Animal Behaviour 81 (2011) 889 – 890
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The Social Intelligence of Lemurs
As humans, we have a natural curiosity about the evolution of our own characteristics, and in particular about the evolution of our unusual cognitive abilities. In reconstructing the history of such traits, the lemurs and lorises of the suborder Strepsirrhini are of particular importance. The strepsirrhines are the primates most distantly related to humans, and at least in that egocentric sense the most ‘ primitive ’ . When these animals share a trait with us, that trait most probably dates as far back as the divergence of the lemur/loris clade from the monkey/ape/human clade, perhaps some 75 million years ago. Therefore, it is of particular interest to examine the cognitive abilities of strepsirrhines, as is done in a paper in this issue (pp. 925 – 931) by Aaron A. Sandel, Evan
MacLean and Brian A. Hare of Duke University.
Sandel and colleagues tested several species of lemurs, starting with ringtailed lemurs (
Fig. 1
), on tasks that required subjects to
Figure 1.
A group of ringtailed lemurs. Photo: David Haring.
make decisions based on their assessment of what a human could or could not perceive. The lemurs were fi rst taught that humans were competitors for food: if a lemur approached food placed directly in front of a human, the food was taken away, whereas if the animal approached food off to the side of the human, the animal was allowed to feed. Then in a fi rst cognitive test, lemurs were given a choice between approaching two food sources, one with a nearby human facing towards the food, and the other with a nearby human facing away from the food. Ringtailed lemurs approached the food with the human facing away about 75% of the time, signi fi cantly more often than expected by chance.
A second test was designed to be somewhat more dif fi cult: a single human was oriented at right angles to the subject, which had to choose between one food source in front of the human and another behind it. Ringtailed lemurs approached the tray behind the human about 69% of the time, again signi fi cantly more often than chance.
In both experiments, individual subjects were tested multiple times and were allowed to feed only from the ‘ correct ’ food sources; however, the lemurs showed no evidence of learning within the experiments, indicating that they could solve the tests with what they knew going in.
Monkeys and apes are able to solve similar tasks, which suggests that the necessary cognitive abilities date from before the split of lemurs and lorises from the monkey/ape clade. This picture is complicated, however, by the results of a third experiment, in which Sandel et al. applied their second cognitive test to three additional lemur species, ruffed, black and mongoose lemurs, as well as to a new set of ringtailed lemurs. The ringtailed lemurs again showed a signi fi cant preference for approaching food behind over food in front of a human.
In contrast, none of the other three species of lemurs showed any indication of solving the problem: for each, more than half the approaches were to the food in front of the human.
These results indicate that the ability to exploit social cues is not widespread in lemurs, and thus may not be ancestral to the lemur/ loris clade as a whole. Sandel and colleagues suggest that, instead, the shared ability of monkeys, apes and ringtailed lemurs to solve these social intelligence problems may be an example of convergent evolution. Why ringtailed lemurs have converged on the social intelligence of higher primates may be explained by the nature of ringtailed lemur societies, which resemble in their complexity the societies of many monkey species more than they do the simpler societies of other lemurs and lorises. Thus the results of the Sandel et al.
study can be taken as supporting the social intelligence hypothesis, which proposes that social interactions have provided a key selective factor favouring the evolution of greater cognitive abilities.
William A. Searcy
Executive Editor
0003-3472/$38.00 2011 The Association for the Study of Animal Behaviour. Published by Elsevier Ltd.
doi: 10.1016/j.anbehav.2011.03.006

890 In Focus / Animal Behaviour 81 (2011) 889 – 890
Why Male Spiders Go For Broke
I don ’ t know if you ever saw Gladiator ? The fi lm in which Russell
Crowe, as General Maximus Decimus Meridius (yes, really .
), eventually avenges the murder of his wife and son as a result of being the craziest, most fearless gladiator in the whole of Rome? When asked why he ’ s not afraid to die, Maximus answers along the lines of ‘ because I ’ m already dead ’ ; with nothing left to lose, Maximus can go for broke. Enjoyable nonsense through and through, but there are some very interesting real-life examples of males acting in this fashion; they just happen to be spiders, and the story is all the more fascinating (if gruesome) as a result. In this month ’ s issue,
Simona Kralj-Fi ser, Matja z Gregori c, Shichang Zhang, Daiqin Li and
Matja z Kuntner (pp. 933 – 939) reveal how male spiders ratchet up their aggression and willingness to fi ght when the loss of their genitalia means that they have nothing left to lose.
Speci fi cally, Kuntner and colleagues investigated mating behaviour in the South-East Asian spider, Nephilengysm alabarensis ; a species that shows high levels of sexual cannibalism, meaning that females eat their mating partners either during or after sex.
As if this wasn ’ t brutal enough, males of this species regularly damage their reproductive organs (their palps) during mating and frequently ‘ self-amputate ’ them entirely, with the result that they become sterile ‘ eunuchs ’
( Fig. 2 ). Although such males lose
all ability to mate, they can protect their mating partners against copulation attempts by other males. Given this lack of future mating opportunities, theory predicts that such males should respond with maximal force when confronted by other males. By the same token, intact males (and half-eunuchs, who have only lost one palp) should show more restraint because they have much more to lose reproductively if they should be injured or killed in a contest. If eunuchs are more aggressive than intact rivals, then the ‘ eunuch phenomenon ’ could be adaptive, especially if the amputated palps also serve as copulatory plugs, blocking the female ’ s copulatory opening and preventing other males from mating.
Kuntner and colleagues tested both of these possibilities in their experiments. They fi rst allowed males to mate with virgin females and then looked to see whether the female subsequently remated with new males. In a second experiment, they introduced two males onto a female ’ s web, and let them fi ght it out to investigate whether eunuchs paired with intact males or half-eunuchs did better. The results supported both hypotheses. The plugging of the female ’ s copulatory opening with male palps led to the prevention of subsequent copulation in 75% of cases, which is impressive but not infallible. In two cases, females were observed removing the plugs themselves, which suggests other males could potentially achieve success. More detailed research involving sperm counts or
DNA analysis is needed to con fi rm that the copulatory plugs increase the reproductive success of eunuchs, but it looks promising.
Eunuchs were also shown to be better fi ghters. Full eunuchs were both more aggressive and active than either half-eunuchs or intact males. Full eunuchs often walked towards the other male to chase and attack, and they were also more likely to be the initiators of aggressive episodes. Intact males also stayed further away from the female when paired with a eunuch than either another intact male or a half-eunuch. Consequently, eunuchs won most contests. What we don ’ t know yet, however, is whether eunuchs are better fi ghters purely because they become more aggressive
Figure 2.
Male spiders chew off their own palps when these are damaged during mating and become more aggressive as a result. Photos: Matja z Kuntner.
once they have lost their palps, or whether the loss of their palps also helps make them more agile and so more effective.
Becoming a eunuch does, therefore, seem to be an adaptive strategy. It is also known that males of this species can only charge each of their palps with sperm once, because spermatogenesis stops once spiders reach adulthood. Becoming a eunuch voluntarily, so to speak, thus makes even more sense, given that males only have, in essence, a single shot at mating. Kuntner and colleagues also suggest a further adaptive advantage that, at present, remains speculative. Given the short insertion times of the male ’ s palps into the female ’ s copulatory openings, along with the high levels of sexual cannibalism in this species, a mechanism by which males could continue sperm transfer even after they have escaped, been forcibly removed or cannibalized by the female could pay dividends. That is, the breakage of the male reproductive organs inside the female may allow males to continue mating
‘ remotely ’ , and so increase their chances of fertilization; an idea that Kuntner and colleagues are testing currently. What is clear, however, is that when male spiders lose their palps, it prompts them to give it their all when it comes to fi ghting.
Louise Barrett
Executive Editor