Effect of larval food stress on male adult behaviour, morphology and reproductive investment in the butterfly Pararge aegeria

Males of several animals increase their reproductive success by territorial behaviour. In butterflies, males may defend a territory (i.e., territorial perching tactic), but this is assumed to be an energetically costly way to locate mates. Limitations of the energy budget may affect fight performance, and may, consequently, force males to adopt an alternative non-territorial searching behaviour (i.e., patrolling tactic) to maximize reproductive success. In this study, we tested to what extent behavioural tactics adopted by adult males of the butterfly Pararge aegeria (L.) were affected by the nutritional conditions during the larval stage. We compared the occurrence of territorial versus patrolling behaviour, lipid mass, flight muscle ratio, metabolic rate and spermatophore production of low quality males that were reared as a larva on drought-stressed host plants and control, high quality males. Low quality males were less likely to adopt the territorial perching tactic and emerged as adults with lower lipid mass than high quality males, but they were able to restore their lipid mass through adult feeding (and perhaps the breakdown of flight muscles). Host plant quality also affected spermatophore size. Independent of the larval food treatment, territorial perching males metabolised more lipids than non-territorial males, produced larger spermatophores and copulated for longer than males adopting non-territorial behaviour. We discuss the results relative to the co-existence of the behavioural tactics (perching and patrolling).     

Thermoregulatory differences between phenotypes in the speckled wood butterfly: hot perchers and cold patrollers?

Males of the speckled wood butterfly Pararge aegeria L. (Satyrinae), actively search for females (“patrolling”) or wait for them at particular places (“perching”). Darker males are more likely to patrol than pale ones, which are mainly territorial perchers. We studied whether this morphological variation relates to thermoregulatory differences. The relationship between thoracic temperature and ambient temperature differed between the colour types under natural conditions: darker males had on average lower body temperatures than paler males. Different activities (e.g. resting, flying) and behavioural strategies (perching or patrolling) were associated with differences in thoracic temperature: patrolling males which mainly engaged in long flights and periods of basking afterwards, had lower thoracic temperatures than perching males which engaged in very short flights, fights and basking. When resting for a while thoracic temperatures did not differ between males practising different strategies. Under laboratory conditions, darker males heated up faster than pale males but there was no difference in the thoracic temperature at which they started to fly. These results indicate that thermal requirements (or general conditions) differ between the behavioural strategies, and that behavioural differences between phenotypes (colour types) relate to differences in thermal ecology. This supports the idea that darker males are better adapted to patrolling. There is no evidence that one mate-locating strategy is always superior to the other, which coincides with the observation that both strategies co-exist. More generally, this study shows that relatively small differences in colour can have a considerable effect on thermoregulation and hence on the behavioural strategies a heliothermic insect will adopt. Received: 15 August 1997 / Accepted: 15 December 1997     

Do Feeding Resources Induce the Adoption of Resource Defence Polygyny in a Lekking Butterfly?

Among polygynous species, males often compete for the possession of mating sites to increase their reproductive success. Weaker individuals frequently adopt alternative non‐territorial mate‐locating tactics, but the adoption of alternative territorial tactics may also occur. Although alternative tactics with territory defence are less common in arthropods, factors that drive its adoption may provide information to understand the organization of different territorial mating systems in the group. Here we investigate the adoption of resource‐based territoriality as an alternative to a non‐resource‐based one by males of the butterfly Paryphthimoides phronius. Male P. phronius commonly defend sunny clearings lacking feeding resources in the forest edge (non‐resource‐based territoriality). However, after experimentally offering fermenting fruit in previously undefended sites, we showed that males also adopt a resource defence tactic. Males in territories with fermenting fruits apparently feed on this resource when they are not defending the territory. However, males in sites without resources did not migrate to territories with resources when given the opportunity. To our knowledge, this is the first experimental investigation to show a non‐resource‐ and an alternative resource‐based mate‐locating tactic in a butterfly. We suggest that this behavioural flexibility may represent an important step to understand the ecological factors responsible for the organization and evolution of different territorial mating systems in insects.     

Body size and alternative mating tactics in the beewolf Philanthus zebratus (Hymenoptera; Sphecidae)

A study of the mating behaviour of males of the beewolf Philanthus zebratus revealed that in one population males display variability in mating tactics and that this variability is related to male body size. There was a tendency for large males to patrol the airspace above the nesting area while smaller males were territorial adjacent to it. The mean sizes of the two groups of males were significantly different, although the size ranges of the two groups overlapped. Only 2.5% of the males were observed to undertake both mating tactics, at different times. Observations are presented on daily and seasonal activity patterns and on the relative location of nests, territories, and patrolling males. A second population, with lower nest density, was observed for several days, revealing only territorial males. It is suggested that the presence of patrolling males is related to the higher nest density of the one population. The fact that patrolling males tend to be relatively large is possibly related to flight energetics or simply to the ability of large males to seize females, which are usually larger than males, in mid-air.     

Body temperature and territory selection by males of the speckled wood butterfly (Pararge aegeria): what makes a forest sunlit patch a rendezvous site?

1. Insects locate mobile resources like prey items or mates using either sit‐and‐wait (‘perching’) or active (‘patrolling’) searching strategies. The sit‐and‐wait strategy can be accompanied by defending and monopolising a site through territorial behaviour. 2. The present study focuses on the territorial perching behaviour in males of the speckled wood butterfly (Pararge aegeria L.). Recent studies suggested that the selection of territories (i.e. sunlit patches on the forest floor) is driven by structural characteristics of the site that affect male visual detection. However, given that adult butterflies are heliothermic organisms and that forests provide a diverse array of light environments, it seems likely that thermal aspects may also be used for territory selection. 3. We tested whether used and unused sunlit patches differed in thermal profile under field conditions in a Belgian woodland. We also used dummy butterflies to quantify variation in operative thoracic temperature and to calculate heating rates within (i.e. different vegetation structures) and between patches. 4. Sunlit patches occupied by a territorial male were larger, and were more frequently characterised by low vegetation structures compared with empty sunlit patches. It took longer to reach optimal thorax temperature (starting from a fixed suboptimal body temperature) in small patches compared with large patches. 5. We suggest that aspects of visual detection need to be combined with thermal aspects to fully understand territory selection in the speckled wood butterfly, as synergetic and/or trade‐off effects of ambient temperature, solar radiation, and canopy/vegetation structure may be involved.     

The Consequences of Predation Risk on the Male Territorial Behavior in a Solitary Bee

Territorial males may adopt a mating tactic that yields greater reproductive success but that at the same time increases the risk of predation. Plasticity in reproductive behavior can reflect a balance between sexual selection and natural selection. In this study, we sought to verify the effect of predation risk on territorial behavior of males of the solitary bee Ptilothrix fructifera (Apidae). Males of the species employ alternative mating tactics and can be territorial in defense of larval food sources. By manipulating predator models in the field, we tested whether (1) males avoid perch flowers containing predator models; (2) males alternate between mating tactics when their territory is associated with a predation risk; and (3) female foraging on flowers in a territory is altered in the presence of a predator model. We measured the responses of males and females in flowers containing and not containing a model of a spider or a stuffed bird. The results show that territorial males of P. fructifera alter their territorial behavior when faced with a high risk of predation. They do not abandon their territory or change to a non‐territorial mating tactic, but instead change the use of their territory, avoiding flowers containing predator models or perching on other flowers when the previous flower presented a potential predation risk. Female P. fructifera decreases the frequency of their visits to flowers and the length of time spent there in the presence of a spider model. In short, in the face of predation risk, females and males alter their behaviors at the cost of less efficient foraging and searching for partners, respectively.     

SEXUAL SELECTION AND BUTTERFLY DESIGN—A COMPARATIVE STUDY

Temperate butterflies of 44 species were examined to determine if their mating system (perching and patrolling) affected flight design. To control for spurious effects due to ancestry, 25 of these species were assigned to eight contrasts within which a change in mating system had occurred. In perching species sexual selection was predicted to favor traits associated with high acceleration ability and speed, while in patrolling species traits associated with flight endurance were predicted. In conformance with these expectations males of perching species had larger thorax/body mass ratios, higher wing loadings, and higher aspect ratios than patrolling species. The male mating system affected females in the same direction in the same variables as males. This could be explained by a genetic correlation with males. When removing the covariance between the sexes, only male design was explained by the mating system. The mating system was also associated with different degrees of sexual dimorphism in wing size. This supported the hypothesis that male design was affected by the mating system.     

Investigating the Consistency of Mate-Locating Behavior in the Territorial Butterfly Hypolimnas bolina (Lepidoptera: Nymphalidae)

The study of butterfly behavior has afforded valuable insights into the evolution of alternative mating tactics. Two hypotheses derived from this area of research contend that (1) territoriality is only viable under low to moderate conspecific densities (due to the costs of site defence) and (2) perching may be employed only when thermal conditions constrain flight activity. These hypotheses were evaluated by investigating mate locating behavior in Hypolimnas bolina, a territorial species that is naturally subject to variation in population density and weather conditions. Male behavior was charted throughout the day during a period of high population density at an encounter site in tropical Australia. Perching was the primary tactic, although a small proportion of individuals patrolled nonaggressively in the afternoon. Population-level male behavior failed to support predictions drawn from either the territory economics or thermal constraint hypotheses. First, the proportion of perching males and the number of aggressive conspecific interactions (per male) increased with increasing male density at the site. Second, few males patrolled at the hottest, brightest time of day (approximately midday), and the diel distribution of perchers did not emulate the U-shaped distribution shown by the occurrence of dorsal basking behavior. These results show that perching in this species is not a suboptimal tactic employed when temperatures constrain flight activity but may represent the best method of locating receptive females. At this stage the reproductive significance of the observed patrolling behavior remains obscure.     

Mate-locating behavior of the butterfly Lethe diana (Lepidoptera: Satyridae): do males diurnally or seasonally change their mating strategy?

The mate-locating behavior of male butterflies has been classified into two major types, territorial and patrolling. Territorial males defend a specific site, whereas patrolling males fly around a wider area without having to defend a site. In this study, I investigated the use of these tactics by males of the satyrine butterfly, Lethe diana. A previous study suggested that the males of L. diana change their mate-locating behavior during the day (they patrol in the morning and defend territories in the afternoon) and that patrolling is the primary mating strategy, whereas defending territories is a supplementary one. In the present study, I found that the daily activity pattern of the males of L. diana was similar to that described in the previous study: males often flew around in the morning and competed for territories in the afternoon. However, contrary to the previous study, all courtships and copulations were performed within male territories during their territorial activity. Closer observations revealed that copulations found in male territories were achieved by the owner of the territory. Males tended to feed in the morning, suggesting that the males flying in the morning searched for food rather than females. I conclude that territory holding is the primary male matelocating tactic in L. diana. I further found that, in summer, males exhibited territorial behavior later than in spring or autumn, which may be a strategy for preventing heat stress.     

Aerial Contests, Sexual Selection and Flight Morphology in Solitary Pompilid Wasps

Aerial contest competition has proven to be a challenging phenomenon to interpret in many territorial insects. Because the duels often consist of elaborate and/or high speed ascending maneuvers, the hypothesis that they are settled due to asymmetries in flight performance is intuitively appealing. We evaluated this hypothesis by contrasting differences in known morphological determinants of flight performance between (1) residents vs. non-residents of the territorial wasp, Hemipepsis ustulata and between (2) H. ustulata vs. a non-territorial relative, Pepsis thisbe . In the first contrast, resident male H. ustulata were seen to be larger, and had a tendency for reduced wing loading, but they did not possess greater flight musculature or wing aspect ratios (i.e., more elongated wings) than their non-resident counterparts. In the second contrast, male H. ustulata exhibited clearly greater flight musculature and greater sexual dimorphism in this parameter (males more muscular), and also exhibited a slight tendency for greater wing loading and smaller aspect ratios than males of the patrolling species P. thisbe . Interestingly, although size is linked with territorial success in H. ustulata , males of this species were not larger than male P. thisbe , nor did the former species exhibit greater sexual size dimorphism. These results do not support the hypothesis that the repeated ascending contests of H. ustulata require, and select for, a high acceleration design. However, the observed intraspecific patterns of flight musculature suggest that high acceleration is favored in males of the perching species, perhaps for the ability to intercept passing receptive females.     

Diurnal and seasonal changes in the mate-locating behavior of the satyrine butterfly <Emphasis Type="Italic">Lethe diana</Emphasis>

The time schedule of mate-locating behavior in the male satyrine butterfly Lethe diana was studied. Males displayed territorial behavior only in the afternoon, but it was not known whether they attempted to locate mates in the morning. In order for males of most butterfly species to mate with a virgin female, it would be most effective to initiate mate-locating behavior in the morning, when synchronous eclosions occur. Males of L.diana flew patrols in the morning and displayed territorial behavior in the afternoon. The cost of territorial behavior is probably less than that of patrolling, as territorial flights are shorter than those when patrolling. The temporal switching of mate-locating behavior is theoretically favored, since the reproductive value of females decreases later in the day, when males perform the less costly mate-locating behavior. Thus, the diurnal switching of male mate-locating behavior may be an adaptive strategy in response to the rapid decline in the reproductive value of females over the course of a day.     

Ecological and phylogenetic perspectives on wing stiffness in nine Theclini species (Lepidoptera: Lycaenidae)

We studied the relationship between wing stiffness and butterfly ecology and phylogeny. Nine species belonging to the tribe Theclini of the family Lycaenidae were selected and examined for the wing stiffness of dried specimens by a three‐point bending test. It was found in Japonica lutea that the wing stiffness was not affected by the humidity to which it had been exposed, but was strongly affected by wing size and sex. Comparisons of sexual differences in four species indicated that females of patrolling species had stiffer wings than conspecific males, but that males of territorial species had stiffer wings than conspecific females. Finally, the wing stiffness was compared among males of nine species that use different mate‐locating tactics, and the results revealed a tendency that males of territorial species have stiffer wings than males of patrolling species. These results, though including a few exceptional cases, are discussed from the perspective of ecological requirements and phylogenetic constraints on the species.     

Relative fitness of alternative male reproductive tactics in a mammal varies between years

1. In many species, males can use different behavioural tactics to achieve fertilization, so-called alternative reproductive tactics (ARTs). Few field studies have measured fitness consequences of ARTs under varying environmental conditions. 2. Here, we describe fitness consequences of three phenotypically plastic ARTs in the African striped mouse (Rhabdomys pumilio) and show that relative fitness of ARTs differs between years. Each year represents a different generation. 3. For the generation living under high population density, tactics differed in relative fitness in accordance with the theory of conditional strategies, with highly successful territorial breeding males having 10 times higher success than solitary roaming males and 102 times higher success than adult natally philopatric males. 4. For the generation living under intermediate population density, the territorial breeding and roaming tactics yielded similar fitness, which would be in agreement with the theory of mixed strategies. No philopatric males occurred. 5. For the generation living under low population density, roaming was the only tactic used and some roamers had very high fitness. 6. The main prediction of status-dependent selection for conditional strategies is a correlation between fitness and status, often measured as body mass, but we did not find this correlation within tactics when more than one tactic was expressed in the population. 7. Female distribution seems to have an effect on which reproductive tactics male chose: female defence polygyny when females are clumped (interference competition), but a searching tactic when females are dispersed (scramble competition). In contrast to predictions arising from theory on scramble competition, male body mass was important in determining fitness only in the year when females were dispersed, but not in other years. 8. Our results indicate that the differentiation between conditional and mixed strategies is not an absolute one. In many other species, environmental conditions might fluctuate temporally and spatially so that the normally suboptimal tactic yields similar fitness to the (usually) dominant tactic or that only a single tactic prevails. 9. We suggest the term single strategy, independent of current fitness consequences, for systems where tactics are not genetically determined, in contrast to genetically determined alternative strategies.     

The Mating System of <Emphasis Type="Italic">Amegilla</Emphasis> (<Emphasis Type="Italic">Asarapoda</Emphasis>) <Emphasis Type="Italic">paracalva</Emphasis> Brooks (Hymenoptera: Apidae)

Males of the solitary bee Amegilla (Asarapoda) paracalva employ two mate-locating tactics: aggressive defense of sites from which virgin females are emerging and patrolling flower patches that are visited by conspecific females. At one study site, a single male was able to control an entire emergence area for one or more days. Multiple males patrolled one flower patch, interacting aggressively on occasion but no one individual was able to monopolize this resource. Territorial males at the emergence site secured mates by waiting by tunnels for receptive virgin females to emerge after metamorphosis. Males patrolling the flower patch pounced upon flower visiting conspecifics and mated with receptive females there. Territorial males at the emergence site were larger than average individuals, probably because of the advantage larger males have when grappling with opponents. Flower patrolling males were smaller than territorial males at the emergence sites, perhaps because of the advantages gained by these males from rapid, agile flight.     

Size-Dependent Male Alternative Reproductive Tactics in the Shell-Brooding Cichlid Fish Lamprologus callipterus in Lake Tanganyika

Reproductive parasitism among males is prevalent in fishes. Typically, small ripe males parasitize the reproductive effort of large bourgeois males by using various behavioural tactics. We examined the size‐dependent advantages of parasitic behavioural tactics in a shell‐brooding cichlid fish of Lake Tanganyika with three male types (large bourgeois males and medium–dwarf parasitic males). The extremely small ‘dwarf males’ weighing only 2.5% on average of large males, perform a specialized tactic in which they avoid attacks by the resident large males by entering the inner part of the whorl of the shell where a female is spawning. Field observations and a manipulation experiment revealed that the very small size of dwarf males is essential for utilizing this positional advantage. Larger dwarf males and medium males opportunistically adopt darting and sneaking which likely result in very low reproductive outcomes. The size associated advantage and disadvantage of parasitic tactics are the major factors shaping the size distribution of ripe males in this species. The success of parasitic spawning by dwarf males is determined not only by body size of the males, but also by the relative sizes of females and shells in which they spawn. These factors would affect the choice of different tactics among dwarf males. The analyses of body condition among ripe and unripe males across a wide range of body sizes suggested that onset of sexual activities at very small body sizes in dwarf males may be associated with higher condition factors that is a pre‐requisite for maintaining investment in testes and intense reproductive activities.     

The Resource-Based Mating System of the Mediterranean Pollen Wasp Ceramius fonscolombei Latreille 1810 (Hymenoptera, Vespidae, Masarinae)

Males of C. fonscolombei patrol and perch at water collection sites or at plants of Reseda, both of which are important resources for female brood care. The mating system can be classified as resource defense polygyny modified by the existence of alternative male mating tactics. Occupying temporary territories at watercollection sites constitutes the primary tactic which is more profitable for larger males. The secondary tactic of patrolling at flowers provides a nonaggressive alternative through which smaller males gain at least some mating success. Males at water collection sites occupy considerably smaller ranges but spend a higher proportion of time patrolling than males at flowers. They frequently grapple with other males, an activity that is absent at flowers. Males at water collection sites copulate about 2.5 times more frequently than males at flowers. The copulation frequency of the males at water collection sites is positively correlated with their body size, while copulation frequency is negatively correlated with body size at flowers. Males patrolling at water collection sites and males patrolling at flowers do not differ in body size, indicating that the decision between alternative mating tactics is not made relative to body size but is influenced by other factors.     

Take-off flight performance in the butterfly Pararge aegeria relative to sex and morphology: a quantitative genetic assessment

Adult fitness components may strongly depend on variation in locomotory performance such as flight; this variation can be sex specific. Fast take-off to intercept females and competing males is an essential behavioral component of the territorial perching behavior in male speckled wood butterflies (Pararge aegeria L.). Females on the other hand avoid frequent take-offs particularly under suboptimal temperatures, typically showing fewer but longer flights than males. We estimated the heritability of take-off acceleration performance under suboptimal body temperatures by a restricted maximum-likelihood model. We calculated genetic correlations between this performance and a selection of morphological traits: size (body mass), flight muscle investment (relative thorax mass), and wing shape (forewing aspect ratio). Our results show significant additive genetic variation for mean acceleration performance and a similar but nonsignificant trend (P= 0.08) for maximal acceleration performance during take-off in males (h(2)= 0.15). In females, heritability was not significantly different from zero for either of the acceleration performance measures. Morphological traits and take-off performance were genetically linked in a sex-specific way. In males, relative thorax mass and forewing aspect ratio were positively genetically correlated with acceleration performance. In females, there was a negative genetic correlation between acceleration performance and abdomen mass, but not with residual abdomen mass (i.e., regressed on total body mass). To fully understand the evolution of sexual differences in flight performances and morphology, several other flight performances will have to be included. This multifunctional nature of flight and its consequences for the evolutionary study of flight has not yet been fully appreciated in the literature.     

Parasitism and alternative reproductive tactics in Northern chamois

Alternative reproductive tactics (ARTs), discrete phenotypic variations evolved to maximize fitness, may entail different cost‐benefit trade‐offs. In large mammals, differences in costs associated with ARTs—including energy expenditure and parasite infection—are typically greatest during the breeding season. Nonetheless, physiological and behavioral differences between ARTs can manifest throughout the year, possibly involving costs that may contribute to maintain ARTs within populations. Using the number of nematode larvae per gram of feces (LPG) as a proxy, we explored the temporal changes in lung parasite infection in territorial and nonterritorial male chamois Rupicapra in the Gran Paradiso National Park (Italy), between 2011 and 2012. We aimed to identify which tactic‐specific physiological and behavioral features (including age, hormonal levels, inter‐ and intrasexual interactions, and space use) or climatic factors (temperature and precipitation) best explained yearly variation in parasite infection within and between ARTs. Generalized additive mixed models showed that the fecal larval counts of lung nematodes underwent strong temporal changes in both male types. Differences between ARTs (with higher LPG values in territorial than nonterritorial males) were greatest during the rut and—to a lesser extent—in spring, respectively, at the peak and at the onset of territoriality. The difference in LPG between tactics was largely explained by the greater levels of hormone metabolites in territorial males during the rut. The other variables did not contribute significantly to explain the different shedding of larvae within and between ARTs. Our analysis suggests that different values of LPG between territorial and nonterritorial males are largely a result of tactic‐specific differences in the secretion of hormone metabolites, but only during the rut. To clarify whether rut‐related parasitism contributes to the maintenance of ARTs, tactic‐specific life history trade‐offs, for example, between reproduction and parasite‐related mortality, must be investigated.     

Relationships between body composition, body size and alternative reproductive tactics in a lekking sandpiper, the Ruff (Philomachus pugnax)

1. The Ruff is a lekking sandpiper in which males have two genetically determined alternative mating strategies: 'satellite' or 'independent'. Satellite males are non-territorial, following groups of females on and off leks. Independent males attempt to establish territories on leks and can be either 'resident' territory holders, or non-territorial 'marginals'. The time budgets of the three behavioural tactics (resident, marginal and satellite) differ notably in time allocated to foraging, aggression and display activity. These differences have led to the suggestion that the benefits of size and energy stores may vary with mating tactic.
2. In this paper in vivo estimates of body composition (fat, fat-free mass) for breeding male Ruffs using total body electrical conductivity (TOBEC) are presented.
3. Satellite males have significantly shorter tarsi and wings than independent males.
4. After correcting for size, independent males are significantly heavier and fatter than satellites, and marginals in particular are heavier and fatter than both residents and satellites.
5. Estimates of energy expenditure during flight suggest that satellites may maintain reduced energy reserves to minimize flight costs, while the larger fat stores of independent males are consistent with the benefits of endurance as a territory holder.     

Resource availability,mating opportunity and sexual selection intensity influence the expression of male alternative reproductive tactics

The expression of alternative reproductive tactics can be plastic and occur simultaneously depending on cues that vary spatially or temporally. For example, variation in resources and sexual selection intensity is expected to influence the pay‐off of each tactic and shape the decision of which tactic to employ. Males of the nuptial gift‐giving spider Pisaura mirabilis can adopt three tactics: offering a genuine prey gift, a ‘worthless’ non‐nutritious gift or no gift. We hypothesized that resources and/or male body condition, and mating opportunity and sexual selection intensity, vary over the course of the mating season to shape the co‐existence of alternative traits. We measured these variables in the field over two seasons, to investigate the predictions that as the mating season progresses, (i) males become more likely to employ a gift‐giving tactic, and (ii) the likelihood of switching from worthless to genuine gifts increases. Prey availability increased over the season and co‐varied with the propensity of males to employ the gift‐giving tactic, but we found no support for condition‐dependent gift giving. Males responded to an increase in female availability by increasing their mating effort (gift production). Furthermore, the frequency of genuine gift use increased with sexual selection intensity, consistent with the assumption that sperm competition intensity increases with time. Our results suggest that the frequency of alternative tactics is shaped by seasonal changes in ecological factors and sexual selection. This leads to relaxed selection for the gift‐giving tactic early in the season when females are less choosy and resources more scarce, and increased selection for genuine gifts later in the season driven by mating opportunity and risk of sperm competition.