Aggressiveness during monogamous pairing in the sleepy lizard, <Emphasis Type="Italic">Tiliqua rugosa</Emphasis>: a test of the mate guarding hypothesis

The Australian sleepy lizard, Tiliqua rugosa, maintains monogamous associations for an average of 6 weeks before mating each spring. One hypothesis to explain this prolonged partnership is that males are guarding their female partners from rival males. This hypothesis has three predictions, that males are more aggressive than females to conspecific males, that male aggression will increase as the time of mating gets closer, and that males will be more aggressive towards conspecific males when they are with their partner than when they are alone. We tested those predictions with indirect evidence of aggression, using counts of scale damage on randomly encountered lizards, and with direct observations of their responses to approaches by conspecific and heterospecific models. As predicted by the mate guarding hypothesis, males showed more evidence of aggression towards conspecifics than did females. However, in contrast to the hypothesis, males did not become more aggressive as the time of mating came closer, and males in pairs were less aggressive than males on their own. Mate guarding cannot be the only process that has led to the prolonged monogamous associations in this species. Parental care is also unknown in these lizards, and we suggest that monogamy may be maintained through some form of female coercion, allowing females to gain additional fitness from the enhanced vigilance that results from male proximity.     

Mate Guarding in the Cricket Gryllodes sigillatus: Influence of Multiple Potential Partners

There are several hypotheses as to the function of postcopulatory mate guarding. Control over the mate-guarding period by either sex could potentially influence relative reproductive success. Mate-guarding behaviour in Gryllodes sigillatus was studied under several conditions: 1. undisturbed pairs; 2. pairs with a single male intruder; 3. pairs exposed acoustically, visually and olfactorily to several other males; 4. pairs exposed freely to several other males; and 5. pairs exposed freely to several other females. The results provide support for the spermatophore retention and rival defence hypotheses. The efficacy of mate guarding was not compromised by the pair being in acoustic, visual and olfactory contact with several other males. Once pairs were exposed to free contact with several other males, the spermatophore retention time by the female declined significantly, indicating that the mate guarder's efficiency declines under competition from several rivals. In pairs exposed to contact with several females after mating, the mate-guarding period and spermatophore retention time declined as the mate guarder abandoned the mated female and pursued the other females. Termination of the effective mate-guarding period by either sex seems to be influenced by the number of other potential partners present.     

Female response to predation risk alters conspecific male behaviour during pre‐copulatory mate guarding

Mating behaviour often increases predation risk, but the vulnerability within mating pairs differs between the sexes. Such a sex difference is expected to lead to differences in responses to predation risk between the sexes. In the two‐spotted spider mite Tetranychus urticae, males engage in pre‐copulatory mate guarding because only the first mating results in fertilisation. We investigated (i) whether pre‐copulatory pairs are more conspicuous to the predatory mite Phytoseiulus persimilis than solitary females, (ii) whether the vulnerability to the predator differs between sexes within the pre‐copulatory pair, (iii) whether each sex of T. urticae responds to predation risk during pre‐copulatory mate guarding and (iv) whether T. urticae's response to predation risk affects predator behaviour. Because T. urticae females are immobile during pre‐copulatory mate guarding, we observed male behaviour to evaluate effects of predation risk. We found that the predators detect more pre‐copulatory pairs than solitary females and that more females than males of the pre‐copulatory pairs are preyed upon by the predators. The preference of spider mite males for pre‐copulatory pairs versus solitary females was affected by whether or not the female had been exposed to predators during development. Male T. urticae exposed to predation risk did not alter their behaviour. These results suggest that only the most vulnerable sex, that is the female, responds to predation risk, which modifies male behaviour. Regardless of T. urticae females’ experience, however, P. persimilis detected more T. urticae pre‐copulatory pairs than solitary females, suggesting that pre‐copulatory mate guarding itself is dangerous for T. urticae females when these predators are present. We discuss our results in the context of sex‐dependent differences in predation risk.     

Indirect female choice mediated by sex pheromones in the hermit crab Pagurus filholi

Males of the hermit crab Pagurus filholi perform precopulatory guarding behavior, and solitary males often show aggressive behavior to take away guarded females. Males behave coercively while guarding females, so direct mate choice by females seems difficult in such a situation. By performing several experiments we examined possible indirect female choice of hermit crab. Males were attached to a shell by their left cheliped to look like guarding pairs (fake guarding pairs). The shells were filled with cotton containing either seawater or pheromone water. The fake guarding pair with only seawater caused male–male combat in 60% of trials whereas with pheromone water combats occurred in 88% of trials. Mean duration of male–male combat was significantly longer in trials with drops of seawater containing pheromones than in those without pheromones. These results suggest guarding pairs themselves cause male–male combat by visual stimulation, that female sex pheromones have further significant function in the recognition of guarding pairs and intensification of male–male combat, and that females release sex pheromones while they are guarded. As a result of the combat, the larger male ended up guarding a female. This strongly suggests that females choose males indirectly by exploiting male–male competition induced by sex pheromones under male coercive behavior.     

Post-copulatory mate guarding by males of the demselfly Hetaerina vulnerata Selys (Odonata: Calopterygidae)

Males of the calopterygid damselfly Hetaerina vulnerata remain with their mates after copulating with them. The species exhibits two unusual features of post-copulatory mate guarding. First, a male will often leave his territory to accompany a female in tandem on a search for oviposition sites elsewhere. Second, a male will perch near his ovipositing female even though she completely submerges when egg-laying and cannot be captured and mated by another male while she is underwater. These activities carry two potential costs: (1) a male may miss other receptive females while guarding one mate and (2) he may lose his territory to an interloper while he is absent. These costs were low, however, because territorial males secured only one mating per 3.6 days on average. Moreover, 23 times out of 26, territorial males reclaimed their plots quickly after being away for 30–60 min. The gain from postcopulatory guarding came from being present to recapture a female should she fly up from the water after rejecting an oviposition site. There was a 40% chance that a female would leave one site to search for another during an oviposition bout. If the male were not present, his mate would be captured and mated by another individual (no female ever selected an oviposition site without being carried to it by a male). Her new partner would fertilize the remaining eggs in the female's clutch (if sperm precedence occurs in this species). The total number of eggs fertilized by a male will be affected by how well he prevents any one mate from copulating again before she lays her entire clutch and the total number of receptive females he captures. The variation in the degree of mate guarding by male odonates seems to be the evolutionary outcome of differences in fitness gains derived from these two competing activities in different ecological settings.     

Mate Guarding in Male Dall's Porpoises (Phocoenoides dalli)

Mate guarding, whereby a male closely attends and defends a fertile female from extra‐pair matings, is one mating tactic males of many species use to protect their paternity. Although female defense occurs in many species of terrestrial mammal, comparable examples among cetaceans are largely absent, potentially as a result of the wide dispersion and mobility of females and their prey. Here, we investigate whether the close association of individual male Dall's porpoises with individual females during the breeding season is consistent with mate guarding. As mate guarding is predicted to be costly, and in other taxa is often associated with a reduction in foraging efficiency, we also examine whether males trade‐off this activity with time at depth. Males maintained longer associations and closer distances with female partners than with male ones. They also surfaced in greater synchrony with, and more often approached, their female partners than male ones. In contrast to males with male partners, males paired with females engaged in agonistic interactions with other adult males, and infrequently affiliated with extra‐pair individuals. These data suggest males are actively attempting to maintain their associations with females, while also acting to reduce female extra‐pair copulations and increase their own paternity. Guarding males also undertook shorter dives than non‐guarding males, suggesting that they trade‐off time at depth with guarding. Such a trade‐off is likely to involve a reduction in foraging opportunities, due to a decrease in time spent at foraging depth. Mate guarding in this species may be facilitated by the relatively smaller size and decreased mobility of newly calved, estrous females, particularly if females also benefit from guarding.     

Mate guarding in a Caribbean village

Behavioral observation, economic, and genealogical data collected in a rural Trinidadian village indicate: (1) males courting the same females have higher rates of agonistic interactions (e.g., arguing, fighting) with each other than they do with other males; (2) females courting the same males do not have higher rates of agonistic interactions with each other than they do with other females; (3) exclusive (monogamous) mating relationships have lower rates of agonistic interactions than nonexclusive (polygamous) mating relationships; (4) coresident mates interact more frequently when the female is fecund; (5) coresident mates have higher rates of agonistic interactions when the female is fecund; (6) males with fecund mates have higher rates of agonistic interactions with other unrelated males than do males with infecund mates; (7) fecund females do not have higher rates of agonistic interactions with other females than do infecund females; and (8) females do not guard prosperous males (those from households with 6 or more acres of land) more intensely than poorer males. These results suggest that mate guarding is an important aspect of reproductive competition, and that there are significant male/female differences in mate guarding strategies in this human population.     

Absence of Mate Guarding in the Yellowhammer (Emberiza citrinella)?

The mate guarding behaviour of male yellowhammer (Emberiza citrinella) was studied with special reference to the effects of age, body size (tarsus length) and coloration of males. Measurements of intra-pair distance do at the most provide evidence for relatively lax mate guarding. On the other hand, patterns of male song activity and inter-male aggression were more in agreement with the predictions of the mate guarding hypothesis. The reasons for the comparatively low mate guarding intensity in the yellowhammer may be that males do not need to guard their mates intensely. Age differences were found in song and aggressive activity, older males singing and fighting the most. Size had no effect on guarding behaviour. Coloration was correlated with inter-male aggressiveness and conflict initiation propensity. Less colourful males fought the most in the pre-fertile period of their mates, whereas colourful and old males fought the most during the fertile period. This suggests that coloration may be an indicator of individual fighting and guarding ability.     

Testosterone, cuckoldry risk and extra-pair opportunities in the Seychelles warbler

In male birds, testosterone (T) plays an important role in aggressive and mate-attraction behaviour. In the cooperatively breeding Seychelles warbler, Acrocephalus sechellensis, extra-group copulations (EGCs) occur frequently, but are not accompanied by sexual courtship displays as in within-pair copulations. Paternity is nearly always gained by primary males. We investigated whether T levels and sperm storage capability (cloacal protuberance (CP)) in adult primary and subordinate males were related to timing of egg laying, levels of cuckoldry and extra-group paternity (EGP) opportunities. During the sexually active period before egg laying, T levels and CP were only elevated or enlarged (respectively) in primary males, and some suggestion was found that subordinate males do not invest in elevated T levels. The peak in T occurred during the fertile period of the female partner and corresponded to the peak period of male sexual displays and mate guarding, but was independent of cuckoldry risk (density of neighbouring primary males). CP was also enhanced during this period; however, CP but not T remained elevated after egg laying by their mates, and CP but not T was positively related to EGP opportunities (density of neighbouring fertile females). We conclude that T is involved in sexual courtship displays and mate guarding, but not in gaining EGCs. These findings contrast with those in other species where EGP involves elaborate sexual displays.     

Size, operational sex ratio, and mate-guarding success of the carrion beetle, Necrophila americana

When male insects guard females until oviposition, the benefitsfrom last-male sperm precedence must outweigh the costs of relinquishingadditional fertilizations. The profitability of guarding isincreased when males guard large, fecund females and when femalesare scarce because fewer fertilizations are sacrificed. However,the male reproductive success is not only determined by theprofitability of guarding but also by his ability to maintainguarding. In this study, we used male carrion beetles (Necrophilaamericana) to examine the effects of sex ratio, male relativesize, and female quality on the ability to guard. First, wepresent a model of mate guarding that explores factors, suchas sperm precedence, sex ratio, male size, and female quality,that influence the profitability of postcopulatory riding. Ourmodel predicts that large N. americana males should preferentiallyguard the largest female only when the sex ratio is male biasedand sperm precedence is above 80%. In contrast, small malesgain little from guarding because they are not likely to maintainit and be the last male to mate. Then, we tested these predictionsby manipulating sex ratio, relative male size, and female quality.All males in equal sex ratio and large males in male-biasedsex ratio guarded females significantly longer than did malesin female-biased sex ratio. In male-biased sex ratio, largemales guarded significantly longer and achieved more takeoversthan small males. Large females were guarded longer. The successof guarding males in this beetle depends on their size relativeto other males and the operational sex ratio.     

Flexible Mate Guarding Tactics in the Dragonfly Sympelrum Internum (Odonata: Libellulidae)

Mate guarding–a behaviour prevalent in odonates–is a post copulatory association during which males prevent females from re-mating. Some species use two forms of guarding: contact mate guarding, which is energetically costly but highly effective and non-contact mate guarding, which is less costly but less effective. This study aimed to determine if male Sympetrum internum (Odonata:Libellulidae) adjust the duration of contact mate guarding according to environmental, temporal and physiological factors. There was a significant interaction between male density and season on duration of contact mate guarding. Early in the season males increased the duration of contact guarding as the density of rivals increased. Later in the season males guarded mates longer irrespective of male density. Wind and temperature did not detectabiy alter the duration of contact mate guarding, suggesting that the trade-off between current and future reproductive success was more important than were physiological costs.     

Energetic costs of mate guarding behavior in male stream-dwelling isopods

In the stream-dwelling isopod Lirceus fontinalis, males and females engage in a precopulatory mate guarding phase prior to mating. We examined the energetic costs of mate guarding behavior in males by separately assaying glycogen and lipid content at different time increments following mating. We found that males that had recently mated possessed reduced glycogen reserves and that these reserves were fully replenished within 36 h. Conversely, we found that male lipid reserves were unaffected by time since mating. We concluded that precopulatory mate guarding behavior is energetically costly to males and that glycogen is the energy source utilized to pay that cost. We also examined whether food deprivation during the mate guarding phase affected male energy reserves (glycogen) at the end of that phase. We found that males that were held in the laboratory and starved during mate guarding possessed reduced glycogen at the termination of the phase when compared to fed males. This reduced quantity was equivalent to the glycogen reserves of recently mated males collected from the field. We propose that food deprivation during the mate guarding phase explains the reduction in glycogen reserves at the termination of that phase. We discuss these results with reference to patterns of refuge use behavior during the mate guarding phase.     

Guarding males protect females from predation in a wild insect

Males frequently remain in close proximity to their mate immediately postcopulation. This behavior has generally been interpreted as a guarding tactic designed to reduce the likelihood that a rival male can rapidly displace the ejaculate of the guarding male [1, 2]. Such attempts by males to control their mates represent a potential source of conflict [3-5], but guarding behaviors in species where it is difficult for males to control their mates suggest that conflict is not inevitable [6, 7]. We employed a network of infrared video cameras to study a wild population of individually marked and genotyped field crickets (Gryllus campestris). Lone females or males suffer similar rates of predation, but when a pair is attacked, the male allows the female priority access to their burrow, and in doing so dramatically increases his probability of being killed. In compensation for this increased predation risk, paired males mate more frequently and father more of the female's offspring. By staying with a male, females increase the sperm contribution of preferred males as well as reducing their predation risk. In contrast to conclusions based on previous lab studies, our field study suggests that mate guarding can evolve in a context of cooperation rather than conflict between the sexes.     

Reproductive Trade-Offs and Direct Costs for Males in Arthropods

Until 30 years ago, the emphasis on reproductive costs for males was mainly on costs related to mate searching, courtship and fighting with rival males. However, costs for males are substantial and varied and often resemble the more thoroughly studied female reproductive costs. Costs can be referred to as trade-off costs, where investment in reproductive activity comes at the expense of another important activity or fitness component. Investment in reproduction at the expense of longevity and future reproduction is the ultimate cost, because it affects fitness directly. In contrast, flawed performance (e.g., of the immune system) is perceived as a mechanistic trade-off, because it affects fitness indirectly through a mediator (i.e., parasites). Finally, direct costs refer to direct measurements of the energy expenditure during involvement in reproduction-related activities. Both direct and mechanistic trade-off costs often result in decreased longevity compared to unmated males (an ultimate cost). Males incur costs during different reproductive phases: before copulation, when producing sperm, while searching for, courting and copulating with females, and subsequently when guarding females or taking care of offspring. This synthesis follows previous pioneering reviews addressing specific aspects of male costs, but strives to summarize all known male reproductive cost types more comprehensively, including their classification. We suggest several directions for targeted future research. While costs for males have been fairly well described, it is now necessary to uncover the ecological and evolutionary factors responsible for differences between closely related species and systems and to better link between directly-measured costs, mechanistic trade-off costs and ultimate trade-off costs.     

Part-Time Mate Guarding Affects Paternity in Male Reed Buntings (Emberiza schoeniclus)

Male mate guarding by close following has been reported in many socially monogamous bird species and is generally believed to function as a paternity guard. Many aspects of the dynamics and effectiveness of this behavior are still however poorly understood. Here, we describe the temporal variation in mate guarding behavior in male reed buntings (Emberiza schoeniclus) with a particular focus on how males allocate their mating effort between mate guarding and extrapair mating in a context of intense sperm competition. In our highly synchronous study population most males have to balance the simultaneous and mutually exclusive demands of mate guarding and seeking extrapair copulations (EPCs). We found that males frequently switched between guarding their mates and performing intrusions to neighboring territories. Both activities seemed to have significant fitness payoffs, as male mate guarding effort had a positive effect on paternity, and a large fraction of extrapair fertilizations occurred during the days when the sire guarded its own female. The reed bunting is thus an example of how discontinuous or part‐time mate guarding can still be effective in securing paternity. Female reed buntings were not particularly active in initiating EPCs as they never were observed performing extraterritorial forays. We argue that the absence of female‐initiated EPCs is a prerequisite for males to trade mate guarding against seeking EPCs. Otherwise, if females circumvent male mate guarding by timing their EPCs to periods of male absence, males should guard their mates almost continuously or rely on alternative paternity guards.     

Mated pairs of owl monkeys (Aotus nancymaae) exhibit sex differences in response to unfamiliar male and female conspecifics

In socially monogamous species, mate‐guarding could be a reproductive strategy that benefits both males and females, especially when males contribute to parental care. By actively guarding mates, males may reduce their chances of being cuckolded, whereas females that mate‐guard may reduce the likelihood that their mates will desert them or acquire additional mates, and hence limit or reduce paternal care of offspring. Owl monkeys (Aotus spp.) are socially monogamous with biparental care of young and, hence, potential beneficiaries of mate‐guarding. We presented mated pairs of captive owl monkeys (A. nancymaae) with unfamiliar male and female conspecifics, to determine if either member of the pair exhibits intraspecific aggression toward an intruder or stays close to its mate, behaviors indicative of mate‐guarding. Male mates were more responsible for the maintenance of close proximity between mates than females. Male mates also exhibited elevated levels of behavior that signify arousal when presented with a male conspecific. These responses by mated male owl monkeys are consistent with patterns that may help prevent cuckoldry. Am. J. Primatol. 72:942–950, 2010. © 2010 Wiley‐Liss, Inc.     

Navigation by Male Crab Spiders <Emphasis Type="Italic">Misumenoides formosipes</Emphasis> (Araneae: Thomisidae): Floral Cues May Aid in Locating Potential Mates

The crab spider Misumenoides formosipes is an ambush predator whose males search for relatively sedentary females within a heterogeneous habitat. Females are receptive to mating immediately after their adult molt and a male biased adult sex ratio together with precopulatory guarding places a premium on male ability to locate females quickly. It is unknown what cues males use to find females; we report here on male movements in association with floral cues. Males in field trials moved towards inflorescences more frequently when both visual and chemical cues were available, than when chemical cues were eliminated. Males in lab trials chose an inflorescence over leaf substrates even in the absence of visual cues. These findings support the hypothesis that M. formosipes males could utilize floral chemistry as a navigational cue in mate searches.     

Mate Choice in Male Mandrills (Mandrillus sphinx)

Male primates that attempt to monopolize access to receptive females by mate‐guarding expend time and energy and risk injury, making reproduction costly. Males should therefore show mate choice and preferentially allocate mating effort to females that are likely to be fertile and those that will produce high‐quality offspring. Specifically, males should preferentially mate‐guard high‐ranking females rather than low‐ranking females, as such females are more likely to be fertile and are able to invest more in offspring. Males should also prefer parous females to nullipares, for similar reasons. Finally, males should avoid mating with close relatives, to avoid the deleterious effects of inbreeding. We investigated 13 group‐years of mate‐guarding observations for two semi‐free‐ranging groups of mandrills to examine the influence of these factors on male investment in mate‐guarding. We found that males mate‐guarded higher‐ranking females more than lower‐ranking females, and parous females more than nullipares. Female age, true relatedness and maternal kinship did not influence male mate‐guarding. Our results suggest that male mandrills do exercise mate choice for higher‐quality females, in the form of higher‐ranking and parous females. As alpha males are responsible for the great majority of mate‐guarding, this can lead to assortative mating, where high‐ranking males reproduce with high‐ranking females, and has important implications for social relationships and kin selection.     

Factors influencing mate guarding and territory defence in the stitchbird (hihi)

Socially monogamous male birds are predicted to maximise their reproductive success by pursuing extra-pair copulations (EPCs) while engaging in anti-cuckoldry behaviour such as mate guarding. In the stitchbird, Notiomystis cincta, high levels of forced EPCs and a high proportion of nestlings resulting from extra- pair fertilisations lead to the prediction that males of this species should exhibit intense paternity guarding behaviours. While studying an isolated stitchbird population on Tiritiri Matangi Island New Zealand (3636'S, 17453'E), I collected daily behavioural data throughout the breeding season from 15 males in 2000/01 and 27 males in 2001/02. In this study, male stitchbirds demonstrated clear paternity guarding by exhibiting: (1) an increased likelihood of being close to their mate during her fertile period, (2) an increased initiation of mate contact during her fertile period, (3) switching from site-specific territorial defence during the pre-fertile period to defending an area centring on the their female partners location during her fertile period, and (4) an increased following of the female to communal feeding sites outside the territory during her fertile period. For polygynous males, mate guarding and territorial defence were conditional on which of their females was fertile. Additional evidence supporting the hypothesis that mate guarding in this species is a form of paternity assurance, rather than protection from harassment, is that males protected their partner from harassment by other stitchbird males but did not intervene when females were harassed by male bellbirds, Anthornis melanura. While mate-guarding intensity in many species is conditional on the stage of female fertility, male stitchbirds also modified their behaviour depending on the location of the female and the rate of intrusions by extra-pair males. Resident males adopted a best-of-a-bad-job tactic when they were unable to locate their female by defending an area around her last known location. Furthermore, when the rate of intrusions by extra-pair males increased they traded-off the area they could defend within their territory against their ability to guard the female. Territory takeovers were uncommon, but when they did occur older males displaced younger males and healthy birds displaced sick ones. Contrary to the prevailing view that mate guarding is a male response to female infidelity, male stitchbirds appear to use mate guarding primarily to prevent paternity losses from forced EPCs. Future assessments of mate guarding function should consider the possibility that mate guarding involves a combination of conflict and co-operation between the sexes.     

Following trails of partners in the monogamous lizard, Tiliqua rugosa

The sleepy lizard, Tiliqua rugosa, is an Australian scincid lizard that forms monogamous pairs for 6–8 weeks in the spring before mating occurs. Previous observations and experiments have shown that when partners are separated they can relocate each other, and one suggested mechanism has been trail following. In this article we report results from field-based Y-maze experiments to investigate trail following. In the first part of the spring season, female lizards were more likely to use the arm of the maze previously taken by their male partner than either a blank arm of the maze or the arm taken by an unfamiliar adult male. Females that were more frequently found with their male partner during the spring season were more likely to follow the path of their male partner than less strongly bonded females. In the second part of the spring, after mating had occurred in the natural population, females no longer showed a preference in the maze. Males showed no significant tendency to follow their female partner in any part of the season. The results suggest there is trail following, at least by females, and that females play an active role in maintaining the partnership. This refutes male-based explanations, like mate guarding, for monogamy. Electronic Publication