Mate assessment in a cockroach, Nauphoeta cinerea

Anim. Behav., 1986, 34, 1160-1165

M a t e assessment in a cockroach, Nauphoeta cinerea A L L E N J. M O O R E & M I C H A E L D. B R E E D

Department of Environmental, Population, and Organismic Biology, Campus Box 334, The University of Colorado, Boulder, Colorado, 80309 U.S.A.

Abstract. The behavioural effects of assessment of male dominance status on male and female courtship

were investigated in the cockroach, Nauphoeta cinerea. Dominance hierarchies were established in laboratory groups of male N. cinerea; virgin females were then given the opportunity to (1) mate with a subordinate male in the presence of dominant male odours; (2) mate with a dominant male in the presence of subordinate male odours; (3) mate with a male in the presence of another male's odour, both males lacking status; (4) mate when only a single male was present and no other male's odour was presented. The presence of the dominant male resulted in a significant delay in the approach of a female to a subordinate male and in the response of a female to a courtship display by the subordinate male. Males that lacked status were significantly slower to initiate courtship behaviours. Copulatory time was significantlyshorter for subordinate males and males without status. Information concerning the dominance status of neighbouring males is used in assessment of appropriate mating behaviour by males and as a possible criterion in female choice.

When resources are limited (e.g. mates, food, territories), individuals typically compete for access to these resources. Competitors often engage in agonistic encounters; contests may vary in intensity and duration depending on the probability of winning (Parker 1974; Maynard Smith & Parker 1976) and the quality of resources (Riechert 1984). Because the payoffor probability of winning varies, not all encounters result in agonistic behaviours (West-Eberhard 1979). Rather, assessment of opponents may lead to termination of interactions without escalation. In many species, there is competition among males for mates. Theoretically, fights to the death should occur only when no other reproductive option exists (Parker 1974; West-Eberhard 1979). If reproductive options exist, i.e. mating opportunities despite defeats in interactions with other males, it is advantageous to avoid escalation to fights with the potential for physical injury (Thornhill 1984). Thus, contestants for mates should be able to assess asymmetries related to fighting ability and act accordingly (Parker 1974; Riechert 1984). Females may also assess males and exert female choice. A female may assess a direct attribute of the male such as body size (Thornhil11983), or she may consider the quality or quantity of male possessions (Thornhill 1979). Alternatively, she may assess an attribute of the male that is correlated with resources or traits that are of value to the female or her offspring (Borgia 1979; Thornhill 1980), such as

dominance status (Thornhill & Alcock 1983; Borgia 1985; Borgia et al. 1985). The purpose of this study was to test the ability of males and females to use cues associated with male dominance status in assessment during courtship and mating. A cockroach, Nauphoeta cinerea, was chosen as the study animal, because this species establishes strict linear dominance hierarchies (Ewing 1972, 1973; Bell & Gorton 1978; Schal & Bell 1983). Dominant males of this species have a higher probability of mating than do lower ranking males (Breed et al. 1980). Females are preferentially attracted to dominant male odours (Breed et al. 1980), and males are able to discriminate between dominant and subordinate individuals on the basis of odours (Smith & Breed 1982). The ability to assess the relative status of males is important to N. cinerea males since the dominance hierarchy may function to decrease interference by conspecifics (Ewing 1973; Schal & Bell 1983). Underestimation of their position in the hierarchy by males may lead to the loss of mating opportunities. Fights with higher ranking individuals may result in injuries such as the loss of antennae and legs, which lead to permanent subordinate status (Schal & Bell 1983). Female N. cinerea may be selected to be able to differentially perceive males of different status since dominant and subordinate males occur together (Ewing 1973; Smith & Breed 1982). We predict that both male and female N. cinerea cockroaches use cues associated with male

1160

Moore & Breed. Mate assessment status in the assessment of mates, and alter their courtship and mating behaviour based on available cues. Similar results were found in a related cockroach, Gromphadorhina portentosa (Leibensperger 1984).

MATERIALS AND METHODS Four experimental treatments were designed to measure the influence of the presence of a second conspecific male on the behaviour of an interacting male and female (see Results for a detailed description of courtship and copulation in N. cinerea). Only interactions that resulted in copulation were analysed since this study restricts itself to the question of how courtship which leads to copulation may be affected. If the presence of a second male affects mating behaviour, it should delay some aspects of courtship and copulation because of the time necessary for assessment of the additional cues present. Three behavioural acts which are apparently under female control were timed: latency to initiation of contact with a male, latency from male display to female response, and the length of courtship, which began when the female approached the male and ended when the female climbed on the male's back. Two behavioural acts under male control were timed: latency to initiation of display and length of copulation (Roth 1964). The treatments were as follows. (1) Single female plus a single male (control). A single virgin adult female and a single male were placed in an observation arena. The male had been housed in social isolation for 7-14 days prior to the test. Behavioural observations were made under red lamps, which emit wavelengths that are imperceptible to cockroaches (Bell & Sams 1973). (2) Single female plus two males that had no previous interactions: one male restrained. Males were maintained in social isolation for 6-14 days. As a result of being raised alone, they lacked dominance status relative to one another. One male was placed in a 4 • 7.5 x 4-cm wire mesh cage to prevent social interaction, while the other was free to move about the arena. Restraint in this manner allows continued perception by the free male and the female of olfactory and auditory cues produced by the restrained animal. This treatment simulated the case in which relative status is unknown. (3) A single female plus two males that had previously interacted and established a dominance

1161

relationship: subordinate male restrained. The dominant male was free to move about the arena. This experiment was conducted identically to treatment 2, with the exception that the dominance status of the free and restrained males had been determined (see below). The observer did not know the relative status of the free or the restrained male. (4) A single female plus two males that had previously interacted and established a dominance relationship: dominant male restrained. The subordinate male was unrestricted in its movements about the arena. This experiment was conducted as described for treatment 3. Prior to tests 1 and 2, individual adult males were placed in separate 0'455-1itre containers and maintained at 25-27~ under 12:12 h L : D photocycle. Food (rat chow) and water were provided ad libitum. The formation of dominance hierarchies was necessary for tests 3 and 4. These males were treated as follows. Cockroaches were randomly selected from stock colonies maintained at the University of Colorado, Boulder. Four males were placed together in a 27 x 15 x 13-cm Plexiglas cage with a Plexiglas cover (cages of the same size were used for the mating arenas). The males were then allowed to interact for 7-14 days under the environmental conditions described for tests 1 and 2 with minimal disturbances. Then, each group was observed for 1 h and the rates of agonistic encounters were recorded. Males were ranked following the description of Bell & Gorton (1978). Only the most dominant and least dominant males were used in further tests. Males had been isolated from females for at least 2 weeks, ensuring no recent matings and thus sufficient, complete spermatophores (Roth 1964). Female N. cinerea (in all four tests) were selected in the last-instar nymph stage and allowed to mature to adulthood in 0.455-1itre containers. This ensured that all females used were virgins and thus potentially receptive. Food and water were provided as above. The date at which females moulted to the adult stage was recorded for each individual. Females were at least 6 days post-adult moult when used experimentally, ensuring their receptivity to males (Roth 1964). Data were analysed statistically utilizing ANOVA. Raw data were log transformed to correct for possible heterogeneity of variances. Other assumptions such as independence of errors, random sampling, and normal distribution of data were either met or corrected for by this transforma-

Animal Behaviour, 34, 4

1162

Table I. Female responses to male courtship

One male

Two males, Two males, Two males, lacking dominant subordinate status male free male free

F ratio

P

Time before female 30.3_+9.3 54.8_+16.2 46.1_+10.8 110.7"_+20.7 5-91 < 0'002 approaches male (s) 16.41 <0.001 11.7"• Time from male display 4.2 + 0.9 6.6_+2.9 4.4_+0.9 to femaleresponse (s) 29.4_+7'6 1.69 NSt Duration of entire 56.8_+ 16.4 77.9_+26.0 22.1_+6.4 male courtship (s) 15 N 18 15 15 All data given as mean -+SE. * Mean is significantlygreater (P < 0.05), Scheffe's a posterior• test. t P > 0.05. tion (Sokal & Rohlf 1981). No male or female was used in more than one test, and all tests were performed blind or with randomly selected individuals. RESULTS

Courtship and Copulation In Nauphoeta cinerea, females are pheromonally attracted to males (Roth & Dateo 1966). When the female comes into contact with the male, he performs a characteristic display, wing-raising (WR), in which he raises his wings while facing away from the female. The female invariably climbs on top of the male's abdomen while his wings are raised and then feeds on a substance released from his exposed tergites (Roth 1964). The male then backs up and probes the female's abdomen with the tip of his abdomen. If the female chooses to copulate she allows the male to grasp her with his left phallomere (a grasping device associated with the male genitalia); if she rejects the copulation attempt she backs away from the male and prevents phallomere contact (personal observation). Copulation is terminated by male release of the female (Roth 1962, personal observation). Females sometimes attempt to pull away from the male prior to release; they are always unsuccessful and there is no significant difference between the length of copulation when the female attempts to pull away (N=34, J(=572.40 s, SE=16-10) and when she remains quiescent ( N = 29, ) ( = 568.10 s, SE=12'35; t=0-21, df=61, P>0-5, NS). Once a female has copulated, she is no longer receptive or

responsive to males until after parturition (N= 10, J?=39.5 days, sE= 1.49 under these laboratory conditions).

Female Behaviour From the above description, it is clear that a female can affect successful courtships in at least three distinct places during the sequence; she may vary (1) the amount of time before the male is approached, (2) the amount of time before she responds to wing-raising by the male, or (3) she may delay the beginning of copulation by rejecting the male's advances. All three acts were timed and analysed. The number of seconds before a female approached an unrestrained male differed significantly among the experimental conditions ( F = 5.91, dr=3, 62, P<0.002, Table I), as did her response to his courtship display ( F = 16.41, df= 3, 62, P < 0.001, Table I). The mean time of approach by the female and female response to courtship when the dominant male was caged and the subordinate was free is significantly greater than the other three mean times for both types of behaviour (Scheffe's a posteriori test, P<0.05). The mean length of courtship was similarly analysed for all four experimental conditions but in this case the ANOVA was not significant ( F = 1-69, dr= 3, 62, P > 0" 1, Table I).

Male Behaviour Males influenced the temporal structure of matings in two ways. First, males varied the length of

Moore & Breed: Mate assessment

1163

Table II. Male courtship acts

One male Time from approach to 21.2+4.9 initiation of courtship (s) Length of copulation (s) 611.3"_+26.7 N 18

Two males, lacking status 68.3+20.3 526.6+19.6 15

Two males, dominant male free 7.7+2.l

Two males, subordinate male free

F ratio

19.7+ 10.7

6.94

<0.001

2.85

<0.05

589.9*_+8.9 545-9-+11.3 15 15

All data given as mean__+s~. * Mean is significantly greater (P < 0.05), Scheffe's a posteriori test.

time before they responded to a female approach. Alternatively, they determined the length of copulations because the male must release the female for copulations to cease. The time from female contact to male initiation of courtship and the copulation time were analysed in the same manner as the female behaviour. There was a significant difference among the treatments in the mean length of time before a male began his wing-raising display ( F = 6.94, df= 3, 62, P < 0.001, Table II). The treatment in which two males with no dominance status were present had a significantly longer time to initiation of courtship than the other three treatments (Scheffe's a posteriori test, P < 0 . 0 5 ) . A male alone or a dominant male with a subordinate restrained in the same cage engaged in significantly longer copulation than did a male with no status or a subordinate male in the presence of a restrained dominant ( F = 2.85, df= 3, 62, P < 0.05, Table II; Scheffe's a posteriori test, P < 0.05). There was no significant difference between either the lone male plus the dominant male or the subordinate male plus the male with no status.

DISCUSSION

Female Behaviour

Our data show that females are unlikely to approach a subordinate male immediately when higher ranking males are present. They will approach a dominant male in a group of males, a male without status, or a single male relatively quickly. Once near a subordinate male, females do not respond to his visual display (WR) as quickly as they respond to any other male's W R display.

These findings, along with previous reports that dominant males mate more frequently than subordinate males (Breed et al. 1980; Schal & Bell 1983), suggest female choice. The present results are consistent with previous experiments implicating female choice in N. einerea. Breed et al. (1980) demonstrated that females of this species have the ability to perceive the dominance status of males. When presented with a choice between the odour of a dominant male and a subordinate male they oriented to the dominant male's odour. This finding supports the idea that females are choosing between males based on dominance status. If this is true, then females might be expected to structure their behaviour based on the status of the males with whom they have the possibility of mating. An alternative view is that dominance may not be the only criterion used by females to judge males. If some element of courtship is used in assessment it might be expected that females would delay their response to a male's initial behaviour. Similarly, a female might be expected to affect the length of courtship if males that are able to court longer are demonstrating superior genetic quality. In this species, the first remains a possibility although the use of dominance alone as a criterion is not ruled out. The second argument does not seem to apply, as we found no significant difference among treatment groups with respect to the length of male courtship. Once the female responds to WR, courtship proceeds stereotypically to copulation. The data presented do not allow us to clearly distinguish between female assessment and simple differential attraction (Parker 1983). Dominant males may produce more sex pheromone and consequently be more attractive; approaching a

l 164

Animal Behaviour, 34,4

male may be a function of increased perception and therefore not a mechanism used in active female choice (Breed et al. 1980; Parker 1983). If this is so, then males without dominance status must be producing the same levels of sex pheromone as dominant males, because they are approached as readily. In such a system females are not actively exerting a choice; rather, they passively affect which male mates. Since females do not respond as quickly to subordinate male WR, active choice at this point remains a possibility, although the delay in response may also be due to reduced pheromone levels. Active female choice does exist in a number of other species (see Thornhill & Alcock 1983; Bateson 1983, and references therein). In N. cinerea, the net result of female behaviour is that they preferentially mate with dominant males when such males are available. Further tests will be necessary to differentiate between active choice and differential attraction.

Finally, the length of copulation varies among mating pairs. Subordinate males and males without relative status have shorter copulations than do dominant or single males. It seems likely that a shorter period of copulation by these males is a means of minimizing interference, if the interference model presented above is correct. Alternatively, the males who mate longer may be passing more sperm or nutrients to the female, thereby increasing her fecundity. At this point we can only speculate on the possible benefits of this behaviour.

ACKNOWLEDGMENTS We thank Heather Haldane for her help in determining male rank. We are grateful to J. Harrison Fewell, J. Harrison, T. Johnston Moore, J. Karron, T. Stiller, and especially M. Bekoff, B. Bennett and an anonymous referee for m a n y helpful criticisms of the manuscript.

Male Behaviour The courtship behaviour of a male is dependent on the presence and status of conspecific males. Because the only variables are the presence and status of a nearby male, any behavioural differences found between males are due to these variables. Thus, males seem to be able to perceive the presence of other males, the relative status among them, and act accordingly. When two males are present, a lack of interference by the other male may be the cue to begin courtship (Schal & Bell 1983; Moore, personal observation). Interference does occur when two unrestrained males are present. Males attack and attempt to dislodge copulating and courting individuals. Subordinate males and males without relative status are more likely to be disrupted than are dominant males (Schal & Bell 1983). The results of our experiments suggest that an individual's dominance status alone does not determine his behaviour when presented with mating opportunities. Subordinate males can and do mate as readily as dominant males. The status and behaviour of adjacent males seems to interact with the status of the individual in determining courtship behaviour. Males may assess the possibility of interference during mating attempts. Males may also use female behaviour (such as being approached) to help assess the probability of interference.

REFERENCES Bateson, P. (Ed.) 1983. Mate Choice. Cambridge: Cambridge University Press, Bell, W. J. & Gorton, R. E. 1978. Informational analysis of agonistic behaviour and dominance hierarchy formation in a cockroach, Nauphoeta cinerea. Behaviour, 67, 217-235. Bell, W. J. & Sams, G. R. 1973. Aggressiveness in the cockroach Periplaneta americana. Behav. Biol., 9, 581 593. Borgia, G. 1979. Sexual selection and the evolution of mating systems. In: Sexual Selection and Reproductive Competition in Insects (Ed. by M. S. Blum & N. A. Blum), pp. 19-80. New York: Academic Press. Borgia, G. 1985. Bower decorations and mating success of male satin bowerbirds. Anita. Behav., 33, 266 271. Borgia, G., Pruett-Jones, S. G. & Pruett-Jones, M. A. 1985. The evolution of bower-building and the assessment of male quality. Z, Tierpsyehol., 67, 225-236. Breed, M. D., Smith, S. K. & Gall, B. G. 1980. Systems of mate selection in a cockroach species with male dominance hierarchies. Anim. Behav., 28, 130-134. Ewing, L. S. 1972. Hierarchy and its relation to territory in the cockroach Nauphoeta cinerea. Behaviour, 42, 152-173. Ewing, L. S. 1973. Territoriality and the influence of females on the spacing of males in the cockroach, Nauphoeta cinerea. Behaviour, 45, 281 304. Leibensperger, L. B. 1984. Cues utilized during mate choice by female Gromphadorhina portentosa. M.A. thesis, Boston University. Maynard Smith, J. & Parker, G. A. 1976. The logic of asymmetric contests. Anita. Behav., 24, 159-175. Parker, G. A. 1974. Assessment strategy and the evolution of animal conflicts. J. theor. Biol., 47, 223-243.

M o o r e & Breed: M a t e assessment Parker, G. A. 1983. Mate quality and mating decisions. In: Mate Choice (Ed. by P. Bateson), pp. 141-164. Cambridge: Cambridge University Press. Riechert, S. E. 1984. Games spiders play. III: Cues underlying context associated changes in agonistic behaviour. Anim. Behav., 32, 1 15. Roth, L. M. 1962. Hypersexual activity induced in females of the cockroach Nauphoeta cinerea. Science, N.Y., 138, 126% 1269. Roth, L. M. 1964. Control of reproduction in female cockroaches with special reference to Nauphoeta cinerea: I. First pre-oviposition period. J. Insect Physiol., 10, 915 945. Roth, L. M. & Dateo, G. P. 1966. A sex pheromone produced by males of the cockroach Nauphoeta cinerea. J. Insect Physiol., 122, 255-265. Schal, C. & Bell, W. J. 1983. Determinants of dominantsubordinate interactions in males of the cockroach Nauphoeta einerea. Biol. Behav., 8, 117 139. Smith, S. K. & Breed, M. D. 1982. Olfactory cues in discriminations among individuals in dominance hierarchies in the cockroach, Nauphoeta cinerea. Physiol. Entomot., 7, 337~ 341. Sokal, R. R. & Rohlf, F. J. 1981. Biomet~y. San Francisco: W. H. Freeman.

1165

Thornhill, R. 1979. Male and female sexual selection and the evolution of mating strategies in insects. In: Sexual Selection and Reproductive Competition in Insects (Ed. by M. S. Blum & N. A. Blum), pp. 81-121. New York: Academic Press. Thornhill, R. 1980. Competitive, charming males and choosy females: was Darwin correct? Fla Entomol., 63, 5-29. Thornhill, R. 1983. Cryptic female choice and its implications in the scorpionfly Harpobittacus nigriceps. Am. Nat., 122, 765-788. Thornhill, R. 1984. Fighting and assessment in Harpobittacus scorpionflies. Evolution, 38, 204-214. Thornhill, R. & Alcock, J. 1983. The Evolution of Insect Mating Systems. Cambridge, Mass.: Harvard University Press. West-Eberhard, M. J. 1979. Sexual selection, social competition, and evolution. Proc. Am. Phil. Soc., 123, 222-234.

(Received 22 May 1985," revised 22 July 1985," MS. number: A4484)