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Diptera: Sepsidae) Flies Away from Oviposition Sites

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BEHAVIOR Behavior and Reproductive Status of Microsepsis armillata (Diptera: Sepsidae) Flies Away from Oviposition Sites WILLIAM G. EBERHARD Smithsonian Tropical Research Institute, and Escuela de Biologõ´a, Universidad de Costa Rica Ciudad Universitaria, Costa Rica Ann. Entomol. Soc. Am. 93(4): 966Ð971 (2000) ABSTRACT The mystery of where virgin female Microsepsis armillata (Melander & Spuler) copulate has been solved with the discovery of sexual activity in small aggregations that are not tightly associated with the oviposition sites, where matings have been observed previously in this and other sepsid species. Nonvirgin females also mate in these aggregations, and matings at such sites may help explain the otherwise puzzling variations in male precopulatory riding behavior in other sepsids. Approximately 25% of the unpaired females in aggregations carried an unlaid egg in her bursa, and larvae had hatched from some of these eggs. Retention of a bursal egg could prevent intromission by males. KEY WORDS Microsepsis armillata, mating, aggregations, virgin females, Sepsidae SEPSID FLIES ARE characterized by an unusual mating solution is suggested by observations of occasional system. Males wait near oviposition sites such as dung mating pairs of Sepsis in large aggregations (Pont 1987) or carrion (Pont 1979), and mount females when they and among ßies in smaller groups away from dung arrive. But the males only mate with females after (Schulz 1999), and a brief note on apparent mating oviposition is Þnished (Parker 1972a, 1972b; Ward attempts by S. neocynipsea Melander & Spuler at an 1983; Eberhard 1999; Schulz 1999). The morphological apparent feeding site (Eberhard 1999). The current Þt between male and female genitalia during copula- article presents a detailed study of reproductive be- tion (Eberhard and Huber 1998) suggests why copu- havior away from oviposition sites. lation is generally postponed until oviposition is com- A second puzzle is that in some species, the males pleted (Eberhard 1996). Males of Archisepsis spp. and of some populations but not others ride the female Microsepsis spp. deposit a large spermatophore that before mating, thus apparently defending her against Þlls the anterior portion of the femaleÕs bursa, where other males (Schulz 1999). The reproductive payoffs each egg must pass on its way toward the ovipositor. to the male from this type of defense are probably At least in A. diversiformis (Ozerov) and M. armillata strongly affected by both the likelihood that the fe- (Melander & Spuler) sperm transfer from the sper- male will eventually mate with him after he has ridden matophore to the femaleÕs spermathecae and sper- her, and whether she is likely to mate subsequently mathecal ducts is not immediate (unpublished data; L. with another male away from this site before she lays Rodriguez, personal communication). Thus, if a male her next clutch of eggs. Mating does not always occur were to copulate with a female before she Þnished after riding in at least some species (40% and 92Ð97% laying the mature eggs in her ovaries, his spermato- of riding males failed to copulate in S. cynipsea (L.) phore would be driven out of her bursa by the next egg and two species of Archisepsis, respectively (unpub- as it passed down her reproductive tract, and little or lished data; Parker 1972b). Subsequent matings away no sperm would be transferred. Alternatively, if a from oviposition sites could also be important, espe- newly deposited spermatophore is difÞcult to dis- cially if the nearly complete second male sperm pre- place, the female would be prevented from laying cedence documented in S. punctum (F.) (Schulz further eggs until she dislodged the spermatophore. 1999) proves to be generally true for sepsids. A pair of puzzles regarding sepsid sexual biology are One possible type of mating site is a large aggrega- associated with this mating system. First, a femaleÕs tion such as those sometimes observed away from initial mating must occur before rather than after her oviposition sites (Pont 1979, 1987). Some aggregations Þrst oviposition bout (Pont 1979). Yet published de- in England were huge, containing up to possibly scriptions of mating only mention copulations follow- 100,000 Sepsis fulgens Meigen ßies (Pont 1987). Ag- ing oviposition, so the many observations of matings gregations this large are not often encountered, how- by females just after oviposition leave unanswered the ever, and detailed behavioral observations of ßies in question of where a femaleÕs Þrst copulation occurs them have never been made. It appears that most (Hafez 1947, Foster 1967, Parker 1972a, Ward 1983, individuals in these aggregations neither feed nor en- Ward et al. 1992, Zerbe 1993, Allen and Simmons 1996, gage in sexual interactions (Pont 1979, 1987). Another Blanckenhorn et al. 1999, Schulz 1999). A possible possible site of mating is a smaller group, such as the 0013-8746/00/0966Ð0971$02.00/0 ᭧ 2000 Entomological Society of America July 2000 EBERHARD:REPRODUCTION IN M. armillata 967 ßies associated with resources such as food or water. made when the female fulÞlled two conditions: she Katja Schulz (personal communication) reported ag- was found in an aggregation in which 90Ð100% of the gregations of S. neocynipsea with a few S. punctum males that were collected on the same or previous days along streams and in moist meadows in the mountains were M. armillata; and she was larger than the median of Arizona, and has also seen mating in several species size of all females collected from the same site. Be- of Sepsis at older dung, which serves for feeding but cause the other species found in these aggregations, M. not oviposition. Silva (1993) mentioned that adults of mitis, is smaller on average than M. armillata, selection Palaeosepsis sensu latu (includes Archisepsis and Mi- of larger females for dissection made it very probable crosepsis) have been captured on grasses, apparently that they were M. armillata. away from dung or carrion. Females to be dissected were either placed in 70% The current study uses behavioral observations and ethanol and dissected within a day, frozen and then dissections to determine both the reproductive con- dissected in saline solution, or placed in a refrigerator dition (ovary development and spermathecal con- at Ϸ5ЊC (where they were completely immobile) for tents) and the recent feeding history (intestine con- 1Ð2 d and then dissected in saline. I noted the follow- tents) of females of M. armillata captured away from ing: (1) the relative volume and color of the contents oviposition sites. Additional fragmentary data are of the enteric cecae or crop, and of the two loops of given for M. mitis (Curran) and A. discolor (Bigot). middle intestine lying between the two ovaries; (2) the contents of the vagina (spermatophore, egg, male genitalia, empty); (3) the length of a large egg in the Materials and Methods ovary; (4) the relative degree of Þlling of the large and Observations were made in pastures and early sec- small spermathecae with sperm (judged by isolating ond growth (shrubs and small trees) near San Antonio the spermathecae on a slide, squashing them under a de Escazu (elevation 1,400 m), San Jose´ Privince, coverslip, and observing sperm density under a com- Costa Rica between December 1998 (just before the pound microscope); and (5) the relative development beginning of the dry season) and the end of April 1999 of the ovaries, including both relative sizes of eggs and (Ϸ2 wk into the next wet season). Brief observations of the ovary itself (judged on the basis of the range of were also made on 10 and 11 April Ϸ5 km W of Atenas, development seen in dissections for a previous study) Alajuela Province, Costa Rica. Counts of ßies were (Eberhard and Huber 1998). Ovaries of females col- performed while walking or crawling very slowly to lected while copulating on dung and that had just laid minimize the number of ßies disturbed. Only ßies a clutch of eggs were judged to be Ϸ20% developed. Ϸ0.5Ð1.5 m ahead were counted, and ßies that were Females with no sperm in either spermatheca were seen landing (some of these were undoubtedly stirred presumed to be virgins. Sample sizes differed for dif- up by my movement) were not counted. The ßiesÕ ferent structures, as some structures were not exam- tendency to spend nearly all their time on the upper ined in some dissections. Means are followed by Ϯ1 rather than lower surfaces of leaves or other planar SD. surfaces, and to fan their wings and walk about actively made it likely that this survey technique included the Results large majority of the ßies present, despite their small size (Ϸ3Ð4 mm long). Flies were collected either by I found six aggregations of M. armillata that con- aspirating individuals or by swinging an insect net over tained from Ϸ50 to Ͼ2,000 individuals. Most ßies in their resting place. aggregations were on the upper surfaces of more or Aggregations were distinguished from scattered in- less horizontal leaves Ͻ15 cm above the ground. Many dividuals somewhat arbitrarily. An aggregation in- species of plants were occupied, and leaf sizes varied cluded a central area where there were several leaves widely (from Ͻ1toϾ1,000 cm2). Maximum densities with at least 3Ð4 ßies per leaf, and where interactions were only 1Ð2 ßies per square centimeter, and oc- between individuals occurred frequently. It is possible curred only on a few, relatively small leaves. The that some ßies judged to be scattered rather than in an largest aggregation was spread along Ϸ30 m of a small aggregation actually belonged to an aggregation stream. Although some aggregations persisted for whose center was missed. My search for ßies was more than a month, they were not stable at a small focused on the upper surfaces of leaves Ͻ1 m above scale.
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    PROVISIONAL ATLAS OF THE REF sis.11L4 SEPSIDAE(DIPTERA) OF THE BRITISH ISLES ADRIAN PONT BIOLOGICAL RECORDS CENTRE NATURAL ENVIRONMENT RESEARCH COUNCIL Printed in Great Britain by Middletons of Ambleside C NERC Copyright 1987 Published in 1987 by Institute of Terrestrial Ecology Merlewood Research Station Orange-over-Sands Cumbria 1411 7H/4 ISBN 1 870393 00 7 The Institute of Terrestrial Ecology was (CIE) established in 1973, from the former Nature Conservancy's research stations and staff, joined later by the Institute of Tree Biology and Culture Centre of Algae and Protozoa. ITE contributes to, and draws upon, the collective knowledge of the 14 sister institutes which make up the Natural Environment Research Council, spanning all the environmental sciences. The Institute studies the factors determining the structure, composition and processes ef land and freshwater systems, and of individual plant and animal species. It is developing a sounder scientific basis for predicting and modelling environmental trends arising from natural or man-made change. The results of this research are available to those respensible for the protection, management and wise use of our natural resources. One quarter of ITE's work is research commissioned by customers, such as the Department of Environment, the European Economic Community, the Nature Conservancy Council and the Overseas Development Administration. The remainder is fundamental research supported by NERC. ITE's expertise is widely used by international organizations in overseas projects and programmes of research. The Biological Records Centre is operated by ITE, and receives financial support from the Nature Conservancy Council. It seeks to help naturalists and research biologists to co-ordinate their efforts in studying the occurrence of plants and animals in the British Isles, and to make the results of these studies available to others.