Body size and lifetime mating success of male midges (Diptera: Chironomidae)

Anita. Behav., 1990, 40, 648-652

Body size and lifetime mating success of male midges (Diptera: Chironomidae) R. M. N E E M S , A. J. M C L A C H L A N

& R. C H A M B E R S

Biology Department, Universityof Newcastle-upon-Tyne, Newcastle-upon-Tyne NE2 1HR, U.K.

Abstract. Among insects that mate on the wing, small males should have the mating advantage by being more acrobatic than large males. However, this benefit could be outweighed by costs to small size in other components of fitness. The hypothesis that mated males of the midge Chironomus plumosus L. are on average smaller than unmated males was tested. Small males were predicted to pay for any such success with a reduced longevity and a reduction in flight endurance. Hence small males should achieve a lower lifetime mating success than their larger conspecifics. As predicted, small males had the mating advantage. However, small size did not accrue the expected costs. Although body size correlated positively with lifespan and flight duration for starved males, when given access to food, small males lived and flew for as long as larger competitors. Ultimately, small size did run into constraints. The rare, smallest males in a population could not maintain continuous flight. Hence small size is beneficial to male midges but reduction in size by sexual selection is balanced by physiological constraints on flight.

Large body size is often taken to be the universal determinant of mating success in males. This truism has developed from the many studies that have found large males to be favoured (e.g. Howard 1980; Davidson 1982; Ward 1983; Simmons t986). However, in species where physical contests are rare, large males do not necessarily have an advantage over smaller males (see review by Gould 1984). Small size may in fact be beneficial in mating systems where males rely more on agility than on strength to capture females. Ghiselin (1974) suggested that agility should be important when mating occurs in a three-dimensional habitat, for example in aquatic or aerial systems. Work on chironomids (Mclachlan & Allen 1987) and dragonflies (Convey 1989) supports this view. Small individuals appear to gain the advantage through greater powers of acceleration and an ability to change direction more quickly than larger individuals. These attributes can be predicted from Newtonian laws of motion (e.g. Steele & Partridge 1988). Thus, as with birds and aircraft, the smaller the insect the greater its acrobatic ability (discussed by Mclachlan 1986a). Other insects in which the small males have a high rate of success at capturing females include Drosophila (Steele & Partridge 1988) and damselflies (Banks & Thompson 1985). The measurement of mating success over only a part of an individual's life has been criticized (e.g. Koenig & Albano 1987; Mclachlan 1987; Thompson 1987). The assumption that the fitness of a particular phenotype can be extrapolated from 0003-3472/90/100648 + 05 $03.00/0

a male's success on one mating occasion is thought to be unreliable (Arnold & Wade 1984). This is because the number of such events may correlate with other variables such as longevity which in turn correlate with body size. Where small males gain the mating advantage, it is widely believed that they lose elsewhere in the fitness stakes. For example, large individuals generally live longer than small ones so, although small males may have the highest rate of mating on any particular day, due to differences in lifespan it is the large males that achieve the highest lifetime mating success and consequently the highest fitness (Banks & Thompson 1985). For insects that form swarms to mate, another important component of fitness is the ability of the male to maintain flight within the swarm. Chironomid males form swarms at dusk and continue swarming until nightfall. During this time females arrive seeking mates. In such mating systems, a small fraction of the males often get the majority of the matings (Vehrencamp & Bradbury 1984) and, therefore, the longer an individual can stay in the swarm the higher its chances of success. Since large flies have a lower wing-beat frequency than small ones, they incur less cost per unit time per unit distance travelled. Increased body size therefore allows individuals to fly for longer periods (e.g. Aphis fabae: Cockbain 1961). In swarming chironomids there thus appears to be a conflict of interests. Large body size is advantageous since it allows the male to swarm for

9 1990 The Association for the Study of Animal Behaviour 648

N e e m s et al.." Size and lifetime mating success

longer. On the other hand, small size brings with it greater aerobatic manoeuvrability. We set out to test two hypotheses: (1) that small males have the short-term mating advantage over large males; and (2) that body size correlates positively with longevity and duration of uninterrupted flight. We use a common midge, Chironomus plumosus, as the test animal.

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only in having had access to food. Any flies unable to maintain uninterrupted flight were omitted from this part of our procedures. A second set of observations took interrupted fliers into account. A group of flies were tethered as before and stimulated to fly. Those unable to maintain flight for 3 min were classed as 'intermittent' while those that could fly for that long were classed as continuous fliers. We recorded the wing lengths of these flies.

METHODS RESULTS

Mating Success We took samples of male flies, both singly and in mating pairs from Washington Waterfowl Park, Tyne and Wear in June 1988 (National Grid reference NZ 332 566). Most mating occurs over a period of an hour at peak swarming time which is around 2130 hours in June. We caught mating pairs individuallyin an entomological net as they floated out of the swarm and single males by sweepnetting the swarm. The swarms are homogeneous with respect to body size (Mclachlan & Neems 1989) so a single net sweep obtains a random sample of males. Wing length, with is a good indicator of body size in midges (Mclachlan 1986b), was measured to the nearest 0.05 mm under a microscope fitted with a linear scale. Measurements were made from the anal lobe to the wing tip.

Longevity Adults were reared at constant temperature (20~ under a 12:12h light:dark regime with abundant food. We collected emerging males daily and placed them in vials (0-5 x 2.0 cm) closed with a cotton-wool plug moistened to prevent desiccation. The flies were left until they died when we recorded lifespan and wing length. We repeated this procedure on a second group of flies where adults had access to food in the form of an aqueous extract of raisins dried on filter paper (Burtt et al. 1986).

Flight Duration Flies reared as above were left for 24 h to reach the end of the teneral period. Males were then tethered using the method of Wigglesworth (1949) and flown to exhaustion. They were deemed exhausted when they ceased to fly and held their wings out horizontally to the body. We carried out this procedure on a second group of flies which differed

Mating Success We compared the size distribution of mated males with that of single males in four replicate samples using the chi-squared test and Student's t-test. A heterogeneity chi-squared tes~ showed that the four replicates did not differ significantly from each other and so were pooled (Z2= 10.31, v= 18, P > 0.05). Swarming males and mated males differed in size (g2 = 39.62, v = 13, P < 0-005). This result is obtained from contingency tables with size in mated and single males in the rows and 14 size classes occupying the columns. The difference lies in the presence of very small males only in the mated population (Fig. 1). Mean size also shifted downwards among the mated males. That is, on average mated males were smaller than single males (Student's t-test: t I = 1-67, P < 0'05; t 2 = 3.71, P O . O 5 ; t4 = 3.43,P
Longevity As predicted, smaller males had a shorter lifespan than large males (Fig. 2a; r=0'45, Y= 56.67X- 102.76, P < 0'01). However, this relationship holds only when adults were deprived of food. When the flies had access to food, the regression of size on longevity breaks down (Fig. 2b) and there is a complete disassociation between wing length and longevity (r = 0'09, Y= 51.62X+ 0.82, P > 0.05). As expected, fed flies lived for longer on average (fed iY= 207.8 h; starved X = 127-1 h).

Flight Duration In the absence of food large males could sustain flight for longer than small males (r=0"74, Y= 75-47X-215-55, P<0"001; Fig. 3a). These differences disappeared when the flies were allowed

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Wing length(mm) Figure 1. Size frequency distributions of males found in the swarm and in mated pairs in four replicate samples. The size class containing the mean is shaded. to feed in the adult stage (Fig. 3b; r=0.25, Y = 2 5 . 9 8 X - I I ' 3 5 , P>0.05). Intermittent fliers were significantly smaller than continuous fliers (Student's t = 5.43, v = 239, P < 0.001 ), DISCUSSION Mating success in C. plumosus depended on the body size of individual males. As with many other non-biting midges, small males had the advantage. However, unlike the species studied previously (Mclachlan & Neems 1989) the small males are not to be found in the vegetation mating with females attracted to the swarm (R. M. Neems, unpublished data). They instead gain their mating success by participating fully in the swarm, supporting the suggestion that small males are more aerobatic in this species. Sexual selection therefore appears to be operating through competition between males in favour of small size in males. However, if this is to be

reflected in lifetime mating success, small size must not carry any significant disadvantages elsewhere in the life history. Our results suggest that small size does not incur any great costs with regard to two important components of fitness: longevity and flight duration. In the laboratory, provided food was available, small males did as well as their larger conspecifics. To extrapolate these findings to the wild, evidence is required that chironomids do normally feed, if only opportunistically, as adults. Feeding by adult chironomids on dried 'honeydew' (aphid excretion) has been widely reported (Downes 1974) and the use to which energy acquired in this way is put has been studied by Burtt et al. (1986). These observations show that food is both readily available and widely used in the wild. Males might extend their lifespan either by feeding during the day or by feeding on 'honeydew' periodically during the swarming period in the evening. Indirect evidence for the latter comes from our own observation that males leave the swarm

N e e m s et al.. Size and lifetime mating success

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occasionally to sit briefly on surrounding leaves before returning to the swarm. We conclude that small males can be present on as many evenings and for as long as large males. The mating success of small males during one mating session is therefore representative of their lifetime mating success. However, there must be an optimal body size below which further reduction would be disadvantageous. This is supported by our observation that rare, dwarf males are unable to sustain continuous flight and therefore remain unmated. The rare dwarves we do find in the field are probably part of a larger population of p o o r fliers that can be found amongst males emerging from the larval habitat but that fail to reach the mating swarm (unpublished data). Thus we can explain why chironomids do not evolve to be smaller but how do we explain the presence of males larger than the optimal size for mating? One possibility that is at present being investigated is that small males have a lower fertility so that even though they achieve the highest number ofmatings this is not reflected in number of offspring. ACKNOWLEDGMENTS We thank Washington Wildfowl Trust for allowing us to carry out the field work in their grounds and Penny Watt for important pilot observations. R.N. is in receipt of an S E R C studentship.

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maculata Linn. (Odonata: Libellulidae). Behaviour, 109, 125-141. Davidson, D. W. 1982. Sexual selection in harvester ants (Hymenoptera: Formicidae: Pogonomyrmex). Behav. Ecol. Sociobiol., 10, 245-250. Downes, J. A. 1974. The feeding habits of adult Chironomidae. Entomol. Tidskr. Suppl., 95, 84-90. Ghiselin, M. T. 1974. The Economy of Nature and the Evolution of Sex. Berkely: University of California Press. Gould, S. J. 1984. Hens' Teeth and Horses" Toes. Harmondsworth, Middlesex: Pelican. Howard, R. D. 1980. Mating behaviour and mating success in woodfrogs, Rana sylvatica. Anita. Behav., 28, 705-716. Koenig, W. D. & Albano, S. S. 1987. Lifetime reproductive success, selection and the opportunity for selection in the white-tailed skimmer, Plathemis lydia (Odonata: Libellulidae). Evolution, 41, 22-36. Mclachlan, A. J. 1986a. Survival of the smallest: advantages and costs of small size in flying animals. Ecol. Entomol., 11,237-240. Mclachlan, A. J. 1986b. Sexual dimorphism in midges: strategies for flight in the rainpool dweller Chironomus imicola (Diptera: Chironomidae). J. Anita. Ecol., 55, 261-267. Mclachlan, A. J. 1987. Male mating success in Diptera: a reply to Thompson. Oikos, 51, 109. Mclachlan, A. J. & Allen, D. F. 1987. Male mating success in Diptera: advantages of small size. Oikos, 48, 11-14. Mclachlan, A. J. & Neems, R. M. 1989. An alternative mating system in small male insects. Ecol. Entomol., 14, 85-91. Simmons, L. W. 1986. Intermale competition and mating success in the field cricket, Gryllus bimaculatus de Greer. Anita. Behav., 34, 567-579. Steele, R. H. & Partridge, L. 1988. A courtship advantage for small males in Drosophila suboscura. Anita. Behav., 36, 1190-I 197. Thompson, D. J. 1987. Male mating success in Diptera: a cautionary note. Oikos, 51, 108. Vehrencamp, S. L. & Bradbury, J. W. 1984. Mating systems and ecology. In: Behavioural Ecology. An Evolutionary Approach (Ed. by J. R. Krebs & N. B. Davies), pp. 251-278. Oxford: Blackwell Scientific Publications. Ward, P. I. 1983. The effects of size on the mating behaviour of the dung fly Sepsis cynipsea. Behav. Ecol. Sociobiol., 13, 75-80. Wigglesworth, V. B. 1949. The utilization of reserve substances in Drosophila during flight. J. exp. Biol., 26, 150-163. (Received 14 August 1989; initial acceptance 18 September 1989;final acceptance 31 October 1989; MS. number: 3442)