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Behavioral Ecology Vol. 13 No. 2: 160-162
© 2002 International Society for Behavioral Ecology
Colony defense in Damaraland mole-rats, Cryptomys damarensis
Large Animal Research Group, Department of Zoology, University of Cambridge, Cambridge CB2 3EJ, UK, and Department of Zoology and Entomology, University of Pretoria, Pretoria, 0002 South Africa
Address correspondence to R. Cooney, WWF International Species Programme, WWF-UK, Panda House, Weyside Park, Godalming, Surrey GU7 1XR, UK. E-mail: rcooney{at}wwf.org.uk .
Received 22 September 2000; revised 11 April 2001; accepted 6 May 2001.
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ABSTRACT |
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 TOP ABSTRACT INTRODUCTIONMETHODSRESULTSDISCUSSIONREFERENCES |
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I examined defense against conspecific intruders in colonies of the Damaraland mole-rat. I introduced foreign animals to captive colonies and examined the effect of the sex and breeding status of the intruder on the sex and breeding status of those that defended. Intruding mole-rats were almost always attacked. Colony defense against intruders was carried out almost exclusively by dominant, reproductive individuals and was directed primarily toward individuals of the same sex. Nonbreeding, subordinate mole-rats participated only rarely. These results contrast sharply with colony defense in the related naked mole-rat and suggest that investment in defense activities in Damaraland mole-rats primarily reflects repulsion of potential competitors for breeding status. Subordinate mole-rats may lack incentive to participate in potentially costly defense, as they are unlikely to gain reproductive opportunities within the colony and probably gain fitness primarily through dispersing to breed.
Key words: cooperative breeding, Cryptomys damarensis, kin selection, mole-rats, sociality, territorial defense.
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INTRODUCTION |
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TOPABSTRACTINTRODUCTIONMETHODSRESULTSDISCUSSIONREFERENCES |
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In social animals, defense of communal resources such as territories or food resources against intrusion by conspecifics or predators may involve considerable costs and risks (e.g., Fitzgibbon, 1997
;
Packer et al., 1990), and
willingness to repel intruders may vary according to the benefits so gained
(Downs and Ratnieks, 2000;
Reeve, 1989). What fitness
benefits do individuals gain from costly defense? Breeding individuals can
clearly enhance their own direct fitness through defending resources or mates.
For nonbreeding individuals, the situation is more complex. Nonbreeders may
gain a range of current or future direct benefits through providing assistance
to reprodutives (e.g., Balshine-Earn et
al., 1998; Cockburn
1998) or simply through safeguarding their own access to
resources. Furthermore, defense by nonbreeders may secure kin-selected fitness
benefits through safeguarding the reproduction of related breeders. In many
social insects, kin selection has led to the evolution of sterile workers
which are behaviorally or morphologically specialized for colony defense
(Emlen and Nijhout, 2000;
Michener, 1974).
Naked mole-rats, Heterocephalus glaber, show the most extreme
group sizes and reproductive skew among vertebrates, with colonies averaging
70-80 individuals (Brett, 1991)
and breeding typically restricted to one female and one or two males
(Jarvis, 1991). Defense is
primarily carried out by larger, nonbreeding individuals
(Lacey and Sherman, 1991;
O'Riain and Jarvis, 1997).
Breeders only rarely participate, and often avoid defense by retreating to the
central nest (O'Riain and Jarvis,
1997) or pushing subordinates out of the nest to face intruders
(Lacey and Sherman, 1991). It
is currently unclear whether this specialization is primarily shaped by kin
selection, colony-level selection or direct selection
(Lacey and Sherman, 1991;
O-Riain and Jarvis, 1997).
I investigated colony defense in Damaraland mole-rats, Cryptomys
damarensis. Sociality has evolved independently in naked and Damaraland
mole-rats (Faulkes et al.,
1997), although their social systems appear superficially similar.
Damaraland mole-rats are completely subterranean and live in large groups
(mean = 11, range 2-41, n = 110 colonies; Jarvis JUM and Bennett NC,
unpublished data) in the Kalahari red sands of southern Africa. Reproduction
is monopolized by a single, breeding female and one to two males
(Jarvis and Bennett, 1993),
and field-based calculations indicate that only a small proportion of
individuals gain a breeding opportunity
(Jarvis et al., 1994). Under
these conditions nonbreeders might be expected to pay the costs of defense to
gain kin-selected benefits. I examined the reactions of breeding and
nonbreeding mole-rats to intrusion by mole-rats of different sexes and
breeding status to determine whether certain classes of mole-rats specialize
in defense and to understand the selective pressures shaping participation in
defense.
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METHODS |
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TOPABSTRACTINTRODUCTIONMETHODSRESULTSDISCUSSIONREFERENCES |
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Mole-rat colonies were housed in large, plastic burrow systems with about 9 m of tubing and several nesting chambers for each colony and provided with paper and wood shavings for bedding, chipboard "gnawboards" for stimulation, and ad libitum food. Colonies had been bred either from pairs or from small groups of related males to which a single female had been added, mimicking the origin and formation of colonies in the wild (Jarvis and Bennett, 1993
).
Details of general husbandry are described elsewhere
(Bennett, 1990). Individuals
were marked for recognition when necessary with gentian violet. Six colonies were used (mean ± SE = 6.8 ± 1.1, range = 3-10 individuals). Each trial was the introduction of one foreign (unrelated) animal from a different colony. Animals introduced are referred to as intruders, colonies to which they were introduced are called defenders. Four categories of intruders were introduced: dominant males, dominant females, subordinate males, and subordinate females. Each defender colony underwent 12 separate trials, with 3 different intruders of each category introduced. Within each category, each individual introduced was from a different colony. At least 24 h were left between each trial undergone by a defender colony. No individual was used as an intruder more than three times throughout the entire experiment, and at least 2 days were left between trials using the same individual as an intruder. The order in which categories of intruder were introduced to a colony was randomized.
Intruders were released into colonies with minimum disturbance and as far as possible from any resident colony members. In most cases defenders showed no reaction indicating awareness of the intrusion until the intruder encountered a resident member in the burrow. Trials were filmed with a Sony professional video camera and VHS video. I followed intruders with the camera and recorded the identities of all individuals encountered and their responses by voice on the videotape. Intruders were removed either immediately if they were attacked, or after 15 min if they were not attacked. The length of introductions ranged from less than 10 s to 15 min. Attacks were unambiguous and distinct, involving sudden, highly aggressive biting and chasing.
Analysis
From videos, I determined for each member of the defending colony, for each
trial, whether it had encountered the intruder and whether it attacked the
intruder. To determine which factors affected the likelihood of attack. I
constructed a generalized linear model (GLM; GENSTAT 5, Release 4.1). I fitted
the number of times the intruder was attacked to a binomial distribution, with
number of trials in which the intruder was encountered as the denominator.
This procedure controls for whether a mole-rat actually encountered the
intruder in assessing the likelihood of attack. I included all likely
explanatory variables in the maximal regression model and dropped terms
sequentially until the model included only terms whose elimination would
significantly decrease the explanatory power of the model.
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RESULTS |
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TOPABSTRACTINTRODUCTIONMETHODSRESULTSDISCUSSIONREFERENCES |
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Reactions to the intruder by defender mole-rats ranged from apparent disregard to immediate, intense aggression. In 94% (68/72) of introductions, the trial was terminated when one or occasionally two defending mole-rats attacked the intruder. In 80% of cases (54/68) several mole-rats were encountered before attack occurred; attacker identity thus does not simply reflect the first mole-rat encountered.
Generalized linear modeling showed that the most important predictor of an attack was the dominance of the defending mole-rat encountered. Dominant mole-rats in the defending colonies were much more likely to attack intruders than were subordinate defenders (Table 1 and Figure 1): 95% (69/73) of attacks on intruders were by dominant individuals. Of the four attacks by defender subordinates, all were by females, and three of these were by the same individual. In each case the intruder was a dominant female. Subordinates frequently came into contact with intruders and usually sniffed them and followed them briefly or entirely ignored them. In two cases, the introduction of males led to sexual solicitations by subordinate females. In each case the encounter was quickly terminated when the intruder was attacked by the dominant male.
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In contrast, the dominance of the intruding mole-rat made no difference to the likelihood of attack. Intruders were attacked in all cases except four. In three of these cases the intruder was a subordinate female, in the other a dominant male. In these cases, the trial was terminated after 15 min in which the intruder was not attacked despite coming into contact with numerous individuals, including the dominant male and dominant female.
Defending mole-rats were much more likely to attack intruding mole-rats of the same sex than the opposite sex, as indicated by the significance of the interaction term defender sex x intruder sex (Table 1 and Figure 1). Of attacks by females, 79% (19/24) were on other females, and 65% (32/49) of attacks by dominant males were on other males. There was a nonsignificant trend for male defenders to be more likely to attack than females (Table 1 and Figure 1).
The interaction term between the dominance of the defender and the sex of the intruder was significant, with female intruders more likely to be attacked by subordinates than male intruders. The results leading to this effect exclusively involved a single subordinate female in one group who attacked three intruding dominant females.
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DISCUSSION |
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TOPABSTRACTINTRODUCTIONMETHODSRESULTSDISCUSSIONREFERENCES |
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Attacks on intruders to mole-rat colonies were carried out almost exclusively by dominant individuals, who primarily attacked intruders of the same sex. Subordinate mole-rats typically played no role at all in the defense of their colonies against intrusion by foreign mole-rats. The leading role of reproductives in attacking intruders resembles the response of colonies of the social wasp Polistes fuscatus, in which the queen is typically the most aggressive or among the most aggressive of attackers (Fishwild and Gamboa, 1992
;
Judd, 2000). However, the
reticence of subordinates contrasts sharply with the behavior of naked
mole-rats, in which subordinates typically play the dominant role in colony
defense, and breeders play only a minor role
(Lacey and Sherman, 1991;
O'Riain and Jarvis, 1997).
Why does this variation exist between two species inhabiting a similar
environment and demonstrating a superficially similar social system? The
results presented here indicate that kin or colony-level selection on
subordinates has not led to their willingness to defend the colony. In
contrast, they strongly suggest that Damaraland mole-rats defend burrows
primarily to defend their breeding status against potential competitors. If
defense in both species was related to defending breeding status, this
divergence would be expected. Subordinate Damaraland mole-rats are typically
prevented by inbreeding avoidance from breeding in their natal burrow
(Cooney and Bennett, 2000),
gaining breeding opportunities primarily by dispersing from their natal colony
(Jarvis et al., 1994). They
thus have little direct incentive to participate in risky defense. The
solicitation of foreign males by defending subordinate females in this study
suggests that rather than a threat, conspecific intrusion may even represent
contact with potential mates. In contrast, naked mole-rats habitually recruit
new breeders from within colonies, and inheritance of the breeding position in
the natal colony represents the main chance of reproduction
(O'Riain and Jarvis 1997; but
see also Braude, 2000). The
payoff for successfully attaining the breeding position may be immense
(Jarvis et al., 1991),
providing an incentive for even costly defense
(O'Riain and Jarvis,
1997).
Two further differences between the species are likely to reduce benefits
to be gained by subordinates through defense against intruders. First,
dispersal is less constrained in Damaraland mole-rats
(Jarvis et al., 1994). Food
resources are less dispersed and rainfall is less variable, two factors that
have been demonstrated to drive sociality in African mole-rats
(Faulkes et al., 1997;
Spinks et al., 2000). This may
reduce the comparative value of the natal burrow resource to Damaraland
mole-rats, giving them less incentive to indulge in risky defense activities.
Second, kin-selected benefits derived from protecting the integrity of the
colony and breeder reproduction probably represent a greater increment of
total potential fitness to subordinate naked mole-rats. In naked mole-rats the
chances of independent reproduction are considerably lower than in Damaraland
mole-rats (naked mole-rats: 0.1%, n > 4000; Damaraland mole-rats
8%, n > 403; Jarvis et al.,
1994), providing a greater incentive to sacrifice current direct
fitness. Likewise, in Polistes fuscata, where reproductives play a
dominant role in defense, it has been suggested that the relative reluctance
of workers to defend colonies reflects their opportunities for direct
reproduction elsewhere (Judd,
2000).
Recent studies of cooperative breeding in a variety of vertebrate taxa
illustrate the importance of direct benefits in shaping cooperative strategies
(Balshine-Earn et al., 1998;
Clutton-Brock et al., 1999,
2000,
in press;
Cockburn, 1998). Here I showed
that colony defense in Damaraland mole-rats is likely to primarily reflect
defense of breeding status and that subordinates only rarely take part,
despite potential kin-selected benefits. It seems clear that even in closely
related and superficially highly cooperative groups, kin selection cannot be
assumed to drive the evolution of costly cooperative strategies.
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ACKNOWLEDGEMENTS |
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I gratefully acknowledge the help of Nigel Bennett with mole-rat with care and maintenance of mole-rat colonies, of Marietjie Oosterhuizen with experiments and animal care, and of Pete Brotherton, Tim Clutton-Brock, and Ruth Waldick for discussion and comments. I was supported by a Commonwealth scholarship during this work.
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