Territorial and Mating Success of Dragonflies That Vary in Muscle Power Output and Presence of Gregarine Gut Parasites

ARTICLE IN PRESS ANIMAL BEHAVIOUR, 2004, 68, 657–665 doi:10.1016/j.anbehav.2003.09.019 Territorial and mating success of dragonflies that vary in muscle power output and presence of gregarine gut parasites JAMES H. MARDEN & JASON R. COBB Department of Biology, Pennsylvania State University (Received 9 May 2003; initial acceptance 7 August 2003; final acceptance 26 September 2003; MS. number: A9609) Competition for mating territories in libellulid dragonflies involves aerial contests that require high levels of exertion and locomotor performance. Here we test the hypothesis that success of male Libellula pulchella dragonflies in territoriality and mating is affected by muscle contractile performance, and we examine how gregarine gut parasites affect muscle performance, energy reserves and territorial behaviour of their hosts. At a pond where gregarine parasites are rare, long-term territorial and mating success of males showed a significant positive association with muscle power output. At a nearby pond that had a much higher incidence and intensity of gregarine parasitism, there was no relationship between muscle performance and short-term territorial success. Instead, males assorted themselves into aggressive territory holders and submissive satellites, with the large majority of territory holders having no parasites and nearly all of the satellites parasitized. Unparasitized males showed a tight positive relationship between muscle power and fat content, which suggests that they use a known phenotypic adjustment in muscle contractile performance to allow the energy consumption rate of the flight muscles to match the rate at which energy can be mobilized from storage pools. Parasitized dragonflies showed a small decrease in average fat content and a marked change in the relationship between fat content and muscle power output. The apparent loss of the ability to match muscle contractility to the size of the energy storage pool in parasitized dragonflies suggests that gregarines may have systemic effects on signalling pathways and energy homeostasis. By indirectly choosing males that had successfully competed for territories, females consistently mated with physiologically or immunologically superior males despite large between-pond differences in male behaviour and the incidence and intensity of parasitic infection. Ó 2004 The Association for the Study of Animal Behaviour. Published by Elsevier Ltd. All rights reserved. Competition for mates and the resources necessary to contractile performance of muscles (Marden et al. 2001) obtain mates is a pervasive and well-studied feature of should enhance success in types of competitive interac- animal behaviour. Much is known regarding the role of tions that depend heavily on exertion and locomotion. externally apparent traits such as ornaments, vocaliza- Knowledge regarding the variability of such traits within tions and chemical signals, but sexual competition also populations, the source of the variation, and its conse- commonly involves contests or battles that require high quences for competitive success are important for un- levels of exertion and locomotor performance. In such derstanding how selection acts on physiological capacities cases, internal physiological traits are likely to play a strong and how they evolve. role in determining success or failure, yet for most types of A common source of performance variation in free- animals we know little about variability in the physiolog- living animals is parasitism. The behaviour and success of ical features that affect intraspecific competition. Attri- parasitized animals during competitive interactions with butes such as high levels of energy reserves (Marden & conspecifics often differ markedly from those of non- Waage 1990), ability to up-regulate metabolic flux and parasitized animals (Schall & Sarni 1987; Howard & produce ATP at a high rate (Harrison & Hall 1993), and Minchella 1990; Moore & Gotelli 1996), but the physiological mechanisms underlying these differences have seldom been elucidated. Parasites may cause specific Correspondence: J. H. Marden, Department of Biology, 208 Mueller lesions or deficiencies that affect performance-related Labs, Pennsylvania State University, University Park, PA 16802, U.S.A. traits (Harrison et al. 2001); they may deprive the host (email: [email protected]). of energy necessary for high levels of exertion (Munger & 657 0003–3472/03/$30.00/0 Ó 2004 The Association for the Study of Animal Behaviour. Published by Elsevier Ltd. All rights reserved. ARTICLE IN PRESS 658 ANIMAL BEHAVIOUR, 68, - Karasov 1989; Siva-Jothy & Plaistow 1999), and they may concentration of their flights along boundaries between cause systemic physiological changes that affect many territories guarded by aggressive males, and their poor aspects of host metabolism and locomotion (Schall et al. ability to successfully copulate with females or guard the 1982). few females with which they copulated. In the particular case of flying animals it has been The focal observations and sampling described above shown that a high ratio of flight muscle mass to total body used males that had been marked individually with weight affects aerial performance and success in compet- coloured powder (Day-Glo Color Corp., Cleveland, Ohio, itive interactions (Marden 1989; Coelho & Holliday 2001; U.S.A.). The powder was applied using a blowgun tech- Berwaerts et al. 2002). The generality of this result nique (Marden 1989) that did not require capture or depends on there being fairly little variation in muscle handling of the dragonflies and had no discernable effect contractile performance (i.e. it requires that the ratio of on their behaviour. Marked males were observed for at muscle mass to body weight captures most of the be- least 1 h before determination of territorial or satellite tween-individual variation in force or power output status. Many of the nonterritorial males that we marked relative to total load). However, muscle contractile perfor- were not site specific; they were primarily feeding and mance can vary widely between individual conspecific their competitive status could not be determined. We animals (Marden et al. 2001), and contractility is a trait classified as satellites only those nonterritorial males that that is likely to be affected by parasites (i.e. perhaps by showed site fidelity, attempts to engage in opportunistic regulatory responses stimulated by metabolic changes or mating, and the submissive behaviours described above. decreased energy availability). Effects of intramuscular Darlington Pond measured approximately 300 m2 and parasites on contractility have been demonstrated (Har- all of the dragonflies present could be observed simulta- wood et al. 1996), but no studies have examined how neously and across many consecutive days, thereby muscle contractile performance is related to the presence allowing quantification of long-term mating success of of parasites in nonmuscle tissues. a large population of males. When each male arrived and Here we test the hypothesis that success of male Libel- began to engage in territorial interactions for the first time lula pulchella dragonflies in territoriality and mating is at Darlington Pond we captured it in an insect net. After affected by muscle contractile performance, and we netting, we used permanent ink to write a number on one examine how gregarine gut parasites affect muscle perfor- wing and marked the tips of all four wings with a unique mance, energy reserves and territorial behaviour of their combination of coloured spots using the Day-Glo powder hosts. described above. The powder rubbed gently onto the wing tips remained visible for up to 3 weeks. Long-lived males were occasionally recaptured to refresh their wing colours. METHODS Records were kept of arrival and departure times for each male, and we counted the number of times they copulated We studied L. pulchella dragonflies at two ponds in Centre with females. We collected a representative sample of County, Pennsylvania, U.S.A., during June and July in males from Darlington Pond near the end of their 2000 and 2001. Our main study site in 2000 was Ten Acre territorial tenure and tested them for muscle contractile Pond (40 480N, 77 560W). In 2001, we primarily studied performance. We also used data from this pond to dragonflies at a small unnamed pond (which we called examine the relationship between territorial effort and Darlington Pond; 40 510N, 77 500W). These two ponds longevity. were separated by approximately 12 km. Dragonflies from both ponds were transported to the Females visit territories defended by male L. pulchella laboratory to determine their muscle contractile perfor- dragonflies to copulate and deposit their eggs while being mance (see Marden et al. 2001 for detailed methodology). guarded by the male (Pezalla 1979). Owing to differences Briefly, we removed the head, wings and legs and in pond size and terrain, our ability to monitor these cemented the thorax and abdomen in a controlled tem- events differed at the two ponds, which required us to use perature chamber. A series of shallow incisions were made different sampling schemes. Ten Acre Pond was too large around the dorsal attachment point of the mesothoracic to monitor the entire pond, so we studied short-term basalar muscle to mechanically isolate the muscle and territorial and mating success of focal individuals or pairs attach it to the lever arm of an ergometer. The lever of individuals. Our focal observations were made on imposed a sinusoidal

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