Mating system of the Amazonian cichlid angel fish, Pterophyllum scalare.

The species, Pterophyllum scalare distinguishes itself by its breeding behavior, involving competition for territory, sexual partners, courtship and parental care. The purpose of this study was to identify the mating system adopted by this species of fish. Twenty males and twenty females were observed under semi-natural and experimental conditions to test the hypothesis of serial monogamy. Under semi-natural conditions, after the third breeding cycle, the couples changed mates. Under experimental conditions, the couples changed partners after the first breeding cycle. Under experimental conditions, mate recognition was investigated through the preference of the females, indicated by the time they spent with the males. The females were available or not for courtship from new males, depending on their aggressiveness or submission. The larger and more aggressive males obtained new mating opportunities while the submissive males were rejected by the females. The mated fish were aggressive towards intruders in the presence of the mate, protecting their pair bond. In the interval between breeding cycles, the couples did not display aggression towards intruders, confirming the hypothesis of serial monogamy. Best mate selection by the females and the opportunity of new matings for both sexes influenced the reproductive success of this species.     

Social monogamy in the cleaning goby Elacatinus evelynae: ecological constraints or net benefit?

We tested predictions from four hypotheses to explain the occurrence of long-term socially monogamous pairs in the Caribbean cleaning goby Elacatinus (=Gobiosoma) evelynae, namely (1) resource limitation, (2) low population and/or low mate density, (3) territorial defence and (4) net benefit of single-mate sequestration. We found no evidence that resources, in terms of available cleaning stations or clients to clean, were limited (1) or that after experimental goby removals, single individuals could not maintain cleaning stations alone (2). Population density was low but this did not prevent artificially widowed fish from remating quickly with individuals as large as their initial partners (3). Social monogamy in E. evelynae appears to result from the benefits associated with sequestering a large, high-quality mate (4). Both males and females showed intrasexual aggression towards experimental intruders consistent with mate guarding. Opportunities for polygynous matings by males, assessed by comparing the sizes, distances between and mating synchrony of neighbouring pairs, appeared both low and of limited value. Males therefore benefit most from guarding a larger, more fecund female. Females spent longer cleaning when paired with a large male, indicating that the benefits of guarding a high-quality mate may extend outside of the reproductive period for socially monogamous species. These results add to an increasing number of studies on coral reef fish showing mate-guarding behaviour and benefits to males and females from sequestering a single mate. Copyright 2003 Published by Elsevier Ltd on behalf of The Association for the Study of Animal Behaviour.      

Mate guarding in an Amazonian cichlid, Pterophyllum scalare

Aggression by Pterophyllum scalare to an opposite sexed intruder was markedly reduced when the mate was absent. Territorial defence was not vigorous just after the eggs had been released and fertilized. Fish of both sexes attacked intruders of the same sex more intensely than they attacked those of the opposite sex, but males were more aggressive than females in this context. These results suggest that their aggression toward intruders serves to maintain the pair bond.     

The natural history of a monogamous coral-reef fish, Valenciennea strigata (Gobiidae): 2. behavior, mate fidelity and reproductive success

This study examined the behavior and reproduction of a monogamous coral-reef fish, Valenciennea strigata, to determine mate fidelity and the proximate causes of monogamy. Most fish were found in monogamous pairs that remained together over several rounds of reproduction. Pairs stayed within close proximity to each other and their burrows. Females fed at a higher rate than their mates, while males spent more time maintaining burrows. Females spawned every 13 days; males guarded eggs in the burrow for 2–3 days. Although females limited the RS of males, males did not mate polygynously under natural conditions. Reproductive success (RS) was affected primarily by survival, and secondarily by size. Both sexes enforced monogamy by guarding their mates. Three factors facilitated mate guarding: (1) all males were able to hold a nest site, (2) both sexes showed strong site fidelity, and (3) residents had an advantage in contests over mates. Thus, mates were economically defensible. Additionally, females formed a crescent of dark pigments on their abdomen that resembled a gravid condition; these marks may enhance continuation of the pair bond. Both sexes preferred large mates, and pairs were positively assorted by size. Males benefited from guarding large females because fecundity increased with size. Females may benefit from the burrowing of males, and larger males should be better burrowers.     

Evolution of monogamy in seaside sparrows, Ammodramus maritimus: tests of hypotheses

Seaside sparrows (Ammodramus maritimus) are monogamous throughout their range. We used male-removal experiments, measurements of territory quality and nest placement in relation to territory boundaries, and observations on foraging behaviour and on intraspecific aggression to assess the applicability of pertinent hypotheses that could explain the occurrence of monogamy in this species. Since experimentally widowed females can rear about two-thirds as many young to independence as pairs, made help is advantageous but not necessary for female reproductive success. Female-female aggression is probably not important in maintaining monogamy, but we need to learn more about it. We induced experimental bigamy in seaside sparrows in New York, thus showing that males will accept second mates. Territory quality (suitable cover, nest-sites and food) is very heterogeneous in the sparrow populations. However, ‘polygyny thresholds’ evidently are not exceeded either because resources on salt marshes are not limiting (cover, nest-sites) or because females can nullify the effects of resource (food) disparity between territories by feeding at distant sites outside their mates' territories.     

Social Monogamy in the Big-Clawed Snapping Shrimp, Alpheus heterochelis

Social monogamy has evolved independently in many taxa, and often involves biparental care of the young. Where it does not, mate guarding and shared territoriality have been invoked as causal factors. We evaluated mate guarding and shared resource defence (a common shelter) as factors that could have led to social monogamy in the snapping shrimp, Alpheus heterochelis. This species is found in male–female pairs that defend a common shelter together. Female receptivity lasts only for a few hours immediately after her periodic moult. Their monogamous pair bond may represent mate guarding or joint defence of a territory. Monogamy in A. heterochelis seems most importantly driven by the cryptic nature of the female's moult cycle. We found that males did not discriminate among females at different intermoult stages for pairing, nor did they modulate their defence of mate and shelter (vs. the risk in finding a new shelter and mate) according to female moult stage. This, together with the short period of female receptivity before her single copulation per cycle, make extended mate guarding the most efficient method for a male to secure a mating opportunity. Comparing eviction rates of paired and unpaired shelter residents by conspecific intruders provided no evidence of enhanced resource defence that would confer a selective advantage to a pair. Male presence during the moult is beneficial for the female, as searching for a male during her soft-bodied receptive phase would put her at mortal risk. Our results show empirically for the first time that guarding may be beneficial, even if males are not able to assess the female's reproductive stage. This extends the theoretical framework for understanding the evolution of social monogamy in taxa without biparental care of young.     

Extra‐pair mating in a socially monogamous and paternal mouth‐brooding cardinalfish

Many vertebrates form monogamous pairs to mate and care for their offspring. However, genetic tools have increasingly shown that offspring often arise from matings outside of the monogamous pair bond. Social monogamy is relatively common in coral reef fishes, but there have been few studies that have confirmed monogamy or extra‐pair reproduction, either for males or for females. Here, long‐term observations and genetic tools were applied to examine the parentage of embryos in a paternally mouth‐brooding cardinalfish, Sphaeramia nematoptera. Paternal care in fishes, such as mouth‐brooding, is thought to be associated with a high degree of confidence in paternity. Two years of observations confirmed that S. nematoptera form long‐term pair bonds within larger groups. However, genetic parentage revealed extra‐pair mating by both sexes. Of 105 broods analysed from 64 males, 30.1% were mothered by a female that was not the partner and 11.5% of broods included eggs from two females. Despite the high paternal investment associated with mouth‐brooding, 7.6% of broods were fertilized by two males. Extra‐pair matings appeared to be opportunistic encounters with individuals from outside the immediate group. We argue that while pair formation contributes to group cohesion, both males and females can maximize lifetime reproductive success by taking advantage of extra‐pair mating opportunities.     

Pair territoriality in the longnose filefish,oxymonacanthus longirostris

The longnose filefish,Oxymonacanthus longirostris, usually lives in heterosexual pairs, the male and female swimming together and sharing the same territory. Pair territoriality in the species was examined in detail in relation to sexual differences in territorial defense activities. Rigorous pair territoriality was maintained only during the breeding season, although pairs used their home ranges exclusively to a certain extent, during the non-breeding season. The frequency of aggression against other conspecific pairs in the breeding season was higher than in the non-breeding season. Agonistic interactions appear to be over both mates and food resources, the strict pair territoriality in the breeding season possibly being due to mutual mate guarding. In intraspecific aggressive interactions, males usually led their partner females when attacking intruders. The feeding frequency of males was much lower than that of females in the breeding season. Mate removal experiments indicated that females could not defend their original territories solitarily and their feeding frequency decreased. Conversely, males could defend territories solitarily without a decrease in feeding frequency. These results suggest that males contribute most to the defense of the pair territory, with females benefiting from territorial pair-swimming with their partner males.     

Territorial cooperation and social monogamy: factors affecting intersexual behaviours in pair-living snapping shrimp

Among the factors that may contribute to the evolution of social monogamy are selection for extended mate guarding of females and selection for territorial ‘cooperation’. Many socially monogamous taxa are also territorial, with ‘partners’ sharing a single territory, suggesting that one or both partners may benefit by sharing territorial maintenance. Snapping shrimp (genus Alpheus) are socially monogamous and territorial, living in excavated burrows or with host organisms, with females performing all parental care. The territorial cooperation hypothesis predicts that male and female partners share (1) territorial defence, resulting in a reduction in the risk of eviction from the burrow, (2) burrow construction duties, such that individuals in pairs spend less time in burrow construction relative to solitary individuals, and/or (3) foraging duties, by returning food to the burrow, where it is consumed by both partners. UsingA. angulatus as a model species, a territorial defence experiment revealed that females in pairs were significantly less likely than solitary females to be evicted by female intruders, but males in pairs were not significantly less likely than solitary males to be evicted by male intruders. A subsequent experiment revealed that paired males were significantly less likely to be evicted by an intruding male if paired with sexually receptive females than if paired with nonreceptive females. Another experiment revealed that (1) paired females spent significantly more time in burrow construction than paired males, and (2) both males and females consistently returned food items to the burrow, perhaps incidentally provisioning their mates. These data suggest that social monogamy may have been selected for in part because of the advantages of territorial cooperation, as both males and females are likely to benefit by dividing the labour of territorial defence and maintenance. These tests of the territorial cooperation hypothesis are synthesized with data from tests of the extended mate-guarding hypothesis to place snapping shrimp pairing behaviour into a larger construct incorporating both the influence of ecological pressures (territoriality) and mating interactions between the sexes. Copyright 2002 The Association for the Study of Animal Behaviour. Published by Elsevier Science Ltd. All rights reserved.     

Male and female cooperatively breeding fish provide support for the "Challenge Hypothesis"

The idea that territorial aggression is regulated by androgensand that aggression itself can modulate androgen levels is wellestablished in males. In many species, females also displayaggressive behavior, yet little work has been conducted on theeffects of female aggression on hormone levels. In this study,we compared the effects of a simulated territory intrusion (amethod for testing the Challenge Hypothesis) on males and femalesof the fish, Neolamprologus pulcher. This cichlid fish fromLake Tanganyika is a particularly useful species to examinesex differences in the behavioral mediation of hormones as breedingpairs remain in a territory year round and both sexes defendthis territory against conspecific and heterospecific intruders.In our study, both sexes indeed aggressively defended theirterritory against a simulated territory intruder. In responseto intruders, both males and females displayed elevated levelsof circulating 11-ketotestosterone, but only females exhibitedincreases in testosterone. Neither aggressing male nor femalefish showed changes in estradiol levels compared to control(nonaggressing) fish. Residents were more aggressive than theintruders and won most of the interactions. However, residents(or winners) did not show higher hormone levels than intruders(or losers). We suggest that aggression commonly modulates androgenlevels in both male and female teleost fish.     

Monogamy in marine fishes

The formation of long-term pair bonds in marine fish has elicited much empirical study. However, the evolutionary mechanisms involved remain contested and previous theoretical frameworks developed to explain monogamy in birds and mammals are not applicable to many cases of monogamy in marine fish. In this review, we summarise all reported occurrences of social monogamy in marine fish, which has so far been observed in 18 fish families. We test quantitatively the role of ecological and behavioural traits previously suggested to be important for the evolution of monogamy and show that monogamous species occur primarily in the tropics and are associated with coral reef environments in which territory defence and site attachment is facilitated. However, there is little evidence that obligately monogamous species are smaller in body size than species that can adopt a polygynous mating system. We review the evidence pertaining to six hypotheses suggested for the evolution of monogamous pair bonds: (1) biparental care, (2) habitat limitation, (3) low population density/low mate availability/low mobility, (4) increased reproductive efficiency, (5) territory defence, and (6) net benefit of single mate sequestration. We outline predictions and associated empirical tests that can distinguish between these hypotheses, and assess how generally each hypothesis explains monogamy within and between breeding periods for species with different types of territories (i.e. feeding only or feeding and breeding). Hypotheses (1) and (2) have limited applicability to marine fishes, while hypotheses (3)-(5) have little empirical support beyond the species for which they were designed. However, the role of paternal care in promoting monogamous pair bonds is not explicit in these hypotheses, yet paternal care has been reported in more than 70 monogamous marine fish. We show that paternal care may act to increase the likelihood of monogamy in combination with each of the proposed hypotheses through decreased benefits to males from searching for additional mates or increased advantages to females from sequestering a single high-quality mate. Among species defending breeding and feeding territories, the benefits, both within and between reproductive periods, of sequestering a single high-quality mate (hypothesis 6) appear to be the best explanation for socially monogamous pairs. For species without parental care (i.e. holding only feeding territories), territory defence (hypothesis 5) in combination with the benefits of guarding a large mate (hypothesis 6) could potentially explain most instances of monogamy. Empirical studies of marine fishes over the past two decades are therefore slowly changing the view of monogamy from a mating system imposed upon species by environmental constraints to one with direct benefits to both sexes.     

Mate Change Reduces the Reproductive Rate of Males in a Monogamous Pipefish Corythoichthys haematopterus: The Benefit of Long-Term Pair Bonding

Monogamy has evolved independently in many taxa, and often involves biparental care of the young and/or low defendability of multiple mates. In many teleost fishes, however, strict monogamy is practised without such limitations. In this study, we examined why males of the pipefish Corythoichthys haematopterus (family: Syngnathidae) reproduce monogamously without changing to another mate. For this we examined the time cost associated with mate change by experimentally removing females from mating pairs and compelling the males to change mates. Mate‐changing males needed longer interspawning intervals, an average of 8.5 d, than their monogamous counterparts, which was primarily because of the time needed for the new female to prepare mature eggs. As a result, we assume that mate change entails considerable reproductive costs associated with a decrease in reproductive rate. Monogamy and long‐term pair bonding in C. haematopterus are likely maintained because of high reproductive rates by repeatedly reproducing with the same mate over a lifetime.     

Riverside wren pairs jointly defend their territories against simulated intruders

Duets are a jointly produced signal where two or more individuals coordinate their vocalizations by overlapping or alternating their songs. Duets are used in a wide array of contexts within partnerships, ranging from territory defence to pair bond maintenance. It has been proposed that pairs that coordinate their songs might also better coordinate other activities, including nest building, parental care and defending shared resources. Here, we tested in the riverside wren (Cantorchilus semibadius), a neotropical duetting species that produces highly coordinated duet songs, whether males and females show similar responses to playback. During territorial disputes in songbird species, individuals tend to direct their attention towards same‐sex territorial intruders, but this bias might be less pronounced in duetting species. We performed a dual‐speaker playback experiment to examine how mated individuals respond to speakers broadcasting female‐versus‐male duet contributions. We found that riverside wrens have high levels of converging behaviour by duetting and remaining in close proximity to one another when responding to simulated paired intruders. Males and females spent more than 80% of their time less than 1 m apart while defending their territory. Both individuals in a pair aggressively engaged with both male and female simulated trespassers by approaching equally close and spending equal time near the two speakers. These results suggest that both sexes perceive a paired territorial intrusion as a similar threat and that both partners are highly invested in defending the shared resources. This study is one of the few to demonstrate equal attention and aggression from mated pairs towards simulated same‐sex and opposite‐sex intruders. We suggest that pairs responding together, in close proximity to one another, might be favourable in duetting species when defending the territory because maintaining a close distance between partners facilitates the extreme coordination of their joint territorial signals.     

Male territoriality and ‘sex confusion’ in recently adapted lizards at White Sands

The evolution of intersexual interactions, like mate choice, during ecological speciation has received widespread attention. However, changes in intrasexual interactions, like male territoriality, during ecological divergence are largely unexamined. We conducted field experiments with adaptively diverged populations of the eastern fence lizard (Sceloporus undulatus) to determine whether territorial males behaved differently towards ecologically similar vs. dissimilar intruders. We performed trials with light‐coloured males from White Sands, New Mexico and dark‐coloured males from the surrounding desert. We found that intruders from White Sands elicited more aggression than intruders from dark‐soil habitat. We also documented a case of ‘sex confusion’ where white‐sand males courted dark‐soil intruders. We found population differences in signalling patch size that can explain both aggression bias and sex misidentification. We argue that direct selection (for population recognition or optimal signal transmission) and indirect selection (by‐products of ecological adaptation) should influence both intersexual and intrasexual interactions during ecological speciation.     

Sex change in either direction by growth-rate advantage in the monogamous coral goby, Paragobiodon echinocephalus

The size-advantage model predicts the evolution of sex changeif the relative reproductive success of the sexes changes withsize or age. In the goby (Paragobiodon echinocephalus) the largesttwo fish, a male and a female matched by size, breed monogamouslyin each host coral. Because the female fecundity and male abilityof egg care increase with body size in a similar way, no size-fecundityadvantage exists. However, we found both protogyny and infrequentprotandry in a natural population of this species in Okinawa.New pairs were often formed after movement between host coralsand also sex change or sex differentiation of one or both members.In most new pairs males were larger than females, and femalesgrew much faster than their mates until breeding (growth-rateadvantage). The smaller member of a new pair should be the femalethat grows faster, because the smaller limits the reproductivesuccess of the pair. To form such a pair, the goby changed sexaccording to the sex and relative size of a new mate, as a status-dependentconditional strategy. The growth-rate advantage predicts predominanceof protogyny, but movement between host corals provides opportunitiesalso for protandry.     

Coloration,Paternity, and Assortative Mating in Western Bluebirds

Coloration in birds can act as an important sexual signal in males, yet in many species, both sexes display bright colors. Social selection may account for this pattern, with more brightly colored individuals pairing together on the best territories. Mutual mate choice may also explain this, as males investing a great deal of parental care in the offspring should be choosy about their social mates. It is less clear whether this pattern of mate choice can apply to extra‐pair partners as well. We examined western bluebirds (Sialia mexicana) to determine whether more colorful individuals tended to pair with one another, both in social pairs and between females and their extra‐pair partners. Both male and female western bluebirds display both UV‐blue structural plumage and a melanin‐based chestnut breast patch, although females are duller than males. Social pairs mated assortatively with regard to UV‐blue brightness, but not chestnut coloration. There was no evidence that extra‐pair partners mated assortatively, but males with brighter UV‐blue coloration had fewer extra‐pair offspring in their nests. Older males were more successful at siring extra‐pair offspring, despite displaying no differences in coloration compared to younger males. Coloration did not play a role in determining extra‐pair male success. These results suggest that coloration plays a role in the formation of social pairs, but not mate choice for extra‐pair partners.     

A high aggression strategy for smaller males

Male-male conflict is common among animals, but questions remain as to when, how and by whom aggression should be initiated. Factors that affect agonistic strategies include residency, the value of the contested resource and the fighting ability of the two contestants. We quantified initiation of aggression in a fish, the desert goby, Chlamydogobius eremius, by exposing nest-holding males to a male intruder. The perceived value of the resource (the nest) was manipulated by exposing half of the residents to sexually receptive females for two days before the trial. Resident male aggression, however, was unaffected by perceived mating opportunities. It was also unaffected by the absolute and relative size of the intruder. Instead resident aggression was negatively related to resident male size. In particular, smaller residents attacked sooner and with greater intensity compared to larger residents. These results suggest that resident desert goby males used set, rather than conditional, strategies for initiating aggression. If intruders are more likely to flee than retaliate, small males may benefit from attacking intruders before these have had an opportunity to assess the resident and/or the resource.     

Monogamy and sex role reversal in the pipefish Corythoichthys haematopterus

We observed the mating pattern and social behaviour of the pipefish Corythoichthys haematopterus in temperate waters of Japan during three successive breeding seasons. Males cared for a clutch in their brood pouch for 9-19 days until hatching and had several broods in the season with nonbrooding intervals of only 1 or 2 days. The population sex ratio was female biased and some females were always excluded from reproduction. Although males were sometimes courted by unmated females together with their regular partners, they always mated with the latter. The pair bond was maintained until the next season if both members survived. When males lost their partners, they remated with neighbouring unmated females within a few days. In contrast, widowed females remained unmated for a long time. Females had larger home ranges and were more active in courtship displays than males. This pipefish provides the first example of sex role reversal among monogamous syngnathid fish. We suggest that mate guarding by females is a primary proximate factor for maintenance of monogamy in this fish. Copyright 2001 The Association for the Study of Animal Behaviour.     

Social Reversal of Sex‐Biased Aggression and Dominance in a Biparental Cichlid Fish (Julidochromis marlieri)

In biparental species, aggression, dominance, and parental care are typically sexually dimorphic. While behavioral dimorphism is often strongly linked to gonadal sex, the environment—either social or ecological—may also influence sex‐biased behavior. In the biparental cichlid fish Julidochromis marlieri, the typical social environment for breeding pairs consists of large females paired with smaller males. While both sexes are capable of providing territory defense and parental care, the larger female provides the majority of defense for the pair, while the smaller male remains in the nest guarding their offspring. We examine the contributions of sex and relative mate size to these sex‐biased behaviors in monogamous J. marlieri pairs. Both female‐larger and male‐larger pairs were formed in the laboratory and were observed for territorial aggression (against conspecifics and heterospecifics), dominance, and parental care. In female‐larger pairs, territorial aggression and intra‐pair dominance were female‐biased, while in male‐larger pairs this bias was reversed. For both pairing types, the presence of an intruder amplified sex differences in territorial aggression, with the larger fish always attacking with greater frequency than its mate. Though less robust, there was evidence for plasticity of sex‐bias for some egg care related behaviors in the inverse direction. Our study suggests that relative mate size strongly influences the sex bias of aggression and dominance in J. marlieri and that this aspect of the social environment can override the influence of gonadal sex on an individual's behavior. The remarkable plasticity of this species makes Julidochromis an exciting model that could be used to address the relationship between proximate and ultimate mechanisms of behavioral plasticity.     

Spatiotemporal and gender‐specific parasitism in two species of gobiid fish

Parasitism is considered a major selective force in natural host populations. Infections can decrease host condition and vigour, and potentially influence, for example, host population dynamics and behavior such as mate choice. We studied parasite infections of two common marine fish species, the sand goby (Pomatoschistus minutus) and the common goby (Pomatoschistus microps), in the brackish water Northern Baltic Sea. We were particularly interested in the occurrence of parasite taxa located in central sensory organs, such as eyes, potentially affecting fish behavior and mate choice. We found that both fish species harbored parasite communities dominated by taxa transmitted to fish through aquatic invertebrates. Infections also showed significant spatiotemporal variation. Trematodes in the eyes were very few in some locations, but infection levels were higher among females than males, suggesting differences in exposure or resistance between the sexes. To test between these hypotheses, we experimentally exposed male and female sand gobies to infection with the eye fluke Diplostomum pseudospathaceum. These trials showed that the fish became readily infected and females had higher parasite numbers, supporting higher susceptibility of females. Eye fluke infections also caused high cataract intensities among the fish in the wild. Our results demonstrate the potential of these parasites to influence host condition and visual abilities, which may have significant implications for survival and mate choice in goby populations.