A Case of Adult Cannibalism in the Gray Mouse Lemur, Microcebus murinus

Abstract

Cannibalism, defined as the eating of conspecific flesh, has been observed in a number of primate species, although it is still a relatively rare phenomenon. In cases where primates were seen feeding on an individual of the same species, the victims have exclusively been infants or juveniles. Here, I report an event of a free-living, adult male gray mouse lemur, Microcebus murinus, cannibalizing an adult conspecific female that died of an unknown cause. This observation has implications for the basic ecology of the species and highlights the potential for great flexibility in diet and behavior by a primate. This is, to my knowledge, the first communication of cannibalistic behavior in this species, as well as the first reported case of a nonhuman primate cannibalizing an adult conspecific. Am. J. Primatol. 74:783-787, 2012. © 2012 Wiley Periodicals, Inc.

INTRODUCTION

Cannibalism has been observed in a wide range of taxa from bacteria to humans [Elgar and Crespi, 1992; Fox, 1975; González-Pastor et al., 2003; Marlar et al., 2000]. Killing and eating of conspecifics occur concurrently as well as separately in the different manifestations of the behavior [Itani, 1982; Persson et al., 2003; Polis, 1981]. The acts of killing that have been known to lead to eating of the victim include sexual cannibalism [Prenter et al., 2006], cultural reasons in humans [Silva, 1962], and infanticide in its various forms [Bartlett et al., 1993; Ebensperger, 1998; Hiraiwa-Hasegawa, 1988; Hrdy, 1979; van Schaik and Janson, 2000]. Furthermore, starvation and malnutrition are thought to have relatively often induced cannibalism [Elgar and Crespi, 1992; Mayntz and Toft, 2006]. In a number of species, it is a frequently seen phenomenon and may influence population dynamics [Fox, 1975; Polis, 1981].

In the vast majority of cases, the victims of intraspecific predation are subadults, but killing and eating of adults (although of usually smaller body size than the attacker) has also been described for instance in some species of insects, fish, amphibians, birds, and mammalian carnivores [Amstrup et al., 2006; Andersen, 2004; Polis, 1981; Rogers, 1983]. Many of the documented cases of cannibalism are from captivity or areas disturbed by humans, where the conditions (such as stress, crowding, or insufficient nutrition) may increase the frequency of the phenomenon and where it is easier to observe [Andersson et al., 2011; Angst and Thommen, 1977; Bartlett et al., 1993; Dellatore et al., 2009; Fox, 1975; Tartabini, 1991].

Variousprimate species are also known to occ-asionally kill or feed on conspecifics [Hiraiwa-Hasegawa, 1992; Itani, 1982]. New reports of infanticide and infant cannibalism [Bezerra et al., 2007; Culot et al., 2011; Dellatore et al., 2009; Fowler and Hohmann, 2010; Sherrow and Amsler, 2007] are quite regularly published as the accumulation of observation hours allows the ad libitum recording of rare behaviors. However, it has been thought that primate cannibalism only occurs in the context of infant eating and adults do not consume the flesh of other adults, even after killing the victim themselves [Hiraiwa-Hasegawa, 1992; Itani, 1982]. Here, I describe the first case of adult–adult cannibalism in a natural population of a primate.

METHODS

The site of the present observation, Kirindy forest in Western Madagascar, is natural habitat for one of the world's smallest primates, the gray mouse lemur (Microcebus murinus). The species is solitary, common in the area, and exhibits behavioral and physiological adaptations to the extreme seasonal variation in this environment: they are, for instance, capable of efficient fattening in the wet season and can utilize daily torpor in the dry season [Canale et al., 2011; Schmid, 2000; Schmid and Kappeler, 1998]. Their diet in the dry season (austral winter) consists of invertebrates and small reptiles, homopteran secretions, gum, and fruit [Dammhahn and Kappeler, 2008]. Their body mass varies over the year as a factor of food availability [Dammhahn and Kappeler, 2008, 2009; Schmid and Kappeler, 1998] and, in our study population, the average body mass is at its lowest for adult females in October and for adult males in November [Dammhahn, unpublished data].

In October–November 2010, I conducted a pilot study on the activity patterns of several M. murinus individuals via location and activity scans and focal observations. The individuals were equipped with radio transmitters. The radio collar was constructed of plastic piping and tagged with strips of reflective tape that facilitated sighting of the animal in the dark. The protocol involved locating each of the collared individuals two to three times during their most active hours (18:00–22:00 hr) and collecting instantaneous location and activity data every minute over a 10-min sampling period twice per night.

The data collection was authorized by the CAFF of the Direction des Eaux et Forêts, the Département de Biologie Animale, Université d'Antananarivo, and CNFEREF Morondava. The research complied with the laws of the Republic of Madagascar and adhered to the American Society of Primatologists’ Principles for the Ethical Treatment of Nonhuman Primates.

RESULTS

On the evening of October 27, 2010, I followed five individuals, including two focal sessions with an aged female (ID: 374B, born: 2003). By the first focal session that started at 19:25 hr, individual 374B had moved a distance of 50 m from her sleeping site. During this focal observation, she was out of sight in a thicket of lianas and only two sightings for instantaneous data points were acquired, although she was seen moving between the sampling times. Individual 374B was out of sight also during the second scan of the evening at 20:53 hr and only an approximate location (30 m distance from the previous sighting) could be assigned based on characteristics of the radio signal. On attempting the second focal session for this individual at 21:52 hr, I encountered her at the approximate same location as an hour earlier, but at this time I could see the reflection of the collar and approached to 10 m distance. I found that she was dead and her body was being fed on by a conspecific male.

The carcass was hanging head down from a branch at 1.5 m elevation from the ground. At the time of discovery, the body cavity had been torn open and the internal organs eaten. The skull had also been broken and the brain consumed. Additionally, the flesh had been torn from one hind and one fore limb. The corpse was known to be fresh since the individual had been seen active earlier and when the body was recovered, rigor mortis had not yet set in. When sighted, the cannibalistic male was ferociously biting into the protruding spinal cord (Fig. 1, supplementary material) and continued feeding on the body (the spine, ribcage, and soft tissue) for approximately 20 min after sighting. After his departure, I collected the body and brought it into the field camp, where a veterinarian conducted an autopsy the following morning. The autopsy provided no further clues to the cause of death or the animal's health status since all the vital organs were missing.

Figure 1. Adult male gray mouse lemur (Microcebus murinus) cannibalizing a conspecific female.

Based on routine trapping data, the deceased individual had been active at least from late September onward after probably hibernating through the peak dry season. She had been carrying a radio collar for 8 days before her death but no problems with the collar had been noticed. The victim was a relatively large individual, but (following a usual pattern) had been losing body mass since September, dropping from 59 g on September 22, 2010 to 54 g at time of collaring on October 19, 2010. Correspondingly, her body condition, calculated as body mass/bizygomatic distance, decreased from 2.66 to 2.43 (body condition index for M. murinus females as measured previously for the same population: median = 2.67, range = 1.96–3.17 [Dammhahn and Kappeler, 2009]). The cannibal was unidentifiable based on external features; hence, I could only establish that it was a previously marked adult male in a reasonably good body condition.

DISCUSSION

The cause of death of the cannibalized individual could not be ascertained, but as the body was hanging from vegetation, it is probable that the animal fell victim to predation. It seems somewhat unlikely that the cannibalistic male was the predator, as adult females are usually dominant over males and can chase them off when approached [Radespiel and Zimmermann, 2001]. According to the body mass measurements, the female was in a reasonably good body condition for the dry season despite the recent weight loss and should in normal circumstances have been able to fend off a male.

An alternative explanation would be predation by another species; however, a predator abandoning its prey would be uncharacteristic and therefore this question remains open. Frequent nocturnal predators of mouse lemurs in the area are certain snakes, owls, the Coquerel's giant mouse lemur, Mirza coquereli, and the fossa, Cryptoprocta ferox [Rahlfs and Fichtel, 2010; Rasoloarison et al., 1995], and here, the general appearance of the cadaver excludes snake or fossa predation. The cracked skull and slashed abdomen can be circumstantial evidence of predation by a lemur [Jolly et al., 2000], which in this case would be M. coquereli. If the victim was killed by a different species predator, this implies that M. murinus can engage in scavenging, which is previously rarely reported behavior not only in this species (at our study site, a mouse lemur has been observed scavenging a reptile once in the recent years [Susanne Schliehe-Diecks, personal communication]) but in all strepsirrhines [Butynski, 1982]. In other primates, intraspecific scavenging is inferred in cases where the consumption of a dead infant began only after a relatively long delay, even after partial decay of the body: one day after the infant's death in bonobos [Fowler and Hohmann, 2010] and in thick-tailed bush babies [Tartabini, 1991] and after up to 8 days in orangutans [Dellatore et al., 2009]. Although cannibalism is usually more frequently recorded in carnivorous or omnivorous species that include other similar prey items in their usual diet [Elgar and Crespi, 1992; Itani, 1982; Jolly et al., 2000; Persson et al., 2003; Polis, 1981; Rogers, 1983; Sherrow and Amsler, 2007], M. murinus has not been previously observed to eat mammalian flesh. It appears that scavenging, extended to mammalian flesh and even cannibalism, may be opportunistic strategies for M. murinus, suggesting high behavioral and dietary flexibility of the species.

The risks associated with eating the flesh of conspecifics include potential risk of injury if cannibalism is connected to intraspecific predation, as well as risk of pathogen transmission [Pfennig et al., 1998], although cannibalism has been judged to usually be a secondary means of disease transmission [Rudolf and Antonovics, 2007]. The implications of cannibalism may differ depending on whether the animals are capable of recognizing conspecifics or simply consider their flesh after death a consumable resource. While the extent of the species recognition capacity of mouse lemurs is currently largely unknown, future studies may be able to address this issue. The frequency of cannibalism in free-living M. murinus is unknown—although the lack of previous reports implies it is rare—and hence the importance of these factors cannot yet be estimated.

Adult–adult cannibalism is a phenomenon that is rarely seen in mammals, and it has to my knowledge never before been reported from wild primates. Infanticide, on the other hand, is known from many primate species [Culot et al., 2011; Hiraiwa-Hasegawa, 1988; Hrdy, 1979; Itani, 1982; van Schaik and Janson, 2000], including lemurs [Foerg, 1982; Jolly et al., 2000; Stanger et al., 1995], and it sometimes leads to the eating of the victim. Infant eating differs from adult cannibalism essentially in the size of the food item: an infant may represent the same size class as other potential prey, while an adult conspecific could in normal circumstances not be safely predated and would therefore not necessarily be seen as consumable by the attacker [Fox, 1975; Polis, 1981; Rogers, 1983; Watts, 2008].

Infanticide in a natural setting has not been reported in M. murinus but captive mothers of the species have been seen occasionally cannibalizing stillborn infants; even eating of dead adults has been witnessed in captive mouse lemurs (Fabienne Aujard, personal observation). The cases in captivity are quite rare, with a few events seen yearly in a large study population of M. murinus. Whereas captive cannibalism (including the killing of conspecifics) has sometimes been connected to crowding, high-stress conditions, or insufficient diet [Andersson et al., 2011; Fox, 1975; Marlar et al., 2000; Tartabini, 1991], none of these factors are likely causes of the cases observed in the mouse lemur colony in question: lethal aggression toward cage-mates has not been reported and the lemurs are normally fed a balanced diet ad libitum.

The occurrence of cannibalism in captive mouse lemurs suggests that the behavior could also occur occasionally in wild populations when the conditions permit it (although extensive hours of focal observations and sheer luck may be prerequisite for a researcher to witness the behavior). For instance, stillborn infants may be consumed by the mother, or conspecifics that die during hibernation could be cannibalized by individuals sharing the tree hole, but as these events always occur within the nest, this behavior would be almost impossible to observe. It may be generally more difficult to witness cannibalism in a solitary, nocturnal species such as the gray mouse lemur, as opposed to somewhat more frequent sightings in habituated groups of diurnal primates [Bartlett et al., 1993; Bezerra et al., 2007Cäsar et al., 2008; ; Culot et al., 2011; Fowler and Hohmann, 2010; Sherrow and Amsler, 2007] that are routinely observed: in group-living animals, the rate of intraspecific encounters is higher and rare behaviors may at least opportunistically be recorded from more than one individual at a time.

Nutritional stress has been considered a potential trigger for cannibalistic behavior [Amstrup et al., 2006; Elgar and Crespi, 1992; Fox, 1975; Manocha and Long, 1977; Mayntz and Toft, 2006; Polis, 1981], and it is also a possible cause for the case reported here. Protein deficiency in particular has been shown to induce infanticide in squirrel monkeys [Manocha and Long, 1977], which suggests that engaging in cannibalism can be an extreme response at time of malnutrition. On the other hand, the relatively good condition of the cannibal observed in this case as well as the ad libitum conditions assumed for the cases in captivity suggest that extreme starvation is not necessary to trigger cannibalism. However, the event I witnessed occurred in a season when the food availability is low and, on the other hand, the coinciding mating season may present additional energy demands. Therefore, finding an additional source of nutrition—particularly protein—without energy expended in hunting could be sufficient motivation to adopt an unusual foraging strategy. We may speculate that if the nutritional gains are high enough with regard to potential costs, such as risk of infection [Pfennig et al., 1998], it could be adaptive to take advantage of the conspecific food source even in the absence of serious nutritional stress [Fowler and Hohmann, 2010; Fox, 1975; Polis, 1981]. In a challenging environment, the capacity to opportunistically exploit alternative food sources can be highly adaptive and could significantly enhance an individual's chances of survival.

The fact that feeding on the corpse continued for at least 20 min indicates strong preference rather than inadvertent behavior. A preference for conspecific flesh may arise due to its higher nutritional quality compared to heterospecific prey [Mayntz and Toft, 2006]. It is, however, also possible that such behavior is not adopted by all individuals in the population even when the opportunity presents itself, and could perhaps be interpreted either as pathology [Dellatore et al., 2009] or individual preference. The rarity of primate cannibalism may signal either a scarceness of opportunities for cannibalism (as well as a low probability of observer presence!) or interindividual differences in exploiting such opportunities due to individual preferences, personality features (such as avoidance of novel food items), or other as yet unknown factors [Mayntz and Toft, 2006; Polis, 1981]. Opportunities for mouse lemur cannibalism must by necessity be quite rare in the wild, since predation is a frequent cause of death and predated corpses will not usually be left uneaten. Furthermore, the relative rarity of cases seen in captivity suggests that intraspecific scavenging is indeed not practiced by every individual even if an opportunity arises.

This case study provides evidence that cannibalism in primates need not be restricted to infanticide as previously thought [Elgar and Crespi, 1992; Hiraiwa-Hasegawa, 1988; Itani, 1982]; when the reason for cannibalism is dietary and there are no apparent, immediate risks, the victim can be of the same size class and even senior to the aggressor. The steadily accumulating evidence from a wide range of species portrays cannibalistic tendencies not as aberrant behavior but rather as an infrequent but natural phenomenon. Cannibalism may confer immediate nutritional and energetic benefits to the cannibal and therefore might have adaptive value at the individual level.

ACKNOWLEDGMENTS

I am grateful to Cornelia Kraus, Peter Kappeler, and two anonymous reviewers for comments on earlier drafts; Elise Huchard for conducting the necropsy; Mia-Lana Lührs, Susanne Schliehe-Diecks, Melanie Dammhahn, and Jörg Wettlaufer for helpful discussions; and Fabianne Aujard for information on cannibalism in captive conditions. The data collection was made possible by funding from the German Research Foundation (DFG) and logistic support from Peter Kappeler and Leon Razafimanantsoa. The data collection was authorized by the CAFF of the Direction des Eaux et Forêts, the Département de Biologie Animale, Université d'Antananarivo, and the CNFEREF Morondava. The research complied with the laws of the Republic of Madagascar and adhered to the American Society of Primatologists’ Principles for the Ethical Treatment of Nonhuman Primates.