Courting male garter snakes (Thamnophis sirtalis parietalis) use multiple cues to identify potential mates

Mating aggregations of red-sided garter snakes (Thamnophis sirtalis parietalis) in Manitoba provide a unique opportunity to identify the cues that attract a male snake and induce him to court. The snakes are abundant, tolerate human presence, and males direct courtship to a subset of other males ("she-males") as well as to females. Previous work has emphasised the role of pheromonal cues (skin lipid profiles) as sexual attractants in snakes. However, pheromones are so widely distributed throughout the den area that these chemical cues may be difficult for males to use to localise females. Our field studies show that males and females differ in several other attributes such as size (females are larger than males), body temperature (very cold snakes are often females), muddiness (females are often covered in mud) and whether or not they are solitary (most females are surrounded by courting males). Experiments show that males use all of these cues to identify possible sexual partners. Visual and thermal cues are particularly important for solitary mate-searching males; but after a mating ball forms around a female, pheromones may be most important. Our study also reveals substantial variation among individuals: females vary in attractiveness, and males vary in their intensity of courtship as well as in the magnitude of their preference for one potential partner versus another. Thus, a male snake's "decision" whom to court depends not only on visual and thermal as well as chemical cues, but also on the male's own preferences and on subtle differences among potential sexual "targets".     

Patterns of host switching in the fish ectoparasite <Emphasis Type="Italic">Argulus coregoni</Emphasis>

Mating is essential for sexually reproducing species to pass on their genes. For sexual parasites, this implies a need to switch the host in the search for a mate when potential partners are not available on the same host, although host switching includes risks like starvation and predation. Studies of mate-searching behavior predict that commonly only one sex searches for mating partners while the other remains stationary. In the present work, we experimentally infected rainbow trout (Oncorhynchus mykiss) with the fish ectoparasite Argulus coregoni and determined whether the sex, age and the presence of mating partners influenced the host switching activity. Our results show that increased host switching by A. coregoni occurred only after the parasite reached the adult stage and a difference between the sexes was also recorded. Host switching by mature males was enhanced when no mating partners were present on the same host, whereas females remained mainly stationary on their host regardless of male presence or absence. Our data therefore support the hypothesis that there is a strategic difference in reproductive behavior between males and females; males invest energy in mate searching while females are rather stationary and invest into body size and hence increased fecundity. Our data also showed that leaving the host to find a mate is potentially costly in terms of predation since a substantial number of free-swimming parasites were eaten by fish.     

Sexual signalling and viability in a wolf spider (Hygrolycosa rubrofasciata): measurements under laboratory and field conditions

This study examined the crucial prediction of the conditional-handicap theory, the relationship between male sexual trait size and male viability, in the wolf spider Hygrolycosa rubrofasciata. In this species, males court females by drumming dry leaves with their abdomen, and males with the highest drumming rate enjoy highest mating success. We determined male drumming rate, body mass, and mobility, which reflects mate-searching activity, in relation to male survival. Because it is often difficult to know how results obtained from laboratory studies reflect the natural world, particularly when the measured variable is survival, we repeated our study in both laboratory and field conditions. Males drumming at the highest rate survived better than males drumming at a lower rate in both laboratory and field conditions. These results are in accordance with the predictions of conditional-handicap models of sexual selection. Survival was independent of male body mass and there was no significant correlation between male drumming activity and body mass. However, large males moved further than smaller males, and males moving longer distances lost less mass than those moving shorter distances. These results suggest that, moving, and consequently mate-searching activity, may be a condition-dependent trait and that there may be a advantage for large males in mate searching. Received: 22 October 1998 / Received in revised form: 28 January 1999 / Accepted: 14 February 1999     

Female association preferences based on olfactory cues in the guppy,<Emphasis Type="Italic"> Poecilia reticulata</Emphasis>

Guppies are highly sexually dimorphic. Females have been shown to mate preferentially with males with various visible traits and previous studies investigating mate choice have focussed on these visual cues. However, guppies have been shown to respond behaviourally to odour cues from conspecifics as well as from predators. Therefore, sexual selection in guppies may act on multiple sensory modalities, but so far only visual cues have been investigated. Here, we used a specially designed olfactory choice tank to determine whether females could detect other guppies on the basis of their olfactory cues only, and to determine whether females preferred to associate with males or females and whether they could distinguish between different males. We show that female guppies associated preferentially with other females when given a choice between water containing the odour cues from another fish and water containing no odour cues. When females were presented with olfactory cues from a male and a female, they investigated the female initially, but then most reversed their decision and swam to the male. Furthermore, we demonstrate that females associated preferentially with certain males based upon olfactory cues alone, but that this choice was in direct opposition to that made when the females received only visual cues from the same males.Communicated by: M. Abrahams     

Female distribution affects mate searching and sexual selection in male northern water snakes (Nerodia sipedon)

Mating systems and sexual selection are assumed to be affected by the distribution of critical resources. We use observations of 312 mating aggregations to compare mate-searching success of male northern water snakes (Nerodia sipedon) in two marshes in which differences in mating substrate availability resulted in more than fourfold differences in female dispersion. Reproductive males had significantly larger home ranges where females were dispersed than where females were clumped. The number of females encountered by males increased significantly with male home range size where females were dispersed, and decreased significantly where females were clumped. Where females were clumped, males were more likely to encounter other males when they located females. We found no evidence in either population that mate searching was energetically expensive or that males with relatively more energy had larger home ranges. However, males with greater fat reserves at the start of the season participated in more mating aggregations when females were dispersed, suggesting that fat reserves could affect a male’s willingness to attempt mating or to persist in aggregations. When females were dispersed there was weak stabilizing selection acting to maintain male body size (β=–0.14), but strong directional selection favoring larger (β=0.50) and fatter (β=0.37) males. Over 7 years, the intensity of selection favoring larger males varied substantially (β=0.14–1.15), but that variation was not related to variation in the operational sex ratio. We found no evidence of directional selection on either body size (β=0.05) or fat reserves (β=0.10) of males when females were spatially clumped. Overall, the distribution of females had a pronounced effect on male behavior, on the factors that affected male success in locating females, and probably on the extent of sperm competition once females had been located. Received: 23 November 1998 / Received in revised form: 9 August 1999 / Accepted: 18 August 1999     

Effects of reproduction on the antipredator tactics of snakes (Tropidonophis mairii, Colubridae)

Does an animal’s reproductive state influence the distance at which it flees from an approaching predator? We predicted that reproduction would increase approach distances in pregnant females (because they are burdened with eggs and thus less able to escape rapidly), but reduce them in males (because of lower vigilance due to males focusing on mate-searching rather than predator detection). Field data on approach distances of keelback snakes (Tropidonophis mairii, Natricinae, Colubridae) supported both of these predictions. We walked the same 1.3-km transect along a dam wall in tropical Australia on 135 nights, and recorded the distances at which snakes fled from our approach. Locomotor speeds were measured for a subset of these animals. Variations in approach distance due to season, weather conditions, prior capture history and snake body size were minor, but reproduction strongly affected approach distances for snakes of both sexes. Gravid females were slower than non-gravid females, and fled at greater distances. Reproductive status did not affect locomotor speeds of males, but males that were reproductive (i.e., contained sperm) permitted closer approach than did non-reproductive adult males. Reproduction thus affected approach distances in snakes of both sexes, but in opposite directions and for different reasons.     

Body size preferences in the pot-bellied seahorse <Emphasis Type="Italic">Hippocampus abdominalis:</Emphasis> choosy males and indiscriminate females

Male seahorses (genus Hippocampus) provide all post-fertilization parental care, yet despite high levels of paternal investment, these species have long been thought to have conventional sex roles, with female mate choice and male–male competition. Recent studies of the pot-bellied seahorse (Hippocampus abdominalis) have shown that sex-role reversal occurs in high-density female-biased populations, indicating that male mating preferences may lead to sexual selection on females in this species. Egg size, egg number, and offspring size all correlate positively with female body size in Hippocampus, and by choosing large mating partners, male seahorses may increase their reproductive success. While male brood size is also positively correlated with body size, small H. abdominalis males can carry exceptionally large broods, suggesting that the fecundity benefits of female preference for large partners may be limited. We investigated the importance of body size in reproductive decisions of H. abdominalis, presenting focal individuals of both sexes with potential mating partners of different sizes. Mating preferences were quantified in terms of time spent courting each potential partner. Male seahorses were highly active throughout the mate-choice trials and showed a clear behavioral preference for large partners, while females showed significantly lower levels of activity and equivocal mating preferences. The strong male preferences for large females demonstrated here suggest that sexual selection may act strongly on female body size in wild populations of H. abdominalis, consistent with predictions on the importance of female body size for reproductive output in this species. An erratum to this article can be found at     

Demonstration of sex pheromones in the predaceous diving beetle Rhantus suturalis (MacLeay 1825) (Dytiscidae)

Sex pheromones are used by a wide variety of species in terrestrial ecosystems. Much less is known about these pheromones in aquatic systems e.g., for diving beetles. To test the use of pheromones and visual signals for mate finding by the diving beetle Rhantus suturalis (MacLeay 1825), behavioral experiments were performed using three different types of vessels containing conspecific. In experiments with non-permeable glass flasks, which did not allow the diffusion of chemical substances, males and females did not stimulate any reaction by conspecific of either sex. In experiments with opaque but water permeable vessels, and in experiments with vessels made of finely woven steel, which allowed the perception of chemical as well as optical cues, male diving beetles were significantly attracted to females. Females were attracted to other females only in the last experiment, when simultaneously perceiving chemical and optical cues. These results indicate that R. suturalis females release sex pheromones to attract mating partners, which is the first experimental demonstration of pheromones in the Dytiscidae.     

Female choice over short and long distances: neighbour effects

Fiddler crabs live at high densities and mate-searching females encounter many males at varying distances. Who is the ideal neighbour for a male? There could be a trade-off if having neighbours that invest more in sexual signals increases the rate at which females initially move towards a focal male, but thereafter decrease the likelihood that he is chosen rather than his neighbour. We used robotic crabs to test whether female choice for focal males (identical claw size/courtship wave rate) varied depending on the relative investment in sexual signals of their two neighbours and the distance at which she first saw the males. The neighbours’ phenotype did not affect which of two focal males she initially approached from long-range (50 cm). When a female initially saw a trio of males at a close-range (20 cm), she preferentially chose the focal male over neighbours that invested less in sexual signals (smaller claw/slower wave rate), but did not show a preference for the focal male over neighbours that invested more in sexual signals (larger claw/faster wave rate). However, a female that started to approach a focal male with neighbours that invest more in sexual signals from 50 cm was significantly less likely to choose the focal male than when she first saw the trio at 20 cm. Our results suggest that the initial distance at which males are seen partly determines how neighbours’ sexual signals affect male mating success. In general, if larger males can retain smaller neighbours they might therefore increase their mating success.     

Experience with chemotactile cues indicating female feeding history impacts male courtship investment in the wolf spider <Emphasis Type="BoldItalic">Schizocosa ocreata</Emphasis>

Male fitness is often determined by the ability of the male to gain access to multiple mates, although in species that exhibit sexual cannibalism, males might increase their likelihood of being cannibalized with each encounter. This risk should create selection for males who are able to perceive potential risks associated with mating encounters. We studied male Schizocosa ocreata wolf spiders to determine whether they use female chemotactile cues (silk, excreta) as indicators of potential risks and how these cues affected subsequent male courtship behaviors. Female treatments included satiated females vs. starved females, as well as a treatment where females had recently cannibalized a male S. ocreata. We performed experiments to assess (1) if males use female chemotactile cues to determine potential risks associated with differing female feeding treatments and alter courtship investment, and 2) how male experience with female chemotactile cues affected courtship investment in subsequent female encounters. At first encounter, males do not vary courtship investment (number of bouts, duration, and vigor) with different female feeding treatments. However, male behaviors during subsequent encounters with female chemotactile cues varied in complex ways, depending on female feeding treatment and male first encounter experience. These data suggest that male experience impacts perception of female chemical cues and offers the male opportunity to avoid sexual cannibalism in high-risk situations.     

The lexicon of love: what cues cause size-assortative courtship by male garter snakes?

Cues that females use to select potential mates have attracted substantial research effort, but the criteria for male mate choice remain very poorly known. Red-sided garter snakes ( Thamnophis sirtalis parietalis) court and mate in large aggregations around overwintering dens in southern Manitoba, Canada. Both courtship and mating are size-assortative: small male snakes court small as well as large females, whereas larger males court only large females. This system provides a unique opportunity to assess the cues that males use in selecting mates, and in particular the mechanisms that generate a size-related shift in mate preference. Experiments in which we manipulated body sizes and scents showed that both vision and scent (sex pheromones) were important. Large males directed intense courtship only when the stimulus provided both visual and chemical (skin lipid) evidence of large body size. Small males were much less discriminating in both respects. Thus, size-assortative mating in this system is generated not by larger males excluding their smaller rivals from the largest females (as has been reported in other reptile species), but by a size-related shift in the visual and pheromonal cues that elicit courtship. Males of some species may thus show complex patterns of mate choice, with the cues that stimulate courtship differing even among males within a single population based on traits such as age or body size.     

Chemosensory cues allow courting male garter snakes to assess body length and body condition of potential mates

When choosing between two potential mates, a male may benefit by picking a larger (longer and/or more heavy-bodied) female because she is likely to produce more or larger offspring. Males of many species use visual cues to evaluate the sizes of their mates, but in some situations (at night or in a crowded mating swarm), vision may be useless. Potentially, males may be able to use chemical cues that convey information about female body size. We manipulated cues available to free-ranging male garter snakes (Thamnophis sirtalis parietalis) in large courting aggregations near communal dens in Manitoba, Canada. Males not only directed disproportionate courtship to longer and heavier-bodied females, but also courted most vigorously in response to lipids extracted from the skins of such females. Our data show that with a flick of his tongue, a male garter snake can identify not only a female's body length, but also her body condition.     

Mate choice in the yellow-shouldered widowbird: correlates of male attractiveness

Recent investigations of male ornaments in sexual selection have used experimental manipulation of tail length in three widowbird species, but only for one of these have correlates of male reproductive success been reported. I examined correlates of male attractiveness to nesting females over two breeding seasons for the polygynous yellow-shouldered widowbird, Euplectes macrourus, in order to discover which cues females may be using to select mates. The black, long-tailed ( 10 cm) males defend large territories and build nest frames, or cock's nests, which females then line and use for nesting. I examined various aspects of male morphology, five behavioral displays, territory characteristics, and the number of cock's nests that males built. Few correlates of mating success were found. The best predictor was the number of cock's nests that a male builds, though one courtship display also correlated with male mating success in 1 year, as did average grass height. Tail length did not correlate with male mating success. A partial correlation analysis confirmed that cock's nests and, in 1 year, grass height, were the primary contributers to male success. Females may choose where to nest primarily on the availability of suitable nesting sites. Long tails may be used by females seeking extra-pair copulations or in male-male competition for territories.     

Males in the shade: habitat use and sexual segregation in the Galápagos sea lion (Zalophus californianus wollebaeki)

In many sexually dimorphic species adult sexes tend to segregate socially, spatially, or in habitat use. Several hypotheses have been formulated regarding underlying mechanisms. We investigated terrestrial habitat use and sexual segregation in a tropical otariid, the Galápagos sea lion (Zalophus californianus wollebaeki), where most of the hypotheses can be ruled out a priori. Factors relating to thermoregulation and costs of locomotion were of prime importance for habitat use. Habitats directly adjacent to the sea, with simple structured flat surfaces, shade, and tide pools were most frequented, but sexes and age classes differed in their usage patterns. Sexual segregation, both spatial and by habitat was pronounced in the reproductive period (RP), but remained high during the nonreproductive period (NRP). A GLM model of habitat use showed that in both seasons adult males frequented habitat types that adult females and other age classes used much less. Males were most abundant in suboptimal inland habitats, which offered only shade for cooling. Females with newborns differed in habitat use from females with older offspring and lone females. Spatial and habitat segregation are explained most parsimoniously as by-products of social processes, primarily intrasexual competition and female avoidance of male harassment, linked to the polygynous mating system.Electronic Supplementary Material Supplementary material is available in the online version of this article at and is accessible for authorized users.     

Evidence for a female sex pheromone mediating male trailing behavior in the red-sided garter snake, Thamnophis sirtalis parietalis

Summary. Male garter snakes locate females during the breeding season utilizing conspecific trailing behavior. It has been hypothesized that the female-derived chemical cue responsible for mediating male reproductive trailing behavior is the sexual attractiveness pheromone, a previously characterized contact pheromone responsible for releasing male courtship behavior. To examine this hypothesis, we tested the response of male red-sided garter snakes, Thamnophis sirtalis parietalis, to pheromone trails produced by males, females and ‘she-males’. She-males are a small subset of males in the natural population that are morphologically and behaviorally similar to other males except that they produce and express the sexual attractiveness pheromone during the breeding season. When tested on a Y-maze, males were found to detect and follow the skin lipid trails of females and she-males, but displayed no behavioral responses to male trails. In addition, males were unable to discriminate between she-male and female trails when given a choice. These results are consistent with the hypothesis that the sexual attractiveness pheromone is the chemical cue primarily utilized by males to mediate reproductive trailing behavior.     

Measuring mate choice using correlation: the effect of female sampling behaviour

For intersexual selection to occur, it is necessary that females choose between males. It is now well appreciated that constraints exist, which preclude females sampling all the available males in a population. These constraints are likely to have caused the evolution of sampling rules (such as the “best-of-n” rule) by which females sample males. Here we investigate the impact of female subsampling of the male population, not on the evolution of sampling behaviour, but on the population-level correlation between a male trait and currencies such as reproductive success. This study is important as it illustrates when population-level correlations can be safely used to infer the presence and strength of sexual selection in the field. We find that the correlation between a male trait and a mate choice variable rises steeply as the number of males sampled by each female increases, flattening above seven to ten males sampled. This shape is found to be remarkably robust, and little affected by, for example, the mate choice variable used, by noise in assessment, by sampling behaviour depending on female quality, or by population size. The only variable found to have a large impact is male clumping according to their “quality”. If females are sampling about four males, the maximum correlation that can be found at the population level is in the range 0.4–0.6, perhaps as little as 0.1 if males are strongly clumped. A recent review of the literature suggests that four is the average number of males that females sample. Thus, the absence of a strong correlation cannot by itself be used to infer that sexual selection is weak, as it may be due to females sampling few males. Received: 18 May 1998 / Accepted after revision: 18 July 1998     

Role of surface glycoproteins in mate-guarding of the marine harpacticoid Tigriopus japonicus

Surface glycoproteins serve as mate- and gamete-recognition molecules in some marine animals such as rotifers and sea urchins. We investigated the role of contact chemoreception of surface glycoproteins in mate recognition, mate-guarding, and spermatophore transfer in the marine harpacticoid Tigriopus japonicus Mori. Adult males accurately distinguished immature females from a pool of mixed-sex juveniles, and their behavior towards both live and dead females is described. A survey of the binding sites of twelve lectins to the surface of juvenile and adult females, and adult males demonstrated localized lectin-binding at sites considered important in mating behavior of each sex/age class. Treating adult males with the Triticum vulgaris lectin sharply inhibited normal mate recognition and guarding behavior, as did the monosaccharide glucosamine. Treatment of males with protease and detergents destroyed their mate-guarding behavior without affecting swimming behavior. These results suggest that protein receptors on the antennules of the males detect glycoprotein signals on the surface of females, recognizing carbohydrate moieties of glycoproteins to identify appropriate partners for guarding or mating. Surface glycoproteins may function as a common mechanism of sexual communication in many marine zooplankters. Received: 6 May 1997 / Accepted: 14 September 1997     

Sexual selection and species recognition in the pygmy swordtail, Xiphophorus pygmaeus: conflicting preferences

Sexual selection and species recognition play important roles in mate choice; however, sexual selection preferences may overlap with traits found in heterospecifics, producing a conflict between sexual selection and species recognition. We examined female preferences in Xiphophorus pygmaeus for male traits that could provide both types of information to determine how females use multiple cues when preferences for these cues would conflict. We also examined X. pygmaeus behavior in the field to determine if females have the opportunity to choose mates. As no male-male competition was observed in the field, and females occasionally chased males from feeding areas, females apparently have the opportunity to exercise mate choice in their natural habitat. In the laboratory, female X. pygmaeus used body size as a sexual selection cue, preferring large heterospecifics (X. cortezi) to small conspecifics. Females also preferred barless X. cortezi over barred X. cortezi when males were size matched. Because X. pygmaeus males do not have bars, this preference suggests that X. pygmaeus females use vertical bars in species recognition, and that large body size and vertical bars are conflicting cues. However, X. pygmaeus females did not have a preference for males of either species when sexual selection and species recognition cues were presented concurrently. This result was surprising, because preferences for species recognition cues are often assumed to be stronger than sexual selection cues. We suggest that females may be using additional species-specific cues in mate choice to prevent hybridization.     

The peculiar case of an insectivorous iguanid lizard that detects chemical cues from prey

Summary. Ecological and phylogenetic factors determine which sensory modalities organisms use in their day-to-day activities. Among lizards, empirical studies indicate a tight association between foraging strategies and the ability to detect chemical cues from prey. Consequently, ambush insectivores do not detect food chemicals and these differences have a phylogenetic basis, as ambush lizards mainly belong to the Iguania clade. These data contrast, however, with the widespread uses of chemoreception in the Iguania genus Liolaemus, which are mostly insectivorous ambush predators. Moreover, observations from different Liolaemus species suggest a capability to find prey through chemoreception. In order to clarify the abilities of Liolaemus to detect chemical cues from prey, the chemoreceptive behavior of the insectivorous ambush predator, L. lemniscatus, was studied. Lizards were given the choice between areas with and without chemical cues from a food item (mealworms). Results show that test animals stayed for longer, moved more, and did more chemical exploration (tongue flicks) in the area where chemical cues from mealworms were present. Furthermore, in this area, more individuals displayed behaviors that suggest maintenance and defense of the prey patch. Thus, L. lemniscatus is the first insectivorous Iguania reported to be able to detect chemical cues from prey. Although I propose a mechanism for acquiring chemical detection of prey cues in Liolaemus, I also remark that it is necessary to reanalyze both the abilities to detect and use chemical foraging cues in Iguania at large, and the methodologies traditionally used to study these issues.     

Correlational evidence of a sexually-selected handicap

Handicap models of sexual selection predict that ornaments must be costly to produce and/or to wear and maintain; only then can they evolve as reliable signals of genetic quality. We investigated in the laboratory one potential cost of possessing ornaments, using the viviparous fish Girardinichthys multiradiatus and its natural predator, the snake Thamnophis melanogaster. We found that female G. multiradiatus show preferences for males with larger fins, as measured from body correlates. Males with a morphology attractive to females, however, were more likely to be captured by snakes than were other males (Fig. 5). Greater vulnerability to snakes cannot be explained as a result of snake visual preferences, because snakes responded similarly to males and females (Fig. 6). Finally, males, particularly dominant ones, were more likely to inspect foraging snakes than were females (Fig. 7). We conclude that male Girardinichthys multiradiatus experience a sexually-selected handicap due to reduced mobility resulting from having enlarged fins.