Does the time spent near a male predict female mate choice in a Malawian cichlid?
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1 Journal of Fish Biology (2001) 59, doi: /jfbi , available online at on Does the time spent near a male predict female mate choice in a Malawian cichlid? V. C. K. COULDRIDGE* AND G. J. ALEXANDER Reptile Thermal Biology and Energetics Research Programme, Ecophysiological Studies Research Group, School of Animal, Plant and Environmental Sciences, University of the Witwatersrand, Private Bag 3, WITS 2050, South Africa (Received 20 December 2000, Accepted 1 June 2001) Gravid female Malawian Pseudotropheus cichlids spent significantly more time with males that they subsequently chose as mates, indicating that time spent near a male is a valid and accurate method of measuring female preference. Furthermore, females preferred to mate with males that had longer pelvic fins and a larger number of eggspots on their anal fins. In some instances, females chose to mate with both of the males with which they were presented, possibly because they were unable to discriminate between them The Fisheries Society of the British Isles Key words: cichlid; Lake Malawi; mate choice; Pseudotropheus; sexual selection. INTRODUCTION Female mate choice is consummated by mating (Darwin, 1871; Ryan & Rand, 1993; Andersson, 1994), and so successful matings are the most direct measure of this choice. However, female mate choice is difficult to measure directly, since matings in many species are infrequent or rapid (Alcock, 1993). Therefore, they are not easily quantified or recorded and may not be repeatable. Female mate choice is therefore often measured indirectly. Indirect measurements include various forms of preference such as the amount of time a female spends with a male, or various female behavioural responses to males. The time spent with a male is easy to measure, but suffers from a lack of credibility unless it can be shown explicitly that it does, in fact, faithfully predict mating; female activities possibly may be misinterpreted by the observer and may not actually represent sexual preferences. Females may also evaluate different male characters at different stages during courtship (Wilczynski & Ryan, 1992; Wiegmann et al., 1996). Therefore, an essential prerequisite of studies using indirect measures of female preference is to validate any indirect measures that are used to determine female choice. The present study attempts to verify that the measure of time spent near a male is indeed a good predictor of a female s choice in a species of Malawian cichlid. This validation experiment is a crucial precursor to several other female choice experiments, which have been performed by the authors on this species and three other closely related species of Pseudotropheus Regan (Couldridge & *Author to whom correspondence should be addressed. Tel.: ; fax: ; Vanessa@gecko.biol.wits.ac.za /01/ $35.00/ The Fisheries Society of the British Isles
2 668 V. C. K. COULDRIDGE AND G. J. ALEXANDER Glass partition Glass partition Male Choice zone Female Choice zone Male 385 mm 150 mm 150 mm 325 mm 900 mm FIG. 1. Diagram of the choice tank. Alexander, 2001). Are male characters correlated with female choice? This is tested to demonstrate explicitly that the choice was based explicitly on the male s characteristics and was not arbitrary. Time spent with a male, rather than courtship behaviour was used as a proximate method of female preference. The reason for this choice was that, among the polygynous Mbuna (rock-dwelling cichlids) of Lake Malawi, male courtship behaviour lacks a well defined structure or organization; it may even be an evolutionary relict or be maintained due to pleiotropic effects, serving no direct function (McElroy & Kornfield, 1990). Furthermore, females do not respond to male courtship displays with set behaviour as has been reported in a monogamous South American cichlid species (Barlow et al., 1990). MATERIALS AND METHODS The cichlids used in the experiment were classified as Pseudotropheus (Metriaclima) zebra (Boulenger) red dorsal, although they have recently been reclassified as three separate species (Stauffer et al., 1997). The geographic origin of the laboratory bred population is uncertain (originally acquired from the local pet trade suppliers). Water temperature was maintained at 27 C throughout and the photoperiod was 12L : 12D. All males were sexually mature and previously mated and were housed separately from each other to avoid the establishment of dominance hierarchies. The females were the same age as the males (12 14 months old), were sexually mature, and each was gravid at the time of her trial. Gravid females were recognized on the basis of a swollen urogenital pore. Choice trials were conducted in an aquarium ( mm; 100 l), the ends of which were partitioned off with glass (Fig. 1). A terracotta plant pot was placed on its side in each of the two end partitions to act as the focal point of a territory for each male, and two heaters were placed in the central enclosure, one next to each of the glass partitions so as not to bias the female towards one side. A 20 mm layer of light brown gravel covered the bottom of the aquarium. Fifteen trials were conducted in which the mating preferences of 15 gravid females were tested. In each trial, the female was given a choice between two males. Males were used
3 CICHLID MATE CHOICE 669 in more than one trial, but were paired with a different male each time that they were re-used so that each female was presented with a different combination of males. Once a gravid female had been identified, she was removed from the stock tank and placed in the centre compartment of the test aquarium. Two males were then introduced, one in each of the two end compartments, on either side of the female (Fig. 1). The fish were left for a minimum period of 5 h to acclimate to their surroundings. The female was then observed for 20 min, and the time that the female spent within 150 mm of each male s enclosure was recorded. The fish were then left in the choice tank and were checked every hour during the day until the female had laid her eggs (usually within 2 days from the start of the trial) in order to observe which male the female had attempted to mate with. Males had to be kept physically isolated from each other in separate enclosures to avoid aggressive encounters and interference competition which could have influenced female choice and also led to injury. This meant that the attempted mating took place without any physical contact possible between the male and the female, and the eggs remained unfertilized. Females always excavated a spawning pit next to the glass partition of the enclosure of the male that they chose as a mate. The pair then attempted to mate through the glass barrier with the female picking up the eggs in her mouth in the usual manner (Baerends & Baerends-van Roon, 1950). If the female chose to mate with both males, she dug two spawning pits, one at either end of the tank. In these instances, it was not possible to ascertain what proportion of her brood the female laid with each of the two males. The entire spawning was not always observed, but the presence of either one or two spawning pits verified whether the female had selected only one male or both, and the presence of eggs in the females mouth verified that mating had been attempted. At the end of each trial, various male characters were quantified. The number of eggspots on the anal fin were counted and body size (total length, L T ), fin lengths and asymmetry of the pelvic fins were measured. Paired fins were averaged for the left and right fin and all fin measurements were divided by L T, resulting in a relative measure. As the data did not always conform to a normal distribution, only non-parametric tests were used. For the trials where females attempted to mate with only one of the males, a Wilcoxon signed rank test for two dependent samples was used to test for a difference between the amount of time females spent with each male. A Mann Whitney U-test for two independent samples was used to test whether the difference in the amount of time females spent with the two males in cases where only one was chosen as a mate, was greater than the difference in the amount of time females spent with the two males where both were chosen as mates. A Wilcoxon signed rank test was also used to analyse differences in eggspot number and pelvic fin length, firstly between winning and losing males in the clear winner category, and secondly between more preferred and less preferred males (based on time spent with a male) where both males were chosen as mates. A 5% level of significance was used in all tests and sequential Bonferroni readjustments (Rice, 1989) were applied to correct for multiple tests. RESULTS In cases where the female attempted to mate with only one of the two males, the females spent a significantly greater amount of time (z= 2 666; n=9; P=0 008) with the winner (preferred male for mating) than with the loser (less preferred male) (Table I). Furthermore, the difference in the amount of time that females spent with the winner and the loser (Table I) was significantly greater (U=52 000; n=15; P=0 003) than the difference in the amount of time that females spent with the two males when both were chosen (Table I). In the trials in which females attempted to mate with only one male, the winner had a significantly greater number of eggspots in comparison to the loser
4 670 V. C. K. COULDRIDGE AND G. J. ALEXANDER TABLE I. Time (% of total) spent by females with each of the two males, total male eggspot number and male pelvic fin length as a proportion of L T. Median (minimum and maximum) values Test variable Mate choice Preferred male Less preferred male Difference Time near male One male chosen ( ) ( ) ( ) Both males chosen ( ) ( ) ( ) Total ( ) ( ) ( ) Number of eggspots One male chosen (4 11) (3 8) (1 8) Both males chosen (8 11) (3 11) ( 3 8) Total (4 11) (3 11) ( 3 8) Pelvic fin length One male chosen ( ) ( ) ( ) Both males chosen ( ) ( ) ( ) Total ( ) ( ) ( ) (z= 2 670; n=9; P=0 008) as well as significantly longer pelvic fins (z= 2 429; n=9; P=0 015). However, in cases where females attempted to mate with both males, the males with which she spent most time with did not have significantly more eggspots (z= 1 787; n=6; P=0 074) or longer pelvic fins (z= 1 557; n=6; P=0 115) than the males with which the females spent less time. None of the other male characters were correlated with female preference. DISCUSSION The amount of time that a female spent with males was a good predictor of which male she subsequently chose as a mate. In every one of the nine cases where the female chose a single male, she spent more time with that male than she did with the loser. Thus, not only is there a congruence between the indirect time spent and mate choice, the indirect measure is an accurate predictor of that choice. In cases where the female did not make a clear choice and attempted to mate with both males, this uncertainty was mirrored in the indirect measure by females spending time more equally between the males. This is probably the first time that an indirect measure of mate choice has been explicitly validated in a cichlid species although it has been used previously (Barlow et al., 1990; Balshine-Earn, 1996). Time spent in close proximity to an individual has also been used as a preference measure in studies conducted on
5 CICHLID MATE CHOICE 671 other species of fishes, such as the pipefish Nerophis ophidon (L.) (Rosenqvist, 1990) and the sand goby Pomatoschistus minutes (Pallas) (Forsgren, 1992) and has been validated in these species. Males with longer pelvic fins and a larger number of eggspots were found to be more successful at attracting mates in the present study. The effect of eggspot number on female choice has been previously documented in Pseudotropheus aurora Burgess (Hert, 1991), a species closely related to P. zebra, and in Astatotilapia elegans Trewavas, a cichlid species that is endemic to Lake George and Lake Edward (Hert, 1989). Female preference for long pelvic fins has only been recorded in Cyathopharynx furcifer (Boulenger) from Lake Tanganyika (Karino, 1997). Six out of 15 females chose to mate with both of the available males. However, there was no way to ascertain the proportion of eggs that each of the two males would have fertilized: fertilization was prevented, the number of eggs laid by the female on each occasion could not be counted and even when egg laying was observed, it was not possible to ascertain if more eggs were laid while the fish were not viewed. It is possible that, at least in some instances, the female laid more eggs with one of the two males, and this unmeasured variation of her choice could explain cases where time spent between males was unequal but the female mated with both males. The present result of multiple matings for females supports Parker & Kornfield s (1996) findings of multiple matings in P. zebra. However, it could have been an artefact of the experimental design: possibly females only appeared to choose two males because the first mating attempt had failed as a result of the glass barrier and, under more natural circumstances, the female would have chosen only one male. This is probably unlikely as females appeared to select males on the basis of pelvic fin length and eggspot number and mated with both males only when they were similar in these characters. Parker & Kornfield (1996) found that in P. zebra, each brood of young that a female produced was sired by an average of 3 8 males, and suggested that females may multiple mate either to avoid inbreeding (Stockley et al., 1993) or as a bet-hedging strategy involving some male character that they are unable to evaluate, such as fertility (Sheldon, 1994; Jennions & Petrie, 2000). Although multiple paternity is common in Mbuna species, including Pseudotropheus (Kellogg et al., 1995; Parker & Kornfield, 1996), it is not certain whether this is due only to females choosing to mate with more than one male or whether parasitic spawning also plays a role. Ethical clearance for this study was obtained from the University of the Witwatersrand Animal Ethics Screening Committee (clearance certificate number 99/30/1). Funding for the project came from a Prestigious Masters Scholarship from the National Research Foundation and from the University Research Committee of the University of the Witwatersrand. References Alcock, J. (1993). Animal Behavior. Sunderland, MA: Sinauer Associates. Andersson, M.B. (1994). Sexual Selection. Princeton, NJ: Princeton University Press.
6 672 V. C. K. COULDRIDGE AND G. J. ALEXANDER Baerends, G. P. & Baerends-van Roon, J. M. (1950). An introduction to the study of the ethology of cichlid fishes. Behaviour (Suppl.) 1, Balshine-Earn, S. (1996). Reproductive rates, operational sex ratios and mate choice in St. Peter s fish. Behavioural Ecology and Sociobiology 39, Barlow, G. W., Francis, R. C. & Baumgartner, J. V. (1990). Do the colours of parents, companions and self influence assortative mating in the polychromatic Midas cichlid? Animal Behaviour 40, Couldridge, V. C. K. & Alexander, G. J. (2001). Colour patterns and species recognition in four closely related species of Lake Malawi cichlids. Behavioral Ecology, in press. Darwin, C. (1871). The Descent of Man and Selection in Relation to Sex. New York: The Modern Library, Random House. Forsgren, E. (1992). Predation risk affects mate choice in a gobiid fish. The American Naturalist 140, Hert, E. (1989). The function of eggspots in an African mouth-brooding cichlid fish. Animal Behaviour 37, Hert, E. (1991). Female choice based on eggspots in Pseudotropheus aurora Burgess 1976, a rock-dwelling cichlid of Lake Malawi, Africa. Journal of Fish Biology 38, Jennions, M. D. & Petrie, M. (2000). Why do females mate multiply? A review of the genetic benefits. Biological Reviews of the Cambridge Philosophical Society 75, Karino, K. (1997). Female preference for males having long and symmetric fins in the bower-holding cichlid Cyathopharynx furcifer. Ethology 103, Kellogg, K. A., Markert, J. A., Stauffer, J. R. Jr & Kocher, T. D. (1995). Microsatellite variation demonstrates multiple paternity in lekking cichlid fishes from Lake Malawi, Africa. Proceedings of the Royal Society of London: Series B 260, McElroy, D. M. & Kornfield, I. (1990). Sexual selection, reproductive behaviour, and speciation in the mbuna species flock of Lake Malawi (Pisces: Cichlidae). Environmental Biology of Fishes 28, Parker, A. & Kornfield, I. (1996). Polygynandry in Pseudotropheus zebra, a cichlid fish from Lake Malawi. Environmental Biology of Fishes 47, Rice, W. R. (1989). Analysing tables of statistical tests. Evolution 43, Rosenqvist, G. (1990). Male mate choice and female-female competition for mates in the pipefish Nerophis ophidon. Animal Behaviour 39, Ryan, M. J. & Rand, A. S. (1993). Species recognition and sexual selection as a unitary problem in animal communication. Evolution 47, Sheldon, B. C. (1994). Male phenotype, fertility, and the pursuit of extra-pair copulations by female birds. Proceedings of the Royal Society of London: Series B 257, Stauffer, J. R. Jr, Bowers, N. J., Kellogg, K. A. & McKaye, K. R. (1997). A revision of the blue-black Pseudotropheus zebra (Teleostei: Cichlidae) complex from Lake Malawi, Africa, with a description of a new genus and ten new species. Proceedings of the Academy of Natural Sciences of Philadelphia 148, Stockley, P., Searle, J. B., MacDonald, D. W. & Jones, C. S. (1993). Female multiple mating behaviour in the common shrew as a strategy to reduce inbreeding. Proceedings of the Royal Society of London: Series B 254, Wiegmann, D. D., Real, L. A., Capone, T. A. & Ellner, S. (1996). Some distinguishing features of models of search behaviour and mate choice. The American Naturalist 147, Wilczynski, W. & Ryan, M. J. (1992). Introduction to the symposium: mechanisms of mate choice. American Zoologist 32,
Received: 16 January 2003 / Revised: 5 March 2003 / Accepted: 14 March 2003 / Published online: 18 September 2003 Springer-Verlag and ISPA 2003
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