Competition in Natural Populations of Mycophagous Drosophila

Competition in Natural Populations of Mycophagous Drosophila Author(s): David Grimaldi and John Jaenike Source: Ecology, Vol. 65, No. 4 (Aug., 1984), pp. 1113-1120 Published by: Ecological Society of America Stable URL: http://www.jstor.org/stable/1938319 Accessed: 12/10/2010 14:02 Your use of the JSTOR archive indicates your acceptance of JSTOR's Terms and Conditions of Use, available at http://www.jstor.org/page/info/about/policies/terms.jsp. JSTOR's Terms and Conditions of Use provides, in part, that unless you have obtained prior permission, you may not download an entire issue of a journal or multiple copies of articles, and you may use content in the JSTOR archive only for your personal, non-commercial use. Please contact the publisher regarding any further use of this work. Publisher contact information may be obtained at http://www.jstor.org/action/showPublisher?publisherCode=esa. Each copy of any part of a JSTOR transmission must contain the same copyright notice that appears on the screen or printed page of such transmission. JSTOR is a not-for-profit service that helps scholars, researchers, and students discover, use, and build upon a wide range of content in a trusted digital archive. We use information technology and tools to increase productivity and facilitate new forms of scholarship. For more information about JSTOR, please contact [email protected].

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Ecology, 65(4), 1984, pp. 1113-1120 © 1984 by the Ecological Society of America

COMPETITION IN NATURAL POPULATIONS OF MYCOPHAGOUS DROSOPHILA1 DAVID GRIMALDI2 AND JOHN JAENIKE3

Departmentof Biological Sciences,State Universityof New York, Binghamton,New York13901 USA Abstract. In the northeasternUnited States,individualmushroomscommonly harborthe larvae of up to four species of Drosophila(D.falleni, D. recens,D. putrida,and D. testacea),as well as larvae of crane flies (Tipulidae),wood gnats (Anisopodidae),and other, small flies. An experimentshowed that larvaeof these speciescommonly exhaustthe food in singlemushroomsundernaturalconditions. Supplementalmushroomincreasedsurvival to adulthoodin three Drosophilaspecies and resultedin largeradult flies. There was substantialvariationamong individualmushroomsin the degreeof food depletion by larvae;while some mushroomswere completelydevoured, others appearedto provide more than enough food for the larvae. Mean body sizes of Drosophilathat maturedin naturewere similar to those of flies rearedin our experimentswithout supplementalfood, which suggeststhat resourcedepletionand larvalcompetitionare common in naturalpopulationsof these species. (While the evidence for resourcelimitationis compelling,our methodsdo not allow us to distinguishbetween intra- and interspecificcompetition.) As a result, fitness of flies in nature should vary greatlyas a function of the amount of food available to larvae. We speculatethat low rates of parasitismallow mycophagousDrosophilapopulationsto depletefood resourcesmorecommonlythando phytophagous insects. Key words. bodysize; competition;density-dependentmortality;Drosophila;fecundity,mycophagous insects,populationregulation. INTRODUCTION

Natural populations of phytophagous insects are generally thought to be more influenced by weather, parasites and predators, and variable host plant qualities than by food limitation (Andrewartha and Birch 1954, Lawton and Strong 1981). This view is reinforced by observations of large numerical fluctuations in many insect species (e.g., Wolda 1978), and by the lack of apparent resource depletion (e.g., Hairston et al. 1960). Great fluctuations, however, do not preclude the potential importance of density-dependent resource limitation (Horn 1968, May 1977). It is entirely possible, for instance, that survival of larval insects may be strongly affected by food availability, while populations of adults, the stage generally censused, are largely influenced by weather. Thus, passive observations of populations are of limited usefulness in understanding the mechanisms of their dynamics. As stressed by Connell (1975), competition is best revealed by experimental manipulations of natural populations. Because of the discrete nature of their larval food resources and the ease with which these resources can be manipulated, mushroom-breeding insects are good subjects for such studies. Although many species of insects, principally Diptera, breed in fleshy fungi (Buxton 1960, Hackman and

Meinander 1979), it seems unlikely that they could specialize on nonoverlapping sets of mushrooms. Since mushroom fructification depends on rainfall and other variables, most species are quite unpredictable in their occurrence (Wilkens and Harris 1946, Richardson 1970). This unpredictability should favor polyphagy in mycophagous insects (Jaenike 1978a, Lacy 1984), although some mushroom-feeding drosophilids are moderately specialized on certain fungi that are rather predictable in occurrence (Shorrocks and Charlesworth 1980, 1982, Lacy 1984). We have seen some mushrooms completely devoured by these insects: resource depletion can be acute. This occasional crowding and substantial niche overlap may cause mycophagous insects to compete both intra- and interspecifically. By manipulating mushrooms in the field we have learned that the larvae of mycophagous Diptera often deplete their food resources, and that this causes immature mortality and reduced adult body size. METHODS

Mushrooms infested with fly larvae were collected at three sites in Broome County, New York: (1) a wet, low-lying hemlock (Tsuga canadensis) wood in Chenango Valley State Park that was studied in 1981 and 1982; (2) a mixed hemlock and beech (Fagus grandifolia) wood on Foley Road in the town of Vestal, studied in 1981; and (3) a mixed deciduous wood in the ' Manuscriptreceived4 January1983;revisedandaccepted State University of New York-Binghamton Nature 13 June 1983; final version received 21 July 1983. Preserve, studied in 1982. Flies to be used for adult 2 Presentaddress:Departmentof Entomology,CornellUni- size measurements were collected in banana traps from versity, Ithaca,New York 14853 USA. 3 Present address: Department of Biology, University of May through September in both years. Mushrooms were collected from July through early September. They Rochester,Rochester,New York 14627 USA.

DAVID GRIMALDIAND JOHN JAENIKE

1114 TABLE

Ecology, Vol. 65, No. 4

1. Numbersof adult flies that emergedfrom control and supplementedhalves of mushrooms. Number of flies (x + SE)

Species Drosophila falleni D. recens D. putrida D. testacea Limonia triocellata Sylvicola alternatus

Controlhalf 12.7 6.5 3.1 12.5 2.6 6.8

+ 3.2 + 2.6 + 0.3 + 3.8 + 1.1 + 2.6

Supplementedhalf 16.5 6.4 6.6 15.2 4.3 20.0

+ + + + + +

2.8 1.5 1.4 4.1 1.3 11.0

z* -2.82 -1.39 -2.65 -1.57 -1.21 -1.27

P

Nu of Number mushrooms

.002 .079 .004 .057 .113 .102

45 32 34 32 17 10

* Wilcoxon matched-pairssigned-rankstest. were most abundant during and after periods of warm, wet weather. Fifty-six experimental mushrooms (Amanita spp. [24], Russula spp. [27], Cortinarius sp. [2], and Entoloma lividum [3]) were sliced into equal halves longitudinally through the cap and down the stipe. These halves were placed separately in fly-proof containers on dampened leaf litter, collected from around the mushroom in the field, all over a bed of sand (for drainage). "Control" halves of mushrooms were untreated; to the "supplemented" halves, we added mushroom of the same species that had been frozen at - 80°C to kill resident larvae. This approximately doubled the wet mass of food available to larvae. In 1981, each mushroom half was placed in an aluminum tray, and nylon-organdy mesh cones were placed over each mushroom half. The base of a cone was sunk into the sand to prevent escape or invasion of flies. The trays were kept on a lawn in the shade of a tree under natural weather conditions. In 1982, mushroom halves, with the litter and sand, were separated into either gauze-covered plastic specimen cups (for smaller mushrooms) or 1-L glass mason jars, and kept on an open patio. A wooden overhang shaded the mushrooms throughout the day. Mushrooms were not exposed to rain in 1982, and so were lightly misted with water every other day to prevent desiccation. The experimental mushrooms were checked regularly for emergent adults, the vast majority of which were the dipterans Drosophila falleni, D. recens, D. putrida, D. testacea (Drosophilidae), Limonia triocellata (Tipulidae), and Sylvicola alternatus (Anisopodidae). After the cuticle had hardened, emergent flies were preserved in 70% ethanol. For each species, the thorax lengths (from the anterior margin to the tip of the scutellum) of 10 individuals of each sex (if available) from every mushroom half were measured with an ocular micrometer at 30 x. We thus have for individuals raised under two conditions (control halves and food-supplemented halves of mushrooms) measures of: (1) relative survival to adulthood, based on the numbers of flies that emerged from the mushroom halves; and (2) adult body size of these flies, as measured by thorax length, which is highly correlated with ovariole number, and thus potential fecundity, in females (Tantawy and Vetukhiv 1960, Atkinson 1979a).

The quality of fresh vs. frozen mushroom tissue as a food source was assessed by raising recently collected stocks of Drosophila falleni, D. recens, and D. putrida on commercial mushroom (Agaricus bisporus). For each species, 10 cultures for each of the two substrates were set up by placing 2-g pieces of mushroom cap, either fresh or previously frozen at -80°, onto cotton plugs in 26-mL (7-dram) vials. Three females per vial were allowed to oviposit for 24 h and then removed. The cultures were maintained at 21° and 70% RH. To prevent food shortages, additional mushroom was added when larvae had consumed most of what was provided initially. After flies emerged, they were preserved in ethanol. For each of the 10 vials of an experimental treatment, the thorax lengths of 20 males and 20 females of each species were measured. Finally, the size distribution of wild-caught flies was compared with that of flies reared from control vs. supplemented halves of mushrooms. Smaller wildcaught flies may indicate food shortage for larvae in nature. Voucher specimens of Diptera reared from mushrooms and the wasps parasitizing them were deposited in the Corell University Insect Collection, Ithaca, New York. RESULTS

For five of the six common species of Diptera, more individuals emerged from the supplemented than the control halves of mushrooms (Table 1). Differences in emergence rate between treatments were tested with Wilcoxon's matched-pairs signed-ranks test (Siegel 1956), where the paired observations were the number of flies of a species that emerged from each of the two mushroom halves. The probability levels for rejecting true null hypotheses of no treatment difference were lowest for D. falleni and D. putrida. On average, over twice as many D. putrida emerged from the supplemented as from the control halves. For D. falleni and D. testacea, between 20 and 30% more flies emerged from the supplemented halves. Thus, in natural conditions many more eggs are laid and hatch than can mature on the amount of food in each mushroom. Larvae of mycophagous Diptera can deplete food sufficiently to reduce their survivorship substantially. Although resource limitation can have a significant

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COMPETITION IN DROSOPHILA

August 1984 2. 0

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D.recens r =.71

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FIG. 1. Relationship between number of emergent Drosophila (N) in control vs. supplemented halves of mushrooms collected from the field. Numbers have been log transformed to reduce scatter; mushrooms for which N= 0 or 1 have been plotted as log (N) = 0. Points below dashed lines represent mushrooms in which the number of emergent flies was greater in the supplemented halves.

effect on survivorship, much of the variance among mushrooms in the numbers of flies that emerged remains unexplained (Fig. 1). If all mushrooms were infested at similar larval densities (per gram of mushroom tissue) and if survivorship were a linear function of larval density, then one might expect the number of flies that emerged from the control half of a mushroom to be highly correlated with the number that emerged from the supplemented half. The correlations between these numbers, although positive and significant (Fig. 1), are actually quite low. In many mushrooms, flies of a given species emerged only from the supplemented halves; the control halves appeared to have been completely devoured, and apparently no larvae obtained enough food to complete development. In some mushrooms approximately equal numbers of flies emerged from both halves, suggesting that food was not limiting in these. In a few, more flies

emerged from the control halves, probably as a result of sampling error (if the two halves did not initially contain equal numbers of larvae or eggs) or because the added mushroom tissue was less suitable for development, as might be the case if it harbored a deleterious yeast or bacterium. Finally, in some mushrooms only one fly emerged from the control and supplemented halves combined; these are represented by points at the origins of graphs in Fig. 1. Perhaps an itinerant female deposited a single egg on a mushroom she perceived as crowded or otherwise unsuitable and then moved on. In any case, the large variance among mushrooms in the degree of resource limitation may facilitate the coexistence of these drosophilids (see Shorrocks et al. 1979), and thus calls for further study. Adults from supplemented halves were significantly larger than those from the control halves, as determined by t tests for paired comparisons (Sokal and


1116


Sizes of flies from control (C) and supplemented(S) halves of mushrooms.Comparisonsby t test paired.Degrees of freedomfor t (=n - 1 mushrooms)usuallyless than numberof mushroomswherea particularspecies was found, since individualsof a sex did not always emergefrom both halves of a mushroom.

TABLE 2.

Number of

Mean thorax length (mm) Species D. falleni D. recens D. testacea D. putrida

L. triocellata S. alternatus

mushrooms

Sex M

Control 1.05

Supplemented 1.10

(C/S) 33/42

t, 2.75**

df 29

F M F M F M

1.15 1.01 1.11 .90 1.06 .80

1.24 1.09 1.18 .97 1.11 .84

33/39 21/33 17/18 19/24 25/27 20/21

2.70*** 4.75*** 3.00* 7.50*** 4.33*** 2.20*

27 14 11 16 23 15

F M F M

.94 1.77 1.88 1.29

.99 1.93 1.98 1.41

21/21 8/10 11/10 6/10

3.60** 2.83* 0.77 7.08***

15 6 6 5

F

1.19

1.35

7/9

6.44***

6

* P < .05, ** P < .01, *** P < .001.

Rohlf 1981), where the data were the mean sizes of flies of a given sex and species that emerged from the two halves of a mushroom. This was true for both sexes of all six species (Table 2). Since a control experiment showed no differences between the sizes of flies raised on fresh vs. frozen mushroom tissue (Table 3), the largersize of adults reared from the supplemented halves was probably a function of food quantity, not quality. Drosophila thorax lengths were also studied by twoway analyses of variance, with the main effects being experimental treatment (control vs. supplemented halves of mushrooms) and mushroom genus (Amanita vs. Russula). Such analyses should reveal not only a general effect of competition, but also whether different kinds of mushrooms vary in their suitability for larval development, assuming the larvae are genetically similar with respect to size. Furthermore, a significant interaction term would show that the intensity of competition differed between Amanita and Russula mushrooms. The analyses show, as expected, that the experimental treatment contributed substantially to overall size variation in both sexes of all four species

TABLE3. Body sizes of Drosophila raised on fresh vs. frozen Agaricus bisporus mushrooms. Analyses of variance were carried out on mean sizes of flies from each of 10 cultures per treatment.

Species

Sex

Mean (+ SE)thorax length (mm) Fresh Frozen mushroom mushroom

D. falleni

M F M F M F

1.03 1.15 1.05 1.16 0.78 0.92

D. recens D. putrida

+ + + + + +

0.01 0.01 0.01 0.01 0.01 0.01

1.01 1.15 1.07 1.15 0.76 0.90

+ + + + + +

0.01 0.01 0.01 0.01 0.01 0.01

(Table 4). But for only one species, D. recens, were individuals significantly affected by the mushroom genus in which they developed; flies emerging from Amanita mushrooms were 6% larger than those from Russula. emerging Finally, neither sex of any species showed a significant interaction between mushroom genus and experimental treatment on body size. Thus, levels of larval competition appear similar in these two genera of fungi. This somewhat surprising outcome is probably the result of our deliberately choosing mushrooms known to be commonly utilized by Drosophila and thus likely to be crowded with larvae. Had we included mushroom taxa that are only rarely used by flies, we would have found more variation among them in levels of competition. Banana-trapped samples of adult Drosophila from natural populations in Broome County showed that

F ratios indicatingsources of body size variation in Drosophila.Treatment= controlvs. supplementedhalves of mushrooms(1 degree of freedom);mushroom= Amanita vs. Russula (1 df); interaction = mushroom x treatment (1 df). Based on two-way analyses of variancefor each species and sex of unweightedmean thorax lengthsof flies from various mushrooms.

TABLE 4.

Species D. falleni

F ratio

P

2.00 0.50 4.00 1.11 3.00 4.00

>.10 >.10 >.05 >.10 >.10 >.05

D. recens D. testacea D. putrida

Sex M F M F M F

Sourceof variation Error Interdf Treatment Mushroom action F value 64 9.67** 3.21 0.00 62 16.40*** 0.77 0.44 40 22.56*** 12.83*** 0.04 31 4.56* 8.14** 0.89 33 14.64*** 2.80 0.02 40 12.43*** 3.14 0.63

M

31

3.59

2.62

0.76

F

31

5.92*

0.23

0.00

* P < .05, ** P < .01, *** P < .001.

COMPETITIONIN DROSOPHILA

August 1984

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1117

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N=149

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1064

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1140

1231

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N=85

.

10-

-

675

790

92

1034

675

790

912

1034

821

912

1003

Thorax length (pm) FIG.2. Frequencydistributionsof Drosophilabody size, as measuredby thorax length. Open bars representflies bred from supplemented halves of mushrooms; shaded bars represent flies bred from either control halves or those captured at banana traps, as indicated. (N = number of flies measured.)

they, too, may have been food limited as larvae. The size distributions of these banana-trapped flies were much more similar to those of flies bred from the control, than to those from the supplemented halves of mushrooms (Fig. 2). Among flies bred from the supplemented halves, there was a significant excess of large individuals and a deficiency of small ones in comparison to the wild-caught flies, as determined by chisquare analyses (Table 5). We tentatively conclude, therefore, that the size distribution of wild flies reflects the operation of larval competition for resources in these populations.

desiccation tolerance (Levins 1969, Parsons 1970, Barker and Barker 1980), male mating advantage (Ewing 1964), and female fecundity (Tantawy and Vetukhiv 1960, Atkinson 1979a). In the four species of

5. Chi-squareanalyses comparingbody size distribution of wild-caughtDrosophilato that of flies bred from control or supplementedhalves of mushrooms.Some size intervals were combined so that in all cells the expected numberof flies was >5.

TABLE

DISCUSSION

Our results demonstrated that at natural densities, larvae of mycophagous Diptera frequently experienced a shortage of food due to competition. This resource limitation affected both the probability of larval survival and the body size of emergent adults, thus paralleling results on laboratory populations of Drosophila melanogaster (Bakker 1961). The reduction in body size can have deleterious effects on a number of components of fitness in Drosophila, including lifespan (Pearl and Parker 1924, Tantawy and Vetukhiv 1960),

Species D. falleni D. recens D. testacea D. putrida

Comparison Wild vs. Wild vs. control supplemented Sex df df x2 x2 4 4 M 20.9*** 58.1*** F 11.0* 3 49.2*** 3 4 4 M 10.6* 33.1*** F 0.9 3 16.9*** 3 M 3 60.0*** 2.8 3 F 7.8 3 61.3*** 3 M 6.1 3 0.9 3 F

*P < .05, *** P < .001.

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logiothoraxlength(,um) FIG.3. Female ovariole number(per ovary) as a function of body size (thoraxlength)in Drosophila. Drosophila considered in this study, there was a very high correlation between ovariole number and thorax length (Fig. 3). Thus, resource depletion under natural conditions can adversely affect an individual's fitness. It is worth noting that reduced size was not limited to just the flies bred from the control halves of mushrooms in our experiments, but characterized wildcaught adults as well. It may be that at times other than the two years of this study, flies could experience much less or much more competition. We doubt, however, that our data are exceptional, since neither flies nor mushrooms were particularly rare or abundant during this study. These data signify the rich and varied possibilities of larval competition for food in these mycophages. One would expect, then, that females should be able to locate as quickly as possible mushrooms that are suitable for oviposition. In fact, they may often oviposit on mushrooms in the "button" stage, as evidenced by the occasional occurrence of the third-instar Drosophila larvae in isolated mushrooms on the very day the mushrooms appeared. In addition, one might expect larvae to respond physiologically to crowding; perhaps the reduced size of flies in nature reflects adaptive plasticity in food-limiting conditions. Finally, any species that can tolerate specific fungal toxins may be able to breed in mushrooms that are relatively unutilized. For instance, we have bred many individuals of several Drosophila species from various species of

Amanita mushrooms, a genus notorious for the variety of toxins it produces, some of which are potentially lethal to Drosophila (Jaenike et al. 1983). However, among the mushrooms in which they are known to breed, the flies Limonia and Sylvicola rarely use Amanita (Buxton 1960, Hackman and Meinander 1979, Shorrocks and Charlesworth 1980), and we did not rear a single individual of these flies from such mushrooms. Perhaps their larvae cannot tolerate the toxins in these fungi. Whatever the reason, Drosophila larvae feeding in Amanita mushrooms are free of at least one source of potentially serious competition. Our experimental method does not allow us to assess the relative intensities of intra- and interspecific competition. It may be that at rather low levels of infestation, larvae of the various species could feed on different parts of a mushroom, in which case any competition would be primarily within species. At high larval densities, however, mushrooms become amorphous, and it seems unlikely that this resource could be partitioned among species. In such cases, competition most likely occurs among species as well as within them. The operation of larval competition has been inferred (but not experimentally demonstrated) in several other species of Drosophila, including the flowerbreeding D.flavopilosa of South America (Brcic 1966), Cheirodendron leaf-breeding drosophilids of Hawaii (Mangan 1978), the cactus-breeding species of the So-

August 1984

COMPETITION IN DROSOPHILA

noran Desert (Fellows and Heed 1972), D. melanogaster in an English fruit market (Atkinson 1979b), and D. athabasca and D. affinis in Maine (Jaenike 1978b). In all of these studies, however, the negative correla-

tions found between the number or body size of a particular Drosophila species and its putative competitor could also be attributed to environmental conditions favoring one species or the other, independent of competition. Our demonstration that mycophagous Diptera may be subject to larval competition raises what seems to be a paradox. That is, why do these insects, which breed in ephemeral and unpredictable resources, become so much more crowded as larvae than many phytophagous species, which feed on resources of more predictable occurrence (leaves) (Lawton and Strong 1981, Strong 1982)? A possible answer may be found in the rates of parasitism these species suffer. Phytophagous insects are often heavily parasitized; parasitism rates of 40-90% are not uncommon (e.g., Askew and Shaw 1974, Lawton and McNeil 1979, Faeth and Simberloff 1981). These species, then, may be kept well below the environmental carrying capacity, and thus rarely experience competition for food. In the present study, mycophagous Drosophila were found to be parasitized by several species of wasps: two Aspilota and one Phaenocarpa species (Braconidae), and two species of Kleidotoma (Cynipidae: Eucolinae). However, the fraction of larvae they parasitized was < 1%. If mushrooms are unpredictable resources for mycophagous Drosophila, think how much more unpredictable must be the occurrence of drosophilids at a suitable stage of development for the parasitic wasps. Rates of parasitism on these Drosophila probably reflect the very low rates of discovery by the parasites. D. flavopilosa, a South American species, is known to be parasitized by just two species of wasps: a braconid (Opius trimaculatus) and a eucoiline cynipid (Ganaspis sp.). However, the breeding site of this fly is quite predictable in occurrence; it breeds in flowers of Cestrum shrubs, which produce hundreds of flowers continuously for about eight months of the year. Since D. flavopilosa breeds in these flowers throughout this period, the larvae would seem to be a predictable resource for the parasitic wasps. As a result, rates of parasitism may reach 50% in this species (Bmcic 1966). Even if mushrooms were predictable, larvae inhabiting them might be subjected to low rates of parasitism because mycophagous insects occur within their food substrate, presumably making them harder to find and less accessible to parasitoids, whereas leaf-feeding insects, in their effectively two-dimensional world, probably are more apparent and easier to oviposit upon. Our results and those of others show that in Drosophila, and probably in other insects, both parasitism and competition may significantly affect population size. However, the notion that competition is most

1119

important in stable environments (Pianka 1970) may have to be reevaluated. ACKNOWLEDGMENTS

We are gratefulto Jake Lehn for permissionto collect flies and mushrooms from the Binghamton, New York, Camping and Hunting Club's preserve. For their extremely useful comments on this paper, we thank Donald Strong, Mark Lomo-

lino, John Titus, Ernst Mayr, Robert Lacy, and two anonymous reviewers. Paul Marsh and A. S. Menke of the Systematic Entomology Laboratory of the United State Department of Agriculture (Beltsville, Maryland) kindly identified the braconids and cynipids. This research was supported by a Sigma Xi Grant-in-Aid-of-Research to D. Grimaldi and by National Science Foundation Grant DEB 80-08574 to J. Jaenike. LITERATURE CITED

Andrewartha, H. B., and L. C. Birch. 1954. The distribution and abundance of animals. University of Chicago Press, Chicago, Illinois, USA. Askew, R. R., and M. R. Shaw. 1974. An account of the Chalcidoidea (Hymenoptera) parasitizing leaf-mining insects of deciduous trees in Britain. Biological Journal of the Linnean Society 6:289-335. Atkinson, W. D. 1979a. A comparison of reproductive strategies of domestic species of Drosophila. Journal of Animal Ecology 48:53-64. 1979b. A field investigation of larval competition

in domestic Drosophila.Journalof Animal Ecology48:91102.

Bakker,K. 1961. An analysis of factors which determine success in competition for food among larvae of Drosophila melanogaster. Archives Neerlandaises de Zoologie 14:200281. Barker, J. F., and A. Barker. 1980. The relation between body size and resistance to desiccation in two species of Zaprionus (Drosophilidae). Ecological Entomology 5:309314. Brncic, D. 1966. Ecological and cytogenetic studies of Drosophilaflavopilosa, a Neotropical species living in Cestrum flowers. Evolution 20:16-29. Buxton, P. A. 1960. British Diptera associated with fungi. III. Flies of all families reared from about 150 species of fungi. Entomologists' Monthly Magazine 96:61-94.

Connell,J. H. 1975. Some mechanismsproducingstructure in natural communities: a model and evidence from field experiments. Pages 460-490 in J. M. Diamond and M. L. Cody, editors. Ecology and evolution of communities. Belknap Press, Harvard University, Cambridge, Massachusetts, USA.

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