Trichinella spiralis infection in voles alters female odor preference but not partner preference

Females may choose mates based on secondary sex traits that reflect disease resistance. Accordingly, females should be able to distinguish between unparasitized and parasitized males, and should prefer to mate with unparasitized individuals. Mate and odor preferences for uninfected males or males infected with the nematode, Trichinella spiralis, were examined among prairie voles (Microtus ochrogaster) and meadow voles (M. pennsylvanicus). In a 15-min odor preference test, only female meadow voles distinguished between bedding from parasitized and unparasitized conspecific males, and preferred to spend time with bedding from unparasitized males. Although T. spiralis infection influenced odor preference in female meadow voles, there was no effect of infection status on mate preference among either species. Testosterone and corticosterone concentrations were not different between parasitized and unparasitized males. However, among prairie voles, males that spent an increased amount of time with females during the mate preference test had elevated testosterone concentrations. Taken together, these data suggest that (1) female meadow voles can discriminate between unparasitized and parasitized males, (2) the effects of infection on steroid hormone concentrations may be masked by the effects of social interactions, and (3) parasites may represent a selective constraint on partner preference in voles; however, the life cycle of parasites may influence female preference and should be considered in studies of female preference. Received: 23 April 1998 / Accepted after revision: 25 October 1998     

Home range and social behavior of three species of European Pitymys (Mammalia,Rodentia)

Summary Habits, home range, and social behavior of three species of voles of the genus Pitymys, P. multiplex, P. subterraneus, and P. savii, were studied in Tessin (Switzerland) by radioactive tagging. P. multiplex and P. savii are fossorial and often use the burrow systems of moles (Talpa); P. subterraneus moves around on the surface under dense vegetation. Males and females of P. multiplex were territorial and their home ranges averaged 342 and 229 m² respectively. The mating system appeared to be monogamous. P. savii male and female home ranges averaged 445 and 298 m² respectively. Groups of up to one to three adult females, one or more adult males, and several young, occupied exclusive communal territories. The mating system appeared to be flexible, including monogamy, polygyny, and polyandry. P. subterraneus females occupied exclusive territories (mean 256 m²) overlapped by the home ranges of one or more males (1025 m²). The mating system appeared to be promiscuous. Individuals of the three species occupied one to seven nests. In P. savii all family members utilized three or more communal nests at the same time or alternatively. Co-nesting between males and females of P. multiplex or P. subterraneus were observed less frequently.     

Space use,longevity, and reproductive success in meadow voles

Summary We addressed the question of how reproductive success (RS) was limited in the shortlived but highly fecund meadow vole, Microtus pennsylvanicus. In so doing, we asked how differential space use patterns could affect longevity and hence RS in each sex. The sample comprised all voles achieving sexual competency over the course of a 40-week breeding season in a live-trapped population in Manomet, MA USA. Matrilineal families were determined using a radionuclide labelling technique; paternity was estimated using a maximum likelihood model. Individual RS was defined as the number of offspring successfully recruited into the trappable population per adult. We found that the variance in RS among female meadow voles was greater than the variance among males. In an attempt to explain this pattern, reproductively successful individuals were compared to reproductively unsuccessful individuals with regard to survivorship, maximum body weight achieved, and spatial mobility. The only difference between fathers and reproductively unsuccessful males was that fathers were heavier. In contrast, mothers differed from unsuccessful females in every measurement. Females lived longer than males, and mothers lived longer than either fathers or reproductively unsuccessful females. The observed differences in longevity may have been largely the result of differences in levels of mobility, assuming more mobile voles were more susceptible to predation. Mothers were significantly more site tenacious than were either males or unsuccessful females. These patterns explain the distribution of RS in our population if predation differentially affects male and female meadow voles. The meadow vole is the only non-polyandrous vertebrate reported to date in which the variance in RS among females exceeds the variance in RS among males.     

Prolonged mating in the milkweed leaf beetle Labidomera clivicollis clivicollis (Coleoptera: Chrysomelidae): a test of the “sperm-loading” hypothesis

Summary Female milkweed leaf beetles (Labidomera clivicollis clivicollis) frequently mate with more than one male, and pairs form mating associations which last for up to 42 h in the field. I tested the hypothesis that males remaining with females for long periods of time benefit by numerically overwhelming the sperm of their competitors. Male L.c.clivicollis copulated intermittently with females throughout an 11 hour period in the laboratory. When virgin females were allowed a single copulation, 94.3% of the sperm they received were located in the spermatheca immediately afterward. Males were not sperm-depleted, for they had large numbers of sperm available after one copulation (mean=230,000±43,200); the maximal number of sperm a male transferred to a female in 24 h was 30,500. There was a positive linear relationship between the number of sperm transferred and time up to 24 h after mounting (r ²=0.178, P<0.003). These data suggest that males transfer increasing numbers of sperm throughout a 24-h-period. Mating duration was the most important determinant of paternity when females were placed with one male for 24 h and another male for 6 hours. Females whose first matings were longer showed first male sperm predominance (as determined by starch-gel electrophoresis), while females whose second matings were longer showed last male sperm predominance. In view of these data, it is puzzling that males do not inseminate with large numbers of sperm immediately after mounting the female. It is possible that female refractory behaviors make insemination difficult and favor prolonged mating by male milkweed leaf beetles.     

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.     

Territory ownership and familiarity status affect how much male root voles (Microtus oeconomus) invest in territory defence

Neighbour–stranger discrimination occurs when individuals respond with more aggression to strangers than to territorial neighbours—a phenomenon termed the “dear enemy phenomenon” (DEP). We investigated the DEP with male and female root voles (Microtus oeconomus Pallas 1776) using field dyadic arena tests conducted in enclosures where we could test for the effects of familiarity (familiar versus stranger), ownership (resident versus intruder status) and resource-holding potential (body mass) on territorial behaviours. The results showed that males put more effort into territorial defence than females, and males could discriminate between neighbours and strangers. In males, aggressiveness was influenced by a significant two-way interaction between treatment and ownership. Male residents were more aggressive towards stranger intruders than towards neighbour intruders, while male intruders were less aggressive towards stranger residents than towards neighbour residents. In females, neither treatment nor ownership status had a significant effect on aggressiveness. Familiar males performed more social behaviours but less non-social behaviours than stranger males. Furthermore, there was a clear dominance hierarchy between residents and intruders in stranger dyads, with the male territory holders dominating the intruder in pairwise interactions. To our knowledge, these results demonstrate for the first time DEP in a small mammal with a known pedigree and present the first evidence for “prior resident advantage” in voles. We argue that both ownership status and familiarity status affect how much an individual invests in territory defence. The benefits of neighbour–stranger discrimination for male root voles and the absence of neighbour–stranger discrimination in female root voles are discussed.     

The evolution of marmot sociality: I. Why disperse late?

Summary Prolonged toleration of offspring in marmots was hypothesized to be (1) a means of preventing dispersal of undersized young (Barash 1974 a) or more generally (2) continued parental investment, increasing the probability of descendant survival and reproduction (Armitage 1981, 1987). These hypotheses are tested in this paper for one of the most social of marmot species, the alpine marmot. The animals studied lived in groups within territories defended by a dominant male and female, or as floaters lacking a well-defined home range. Offspring did not disperse before sexual maturity at age 2 (Fig. 1). Only territorial females bred, whereas territorial males were not able to monopolize reproduction likewise (Table 2). Dispersers had similar spring mass to nondispersers (Table 4). Hence, hypothesis 1 is not supported, at least not for adult-sized, > 2 years old animals. During their residency, 19% of subordinates obtained their natal territory or a neighboring one (Fig. 2). Long distance dispersal bore a high mortality risk. Thus, toleration of mature offspring could well represent parental investment. Other results, however, suggest additional influences on the timing of dispersal. (i) Males dispersed later than females (Fig. 3), possibly because of mate sharing by territorial males (see Emlen 1982). (ii) The higher mass loss of dispersers during the previous winter indicates that weak animals were forced to leave (Table 5) despite presumably lower chances of becoming territorial (Table 3). (iii) Subordinate animals which could not be the offspring of both territorials present were not more likely to disperse (Fig. 3). (iv) Lower dispersal rates when immatures lived in the group (Fig. 3) may indicate benefits from the subordinates' presence for rearing young.     

Role of female territoriality in social and mating systems of Canthigaster valentini (Pisces: Tetraodontidae): evidence from field experiments

Sharpnose puffers, Canthigaster valentini (Pisces: Tetraodontidae) at Lizard Island, Australia, live in made-dominated haremic social and mating systems. The hypothesis was that mature females are restricted in their movements and can be monopolized by some males. Field experiments at Lizard Island, Great Barrier Reef, between January and March 1983 showed that mature females were still territorial in the absence of males and movements of females were not controlled by males. Males abandoned their territories when their females were removed. The territorial behavior of those males with access to females (territorial males) restricted the access of other males (bachelor males) to them. Bachelor males took over harems and became territorial males when established territorial males were removed. The results of the experiments thus supported the hypothesis.     

Spatial organization and mating system of Microtus townsendii

Summary Space use by individual Townsend's voles, Microtus townsendii, was investigated in spring and summer by means of radiotelemetry and intensive live trapping in undisturbed grasslands near Vancouver, British Columbia. Home ranges of males were larger than those of females; females had significantly larger ranges in spring than in summer. Most males and females maintained territories free of individuals of the same sex in spring. Male-female pairs had their exclusive territories closely overlapping each other. The 1:1 operational sex ratio and the spatial association of pairs of males and females suggest that the voles were monogamous in the spring of 1988 and that 50% of the males were monogamous in the spring of 1989. In summer, there was more intrasexual overlap between home ranges of males and females and female ranges were considerably smaller than those of males. Females were more philopatric than males and females thought to be members of the same family group lived adjacent to each other or had overlapping home ranges. Males overlapped with more than one female in summer, but most females still overlapped with only one male, which suggests that the mating system is polygynous in summer. Thirty-five percent of the philopatric females became pregnant for the first time when the male spatially associated with their mother in the spring was still alive and thus could potentially have mated with their fathers. Male and female territoriality in spring is the proximate mechanism for the limitation of breeding density by spacing behaviour.[/p] Offprint requests to: C.J. Krebs     

Female territoriality and the function of scent-marking in a monogamous antelope (Oreotragus oreotragus)

In monogamous species, females often choose between males according to the quality of the territories they defend, but the extent to which females themselves contribute to territory defence is frequently underestimated. Here we test for differences in male and female roles during paired scent-marking bouts, a key component of territorial defence, in a monogamous antelope. In two populations (Kenya, Zimbabwe) of klipspringer, Oreotragus oreotragus, both males and females usually scent-marked at the same site, but there were significant differences between sexes in terms of investment within bouts. Females initiated most bouts, thus dictating the marking strategy of the pair. Males initiated relatively few bouts, but deposited more scent marks per bout than females and were usually the last to scent-mark before leaving the site; they marked on the same branches as the female and thus overmarked her scent. Both sexes deposited more marks during paired than solo visits. Immediately preceding and following scent-marking bouts, males approached females and females left males more often than expected. Female scent-marking rates were higher when they were receptive than at other times, and this increase was matched by elevated marking rates of males. Females may increase marking rates when they are receptive in order to test the quality of their mate or to incite male competition. However, these ideas are unlikely to explain female scent-marking behaviour outside the mating season, which appears to be related primarily to territorial defence. We suggest that these differences in investment in scent-marking bouts are consistent with predictions that females may be autonomously territorial and that overmarking of female scent by males is a form of mate-guarding. Received: 17 November 1999 / Received in revised form: 24 February 2000 / Accepted: 13 March 2000     

Kinships in a natural meadow vole population

Summary We have devised a radionuclide technique that allows the assessment of matrilineal kinship by the transfer of unique combinations of gamma-emitting radionuclides from pregnant and lactating female meadow voles (Microtus pennsylvanicus) to their offspring. A pool of prospective fathers can be established from field records of reproductively active males that were alive at the time of conception of the female's litter. Electrophoresis of 6 proteins allowed us to eliminate genetically incompatible males from the prospective pool of fathers. A log-likelihood statistic provided an estimate of the probability of paternity. In the case of numerical ties physical proximity of the males to the mother at the time of conception was used. With these techniques, we established 40 kinships in a field population of meadow voles.     

Sex differences in fitness following a group take-over among Toque macaques: testing models of social evolution

Summary A group of toque macaques took-over the home range of one of its subordinate neighboring groups and fused with it to form a larger cohesive group. In the 7 years before the take-over, the dominant group had consistently won all contests at common feeding sites, yet the fitnesses of the females of these two groups did not differ significantly (Fig. 2A). After the take-over the females of the subjugated group occupied the lowest ranks in the combined dominance hierarchy of the merged groups (Fig. 1) and thereby lost the advantages of an own home range, such as priority of access to food. Consequently, in the merged group, survivorship and reproductive success among the subjugated females were significantly less than among the females of the dominant subgroup (Table 2, 4). The dominant matrilines grew numerically and replaced all of the subjugated females, and all but one of their offspring, within 8 years after the take-over (Fig. 2B). These data support the hypothesis that cooperation among female kin in defending resources against strange females is important in the evolution of female-bonded groups. Before the merger all 5 natal males of the subordinate group had transferred to the dominant group, where they occupied high and mid-level dominance ranks (Fig. 1). These males survived at a significantly greater rate than their subordinate female kin. Thus, the cost of group transfer seems to be greater for females than for males, and this may be one reason that females generally do not emigrate or that groups do not fuse. The data suggested three hypotheses. First, since large body size and other adaptations for fighting, giving males an advantage in male-male competition for mates, are also of advantage in resource competition with males and females, such male characters may also be favored by non-sexual selection, especially where male reproductive strategy involves group transfer. Second, female bonded groups evolved as female defensive coalitions against not only female but also male resource competitors, there having been a mutual influence in the coevolution of large-sized males and female gregariousness. Third, female defensive coalitions against large-sized aggressive males are also advantageous out-side the context of food competition, or, independent of foraging strategy.     

The reproductive behavior of Anthidium manicatum (Hymenoptera: Megachilidae) and the significance of size for territorial males

Summary Males of the wool-carder bee, Anthidium manicatum, patrol clumps of garden plants. Females of this species visit these plants for pollen, nectar, and pubescence; they also mate there. Females are polyandrous, with intervals between copulations as short as 35 s. Patrolling males defend their territories (0.1–1.3 m²) against other males and against other species of flower-visiting insects. Honey bees may be rendered unable to fly by the attacks of A. manicatum.Territory owners perform exploratory flights to other males' territories, changing territories often (median ownership 4–7 days; maximum 30 days) and flying up to 450 m to establish new territories. Territorial usurpations are nearly always by larger males.Female visitation rate is significantly correlated with number of flowers on a territory. The head size of territory-owner males shows significant correlation with territorial quality (measured by number of flowers, not area) and thus with number of female visits and copulatory opportunities. Some males fail to maintain territories and instead attempt to forage and copulate in other males' territories while the owners are otherwise occupied. Nonowner males are significantly smaller than owners, forage less often and from fewer flowers, and achieve significantly fewer copulations than owners. Females, however, do not reject smaller, nonowner males at a higher rate than they do larger, owner males; their choice for male size appears to be indirect, based instead on choice of food resource.The interval between a copulation and the male's next attempt with a different female is not shorter than that involving the same female. Males do not escort just-mated females about their teritories, as observed in Anthidium maculosum. Territorial behavior in this species most likely evolved through intrasexual competition for reproductive success which led to sexual dimorphism. The defense of a resourcebased territory is the mechanism used by a male to maximize his reproductive potential.     

Attraction and learning in mate-finding by solitary bees,Lasioglossum (Dialictus) figueresi Wcislo and Nomia triangulifera Vachal (Hymenoptera : Halictidae)

Summary Males of the solitary sweat bee, Nomia triangulifera, patrol over large areas where thousands of females emerge, searching for receptive females. The daily operational sex ratio is strongly male-biased. Males contact dead, frozen (untreated) females more frequently than they contact females which were washed in hexane, showing that olfactory cues are utilized in mate-finding. A major source of female sex pheromone is in the head. Male pouncing on females is temporally non-random, indicative of group stimulation. Bioassays show that newly emerged females are more attractive to males than are older pollen-collecting females. Female odors are individually distinctive, based on male responses, and there is much variation among females in their attractive properties. Male responses to female odors suggest that learning is important for mating in natural populations. In contrast, the following hypotheses are unlikely to account for the observed behavior: (1) dissipation of female odors; (2) site learning and avoidance behavior by males; (3) decay of male motivation; or (4) male-produced repellents effective against other males. Laboratory and field studies show that female Lasioglossum figueresi produce individually-distinctive odors, which are attractive to males. There is considerable inter-individual variation among females in their attractiveness to males among sexually immature females. Male responses to female odors decay over the course of the presentation, suggesting the importance of learning in natural populations, although several alternatives could not be tested.     

Female preferences for male calling bout duration in a field cricket

Summary The calls of male field crickets attract sexually receptive females. In Gryllus integer, males differ from one another in their durations of uninterrupted calling (calling bout lengths). Tape recordings of the calls of 50 wild-caught males revealed that 14 males spent most of their calling time in short bouts (Fig. 1A), 18 in both short and long bouts (Fig. 1B), and 18 in long bouts (Fig. 1C). Re-recordings of 32 males after 3 weeks showed that calling bout lengths of individual males are stable with time (age) (Fig. 2). Three phonotaxis experiments investigated whether calling bout lengths of males affect female preferences. They demonstrated that (1) females can discriminate among conspecific males on the basis of calls alone; (2) females are preferentially attracted to males with long calling bout lengths; and (3) calling bout length is the specific factor responsible for preferential attraction. These results precisely identify a criterion that females use to discriminate among potential mates of their own species.     

Lekking behavior in the neotropical frog Ololygon rubra

Summary This is the first study to document in detail the satisfaction of Bradbury's four criteria for categorizing any anuran as a classical lekking species. The paternal care of male neotropical frogs, Ololygon rubra, consisted of minimal contributions of their genes. Males competed acoustically at traditional, defended, clustered sites (Fig. 1, Table 3) to attract gravid females, who paired with the males at these locations but took the amplectant males to oviposition sites away from the pairing sites. Individual males apparently did not control resources necessary for attracting females, because there were no correlations between male numbers and measured habitat variables, or between male numbers and oviposition sites. On chorusing nights, males always arrived at their display arenas before any females were observed. Females moved freely among clusters and males, before making their choices of mates. However, males employed other mate acquisition strategies that tended to undermine the initial female choices. The predictions that lekking species should have a relatively extended breeding season, a highly biased operational sex ratio (OSR), and an absence of male control of resources essential for female acquisition were also evaluated and corroborated. These frogs have two long breeding seasons encompassing a total of about 6 months (Fig. 2). There were strongly male biased nightly OSRs (Table 1), that contributed to high variance in male reproductive success (RS), but reduced indices of sexual selection, and a relatively low coefficient of variation (CV) of male RS (Table 5) compared to other amphibians. Thus, all of this evidence supports the conclusion that O. rubra in coastal Guyana uses a lek mating system.     

Sex ratios in high-density populations of the montane vole,Microtus montanus,and the behavior of territorial males

Summary Montane voles (Microtus montanus nanus, Rodentia: Muridae) were studied in unconfined populations and in an exclosure in open fields in Wyoming, USA. Field work involved capture-mark-recapture grids, tagging select individuals with irradiated wires, subcutaneous implantation of dye pellets, and behavioral observations.Territorial males were found in both high and low density populations. They were characterized as having scrotal testes, actively defended territories, residency over time, association with females, few scars, and scent-marking behavioral patterns.Males maintaining territories in high-density populations were nearly the only males in breeding condition. Five high-density populations were trapped in late fall, and age distributions were determined by an eye lens technique. There were two age cohorts of territorial males: those born earlier in the season and those which had overwintered. For each grid, the distribution of males by age was discontinuous at about 95 days. The ratio of older males to older females of comparable ages in these five populations varied between 1:2.1 and 1:3.8. The operational sex ratio was even more unequal.The observations of territoriality at such high densities did not support the hypothesis that territoriality and social rank are two poles of a behavioral continuum related to density.The system of polygyny found, wherein the male has a territory overlapping those of several females, does not neatly fit previous schemata considered favorable for the evolution of polygyny, but is considered adaptive in view of female movements and the labile response of female reproduction to the male.     

How do weaponless male fiddler crabs avoid aggression?

Mimicry of females enables weaker males in many species to avoid intrasexual aggression. In fiddler crabs (Uca annulipes), males use their major claw in aggressive interactions to acquire and defend a territory. Males that have autotomised their major claw will be disadvantaged in fighting, but might use their temporary resemblance to females to avoid costly aggressive encounters with other males. We investigated whether: (1) courting males mistake clawless male fiddler crabs for females; (2) clawless males are able to acquire, defend and retain territories as successfully as intact males; and (3) clawless males are more cautious than intact males. Clawless and intact males differed in burrow acquisition methods and fighting behaviour, but were equally successful at acquiring and retaining burrows. While courting males treated clawless males as female, we found no evidence that clawless males mimic the behaviour of females, or that they exploit the advantage of their mistaken identity. Clawless males further appear to avoid male aggression by altering their territorial strategies to minimise the potential for conflict.     

Mating patterns and a test for female mate choice in Etheostoma spectabile (Pisces,Percidae)

Neither size nor breeding color correlated with spawning success of male orangethroat darters, Etheostoma spectabile (Pisces, Percidae), under natural field conditions. When females were presented experimentally with a simultaneous choice they spent no more time in proximity to large than small males, and were subsequently no more likely to spawn with large than with small males. Females also displayed no preference for bright versus dull males. Males and females did not differ significantly in size. Etheostoma spectabile may lack sexual size dimorphism as a result of the lack of female choice for size and the ineffectiveness of male attempts to monopolize females, or selection may be for increased size of females. Males are not dwarfs because of sperm competition. Contest competition among males appeared to be important in initiating spawnings but many males obtained spawnings by participating in ongoing spawning events. Etheostoma spectabile is an example of a sexually dimorphic species with no evident female preference for male size or color.     

Female choice in sage grouse: the roles of attraction and active comparison

Previous studies of female choice in sage grouse Centrocercus urophasianus have implicated both the acoustic quality and repetition rate of the stereotyped strut display as putative cues for female choice. Stages in the choice process at which specific components of male courtship display influence female decisions were investigated using field observations of female pre-mating behavior. Females visited a subset of territorial males and then actively chose one of these as a mate. The order in which males were visited suggested that females searched until an acceptable mate was found, rather than employing a “best-of-n” tactic. Numbers of females visiting a male were related to differences in an acoustical component of display (inter-pop interval) whereas the probability that a visiting female mated was related to display rate (Table 3), indicating that initial attraction and active choice are influenced by different components of display. In addition, inter-pop interval and display rate tended to covary inversely (Fig. 1), suggesting that attraction and active choice may impose conflicting selection pressures on display performance. Received: 11 November 1995/Accepted after revision: 16 March 1996