Satellite Males Research Articles

Intersexual dynamics mediate the expression of satellite mating tactics: unattractive males and parallel preferences

Male green treefrogs, Hyla cinerea, attract both potential mates and satellite males with their advertisement calls. Males using the satellite mating tactic position themselves silently near a calling male and attempt to intercept females attracted to the caller. Although use of conditional mating strategies may result from competition among males, few studies have considered the importance of female mate-choice preferences on the adoption and expression of alternative mate-acquisition behaviours. In this study, I tested two hypotheses. First, satellite males produce relatively unattractive advertisement signals and hence are at a competitive disadvantage when using the primary tactic. Second, satellite males associate with males producing the most attractive advertisement calls and hence increase the chance that they will intercept a female. Satellite males recorded in the field produced advertisement calls higher in frequency and shorter in duration than those produced by callers. Females consistently preferred the lower-frequency call alternative presented in two-speaker choice experiments, although they showed no preference in regard to call duration. In a second set of two-speaker choice experiments, noncalling males showed phonotactic behaviour similar to that of females, and their acoustic preferences roughly paralleled those of females. This phonotactic response may enable males producing unattractive calls to use the satellite mating tactic in a manner that maximizes potential reproductive fitness.

Steroid hormones in bluegill, a species with male alternative reproductive tactics including female mimicry.

The proximate mechanisms underlying the evolution and maintenance of within-sex variation in mating behaviour are still poorly understood. Species characterized by alternative reproductive tactics provide ideal opportunities to investigate such mechanisms. Bluegill (Lepomis macrochirus) are noteworthy in this regard because they exhibit two distinct cuckolder (parasitic) morphs (called sneaker and satellite) in addition to the parental males that court females. Here we confirm previous findings that spawning cuckolder and parental males have significantly different levels of testosterone and 11-ketotestosterone. We also report, for the first time, that oestradiol and cortisol levels are higher in cuckolders than in parental males. The two cuckolder morphs did not differ in average levels of any of the four hormones. However, among satellite males which mimic females in appearance and behaviour, there was a strong negative relationship between oestradiol levels and body length, a surrogate for age. This finding suggests that for satellite males, oestradiol dependency of mating behaviour decreases with increasing mating experience. Although such decreased hormone dependence of mating behaviour has been reported in other taxa, our data represent the first suggestion of the relationship in fishes.

The role of visual and chemical cues in the mating decisions of satellite male horseshoe crabs, Limulus polyphemus

Satellite male horseshoe crabs form spawning groups around some nesting pairs (female plus attached male) while leaving others to nest alone. Furthermore, females of pairs that attract satellites are larger and lay more eggs than females of pairs that do not attract satellites. We experimentally tested whether satellite males use visual cues to discriminate among large and small females and if satellites use chemical cues from eggs to distinguish among females. We conducted experiments in the field in the northern Gulf of Mexico at Seahorse Key, FL, U.S.A. in which we observed the behaviour of satellite males as they approached cement models of horseshoe crab pairs. Satellites were significantly more likely to approach and join model pairs with large females than with small females. However, there was no difference in the length of time satellites remained joined to the models. When chemical cues were examined, there was no difference in the number of males that approached or joined identical female models with and without eggs. However, once a satellite joined, it remained attached significantly longer to the model pair with eggs underneath. This study shows that satellite male horseshoe crabs use multiple cues, first visual to locate nesting pairs, then chemical to decide whether to remain with a nesting female. Our results show that males that are approaching from the water use visual cues from the amount of exposed carapace to distinguish the size of females nesting on land, even when those females are well buried in the sand.

Ecological Correlates of Roost Fidelity in the Tent-Making Bat Artibeus watsoni

Roost switching is a common occurrence in bats, yet the causes and consequences of such behavior are poorly understood. In this study we explore the ecological correlates of roost fidelity in the tent-making bat Artibeus watsoni, particularly focusing on the effect of sex, reproductive status, and roost availability using a three-factor general linear model (GLM). We estimated roost fidelity of radio-tracked individuals and found that the GLM was significant (R2 = 0.72, F10,34 = 8.91, p < 0.001). Significant interaction terms were observed for relative roost availability and sex (F4,34 = 16.96, p < 0.001), and relative roost availability and reproductive status (F6,34 = 7.62, p < 0.001), indicating that variation in roost fidelity among males and females, and among individuals under different breeding conditions, depended on relative roost availability at the site where they were radio-tracked. Individuals in areas of high roost availability exhibited lower roost fidelity than those sampled in areas of lower roost availability. Females exhibited less roost fidelity than males for all roost availability categories, but the difference between males and females was only significant at high roost availability. The general pattern of decreased roost fidelity as roost availability increased was also prevalent among individuals in different breeding conditions. Additionally, satellite males exhibited higher roost fidelity than resident males in areas of low roost availability, and lactating females had higher roost fidelity than non-breeding females in areas of medium roost availability. Our study thus demonstrates that sex, reproductive status, and roost availability all affect roost fidelity in the tent-making bat A. watsoni, and also suggests that roost availability is the most important factor influencing roost fidelity in this bat, providing the first quantitative evidence that roost fidelity is correlated with roost abundance in a single species.

Reproductive-Tactic-Specific Variation in Sperm Swimming Speeds in a Shell-Brooding Cichlid1

Theory predicts that males experiencing elevated levels of sperm competition will invest more in gonads and produce faster-swimming sperm. Although there is ample evidence in support of the first prediction, few studies have examined sperm swimming speed in relation to sperm competition. In this study, we tested these predictions from sperm competition theory by examining sperm characteristics in Telmatochromis vittatus, a small shell-brooding cichlid fish endemic to Lake Tanganyika. Males exhibit four different reproductive tactics: pirate, territorial, satellite, and sneaker. Pirate males temporarily displace all other competing males from a shell nest, whereas sneaker males always release sperm in the presence of territorial and satellite males. Due to the fact that sneakers spawn in the presence of another male, sneakers face the highest levels of sperm competition and pirates the lowest, whereas satellites and territorials experience intermediate levels. In accordance with predictions, sperm from sneakers swam faster than sperm from males adopting the other reproductive tactics, whereas sperm from pirates was slowest. Interestingly, we were unable to detect any variation in sperm tail length among these reproductive tactics. Thus, sperm competition appears to have influenced sperm energetics in this species without having any influence on sperm size.

Reproductive tactics of sexes and fitness in the dragonfly, Diastatops obscura.

The sexual selection strategies of territorial Odonata that do not present courtship behavior is still not completely understood, especially the role of the females. Diastatops obscura Fabricius (Odonata: Libellulidae) females participate in mate selection in a passive manner, allowing copulation with the first male that captures them and afterwards choosing whether to oviposit or not. This study introduces the idea of female passive choice as an adaptative tactic in intersexual selection. Also discussed is the adaptative value of this tactic and its flexibility according to environmental conditions and reproductive strategies adopted by the males. A natural population of Diastatops obscura was observed in the Pitimbu River of northeast Brazil. Focal continuous and ad libitum techniques were used to record attempted copulation, copulation, and oviposition behavior, in addition to registering male territoriality. An estimate of individual reproductive success (IRS) was obtained by recording 187 reproductive events. Territorial males, mainly occupying areas near the river margin, achieved greater copulation and oviposition success (IRS = 0.371) than did satellite males (IRS = 0.028). Females that copulated with territorial males experienced, for the most part, only one copulation and oviposition event, while those that copulated with satellite males fled or performed a second copulation with a territorial male. Thus, the best tactic adopted by the D. obscura males was to occupy a territory providing the greatest access to females, while the females used passive choice for fitness optimization.

Pseudocopulation and male-male conflict elicited by subadult females of the subsocial spider Anelosimus cf. studiosus (Theridiidae)

AbstractIn spider species with first male sperm priority, males guard subadult females as a tactic for improving their paternity. Preliminary observations in Anelosimus cf. studiosus, a subsocial species from Uruguay, showed that males court and guard subadult females. To elucidate the sexual tactics of this species, we placed two adult males with one adult female, and two other males with one subadult (penultimate) female under laboratory conditions (20 trials for each female status/group). Males courted both adult and subadult females, and subadult females were as receptive as adults, adopting the acceptance posture and pseudocopulating with males. Males performed conspicuous fights under both situations. Winner males copulated (or pseudocopulated), while the losers remained as satellites. Some females remated with satellite males. Subadult female behaviour simulating the adult receptive display could be a cheating tactic for retaining males and eliciting combats. Male-male fights and the guarding of subadult females suggest the occurrence of first male sperm priority, but the persistence of satellite males also suggests second males have some degree of paternity success. Competition could be caused by an asynchrony in female maturation at the beginning of the reproductive season, turning adult females in to the scarce resource.

Alternative tactics and individual reproductive success in natural associations of the burying beetle, Nicrophorus vespilloides

Alternative reproductive tactics can be maintained through different evolutionary avenues. They can be genetically or stochastically determined, in which case they must yield equal fitness, or their use can be conditional, in which case the fitness payoff of alternatives may differ. We attempted to assess the reproductive success of alternative reproductive tactics employed by wild male and female burying beetles in natural associations on carcasses placed in the field. A beetle’s reproductive tactic was defined by its potential involvement in care of larvae, and parentage was assessed using oligolocus DNA fingerprinting of offspring and potential parents. Both in males and in females, alternative tactics yielded significantly different reproductive benefits: subordinate females (brood parasites) and males (satellite males) had considerably lower reproductive success than dominant or uncontested individuals. Joint breeding was too infrequent for statistical inferences, generating intermediate offspring numbers. About 15% of offspring were sired by males not present on the carcass, suggesting that mating away from reproductive resources can produce reproductive benefits to males. Our results, in concert with the observation that beetles using one tactic can be manipulated into employing the alternative, support the notion that Nicrophorus vespilloides uses alternatives conditionally, opportunistically employing lower-benefit tactics when more profitable tactics are not available, or as additional ‘‘on-the-side’’ tactics to bolster reproductive success. Key words: alternative tactics, brood parasitism, burying beetles, communal breeding, DNA fingerprinting, Nicrophorus, parentage, satellite males. [Behav Ecol]

COMPARATIVE PHYLOGENETIC ANALYSIS OF MALE ALTERNATIVE REPRODUCTIVE TACTICS IN RAY-FINNED FISHES

Using comparative phylogenetic analysis, we analyzed the evolution of male alternative reproductive tactics (MARTs) in ray-finned fishes (Actinopterygii). Numerous independent origins for each type of MART (involving sneaker males, female mimics, pirates, and satellite males) indicate that these behaviors have been highly labile across actinopterygiian evolution, consistent with a previous notion that convergent selection in fishes can readily mold the underlying suites of reproductive hormones into similar behaviors. The evolutionary appearance of MARTs was significantly correlated with the presence of sexually selected traits in bourgeois males (P = 0.001) but not with the presence of male parental care. This suggests that MARTs often arise from selection on some males to circumvent bourgeois male investment in mate monopolization, rather than to avoid male brood care per se. We found parsimony evidence for an evolutionary progression of MARTs wherein sneaking is usually the evolutionary precursor to the presumably more complex MARTs of female mimicry and cooperative satellite behavior. Nest piracy appears not to be part of this evolutionary progression, possibly because its late onset in the life cycle of most ray-finned fishes reduces the effects of selection on this reproductive tactic.

Complex Non-Aerial Contests in the Lekking Butterfly Charis cadytis (Riodinidae)

Lekking butterflies typically defend territories using acrobatic aerial pursuits. Focal-method observations on marked Charis cadytis in SE Brazil revealed an unusual lek organization in which contest males disputed small core areas, whereas non-combative satellite males perched just outside their borders. Territorial interactions commonly began with two adversaries facing one another in a slow, non-contact ascending flight seemingly related to assessment. In disputes that continued, rival males perched on leaves where they engaged in one or more pushing bouts separated by short pursuits. In these sumo-like contests, obliquely facing males pushed their partially opened wings against one another until one was tilted sideways and flew off. Contest structure may be controlled by intruders that, by perching, provoke low-intensity contests that help prolong their stay in high-quality mating areas.

COMPARATIVE PHYLOGENETIC ANALYSIS OF MALE ALTERNATIVE REPRODUCTIVE TACTICS IN RAY-FINNED FISHES

Using comparative phylogenetic analysis, we analyzed the evolution of male alternative reproductive tactics (MARTs) in ray-finned fishes (Actinopterygii). Numerous independent origins for each type of MART (involving sneaker males, female mimics, pirates, and satellite males) indicate that these behaviors have been highly labile across actinopterygiian evolution, consistent with a previous notion that convergent selection in fishes can readily mold the underlying suites of reproductive hormones into similar behaviors. The evolutionary appearance of MARTs was significantly correlated with the presence of sexually selected traits in bourgeois males (P = 0.001) but not with the presence of male parental care. This suggests that MARTs often arise from selection on some males to circumvent bourgeois male investment in mate monopolization, rather than to avoid male brood care per se. We found parsimony evidence for an evolutionary progression of MARTs wherein sneaking is usually the evolutionary precursor to the presumably more complex MARTs of female mimicry and cooperative satellite behavior. Nest piracy appears not to be part of this evolutionary progression, possibly because its late onset in the life cycle of most ray-finned fishes reduces the effects of selection on this reproductive tactic.

Asynchronous arrival pattern, operational sex ratio and occurrence of multiple paternities in a territorial breeding anuran, Rana dalmatina

Understanding why females mate multiply is a major issue in evolutionary ecology. We investigated the consequences of an asynchronous arrival pattern on male competition and multiple paternity in the apparently monoandrous agile frog (Rana dalmatina). The largest frogs arrived first and both males and females lost weight significantly during the spawning period. Asynchronous arrival at breeding sites resulted in a male-biased operational sex ratio (OSR). The OSR was more strongly male-biased at the beginning and at the end of the breeding period when the number of satellite males increased. All females mated only once, but multiple paternity within clutches occurred at the beginning and the end of the breeding period. The influence of asynchronous arrival and biased sex ratio suggests that reduced variance or bet-hedging promoting female fitness had only a reduced role in the evolution of polyandry, and polyandry is likely to be associated with male benefits. Polyandry in frogs can be explained either by forced mating as a result of sexual conflict or by clutch piracy. By modifying intrasexual competition, asynchronous arrival and changes in OSR may have a decisive influence upon the evolution of mating systems and favour both polyandry and stable coexistence of alternative mating behaviour.

Eye and clasper damage influence male mating tactics in the horseshoe crab, Limulus polyphemus

In the horseshoe crab mating system, mated pairs are frequently accompanied by unattached satellite males as they spawn on intertidal beaches. Previous studies have shown that males locate females visually using their lateral (compound) eyes, and that attached (mated) males generally have less heavily worn or damaged carapaces than unattached males. The purpose of this study was to investigate the influences of lateral eye condition and clasper abnormalities on male mating tactics. Sexually mature males had two kinds of eye damage: deterioration caused by disease, and overgrowth by sessile invertebrates, such as bryozoans, mussels, and tube-building polychaetes. The lateral eyes of attached males had significantly less decay than unattached males. On the other hand, coverage of the lateral eyes by encrusting invertebrates was more extensive among attached than unattached males. Although overgrowth did not appear to impair a male’s ability to pair with a female as severely as eye decay, it is conceivable that amplexus may have occurred before epibiont coverage was sufficient to obscure vision. Male crabs that were experimentally “blindfolded” by painting their lateral eyes with black nail polish were less likely to reattach to a female than controls. Appendage injuries were more frequent among unattached males than among attached males; in particular, 6.4% of unattached males but 0.0% of attached males had damaged claspers (the modified first legs required for amplexus). Unattached males in the population were “older,” as judged by the degree of carapace wear, than attached males. Severe visual impairment and/or clasper damage may explain the reduced pairing success of older male horseshoe crabs, and underlie their choice of the alternative satellite male mating tactics.

Body size, age, growth and alternative mating tactics in toads: satellite males are smaller but not younger than calling males

Body size–age relationships may have important implications for the evolution and maintenance of alternative mating tactics, but these relationships remain largely unexplored in anuran amphibians (frogs and toads). In a single territorial anuran species, smaller noncalling ‘satellite’ males are younger than calling males. These results have led to the general assumption that such an age difference also holds for other anuran species with body size differences among behavioural phenotypes. However, individuals of many organisms show different developmental and/or growth trajectories that correspond to variation in adult morphology and behaviour. To test the generality of smaller satellite males being younger than larger calling males in anurans, we examined body size–age–behaviour relationships in Woodhouse's toads, Bufo woodhousii , and Great Plains toads, B. cognatus . Age estimates, based on skeletochronologic analysis of lines of arrested growth (LAGs) from phalanges, indicated that males sampled while adopting a noncalling satellite tactic were smaller, but not younger, than males sampled while adopting a calling tactic. Furthermore, examination of inter-LAG areas of bone deposition indicated that smaller satellite male B. woodhousii showed lower growth rates relative to calling males. A similar trend occurred for B. cognatus . We discuss our results in the context of developmental patterns associated with alternative mating tactics in other species and endocrine regulation of behavioural tactics in anurans.

Description of alternative male reproductive tactics in a shell-brooding cichlid, Telmatochromis vittatus, in Lake Tanganyika

Telmatochromis vittatus (Cichlidae) is a Tanganyikan substrate brooder which spawns in the gastropod-shell nests of a cichlid, Lamprologus callipterus. We describe male reproductive tactics of T. vittatus in and around the shell nests, where males of various sizes were found. Based on utilization patterns of the shell nests, interactions among males, and spawning behaviors, males could be categorized into four types based on reproductive tactics and in order of body size: sneaker males, satellite males, territorial males and piracy males. Size range of males in tactic groups rarely overlapped. Territorial males defended shell nests harboring multiple females, but during pair-spawning they were occasionally taken over by large piracy males that visited several nests repeatedly. Small sneaker males darted to pair-spawning territorial males and might ejaculate sperm. Satellite males did not perform parasitic spawning but pair-spawned in a single shell outside the nests. Spawning of satellite males was infrequently parasitized. The largest gonado-somatic index (GSI) was found in sneaker males followed by piracy males, territorial males and satellite males, suggesting that gonadal investment of males using the four tactics may be consistent with intensity or risk of sperm competition.

Arginine vasotocin activates advertisement calling and movement in the territorial Puerto Rican frog, Eleutherodactylus coqui

Arginine vasotocin (AVT) is a neuropeptide that modulates social behavior in amphibians and activates calling in frogs. The Puerto Rican coquí frog, Eleutherodactylus coqui, is a terrestrial anuran that exhibits complex social behaviors, including territoriality and paternal care. Males have a distinctive social hierarchy and can be any of the following: satellite (non-calling), territorial (calling), or paternal (guards and broods embryos). Field experiments were conducted to determine the effects of AVT on satellite behavior and the male social hierarchy of E. coqui. Satellite males were captured within the territory held by a resident male, given injections (IP) of AVT or saline (control) and placed back in their original location. To determine if AVT affects all males, not merely satellite males, territorial (calling) males were injected with AVT. Significantly more satellite males commenced advertisement calling following AVT injections than did control males injected with saline. AVT-activated satellites did not challenge the resident territorial male for possession of the territory but instead moved into a new area before commencing to call. In fact, AVT-activated satellite males were significantly more likely to move into a new territory following AVT injections than AVT-injected territorial males. The effect of AVT was short lived, lasting only one night in all but two cases. It is concluded that AVT stimulates advertisement calling and AVT-activated males displayed territorial characteristics of E. coqui.

Sex, drugs and mating role: testosterone-induced phenotype-switching in Galapagos marine iguanas

Males of many vertebrate species have flexible reproductive phenotypes and must decide before each mating season whether to adopt sneaker, satellite, or territorial mating tactics. How do males gauge their abilities against others in the population? We tested experimentally whether hormone–behavior feedback loops allow Galapagos marine iguana males to activate their three behavioral phenotypes as predicted by the relative plasticity hypothesis. Territorial males defended small mating areas and had significantly higher plasma testosterone (T) levels (75 6 11 ng/ml) than did satellite males that roamed around territories (64 6 8 ng/ml) or sneaker males that behaved like females within territories (43 6 11ng/ml). In territorial males, temporary pharmacological blockade of T slowed head-bob patrolling, decreased territory size threefold, and reduced the number of females on territories 20-fold. This supports previous data that females may gauge male attractiveness by using head-bob patrolling, here shown to be a T-dependent trait. Control-treated neighbors reacted to the weakening of T-blocked males by increasing head-bob rate fivefold and territory size 1.6-fold, and female numbers increased 2.5-fold. Unmanipulated or controlinjected males remained unchanged. Behavioral effects were partly reversed after 7 days. T injections induced satellite males to establish temporary territories, even at unconventional locations. Some T-boosted satellite males suffered serious fighting injuries. T-injected sneakers left female clusters and behaved like larger satellite males that roam around territories. Thus, territorial and mating tactics are activated by T, but experimental (de-) activation at the wrong ontogenetic stage is costly: manipulated males switched phenotype but thereby lowered their access to females. We hypothesize that T levels of males that are based on early-season behavioral interactions influence a males’ subsequent phenotypic role. Key words: activationorganization of phenotypes, mating strategies, relative plasticity hypothesis, testosterone. [Behav Ecol]

Anuran Population Monitoring: Comparison of the North American Amphibian Monitoring Program's Calling Index with Mark-Recapture Estimates for Rana clamitans

Abstract The North American Amphibian Monitoring Program uses a ranked, categorical calling index to estimate anuran abundance. However, there are few data assessing the assumption that calling index values are accurate indicators of population sizes or to suggest ranges of population sizes associated with specific values of the calling index. This study compared mark-recapture population estimates and call rates to calling index values for Green Frogs (Rana clamitans) in the Upper Peninsula of Michigan. Mean mark-recapture population size estimates and mean calls per minute were greater in ponds with larger calling index values. Similarly, calls per minute increased with increasing population size, although rate of increase declined at high population sizes possibly caused by a higher proportion of noncalling satellite males at high densities. Sex ratios in breeding habitat along the edges of ponds were increasingly male biased as population size increased. These data support the assumption that calling ...

Steroid hormone profiles and relative body condition of calling and satellite toads: implications for proximate regulation of behavior in anurans

Males of most anuran species (frogs and toads) vocalize to attract mates. However, individuals of many vocal species may also adopt alternative noncalling ‘‘satellite’’ tactics. Satellite males characteristically remain in close proximity to calling conspecifics and attempt to intercept incoming females attracted to advertising males. Emerson proposed that alternation between calling and noncalling behavior in anurans is mediated by a reciprocal interaction between circulating levels of corticosterone and androgens that is driven by depletion of energy reserves during vocalization. We tested this hypothesis by examining steroid hormone profiles and the relative body condition of calling and satellite Woodhouse’s toads (Bufo woodhousii) and Great Plains toads (B. cognatus). Consistent with Emerson’s hypothesis, callers had significantly higher circulating corticosterone levels and were in better condition than satellites. However, levels of testosterone and dihydrotestosterone did not differ significantly between satellites and callers, and we found no evidence that high levels of corticosterone had an inhibitory effect on androgen production in either species. These data thus support a relationship between corticosterone levels and depletion of energy reserves during bouts of vocalization but suggest that alternation between calling and satellite behavior may be associated with direct effects of corticosterone on brain vocal control centers. We propose a model that incorporates relationships among energy reserves, androgens, corticosterone, and arginine vasotocin-producing neurons in the telencephalon to explain transitions between calling and satellite tactics in toads. Key words: alternative mating tactics, anurans, body condition, hormones, satellite behavior, steroids. [Behav Ecol 15:313–320 (2004)]

Indirect and direct acoustic aggression in cicadas: first observations in the Palaearctic genus Tibicina Amyot (Hemiptera: Cicadomorpha: Cicadidae)

Tibicina Amyot is a cicada genus of the Palaearctic biogeographical region with seven taxa (species and subspecies) distributed in France. As in other cicadas, the sound production by tymbal vibration is restricted to males. In Tibicina, males are attracted by conspecific calling songs and tend to form groups of several individuals which maintain a minimal distance between each other. Observations based upon male–male interactions in such aggregations and on some preliminary experiments conducted with males kept in captivity revealed for the first time both indirect and direct aggression. Spacing and chorusing are interpreted as a by-product of indirect aggression mediated through the calling song. Direct aggression occurred when spacing is not respected. It is achieved through a ritualistic sequence that involves mainly the production of the rivalry song, an acoustic signal previously reported in the literature for two cicada species only. In addition, satellite males and male–male courting are reported. These preliminary results suggest that the sound social organization in the genus Tibicina is more elaborate than first suspected and should be reconsidered in terms of lek behaviour and sexual selection.