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A Review and Interspecific Comparison of Nocturnal and Cathemeral Strepsirhine Primate Olfactory Behavioural Ecology

A Review and Interspecific Comparison of Nocturnal and Cathemeral Strepsirhine Primate Olfactory... Hindawi Publishing Corporation International Journal of Zoology Volume 2011, Article ID 362976, 11 pages doi:10.1155/2011/362976 Review Article A Review and Interspecific Comparison of Nocturnal and Cathemeral Strepsirhine Primate Olfactory Behavioural Ecology Ian C. Colquhoun Department of Anthropology and The Centre for Environment and Sustainability, The University of Western Ontario, London, ON, Canada N6A 5C2 Correspondence should be addressed to Ian C. Colquhoun, colquhou@uwo.ca Received 13 November 2010; Revised 2 February 2011; Accepted 17 March 2011 Academic Editor: Lesley Rogers Copyright © 2011 Ian C. Colquhoun. This is an open access article distributed under the Creative Commons Attribution License, which permits unrestricted use, distribution, and reproduction in any medium, provided the original work is properly cited. This paper provides a comparative review of the known patterns of olfactory behavioural ecology among the nocturnal strepsirhine primates and the cathemeral lemurid genus Eulemur. Endemic to Madagascar, all Eulemur species exhibit both diurnality and nocturnality (i.e., cathemerality), and are gregarious, making them an interesting group of taxa to compare with the nocturnal strepsirhines. This paper represents the first comparative review of patterns of olfactory communication among the nocturnal strepsirhines and the cathemeral Eulemur species. Inductive assessment of these comparative data indicates that olfactory communication serves multiple functions in both groups, including individual recognition, sex recognition, indication of social dominance, and coordination of mating behaviour. However, the urine-washing behaviour characteristic of many nocturnal strepsirhines has no clear homologue among Eulemur species (although the latter may use urine droplets in scent marking). Despite sparse and scattered comparative data, it appears that Eulemur species exhibit different olfactory communication patterns that are associated with differing social organizations in this genus. 1. Introduction lemuriform primate genus Eulemur has received concerning this distinctive activity pattern, (e.g., [5–7], and references In their 2004 paper reviewing comparative data on latrine therein). behaviour among lemur species, Irwin and coauthors [1] Genus Eulemur and all the other lemuriform primates contended that, “... the use of chemical signals in primate native to Madagascar, together with the lorisiform primates communication is well documented.” On this point, they of Africa and Asia, represent a major adaptive radiation cited two fundamental sources: first, Alain Schilling’s 1979 within the Order Primates—the Suborder Strepsirhini. These review paper, “Olfactory Communication in Prosimians” primates retain the ancestral mammalian characteristic of the [2], and second, Gisela Epple’s 1986 review of primate rhinarium (or “wet nose”). Strepsirhine primates include all olfactory behaviour, “Communication by Chemical Signals” the lemur species of Madagascar and the Comoro Islands, the [3]. lorises of south and southeastern Asia, and the pottos and There are two important things to note concerning this galagos (or, bushbabies) of sub-Saharan Africa. In the closing pair of key publications on primate olfactory behaviour. The section section of his 1979 paper, Schilling [2]remarkedon first is that, although it has been 32 and 25 years, respectively, the apparent distinction between the predominantly deferred since these works were published, both continue to be olfactory signals of nocturnal strepsirhines and the combined required reading in the field of primate olfactory commu- direct olfactory and visual signalling of diurnal strepsirhines, nication. The second is that both these publications predate stating, “It would be interesting to study this aspect of the 1987 definition of primate species with both diurnal and olfactory communication in species that are intermediate nocturnal activity patterns as being “cathemeral,” or active between the two types (emphasis added), that is, which are “through the day” (i.e., through the 24-hour daily cycle) greagrious to the extent that they live in family groups, and [4]. This definition ushered in the extensive attention the which are more or less nocturnal, like Hapalemur griseus, 2 International Journal of Zoology Avahi laniger,and Lemur mongoz.” Thus, the present paper the functional role of the VNC has not been fully examined represents the first comparative review of olfactory commu- across these former taxa [21, 30]. nication exhibited by nocturnal strepsirhine primates and The accessory olfactory bulb (AOB) of the accessory the cathemeral Eulemur species. The major aim of this paper olfactory system (AOS) is described as large to very large is to provide an initial assessment of the types and contexts relative to body size in those strepsirhine species that have of olfactory communication of the nocturnal strepsirhines been examined [15]. There is considerable variation in relative to those of the cathemeral genus Eulemur (aswellas AOB size relative to body size in those strepsirhine and the cathemeral lemurid species Hapalemur griseus). platyrrhine species for which there are data [15]. The AOB is described as relatively well developed in platyrrhine species, but the available comparative data also indicate that AOBs in New World monkeys are generally reduced in absolute 2. Strepsirhine Olfactory Biology in size compared to those of strepsirhine species [15]. In those Comparative Perspective Old World monkey species (Cercopithecoidea) studied thus Before comparing patterns of olfactory communication far, the AOS is absent in adults [10, 21, 30]. In the ape amongst nocturnal and cathemeral strepsirhine primates, species (Hominoidea) that have been studied, including it is useful to first consider strepsirhine olfactory biology humans, the AOB is absent in adults [10, 15]. If the VNO is present in hominoid species (again, including humans), in broader primate and mammalian comparative contexts. Relative to many other mammalian orders (e.g., rodents, it appears vestigial in structure and is thought to likely artiodactyls, perissodactyls, carnivores), primates have his- be nonfunctional [10, 13–16, 19, 20, 22–24, 30]. Among the strepsirhines studied to date, nocturnal strepsirhines are torically been regarded as microsmatic [8–10]. But the olfac- tory systems of strepsirhine and haplorhine primates also reported to both have larger AOBs [15], and larger olfactory exhibit considerable differences in the relative proportions bulbs (OBs) [10] than diurnal strepsirhines. Barton and and complexities of their anatomical structures [10–19]. colleagues [12] reported that among nocturnal strepsirhines, Early work in this area produced the proposal that those there is a positive correlation between the proportion of fruit in the overall diet and the relative size of the OB, (see also primate species possessing functional vomeronasal organs (VNOs) might be regarded as relatively macrosmatic while [25]). Haplorhine primates, by contrast, have relatively small those primate species without functional VNOs could be OBs in comparison to most other mammals [19, 26]. There have been several reports noting that olfaction considered microsmatic, (e.g., [8]). Further, these compara- tive anatomical data have also been interpreted as indicating, in primates is relatively under-studied and remains poorly in general, relatively sensitive olfaction among strepsirhines, understood (e.g., [10, 20, 21, 26]). Recently, the view has also tarsiers, and platyrrhines, and less keen olfactory abilities been expressed that interpreting primate olfactory reception among catarrhine primates (i.e., Old World cercopithecoid and processing as being functionally divided between the monkeys and hominoids); these latter taxa are considered main olfactory system (MOS) and the AOS is too simplistic more visually adapted, exhibiting specializations such as [8, 10, 19, 20, 27, 28]. Specifically, the complexity of primate trichromatic vision [8–12, 14, 19–26]. More recently, how- olfaction is not reflected in a functional interpretation that sees the MOS primarily detecting airborne volatile odours ever, this interpretation and classification schema has been discarded due to mounting evidence that there is not a direct from a variety of stimuli in the environment, such as correspondence between the presence or relative sizes of food or predators [19, 27], and the AOS being primarily sensitive to heavy, nonvolatile, fluid-borne chemical stimuli, olfactory structures and olfactory function, (e.g., [10, 19, 27, 28]). such as urine and scent-marks, as well as pheromones, that In terms of comparative anatomy, the extant strepsirhine communicate sociosexual information [10, 19, 27]. Rather, primates (together with the extinct adapoid primates of the the emerging view is that there must be a degree of overlap, Eocene epoch) are considered to have retained the primitive or integration, in the functioning of the MOS and AOS [8, 10, 19, 20, 27, 28]. eutherian mammal “nasal ground plan” [10]. All strepsirhine primates possess the rhinarium, the naked, moist tissue This more nuanced interpretation of primate olfac- surrounding the nostrils, which is also found in many other tion has been pushed ahead by innovative studies that have made novel applications of research techniques. For mammalian taxa but has been lost in all haplorhine pri- mates (i.e., New World monkeys, Old World monkeys, and example, advances in genomic analyses have made possible hominoids [10, 29]). The available comparative anatomical the comparison of olfactory receptor (OR) gene families coding for olfactory receptor proteins (ORPs) in different data for members of the Order Primates indicate that both the VNO and the entire vomeronasal complex (VNC) are primate species and other mammals, (e.g., [9, 11, 18, 19, most fully developed in strepsirhines [13, 14, 30], and likely 23, 24, 28]). Advances have also been realized in several play critical roles in discrimination among chemical classes recent studies of primate olfaction through the use of gas of odourants [19] and in pheromonal communication [20]. chromatography-mass spectrometry (GC-MS) to identify both the volatile components of the glandular secretions The available anatomical data on species in the haplorhine infraorders Tarsiiformes (tarsiers) and Platyrrhini (New used in scent marking, (e.g., [31–34]), and the chemical World, or platyrrhine, monkeys) indicate that these taxa composition of urine [35]. Notably, genetic studies have provided new insights also possess VNCs that are “structurally comparable” [30] to those found in strepsirhines [10, 14, 17, 18, 30]; however, into primate olfactory function. Although testing across the International Journal of Zoology 3 Order Primates has not been exhaustive to this point, the olfactory behavioural ecology. This relates to the general V1R and V2R olfactory receptor (OR) gene families and the point raised repeatedly in the literature that research into TRP2 gene (which is crucial for pheromone signal transduc- primate olfaction lags far behind that on primate visual and tion in the VNO) have been examined across several primate vocal systems, for example, [10, 20, 21, 26]. For example, genera. These preliminary assessments of the genetics of the comments of Rowell [46] over 30 years ago remain olfaction have shown that catarrhine primates, with their surprisingly current: “Prosimians are smelly animals... ol- trichromatic vision, exhibit a significantly higher proportion factory communication occurs both at a distance and in of nonfunctional OR pseudogenes than do either platyrrhine body contact, but monitoring the “conversation” presents monkeys or strepsirhines [9, 11, 18, 19, 23, 24]. An exception difficulties for our olfactorily unsophisticated species and to this taxonomic pattern is the platyrrhine genus Alouatta, proceeds slowly.” Over the last decade, for every peer- the howler monkeys, which have evolved trichromatic vision reviewed paper dealing with primate olfaction, 115 dealing via convergent evolution and exhibit a level of OR pseudo- with primate vision have been published (e.g., see the genization similar to that among catarrhine taxa [11]. Yet, PrimateLit database: http://primatelit.library.wisc.edu;see this does not mean that cercopithecoids and hominoids (or also [26]). From this, we can appreciate why Heymann [26] Alouatta, for that matter) do not use, or respond to, olfactory concluded that, “Thus, it is appropriate to consider olfaction communication [19, 29, 36]. Despite lacking the AOS as as a sense that is still neglected in the study of nonhuman adults, some cercopithecoid monkeys do exhibit scent- primates.’’ marking behaviour (e.g., [37, 38]). Although scent-marking All this is by way of pointing out that the present, and any behaviour has not been recorded among hominoid taxa other, comparative review of olfactory behavioural ecology [10, 39, 40], available comparative data show that specialized across strepsirhine primate species must rely on a body of cutaneous scent glands, such as the axillary apocrine glands, information that is fragmentary and scattered. Thus, this are known in all hominoid genera [10, 39, 40]; this provides review must be regarded as entirely preliminary. Recent tax- a likely channel for interindividual olfactory communication onomies recognize at least 26 lorisiform strepsirhine species and individual recognition in hominoids, including humans [27, 39–42]. Similarly, recent GC-MS analyses of the volatile (i.e., the lorises, pottos, and galagos, or bushbabies; see [47]) components in mandrill (Mandrillus sphinx)scent marks while the number of recognized lemuriform strepsirhine indicated that, despite the mandrill apparently lacking a species endemic to Madagascar approaches 100 and is still functional AOS, individual odour profiles convey informa- climbing [48–50]. For most of these lorisiform and lemuri- tion about the signaller, including age, sex, dominance rank form taxa, however, there is no information available on the of adult males, and perhaps identity of the signaller [43]. behavioural ecology of their olfactory communication. Additionally, odour similarity between signaller and receiver is related to major histocompatibility (MHC) concordance, and represents a potential mechanism for mate selection by females in favour of MHC-diverse males [44]. These 3. Nocturnal and Cathemeral Strepsirhines: new insights into olfactory communication in a catarrhine Comparative Data primate seem to provide an example of the suggestion that, even without functional AOSs or VNOs, catarrhines In order to review the literature relating to strepsirhine can still detect and respond to sociosexual odour cues and primate olfactory behavioural ecology as completely as pheromonal stimuli through ORPs that are expressed in the possible, and given the scant literature that deals explicitly main olfactory epithelium [10, 19, 20, 22, 27, 28]. with primate olfaction (see above), it was also necessary to So, while we have an emerging picture of humans and consult reports, on strepsirhine primate species, that have other catarrhine primates being capable of responding to dealt primarily with other topics (such as social organization, an array of odour cues, including chemosensory responses social behaviour, ranging ecology, etc.), and glean whatever to volatile components of some odours [10, 19, 20, 27, material could be found concerning olfactory communi- 28, 43, 44], the available comparative data on strepsirhine cation. This entailed having to pull information from a primates (where we find species that exhibit retention sentence here or an anecdote there, in a literature that is very of the rhinarium, well-developed AOSs, relatively large scattered (relevant material was found in publications that AOBs, functional VNOs, intact OR gene families coding focused on primatology, anthropology, behaviour, chemical for functional ORPs, plus functional integration of the ecology, mammalogy, and zoology). This simply underscores AOSs and the MOSs), indicate that strepsirhine primate the fact that the behavioural ecology of strepsirhine primate taxa experience considerable complexity in their olfactory olfaction and olfactory behaviour remains both a poorly communication [10, 19, 20, 28, 35]. The important role of researched and poorly understood dimension of the overall scent marking and olfactory communication in strepsirhine behavioural ecology of these taxa. It also points to this area behavioural ecology, particularly in regard to reproductive being an extremely fertile and promising area for future behaviour, has been recognized for decades, (e.g., [45]). Yet, research on the behavioural ecology of strepsirhine primates despite this, and despite important comparative works like (moreover, the same applies to the study of primate olfactory those by Schilling [2] and Epple [3], it is surprising how little-studied strepsirhine olfactory communication remains behavioural ecology in general, as several recent publications and how little we know with certainty about strepsirhine reflect, e.g., [20, 26–28, 42, 43, 51]). 4 International Journal of Zoology 3.1. Nocturnal Lemuriforms are totally arboreal, patterns of defecation produce terrestrial latrines that seem to be linked to resource defence [1–3, 68]. 3.1.1. Genus Microcebus: The Mouse Lemurs. Microcebus mu- rinus, the gray mouse lemur, is the lemuriform species for 3.1.6. Genus Daubentonia: The Aye-Aye. Both sexes exhibit which the accessory olfactory system (AOS), including the vomeronasal organ, has most fully been investigated [52]. anogenital scent marking [2, 69], and female anogenital scent marking increases during estrus [70]. Aye-ayes also engage in In M. murinus, male-male, male-female, and female-female urine trail marking [2, 71, 72]. socio-sexual interactions are mediated and coordinated by urinary chemosensory cues [53–55]. Studies of M. murinus in captivity have shown that male urinary marking behaviour 3.1.7. Genus Avahi: The Woolly Lemurs. The woolly lemurs decreases with age [56, 57]. The suite of scent-marking are not at all well-studied; there is a dearth of research on behaviours known for the gray mouse lemur includes punc- their behavioural ecology. I could not find any published tuated urine marking (sometimes with “perineal wiping”), information on the olfactory behavioural ecology of Avahi. head rubbing and muzzle or lip wiping, branch chewing with salivary deposition, and, especially, “urine washing” (where individuals purposefully urinate on their hands and feet), 3.2. The Lorisiformes. All taxa that have been studied in this which accounts for over 80% of all scent-marking behaviours nocturnal primate infraorder (that is, the lorises, pottos, performed [2, 3, 58–61]. In a recent field study of the and galagos, or bushbabies) scent mark extensively with golden brown mouse lemur (M. ravelobensis), Braune and urine [58], and urine marking is much more frequent colleagues [62] recognized two forms of scent marking: urine than glandular scent marking. Together with the lorisine washing, and mouth wiping (sometimes with face and/or genus Loris, all galagine primates studied to date (except head rubbing). the galago genus Euoticus) exhibit both urine washing and punctuated urine marking (or “rhythmic micturition”) [73– 76]. Urine washing can occur in a variety of contexts, 3.1.2. Genus Mirza: The “Giant” Mouse Lemurs. Olfactory including mobbing behaviour, moving into an unfamiliar communication among Mirza during reproductive behav- area, during agonistic and aggressive encounters, and, in iour includes nasonasal, nasobody and nasogenital con- social interactions, especially when a female is in estrus [76– tact [63]. Both punctuated urine marking and urine trail 78]. Greater galagos (Otolemur crassicaudatus)havebeen marking occur, and experimental work indicates males can shown experimentally to differentiate scent marks by sex discriminate among the urine marks of conspecifics [3, 58]. and by individual [78, 79]. Allen’s galago (Sciurocheirus Both males and females anogenital scent mark, and, like alleni) shows high frequencies of urine marking in territorial Microcebus, Mirza also engages in salivary marking [59]. boundary zones [80]. Scent marking seems also to function Notably, Mirza would also appear to exhibit flehmen (see as a stress-reducing mechanism in the small-eared bushbaby photo Figure 8 in [59]—the caption reads, “The typical (Otolemur garnettii)[81]. Urine washing in Loris, the slender posture for smelling a mark of a conspecific; note the open loris, has been reported to often occur in the context of mouth, and retracted tongue,” emphasis added; cf. [64]). consuming noxious insect prey, both before catching the prey and after consuming the prey; urine washing would also 3.1.3. Genus Cheirogaleus: The Dwarf Lemurs. Data on olfac- occur if a loris was stung by an insect [82]. Loris females have tory communication are available for the greater dwarf lemur also been observed to urine wash before they groom their (Cheirogaleus major) and the fat-tailed dwarf lemur (C. infants—this has been proposed to possibly have an anti- medius). Both species exhibit punctuated urine marking and predator function when females “park” their infants while urine trail marking, as well as anogenital scent marking they forage (i.e., the possible anti-predator function of a [2, 58], but the dwarf lemurs are notable for their specialized female urine washing and then grooming her infant could be fecal marking of branches [2, 65], which Irwin and colleagues either that it provides an olfactory screen or barrier against [1] identify as arboreal latrine behaviour. Dwarf lemur fecal potential predators, or that it acts as a form of predator marking may be related to territorial advertisement. mimicry while the infant is “parked”) [82]. All lorisine primates studied thus far exhibit urine trail marking in addition to punctuated urine marking [2, 58, 3.1.4. Genus Phaner: The fork-Marked Lemurs. Phaner stands 76, 83]. In Loris, inter-sexual social interactions often see out amongst the nocturnal lemuriforms because of the males either sniffing the muzzle or anogenital region of apparent absence of any form of urine marking in this genus females [82, 84]. During allogrooming bouts, Loris males [2, 66]. Males may rarely scent mark branches with their and females will lick and rub a specialized brachial gland on throat gland [67]; more often, males use their throat gland their own face and body and on the body of the grooming to scent mark females during allogrooming bouts [66]. partner [82]. Perodicticus, the potto, exhibits “genital scratch grooming” during which grooming partners of both sexes 3.1.5. Genus Lepilemur: The Sportive Lemurs. Like most scent mark each other—this behaviour is not linked to repro- other nocturnal strepsirhines studied to date, sportive lemurs duction [85]. In Perodicticus, urine marking may accompany exhibit urine marking [2, 3, 58]. Only males are reported allogrooming [86]. During allogrooming, pottos also mark to anogenital scent mark [1–3]. Although Lepilemur species each other with saliva and genital secretions [87]. Arctocebus, International Journal of Zoology 5 Table 1: Comparative interspecific profiles of scent marking behaviours among nocturnal strepsirhine genera (i.e., lemuriforms, galagines, and lorisines) and the cathemeral lemurid genera Eulemur and Hapalemur, as derived from the published literature on these taxa [1–3, 52– 112]. Scent-marking behaviours: 1, urine washing; 2, punctuated urine marking; 3, urine-trail marking; 4, muzzle wipe/branch chewing (saliva deposition); 5, flehmen; 6, fecal marking; 7, latrine behaviour; 8, anogenital scent marking; 9, head marking (males). Scent-marking behaviours Strepsirhine taxon (refs) 1 2 3 4567 8 9 Nocturnal lemuriforms Microcebus [2, 3, 52–62]] + + − +? −− − + Mirza [3, 58, 59, 63, 64] − ++ + + −− ? (Both sexes) Cheirogaleus [1, 2, 58, 65] − ++ ? ? + − +? Phaner [2, 6, 66, 67] − ?? ? ? −− − (?) (Male throat gland) Lepilemur [1–3, 58, 68] − + − ?? − + ? (Males) Daubentonia − ?+ ? ? −− + − [2, 68, 69, 71, 72] Avahi (no refs.) − (?) ? ? ? ? − (?) − (?) +(?) ? Galagines [58, 73–83] Galagoides ++ − ?? −− ?? Galago ++ − ?? −− ?? Euoticus −−− ?? −− ?? Sciurocheirus ++ − ?? −− ?? Otolemur ++ − ?? −− +? Lorisines [2, 58, 76, 82, 84–89] Loris +++ ? + −− + − Nycticebus − ++ ? ? −− ? − Perodicticus − ++ ? + −− + − Arctocebus − ++ ? ? −− − + = “passing over” Cathemeral lemuriforms [1–3, 90–113] Eulemur − + − ++ −− ++ Hapalemur − + − +? − ++ − the golden potto, exhibits distinctive “passing over” scent- marks. Males countermark the urine marks of other males marking behaviour, where the male straddles the female and with significant amounts of urine. In this species, estrus scent-marks her dorsum [85]. “Passing over” has also been females appear to prefer countermarking males [88], and males whose scent-mark odours are already familiar to them observed in Loris and Perodicticus [82]. Flehmen behaviour [89]. has recently been described in these two genera [82]; in Loris, it followed the licking of a urine mark while in Perodicticus it followed a male sniffing a substrate in a female’s home range 3.3. The Cathemeral Lemurids. Comparative data on the [82]. Nycticebus, the slow loris, apparently possesses a “fear olfactory communication of cathemeral lemurids, a good scent” (an “Angstgeruch”), and this has also been suggested deal of it from field research reported since 1990, reveals both for Perodicticus and Arctocebus (especially in the context broad similarities with nocturnal strepsirhines (see Table 1; of mother-infant alarm communication [86]); similarly, [1–3, 52–113]), as well as interesting, and unforeseen, Loris has been suggested to have an anti-predator “alarm distinctions among the cathemeral lemurids themselves (see pheromone” [82]. Male pygmy slow lorises (N. pygmaeus) Table 2;[1–3, 90–113]). In addition to anogenital scent- countermark, with urine, on both male and female urine marking, most cathemeral lemurid species also make use 6 International Journal of Zoology Table 2: Comparative interspecific profiles of scent marking behaviours among lemurid species of the genera Eulemur and Hapalemur,as derived from the published literature on these taxa [1–3, 90–113]. Thepatternsseeninthe twopair-bonded Eulemur species, E. mongoz and E. rubriventer, are very similar to each other, and contrast in significant ways to the patterns exhibited amongst the Eulemur taxa that occur in multimale, multifemale social groups (i.e., the E. fulvus group of taxa, E. macaco,and E. coronatus). Scent-marking E. fulvus group E. macaco E. coronatus E. mongoz E. rubriventer Hapalemur behaviours Anogenital scent-mark +++ ++ + surfaces Urine mark + + + + ? + Teeth grinding Bite mark (saliva during + + + Cheek rubbing + deposition) males inter-group encounters Anogenital mark M→FM→ F Conspecifics M→FM→FM→ F M→ F F→MF→ M HeadMarking(males) +++ ++ − Hand/palmarmarking Antebrachial +++ ++ (males) gland marking Anogenital sniff (M→F) +++ ++ + Mmarks tail with Observed in Observed in antebrachial Self-marking −− − captivity captivity glands to “stink fight” other Ms Variable.Vocal & Marking during Vocal and visual Vocal & visual ++ visual displays; inter-group encounters displays displays (Incl. F (Both substrate some marking overmarking of and self-marking) M anogen marks) Flehmen ? ?? ? ? (pers. obs.) Latrine behaviour −−− −− + of punctuated urine marking (deposited concurrently with in this process is unclear. In both of these pair-bonded the anogenital scent mark—cf. [35], where lemurids, includ- Eulemur species, anogenital scent marking of conspecifics of ing several Eulemur taxa, are characterized as “nonurine the opposite sex is performed by both sexes, rather than only marking” species). I could not find any report, however, males anogenitally scent marking females (a pattern seen in of punctuated urine marking in Eulemur rubriventer, the the multi-male, multi-female group-living Eulemur species). red-bellied lemur (also, Tecot, personal communication). Scent marking also figures prominently during intergroup Urine washing has never been reported in any cathemeral encounters with conspecific groups in both E. mongoz and E. strepsirhine. Head marking by males occurs across the entire rubriventer, including females overmarking male anogenital genus Eulemur. marks in E. rubriventer [93, 94]. These differential patterns of Notably, the mongoose lemur (E. mongoz) and the red- scent-marking behaviour were only uncovered as emergent bellied lemur (E. rubriventer), which are both pair-bonded patterns because of this comparative review of olfactory and territorial species, share similar patterns of olfactory communication in the genus Eulemur and other strepsirhine communication [90–94]. These two Eulemur species con- primates. trast in their patterns of scent-marking behaviour vis-a-v ` is In contrast to mongoose and red-bellied lemurs (i.e., the their congeners that exhibit multi-male, multi-female social two Eulemur species that exhibit pair bonding), there is a organization: the crowned lemur (E. coronatus)[95, 96], the tendency among the crowned, black, and brown lemurs (i.e., black lemurs (E. macaco and E. flavifrons)[97–101], and the Eulemur taxa that exhibit multi-male, multi-female social the brown lemur taxa (E. fulvus, E. rufus, E. sanfordi, E. groups), to engage in vigorous visual and vocal intergroup albifrons, E. rufifrons, E. collaris,and E. cinereiceps)[102– displays rather than intergroup displays involving concerted 109]. I could not find any report of male “bite marking” scent marking. In captivity, however, adjacently housed (a behaviour in which a male chews a branch and deposits groups of brown lemurs have been observed to exhibit a salivary mark) in either mongoose or red-bellied lemurs. scent marking in addition to the aforementioned visual and Although male bite marking has not been reported in these vocal inter-group displays. Self-marking has been reported twospecies,malemongooselemurshavebeenobservedto in captive brown lemurs (E. fulvus)[2], and the gray gentle cheek rub branches [91]; whether or not saliva is deposited lemur Hapalemur griseus [113]. Male Hapalemur griseus rub International Journal of Zoology 7 their antebrachial glands on their tail in advance of facing and differences among strepsirhine primate species in their off against other males in tail-waving “stink fights”; these chemosensory biology and olfactory communication can are similar in nature to the “stink fight” displays of male be expected from future studies that link odour, genetics, ring-tailed lemurs (Lemur catta)[44]. I have observed a behaviour, and ecology [20, 26, 35, 50, 114]. captivemaleblack lemur(E. macaco) self-mark by repeatedly making palmar markings over his tail. Flehmen behaviour Acknowledgments has been reported in the diurnal L. catta ([64]; personal observation). I have also observed a wild male black lemur A brief version of this paper was presented in the Symposium (E. macaco) exhibit flehmen during the breeding season— on “Olfactory Communication in Nocturnal and Cathemeral once when he exhibited the characteristic facial grimace Primates” held during the XXII Congress of the International associated with flehmen after actively sniffing the air, and a Primatological Society in Edinburgh, Scotland, August 3– second time after the same male sniffed a tree branch while 8, 2008. The author thanks to Dr. Sharon Gursky for the in proximity to a juvenile male from another social group invitation to participate in that symposium and for encour- [100]. The latrine behaviour reported in Hapalemur [1]is agement in the first place to undertake this comparative look unique among the cathemeral lemurids. at the behavioural ecology of olfactory communication in nocturnal and cathemeral strepsirhines. Comments provided by two anonymous reviewers and Dr. Lesley Rogers, editor 4. Conclusions of the paper, were most useful and helped to improve earlier drafts of the paper. The paper was also improved In broad terms, cathemeral lemurids exhibit many forms of by detailed comments that were kindly provided by Dr. olfactory communication that are the same as, or similar Susan Muir. Heartfelt thanks must go to Caleigh Farrell, the to, those seen in nocturnal strepsirhine species, including author’s student research assistant, for the untold hours and punctuated urine marking, anogenital scent marking of boundless energy she devoted to helping him track down the conspecifics, male overmarking of female scent marks, and, relevant sources in a very scattered literature. This paper is in the two pair-bonded Eulemur species, scent marking in dedicated to the late Dr. Shelley Saunders. territorial boundary zones. 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A Review and Interspecific Comparison of Nocturnal and Cathemeral Strepsirhine Primate Olfactory Behavioural Ecology

International Journal of Zoology , Volume 2011 – Jul 7, 2011

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Copyright © 2011 Ian C. Colquhoun. This is an open access article distributed under the Creative Commons Attribution License, which permits unrestricted use, distribution, and reproduction in any medium, provided the original work is properly cited.
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Hindawi Publishing Corporation International Journal of Zoology Volume 2011, Article ID 362976, 11 pages doi:10.1155/2011/362976 Review Article A Review and Interspecific Comparison of Nocturnal and Cathemeral Strepsirhine Primate Olfactory Behavioural Ecology Ian C. Colquhoun Department of Anthropology and The Centre for Environment and Sustainability, The University of Western Ontario, London, ON, Canada N6A 5C2 Correspondence should be addressed to Ian C. Colquhoun, colquhou@uwo.ca Received 13 November 2010; Revised 2 February 2011; Accepted 17 March 2011 Academic Editor: Lesley Rogers Copyright © 2011 Ian C. Colquhoun. This is an open access article distributed under the Creative Commons Attribution License, which permits unrestricted use, distribution, and reproduction in any medium, provided the original work is properly cited. This paper provides a comparative review of the known patterns of olfactory behavioural ecology among the nocturnal strepsirhine primates and the cathemeral lemurid genus Eulemur. Endemic to Madagascar, all Eulemur species exhibit both diurnality and nocturnality (i.e., cathemerality), and are gregarious, making them an interesting group of taxa to compare with the nocturnal strepsirhines. This paper represents the first comparative review of patterns of olfactory communication among the nocturnal strepsirhines and the cathemeral Eulemur species. Inductive assessment of these comparative data indicates that olfactory communication serves multiple functions in both groups, including individual recognition, sex recognition, indication of social dominance, and coordination of mating behaviour. However, the urine-washing behaviour characteristic of many nocturnal strepsirhines has no clear homologue among Eulemur species (although the latter may use urine droplets in scent marking). Despite sparse and scattered comparative data, it appears that Eulemur species exhibit different olfactory communication patterns that are associated with differing social organizations in this genus. 1. Introduction lemuriform primate genus Eulemur has received concerning this distinctive activity pattern, (e.g., [5–7], and references In their 2004 paper reviewing comparative data on latrine therein). behaviour among lemur species, Irwin and coauthors [1] Genus Eulemur and all the other lemuriform primates contended that, “... the use of chemical signals in primate native to Madagascar, together with the lorisiform primates communication is well documented.” On this point, they of Africa and Asia, represent a major adaptive radiation cited two fundamental sources: first, Alain Schilling’s 1979 within the Order Primates—the Suborder Strepsirhini. These review paper, “Olfactory Communication in Prosimians” primates retain the ancestral mammalian characteristic of the [2], and second, Gisela Epple’s 1986 review of primate rhinarium (or “wet nose”). Strepsirhine primates include all olfactory behaviour, “Communication by Chemical Signals” the lemur species of Madagascar and the Comoro Islands, the [3]. lorises of south and southeastern Asia, and the pottos and There are two important things to note concerning this galagos (or, bushbabies) of sub-Saharan Africa. In the closing pair of key publications on primate olfactory behaviour. The section section of his 1979 paper, Schilling [2]remarkedon first is that, although it has been 32 and 25 years, respectively, the apparent distinction between the predominantly deferred since these works were published, both continue to be olfactory signals of nocturnal strepsirhines and the combined required reading in the field of primate olfactory commu- direct olfactory and visual signalling of diurnal strepsirhines, nication. The second is that both these publications predate stating, “It would be interesting to study this aspect of the 1987 definition of primate species with both diurnal and olfactory communication in species that are intermediate nocturnal activity patterns as being “cathemeral,” or active between the two types (emphasis added), that is, which are “through the day” (i.e., through the 24-hour daily cycle) greagrious to the extent that they live in family groups, and [4]. This definition ushered in the extensive attention the which are more or less nocturnal, like Hapalemur griseus, 2 International Journal of Zoology Avahi laniger,and Lemur mongoz.” Thus, the present paper the functional role of the VNC has not been fully examined represents the first comparative review of olfactory commu- across these former taxa [21, 30]. nication exhibited by nocturnal strepsirhine primates and The accessory olfactory bulb (AOB) of the accessory the cathemeral Eulemur species. The major aim of this paper olfactory system (AOS) is described as large to very large is to provide an initial assessment of the types and contexts relative to body size in those strepsirhine species that have of olfactory communication of the nocturnal strepsirhines been examined [15]. There is considerable variation in relative to those of the cathemeral genus Eulemur (aswellas AOB size relative to body size in those strepsirhine and the cathemeral lemurid species Hapalemur griseus). platyrrhine species for which there are data [15]. The AOB is described as relatively well developed in platyrrhine species, but the available comparative data also indicate that AOBs in New World monkeys are generally reduced in absolute 2. Strepsirhine Olfactory Biology in size compared to those of strepsirhine species [15]. In those Comparative Perspective Old World monkey species (Cercopithecoidea) studied thus Before comparing patterns of olfactory communication far, the AOS is absent in adults [10, 21, 30]. In the ape amongst nocturnal and cathemeral strepsirhine primates, species (Hominoidea) that have been studied, including it is useful to first consider strepsirhine olfactory biology humans, the AOB is absent in adults [10, 15]. If the VNO is present in hominoid species (again, including humans), in broader primate and mammalian comparative contexts. Relative to many other mammalian orders (e.g., rodents, it appears vestigial in structure and is thought to likely artiodactyls, perissodactyls, carnivores), primates have his- be nonfunctional [10, 13–16, 19, 20, 22–24, 30]. Among the strepsirhines studied to date, nocturnal strepsirhines are torically been regarded as microsmatic [8–10]. But the olfac- tory systems of strepsirhine and haplorhine primates also reported to both have larger AOBs [15], and larger olfactory exhibit considerable differences in the relative proportions bulbs (OBs) [10] than diurnal strepsirhines. Barton and and complexities of their anatomical structures [10–19]. colleagues [12] reported that among nocturnal strepsirhines, Early work in this area produced the proposal that those there is a positive correlation between the proportion of fruit in the overall diet and the relative size of the OB, (see also primate species possessing functional vomeronasal organs (VNOs) might be regarded as relatively macrosmatic while [25]). Haplorhine primates, by contrast, have relatively small those primate species without functional VNOs could be OBs in comparison to most other mammals [19, 26]. There have been several reports noting that olfaction considered microsmatic, (e.g., [8]). Further, these compara- tive anatomical data have also been interpreted as indicating, in primates is relatively under-studied and remains poorly in general, relatively sensitive olfaction among strepsirhines, understood (e.g., [10, 20, 21, 26]). Recently, the view has also tarsiers, and platyrrhines, and less keen olfactory abilities been expressed that interpreting primate olfactory reception among catarrhine primates (i.e., Old World cercopithecoid and processing as being functionally divided between the monkeys and hominoids); these latter taxa are considered main olfactory system (MOS) and the AOS is too simplistic more visually adapted, exhibiting specializations such as [8, 10, 19, 20, 27, 28]. Specifically, the complexity of primate trichromatic vision [8–12, 14, 19–26]. More recently, how- olfaction is not reflected in a functional interpretation that sees the MOS primarily detecting airborne volatile odours ever, this interpretation and classification schema has been discarded due to mounting evidence that there is not a direct from a variety of stimuli in the environment, such as correspondence between the presence or relative sizes of food or predators [19, 27], and the AOS being primarily sensitive to heavy, nonvolatile, fluid-borne chemical stimuli, olfactory structures and olfactory function, (e.g., [10, 19, 27, 28]). such as urine and scent-marks, as well as pheromones, that In terms of comparative anatomy, the extant strepsirhine communicate sociosexual information [10, 19, 27]. Rather, primates (together with the extinct adapoid primates of the the emerging view is that there must be a degree of overlap, Eocene epoch) are considered to have retained the primitive or integration, in the functioning of the MOS and AOS [8, 10, 19, 20, 27, 28]. eutherian mammal “nasal ground plan” [10]. All strepsirhine primates possess the rhinarium, the naked, moist tissue This more nuanced interpretation of primate olfac- surrounding the nostrils, which is also found in many other tion has been pushed ahead by innovative studies that have made novel applications of research techniques. For mammalian taxa but has been lost in all haplorhine pri- mates (i.e., New World monkeys, Old World monkeys, and example, advances in genomic analyses have made possible hominoids [10, 29]). The available comparative anatomical the comparison of olfactory receptor (OR) gene families coding for olfactory receptor proteins (ORPs) in different data for members of the Order Primates indicate that both the VNO and the entire vomeronasal complex (VNC) are primate species and other mammals, (e.g., [9, 11, 18, 19, most fully developed in strepsirhines [13, 14, 30], and likely 23, 24, 28]). Advances have also been realized in several play critical roles in discrimination among chemical classes recent studies of primate olfaction through the use of gas of odourants [19] and in pheromonal communication [20]. chromatography-mass spectrometry (GC-MS) to identify both the volatile components of the glandular secretions The available anatomical data on species in the haplorhine infraorders Tarsiiformes (tarsiers) and Platyrrhini (New used in scent marking, (e.g., [31–34]), and the chemical World, or platyrrhine, monkeys) indicate that these taxa composition of urine [35]. Notably, genetic studies have provided new insights also possess VNCs that are “structurally comparable” [30] to those found in strepsirhines [10, 14, 17, 18, 30]; however, into primate olfactory function. Although testing across the International Journal of Zoology 3 Order Primates has not been exhaustive to this point, the olfactory behavioural ecology. This relates to the general V1R and V2R olfactory receptor (OR) gene families and the point raised repeatedly in the literature that research into TRP2 gene (which is crucial for pheromone signal transduc- primate olfaction lags far behind that on primate visual and tion in the VNO) have been examined across several primate vocal systems, for example, [10, 20, 21, 26]. For example, genera. These preliminary assessments of the genetics of the comments of Rowell [46] over 30 years ago remain olfaction have shown that catarrhine primates, with their surprisingly current: “Prosimians are smelly animals... ol- trichromatic vision, exhibit a significantly higher proportion factory communication occurs both at a distance and in of nonfunctional OR pseudogenes than do either platyrrhine body contact, but monitoring the “conversation” presents monkeys or strepsirhines [9, 11, 18, 19, 23, 24]. An exception difficulties for our olfactorily unsophisticated species and to this taxonomic pattern is the platyrrhine genus Alouatta, proceeds slowly.” Over the last decade, for every peer- the howler monkeys, which have evolved trichromatic vision reviewed paper dealing with primate olfaction, 115 dealing via convergent evolution and exhibit a level of OR pseudo- with primate vision have been published (e.g., see the genization similar to that among catarrhine taxa [11]. Yet, PrimateLit database: http://primatelit.library.wisc.edu;see this does not mean that cercopithecoids and hominoids (or also [26]). From this, we can appreciate why Heymann [26] Alouatta, for that matter) do not use, or respond to, olfactory concluded that, “Thus, it is appropriate to consider olfaction communication [19, 29, 36]. Despite lacking the AOS as as a sense that is still neglected in the study of nonhuman adults, some cercopithecoid monkeys do exhibit scent- primates.’’ marking behaviour (e.g., [37, 38]). Although scent-marking All this is by way of pointing out that the present, and any behaviour has not been recorded among hominoid taxa other, comparative review of olfactory behavioural ecology [10, 39, 40], available comparative data show that specialized across strepsirhine primate species must rely on a body of cutaneous scent glands, such as the axillary apocrine glands, information that is fragmentary and scattered. Thus, this are known in all hominoid genera [10, 39, 40]; this provides review must be regarded as entirely preliminary. Recent tax- a likely channel for interindividual olfactory communication onomies recognize at least 26 lorisiform strepsirhine species and individual recognition in hominoids, including humans [27, 39–42]. Similarly, recent GC-MS analyses of the volatile (i.e., the lorises, pottos, and galagos, or bushbabies; see [47]) components in mandrill (Mandrillus sphinx)scent marks while the number of recognized lemuriform strepsirhine indicated that, despite the mandrill apparently lacking a species endemic to Madagascar approaches 100 and is still functional AOS, individual odour profiles convey informa- climbing [48–50]. For most of these lorisiform and lemuri- tion about the signaller, including age, sex, dominance rank form taxa, however, there is no information available on the of adult males, and perhaps identity of the signaller [43]. behavioural ecology of their olfactory communication. Additionally, odour similarity between signaller and receiver is related to major histocompatibility (MHC) concordance, and represents a potential mechanism for mate selection by females in favour of MHC-diverse males [44]. These 3. Nocturnal and Cathemeral Strepsirhines: new insights into olfactory communication in a catarrhine Comparative Data primate seem to provide an example of the suggestion that, even without functional AOSs or VNOs, catarrhines In order to review the literature relating to strepsirhine can still detect and respond to sociosexual odour cues and primate olfactory behavioural ecology as completely as pheromonal stimuli through ORPs that are expressed in the possible, and given the scant literature that deals explicitly main olfactory epithelium [10, 19, 20, 22, 27, 28]. with primate olfaction (see above), it was also necessary to So, while we have an emerging picture of humans and consult reports, on strepsirhine primate species, that have other catarrhine primates being capable of responding to dealt primarily with other topics (such as social organization, an array of odour cues, including chemosensory responses social behaviour, ranging ecology, etc.), and glean whatever to volatile components of some odours [10, 19, 20, 27, material could be found concerning olfactory communi- 28, 43, 44], the available comparative data on strepsirhine cation. This entailed having to pull information from a primates (where we find species that exhibit retention sentence here or an anecdote there, in a literature that is very of the rhinarium, well-developed AOSs, relatively large scattered (relevant material was found in publications that AOBs, functional VNOs, intact OR gene families coding focused on primatology, anthropology, behaviour, chemical for functional ORPs, plus functional integration of the ecology, mammalogy, and zoology). This simply underscores AOSs and the MOSs), indicate that strepsirhine primate the fact that the behavioural ecology of strepsirhine primate taxa experience considerable complexity in their olfactory olfaction and olfactory behaviour remains both a poorly communication [10, 19, 20, 28, 35]. The important role of researched and poorly understood dimension of the overall scent marking and olfactory communication in strepsirhine behavioural ecology of these taxa. It also points to this area behavioural ecology, particularly in regard to reproductive being an extremely fertile and promising area for future behaviour, has been recognized for decades, (e.g., [45]). Yet, research on the behavioural ecology of strepsirhine primates despite this, and despite important comparative works like (moreover, the same applies to the study of primate olfactory those by Schilling [2] and Epple [3], it is surprising how little-studied strepsirhine olfactory communication remains behavioural ecology in general, as several recent publications and how little we know with certainty about strepsirhine reflect, e.g., [20, 26–28, 42, 43, 51]). 4 International Journal of Zoology 3.1. Nocturnal Lemuriforms are totally arboreal, patterns of defecation produce terrestrial latrines that seem to be linked to resource defence [1–3, 68]. 3.1.1. Genus Microcebus: The Mouse Lemurs. Microcebus mu- rinus, the gray mouse lemur, is the lemuriform species for 3.1.6. Genus Daubentonia: The Aye-Aye. Both sexes exhibit which the accessory olfactory system (AOS), including the vomeronasal organ, has most fully been investigated [52]. anogenital scent marking [2, 69], and female anogenital scent marking increases during estrus [70]. Aye-ayes also engage in In M. murinus, male-male, male-female, and female-female urine trail marking [2, 71, 72]. socio-sexual interactions are mediated and coordinated by urinary chemosensory cues [53–55]. Studies of M. murinus in captivity have shown that male urinary marking behaviour 3.1.7. Genus Avahi: The Woolly Lemurs. The woolly lemurs decreases with age [56, 57]. The suite of scent-marking are not at all well-studied; there is a dearth of research on behaviours known for the gray mouse lemur includes punc- their behavioural ecology. I could not find any published tuated urine marking (sometimes with “perineal wiping”), information on the olfactory behavioural ecology of Avahi. head rubbing and muzzle or lip wiping, branch chewing with salivary deposition, and, especially, “urine washing” (where individuals purposefully urinate on their hands and feet), 3.2. The Lorisiformes. All taxa that have been studied in this which accounts for over 80% of all scent-marking behaviours nocturnal primate infraorder (that is, the lorises, pottos, performed [2, 3, 58–61]. In a recent field study of the and galagos, or bushbabies) scent mark extensively with golden brown mouse lemur (M. ravelobensis), Braune and urine [58], and urine marking is much more frequent colleagues [62] recognized two forms of scent marking: urine than glandular scent marking. Together with the lorisine washing, and mouth wiping (sometimes with face and/or genus Loris, all galagine primates studied to date (except head rubbing). the galago genus Euoticus) exhibit both urine washing and punctuated urine marking (or “rhythmic micturition”) [73– 76]. Urine washing can occur in a variety of contexts, 3.1.2. Genus Mirza: The “Giant” Mouse Lemurs. Olfactory including mobbing behaviour, moving into an unfamiliar communication among Mirza during reproductive behav- area, during agonistic and aggressive encounters, and, in iour includes nasonasal, nasobody and nasogenital con- social interactions, especially when a female is in estrus [76– tact [63]. Both punctuated urine marking and urine trail 78]. Greater galagos (Otolemur crassicaudatus)havebeen marking occur, and experimental work indicates males can shown experimentally to differentiate scent marks by sex discriminate among the urine marks of conspecifics [3, 58]. and by individual [78, 79]. Allen’s galago (Sciurocheirus Both males and females anogenital scent mark, and, like alleni) shows high frequencies of urine marking in territorial Microcebus, Mirza also engages in salivary marking [59]. boundary zones [80]. Scent marking seems also to function Notably, Mirza would also appear to exhibit flehmen (see as a stress-reducing mechanism in the small-eared bushbaby photo Figure 8 in [59]—the caption reads, “The typical (Otolemur garnettii)[81]. Urine washing in Loris, the slender posture for smelling a mark of a conspecific; note the open loris, has been reported to often occur in the context of mouth, and retracted tongue,” emphasis added; cf. [64]). consuming noxious insect prey, both before catching the prey and after consuming the prey; urine washing would also 3.1.3. Genus Cheirogaleus: The Dwarf Lemurs. Data on olfac- occur if a loris was stung by an insect [82]. Loris females have tory communication are available for the greater dwarf lemur also been observed to urine wash before they groom their (Cheirogaleus major) and the fat-tailed dwarf lemur (C. infants—this has been proposed to possibly have an anti- medius). Both species exhibit punctuated urine marking and predator function when females “park” their infants while urine trail marking, as well as anogenital scent marking they forage (i.e., the possible anti-predator function of a [2, 58], but the dwarf lemurs are notable for their specialized female urine washing and then grooming her infant could be fecal marking of branches [2, 65], which Irwin and colleagues either that it provides an olfactory screen or barrier against [1] identify as arboreal latrine behaviour. Dwarf lemur fecal potential predators, or that it acts as a form of predator marking may be related to territorial advertisement. mimicry while the infant is “parked”) [82]. All lorisine primates studied thus far exhibit urine trail marking in addition to punctuated urine marking [2, 58, 3.1.4. Genus Phaner: The fork-Marked Lemurs. Phaner stands 76, 83]. In Loris, inter-sexual social interactions often see out amongst the nocturnal lemuriforms because of the males either sniffing the muzzle or anogenital region of apparent absence of any form of urine marking in this genus females [82, 84]. During allogrooming bouts, Loris males [2, 66]. Males may rarely scent mark branches with their and females will lick and rub a specialized brachial gland on throat gland [67]; more often, males use their throat gland their own face and body and on the body of the grooming to scent mark females during allogrooming bouts [66]. partner [82]. Perodicticus, the potto, exhibits “genital scratch grooming” during which grooming partners of both sexes 3.1.5. Genus Lepilemur: The Sportive Lemurs. Like most scent mark each other—this behaviour is not linked to repro- other nocturnal strepsirhines studied to date, sportive lemurs duction [85]. In Perodicticus, urine marking may accompany exhibit urine marking [2, 3, 58]. Only males are reported allogrooming [86]. During allogrooming, pottos also mark to anogenital scent mark [1–3]. Although Lepilemur species each other with saliva and genital secretions [87]. Arctocebus, International Journal of Zoology 5 Table 1: Comparative interspecific profiles of scent marking behaviours among nocturnal strepsirhine genera (i.e., lemuriforms, galagines, and lorisines) and the cathemeral lemurid genera Eulemur and Hapalemur, as derived from the published literature on these taxa [1–3, 52– 112]. Scent-marking behaviours: 1, urine washing; 2, punctuated urine marking; 3, urine-trail marking; 4, muzzle wipe/branch chewing (saliva deposition); 5, flehmen; 6, fecal marking; 7, latrine behaviour; 8, anogenital scent marking; 9, head marking (males). Scent-marking behaviours Strepsirhine taxon (refs) 1 2 3 4567 8 9 Nocturnal lemuriforms Microcebus [2, 3, 52–62]] + + − +? −− − + Mirza [3, 58, 59, 63, 64] − ++ + + −− ? (Both sexes) Cheirogaleus [1, 2, 58, 65] − ++ ? ? + − +? Phaner [2, 6, 66, 67] − ?? ? ? −− − (?) (Male throat gland) Lepilemur [1–3, 58, 68] − + − ?? − + ? (Males) Daubentonia − ?+ ? ? −− + − [2, 68, 69, 71, 72] Avahi (no refs.) − (?) ? ? ? ? − (?) − (?) +(?) ? Galagines [58, 73–83] Galagoides ++ − ?? −− ?? Galago ++ − ?? −− ?? Euoticus −−− ?? −− ?? Sciurocheirus ++ − ?? −− ?? Otolemur ++ − ?? −− +? Lorisines [2, 58, 76, 82, 84–89] Loris +++ ? + −− + − Nycticebus − ++ ? ? −− ? − Perodicticus − ++ ? + −− + − Arctocebus − ++ ? ? −− − + = “passing over” Cathemeral lemuriforms [1–3, 90–113] Eulemur − + − ++ −− ++ Hapalemur − + − +? − ++ − the golden potto, exhibits distinctive “passing over” scent- marks. Males countermark the urine marks of other males marking behaviour, where the male straddles the female and with significant amounts of urine. In this species, estrus scent-marks her dorsum [85]. “Passing over” has also been females appear to prefer countermarking males [88], and males whose scent-mark odours are already familiar to them observed in Loris and Perodicticus [82]. Flehmen behaviour [89]. has recently been described in these two genera [82]; in Loris, it followed the licking of a urine mark while in Perodicticus it followed a male sniffing a substrate in a female’s home range 3.3. The Cathemeral Lemurids. Comparative data on the [82]. Nycticebus, the slow loris, apparently possesses a “fear olfactory communication of cathemeral lemurids, a good scent” (an “Angstgeruch”), and this has also been suggested deal of it from field research reported since 1990, reveals both for Perodicticus and Arctocebus (especially in the context broad similarities with nocturnal strepsirhines (see Table 1; of mother-infant alarm communication [86]); similarly, [1–3, 52–113]), as well as interesting, and unforeseen, Loris has been suggested to have an anti-predator “alarm distinctions among the cathemeral lemurids themselves (see pheromone” [82]. Male pygmy slow lorises (N. pygmaeus) Table 2;[1–3, 90–113]). In addition to anogenital scent- countermark, with urine, on both male and female urine marking, most cathemeral lemurid species also make use 6 International Journal of Zoology Table 2: Comparative interspecific profiles of scent marking behaviours among lemurid species of the genera Eulemur and Hapalemur,as derived from the published literature on these taxa [1–3, 90–113]. Thepatternsseeninthe twopair-bonded Eulemur species, E. mongoz and E. rubriventer, are very similar to each other, and contrast in significant ways to the patterns exhibited amongst the Eulemur taxa that occur in multimale, multifemale social groups (i.e., the E. fulvus group of taxa, E. macaco,and E. coronatus). Scent-marking E. fulvus group E. macaco E. coronatus E. mongoz E. rubriventer Hapalemur behaviours Anogenital scent-mark +++ ++ + surfaces Urine mark + + + + ? + Teeth grinding Bite mark (saliva during + + + Cheek rubbing + deposition) males inter-group encounters Anogenital mark M→FM→ F Conspecifics M→FM→FM→ F M→ F F→MF→ M HeadMarking(males) +++ ++ − Hand/palmarmarking Antebrachial +++ ++ (males) gland marking Anogenital sniff (M→F) +++ ++ + Mmarks tail with Observed in Observed in antebrachial Self-marking −− − captivity captivity glands to “stink fight” other Ms Variable.Vocal & Marking during Vocal and visual Vocal & visual ++ visual displays; inter-group encounters displays displays (Incl. F (Both substrate some marking overmarking of and self-marking) M anogen marks) Flehmen ? ?? ? ? (pers. obs.) Latrine behaviour −−− −− + of punctuated urine marking (deposited concurrently with in this process is unclear. In both of these pair-bonded the anogenital scent mark—cf. [35], where lemurids, includ- Eulemur species, anogenital scent marking of conspecifics of ing several Eulemur taxa, are characterized as “nonurine the opposite sex is performed by both sexes, rather than only marking” species). I could not find any report, however, males anogenitally scent marking females (a pattern seen in of punctuated urine marking in Eulemur rubriventer, the the multi-male, multi-female group-living Eulemur species). red-bellied lemur (also, Tecot, personal communication). Scent marking also figures prominently during intergroup Urine washing has never been reported in any cathemeral encounters with conspecific groups in both E. mongoz and E. strepsirhine. Head marking by males occurs across the entire rubriventer, including females overmarking male anogenital genus Eulemur. marks in E. rubriventer [93, 94]. These differential patterns of Notably, the mongoose lemur (E. mongoz) and the red- scent-marking behaviour were only uncovered as emergent bellied lemur (E. rubriventer), which are both pair-bonded patterns because of this comparative review of olfactory and territorial species, share similar patterns of olfactory communication in the genus Eulemur and other strepsirhine communication [90–94]. These two Eulemur species con- primates. trast in their patterns of scent-marking behaviour vis-a-v ` is In contrast to mongoose and red-bellied lemurs (i.e., the their congeners that exhibit multi-male, multi-female social two Eulemur species that exhibit pair bonding), there is a organization: the crowned lemur (E. coronatus)[95, 96], the tendency among the crowned, black, and brown lemurs (i.e., black lemurs (E. macaco and E. flavifrons)[97–101], and the Eulemur taxa that exhibit multi-male, multi-female social the brown lemur taxa (E. fulvus, E. rufus, E. sanfordi, E. groups), to engage in vigorous visual and vocal intergroup albifrons, E. rufifrons, E. collaris,and E. cinereiceps)[102– displays rather than intergroup displays involving concerted 109]. I could not find any report of male “bite marking” scent marking. In captivity, however, adjacently housed (a behaviour in which a male chews a branch and deposits groups of brown lemurs have been observed to exhibit a salivary mark) in either mongoose or red-bellied lemurs. scent marking in addition to the aforementioned visual and Although male bite marking has not been reported in these vocal inter-group displays. Self-marking has been reported twospecies,malemongooselemurshavebeenobservedto in captive brown lemurs (E. fulvus)[2], and the gray gentle cheek rub branches [91]; whether or not saliva is deposited lemur Hapalemur griseus [113]. Male Hapalemur griseus rub International Journal of Zoology 7 their antebrachial glands on their tail in advance of facing and differences among strepsirhine primate species in their off against other males in tail-waving “stink fights”; these chemosensory biology and olfactory communication can are similar in nature to the “stink fight” displays of male be expected from future studies that link odour, genetics, ring-tailed lemurs (Lemur catta)[44]. I have observed a behaviour, and ecology [20, 26, 35, 50, 114]. captivemaleblack lemur(E. macaco) self-mark by repeatedly making palmar markings over his tail. Flehmen behaviour Acknowledgments has been reported in the diurnal L. catta ([64]; personal observation). I have also observed a wild male black lemur A brief version of this paper was presented in the Symposium (E. macaco) exhibit flehmen during the breeding season— on “Olfactory Communication in Nocturnal and Cathemeral once when he exhibited the characteristic facial grimace Primates” held during the XXII Congress of the International associated with flehmen after actively sniffing the air, and a Primatological Society in Edinburgh, Scotland, August 3– second time after the same male sniffed a tree branch while 8, 2008. The author thanks to Dr. Sharon Gursky for the in proximity to a juvenile male from another social group invitation to participate in that symposium and for encour- [100]. The latrine behaviour reported in Hapalemur [1]is agement in the first place to undertake this comparative look unique among the cathemeral lemurids. at the behavioural ecology of olfactory communication in nocturnal and cathemeral strepsirhines. Comments provided by two anonymous reviewers and Dr. Lesley Rogers, editor 4. Conclusions of the paper, were most useful and helped to improve earlier drafts of the paper. The paper was also improved In broad terms, cathemeral lemurids exhibit many forms of by detailed comments that were kindly provided by Dr. olfactory communication that are the same as, or similar Susan Muir. Heartfelt thanks must go to Caleigh Farrell, the to, those seen in nocturnal strepsirhine species, including author’s student research assistant, for the untold hours and punctuated urine marking, anogenital scent marking of boundless energy she devoted to helping him track down the conspecifics, male overmarking of female scent marks, and, relevant sources in a very scattered literature. This paper is in the two pair-bonded Eulemur species, scent marking in dedicated to the late Dr. Shelley Saunders. territorial boundary zones. 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