwitzer C, Langrand O, Rylands A, et al. Lemurs of Madagascar. 3rd ed. Arlington: Conservation International; 2010.Google Scholar
- Rakotonirina H, Kappeler PM, Fichtel C. Evolution of facial color pattern complexity in lemurs. Sci Rep. 2017;7:15181.View ArticlePubMedPubMed CentralGoogle Scholar
- Marechal L, Genty E, Roeder JJ. Recognition of faces of known individuals in two lemur species (Eulemur fulvus and E. macaco). Anim Behav. 2010;79(5):1157–63.View ArticleGoogle Scholar
- Cooper VJ, Hosey GR. Sexual dichromatism and female preference in Eulemur fulvus subspecies. Int J Primatol. 2003;24(6):1177–88.View ArticleGoogle Scholar
- Harrington JE. Responses of Lemur fulvus to scents of different subspecies of L. fulvus and to scents of different species of Lemuriformes. Z Tierpsychol. 1979;49:1–9.View ArticleGoogle Scholar
- Kappeler PM. The transmission and function of chemical signals in Lemur catta. Behav Ecol Sociobiol. 1998;42:411–21.View ArticleGoogle Scholar
- delBarco-Trillo J, Sacha CR, Dubay GR, Drea CM. Eulemur, me lemur: the evolution of scent-signal complexity in a primate clade. Phil Trans R Soc Lond B Biol Sci. 2012;367:1909–22.View ArticleGoogle Scholar
- Braune P, Schmidt S, Zimmermann E. Acoustic divergence in the communication of cryptic of nocturnal primates (Microcebus spp.). BMC Biol. 2008;6:19.View ArticlePubMedPubMed CentralGoogle Scholar
- Jacobs GH, Deegan JF. Photopigments underlying color vision in ringtail lemurs (Lemur catta) and brown lemurs (Eulemur fulvus). Am J Primatol. 1993;30(3):243–56.View ArticleGoogle Scholar
- Jacobs GH. Primate color vision: a comparative perspective. Vis Neurosci. 2008;25(5–6):619–33.View ArticlePubMedGoogle Scholar
- Tan Y, Li WH. Vision: Trichromatic vision in prosimians. Nature. 1999;402(6757):36.View ArticlePubMedGoogle Scholar
- Baden AL, Morelli TL, Irwin MT, Lawler RR, Pastorini J, Mayor M, et al. Novel opsin gene variation in large-bodied, diurnal lemurs. Biol Lett. 2017;13:20170050.View ArticlePubMedGoogle Scholar
- Peichl L, Kaiser A, Rakotondraparany F, Dubielzig RR, Goodman SM, Kappeler PM. Diversity of photoreceptor arrangements in nocturnal, cathemeral and diurnal Malagasy lemurs. J Comp Neurol. 2017; https://doi.org/10.1002/cne.24167.
- Rumpler Y. The significance of chromosomal studies in the systematics of the Malagasy lemurs. In: Tattersall I, Sussman RW, editors. Lemur Biology. New York: Plenum Press; 1975. p. 25–40.View ArticleGoogle Scholar
- Hamilton AE, Buettner-Janusch J. Chromosomes of Lemuriformes III. The genus Lemur: Karyotypes of species, subspecies, and hybrids. Ann N Y Acad Sci. 1977;293(1):125–59.View ArticlePubMedGoogle Scholar
- Pastorini J, Zaramody A, Curtis DJ, Martin RD, Forstner MRJ. Sympatric hybridisation between Eulemur fulvus and E. mongoz. Folia Primatol. 2001;72:176.Google Scholar
- Delmore KE, Louis EE, Johnson SE. Morphological characterization of a brown lemur hybrid zone (Eulemur rufifrons × E. cinereiceps). Am J Phys Anthropol. 2011;145:55–66.View ArticlePubMedGoogle Scholar
- Johnson SE. Ecology and speciation in brown lemurs: white-collared lemurs (Eulemur albocollaris) and hybrids (Eulemur albocollaris * Eulemur fulvus rufus) in southeastern Madagascar, Ph.D. dissertation. Austin: University of Texas at Austin; 2002.Google Scholar
- Johnson SE. Evolutionary divergence in the brown lemur species complex. In: Gould L, Sauther ML, editors. Lemurs: ecology and adaptation. New York: Springer; 2007. p. 187–210.Google Scholar
- Kappeler PM, Fichtel C. A 15-year perspective on the social organization and life history of sifaka in Kirindy Forest. In: Kappeler PM, Watts DP, editors. Long- term field studies of primates. Berlin Heidelberg: Springer; 2012. p. 101–21.View ArticleGoogle Scholar
- Kappeler PM, Fichtel C. Female reproductive competition in Eulemur rufifrons: eviction and reproductive restraint in a plurally breeding Malagasy primates. Mol Ecol. 2012;23:685–98.View ArticleGoogle Scholar
- Markolf M, Kappeler PM. Phylogeographic analysis of the true lemurs (genus Eulemur) underlines the role of river catchments for the evolution of micro-endemism in Madagascar. Front Zool. 2013;10(1):1.View ArticleGoogle Scholar
- Watanabe K, Matsumura S. The borderlands and possible hybrids between three species of macaques, M. nigra, M. nigrescens, and M. hecki, in the northern peninsula of Sulawesi. Primates. 1991;32(3):365–70.View ArticleGoogle Scholar
- Markolf M, Rakotonirina H, Fichtel C, Grumbkow P, Brameier M, Kappeler PM. True lemurs... True species – species delimitation using multiple data sources in the brown lemur complex. BMC Evol Biol. 2013;13:233.View ArticlePubMedPubMed CentralGoogle Scholar
- Sumner P, Mollon JD. Colors of primate pelage and skin: objective assessment of conspicuousness. Am J Primatol. 2003;59(2):67–91.View ArticlePubMedGoogle Scholar
- Surridge AK, Osorio D, Mundy NI. Evolution and selection of trichromatic vision in primates. Trends Ecol Evol. 2003;18(4):198–205.View ArticleGoogle Scholar
- Ettlinger G, Wilson WA. Cross-modal performance: behavioural processes, phylogenetic considerations and neural mechanisms. Behav Brain Res. 1990;40(3):169–92.View ArticlePubMedGoogle Scholar
- Matyjasiak P. Birds associate species-specific acoustic and visual cues: recognition of heterospecific rivals by male blackcaps. Behav Ecol. 2004;16(2):467–71.View ArticleGoogle Scholar
- Proops L, McComb K. Cross-modal individual recognition in domestic horses (Equus caballus) extends to familiar humans. Proc R Soc Lond B. 2012;279(1741):3131–8.View ArticleGoogle Scholar
- Evans TA, Howell S, Westergaard GC. Auditory-visual cross-modal perception of communicative stimuli in tufted capuchin monkeys (Cebus apella). J Exp Psychol Anim Behav Process. 2005;31(4):399–406.View ArticlePubMedGoogle Scholar
- Sliwa J, Duhamel JR, Pascalis O, Wirth S. Spontaneous voice–face identity matching by rhesus monkeys for familiar conspecifics and humans. Proc Natl Acad Sci U S A. 2011;108(4):1735–40.View ArticlePubMedPubMed CentralGoogle Scholar
- Adachi I, Kuwahata H, Fujita K, Tomonaga M, Matsuzawa T. Japanese macaques form a cross-modal representation of their own species in their first year of life. Primates. 2006;47(4):350–4.View ArticlePubMedGoogle Scholar
- Kulahci IG, Drea CM, Rubenstein DI, Ghazanfar AA. Individual recognition through olfactory–auditory matching in lemurs. Proc R Soc Lond B. 2014;281(1784)Google Scholar
- Schnoell AV, Fichtel C. Wild red-fronted lemurs (Eulemur rufifrons) use social information to learn new foraging techniques. Anim Cogn. 2012;15(4):505–16.View ArticlePubMedPubMed CentralGoogle Scholar
- Kuznetsova A, Brockhoff PB, Christensen RHB. LmerTest: tests for random and fixed effects for linear mixed effect models. R package Version 2.0–3. 2013. https://cran.r-project.org/web/packages/lmerTest/index.html.