Non-territorial Males Research Articles

Subordinate male cichlids retain reproductive competence during social suppression

Subordinate males, which are excluded from reproduction often save energy by reducing their investment in sperm production. However, if their position in a dominance hierarchy changes suddenly they should also rapidly attain fertilization capability. Here, we asked how social suppression and ascension to dominance influences sperm quality, spermatogenesis and reproductive competence in the cichlid Astatotilapia burtoni, where reproduction is tightly coupled to social status. Dominant territorial (T) males are reproductively active while subordinate non-territorial (NT) males are suppressed, but given the opportunity, NT males will perform dominance behaviours within minutes and attain T male testes size within days. Using the thymidine analogue 5-bromo-2-deoxyuridine (BrdU) to label germ cell proliferation, we found that the spermatogenic cycle takes approximately 11-12 days, and social status had no effect on proliferation, suggesting that spermatogenesis continues during reproductive suppression. Although sperm velocity did not differ among social states, NT males had reduced sperm motility. Remarkably, males ascending in status showed sperm motility equivalent to T males within 24 h. Males also successfully reproduced within hours of social opportunity, despite four to five weeks of suppression and reduced testis size. Our data suggest that NT males maintain reproductive potential during suppression possibly as a strategy to rapidly improve reproductive fitness upon social opportunity.

Strong male/male competition allows for nonchoosy females: high levels of polygynandry in a territorial frog with paternal care

Our knowledge about genetic mating systems and the underlying causes for and consequences of variation in reproductive success has substantially improved in recent years. When linked to longitudinal population studies, cross-generational pedigrees across wild populations can help answer a wide suite of questions in ecology and evolutionary biology. We used microsatellite markers and exhaustive sampling of two successive adult generations to obtain population-wide estimates of individual reproductive output of males and females in a natural population of the Neotropical frog Allobates femoralis (Aromobatidae), a pan-Amazonian species that features prolonged iteroparous breeding, male territoriality and male parental care. Parentage analysis revealed a polygynandrous mating system in which high proportions of males (35.5%) and females (56.0%) produced progeny that survived until adulthood. Despite contrasting reproductive strategies, successfully reproducing males and females had similar numbers of mating partners that sired the adult progeny (both sexes: median 2; range 1-6); the numbers of their offspring that reached adulthood were also similar (both sexes: median 2; range 1-8). Measures of reproductive skew indicate selection on males only for their opportunity to breed. Reproductive success was significantly higher in territorial than in nonterritorial males, but unrelated to territory size in males or to body size in both sexes. We hypothesize that female polyandry in this species has evolved because of enhanced offspring survival when paternal care is allocated to multiple partners.

Histomorphology of preorbital gland in territorial and non-territorial male blackbuck Antelope cervicapra, a critically endangered species

The preorbital gland is a specialized dermal gland of antelopes which plays an important role in territorial marking behavior and pheromonal communication. To our knowledge, there is little information available on the role of preorbital gland marks in Indian antelopes (blackbucks). Males are seen averting the gland during behavioural display and territorial marking but the functional aspect of this gland has not been examined. Hence, the aim of this study was to describe the histomorphology of the preorbital gland in territorial and non-territorial male blackbucks to determine its morphology and secretory function. The results showed that the preorbital gland is composed of modified sebaceous and apocrine glands. The apocrine gland is lined by simple cuboidal epithelial cells; the serous parts of the secretory products are often seen in the apical portions of the cells. The myoepithelial cells contain actin filaments lying on the basal membranes of the apocrine gland. There are some considerable histological changes in the presence of the sebaceous and apocrine glands in territorial males in comparison to non-territorial males. The following histological changes associated with occurrence of the sebaceous and apocrine glands have been observed in territorial and non-territorial male blackbucks: (1) increase of size of sebaceous and apocrine glands and (2) increase in density of sebaceous and apocrine glands in territorial males compared to non-territorial males. It is suggested that the higher development (i.e., size) and density of sebaceous and apocrine glands in territorial males could depend on hormone production (i.e., testosterone). Based on the histological observation and the role of sebaceous and apocrine glands in the preorbital gland supported by literature, it is possible to conclude that both territorial and non-territorial blackbuck males may produce pheromonal substances through preorbital gland (secretion) for olfactory communication.

Social organization in the Chinese water deer, Hydropotes inermis

The social organization of Chinese water deer was studied in a zoological park. Most adults lived together in the mixed zone, although other habitats were available. The overlap between individual areas was largest in females. In the mating season alone, less than half of the males established territories which overlapped in small spots where most encounters occurred. Females travelled freely throughout the entire available area, but non-territorial males stayed between the territories. Except in males during mating season, very few physical contacts other than sniffing took place between individuals regardless of age, sex or status. Each animal lived alone and did not show attraction or aggressiveness towards congeners. Grouping was temporary with no durable link between individuals, not even between mothers and daughters older than 5 months. The solitary life of individuals on a common ground and the establishment of seasonal territories make the water deer unique among ruminants. The species appears to be no more social than the water chevrotain, an “ancient” species. This fits well with other characteristics of the species.

Do Antlers Honestly Advertise the Phenotypic Quality of Fallow Buck (Dama dama) in a Lekking Population?

Size and symmetry of secondary sexual traits are supposed to be honest signals of male phenotypic quality in vertebrates. Antler size and symmetry, male quality and mating success have not been fully demonstrated to be correlated in cervids. Such correlations can be particularly intriguing in the case of species adopting costly mating strategies, which imply territorial defence without feeding. In these cases, body condition appears to be crucial at the onset of the rut, and large and symmetrical antlers may be borne by successful males. For these reasons, during four consecutive years, we analysed growth rate, size and symmetry of 26 fallow bucks’ antlers in relation to individual mating strategy and success in a lekking population. Territorial (T) males, which gained higher mating success in the lek, showed a faster antler growth (about 10 g/d per antler) than non-territorial (NT) males (3.6–5.2 g/d per antler) during the velvet period, and this was likely because of optimized foraging strategies. At the onset of the rut, when antler growth was completed, T males had larger antlers than NT males. Possibly because of worsened body conditions, NT males showed a pronounced antler directional asymmetry, while T males did not. However, no direct link between antler symmetry and mating success was found, thus confirming the ambiguous role of antler asymmetry as an indicator of fitness. The faster the antler growth, the larger its final size and the higher its beholder’s mating success. Our results confirmed that, like groaning and scent marking, antler size reflects social status and dominance in male fallow deer, and therefore represents an honest advertisement of phenotypic quality.

Relationships between circulating androgens, aggressive behaviour and breeding tubercles in males of the common bream Abramis brama L. in an aquarium environment

In this study, relationships between circulating androgens, aggressive behaviour and breeding tubercles in males of common bream Abramis brama were examined in an aquarium environment. The breeding tubercles of fish were counted, the number of attacks was quantified by male status and circulating rates of testosterone and 11-ketotestosterone from blood plasma were analysed using radioimmunoassay procedures. The results revealed that no significant differences were found between circulating testosterone and 11-ketotestosterone in territorial and nonterritorial males. Furthermore, no significant correlations were found between circulating androgens, androgens and aggression, androgens and tubercles and breeding tubercles and aggression in common bream by male status. However, territorial fish displayed a significantly higher level of aggressive behaviour and breeding tubercles than nonterritorial fish. In natural environments, the occurrence of breeding tubercles during the spawning season could contribute to identifying the behavioural status of common bream males.

Predation selects for increased immune function in male damselflies, Calopteryx splendens.

Predation selects for numerous traits in many animal species, with sick or parasitized prey often being at high risk. When challenged by parasites and pathogens, prey with poor immune functions are thus likely to be at a selective disadvantage. We tested the hypothesis that predation by birds selects for increased immune function in a wild population of male damselflies Calopteryx splendens, while controlling for a trait known to be under selection by bird predation, dark wing-spots. We found that selection on both immune function and wing-spot size was significantly positive, and that selection on either trait was independent of selection on the other. We found no evidence of nonlinear quadratic or correlational selection. In contrast to previous studies, we found no phenotypic correlation between immune function and wing-spot size. There was also no difference in immune response between territorial and non-territorial males. Our study suggests that predation may be an important agent of selection on the immune systems of prey, and because the selection we detected was directional, has the potential to cause phenotypic change in populations.

Coloration indicates body size inCalopteryx maculata(Odonata: Calopterygidae)

Abstract Calopteryx maculata has become a model system for studying behaviour and reproduction in odonates. Its iridescent coloration is thought to be important in intraspecific interactions but no study has yet measured coloration in a quantitative manner. In a recent study, Fitzstephens & Getty (2000. Animal Behaviour 60: 851-855) showed that lipld levels predict coloration as determined by Munsell chips, such that fat males were blue and lean males were green. In this study we quantified color in C. maculata with a spectrometer to test the prediction of Fitzstephens & Getty (2000) using quantitative measures. We found that body size, but not lipid levels, correlates with color. In our study, larger males were green and smaller males blue. Territorial males did not differ from non-territorial males in color, size, or lipid levels. Coloration thus predicts size in male C. maculata, but the significance of this in intraspecific interactions remains unclear.

Social status regulates kisspeptin receptor mRNA in the brain of Astatotilapia burtoni

The brain controls reproduction in response to relevant external and internal cues. Central to this process in vertebrates is gonadotropin-releasing hormone (GnRH1) produced in neurons of the hypothalamic-preoptic area (POA). GnRH1 released from the POA stimulates pituitary release of gonadotropins, which in males causes sperm production and concomitant steroid hormone release from the testes. Kisspeptin, a neuropeptide acting via the kisspeptin receptor (Kiss1r), increases GnRH1 release and is linked to development of the reproductive system in mammals and other vertebrates. In both fish and mammals, kiss1r mRNA levels increase in the brain around the time of puberty but the environmental and other stimuli regulating kisspeptin signaling to GnRH1 neurons remain unknown. To understand where kiss1r is expressed and how it is regulated in the brain of a cichlid fish, Astatotilapia burtoni, we measured expression of a kiss1r homolog mRNA by in situ hybridization and quantitative reverse transcription-PCR (qRT-PCR). We found kiss1r mRNA localized in the olfactory bulb, specific nuclei in the telencephalon, diencephalon, mesencephalon, and rhombencephalon, as well as in GnRH1 and GnRH3 neurons. Since males’ sexual physiology and behavior depend on social status in A. burtoni, we also tested how status influenced kiss1r mRNA levels. We found higher kiss1r mRNA levels in whole brains of high status territorial males and lower levels in low status non-territorial males. Our results are consistent with the hypothesis that Kiss1r regulates many functions in the brain, making it a strong candidate for mediating differences in reproductive physiology between territorial and non-territorial phenotypes.

Diurnal variation in preorbital gland scent marking behaviour of captive male Indian Blackbuck (Antelope cervicapra L.) and its territorial significance

Scent marking is a common behaviour among mammals, which involves the deposition of a pheromone, intended to elicit a response from conspecifics. The present study is aimed to establish the diurnal profile of the distribution of scent marking behaviour and its influence of the marker. The frequency of preorbital gland scent marking behaviour was observed in territorial and non-territorial male Indian blackbucks on 72 days, over a period of 18 weeks, starting data collection at 06.00 and continuing until the end of the photophase at about 16.00. An ANOVA with post hoc (DMRT) test was assessed to compare the frequency of preorbital gland scent marking at six 2-hour intervals using pooled data for territorial and non-territorial males. The result showed that the preorbital gland scent marking behaviour occurred significantly (P < 0.001) more often between 10:00–12:00 hrs and 16:00–18:00 hrs. It suggests that scent-marking behaviour in Indian blackbuck has a preferential incidence at a particular time, and this might have occurred in association with feeding hours. Moreover, an ANOVA with a post hoc comparison (DMRT) test revealed that the frequency of scent marking is significant (P < 0.001) when territorial males are compared to non-territorial males. We conclude that territorial male preorbital gland scent marking has the following proposed functions: (i) marking related to use for defense of the home range or territorial region may serve as a permanent threat signal and (ii) marking related to suppressing daily activities in non-territorial males (i.e. feeding, aggression, mating, scent marking, and territorial patrolling activities etc.), and involves maintenance of hierarchy and the avoidance of physical combat.

Social factors of group spawning as an alternative mating tactic in the territorial males of the threespot wrasse Halichoeres trimaculatus

In most labrid fishes, large males with bright terminal phase (TP) coloration normally defend mating territories and pair spawn after following (i.e., courting) solitary females. It has also been reported that the TP males may abandon their territories and participate in group spawning when mating groups of small non-territorial males with drab initial phase (IP) coloration frequently intrude into the territories of TP males. In the similar situation of the present study, however, the territorial TP males of the threespot wrasse, Halichoeres trimaculatus, did not always participate in group spawning but continued pair spawning. Only the TP males that had few opportunities to encounter solitary IP individuals participated in group spawning, frequently following the mating groups of IP individuals. It is therefore suggested that group spawning of the territorial TP males is regarded as a tactic of making the best of the bad situation by the TP males with few opportunities to pair spawn in an area where group spawning dominates.

Experimental demonstration of alternative mating tactics of male Ptilothrix fructifera (Hymenoptera, Apidae)

Ptilothrix fructifera is a solitary, oligolectic bee dependent on the flowers of Opuntia (Cactaceae). We conducted field studies to identify the mating tactics used by P. fructifera males and to determine whether factors such as male body size and available resource flowers contribute to variation in male mating tactic. Males in a population in southern Brazil showed pronounced variation in body size, but no distinct size classes. Larger males aggressively defended territories of flowering Opuntia plants, the sole pollen source for the females. Smaller males nonaggressively patrolled nonflowering shrubs growing between the nest aggregation and patches of Opuntia . Only unmated females were attractive to males. When offered to males in patrolled shrubs, up to eight males attempted to mate with the same female, but in territories only the territory owner mated with the introduced female. About 10 min after mating, females were unattractive to males. These results identify the species as monogamous and indicate that territoriality is an adaptive mating tactic. Experimental addition of Opuntia flowers to patrolled shrubs showed that nonterritorial males can switch to territorial behaviour. Thus, the number of available flowers together with the number of competitor males determines the ratio of territorial males to patrolling males at a given site. The experiment shows that male P. fructifera show a conditional reproductive strategy in which males adopt alternative tactics according to their size.

Immune system activation interacts with territory-holding potential and increases predation of the damselfly Calopteryx splendens by birds

Activation of the immune system in insects has been shown to be costly in the laboratory setting, but experimental studies in the field are lacking. The costs of immunity in the wild may be different to those in the laboratory because animals in the wild are simultaneously subjected to a suite of selective agents. We have measured the costs of immune system activation in a wild population of the territorial damselfly Calopteryx splendens. Immune-challenged males were found to be less likely to be territorial and had lower overall survival rates than control or sham-manipulated males. Because territorial males have a higher mating success than nonterritorial males, this result suggests that immune-challenged males are also likely to suffer reduced mating success. However, the activation of the immune system as such did not increase predation risk; this occurred due to a combination of the former with a reduced territory-holding potential. As such, immune-challenged males not holding a territory were most susceptible to predation by birds. The size of the wing spots, a known sexually selected male trait, predicted territorial behaviour in control and sham-manipulated males, but not in immune-challenged males. Our data show that immune system activation can have several costs acting in unison and that ubiquitous ecological interactions, such as predation, may affect trade-offs between immunity and other life history traits.

Body temperature and body size affect flight performance in a damselfly

Flight performance is undoubtedly an important factor for behavioral success in flying insects. Though it is well-known that the flight performance is influenced by body temperature and body size, the relative importance of these factors is not well-understood. We performed laboratory experiments using the male-polymorphic damselfly Mnais costalis with larger territorial males and smaller non-territorial males in a population. We analyzed the effects of body temperature and body size, measured as the thoracic temperature and left hind-wing length, respectively, on two indices of flight performance: maximum lifting force and size-corrected lifting force. The latter is an index of acceleration that is related to aerial agility. The results showed that higher body temperature produced both larger maximum lifting force and larger size-corrected lifting force. In contrast, while larger size produced a larger maximum lifting force, it produced a lower size-corrected lifting force. The results of field measurements showed that territorial males had variable thoracic temperatures depending on the insolation in their territories. In contrast, non-territorial males had less variable and generally higher thoracic temperatures than territorial males as they are mostly found in sunny spots. Until now, the influence of body temperature on behavioral performance has remained unclear although considerable studies have suggested such influence. We showed, here, for the first time, combined effects of body size and body temperature on flight performance. We also showed that body temperature was influenced by the mating strategies of a damselfly. These findings provide new insights into the cost and benefits of territorial behavior in ectothermic animals.

Do territorial male three-spined sticklebacks have sperm with different characteristics than nonterritorial males?

The three-spined stickleback ( Gasterosteus aculeatus aculeatus L., 1758) shows unequal energetic expenditure upon reproduction as some males defend territories and build nest (territorials: TM) where they spawn singly with females, whereas other males remain nonterritorial (NTM), do not build nests, and resort to sneaking fertilizations from nesting males. We examined the effects of reproductive strategy on various sperm parameters. Territorial status was assessed by introducing males in small wading pools and recording the number of males with a nest. Males from all pools were remixed and nesting status was reassessed. This allowed us to discriminate a group of males with repetitive territorial or nonterritorial behaviours (TM and NTM) or a “facultative” territorial behaviour (FM). TM had a significantly larger gonadosomatic index (GSI) than both FM and NTM. FM had a GSI that was significantly larger than NTM, but significantly smaller than TM. Sperm motility did not differ among males with different reproductive tactics. There were no significant differences in citrate synthase (CS) and pyruvate kinase (PK) activities among males with different status. Curiously, we found a significant negative relationship between CS and PK activities and total number of sperm.

Influence of alternative mating tactics on predation risk in the damselfly Calopteryx virgo

Alternative mating tactics are a widespread feature in insects. A typical form of alternative mating behaviour is being a sneaker in the vicinity of a territorial male. Such nonterritorial males have lower mating success, but they may benefit from lower energetic costs and decreased predation risk. In this study, we examined whether nonterritorial male damselflies Calopteryx virgo (L., 1758) are subject to lower predation risk than territorial males. To distinguish predation from other sources of mortality, we used models. The experiment consisted of dried male damselflies settled into the typical perching positions of territorial and nonterritorial males. Also the spatiotemporal patterns of predation risk were studied. The survival of nonterritorial male models was consistently higher than that of territorial male models, which can be attributed to different predation risk. Survival of the models was lower in the presence of avian predators and in large populations. Survival rates were affected by habitat type but did not change during the season. We conclude that nonterritorial male damselflies are less vulnerable to predation and that there may be a trade-off which could potentially make the fitness of sneakers equal to that of territorial males.

Copulation Duration in Nonterritorial Odonate Species Lasts Longer Than in Territorial Species

AbstractWe tested whether long copulation duration is more likely to have evolved in nonterritorial odonate species than in territorial species, given that nonterritorial males do not incur the costs of territory defense. A phylogenetic comparative method that controls for the phylogenetic nonindependence of species was used to compare copulation duration among 46 species of the two main odonate suborders (Anisoptera and Zygoptera). Copulation duration of nonterritorial anisopteran species was longer than for territorial dragonflies; however, this relationship was not found for Zygoptera. Long copulations in Anisoptera may be related to a male's ability to manipulate a female's stored sperm. It is suggested that constraints that prevent a territorial male from lengthening copulation do not seem to operate in Zygoptera. Other selective processes (i.e., cryptic female choice and/or sexual conflict) may also be important determinants of copulation duration in the Zygoptera. To our knowledge, this is the first exploration of the relation copulation duration and mating systems in insects.

Visual mate detection and mate flight pursuit in relation to sunspot size in a woodland territorial butterfly

Territory residency is associated with considerable benefits. In the speckled wood butterfly, Pararge aegeria , males fight over ownership of large sunspots in open forest habitats ; winners become sunspot residents, and losers become nonterritorial and sit and wait for females in small sunspots. A previous study has shown that residents have higher mating success than nonterritorial males, although females are not more attracted to territorial males or sunspot territories per se. Here we tested the hypotheses (1) that the higher success of resident males is caused by visual mate detection being more efficient in a large than in a small sunspot, and (2) that only sunspots above a certain size are defended as territories. Field assessment of territorial sunspot size showed that defended sunspots were significantly larger than ‘average sunspots’ on the forest floor. Experimental tests of male ability to detect visually a model butterfly passing through a sunspot showed that males were more successful in pursuing and intercepting a passing model when flown a longer distance in the sunspot. Hence, we conclude that light conditions and associated visual mate detection and ability to complete mate flight pursuit can explain why P. aegeria males defend territories in large sunspots in forest habitats.

Dorsal cortex volume in male side-blotched lizards, Uta stansburiana, is associated with different space use strategies

Spatial abilities have been associated with many ecologically-relevant behaviors such as territoriality, mate choice, navigation and acquisition of food resources. Differential demands on spatial abilities in birds and mammals have been shown to affect the hippocampus, the region of the brain responsible for spatial processing. In some bird and mammal species, higher demands on spatial abilities are associated with larger hippocampal volumes. The medial and dorsal cortices are the putative reptilian homologues of the mammalian hippocampus, yet few studies have examined the relationship between these brain areas and differential spatial use strategies in reptiles. Further, many studies in birds and mammals compare hippocampal attributes between species that utilize space differently, potentially confounding species-specific effects with effects due to differential behaviors in spatial use. Here, we investigated the relationship between spatial use strategies and medial and dorsal cortical volumes in males of the side-blotched lizard (Uta stansburiana). In this species, males occur in three different morphs, each morph using different spatial niches: large territory holders, small territory holders and non-territory holders with home ranges smaller than the territories of small territory holders. We found that large territory holders had larger dorsal cortical volumes relative to the remainder of the telencephalon compared with non-territorial males, and small territory holders were intermediate. These results suggest that some aspect of holding a large territory may place demands on spatial abilities, which is reflected in a brain region thought partially responsible for spatial processing.

Seasonal variation in genital and body size, sperm displacement ability, female mating rate, and male harassment in two calopterygid damselflies (Odonata: Calopterygidae)

Sperm competition is a pervasive force. One adaptation is the male ability to displace the rivals' sperm that females have stored from previous copulations. In the damselfly, Calopteryx haemorrhoidalis asturica, males with wider aedeagi displace more spermathecal sperm. The present study documents that the same mechanism operates in another damselfly, Hetaerina americana. However, this genital width in both species decreases along the season, but late-emerging females have more sperm displaced than early-emerging females. Because territorial males mated more and were larger in body and genital size than nonterritorial males, late-season females mated with considerably larger males with respect to female size and this produced higher sperm displacement. Assuming female benefits from storing sperm but that such benefit does not prevail if males displace sperm, it is predicted that, along the season, females will mate less and male harassment (in terms of male mating attempts and oviposition duration) will increase. These predictions were corroborated. In H. americana, it was also tested whether spermathecal sperm became less viable along the season. The results obtained did not corroborate this. This is the first evidence indicating that season affects sperm displacement ability and female mating frequency due to changes in male body and genital size. © 2009 The Linnean Society of London, Biological Journal of the Linnean Society, 2009, 96, 815–829.