Interspecific attractiveness of structures built by courting male fiddler crabs: experimental evidence of a sensory trap

Male fiddler crabs Uca musica sometimes build sand hoods and male Uca beebei sometimes build mud pillars next to their burrows to which they attract females for mating. Mate-searching females preferentially approach these structures and subsequently mate with structure builders. Here we show that the preference for structures is not species-specific and argue that it may not have evolved for mate choice. When not near burrows, many species of fiddler crabs approach and temporarily hide near objects, suggesting that hoods and pillars may attract females because they elicit this general predator-avoidance behavior. To test this sensory trap hypothesis we individually released female U. musica, U. beebei and Uca stenodactylus, a non-builder, in the center of a circular array of empty burrows to which we added hoods and pillars and then moved a model predator toward the females. All species ran to structures to escape the predator and the two builders preferred hoods. Next, we put hood replicas on male U. beebei burrows and pillar replicas on male U. musica burrows. When courted, females of both species preferentially approached hoods as they did when chased with a predator. However, males of both species with hoods did not have higher mating rates than males with pillars perhaps because hoods block more of a male's visual field so he sees and courts fewer females. Sexual selection may often favor male signals that attract females because they facilitate general orientation or navigation mechanisms that reduce predation risk in many contexts, including during mate search.     

To court or not to court: reproductive decisions by male fiddler crabs in response to fluctuating food availability

For males, courting and foraging are often behavioral alternatives, which take time and consume energy. When males have a possibility of mating with receptive females, there may be a behavioral trade-off between courtship and feeding; the outcome of which may be affected by male physiological condition and food availability. Although many mathematical models and empirical studies suggest that the expression of male courtship signals are condition-dependent, decisions about courtship and mating strategies in relation to food availability have not attracted much attention. In this study, we tested whether daily changes in food availability affect males’ decisions about whether to court. We conducted experiments with the fiddler crab Uca lactea by providing males with additional food every other day. In food-supplemented enclosures, males did not increase courtship activity on the days when food was supplemented. However, they built more courtship structures (semidomes) and waved more on the days when they were not given additional food. Male size had a strong influence on the number of days the males courted. We also tested whether the frequency of surface mating, as an alternative reproductive tactic, decreased when food was supplemented. Contrary to our expectation, the number of males that exhibited the surface-mating tactic increased when food was supplemented whereas the number of mate-searching females did not change. Our findings in this field study suggest that reproductive decisions by male fiddler crabs are affected by fluctuating food availability and present body condition, and the alternative mating tactic of this species may be more frequently used by males under good condition.     

The influence of sexual selection and predation on the mating and postcopulatory guarding behavior of stone crabs (Xanthidae,Menippe)

Summary Postcopulatory mate guarding in crustaceans traditionally has been viewed as a behavioral mechanism that prevents predation on the soft post-molt female. This study tests the effects of sexual selection and predation on the postcopulatory guarding durations of male stone crabs, Menippe mercenaria, M. adina, and their hybrid. Male stone crabs were held with a pre-molt female, and either another adult male stone crab, an intermolt female, or a male blue crab, which corresponded to intermale competition, control, and predation treatments, respectively. The mating behavior of the heterosexual pair was recorded with a time lapse video system and the durations of copulation and postcopulatory guarding were measured. Males guarded longer in the intermale competition treatment than either the control or predation treatments. In the competition treatment, agonistic encounters occurred between the males at the den containing the female and several mate takeovers occurred. Females survived the predation treatment in trials in which the guarding durations were the longest, whereas females were eaten by the blue crab in trials with the shortest guarding durations. Sexual selection appears to be important in maintaining postcopulatory mate guarding in stone crabs.     

Reproductive biology of a small isopod symbiont living on a large isopod host: from the maternal marsupium to the protective grip of guarding males

Mating systems of many symbiotic crustaceans are characterised by a high degree of mate guarding. A peculiar case of mate guarding has been reported for small symbiotic janirid isopods where males mate with immature females. Field samples of individual hosts and laboratory experiments were conducted to reveal the mating behaviour of the symbiont in a natural environment, that is, on their hosts. Along the coast of the Magellan Strait, Chile, the janirid isopod Iais pubescens was frequently found on the shore-living isopod Exosphaeroma gigas. Symbiont prevalence (percent hosts occupied) was high at eight of the nine sampling sites. Mean symbiont intensity was very low at one site (<<1 individual host^-1), intermediate at two sites (1-10 individuals host^-1) and high at the other sites (10-40 individuals host^-1). The mean sex ratio (males:females) was male biased at most sampling sites (n=7). Females of I. pubescens reached substantially larger sizes (1.5-3.0 mm body length, BL) than males (1.1-1.9 mm BL). The majority of males were carrying small juveniles (66.15%), and males with juveniles were significantly larger than males without juveniles - this suggests that males prefer virgin juveniles to adult females and that they compete for small juveniles. In laboratory observations, males were seen to manipulate the marsupium of adult females that were about to release small juveniles. Males obtained virgin juveniles in this manner. Juveniles were carried for ~7 days, and they moulted shortly before being fertilised and released by males. The high proportion of juveniles carried by males in the field (68.2%) supports previous observations that males initially are not able to distinguish male and female juveniles. It is suggested that the mating system of symbiotic janirid isopods with long-term sperm storage and continuous receptivity in females and male mating with virgin females has evolved in response to highly unpredictable encounter probabilities between the sexes. Mate guarding and manipulation of small virgin juveniles may be favoured on the highly mobile hosts of symbiotic janirid isopods. Furthermore, adult females may gain by leaving their emerging offspring in the protective grip of guarding males, thereby reinforcing the maintenance of this peculiar mating system.     

Repeatable female preferences, mating order and mating success in the poeciliid fish, Heterandria formosa

Sexual selection via female choice can afford preferred males comparably higher mating success than those males that lack preferred traits. In addition, many models of sexual selection assume that both male traits and female preferences are heritable. In this study we test whether females of the poeciliid fish, Heterandria formosa, have repeatable pre-copulatory preferences for larger males. We also test whether female pre-copulatory preferences are always reliable indicators of male mating success. When given a choice between a large and a small male, females prefer larger males, and the repeatability of this preference is high. Although there are no overall differences in male mating success between large and small males, large males have a higher mating success when they are the first to mate than when they are the second to mate. Likewise, preferred males also have higher mating success when they are the first to mate than when they mate second. Therefore, the repeatable female preferences observed in this study only predict male mating success when the preferred male mates first. These results illustrate that even significantly repeatable female preferences do not translate into male mating success, which is an assumption of many examinations of the importance of female choice in sexual selection.     

Male–male competition and alternative male mating tactics influence female behavior and fertility in Japanese medaka (Oryzias latipes)

Intense male–male competition driven by high male density during mating can result in the evolution of alternative mating tactics that increase male fertilization success. The effects of alternative male mating tactics on females can range from increased fertilization and genetic benefits to decreased fertilization and loss of paternal care. However, the influence of male competitive behavior and alternative mating tactics on female behavior and reproductive success has seldom been addressed. In this work, I investigated the occurrence of alternative male mating tactics and their potential influence on female behavior and fertilization success in Japanese medaka (Oryzias latipes). Groups of one, two, or four males competed for access to a female in a repeated-measures experiment. Male density had a significant influence on female reproductive output as a result of a change in competitive mode from contest to scramble competition that coincided with more disruption during mating when more than one male attempted to mate. By contrast, sneaking during mating was beneficial to males, as more than one male sired offspring in most spawnings involving sneaker males. These results suggest that there may be conflict between males and females over mating, such that females are detrimentally affected by the occurrence of alternative mating tactics, whereas males may benefit from sneak mating. The occurrence of conflict between the sexes can be related to ecological factors, such as male density, which cause behavioral change in both males and females.     

Mate guarding in the swallowHirundo rustica

Summary The importance of mate guarding by males in the monogamous swallowHirundo rustica was studied by temporarily detaining the males. Mate guarding reduced the frequency of extra-pair copulations and of sexual chases involving female mates. Males participated in sexual chases more frequently if they had a non-fertile female. Neighbouring males of ‘widowed’ females increased their own mate guarding presumably in response to the experimentally increased rate of sexual chases. Neighbouring males with a fertile female increased their mate guarding more than did males with a non-fertile female. Addition of eggs to swallow nests in the post-fledging period of the first brood induced mate guarding by male nest owners. These males also copulated more frequently with their mates than did control males. Neighbouring male swallows responded to the increased mate guarding by showing sexual interest in the guarded females. removal of eggs from swallow nests during the laying period, leaving only one egg in the nest, resulted in reduced nest attendance by females. Male mates responded by increasing their mate guarding intensity as compared to controls, and neighbouring males showed an increased sexual interest in these females.     

Mating system of the intertidal copepod Tigriopus californicus

Male Tigriopus californicus clasp immature females (copepodid stages II–V) for a period of up to a week prior to the female's terminal molt; upon maturation (stage VI) the female is inseminated and released. While females can mate anytime after their terminal molt, experiments using electrophoretically-detected genetic markers indicate that each mates only once in her lifetime. No evidence of sperm displacement was observed. Hence, male mating behavior can be interpreted as pre-copulatory mate guarding, a strategy employed to assure that a potential mate has not been previously inseminated. Males minimize the time investment required to insemiate a single female successfully by preferentially choosing to clasp more developmentally-advanced females; males clasped to stage III females will release them in order to clasp stage V females if the latter are present. Since males are capable of multiple mating, under most conditions of population sex ratio, this mating system results in low availability of unclasped, developmentally-advanced females; consequently, males must clasp successively younger (i.e. developmentally less-advanced) females in order to obtain a successful insemination.     

Sexual coercion by male chimpanzees shows that female choice may be more apparent than real

The extent to which active female mating preferences influence male reproductive success in mammals is unclear, particularly for promiscuously breeding species like chimpanzees (Pan troglodytes). Previous studies from multiple long-term study sites have shown that female chimpanzees mate more restrictively around ovulation, and this has been taken as evidence for female choice. However, none of these studies rigorously evaluated the alternative hypothesis that restrictive mating results not from unconstrained choice, but in response to coercive mate guarding, in which males use punishment and intimidation to reduce female promiscuity and promote their own mating interests. Nor did they consider evidence for the potential genetic or phenotypic benefits that females might be choosing. Using 11 years of data from the Kanyawara community in Kibale National Park, Uganda, we previously demonstrated that males achieve elevated mating success with those females toward whom they direct high levels of aggression. Here we extend those findings to show that even female copulatory approaches, which have previously been attributed to female choice, are correlated with male aggression. Specifically, individual females at our site initiated periovulatory copulations most frequently with the males who were most aggressive toward them throughout their cycles. Those males showed high rates of aggression toward females throughout estrus, despite achieving high copulation rates, demonstrating a continuing conflict of interest over the exclusivity of mating access. Because sexual coercion is potentially widespread in primates and other mammals, our results stress the importance of considering the influence of male aggression in studies of female choice.     

Male reproductive tactics to increase paternity in the polygynandrous Columbian ground squirrel (<Emphasis Type="Italic">Urocitellus columbianus</Emphasis>)

In polyandrous and polygynandrous species where females mate with multiple partners, males are expected to maximize their fitness by exhibiting an array of reproductive behaviors to ensure fertilization success, such as competing for the best mating order within a mating sequence, optimizing their investment in copulation, and mate guarding. Though there is genetic evidence of a first-male precedence in siring success for many mammalian species, the causes of this effect are poorly understood. We studied influences on first-male precedence in Columbian ground squirrels (Urocitellus columbianus). We found that the time a male spent consorting and mate guarding declined with his mating order (both the highest for the first male to mate). Mate guarding by the first male significantly reduced, but did not exclude, the number of additional males a female accepted. Later mating males reduced the time spent consorting, suggesting a perceived decreased chance of fertilization success. Consortship and mate guarding durations were positively related to the male’s siring success and to each other, suggesting that males adjusted these behaviors strategically to increase their chances of fertilization success. Our results suggest that besides being the first male to consort, first-male sperm precedence is further enhanced through longer mating bouts and by suppressing the chances and/or efforts of later mating males.     

Costs of courtship and mating in a sexually cannibalistic orb-web spider: female mating strategies and their consequences for males

The costs of courtship and mating may include increased risks of predation, the transmission of pathogens, and a loss of foraging opportunities. Thus, a female's decision to tolerate a courting male will depend upon how these costs offset the benefits of mating, which will depend on her reproductive and nutritional status. While these costs may be similar for mated and unmated females, the benefits of mating will be less for mated than virgin females. However, the cost of lost foraging opportunities may be higher for females with fewer nutritional reserves necessary for forming eggs. We examined how these costs and benefits influence the courtship and mating behaviour of male and female orb-web spiders, Argiope keyserlingi. In the field, females on webs that also contained a courting male intercepted fewer prey items per hour than females on webs without a male. In the laboratory, the presence of a courting male at the hub also attracted mantid predators to the web, increasing the risk of predation for both male and female. Staged mating experiments in the laboratory revealed that the frequency of female attacks and pre-copulatory cannibalism was greater among mated than virgin females. Feeding history did not affect aggression in virgin females but, among mated females, food-deprived spiders attacked and cannibalized males more frequently than sated females and only the latter ever remated. These differences in female behaviour influenced male mating strategies. Choice experiments demonstrated that males preferred to venture onto the silk threads of virgin rather than those of mated females. Similar patterns of mate selectivity were observed in the field; females with narrow abdomens attracted more males to the webs than females with broad abdomens, and copulations were observed more frequently among females with narrow abdomens. These smaller females are likely to be virgins that have recently molted. Males that preferentially mate with virgin females will not only avoid potentially fatal attacks but also obtain, on average, a higher fertilization success.     

Polyandrous mating in treetops: how male competition and female choice interact to determine an unusual carnivore mating system

The diversity of mammalian mating systems is primarily shaped by sex-specific reproductive strategies. In the present study, we explored determinants and consequences of a unique mating system exhibited by fossas (Cryptoprocta ferox), the largest Malagasy carnivore, where females mate polyandrously on traditional mating trees, and males exhibit intrasexual size dimorphism. Males face both contest and scramble competition, and inter-sexual size dimorphism can be pronounced, but its magnitude depends on the male morph. Using a continuous behavioral observation of six estrous females over 4 years, we investigated correlates of male contest competition and female choice based on 316 copulations. Furthermore, we assessed correlates of male scramble competition based on testes size and movement data obtained from GPS tracking. We found that females dominated males regardless of their smaller size and that females actively solicited copulations. Heavy males had highest mating success during the female’s peak mating activity, but were discriminated against afterwards. Female choice and male–male competition thus converged to generate a mating advantage for heavier males. Our results suggest that females actively seek polyandrous matings, presumably for indirect genetic benefits. Since body mass is the major determinant of male mating success and is at the same time dependent on the degree of sociality and associated hunting mode of the respective male morph, a male’s feeding ecology is likely to influence its reproductive tactic. A combination of benefits from female polyandry and the consequences of different subsistence strategies may thus ultimately explain this unusual mating system.     

A female preference for experienced males in the almond moth, Cadra cautella

Male mating status can affect female reproductive output if male ejaculate investment declines over consecutive matings. Accordingly, females are predicted to mate preferentially with virgin males. In mildly polyandrous lepidopterans, female fitness is less affected by reduced male investment than in more polyandrous species, and so the predictions for female mating preferences are less clear. We examined female mating preferences in the mildly polyandrous almond moth, Cadra cautella, in which ejaculate size does not affect female reproductive output. First, we allowed females to mate with virgin or once-mated males, in which the males were presented individually or simultaneously. We recorded the latency to mating and, in the case of the simultaneously presented trials, the identity of the successful, copulating male. We found that females mated more frequently with mated males (when simultaneously presented with both males), yet females did not differ in the time taken to initiate copulation with any male. We further examined if this mated male advantage was due to differential mate detection or locomotory behaviour of the male treatments. We tested the ability of virgin and mated males to locate a receptive female within a wind tunnel using long-distance pheromone cues and recorded their activity budget. We found no difference in the ability of mated or virgin males to locate or approach a receptive female, or in their activity levels. These data suggest a female preference for mated males in this species, a preference that may minimise other potential costs of mating.     

Mouse lemurs in space and time: a test of the socioecological model

Socioecological theory predicts that the distribution of fertile females in space and time is the major determinant of male spacing behavior and mating strategies. Using a small nocturnal Malagasy primate, the gray mouse lemur (Microcebus murinus), we determined the spatiotemporal distribution of estrous females during the brief annual mating season to examine the predictive power of the socioecological model for male mating strategies. Mouse lemurs are particularly interesting in this respect because this polygynous species is characterized by seasonal reproduction, seasonally reversed sexual dimorphism, and relatively large testes. All resident animals in our 8-ha study area, a total of 30 adult males and 27 adult females, were individually marked and regularly recaptured to determine female reproductive status and to obtain home range data. We found that the mating season is limited to 4 weeks following female emergence from hibernation. Only 3-9 females could have synchronized estruses during a given week, indicating a moderately high male monopolization potential. However, receptive females were not spatially clumped and male ranges overlapped with those of many other rivals. Therefore, we suggest that individual powerful males may be unable to defend exclusive permanent access to receptive females because of prohibitive costs of range defense resulting from the strongly male-biased operational sex ratio and the corresponding intruder pressure. Our general conclusions are (1) that the socioecological model provides a useful heuristic framework for the study of mating systems, but that (2) it does not specify the degree of spatiotemporal clumping of receptive females at which male mating strategies switch among mate guarding, spatial exclusion of rivals, and roaming, and that (3) the operational sex ratio can have profound effects on male mating strategies as well.     

Coalitionary mate guarding by male chimpanzees at Ngogo, Kibale National Park, Uganda

Cooperative mate guarding by males is unusual in mammals and birds, largely because fertilizations are non-shareable. Chimpanzees live in fission-fusion communities that have cores of philopatric males who cooperate in inter-group aggression and in defending access to the females in their community. Male contest mating competition is restrained within communities, but single high-ranking males sometimes try to mate guard estrous females. Data from an unusually large chimpanzee commmunity at Ngogo, Kibale National Park, Uganda, that contains more males than any previously studied community show new variation in chimpanzee mate-guarding behavior. Contrary to expectation given the large number of males, mate guarding was as common as, or more common than, at other sites, and males other than the alpha male guarded more often. More strikingly, pairs or trios of top-ranking males sometimes engaged in cooperative aggression to prevent estrous females from mating with other males, but tolerated each other's mating activities. Both single males and coalitions mostly guarded periovulatory females. Mate-guarding coalitions were previously unknown in chimpanzees. Coalitions occurred in large mating parties, seemingly because these often contained too many males for single males to maintain exclusive access to estrous females. Coalition members gained higher shares of copulations than they could have expected from solo mate guarding, and suffered lower per capita costs of guarding (as inferred from aggression rates). Two males who most often participated in coalitions formed two-male coalitions at about the point where the number of males present made it unlikely that either could get 50% or more of total copulations on his own, and formed trios when this value dropped below 33%. Kin selection could be a factor in cooperation among male chimpanzees, but coalition members were not necessarily close relatives and the apparent structure of payoffs fit that of mutualism. Furthermore, reliance of male chimpanzees on support from allies to maintain high rank could have led to trading of mating exclusivity for support against mating competitors. Received: 28 May 1997 / Accepted after revision: 16 May 1998     

Temporal constraints and female preference for burrow width in the fiddler crab, <Emphasis Type="Italic">Uca mjoebergi</Emphasis>

We studied sampling behaviour and mate choice in the fiddler crab Uca mjoebergi. Once a female selects a mate, she copulates in his burrow and remains there until releasing her aquatic larvae. U. mjoebergi occurs in habitats that are inundated only by the highest amplitude spring tides. Females can only release their larvae during these tides, and release before or after will result in complete failure of reproductive effort. Matings occur over a 5-day period near the end of neap tides. Our results suggest that within the mating period, females adjust their larval developmental rates by selecting specific burrows in which to incubate their clutches. We found that at the start of the mating period, females chose larger males as mates. Since male size was positively correlated to burrow width, females were selecting wide burrows and effectively incubating at lower temperatures. This would slow down the developmental rates of larvae. In contrast, females that mated late in the mating period selectively chose small males. By incubating in narrower, warmer burrows, these females may increase the developmental rates of larvae. We propose that females are selecting burrows to influence incubation rate and ensure timely release of their larvae. Female U. mjoebergi appear to adjust their preference for the direct benefits of mate choice to increase their reproductive success.     

Non-independent mate choice in a fiddler crab: a case of stimulus enhancement

Non-independent mate selection occurs when the choice behavior of a female is altered by the interactions between other females and males. In the fiddler crab Uca mjoebergi, males court mate-searching females by waving their one greatly enlarged claw. When a female approaches a male, he initiates high-intensity waving. We conducted one natural mate choice experiment and two mate choice experiments using custom-built robotic crabs. We show that the decision of one female to approach a group of males increases the probability that another female will approach and visit a male from the same group. We suggest that this behavior is best explained by the ‘stimulus enhancement’ hypothesis, where the presence of a female near a group of males makes them more likely to be detected by other females due to an increase in male display rate.     

Time constraints and multiple choice criteria in the sampling behaviour and mate choice of the fiddler crab,Uca annulipes

Active female sampling occurs in the fiddler crab Uca annulipes. Females sample the burrows of several males before remaining to mate in the burrow of the chosen partner. Females time larval release to coincide with the following nocturnal spring tide and must therefore leave sufficient time for embryonic development after mating. Here we show how this temporal constraint on search time affects female choosiness. We found that, at the start of the sampling period (when time constraints are minimal), females selectively sample the larger males in the population. Towards the end of the sampling period (when the temporal constraints increase the costs of sampling), females are less selective. Furthermore, we suggest that the number of males sampled (and other indices of ‘‘sampling effort’’) may not be reliable indicators of female choosiness and may not reflect the strength of female mating preferences under certain conditions. Burrow quality also emerged as an important criterion in final mate choice. Burrow structure potentially influences reproductive success, and mate acceptance based on burrow structure appears to involve a relatively invariant threshold criterion. Since there is no relationship between male size and burrow quality, females are using at least two independent criteria when choosing potential mates. We envisage mate choice as a two-stage process. First, females select which males to sample based on male size. They then decide whether or not to mate with a male based on burrow features. This sampling process explains how two unrelated variables can both predict male mating success. Received: 23 March 1995/Accepted after revision: 14 January 1996     

Weapons or mating signals? Claw shape and mate choice in a fiddler crab

Males often possess traits, such as horns, claws, and tusks, which are used during male–male combat. Studies suggest that selection has fine tuned these weapons to improve their effectiveness and that the shape of these weapons provides cues for males to assess the strength of rivals. Similarly, females might also assess a male’s weaponry to determine his value as a mate. The largest weapon relative to body size is the major claw of male fiddler crabs (genus: Uca). Males use their claws both as a weapon and as a courtship signal, waving it to attract females. We used robotic crabs in two-choice experiments to test female mating preferences based on male claw shape in Uca mjoebergi. First, females did not prefer conspecific claws over any of three alternatively shaped stimuli matched for color and for the rate and pattern of waving. The alternative stimuli were two different heterospecific claws and a plain rectangular shape. Second, females significantly preferred the alternative stimuli when they were presented at a faster wave rate. We conclude that claw shape in U. mjoebergi has not evolved under sexual selection imposed by female mating preferences and is more likely to have evolved under selection for effectiveness during male–male competition.     

Vocalizations by Alaskan moose: female incitation of male aggression

Evidence of female fomentation of male–male aggression as a mechanism of mate choice is rare, especially in mammals. Female choice of mates in polygynous species may be masked by intense male competition or by males attempting to restrict female choice. We studied protest moans of female Alaskan moose Alces alces gigas in interior Alaska, USA, from 1987 to 1990, to determine if moans incited male–male aggression. Alaskan moose exhibit a mating system in which one dominant male (the harem master) herds, defends, courts, and attempts to mate with females in his harem. Protest moans were given by females only in response to courtship. We hypothesized that if protest moans were related to females reducing harassment and exercising mate choice, females should give protest moans more frequently when courted by small males and less often when courted by large males, and that rates of male–male aggression would be elevated following protest moans. Harems were composed of one large male, with a mean of 4.4 females (median = 3 females); 10% of 132 harems included ≥10 females. The temporal pattern of protest moans from late August through November was associated with, but tended to lag behind, mating behavior. The rate of protest moans given by females decreased with increasing size of males courting them. Male–male aggression was significantly less during periods without protest moans than during periods in which protest moans occurred. These results indicate that female moose gave protest moans to reduce harassment by smaller males, and assure a mating opportunity with the most dominant male. Such a subtle mechanism of indirect mate choice by females may occur in other vertebrates in which choice is limited by a mating system in which male–male combat and male dominance over females reduces opportunities for female choice. The importance of female choice may be undervalued in studies of sexual selection in mammals.