Vasotocin neurons and septal V1a-like receptors potently modulate songbird flocking and responses to novelty

Previous comparisons of territorial and gregarious finches (family Estrildidae) suggest the hypothesis that arginine vasotocin (VT) neurons in the medial bed nucleus of the stria terminalis (BSTm) and V_1a-like receptors in the lateral septum (LS) promote flocking behavior. Consistent with this hypothesis, we now show that intraseptal infusions of a V_1a antagonist in male zebra finches (Taeniopygia guttata) reduce gregariousness (preference for a group of 10 versus 2 conspecific males), but have no effect on the amount of time that subjects spend in close proximity to other birds (“contact time”). The antagonist also produces a profound increase in anxiety-like behavior, as exhibited by an increased latency to feed in a novelty-suppressed feeding test. Bilateral knockdown of VT production in the BSTm using LNA-modified antisense oligonucleotides likewise produces increases in anxiety-like behavior and a potent reduction in gregariousness, relative to subjects receiving scrambled oligonucleotides. The antisense oligonucleotides also produced a modest increase in contact time, irrespective of group size. Together, these combined experiments provide clear evidence that endogenous VT promotes preferences for larger flock sizes, and does so in a manner that is coupled to general anxiolysis. Given that homologous peptide circuitry of the BSTm-LS is found across all tetrapod vertebrate classes, these findings may be predictive for other highly gregarious species.     

Endogenous vasotocin exerts context-dependent behavioral effects in a semi-naturalistic colony environment

Arginine vasotocin (VT), and its mammalian homologue arginine vasopressin (VP), are neuropeptides involved in the regulation of social behaviors and stress responsiveness. Previous research has demonstrated opposing effects of VT/VP on aggression in different species. However, these divergent effects were obtained in different social contexts, leading to the hypothesis that different populations of VT/VP neurons regulate behaviors in a context-dependent manner. We here use VP antagonists to block endogenous VT function in male zebra finches (Taeniopygia guttata) within a semi-natural, mixed-sex colony setting. We examine the role of VT in the regulation of aggression and courtship, and in pair bond formation and maintenance, over the course of three days. Although our results confirm previous findings, in that antagonist treatment reduces aggressive mate competition during an initial behavioral session during which males encounter novel females, we find that the treatment effects are completely reversed within hours of colony establishment, and the antagonist treatment instead facilitates aggression in later sessions. This reversal occurs as aggression shifts from mate competition to nest defense, but is not causally associated with pairing status per se. Instead, we hypothesize that these divergent effects reflect context-specific activation of hypothalamic and amygdalar VT neurons that exert opposing influences on aggression. Across contexts, effects were highly specific to aggression and the antagonist treatment clearly failed to alter latency to pair bond formation, pair bond stability, and courtship. However, VT may still potentially influence these behaviors via promiscuous oxytocin-like receptors, which are widely distributed in the zebra finch brain.     

Effects of central vasotocin and mesotocin manipulations on social behavior in male and female zebra finches

Male and female zebra finches (Taeniopygia guttata; total n = 40) were fitted with chronic guide cannulae directed at the lateral ventricle and were tested for aggression, affiliation, and partner preference following infusions of mesotocin (MT), vasotocin (VT), their antagonists, and vehicle control. Aggressive behavior was tested in a mate competition paradigm and tests of intersexual affiliation and partner preference were conducted following 1 day of cohabitation with an opposite-sex individual. These tests also provided data on male courtship singing. The results demonstrate a modest dose-dependent facilitation of aggression by VT, but not MT, in both male and female finches. However, only males were sensitive to infusions of a vasopressin antagonist, suggesting that endogenous VT is more important for behavioral modulation in males. Peptide effects were specific to aggression, as no treatments influenced intersexual affiliation, partner preference, or male courtship singing. Thus, in contrast to rodents, partner preference is not readily induced by VT or MT in this species. However, the potential necessity of endogenous VT and MT for natural pair-bond formation remains to be tested.     

Intra- and interspecific aggression do not modulate androgen levels in dusky gregories,yet male aggression is reduced by an androgen blocker

Discussions about social behavior are generally limited to fitness effects of interactions occurring between conspecifics. However, many fitness relevant interactions take place between individuals belonging to different species. Our detailed knowledge about the role of hormones in intraspecific interactions provides a starting point to investigate how far interspecific interactions are governed by the same physiological mechanisms. Here, we carried out standardized resident–intruder (sRI) tests in the laboratory to investigate the relationship between androgens and both intra- and interspecific aggression in a year-round territorial coral reef fish, the dusky gregory, Stegastes nigricans. This damselfish species fiercely defend cultivated algal crops, used as a food source, against a broad array of species, mainly food competitors, and thus represent an ideal model system for comparisons of intra-and interspecific territorial aggression. In a first experiment, resident S. nigricans showed elevated territorial aggression against intra- and interspecific intruders, yet neither elicited a significant increase in androgen levels. However, in a second experiment where we treated residents with flutamide, an androgen receptor blocker, males but not females showed decreased aggression, both towards intra- and interspecific intruders. Thus androgens appear to affect aggression in a broader territorial context where species identity of the intruder appears to play no role. This supports the idea that the same hormonal mechanism may be relevant in intra- and interspecific interactions. We further propose that in such a case, where physiological mechanisms of behavioral responses are found to be context dependent, interspecific territorial aggression should be considered a social behavior.     

The couple that sings together stays together: duetting,aggression and extra-pair paternity in a promiscuous bird species

When individuals mate outside the pair bond, males should employ behaviours such as aggression or vocal displays (e.g. duetting) that help assure paternity of the offspring they care for. We tested whether male paternity was associated with aggression or duetting in the red-backed fairy-wren, a species exhibiting high rates of extra-pair paternity. During simulated territorial intrusions, aggression and duetting were variable among and repeatable within males, suggesting behavioural consistency of individuals. Males with quicker and stronger duet responses were cuckolded less often than males with slower and weaker responses. In contrast, physical aggression was not correlated with male paternity. These results suggest that either acoustic mate guarding or male–female vocal negotiations via duetting lead to increased paternity assurance, whereas physical aggression does not.     

Sex Differences in Territorial Behavior Exhibited by the Spotted Hyena (Hyaenidae, Crocuta crocuta)

Spotted hyenas ( Crocuta crocuta ) are gregarious carnivores that defend group territories against encroachment by neighboring conspecifics. Here we monitored the behavior of members of one clan of free-ranging spotted hyenas during border patrols, 'wars' with neighboring clans, and other interactions with alien intruders, to document differences between the sexes in territorial behavior in this species. We also examined the possibility that the probability or rate of attack on alien hyenas encountered within the clan's territory would vary with the sex of the intruders. Initiation and leadership of most cooperative territorial behaviors were by adult female clan members, although border patrols were occasionally conducted by groups composed exclusively of resident males. The vast majority of alien intruders into the territory of the study clan were males. Resident females were more likely to attack intruding females than intruding males, but hourly rates of aggression directed by females towards aliens did not vary with intruder sex. Resident males were more likely than resident females to attack alien males, and resident males directed significantly higher hourly rates of aggression towards intruding males than females. Although female leadership in most cooperative territorial behaviors distinguishes spotted hyenas from many mammalian carnivores, other sex differences in the territorial behavior of spotted hyenas resemble those documented in other gregarious predators. Sex differences observed in hyena territoriality are consistent with the hypothesis that male and female clan members derive different selective benefits from advertisement and defense of group territories.     

Neuropeptide binding reflects convergent and divergent evolution in species-typical group sizes

Neuroendocrine factors that produce species differences in aggregation behavior ("sociality") are largely unknown, although relevant studies should yield important insights into mechanisms of affiliation and social evolution. We here focused on five species in the avian family Estrildidae that differ selectively in their species-typical group sizes (all species are monogamous and occupy similar habitats). These include two highly gregarious species that independently evolved coloniality; two territorial species that independently evolved territoriality; and an intermediate, modestly gregarious species that is a sympatric congener of one of the territorial species. Using males and females of each species, we examined binding sites for (125)I-vasoactive intestinal polypeptide (VIP), (125)I-sauvagine (SG; a ligand for corticotropin releasing factor, CRF, receptors) and a linear (125)I-V(1a) vasopressin antagonist (to localize receptors for vasotocin, VT). VIP, CRF and VT are neuropeptides that influence stress, anxiety and/or various social behaviors. For numerous areas (particularly within the septal complex), binding densities in the territorial species differed significantly from binding in the more gregarious species, and in most of these cases, binding densities for the moderately gregarious species were either comparable to the two colonial species or were intermediate to the territorial and colonial species. Such patterns were observed for (125)I-VIP binding in the medial bed nucleus of the stria terminalis, medial septum, septohippocampal septum, and subpallial zones of the lateral septum; for (125)I-SG binding in the infundibular hypothalamus, and lateral and medial divisions of the ventromedial hypothalamus; and for the linear (125)I-V(1a) antagonist in the medial septum, and the pallial and subpallial zones of the caudal lateral septum. With the exception of (125)I-SG binding in the infundibular hypothalamus, binding densitites are positively related to sociality.     

VPAC receptor signaling modulates grouping behavior and social responses to contextual novelty in a gregarious finch: A role for a putative prefrontal cortex homologue

In both mammals and birds, vasoactive intestinal polypeptide (VIP) neurons and fibers are present in virtually every brain area that is important for social behavior. VIP influences aggression in birds, social recognition in rodents, and prolactin secretion in both taxa, but other possible functions in social modulation remain little explored. VIP effects are mediated by VPAC receptors, which bind both VIP and pituitary adenylate cyclase activating peptide. Within the lateral septum and medial bed nucleus of the stria terminalis, VPAC receptors are found at higher densities in gregarious finch species relative to territorial species, suggesting that VPAC receptor activation promotes social contact and/or preference for larger groups. Here we here test this hypothesis in zebra finches (Taeniopygia guttata), and also examine the relevance of VPAC receptors to anxiety-like processes. Intraventricular infusions of the VPAC receptor antagonist, neurotensin6–11 mouseVIP7–28, strongly reduce social contact when animals are tested in a novel environment, and exert sex-specific effects on grouping behavior. Specifically, VPAC receptor antagonism reduces gregariousness in females but increases gregariousness in males. Interestingly, VPAC antagonism in the medial pallium (putative prefrontal cortex homologue) significantly reduces gregariousness in both sexes, suggesting site-specific effects of VIP signaling. However, VPAC antagonism does not modulate novel-familiar social preferences in a familiar environment or general anxiety-like behaviors. The current results suggest that endogenous activation of VPAC receptors promotes social contact under novel environmental conditions, a function that may be accentuated in gregarious species. Moreover, endogenous VIP modulates gregariousness in both males and females.     

Androgen response to social competition in a shoaling fish

Androgens respond to social challenges and this response has been interpreted as a way for males to adjust androgen-dependent behavior to social context. However, the androgen responsiveness to social challenges varies across species and a conceptual framework has been developed to explain this variation according to differences in the mating system and parental care type, which determines the regimen of challenges males are exposed to, and concomitantly the scope (defined as the difference between the physiological maximum and the baseline levels) of response to a social challenge. However, this framework has been focused on territorial species and no clear predictions have been made to gregarious species (e.g. shoaling fish), which although tolerating same-sex individuals may also exhibit intra-sexual competition. In this paper we extend the scope of this conceptual framework to shoaling fish by studying the endocrine response of zebrafish (Danio rerio) to social challenges. Male zebrafish exposed to real opponent agonistic interactions exhibited an increase in androgen levels (11-ketotestosterone both in Winners and Losers and testosterone in Losers). This response was absent in Mirror-fighters, that expressed similar levels of aggressive behavior to those of winners, suggesting that this response is not a mere reflex of heightened aggressive motivation. Cortisol levels were also measured and indicated an activation of the hypothalamic–pituitary–interrenal axis in Winners of real opponent fighters, but not Losers or in Mirror-fighters. These results confirm that gregarious species also exhibit an endocrine response to an acute social challenge.     

Resource defense and juvenile hormone: the "challenge hypothesis" extended to insects

As predicted for vertebrates by the challenge hypothesis, the endocrine system of invertebrates can respond to social stimuli to modulate aggression. Testosterone (T) is generally considered to moderate aggression associated with reproduction, i.e. the establishment of breeding territories, mate guarding and offspring defense; juvenile hormone (JH) serves an analogous function in burying beetles. Hemolymph titers of JH increase significantly in Nicrophorus orbicollis, a species with facultative biparental care, when challenged by an intruder to defend their resource. During the first 12 h after the discovery of a carcass, the necessary breeding resource, competition is intrasexual, and JH of males responds only to a challenge by males, and JH of females responds only to a challenge by female intruders. After this period, competition is intersexual, and JH increases significantly in both males and females challenged by an intruder of either sex. In contrast, JH titers in a nonparental species are much higher throughout the breeding season, and neither males nor females respond hormonally to an intruder. These findings support the challenge hypothesis and suggest that mating systems and breeding strategies can promote plastic responses in insect, as well as vertebrate, endocrine systems.     

A Comparative Study of Sex Ratio and Clutch Size in Gregarious Ichneumonoid Wasps

Some convincing support for sex ratio theory comes from the cross-species relationship between sex ratio and brood size in gregarious bethylid wasps (Hymenoptera: Bethylidae), in which the proportion males declines as brood size increases as predicted under local mate competition. It is unknown how widely such relationships hold within parasitoid wasps as a whole. We assemble a dataset on sex ratio and brood size for gregarious Braconidae and Ichneumonidae. Their sex ratios deviate substantially from those of bethylids; sex ratios differ widely across species; and they are not significantly related to brood size across species. Several factors explain the heterogeneity in sex ratios including across-species differences in mating system, sex determining mechanism, and sexual asymmetries in larval competition and polyembryony leading to single-sexed broods.     

Sex-specific territorial responses in Tawny Owls Strix aluco

A territorial intruder often poses more of a threat to the territory holder of the same sex as itself. As territorial aggression is associated with costs, aggression shown by birds towards territorial intruders of the opposite sex deserves investigation. This behaviour could arise due to the reproductive value of a mate or through mutualism between members of a pair. We investigated these hypotheses by presenting mated pairs of Tawny Owls Strix aluco with playback of male calls, female calls and a male and female duetting, and recording the number and intensity of responses by the male and female territory holders. Females responded significantly more often to female than to male calls. Males responded equally often to male and female playback. Males which had previously bred successfully with their mate were significantly more likely to respond to female playback in the spring, which suggested males were responding to female playback due to the reproductive value of their mate. There was no evidence of mutualism between members of a pair.     

Aggressive encounters differentially affect serum dehydroepiandrosterone and testosterone concentrations in male Siberian hamsters (Phodopus sungorus)

The gonadal hormone testosterone (T) regulates aggression across a wide range of vertebrate species. Recent evidence suggests that the adrenal prohormone dehydroepiandrosterone (DHEA) may also play an important role in regulating aggression. DHEA can be converted into active sex steroids, such as T and estradiol (E₂), within the brain. Previous studies show that circulating DHEA levels display diurnal rhythms and that melatonin increases adrenal DHEA secretion in vitro. Here we examined serum DHEA and T levels in long-day housed Siberian hamsters (Phodopus sungorus), a nocturnal species in which melatonin treatment increases aggression. In Experiment 1, serum DHEA and T levels were measured in adult male hamsters during the day (1200 h, noon) and night (2400 h, midnight). In Experiment 2, aggression was elicited using 5-min resident–intruder trials during the day (1800 h) and night (2000 h) (lights-off at 2000 h). Serum DHEA and T levels were measured 24 h before and immediately after aggressive encounters. In Experiment 1, there was no significant difference in serum DHEA or T levels between noon and midnight, although DHEA levels showed a trend to be lower at midnight. In Experiment 2, territorial aggression was greater during the night than the day. Moreover, at night, aggressive interactions rapidly decreased serum DHEA levels but increased serum T levels. In contrast, aggressive interactions during the day did not affect serum DHEA or T levels. These data suggest that nocturnal aggressive encounters rapidly increase conversion of DHEA to T and that melatonin may play a permissive role in this process.     

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

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

Divergent hormonal responses to social competition in closely related species of haplochromine cichlid fish

The diverse cichlid species flocks of the East African lakes provide a classical example of adaptive radiation. Territorial aggression is thought to influence the evolution of phenotypic diversity in this system. Most vertebrates mount hormonal (androgen, glucocorticoid) responses to a territorial challenge. These hormones, in turn, influence behavior and multiple aspects of physiology and morphology. Examining variation in competition-induced hormone secretion patterns is thus fundamental to an understanding of the mechanisms of phenotypic diversification. We test here the hypothesis that diversification in male aggression has been accompanied by differentiation in steroid hormone levels. We studied two pairs of sibling species from Lake Victoria belonging to the genera Pundamilia and Mbipia. The two genera are ecologically differentiated, while sibling species pairs differ mainly in male color patterns. We found that aggression directed toward conspecific males varied between species and across genera: Pundamilia nyererei males were more aggressive than Pundamilia pundamilia males, and Mbipia mbipi males were more aggressive than Mbipia lutea males. Males of both genera exhibited comparable attack rates during acute exposure to a novel conspecific intruder, while Mbipia males were more aggressive than Pundamilia males during continuous exposure to a conspecific rival, consistent with the genus difference in feeding ecology. Variation in aggressiveness between genera, but not between sibling species, was reflected in androgen levels. We further found that M. mbipi displayed lower levels of cortisol than M. lutea. Our results suggest that concerted divergence in hormones and behavior might play an important role in the rapid speciation of cichlid fishes.     

Extra-pair copulations,intra-specific brood parasitism,and quasi-parasitism in birds: a theoretical approach

Although 90 % of all bird species are monogamous, many species practice alternative reproductive strategies as extra-pair copulations, intra-specific brood parasitism, and quasi-parasitism. In territorial monogamous species, both partners hold and defend the territory from intruders. Often, the intruders are males and usually the local male banishes the intruders. Indeed, many studies focused on the response of the local male toward intruder males. However, the benefits and costs associated with the responses of the local male toward intruder females have been largely overlooked. Focusing mainly on alternative reproductive strategies, we developed a model to predict the aggression a monogamous male may demonstrate toward an intruder female during the pre-egg laying stage of his local female partner. This model demonstrates that the intensity of aggression that the local male shows toward an intruder female depends on the extra-pair copulations that his local female partner may perform. Further, the aggression also depends upon intra-specific brood parasitism and quasi-parasitism that might be carried out by the intruder female. Our approach suggests that when considering mating strategies, there is a need to assess how these three alternative reproductive strategies may affect the local male's aggression toward intruder females.     

How does a parent respond when its mate emphasizes the wrong role? A test using a monogamous fish

The convict cichlid fish, Archocentrus nigrofasciatus, is biparental: the male spends the majority of his time defending the territory and the female spends much of her time close to the offspring. Under natural conditions, this separation into sex-typical roles is somewhat blurred as males do spend some time with the offspring and females do attack intruders. Here we tested whether an individual selects a parental role based on the location (i.e. parental role) of its mate. For example, do females emphasize offspring care because the male is away from the offspring? Will males be more likely to care for the offspring when the female is away from the offspring? We manipulated the location of one parent by placing it in a transparent plastic box, either near the offspring or at the far end of the tank near a clear plastic compartment that held a conspecific male intruder. We tested both male and female parent under the following four conditions: boxed mate near offspring with no intruder present, boxed mate near offspring with intruder present, boxed mate near intruder compartment with no intruder present, and boxed mate near intruder compartment with intruder present. We found that both parents spent more time with the offspring and less time attacking the intruder when the mate was positioned near the offspring and more time away from the offspring and more time attacking the intruder when the mate was near the intruder. Males were more affected by the location of their mates than were females and we concluded that males were attracted both to their mates' location and their offspring while females were mostly attracted to their offspring. Overall, the location of the mate had little effect on the types of aggressive activities used against the intruder. We did find that males increased their aggression towards boxed females when they were positioned far from the offspring, whereas the aggressive behaviour of females towards boxed males when they were positioned near the offspring was ambiguous. We suggest that males in particular enforce the separation of sex-specific parental roles via this aggression.     

Cross-fostering Does Not Influence the Mate Preferences and Territorial Behaviour of Males in Lake Victoria Cichlids

The ability to recognise conspecifics in contexts of mate choice and territorial defence may have large effects on an individual's fitness. Understanding the development of assortative behaviour may shed light on how species assortative behaviour evolves and how it may influence reproductive isolation. This is the case not only for female mate preferences, but also for male mate preferences and male territorial behaviour. Here we test with a cross-fostering experiment whether early learning influences male mate preferences and male–male aggression biases in two closely related, sympatrically occurring cichlid species Pundamilia pundamilia and Pundamilia nyererei from Lake Victoria. Males that had been fostered, either by a conspecific female or by a heterospecific female, were tested for their aggression bias, as well as for their mate preferences, in two-way choice tests. Males cross-fostered with conspecific and heterospecific foster mothers selectively directed their aggression towards conspecific intruders. The cross-fostering treatment also did not affect male mate preferences. These results are in striking contrast with the finding that females of these species show a sexual preference for males of the foster species.     

Male-male competition and speciation: aggression bias towards differently coloured rivals varies between stages of speciation in a Lake Victoria cichlid species complex

Sympatric speciation driven by sexual selection by female mate choice on a male trait is a much debated topic. The process is problematic because of the lack of negative frequency-dependent selection that can facilitate the invasion of a novel colour phenotype and stabilize trait polymorphism. It has recently been proposed that male-male competition for mating territories can generate frequency-dependent selection on male colouration. Rare male cichlid fish would enjoy a fitness advantage if territorial defenders bias aggression towards male cichlid fish of their own colour. We used blue (ancestral type) and red phenotypes of the Lake Victoria cichlid species complex Pundamilia. We tested the aggression bias of wild-caught territorial blue male cichlid fish from five separate populations for blue vs. red rival male cichlid fish using simulated intruder choice tests. The different populations vary in the frequency of red male cichlid fish, and in the degree of reproductive isolation between red and blue, reflecting different stages of speciation. Blue male cichlid fish from a population that lack red phenotypes biased aggression towards blue stimulus male cichlid fish. The same was found in two populations where blue and red are reproductively isolated sister species. This aggression bias may facilitate the invasion of a novel colour phenotype and species coexistence. Blue male cichlid fish from two populations where red and blue are hybridizing incipient species biased aggression towards red stimulus male cichlid fish. Thus, after a successful invasion of red, aggression bias alone is not likely to generate frequency dependence required to stabilize the coexistence of phenotypes. The findings show that aggression bias varies between stages of speciation, but is not enough to stabilize the process of speciation.     

Influence of Adult Size on Mate Choice in the Solitary and Gregarious Parasitoids, Cotesia marginiventris and Cotesia flavipes

Female and male mate choice in relation to adult size were examined for the solitary and gregarious parasitoids, Cotesia marginiventris (Cresson) and Cotesia flavipes Cameron, respectively. In addition, male precopulatory behaviors were observed for evidence of male competition or a large-male advantage in mate acquisition. Male parasitoids are not known to offer female mates direct benefits, but females that mate high quality males may obtain indirect benefits, such as offspring that are more successful in obtaining mates. Female choice experiments for C. marginiventris found that large males approached females first more frequently than small males, and that females mated large males significantly more often than small males. Male choice experiments for C. marginiventris did not demonstrate a male preference for female size. In contrast, female choice experiments with C. flavipes found that females mated equally with large or small males, while male choice experiments showed that males attempted copulation and mated more frequently with smaller females. Male competition was not observed in the gregarious species C. flavipes, but competition in this gregarious parasitoid could be moderated by dispersal.