Evolution of male mating behavior: male spadefoot toads preferentially associate with conspecific males

The evolution of male breeding aggregations is difficult to explain because males may reduce their reproductive success by associating with their closest competitors. We examined aggregative behavior by male New Mexico spadefoot toads, Spea multiplicata, which form breeding choruses in rain-filled pools. We specifically asked whether males are attracted to conspecific calls and, if so, whether they preferentially associate with those male calls that are also attractive to females. Field observations revealed that males showed significant clustering with conspecifics within breeding ponds, whereas laboratory phonotaxis experiments revealed that males preferentially associated with conspecific male calls. Moreover, when males were presented with conspecific calls that differed in call rate, smaller males associated with the stimulus preferred by females (average call rate). Thus, males appear to evaluate the attractiveness of competitors using the same trait employed by females to assess potential mates, and males adjust their positions relative to competitors depending on their size. We discuss these results in the light of several current hypotheses on the adaptive significance of male breeding aggregations. Received: 20 December 1999 / Accepted: 18 March 2000     

Mating behavior of female rock shrimp Rhynchocinetes typus (Decapoda: Caridea)—indication for convenience polyandry and cryptic female choice

While studies on a wide diversity of organisms have demonstrated the importance of female behavior during matings, in crustacean studies, a strong bias towards male mating behavior prevails. Reproductively mature rock shrimp (Rhynchocinetes typus) exist as several ontogenetic stages that differ in their morphological and physiological capacities. In natural populations, the majority of males are in early ontogenetic stages (termed typus), many are in intermediate stages (intermedius), and few are in the terminal molt stage (robustus). Dominant robustus males, which have already demonstrated their biological fitness by surviving to this stage, have previously been shown to have a higher potential than subordinate typus males to defend receptive females against other males, and fertilize the entire clutch of a female. While females should thus show a preference for robustus males, they nevertheless frequently receive sperm from typus males. These observations suggested that females might have mechanisms to discriminate against sperm from subordinate males. In laboratory experiments, we observed that females avoided being seized by typus males for longer time periods in the absence of robustus males than in their presence. Following seizure, females that were initially held by typus males, required more time to initiate spawning than those held by robustus males. Many typus males transferred spermatophores to females before these started to spawn while robustus males waited until females began to spawn before they transferred spermatophores. Females manipulated spermatophores received from typus males for long time periods (minutes), but not those they received from robustus males. By accepting sperm from subordinate typus males, females may avoid further harassment (convenience polyandry), but they subsequently may discriminate against these subordinate males by delaying spawning and removing their sperm. These observations suggest that female behavior influences the outcome of matings, favoring fertilization of eggs by sperm from dominant males. Convenience polyandry and cryptic female choice may be common in other crustaceans as well.Electronic Supplementary Material Supplementary material is available in the online version of this article at .Communicated by T. Czeschlik     

Adaptive peaks and alternative foraging tactics in brook charr: evidence of short-term divergent selection for sitting-and-waiting and actively searching

Some recently emerged brook charr (Salvelinus fontinalis) inhabiting still-water pools along the sides of streams are sedentary and eat crustaceans from the lower portion of the water column. Others are more active and eat insects from the upper portion of the water column. We provide evidence that this divergent foraging behavior reflects short-term divergent selection brought about by intraspecific competition in the presence of alternative food sources. Rates of encounters and interactions between individuals were density dependent, and encounter and interaction events were closely timed with prey capture attempts. In addition, aggressive fish made more foraging attempts per minute than nonaggressive fish. Aggressive fish were also either inactive or very active, while nonaggressive fish exhibited intermediate levels of activity. Growth rate potential, an important component of fitness during the early life stages of brook charr, was assessed using tissue concentrations of RNA and found to be highest for sedentary fish and for active fish making frequent foraging attempts, and lower for fish exhibiting intermediate levels of activity. Our findings support contentions that individual behavior plays an important role during initial steps in the evolution of resource polymorphisms. Received: 27 July 1998 / Accepted after revision: 16 November 1998     

Correlated evolution of prey chemical discrimination with foraging, lingual morphology and vomeronasal chemoreceptor abundance in lizards

Comparative data from ten families of lizards suggest that correlated evolution has occurred between the ability to identify prey chemicals and several aspects of lingual function and morphology, abundance of vomeronasal chemoreceptor cells, and foraging behavior. Ability to discriminate prey chemicals from control substances was measured experimentally and correlated with other variables by Felsenstein's method. This ability increased with evolutionary increases in degree of lingual protrusion during tongue-flicking, which may reflect the tongue's ability to reach substrates to be sampled. It increased with deepened lingual forking and greater lingual elongation, which may be important for scent-trailing and sampling ability, respectively. Discriminatory ability also increased with abundance of vomerolfactory chemoreceptors, which presumably reflects some aspects of analytical capacities of the vomeronasal system. Prey chemical discrimination increased with degree of active foraging. Natural selection for improved vomerolfactory sampling and analysis of prey chemicals by active, but not ambush, foragers appears to account for the observed relationships. In active foragers that use vomerolfaction to locate prey, natural selection favors increased abilities to lingually sample chemicals from environmental substrates, analyze the samples for prey chemicals, and respond appropriately if prey chemicals or possible prey chemicals are detected. Such selection can account for the observed relationships among the sampling device and its movements, the sense, the discriminations, and variations in foraging ecology. Received: 13 February 1997 / Accepted after revision: 12 June 1997     

Innate movement rules in foraging bees: flight distances are affected by recent rewards and are correlated with choice of flower type

The non-random movement patterns of foraging bees are believed to increase their search efficiency. These patterns may be innate, or they may be learned through the bees’ early foraging experience. To identify the innate components of foraging rules, we characterized the flight of naive bumblebees, foraging on a non-patchy “field” of randomly scattered artificial flowers with three color displays. The flowers were randomly mixed and all three flower types offered equal nectar volumes. Visited flowers were refilled with probability 0.5. Flight distances, flight durations and nectar probing durations were determined and related to the bees’ recent experiences. The naive bees exhibited area-restricted search behavior, i.e., flew shorter distances following visits to rewarding flowers than after visits to empty flowers. Additionally, flight distances during flower-type transitions were longer than flight distances between flowers of the same type. The two movement rules operated together: flight distances were longest for flights between flower types following non-rewarding visits, shortest for within-type flights following rewarding visits. An increase in flight displacement during flower-type shifts was also observed in a second experiment, in which all three types were always rewarding. In this experiment, flower-type shifts were also accompanied by an increase in flight duration. Possible relationships between flight distances, flight durations and flower-type choice are discussed. Received: 20 November 1995/Accepted after revision: 10 May 1996     

Effects of sex-associated competitive asymmetries on foraging group structure and despotic distribution in Andean condors

Phenotype-limited interference models assume competitive asymmetries among conspecifics and unequal sharing of resources. Their main prediction is a correlation between dominance status and patch quality: dominant individuals should preferentially exploit better-quality habitats. We tested assumptions and predictions of the phenotype-limited interference model in Andean condors (Vultur gryphus), a New World vulture with strong sexual size dimorphism (males are 30–40% heavier than females). We recorded searching birds in habitats differing in quality: mountains and plains. We also observed scavenging behaviour at 20 sheep carcasses, and videotaped 5 of them. Intraspecific hierarchy at carcasses was based on size: males dominated females and, within each sex, older birds dominated younger ones. Adult males and juvenile females occupied extreme positions in the feeding hierarchy. Aggression was directed at those individuals belonging to lower hierarchical levels. In high-quality areas (mountains), more condors arrived at carcasses. Juvenile females were more often observed searching in low-quality areas (plains), far from breeding areas and main roost sites. GLM analyses of individual behaviour showed that the hierarchy did not influence time of arrival, but low-ranking individuals spent more time at carcasses, especially if the number of condors at arrival was high. Additionally, low-ranking condors spent less time feeding at carcasses when individuals of higher hierarchical levels were present. On the other hand, the number of condors present had a positive effect on feeding rates of dominant individuals, probably because of a reduction in individual vigilance. These results support most of the assumptions and predictions of the phenotype-limited distribution model, although a spatial truncated distribution between phenotypes was not observed. Asymmetric feeding pay-off, unequal parental roles and sexual selection constraints could favour sexual divergence in body size in Andean condors. Received: 6 April 1998 / Accepted after revision: 11 July 1998     

Assessment of predation risk via illumination level: facultative central place foraging in the cricetid rodent Phyllotis darwini

It is well known that the risk of predation affects prey decision making. However, few studies have been concerned with the cues used by prey to assess this risk. Prey animals may use indirect environmental cues to assess predation hazard since direct evaluation may be dangerous. I studied the assessment of predation risk, manipulated via environmental illumination level, and the trade-off between foraging and predation hazard avoidance in the nocturnal rodentPhyllotis darwini (Rodentia: Cricetidae). In experimental arenas I simulated dark and full moon nights (which in nature correlate with low and high predation risk, respectively) and measured the immediate responses of animals to flyovers of a raptor model. Second, varying illumination only, I evaluated patch use, food consumption, central place foraging, and nocturnal variation of body weight. During flyover experiments, animals showed significantly more evasive reactions under full moon illumination than in moonless conditions. In the patch use experiments, rodents significantly increased their giving-up density and decreased their total food consumption under moonlight. On dark nights, rodents normally fed in the food patch, but when illumination was high they became central place foragers in large proportion. Moreover, the body weight of individuals decreased proportionately more during bright nights. These results strongly suggest thatP. darwini uses the level of environmental illumination as a cue to the risk of being preyed upon and may sacrifice part of its energy return to avoid risky situations.     

Effects of parasitic mites and protozoa on the flower constancy and foraging rate of bumble bees

Parasites can affect host behavior in subtle but ecologically important ways. In the laboratory, we conducted experiments to determine whether parasitic infection by the intestinal protozoan Crithidia bombi or the tracheal mite Locustacarus buchneri alters the foraging behavior of the bumble bee Bombus impatiens. Using an array of equally rewarding yellow and blue artificial flowers, we measured the foraging rate (flowers visited per minute, flower handling time, and flight time between flowers) and flower constancy (tendency to sequentially visit flowers of the same type) of bees with varying intensities of infection. Bumble bee workers infected with tracheal mites foraged as rapidly as uninfected workers, but were considerably more constant to a single flower type (yellow or blue). In contrast, workers infected with intestinal protozoa showed similar levels of flower constancy, but visited 12% fewer flowers per minute on average than uninfected bees. By altering the foraging behavior of bees, such parasites may influence interactions between plants and pollinators, as well as the reproductive output of bumble bee colonies. Our study is the first to investigate the effects of parasitic protozoa and tracheal mites on the foraging behavior of bumble bees, and provides the first report of Crithidia bombi in commercial bumble bees in North America.     

A female evolutionary response when survival is at risk: male harassment mediates early reallocation of resources to increase egg number and size

One unexplored area in sexual conflict studies is the female physiological costs and possible resource reallocation that accompany evolutionary costs due to male harassment. Using females of the damselfly Hetaerina americana, I first investigated whether male harassment affected female mating rate and survival and explored whether such effects induced a resource allocation from immunity (in the form of phenoloxidase activity) and muscular fat reserves to egg number and size. Using two seasons that differed in male harassment, it was found that the higher the male harassment, the fewer are the female matings and the lower is the female survival. These results were corroborated using an experimental approach in which a situation of high male harassment was induced. It was also found that when the first mating takes place and at high male harassment, females had more reduced phenoloxidase activity and fat reserves and tended to lay most of the eggs they produce in their lifetime and these were considerably large. However, at low male harassment, egg number and size were more equally produced across matings. Females under high male harassment seemed to suffer the survival costs but may show a plastic evolutionary response of reallocating resources to egg traits to maximize fitness.     

Changes in singing behavior of male black-capped chickadees (Parus atricapillus) following mate removal

We removed the mates of ten male black-capped chickadees (Pares atricapillus) during the nest-building period to determine the effect of female presence on dawn singing. During the first dawn chorus following mate removal, males sang significantly longer, increased movement within their territory, and increased the percentage of their territory covered while singing. After the female was returned, these parameters returned to the pre-removal values. Males did not alter the frequency range or modal frequency of their songs when the mate was removed, nor did they change the degree of frequency shifting in the fee-bee song. We conclude that dawn singing in the black-capped chickadee acts, in part, as an intersexual signal, and that the behavior of frequency shifting in the song may be directed more toward rival males than females. Correspondence to: K. Otter     

Testosterone-induced depression of male parental behavior in the barn swallow: female compensation and effects on seasonal fitness

In birds, many aspects of male socio-sexual and parental behavior are influenced by androgens, most notably testosterone (T). We report the effects of subcutaneous T-implants in male barn swallows (Hirundo rustica) on male and female parental behavior and on seasonal reproductive success. Males were assigned to one of three experimental groups: (i) implanted with a T-filled Silastic tube; (ii) implanted with an empty Silastic tube; and (iii) not implanted. T-implanted males provided a smaller proportion of feedings (number of feedings by the male/total number of feedings by both parents) and fed nestlings less frequently (number of feedings/h) than males of the other two groups. Females paired to T-implanted males fed nestlings significantly more often than females paired with unimplanted males. Females almost fully compensated for their mates' shortfall, and this resulted in similar combined feeding efforts among treatments. Reproductive success in their first broods or during the entire breeding season was unaffected by T- treatment. These results confirm earlier reports of the suppressive effects of T on male parental behavior. However, they are inconsistent with current ESS models that predict partial compensation as the optimal response by one individual to reduction of parental effort by its mate in monogamous, biparental systems.     

Nectar-receiver behavior in relation to the reward rate experienced by foraging honeybees

Since forager honeybees change their food-unloading behavior according to nectar-source profitability, an experiment was performed in order to analyze whether food-receivers modify their within-hive tasks related to different reward conditions. We offered individual foragers two reward conditions at a rate feeder while an additional feeder offered a constant reward and was of free access to the rest of the hive. Both feeders were the only food sources exploited by the colony during the assays since a flight chamber was used. After receiving nectar, hive bees performed processing cycles that involved several behaviors and concluded when they returned to the delivery area to receive a new food sample. During these cycles, receivers mainly performed oral contacts offering food, or inspected cells, and often both. In the latter case, both behaviors occurred simultaneously and at the same distance from the hive entrance. When they performed a single task, either the occurrence of cell inspections increased or contact offerings decreased for the highest reward rate offered to the donor-forager. Receivers also begged for food more often after interacting with low-profit foragers. Thus, the profitability of the food source exploited by nectar-forager honeybees could affect receiver behaviors within the hives based on individual-to-individual interactions.Communicated by R.F.A. Moritz     

Resource defense polygyny shifts to female defense polygyny over the course of the reproductive season of a Neotropical harvestman

Although studies classify the polygynous mating system of a given species into female defense polygyny (FDP) or resource defense polygyny (RDP), the boundary between these two categories is often slight. Males of some species may even shift between these two types of polygyny in response to temporal variation in social and environmental conditions. Here, we examine the mating system of the Neotropical harvestman Acutisoma proximum and, in order to assess if mate acquisition in males corresponds to FDP or RDP, we tested four contrasting predictions derived from the mating system theory. At the beginning of the reproductive season, males fight with other males for the possession of territories on the vegetation where females will later oviposit, as expected in RDP. Females present a marked preference for specific host plant species, and males establish their territories in areas where these host plants are specially abundant, which is also expected in RDP. Later in the reproductive season, males reduce their patrolling activity and focus on defending individual females that are ovipositing inside their territories, as what occurs in FDP. This is the first described case of an arachnid that exhibits a shift in mating system over the reproductive season, revealing that we should be cautious when defining the mating system of a species based on few observations concentrated in a brief period. Electronic supplementary material  The online version of this article (doi:) contains supplementary material, which is available to authorized users.     

The reproductive behavior and energetics of male gray seals (Halichoerus grypus) breeding on a land-fast ice substrate

The reproductive behavior of male gray seals (Halichoerus grypus) breeding on land-fast ice at Amet Island, Nova Scotia, was studied. Data on energy expenditure (rate of mass loss over time) were collected. The average time budget of males at Amet Island was comparable to that of land-breeding males. The behavior of males showed seasonal changes, with a decrease in the proportion of time spent in the water and an increase in agonistic behavior during the peak mating period. The estimated amount of body mass lost over the season ranged between 25.6 and 77.1 kg, and the estimated percent of initial body mass lost ranged between 7.7 and 26.5% (n=10). The maximum number of observed copulations for an individual male was nine. Only 15 out of 42 males observed during 1992 and 1993 were seen copulating. The number of observed copulations per male was strongly correlated with success in remaining close to, or attending, females (r=0.91, P<0.001, n=42). The mean duration of attendance was 4.5 ± 5.54 days (n=42). Large size was not an important factor in determining attendance success, but reproductive effort (the estimated proportion of body mass lost over the season) and success in agonistic interactions with other males were both correlated with male success.     

Parasitism in a social wasp: effect of gregarines on foraging behavior, colony productivity, and adult mortality

Behavior in eusocial insects likely reflects a long history of selection imposed by parasites and pathogens because the conditions of group living often favor the transmission of infection among nestmates. Yet, relatively few studies have quantified the effects of parasites on both the level of individual colony members and of colony success, making it difficult to assess the relative importance of different parasites to the behavioral ecology of their social insect hosts. Colonies of Polybia occidentalis, a Neotropical social wasp, are commonly infected by gregarines (Phylum Apicomplexa; Order Eugregarinida) during the wet season in Guanacaste, Costa Rica. To determine the effect of gregarine infection on individual workers in P. occidentalis, we measured foraging rates of marked wasps from colonies comprising both infected and uninfected individuals. To assess the effect of gregarines on colony success, we measured productivity and adult mortality rates in colonies with different levels of infection prevalence (proportion of adults infected). Foraging rates in marked individuals were negatively correlated with the intensity of gregarine infection. Infected colonies with high gregarine prevalence constructed nests with fewer brood cells per capita, produced less brood biomass per capita, and, surprisingly, experienced lower adult mortality rates than did uninfected or lightly infected colonies. These data strongly suggest that gregarine infection lowers foraging rates, thus reducing risk to foragers and, consequently, reducing adult mortality rates, while at the same time lowering per-capita input of materials and colony productivity. In infected colonies, queen populations were infected with a lower prevalence than were workers. Intra-colony infection prevalence decreased dramatically in the P. occidentalis population during the wet season.An erratum to this article can be found at     

Determinants of male spacing behavior in microtines: an experimental manipulation of female spatial distribution and density

Theory on microtine mating systems predicts that male spacing behavior will be related to female spatial and temporal distribution. However, data from a natural population of field voles, Microtus agrestis, indicated a potential influence of female density on the spacing behavior of males. Therefore, I experimentally investigated the relative importance of female density and female spatial distribution for the spacing behavior of males in M. agrestis. Males were radio-tracked in enclosed natural habitats in which females at different densities were placed in two different spatial arrangements: clumped versus even distribution. Female density was the main factor determining male spacing behavior. At the high female density males had smaller home ranges and moved shorter distances between radio-tracking recordings. Also, home ranges were more exclusive at high female density. However, since there was a significant positive correlation between home range size and range overlap, range exclusiveness seemed to be influenced by female density indirectly through the effect of range size. Female spatial distribution, on the other hand, had no influence on male home range exclusiveness.     

The effect of reproductive condition on the foraging behavior of female hoary bats,Lasiurus cinereus

Summary Female mammals experience larg changes in time and energy budgets associated with reproduction and these may influence the foraging strategies of individuals. I studied the changes in foraging behavior associated with reproduction in female hoary bats, Lasiurus cinereus. As lactation progressed, individuals departed to forage earlier in the evening and spent more time foraging per night and less time roosting with their young. Foraging time increased by at least 73% between early lactation and fledging and then declined as the young became independent. Females with two young foraged for longer than did those with one and females with pre- and postfledging young foraged in different habitats. The changes in foraging time suggest that foraging activity of female L. cinereus is constrained and individuals act as time minimizers, adjusting their foraging behavior to meet current energy demand. Predation risk is unlikely to constrain the behavior of these bats. However, maximizing energy intake throughout lactation may not be the optimal strategy because storing excess energy increases flight cost and may reduce foraging efficiency. The need to keep newborn young warm may also influence foraging time. Such constraints, causing changes in foraging activity, may alter the availability of habitats and prey and must be considered when modelling foraging strategies. In addition, changes in flight time may significantly alter the energy budgets of bats in different stages of reproduction.     

Effects of colony food shortage on behavioral development in honey bees

Three experiments were conducted to explore the effects of severe food shortage on the control of two important and interrelated aspects of temporal division of labor in colonies of the honey bee (Apis mellifera): the size and age distribution of a colony's foraging force. The experiments were conducted with single-cohort colonies, composed entirely of young bees, allowing us to quickly distinguish the development of new (precocious) foragers from increases in activity of bees already competent to forage. In experiment 1, colony food shortage caused an acceleration of behavioral development; a significantly greater proportion of bees from starved colonies than from fed colonies became precocious foragers, and at significantly younger ages. Temporal aspects of this starvation effect were further explored in experiment 2 by feeding colonies that we initially starved, and starving colonies that we initially fed. There was a significant decrease in the number of new foragers in starved colonies that were fed, detected 1 day after feeding. There also was a significant increase in the number of new foragers in fed colonies that were starved, but only after a 2-day lag. These results suggest that colony nutritional status does affect long-term behavioral development, rather than only modulate the activity of bees already competent to forage. In experiment 3, we uncoupled the nutritional status of a colony from that of the individual colony members. The behavior of fed individuals in starved colonies was indistinguishable from that of bees in fed colonies, but significantly different from that of bees in starved colonies, in terms of both the number and age distribution of foragers. These results demonstrate that effects of starvation on temporal polyethism are not mediated by the most obvious possible worker-nest interaction: a direct interaction with colony food stores. This is consistent with previous findings suggesting the importance of worker-worker interactions in the regulation of temporal polyethism in honey bees as well as other social insects. Received: 17 April 1997 / Accepted after revision: 26 December 1997     

Ecological niche and phylogeny: the highly complex echolocation behavior of the trawling long-legged bat, Macrophyllum macrophyllum

Bats produce echolocation signals that reflect the sensory tasks they perform. In open air or over water, bats encounter few or no background echoes (clutter). Echolocation of such bats is the primary cue for prey perception and varies with the stage of approach to prey, typically comprising search, approach, and terminal group calls. In contrast, bats that glean stationary food from rough surfaces emit more uniform calls without a distinct terminal group. They use echolocation primarily for orientation in space and mostly need additional sensory cues for finding food because clutter echoes overlap strongly with food echoes. Macrophyllum macrophyllum is the only Neotropical leaf-nosed bat (Phyllostomidae) that hunts in clutter-poor habitat over water. As such, we hypothesized that, unlike all other members of its family, but similar to other trawling and aerial insectivorous bats, M. macrophyllum can hunt successfully by using only echolocation for prey perception. In controlled behavioral experiments on Barro Colorado Island, Panamá, we confirmed that echolocation alone is sufficient for finding prey in M. macrophyllum. Furthermore, we showed that pattern and structure of echolocation signals in M. macrophyllum are more similar to aerial and other trawling insectivorous bats than to close phylogenetic relatives. Particularly unique among phyllostomid bats, we found distinct search, approach, and terminal group calls in foraging M. macrophyllum. Call structure, however, consisting of short, multiharmonic, and steep frequency-modulated signals, closely resembled those of other phyllostomid bats. Thus, echolocation behavior in M. macrophyllum is shaped by ecological niche as well as by phylogeny.     

Evidence of a maternal foraging cycle resembling that of otariid seals in a small phocid,the harbor seal

Summary Lactation strategies in the two largest families of seals have been characterized as a phylogenetic dichotomy, with sea lions and fur seals (Otariidae) exhibiting foraging cycles and true seals (Phocidae) a strategy of fasting. We show that a lactating phocid, the harbor seal, Phoca vitulina, has a foraging cycle similar to that of otariids. Time-depth recorders attached to lactating harbor seal mothers revealed that 9 of 11 females began bouts of diving, averaging 12–40 m, by mid-lactation (12 days). During the remainder of lactation, females made an average of seven diving trips, lasting about 7 h. They returned to the rookery during the interval between successive bouts to nurse their pups. Diving was more frequent during daylight than at night and diving bouts increased in duration as lactation progressed. The diving behavior of females that had weaned their pups and previously collected data from stomach lavage, suggest that the bouts of diving represent successful foraging. We propose that the lactation strategy of the harbor seal is intermediate to that of the otariids and other phocids studied. The harbor seal has a foraging cycle like the otariids, but typically resembles other phocids in length of lactation, rate of mass gain in pups, and in milk fat content. As harbor seals are among the smallest phocids, and only slightly larger than most otariids, it seems likely that maternal size constrains the amount of stored energy harbor seal females can bring to the rookery, forcing them to start feeding during the lactation period.Correspondence to: D.J. Boness