Male Great Tits Research Articles

Is microevolution the only emergency exit in a warming world? Temperature influences egg laying but not its underlying mechanisms in great tits

Many bird species have advanced their seasonal timing in response to global warming, but we still know little about the causal effect of temperature. We carried out experiments in climate-controlled aviaries to investigate how temperature affects luteinizing hormone, prolactin, gonadal development, timing of egg laying and onset of moult in male and female great tits. We used both natural and artificial temperature patterns to identify the temperature characteristics that matter for birds. Our results show that temperature has a direct, causal effect on onset of egg-laying, and in particular, that it is the pattern of increase rather than the absolute temperature that birds use. Surprisingly, the pre-breeding increases in plasma LH, prolactin and in gonadal size are not affected by increasing temperature, nor do they correlate with the onset of laying. This suggests that the decision to start breeding and its regulatory mechanisms are fine-tuned by different factors. We also found similarities between siblings in the timing of both the onset of reproduction and associated changes in plasma LH, prolactin and gonadal development. In conclusion, while temperature affects the timing of egg laying, the neuroendocrine system does not seem to be regulated by moderate temperature changes. This lack of responsiveness may restrain the advance in the timing of breeding in response to climate change. But as there is heritable genetic variation on which natural selection can act, microevolution can take place, and may represent the only way to adapt to a warming world.

Male great tit song perch selection in response to noise‐dependent female feedback

Summary1. Anthropogenic noise can affect intra‐pair communication and therefore interfere with reproductive success. However, many animals have various signal strategies to cope with noise, although it is unclear whether they rely on direct auditory feedback from their own perception of noise or signal‐to‐noise level or on indirect social feedback from receivers.2. We studied the role of social feedback on male great tit (Parus major) song adjustment by exclusively exposing females to artificial traffic noise inside their nest box.3. We found a delay in female response latencies to male song in the noisy condition compared to the control condition on the first day of noise exposure. Males from the noise treatment group, not directly exposed to noise themselves, sang closer to the nest box within 3 days after the start of exposure.4. The male's closer proximity to the nest box most likely led to the observed higher song amplitudes at the noisy nest boxes compared to quiet control nest boxes, and explains why the inside signal‐to‐noise ratios were restored to equal levels between treatment and control nest boxes after several days of exposure.5. The initial difference between treatment groups in female response latencies at the start of exposure also disappeared accordingly.6. Our results strongly suggest an active role for female birds in steering male song behaviour under noisy conditions. Males did not receive direct exposure during intra‐pair communication, but adjusted their behaviour in the predicted direction. These data are important to understand the mechanisms related to communication in noise and reveal the critical role of ecology in shaping animal interactions.

Worms under cover: relationships between performance in learning tasks and personality in great tits (Parus major)

In animals, individual differences in learning ability are common and are in part explained by genetic differences, developmental conditions and by general experience. Yet, not all variations in learning are well understood. Individual differences in learning may be associated with elementary individual characteristics that are consistent across situations and over time, commonly referred to as personality or temperament. Here, we tested whether or not male great tits (Parus major) from two selection lines for fast or slow exploratory behaviour, an operational measure for avian personality, vary in their learning performance in two related consecutive tasks. In the first task, birds had to associate a colour with a reward whereas in the second task, they had to associate a new colour with a reward ignoring the previously rewarded colour. Slow explorers had shorter latencies to approach the experimental device compared with fast explorers in both tasks, but birds from the two selection lines did not differ in accomplishing the first task, that is, to associate a colour with a reward. However, in the second task, fast explorers had longer latencies to solve the trials than slow explorers. Moreover, relative to the number of trials needed to reach the learning criteria in the first task, birds from the slow selection line took more trials to associate a new colour with a reward while ignoring the previously learned association compared with birds from the fast selection line. Overall, the experiments suggest that personality in great tits is not strongly related to learning per se in such an association task, but that birds from different selection lines might express different learning strategies as birds from the different selection lines were differently affected by their previous learning performance.

Anticipating Spring: Wild Populations of Great Tits (Parus major) Differ in Expression of Key Genes for Photoperiodic Time Measurement

Measuring day length is critical for timing annual changes in physiology and behavior in many species. Recently, rapid changes in several photoperiodically-controlled genes following exposure to a single long day have been described. Components of this ‘first day release’ model have so far only been tested in highly domesticated species: quail, sheep, goats and rodents. Because artificial selection accompanying domestication acts on genes related to photoperiodicity, we must also study this phenomenon in wild organisms for it to be accepted as universal. In a songbird, the great tit (Parus major), we tested whether a) these genes are involved in photoperiodic time measurement (PTM) in a wild species, and b) whether predictable species and population differences in expression patterns exist. Using quantitative RT-PCR, we compared gene expression after a single long day in male great tits from Sweden (57°42′N) with that from a German (47°43′N) population. Hypothalamic gene expression key for PTM changed only in the northern population, and occurred earlier after dawn during the single long day than demonstrated in quail; however, gonadotropins (secretion and synthesis) were stimulated in both populations, albeit with different timing. Our data are the first to show acute changes in gene expression in response to photostimulation in any wild species not selected for study of photoperiodism. The pronounced differences in gene expression in response to a single long day between two populations raise exciting new questions about potential environmental selection on photoperiodic cue sensitivity.

Maternal effects reduce oxidative stress in female nestlings under high parasite load

Mothers can adjust the phenotype of their offspring to the local environment through a modification of their egg investment and/or nestling provisioning. However, offspring health may be severely impaired if the conditions experienced by nestlings do not match with those anticipated by the mother. If maternal effects differentially affect the sexes or if one sex is more strongly affected by an environmental stressor, fitness benefits may also differ between male and female offspring. Here, we study maternal effects in male and female great tit Parus major nestlings by means of an ectoparasite treatment before egg‐laying combined with a partial cross‐foster experiment between broods of infested and uninfested nests. Nestlings that were raised in their own nest experienced the same conditions before and after cross‐fostering (either in parasite infested or uninfested nests), while cross‐fostered ones experienced different conditions (either changing from infested to uninfested or the other way around). We measured effects on nestling plasma levels of oxidative stress [reactive oxygen metabolites (ROMs) and total antioxidant capacity (OXY)], body condition (body size and mass) and post‐fledging survival. Daughters, but not sons, from matching conditions showed the lowest ROM and high OXY levels when exposed to parasites, while there was no effect of parasite exposure in any of both sexes in case of a mismatch. In contrast, body condition and post‐fledging survival were not (or only slightly) affected by any of the experimental treatments. Results of this study show that maternal effects can affect oxidative stress levels of nestlings in a sex‐specific way and that the outcome depends on the exposure to environmental stressors, such as parasites.

Intraspecific social information use in the selection of nest site characteristics

Animals commonly acquire information about the environment by monitoring how others interact with it. The importance of social information use probably varies among species. In particular, many migratory birds breeding in northern latitudes rely on social information provided by resident tits when making important decisions and are able to copy or reject selectively the decisions of tits exhibiting good or bad fitness correlates, respectively. However, little is known about the role of social information use among resident tits. In a field experiment we tested whether great tits, Parus major, given a choice between two novel alternative features on adjacent nest sites, copy or reject conspecific choice represented by a simulated tit nest nearby, when the nest exhibits a high or low fitness correlate (clutch size). In contrast to the results in the interspecific setting, the portrayed fitness of the simulated nest did not affect tits’ nest site choices. However, the age of males had an effect, irrespective of the fitness correlate. Pairs with an old male preferred, while pairs with a young male tended to reject, the nest site choices of the simulated previously settled conspecifics. This result is surprising, as the final nest site choice in this species is presumably made by females, whose age and other phenotypic traits did not have an effect here. Our results imply stronger influence of the male great tits on nest site choice than previously thought. Dominance relationships and intraspecific competition are possible explanations for the age-dependent patterns in social information use.

Promiscuity, paternity and personality in the great tit

Understanding causes of variation in promiscuity within populations remain a major challenge. While most studies have focused on quantifying fitness costs and benefits of promiscuous behaviour, an alternative possibility--that variation in promiscuity within populations is maintained because of linkage with other traits-has received little attention. Here, we examine whether promiscuity in male and female great tits (Parus major)--quantified as extra-pair paternity (EPP) within and between nests--is associated with variation in a well-documented personality trait: exploration behaviour in a novel environment. Exploration behaviour has been shown to correlate with activity levels, risk-taking and boldness, and these are behaviours that may plausibly influence EPP. Exploration behaviour correlated positively with paternity gained outside the social pair among males in our population, but there was also a negative correlation with paternity in the social nest. Hence, while variation in male personality predicted the relative importance of paternity gain within and outside the pair bond, total paternity gained was unrelated to exploration behaviour. We found evidence that males paired with bold females were more likely to sire extra-pair young. Our data thus demonstrate a link between personality and promiscuity, with no net effects on reproductive success, suggesting personality-dependent mating tactics, in contrast with traditional adaptive explanations for promiscuity.

Immune activation reduces sperm quality in the great tit.

Mounting an immune response against pathogens incurs costs to organisms by its effects on important life-history traits, such as reproductive investment and survival. As shown recently, immune activation produces large amounts of reactive species and is suggested to induce oxidative stress. Sperm are highly susceptible to oxidative stress, which can negatively impact sperm function and ultimately male fertilizing efficiency. Here we address the question as to whether mounting an immune response affects sperm quality through the damaging effects of oxidative stress. It has been demonstrated recently in birds that carotenoid-based ornaments can be reliable signals of a male's ability to protect sperm from oxidative damage. In a full-factorial design, we immune-challenged great tit males while simultaneously increasing their vitamin E availability, and assessed the effect on sperm quality and oxidative damage. We conducted this experiment in a natural population and tested the males' response to the experimental treatment in relation to their carotenoid-based breast coloration, a condition-dependent trait. Immune activation induced a steeper decline in sperm swimming velocity, thus highlighting the potential costs of an induced immune response on sperm competitive ability and fertilizing efficiency. We found sperm oxidative damage to be negatively correlated with sperm swimming velocity. However, blood resistance to a free-radical attack (a measure of somatic antioxidant capacity) as well as plasma and sperm levels of oxidative damage (lipid peroxidation) remained unaffected, thus suggesting that the observed effect did not arise through oxidative stress. Towards the end of their breeding cycle, swimming velocity of sperm of more intensely colored males was higher, which has important implications for the evolution of mate choice and multiple mating in females because females may accrue both direct and indirect benefits by mating with males having better quality sperm.

A rapid effect of handling on counts of white blood cells in a wintering passerine bird: a more practical measure of stress?

Measuring circulating glucocorticoids is a widely used method to assess stress in animals. However, hormones must be sampled within the first few minutes of capture, which makes it difficult to discriminate between hormone baseline levels and the levels caused by capture and handling stress. The use of white blood cell (WBC) counts made from blood smears represents an alternate method for measuring physiological stress. Since the increase in glucocorticoid hormones causes characteristic long-lasting changes in the leukocyte numbers, we tested whether stress-related handling of male Great Tits (Parus major) may cause rapid changes in their leukocyte profile. We found that handling stress significantly increased heterophil counts between 30 and 60 min after capture, while lymphocyte and eosinophil counts significantly declined between 60 and 120 min after capture. The increase in heterophil counts and reduction in lymphocyte counts caused an increase of the heterophil and lymphocyte ratio (H/L) between 60 and 120 min after capture. Overall, these results indicate that leukocyte profiles in wintering male Great Tits may change more rapidly than previously thought, reflecting acute stress of individual birds.

Correlated response to selection of testosterone levels and immunocompetence in lines selected for avian personality

Individuals within species differ in their behavioural reactions to the environment. Consistent individual differences in these behaviours (personality traits) are often correlated and known to be under natural selection. These differences are frequently associated with variation in physiological traits, such as endocrine profiles. For example, variation in circulating testosterone levels is associated with variation in several personality traits and has been hypothesized to be a marker for personality in humans and rodents. The importance of testosterone in controlling both behavioural strategies and individual physiological differences suggests that direct selection on personality traits might cause pleiotropic selection on the physiological mechanisms underlying these traits. To test this hypothesis, we quantified levels of plasma testosterone levels and measured phytohaemagglutinin (PHA)-induced immune responses of male great tits, Parus major, in lines artificially selected for diverging levels of avian personality (‘fast’ and ‘slow’ exploratory behaviour). We found that testosterone levels were highly repeatable within individuals and fluctuated predictably over the season. Contrary to our expectations, ‘slow’ explorers had consistently higher levels of baseline testosterone and higher immune responses than ‘fast’ explorers. These results show that phenotypic selection for variation in personality traits corresponds to consistent differences in hormone profile and immune function, but that higher aggression levels do not need to be associated with higher baseline testosterone levels. Our results confirm that personality traits have evolved as a result of selection on both the underlying controlling physiological mechanisms and the phenotypic traits.

Songs differing in consistency elicit differential aggressive response in territorial birds

Acoustic signals during intrasexual interactions may help receivers to establish the cost and benefits of engaging in a confrontation versus avoiding the cost of escalation. Although birdsong repertoires have been previously suggested as providing information during agonistic encounters, the cost (time/neural resources) of assessing large repertoires may decrease the efficiency of the signal for mutual assessment. Acoustic-structural features may, therefore, be used to enable a fast and accurate assessment during this kind of encounters. Recently, it has been suggested that the consistency of songs may play a key role during intrasexual interactions in bird species. Using a playback experiment in a colour-ringed great tit population, we tested the hypothesis that songs differing in consistency may elicit a differential response, indicating that the signal is salient for the receivers. Great tit males clearly responded more aggressively towards highly consistent songs. Our findings, together with previous evidence of increased song consistency with age in the great tit, suggest that song consistency provides information on experience or dominance in this species, and this phenomenon may be more widespread than currently acknowledged.

Repertoire Sharing and Song Similarity between Great Tit Males Decline with Distance between Forest Fragments

AbstractBirdsong can play a critical role in establishing a territory and finding a mate among individuals from local and foreign populations. Variation in birdsong among populations can be influenced by habitat fragmentation and might affect successful dispersal among habitat fragments. We studied variation in great tit song in a long‐term study population distributed over nine forest fragments. All individual males recorded had a known dispersal history within the fragmented forest habitat. We found spatial structure of declining song‐type sharing with distance, with a marked drop from an individual’s own forest fragment to another across a habitat gap. We also found decreasing song similarity among increasingly distant fragments in terms of temporal and spectral characteristics of shared song types. The change in acoustic structure was more gradual and seemed less affected by habitat discontinuity but also showed a tight correlation with dispersal index among forest fragments. Immigrant birds shared fewer song types with neighbouring birds that were born within the same forest fragment, but not less compared to birds born in another forest fragment within the study area. Our data provide detailed insight into the relationship between song differentiation and male dispersal and contribute to our understanding of the potential role of song in reproductive exchange and avian speciation. The fact that birds in small forest fragments shared more songs than birds in larger forest fragments confirms that song analysis has potential as a tool for conservation in rare species.

How blue are British tits? Sex, age and environmental effects

Capsule The blue colour of the coverts and crowns of Blue Tits Cyanistes caeruleus and Great Tits Parus major is influenced by sex, age and environmental factors. Aims To quantify the blueness of two species of tits breeding in different habitats in Britain. Methods By manipulating daylength in the laboratory, adult Blue Tits were induced to moult at fast and slow speeds. When they had finished, the blue colour of their wing coverts and crowns was measured (in the range visible to human observers), and compared with the colour of birds caught in the field. Results As well as highly significant sex and age differences in colour, Blue Tits were 26% bluer in 1998 than 2000, and male Great Tits were 15% less blue in small woods than in large woods in our study population in East Anglia, England. Both species became more saturated with blue up to the age of three years. British Cy. c. obscurus were darker blue than Cy. c. caeruleus of Continental Europe Conclusions There are significant environmental influences on the blueness of British tits in addition to the well‐known age and sex effects.

Effects of personality on territory defence in communication networks: a playback experiment with radio-tagged great tits

Individuals often differ consistently in behaviour across time and contexts, and such consistent behavioural differences are commonly described as personality. Personality can play a central role in social behaviour both in dyadic interactions and in social networks. We investigated whether explorative behaviour, as proxy of personality of territorial male great tits (Parus major), predicts their own and their neighbours' territorial responses towards simulated intruders. Several weeks prior to playback, subjects were taken from the wild to test their exploratory behaviour in a standard context in the laboratory. Exploratory behaviour provides a proxy of personality along a slow-fast explorer continuum. Upon release, males were radio-tracked and subsequently exposed to interactive playback simulating a more or a less aggressive territorial intruder (by either overlapping or alternating broadcast songs with the subjects' songs). At the same time, we radio-tracked a neighbour of the playback subject. Male vocal responses during playback and spatial movements after playback varied according to male explorative behaviour and playback treatment. Males with lower exploration scores approached the loudspeaker less, and sang more songs, shorter songs and songs with slower element rates than did males with higher exploration scores. Moreover, neighbour responses were related to the explorative behaviour of the subject receiving the playback but not to their own explorative behaviour. Our overall findings reveal for the first time how personality traits affect resource defence within a communication network providing new insights on the cause of variation in resource defence behaviour.

Plumage coloration can be perceived as a multiple condition‐dependent signal by Great Tits Parus major

The evolution of multiple signals can be explained because they enhance the perception of a general message by recipients. Plumage coloration frequently acts as a condition‐dependent signal, so that species displaying different colour patches have the potential to transmit information on condition through a multiple signalling system. The Great Tit Parus major exhibits plumage colour patches generated by the main types of colour production, some of which, particularly those based on melanins and carotenoids, are known to be related to body condition. However, the colour expressions of all of the different colour types have never been investigated simultaneously to determine whether they function as multiple signals of condition. In addition, visual perception models have never been applied to a multiple signalling system in a wild population of birds. Here I present information that links body condition with the colour expression of almost all of the different plumage patches of male Great Tits captured during the winter. Birds in better condition had greater reflectance values at short wavelengths in all plumage patches, and this was especially so in the white (i.e. structural) colour of the cheeks. Plumage colour characteristics were calculated by means of avian visual models, suggesting that Great Tits have the capacity to perceive information contained in the plumage coloration of conspecifics. These results show that short‐wavelength reflectance has great potential to transmit biologically significant information on the body condition of birds, even in achromatic plumage patches.

Interspecific cross-fostering of great tits (Parus major) by blue tits (Cyanistes caeruleus) affects inter- and intraspecific communication

Summary Bird song is used to attract mates and deter rivals, and also functions as a species recognition cue. It is a flexible trait affected by learning, hence the choice of song tutors may affect an individuals’ singing. By interspecifically cross-fostering great tits (Parus major) to blue tits (Cyanistes caeruleus) in the wild, we have manipulated the species recognition of great tits, which in turn has influenced their song. In the present study, we presented breeding great tit and blue tit control males with playback of the aberrant song of cross-fostered great tit males and playback of the normal song of control great tit males. Blue tit males responded more to cross-fostered than control great tit song while great tit males showed the inverse response pattern. This shows that interspecific cross-fostering may affect both inter- and intraspecific communication. However, the response of males of both species towards the song of crossfostered great tit males was not of the same magnitude as the response towards ordinary blue tit song; thus, the real species identity is to some extent maintained in the aberrant song of cross-fostered males.

Cheek Plumage Uniformity as a Social Status Signal in Great Tits

Some plumage patterns in birds, such as irregularities of feathers, are potential amplifiers because they can reveal damage by conspecifics and therefore social status. We experimentally manipulated the pattern of the white cheeks of male great tits (Parus major) in order to simulate the effects of peckings by others and thus investigate possible changes in dominance during agonistic encounters at artificial feeders exposed to different risks of predation during winter. As predicted, manipulated birds were displaced by controls from safe feeders, and performed a lower number of aggressions and with lower success, although they did not receive more aggressions as expected from the fact that efficient agonistic displays can avoid the occurrence of overt aggressions. Thus, our manipulation changed the social status of birds by converting individuals with manipulated cheeks into subordinates. We propose that cheek colour uniformity acts as an amplifier of the outcomes of aggressions in great tits.

Brighter Great Tit parents build bigger nests

Nest size is commonly believed to be naturally selected,and to covary with requirements of developing eggs andnestlings (Collias & Collias 1984). In many altricial birdspecies, it is an important component of parental effort,as parents devote an important amount of energy andtime to nest building, but by doing so they expose them-selves and their offspring to a substantial predation risk(Martin et al. 2000). In this paper, we studied nest-sizevariation in a Great Tit Parus major population in rela-tion to breeding factors and parental carotenoid-basedplumage characteristics. The Great Tit is a secondary-cavity nesting species and females are solely responsiblefor building the nest (Gosler 1993). Sexual signalling viacarotenoid-based plumage coloration is known to occurin this species (Hill & McGraw 2006). We found thatplumage chroma of female and especially male GreatTits was positively related to nest size, suggesting greaterfemale investment in nest building when mated to malesin good condition.Nest-building behaviour and ultimately the nest itselfare often associated with courtship and pair formation(Collias & Collias 1984, Soler et al. 1998a). Further,nest-building behaviour may be involved in post-matingsexual communication between partners (Soler et al.1998a). In this way, individuals may increase their nest-building effort to signal their quality, or willingness toinvest in the current reproductive event (e.g. Soler et al.2001). Likewise, they may respond to their partner’scharacteristics in a similar way, to promote their invest-ment. However, knowledge of the use of the nest as apost-mating sexual display is limited, and most empiricalevidence comes from species where males are responsi-ble for nest building (Moreno et al. 1994, Hoi et al.1996, Soler et al. 1998b, 2001).Plumage coloration is known to be a sexually selectedcharacter signalling individual quality, and is ofteninvolved in pair formation and courtship (Hill &McGraw 2006). In particular, carotenoid-based plumagecoloration has been the focus of numerous recent stud-ies, and as carotenoids can only be obtained through thediet, they can be reliable indicators of the bearer’s feed-ing efficiency (Senar & Escobar 2002, Senar et al. 2008),body condition (Saks et al. 2003a, 2003b, Ferns & Hins-ley 2008) and survival (Horak et al. 2001). Thus, carot-enoid-based plumage coloration can reflect individualparenting ability (Senar et al. 2002, Doutrelant et al.2008), and consequently could be expected to affect sev-eral components of parental investment and resourceallocation (Clutton-Brock & Godfray 1991). In this way,nest-size variation may be related to parental quality,which in turn may be reflected by the parents’ plumagecoloration.METHODSThe study was performed in a forest area (c.4km

Temperature-induced elevation of basal metabolic rate does not affect testis growth in great tits

The timing of reproduction varies from year to year in many bird species. To adjust their timing to the prevailing conditions of that year, birds use cues from their environment. However, the relative importance of these cues, such as the initial predictive (e.g. photoperiod) and the supplemental factors (e.g. temperature), on the seasonal sexual development are difficult to distinguish. In particular, the fine-tuning effect of temperature on gonadal growth is not well known. One way temperature may affect timing is via its strong effect on energy expenditure as gonadal growth is an energy-demanding process. To study the interaction of photoperiod and temperature on gonadal development, we first exposed 35 individually housed male great tits (Parus major) to mid-long days (after 6 weeks of 8 h L:16 h D at 15 degrees C, photoperiod was set to 13 h L:11 h D at 15 degrees C). Two weeks later, for half of the males the temperature was set to 8 degrees C, and for the other half to 22 degrees C. Unilateral laparotomies were performed at weeks 5 (i.e one week before the birds were transferred to mid-long days), 8 and 11 to measure testis size. Two measures of basal metabolic rate (BMR) were performed at the end of the experiment (weeks 11 and 12). Testis size increased significantly during the course of the experiment, but independently of the temperature treatment. BMR was significantly higher in birds exposed to the cold treatment. These results show that temperature-related elevation of BMR did not impair the long-day-induced testis growth in great tits. As a consequence, temperature may not be a crucial cue and/or constraint factor in the fine-tuning of the gonadal recrudescence in male great tits, and testis growth is not a high energy-demanding seasonal process.

Interspecific cross-fostering affects mate guarding behaviour in great tits (Parus major)

Mate guarding is thought to decrease the likelihood of cuckoldry and, hence, increase the fitness of guarding males. Mate guarding is costly for males and must be traded off with other fitness-enhancing behaviours. Over several years, we have cross-fostered great tits ( Parus major ) to blue tits ( Cyanistes caeruleus ) and this experimental treatment has influenced the mate and rival recognition of cross-fostered birds. Here we show that cross-fostered great tit males mate guard their females less than do control great tits, regardless of whether the cross-fostered males were mated to great tit females or cross-fostered blue tit females. Cross-fostered great tit males sang more and interacted more frequently with blue tit males than did controls. Females paired to males of the two groups did not differ in the extent to which they initiated movements away from their mates. We conclude that the altered species-assortative behaviour resulting from interspecific cross-fostering influences mate guarding in great tit males, probably by cross-fostered males increasing investment in territorial behaviour at the expense of mate guarding, and/or by cross-fostered males mate guarding less due to a reduced affinity for their female. Such trade-offs may have a general significance for mate guarding species.