Gender Differences in the Costs that Subordinate Group Members Impose on Dominant Males in a Cooperative Breeder

In group-living species, a dominant male's ability to monopolize reproduction, and the cost of doing so, are expected to vary with a group's gender composition. We used spawning observations of a group-living cichlid, Neolamprologus pulcher , to test this expectation. We constructed groups that contained a dominant breeding pair and either two male subordinates, one male and one female subordinate or two female subordinates. Parasitic spawning by male subordinates was more common in groups with two male subordinates than in groups with one male and one female subordinate. Female subordinates were never observed laying eggs in dominant females' clutches, but three female subordinates laid independent clutches. During spawning, frequencies of dominant male aggression towards male and female subordinates were similar. Dominant males were less aggressive during non-reproductive periods. The declines were greater for female subordinates, such that, during non-reproductive periods, dominant males were more aggressive towards male subordinates. Aggression towards each subordinate was also affected by the second subordinate's gender; the direction of that effect differed for large and small subordinates. Male subordinates approached breeding shelters less often than female subordinates, and both male and female subordinates approached shelters more frequently when the second subordinate was male. Collectively, these patterns suggest: (1) that male subordinates impose higher costs on dominant males than female subordinates do and (2) that the presence of a second male subordinate imposes additional costs beyond those of the first male subordinate. We discuss the implications of these effects for dominant and subordinate group members.     

Small Subordinate Male Advantage in the Zebrafish

Dominance is an important determinant of reproductive success in many species, and size is usually an indicator of dominance status, with larger, dominant individuals physically and physiologically preventing smaller subordinates from mating. However, small size may be advantageous in some mating contexts because enhanced manoeuvrability enables males to get closer to females during mating. Here, we determined the paternity success and testes size of dominant and subordinate male zebrafish (Danio rerio), in pairs that controlled for social status. There was no statistical difference in both body size and testes size between dominant and subordinate males. Dominant males sired significantly more offspring than subordinates, but when subordinates were small, they had a greater share of the paternity than larger subordinates. Small male advantage may be one mechanism by which variation in body size is maintained in this species.     

Group composition affects male reproductive partitioning in a cooperatively breeding cichlid

Individuals within groups of cooperatively breeding species may partition reproduction, with the dominant pair often taking the largest share. The dominant's ability to reproductively control subordinates may depend on differences in competitive ability, due to, e.g. body size differences, but may also depend on the number of same‐sex competitors inside the group. We tested experimentally whether subordinates reproduce more when these subordinates are large or when a second subordinate of the same sex need to be controlled by the dominants, using the cooperatively breeding cichlid Neolamprologus pulcher. Dominant pairs were assisted by a large and a small unrelated subordinate; sexes of these fish were varied in a full‐factorial design (giving four treatments). Dominant males lost significantly more parentage to the large subordinate male when a small subordinate male was also present, compared to when a small subordinate female was present. However, subordinate paternity was generally low and did not significantly curb total dominant male reproductive output, which was more affected by the sizes and numbers of reproductive females present inside his group. Dominant female maternity, clutch sizes and total output did not depend on the treatments. Subordinate–subordinate reproduction was virtually absent (one out of 874 offspring). Female subordinates were more likely to provide care for their own broods. In contrast, male subordinates did not adjust their level of care to their parentage. Variability in female subordinate alloparental brood care was particularly high, with females showing more care than males in general. We also detected effects of growth rate and food ration on parentage independent of the treatments, most notably: (i) a trade‐off between dominant male growth rate and paternity; (ii) a decrease in dominant male paternity with increasing food ration; (iii) a positive effect of growth rate on paternity in small males. We conclude that dominant males should be sensitive to the number and sizes of subordinate males present in their group, particularly when these subordinates are not helpful or grow fast, and food is plentiful. Dominant females should be less sensitive, because female subordinates do not appear to impose reproductive costs and can be helpful through alloparental brood care.     

Mating Resets Male Cricket Aggression

An animal’s motivational state can significantly impact its behavior. We examined the effects of mating on the aggression of male Acheta domesticus crickets. Pairs of males were allowed to establish dominance and subordinance and were then physically separated. Subordinate males were then allowed to either copulate with a female or to have chemo-tactile contact with, but to not copulate with, a female. Less than 15 min after separation, all male pairs engaged in a second agonistic encounter. Subordinate males that copulated with females were significantly more aggressive toward their dominant partners than un-mated subordinate males. Many mated subordinates became dominant. Allowing a subordinate male to contact, but not copulate with, a female had a similar effect, suggesting that chemo-tactile cues from the female are sufficient to elicit this change in aggression.     

The biosynthesis of Dufour's gland constituents in queens of the honeybee (Apis mellifera)

Chemical analysis of queen Dufour's gland by GC/MS revealed the presence of long chain esters and hydrocarbons. To evaluate whether the biosynthesis of Dufour's gland components is modulated by physiological factors, we studied thede novo biosynthesis of esters and hydrocarbons in virgin and mated queen glandsin vivo andin vitro. Using [1-¹⁴C] sodium acetate as a precursor, it was shown thatin vivo, esters and hydrocarbons comprised the majorde novo products. The relative proportion of the hydrocarbon fraction was significantly higher in mated queens than in virgins, while in esters the situation was reversed. Comparision between reproductive and non reproductive virgin queens revealed that mating and not egg laying induced changes in glandular activity. Glands incubatedin vitro, on the other hand, synthesized mainly esters and alcohols but not hydrocarbons. These results suggest that either hydrocarbons are produced elsewhere and subsequently sequestered by Dufour's gland, or that the gland biosynthetic expressionin vivo is modulated. Differences between the gland activityin vivo andin vitro further support the hypothesis of a physiological mechanism in regulation of glandular performance.     

Source of the host marking pheromone in the egg parasitoid Trissolcus basalis (Hymenoptera: Scelionidae)

After oviposition, Trissolcus basalis females always mark the host's surface, depositing host marking substances for herself and to warn other ovipositing females. The perception of these host marking substances, probably through the antennae, can induce the female to leave and seek healthy hosts. Parasitoid females exposed to conspecific parasitized egg masses left the host egg masses significantly more often than when exposed to non-parasitized egg masses. More egg mass leaving behavior also was observed when the egg masses were treated with Dufour's gland secretion but not when treated with secretion from the common oviducts. The common oviduct has a secretory epithelium that produces electron-dense vesicles, probably containing proteinaceous substances. The secretory cells of the accessory gland, Dufour's gland, contain electron-lucid vesicles, whose secretion appears to be a lipid similarly to that found in pheromone secreting glands. Ultrastructural and behavioral evidence suggests that Dufour's gland is the host marking pheromone source.     

Relations of intraspecific variations in fecundity, clutch size, and oviposition frequency to the body size in three species of stoneflies, Sweltsa sp., Isoperla aizuana, and Stavsolus japonicus

Most stoneflies oviposit several times during their adult stage. In this study, the relations among oviposition frequency, the number of eggs per egg mass, and body size were examined in the chloroperlid stonefly Sweltsa sp. and two perlodid stoneflies, Isoperla aizuana and Stavsolus japonicus. It was found that larger individuals tended to oviposit more frequently than smaller ones, but the relation was significant only in Isoperla aizuana. In Sweltsa sp. and Isoperla aizuana, the number of eggs per egg mass was higher for the less-frequently ovipositing individuals than for those ovipositing more frequently, and the number of eggs per egg mass decreased with successive oviposition events. Stavsolus japonicus showed the same tendency but it was not statistically significant.     

Female dominance rank and behavior during artificial menstrual cycles in social groups of rhesus monkeys (Macaca mulatta)

We recently reported (Michael & Zumpe: American Journal of Primatology 15:157–170, 1988) evidence for the hypothesis that copulations by pairs of rhesus monkeys are linked more closely to the ovulatory phase of the female's menstrual cycle when a male has access to several females in different cycle phases rather than access to females in the same cycle phase. We have now used data from this earlier study to assess the role of female dominance. Artificial menstrual cycles were induced with hormone injections in two of four ovariectomized females in eight social groups (each consisting of one male and four females). The artificial cycles were either synchronized or offset by 7-day increments. There were differences in the behavioral interactions of the higher-ranking (dominant) and lower-ranking (subordinate) hormone-treated females in each group. The amount of male sexual activity received by dominant and subordinate females differed little, but dominant females initiated significantly more sexual activity (P<.0001) than did subordinate females. Dominant females were significantly more aggressive (P<.0001) toward other females and received more direct and redirected aggression from males. Males generally initiated and maintained more social contacts with dominant than with subordinate females, and dominant females were less active than subordinates in initiating and maintaining social interactions with males. The findings provide new evidence for both female mate competition and mate choice by males for higher-ranking females.     

Distinguishing kinds of prior dominance and subordination experiences in males of green swordtail fish (Xiphophorus helleri)

In experiments, there are usually two general ways of obtaining dominants and subordinates to test for the effect of recent experience upon ulterior behavior and dominance. One is to ‘impose’ such an experience on the contestants by a priori deciding which individual of the pair will become the dominant and which will become the subordinate through the use of rigged contests. The second technique is to let contestants ‘self-select’ the winner and loser by waiting for the spontaneous outcome of dyadic encounters between two usually well matched opponents. These two techniques of obtaining dominants and subordinates probably represent extreme cases on a single continuum of investment made by animals to settle dominance. To test this, we compared dominants and subordinates obtained from these two techniques in Xiphophorus fish males. It was found that pairs obtained through rigged contest (R) were much more aggressive in subsequent encounters than pairs in which the dominant and subordinate could self-select (S). They recuperated more rapidly from handling, initiated contact earlier, took more time to assess each other, and fought for a longer period of time. Prior-winners and prior-losers of the R condition more frequently relied on aggressive behavior during contest than that of the S condition. As a consequence, prior-winners and prior-losers of the R condition won equally the subsequent contest. On the contrary, prior-winners of the S condition defeated their prior-loser opponent in a majority of cases. These results can be tentatively explained by the following principle, winning or losing against a well matched opponent would leave more ‘experience’ than winning over a much weaker opponent, or losing to a much stronger one. This reinforces the hypothesis that prior-experiences are not qualitative states but come in various degrees.     

Ontogenetic patterns of volatiles identified in Dufour's gland extracts from queens and workers of the primitively eusocial halictine bee,Lasioglossum malachmum (Hymenoptera: Halictidae)

Summary Ontogenetic patterns of volatile compounds identified in Dufour's gland extracts from queens and workers of the primitively eusocial sweat beeLasioglossum malachurum (K.) were compared. Only young unmated queens showed high proportions of isopentenyl esters, while macrocyclic lactones were dominant in old breeding queens, spring queens, and workers. In young queens the relative and absolute amounts of volatiles changed one day after mating. A discriminant analysis revealed significant differences in odor patterns of unmated and mated young queens. The fat body was the largest in young females, while eggs could be recorded only in breeding queens. Possible functions of different odor components in the investigated female groups are discussed.     

Juvenile hormone and the ontogeny of cockroach aggression

Our previous study [Kou et al., 2008. Juvenile hormone levels are increased in winners of cockroach fights. Horm. Behav. 52, 252–260] showed that the basic principle of the challenge hypothesis (hormone levels can respond to social stimuli to modulate aggression in vertebrates] could be applied to juvenile hormone (JH) levels and aggression in the lobster cockroach Nauphoeta cinerea. In that study, 80- to 85-day-old socially naïve males were used, as fighting is much more easily initiated in these older animals than in younger males, and JH III levels in the dominant were found to be significantly increased after an encounter compared to before the encounter and were significantly higher than those in the subordinates. In N. cinerea, newly emerged males usually show no aggressiveness towards each other and aggression is only initiated after several days of close contact. To investigate the development of aggression from an early age, in the present study, newly emerged males were paired to investigate the relationship between JH levels and aggression. The results showed that injection of JH III significantly increased the probability of the young males being fight winners. In each age group in which aggression was initiated, the dominants had significantly higher JH levels than either the subordinates or the same aged non-fighters. JH injection of subordinates on the day of rank establishment had no effect on the probability of rank switch. These results indicate that, (i) in newly emerged male pairs, JH plays a decisive role in rank establishment and the fact that dominant status is significantly associated with a higher JH titer and subordinate status with a lower JH titer is consistent with the basic principle of the challenge hypothesis, and (ii) after rank establishment, the lack of effect of JH treatment on rank change is consistent with the idea of “social inertia” in vertebrates.     

Effect of the Presence of Subordinates on Dominant Female Behaviour and Fitness in Hierarchies of the Dwarf Angelfish Centropyge bicolor

In many hierarchical animal societies, dominant individuals control group membership owing to their power to evict subordinates. In such groups, the presence of subordinates, and therefore group stability, is continually dependent on subordinates being tolerated by dominants. The dominant decision to tolerate or evict is, in turn, dependent on the costs and benefits to dominants of subordinate presence. We investigated the effect of subordinate presence on dominants in the female dominance hierarchy of the dwarf angelfish Centropyge bicolor, using both observations of natural groups and experimental removals of subordinates. We found that the presence of subordinates had no effect on dominant access to resources, as measured by dominant foraging rates and home range areas, nor on dominant fitness, as measured by growth rates and spawning frequencies. Our results suggest that the presence of subordinates has a neutral effect on the current fitness of dominants, so that dominants have no great incentive to evict subordinates. We discuss the possibility that tolerance of subordinates might be further explained by considering future fitness, as dominant females in these haremic protogynous angelfish stand to inherit the male position, whereupon subordinate females change from potential competition to useful mates.     

Costly reproductive competition between females in a monogamous cooperatively breeding bird

In many cooperatively breeding societies, only a few socially dominant individuals in a group breed, reproductive skew is high, and reproductive conflict is common. Surprisingly, the effects of this conflict on dominant reproductive success in vertebrate societies have rarely been investigated, especially in high-skew societies. We examine how subordinate female competition for breeding opportunities affects the reproductive success of dominant females in a monogamous cooperatively breeding bird, the Southern pied babbler (Turdoides bicolor). In this species, successful subordinate reproduction is very rare, despite the fact that groups commonly contain sexually mature female subordinates that could mate with unrelated group males. However, we show that subordinate females compete with dominant females to breed, and do so far more often than expected, based on the infrequency of their success. Attempts by subordinates to obtain a share of breeding impose significant costs on dominant females: chicks fledge from fewer nests, more nests are abandoned before incubation begins, and more eggs are lost. Dominant females appear to attempt to reduce these costs by aggressively suppressing potentially competitive subordinate females. This empirical evidence provides rare insight into the nature of the conflicts between females and the resultant costs to reproductive success in cooperatively breeding societies.     

Arbuscular mycorrhizal fungi reduce the differences in competitiveness between dominant and subordinate plant species

In grassland communities, plants can be classified as dominants or subordinates according to their relative abundances, but the factors controlling such distributions remain unclear. Here, we test whether the presence of the arbuscular mycorrhizal (AM) fungus Glomus intraradices affects the competitiveness of two dominant (Taraxacum officinale and Agrostis capillaris) and two subordinate species (Prunella vulgaris and Achillea millefolium). Plants were grown in pots in the presence or absence of the fungus, in monoculture and in mixtures of both species groups with two and four species. In the absence of G. intraradices, dominants were clearly more competitive than subordinates. In inoculated pots, the fungus acted towards the parasitic end of the mutualism–parasitism continuum and had an overall negative effect on the growth of the plant species. However, the negative effects of the AM fungus were more pronounced on dominant species reducing the differences in competitiveness between dominant and subordinate species. The effects of G. intraradices varied with species composition highlighting the importance of plant community to mediate the effects of AM fungi. Dominant species were negatively affected from the AM fungus in mixtures, while subordinates grew identically with and without the fungus. Therefore, our findings predict that the plant dominance hierarchy may flatten out when dominant species are more reduced than subordinate species in an unfavourable AM fungal relationship (parasitism).     

The unusual social organization of the antPachycondyla tridentata (Formicidae,ponerinae)

Colonies of the ponerine antPachycondyla tridentata from Malaysia occur with and without queens. In a total of 7 colonies we found more than 80% of the workers to be mated, irrespective of the presence or absence of queens. This is a hitherto unknown social organisation in ants. Queens and workers competed equally for reproduction. In the colonies investigated several ants were laying eggs. Behavioral observations revealed persistent dominance interactions between colony members. A few ants, but not necessarily a queen, occupied top positions. Removal of the most dominant ants led to a new hierarchy in which subordinate ants with developed ovaries were attacked significantly more frequently than non-reproductive ants. On the average, callows were more aggressive than older subordinate ants, displacing most of the older laying workers in one colony. Nestmate recognition tests revealed that non-reproductive ants were much more aggressive towards foreign ants than were ants with developed ovaries.     

A Trouble Shared Is a Trouble Halved: Social Context and Status Affect Pain in Mouse Dyads

In mice behavioral response to pain is modulated by social status. Recently, social context also has been shown to affect pain sensitivity. In our study, we aimed to investigate the effects of interaction between status and social context in dyads of outbred CD-1 male mice in which the dominance/submission relationship was stable. Mice were assessed for pain response in a formalin (1% concentration) test either alone (individually tested-IT), or in pairs of dominant and subordinate mice. In the latter condition, they could be either both injected (BI) or only one injected (OI) with formalin. We observed a remarkable influence of social context on behavioral response to painful stimuli regardless of the social status of the mice. In the absence of differences between OI and IT conditions, BI mice exhibited half as much Paw-licking behavior than OI group. As expected, subordinates were hypoalgesic in response to the early phase of the formalin effects compared to dominants. Clear cut-differences in coping strategies of dominants and subordinates appeared. The former were more active, whereas the latter were more passive. Finally, analysis of behavior of the non-injected subjects (the observers) in the OI dyads revealed that dominant observers were more often involved in Self-grooming behavior upon observation of their subordinate partner in pain. This was not the case for subordinate mice observing the pain response of their dominant partner. In contrast, subordinate observers Stared at the dominant significantly more frequently compared to observer dominants in other dyads. The observation of a cagemate in pain significantly affected the observer''s behavior. Additionally, the quality of observer''s response was also modulated by the dominance/submission relationship.     

The Effect of Social Hierarchy on Captive Coyote (Canis latrans) Foraging Behavior

Foraging efficiency of individuals in pack forming species may be influenced by social dynamics within a pack. The effects of social hierarchy in particular may influence individual foraging behavior in canids, such as coyotes (Canis latrans). To examine the impact of social hierarchy on foraging behavior, we tested 16 captive coyotes in eight naturally established dominant–subordinate pairs, using the guesser–knower paradigm. We measured the efficiency of subordinate coyotes to relocate a food resource when alone and then allowed pairs to forage together, such that subordinates had prior knowledge of food location but dominants did not. To determine whether (1) subordinates used a direct or discursive strategy to obtain food in the presence of a dominant and (2) dominants used an exploitative or independent strategy to obtain food in the presence of a subordinate with previous knowledge, we measured their search efficiency (e.g., correct choice of area, feeder, and latency to correct feeder). Results showed subordinates learned to relocate food and increase efficiency when alone. In a social context, however, subordinate efficiency decreased. That is, subordinates approached the correct area, but searched more feeders before finding the correct one. Dominants initially used an independent search strategy but then quickly displaced the subordinate and monopolized the resource, reducing subordinate efficiency further. Despite continual displacement and reduction in efficiency, subordinates did not alter their foraging strategy over time. Our results suggest prior information can improve individual foraging advantage, but that social status strongly impacts individual foraging efficiency in social species such as coyotes.     

Social stress decreases marking behavior independently of testosterone in Mongolian gerbils

This study examined the endogenous androgen regulation of the marking behavior in Mongolian gerbils (Meriones unguiculatus). In the first experiment, developmental changes of fecal testosterone levels, ventral gland growth, and the marking frequency of male gerbils were investigated. From 9 weeks of age, marking frequency increased with increases in fecal testosterone levels and ventral gland size. The ventral gland size and marking frequency were significantly correlated to the fecal testosterone level. In the second experiment, we hypothesized that reduction in the marking frequency of subordinate males after social confrontations was controlled by a decrease in the circulating testosterone level, and we followed changes in marking frequency, endocrine status, and ventral gland size after social confrontations in which two adult male gerbils established their social ranks by fighting. As expected, marking frequency and ventral gland size were significantly related to social rank, that is, marking frequency was higher among dominant gerbils and lower among subordinates. In addition, fecal corticosterone levels among subordinates were higher than those of dominant animals. However, neither the fecal and plasma testosterone levels, nor testis size, differed between dominant and subordinate gerbils. These results revealed that endogenous androgen played a role in regulating marking behavior and ventral gland size during the developmental stage and that the reductions in marking frequency and ventral gland size occurring in subordinate males after social confrontations were not directly regulated by androgen changes.     

Differential influence of native and introduced arbuscular mycorrhizal fungi on growth of dominant and subordinate plants

The impact of arbuscular mycorrhizal fungi (AMF) on plant ecosystems has been intensively reported. In this research, we explored the difference between native and introduced AMF in promoting the growth of dominant and subordinate plant species. In glasshouse experiments, dominants and subordinates from subtropical grasslands were colonized by native AMF or introduced AMF, Glomus versiforme. The biomass revealed that mycorrhizal dependencies (MD) on the native AMF of the dominants were much higher than those of the subordinates, while MD on the introduced AMF changed following the replacement of native AMF with introduced AMF. A close relationship between biomass promotion and increase in phosphorus uptake was observed, indicating the important role of AMF-enhanced nutrient acquisition by roots. Our results show that plant community structures are partly determined by MD on native AMF, and could be modified by introducing exogenous AMF species.     

Host age and host selection byTrichogramma nubilale

Selection byTrichogramma nubilale (Ertle & Davis) for different aged egg masses ofOstrinia nubilalis (Hübner) was examined by separating components of parasitism. FemaleT. nubilale were exposed to egg masses of 2 different ages (freshly laid egg masses versus 1, 2, 3 or 4 day old egg masses), and the age of the initial egg mass inspected, number and percent of eggs and egg masses parasitized, and the emergence rate of pharate parasitoids was recorded. When there was a large difference in age between young and old egg masses, ♀♀ inspected initially more young egg masses (>2 days difference), parasitized a greater percent of young egg masses (>2 days difference), and parasitized more eggs/parasitized egg mass in young egg masses (>3 days difference) than old egg masses. Females did not discriminate between host age when hosts were similar in age. Successful emergence of parasitoids was greater from younger eggs than older eggs, although emergence was better from one-day-old eggs than from fresh eggs. These results imply that when the hosts were sufficiently different in age, ♀♀ were attracted to younger egg masses more than older egg masses, and they tended to remain ovipositing for longer periods of time on younger egg masses than older egg masses. Moreover, ♀♀ appeared to prefer to oviposit in hosts in which their young are more likely to complete development.