Monogamy in a feeding generalist, <Emphasis Type="Italic">Chaetodon trichrous</Emphasis>, the endemic Tahitian Butterflyfish

Butterflyfishes have been well studied for their feeding ecology and mating systems. In particular, studies of corallivorous butterflyfishes have supported models of monogamy based on their predictable, low quality food; a patch of coral that is economically defensible by a pair. Moreover, pairs often exhibit trade-offs in territorial defense (greater by males) and feeding (greater by females) that improve their reproductive success. However, this model has not been well tested for more generalist feeders. In addition, recent hypotheses for monogamy in fish have emphasized parental care, but butterflyfishes do not provide parental care. This study tests five hypotheses for monogamy in the endemic Tahitian butterflyfish, Chaetodon trichrous: 1) uniform distribution of limiting resources, 2) joint defense of a territory, 3) low mate availability, 4) predator detection, and 5) benefits of cooperative behavior. Chaetodon trichrous was the most abundant butterflyfish in bays. Pairs jointly patrolled feeding territories. They preferentially fed over hard substrate other than live coral, however, this substrate was available outside of territories. They also ate plankton. Pairs were sorted positively for size, and all pairs were heterosexual. Males were larger than their partners, but females fed at higher rates. These results suggest that C. trichrous is monogamous, but reject the hypotheses that pairs form for joint defense of a territory (pairs swam together), that pairs remain together because of low mate availability (frequent interactions with neighbors), or that pairs form for predator detection (no homosexual pairs). Monogamy in C. trichrous is associated with the uniform distribution of hard substrate, although this resource is not limiting. Further, the higher feeding rate of females may represent a benefit provided by their monogamous mates.     

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.     

Butterflyfish social behaviour,with special reference to the incidence of territoriality: a review

Synopsis Butterflyfishes (Chaetodontidae) are among the best studied of coral reef fishes. Feeding ecology and some aspects of behaviour have been firmly established. However, spacing behaviour remains controversial. Two major studies made in the 1970s concluded that the majority of species were not territorial. We suggest that these and other studies which have concluded that territories are not held have generally suffered from short observation periods, and have not mapped the ranges occupied by individuals. Further, low frequencies of agonistic behaviour have been interpreted as evidence of non-territoriality. By contrast, studies which have proven territoriality have had long observation periods and have mapped ranges. These have shown that territories are usually maintained with very little overt aggression. Spacing behaviour and feeding behaviour are clearly linked, with territoriality common among benthic-feeding species, especially obligate corallivores. Species with broad dietary flexibility tend to have flexible social systems, while plankton feeders are usually gregarious. The widespread occurrence of monogamy in butterflyfishes appears linked to territoriality, the majority of territorial species identified to date occurring predominantly as pairs. Data currently available suggest that this is because pair defence of the territory is more efficient than by individuals. However, several alternative hypotheses for the evolution of monogamy based on spawning constraints and predation risk cannot yet be ruled out.     

Behavioral rules and tail-up display in extra- and intra-pair interactions of the butterflyfish,Chaetodon lunulatus

The butterflyfish,Chaetodon lunulatus, forms monogamous pair bonds. Each pair defends a feeding territory against conspecifics. The tail-up or lateral display of the butterflyfish is performed not only towards non-partners in territorial disputes (extra-pair interaction), but also towards partners (intra-pair interaction). In order to explain this phenomenon, I investigated the two interaction types, and found that a simple model explains both interactions very well. The model consists of four behavioral rules and two provisos for applying the rules. Rule 1: Perform the tail-up display when approached by another individual. Rule 2: Perform the tail-up display when another individual performs the tail-up display. Rule 3: Attack another individual that neither approaches nor performs the tail-up display. Rule 4: Swim with your partner. Proviso 1: Apply Rules 1 and 2 when you do not intend to run away. Proviso 2: Apply Rules 1, 2, and 3 when you do not recognize another individual as your partner. When Rules 1–4 and Provisos 1–2 are applied, the display can prevent improper attacks between partners caused by imperfect partner recognition.     

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.     

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.     

Social groupings in 18 species of butterflyfish and pair bond weakening during the nonreproductive season

I surveyed social groupings in 18 butterflyfish species of genus Chaetodon, focusing on how many individuals usually swim together in the reproductive season. Social groupings in 4 of the 18 species were first reported. Six of the 18 species were also observed in the nonreproductive seasons. Three species, of which 2 species were found to be monogamous, spent less time swimming with their partner during the nonreproductive season than the reproductive season. This observation is consistent with the hypothesis that the function of pair swimming is to increase the egg production of the female.     

鸟类婚配制度的生态学分类

在Ｅmlen和Ｏring鸟类婚配制度生态学分类系统的基础上,根据近年来鸟类行为生态学研究的成果,对鸟类的婚配制度进行了补充分类,并强调了应以进化稳定策略的观念来认识乌类的婚配制度。补充的鸟类婚配制度生态型包括：合作型一雄一雌制（cooperative monogamy)、临界型一雄一雌制（critical monogamy)、保卫雌性型一雄一雌制（female defense mognogamy)、从领域型一雄多雌制（poly-terri-tory polygyny)和社群繁殖制。合作型一雄一雌制的鸟 类雌雄个体爱力合作才保证繁殖的成功;临界型一悲欢离合一雌制鸟类雌雄个体都有多配倾向,但迫于生态压力必须共同抚育后代才能繁殖成功;保卫雌性型一雄一雌制的鸟 类通过保卫一个雌鸟不被其它雄鸟占有而保证繁殖成功,多领域型一雄多雌制的雄鸟通过占有多个领域而多个雌鸟交配;社群繁殖制的鸟 类由三个以上个体参与工部分参与繁殖,所有个体共同抚育一批后代,现有的鸟类婚配制度可以归为一雄一雌制（monogamy)、一雄多雌繁殖,所有个体共同抚育一批后代。现有的鸟类婚配制度可以归为一雄一雌制(polygyny)、一雌多雄制（polyandry)快速多窝型多配制（rapid-multiple-clutch polygamy)和社群繁殖制（social breeing systen）五大类型。     

Duetting behavior in a Neotropical ovenbird: sexual and seasonal variation and adaptive signaling functions

Duetting is a collective behavior and might have multiple functions, including joint territory defense and mate guarding. An important step toward understanding the adaptive function of bird song is to determine if and how singing behavior varies seasonally. However, seasonal patterns for duetting species are different from the pattern described for species in which only the male sings, because song function may vary according to sex, singing role (initiator vs responder) and level of duet organization (individual vs pair). We investigated whether patterns of seasonal variation in duetting depends on these factors, which would suggest different interpretations of song function. We studied social pairs of a Neotropical bird species (rufous hornero Furnarius rufus) for seven consecutive months, recording vocal and territorial behaviors. Overall, partners coordinated 61% of their songs into duets and many song traits (song initiation rate, song output and duet rate) peaked in territorial contexts. Males engaged in territorial interactions with strangers more often, initiated more songs, and answered proportionately more of their partners’ songs than females. Male song initiation rate peaked during the pre‐ and post‐breeding stages, whereas females initiated more songs during the non‐breeding season. Both sexes answered partner songs faster and at higher rates during the pre‐breeding and female fertile stages. Partners duetted at a higher rate during the pre‐ and post‐breeding stages. Finally, song initiation rates and duet rate, but not song answering rates, correlated with frequency of territorial interactions with strangers. Although our findings indicate that song function may vary with sex, singing role and level of duet organization, our results suggest that in general duet functions to defend common territories and as a mutual mate guarding strategy in the rufous hornero.     

Social monogamy in a territorial salamander

Social monogamy, which does not necessarily imply mating or genetic monogamy, is important in the formation of male-female pair associations. We operationally define social monogamy as occurring when two heterosexual adults, exclusive of kin-directed behaviour, direct significantly less aggression and significantly more submission towards each other, and/or spend significantly more time associating with each other relative to other adult heterosexual conspecifics. Long-term pair associations (i.e. those lasting through a lengthy breeding season) that are characteristic of social monogamy are common in some taxa but are virtually unknown in amphibians. Recent studies, however, have suggested that red-backed salamanders, Plethodon cinereus, have complex (for amphibians) social systems. Our laboratory experiments tested the hypothesis that red-backed salamanders found in pairs in the forest display behaviours consistent with social monogamy. During the summer noncourtship season, newly collected male-females pairs showed no preference to associate with their partners more than with a novel conspecific of the opposite sex. However, during the autumn courtship season, paired males and females significantly directed preferential behaviours towards their partners rather than towards a surrogate or a novel paired salamander. Focal animals showed no significant preferences when presented with their partner and a novel single salamander, but they never directed preferential behaviours towards a novel salamander (whether paired or single) or a surrogate. These results are the first to suggest that a salamander species engages in social monogamy. Furthermore, our results suggest that social monogamy may not inhibit paired males and females from displaying alternative strategies: preferring partners when extrapair associations may be disadvantageous (i.e. the extrapair animal is already paired) but not preferring partners when extrapair associations may be advantageous (i.e. the extrapair animal is single). Copyright 2000 The Association for the Study of Animal Behaviour.     

Mating Systems,Maternal and Biparental Care in Triggerfish (Balistidae)

Groups of the triggerfish Pseudobalistes fuscus and Odonus niger were studied from the underwater laboratory Neritica in Eilat, Gulf of Akaba, in the Red Sea. Mating and the roles of the sexes during broodcare seem to depend strongly on territory size, probably determined by shelter site and food availability, and territorial control- and defendability. The discussion considers why evolution has favoured maternal broodcare in the one case and biparental in the other.     

Unbalanced biparental care during colony foundation in two subterranean termites

Parental care is a major component of reproduction in social organisms, particularly during the foundation steps. Because investment into parental care is often costly, each parent is predicted to maximize its fitness by providing less care than its partner. However, this sexual conflict is expected to be low in species with lifelong monogamy, because the fitness of each parent is typically tied to the other's input. Somewhat surprisingly, the outcomes of this tug‐of‐war between maternal and paternal investments have received important attention in vertebrate species, but remain less known in invertebrates. In this study, we investigated how queens and kings share their investment into parental care and other social interactions during colony foundation in two termites with lifelong monogamy: the invasive species Reticulitermes flavipes and the native species R. grassei. Behaviors of royal pairs were recorded during six months using a non‐invasive approach. Our results showed that queens and kings exhibit unbalanced investment in terms of grooming, antennation, trophallaxis, and vibration behavior. Moreover, both parents show behavioral differences toward their partner or their descendants. Our results also revealed differences among species, with R. flavipes exhibiting shorter periods of grooming and antennation toward eggs or partners. They also did more stomodeal trophallaxis and less vibration behavior. Overall, this study emphasizes that despite lifelong monogamy, the two parents are not equally involved in the measured forms of parental care and suggests that kings might be specialized in other tasks. It also indicates that males could play a central, yet poorly studied role in the evolution and maintenance of the eusocial organization.     

Behaviors in agonistic interaction of the butterflyfish (Chaetodon lunulatus)

The butterflyfish (Chaetodon lunulatus) forms heterosexual pair bonds. Each pair defends a feeding territory against conspecifics. In the field, I observed the agonistic interactions related to territoriality, and recognized nine behavioral patterns: staring, parallel swimming, rushing, tail-up display, chasing, fleeing, encircling, TT-fighting (two-piled-tops fighting), and attacking. Almost all interactions were conventional fighting in which attacking seldom occurred. In rare cases, interactions escalated to TT-fighting. In these cases, attacks were frequent, and outcomes were significant (e.g., territorial takeover and serious injuries). Received: October 24, 1998 / Accepted: August 23, 1999     

BEHAVIORAL CONVERGENCE AND ADAPTIVE RADIATION: EFFECTS OF HABITAT USE ON TERRITORIAL BEHAVIOR IN ANOLIS LIZARDS

Most studies of adaptive radiations focus on morphological aspects of differentiation, yet behavior is also an important component of evolutionary diversification, often mediating the relationship between animal ecology and morphology. In species within radiations that are convergent in ecology and morphology, we then also expect convergence in behavior. Here, we examined 13 Anolis lizard species to determine whether territorial strategies have evolved convergently with morphology and habitat use. We evaluated two aspects of territoriality: behavioral defense of space via territorial displays, and territory overlap within and between sexes. Controlling for the phylogenetic relationships of the taxa in our study, we found that species similar in perch height and diameter convergently evolved patterns of territory overlap, whereas species similar in habitat visibility (the proportion of space that can be seen from a perch) convergently evolved display behavior. We also found that species with greater display time have more extensive male–male territory overlap. This study provides strong evidence for the role of habitat in the evolution of territoriality and suggests that the social structure of a species ultimately evolves in concert with habitat use and morphology.     

Uncertainty in partner recognition and the tail-up display in a monogamous butterflyfish

Many monogamous birds and fish perform displays towards mates that are either identical or very similar to threat displays. Uncertainty in partner recognition may be a key to explaining this behaviour in the monogamous butterflyfishChaetodon lunulatus . From a causal perspective, when partner recognition is uncertain, the butterflyfish may follow the same decision rules as in territorial interactions with nonpartners. From this hypothesis, I derived three predictions of the frequencies of social behaviours, that is, solo displays, mutual displays, attacks and rejoinings. If the frequencies areS , M, A and R, respectively, the predictions are that (1) M/ (M+A) andM/ (M+S) should be higher in rejoining situations than in a pair-swimming situation; (2) (M+S)/R and (M+A) /R should increase with the duration of separation; and (3) M/ (M+A) should be larger than M/ (M+S). To test the predictions, I made field observations. The results supported all of these predictions. Therefore, I suggest that uncertainty of partner recognition causes the butterflyfish to perform the tail-up display, which is usually used in territorial interactions, towards the partner. From a functional perspective, this hypothesis implies that the display serves to reduce the risk of failure to recognize a partner, which could result in an attack. The display causes the conspecific to hesitate before attacking, providing sufficient time for partner recognition. Field data indicated that more than 70% of dangerous attacks were prevented by a tail-up display.     

High levels of extra-group paternity in a population of Australian magpies Gymnorhina tibicen: evidence from microsatellite analysis

Breeding systems vary widely in birds, from monogamous pairs through to complex group systems where subordinates assist breeding individuals to rear young each season. The Australian magpie varies geographically both in plumage patterns and social organization. Some populations of both eastern and western plumage forms are plural breeders with group size varying from three to over 15 mature individuals. This study used variation at microsatellite loci to determine the level of extra-group paternity in a population of the western form near Perth in Western Australia. Extra-group paternity was the highest recorded for any bird species to date (82%) and indicates that few offspring within a territory are sired by the social partner of the female. In addition, the data indicated that nearly 10% of juveniles were not the genetic offspring of any female within their territory, suggesting some intraspecific brood parasitism. Taken together, these findings are remarkable considering the highly territorial nature of the species and the extent of territorial defence practised by all members of the group towards extra-group conspecifics during daylight hours.     

The evolution of monogamy in primates

The evolution of primate monogamy is described as an ordered sequence of choices by generalized, hypothetical females and males. Females first choose whether or not to associate with other females. Predators encourage gregariousness in diurnal primates; however, nocturnality or scarce and evenly distributed food supplies may enforce separation. A testable group size model based on food patch size is developed and qualitatively supported.If females choose solitude, males then choose either to defend a single female and invest in her offspring, or to compete with other males for access to several females, usually by defending a territory or establishing dominance over the home ranges of several females. The decision rests on the defensibility of females and on the availability of an effective form of male parental investment. Both of these factors are dependent on local female population density. A model is developed that assumes that territorial defense is the principal form of male parental investment, and it predicts that monogamy should occur at intermediate densities: at high densities, males should switch to defense of multiple females, and at low densities there is no investment value in male territorial defense. The model is shown to be only partly adequate. Variation in local population densities prevents the establishment of obligate monogamy through territoriality in small monkeys, since male territorial behavior is inconsistent over the long run. Here, carrying of offspring by males can succeed territoriality, providing an effective and reliable form of parental investment to maintain the pair bond in the face of population fluctuations and changes in group structure. This hypothesis is supported by the scarcity of obligate monogamy among the prosimians, which frequently do not carry their young.     

Compensatory investment in zebra finches: females lay larger eggs when paired to sexually unattractive males

The classical version of the differential allocation hypothesis states that, when females reproduce over their lifetime with partners that differ in their genetic quality, they should invest more in reproduction with high-quality males. However, in species with lifetime monogamy, such as the zebra finch, partner quality will typically remain the same. In this case, the compensatory investment (CI) hypothesis predicts higher investment for low-quality males, because low genetic quality offspring are more dependent on maternal resources. Here, we show that female zebra finches invested more resources, both in terms of egg volume and yolk carotenoid content, when paired to a low genetic quality male, as judged from his previous ability to obtain extra-pair paternity in aviary colonies. We also found that females deposited slightly larger amounts of testosterone into eggs when paired to a low parental quality male, as judging from his previous success in rearing offspring. This is, to our knowledge, the first experimental support for the CI hypothesis in a species with lifetime monogamy. We stress that in more promiscuous species, the benefits of classical differential allocation may partly be neutralized by the supposed benefits of CI.     

The relationship between cumulative number of cohabiting partners and number of children for men and women in modern Sweden

Societies with institutional monogamy may be effectively polygynous through some males having several wives in succession: serial monogamy. This study investigates the relationship between the number of cohabiting partners and the number of children in a modern society where serial monogamy is common in both sexes. Data from an investigation on cohabitation and reproduction were provided by the Swedish Statistics Bureau, where the oldest cohort were used to estimated “lifetime” number of partners and children. The analyses were repeated for the next-to-oldest cohort. About 78% males and 79% females had one partner, and about 15% of both sexes had more than one partner during their reproductive lifespan in the oldest cohort. Thus, monogamy was predominant, and serial monogamy was equally common among men and women. Serial monogamy was somewhat more frequent in the next-to-oldest cohort. Remating increased the number of offspring for males, but not for females, in both cohorts. This is in accordance with the idea of serial monogamy being a conditional reproductive strategy for males in a society with institutional monogamy. However, the reproductive costs and benefits for females of remating are obscure. In the oldest cohort of males there were significantly more unskilled laborers with no partner and no children compared to other socioeconomic categories. The same pattern, however nonsignificant, was found for the next-to-oldest cohort and, according to SSB data, is strong when even younger age groups are included. Data on socioeconomic status for females were not provided.