“Stink flirting” in ring‐tailed lemurs (Lemur catta): Male olfactory displays to females as honest, costly signals

Abstract

Sexual selection for honest behavioral displays of quality has driven the development of remarkably complex courtship behavior in many animal species. Olfactory displays are often overlooked as an area of inquiry compared to auditory and visual displays. Ring-tailed lemur (Lemur catta) scent marking of substrates has been studied extensively, although the male olfactory displays of anointing and wafting tails to females has received relatively little attention. We studied the role of male olfactory displays to females, evaluating whether such signals function as honest, costly signals of male dominance status in two groups of wild L. catta at Berenty Reserve, Madagascar. Our results suggest that male tail anointing and tail wafting displays to pre-estrous and estrous females are correlated with male dominance rank, and moreover appear to operate as costly signals, as such displays increase aggression received from males and females while other types of scent marking do not. Furthermore, females showed greater mating preference (as measured by sexual presents) for resident males who performed the "anoint tail" and "waft tail" displays towards them. When males perform the "anoint tail" and "waft tail" displays to females, they receive higher levels of aggression than if they were to perform other types of scent marking. Interestingly, immigrating (peripheral) males performed the "anoint tail" and "waft tail" displays at higher rates than resident males, which could honestly indicate their quality or may simply be associated with the alternative mating strategy of transferring between groups to gain mating opportunities. Our finding that tail anointing and tail wafting displays function as honest signals of dominance for resident males-and that these costly displays appear to positively affect female mate choice-is the first evidence of this function for this particular olfactory signal in L. catta.

Costs of injury for scent signalling in a strepsirrhine primate

“…When coupled with mechanisms for individual recognition 45 , 52 , sensitivity to changes in competitor condition helps avoid risks and fitness costs of unnecessary fighting by allowing males to (1) reliably assess competitor fighting ability, (2) assess their likelihood of winning an aggressive encounter with a potential competitor, and (3) selectively engage in aggressive interactions with animals of compromised or poor competitive ability 5 , 77 , 78 . Wrist marking and tail anointing are multimodal (i.e., combined visual, olfactory and, sometimes, auditory) displays of dominance in male ring-tailed lemurs 55 , 79 , 80 , whose dominance hierarchies are fluid. Status maintenance may thus require continual scent marking and assessment of competitor marks 46 , 80 .…”

“…The higher rates of wrist marking we observed directed at odorants from injured animals (relative to odorants obtained when the same animals were healthy) is consistent with recipient males using counter-marking strategies to gain social dominance over competitively weak conspecifics 76 , 81 . Similarly, dominant resident males are more likely to engage in conspicuous tail-anointing and ‘stink-fighting’ behaviour, which functions as a potentially costly ‘badge of status’ relevant to both male and female recipients 79 . Alternately, injured animals might modulate their overt displays of aggression, including scent-marking behaviour, to avoid being attacked by dominant or otherwise healthy individuals 75 .…”

Design, delivery and perception of condition-dependent chemical signals in strepsirrhine primates: implications for human olfactory communication

“…Perhaps the impetus to deposit pure scents versus mixtures is to target different audiences by influencing the time-course over which a signal remains functional: an immediate function could be to relay short-lived, condition-dependent messages to one's group members, whereas a deferred function could be to advertise long-term, territorial usage to extra-group conspecifics [106] (figure 5g). These same males can also self-anoint by rubbing both secretions onto their tail to imbue the hairs with a combined odorant 'cocktail'-creating a composite, unimodal signal-that is then wafted at an opponent or a potential mate during face-to-face 'stink-fighting' [35,39] or 'stink-flirting' [134], respectively ( §3c). Active scent deployment in both cases (fight and flirt) requires a recipient and serves an immediate, evaluative, social function.…”

Affiliative Contact Calls during Group Travel: Chirp and Wail Vocalization Use in the Male Ring-Tailed Lemur (Lemur catta)

“…As a female-dominant, female-philopatric species [Jolly, 1966;Sussman, 1992;Sauther, 1993], males typically disperse for the first time at the age of 3-4 years and subsequently every few years after [Budnitz and Dainis, 1975;Jones, 1983;Sussman, 1991;Parga and Lessnau, 2008;Parga, 2010]. Males join new groups to optimize mating opportunities during female oestrus, which happens annually in April-May in Madagascar and consists of 577 Folia Primatol 2020;91:575-594 DOI: 10.1159/000508808 individual females going into asynchronous oestrus during 2-to 24-h periods, during which time they typically mate with multiple males [Jolly, 1966;Van Horn and Resko 1977;Taylor and Sussman, 1985;Koyama, 1988;Sauther, 1991;Parga, 2006a;Walker-Bolton, 2017]. Although lower ranking than females, male ring-tailed lemurs have their own dominance hierarchy, which is mediated by agonistic behaviour ranging from ritualized displays to physical combat [Jolly, 1966;Mertl, 1976;Gould, 1994;Macedonia, 1990Macedonia, , 1993Pereira and Kappeler, 1997;Mertl-Millhollen, 2006;Bolt, 2013bBolt, , c, 2014Walker-Bolton and Parga, 2017].…”