J. Anim. Ecol.

(1977), 46, 783-798

NON-EQUILIBRIUM 'ISLAND' COMMUNITIES: DIPTERA

BREEDING IN DEAD SNAILS
BY R. A. BEAVER

School of Biological Sciences, Universiti Sains Malaysia, Penang, Malaysia

INTRODUCTION
The classification of habitats devised by Elton & Miller (1954) includes in its 'general
system' a variety of habitats such as dying or dead wood, dung and carrion. These
habitats have a number of charactersin common. They are small and distinct, and consist
largely or solely of decaying organic matter (Elton 1966). They form discrete habitat
units or ecological 'islands' scattered through other habitats. Communities develop
within them that are characterized by the absence of green plants and the presence of a
diverse fauna of arthropods as well as multitudinous microorganisms. These communities
have at their disposal a limited amount of energy, which is gradually used up by the
activities of the community members. The successional changes that take place in these
'islands' are usually rapid, occurring on a scale of days (or even hours) rather than years.
The changes are largely the results of the activities of the organisms themselves. The
physical environment often has relatively'little direct effect. Because of the rapidity of the
successional changes, there is usually only a single generation of any species (excluding
microorganisms) before the habitat unit has become either unsuitable or exhausted.
Dispersal is then necessary to find other suitable units for colonization. These ecological
'islands' are not self-sustaining, and the communities in them can never reach an equilib-
rium at least on the scale of the individual 'island'. Thus they differ in several respects
from the geographical islands considered by MacArthur & Wilson (1967), the habitat
islands on the mainland (Vuilleumier 1970; MacArthur 1972), and the host plants con-
sidered as islands by Janzen (1968, 1973).
Dead snails form small habitat units of the type considered above.; They are usually
soon exploited by a variety of Diptera. The fly larvae feed on and complete their develop-
ment within a single snail. Eachisnail is essentially an isolated unit. Interchanges with the
external environment are usually limited to the import of Dipteran eggs (or larvae in the
case of the ovoviviparous Sarcophagidae), and the export of mature larvae, ready to
pupate in the soil, or of adult flies. The community that develops in the snail is short-
lived and each species normally has only a single generation before the food supply is
exhausted. The number of species and individuals is limited, compared to the communi-
ties of larger carrion, and it is possible-to make a complete census of all those attaining
the pupal or puparial stage. It is also easy to set up many replicate habitats and study the
variation among the communities in different snails in a small area and at different times
of the year.
This paper is concerned with the community in the dead snails from the aspect both of
the single snail and the set of snails exposed to attack at one time. It examines the patterns
of abundance of species and individuals among the snails, and successional and seasonal
changes in these patterns. It then looks at the effects of predation, parasitism and com-
petition on the communities. The life history strategies used by the different species and
783

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784 Non-equilibriumDipteran communities
the compromises involved are discussed, and the mechanisms by which the species persist
and coexist. The importance of heterogeneity, both in the spatial and temporal distribu-
tion of habitat units, and in the composition of their communities, to the dynamics of
the populations and communities is stressed. Much of the discussion should be applicable
to other carrion and dung communities. A future paper will compare the temperate zone
communities studied here with those found in dead snails in tropical Malaysia.

MATERIALS AND METHODS

The snail used in this study was Cepaea nemoralis(L.) (Helicidae), which is about 2O0-2-2
cm in diameter when mature. Collections of snails were exposed to attack at intervals
over a period of 10 months among the dune slacks of Newborough Warren, Anglesey.
Details are given by Beaver (1972). Collection 2 of that paper has been omitted here
because it was made in a different part of Newborough Warren where conditions may
have been somewhat different. The snails were chosen to be of as similar a size as possible
so that variations in the amount of food available in each were reduced to a minimum.
The length of time that the snails were exposed to attack was varied according to the rate
of decay of the snail. In summer, this is relatively fast and after about I week, the snails
are no longer attractive to adult flies for oviposition. Collections 1-5 were exposed for
approximately 1 week. Collection 6, taken in September when temperatures were lower,
was divided into two halves, exposed for 1 and 2 weeks respectively. Collection 7,
exposed during winter, was left out for 1 month, but only 30% of the snails were attacked.
In the other collections, the percentage was 95-100%. After exposure, the snails were
kept in the laboratory and the adult flies bred out. The numbers of pupae or puparia of
each species are used rather than the number of adults. A complete list of the eighteen
Dipteran species bred can be found in Beaver (1972). Species mentioned in the present
paper are listed in the Appendix. Two Hymenopteran parasites are also included in some
of the analyses. Temporary visitors, mainly Coleoptera, which did not breed in the snails
are excluded.
Various aspects of the biology of the Diptera bred have been considered earlier
(Beaver 1969, 1972, 1973). Most of the species over-winter as pupae or puparia. The
adults emerge in late spring and there is a series of generations through the summer. The
length of the development period of a number of species (Beaver 1972) suggests that there
are likely to be 3-5 generations of most species during the breeding season.
The spatial distribution of the snails that died naturally in the dunes at Newborough
Warren was very patchy. Aggregations were usually found in or near areas where Salix
repens (Linnaeus) was the dominant plant. The temporal distribution was also hetero-
geneous. In late spring and early summer, large numbers of Cepaea die in the sand
dunes at Newborough Warren. There is thus an ample supply of breeding material for
the Diptera. The availability of dead snails decreases later in the year, but the majority
of species bred can also breed in other carrion, and sometimes in other decaying organic
matter (Beaver 1969, 1972). Dead birds, especially gulls which nest in the dunes, and
small mammal corpses may be a more abundant resource than the snails at some periods
of the year.
It is possible to look at the communities from two points of view. The 'general' or
'regional' viewpoint (Lloyd & Ghelardi 1964) considers the whole collection as a single
sample from the total fauna of the area and parameters are obtained for the collection
considered as a whole. The 'local' viewpoint (Lloyd & Ghelardi 1964) considers each

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 R. A. BEAVER 785
snail as;a replicate habitat. Using this viewpoint, it is possible to apply standard statistical
tests to the community parameters obtained for the individual snails of each collection.
This can be done since the snails formed discrete habitat units, were all of the same size,
anidall completely censused.
I have generally assumed that all snails are potentially inhabitable by all species found
to havesattacked at least one snail in the area during the exposure period. It is known that
most saprophagous species are relatively indiscriminate in their choice of food (Elton
1966), and it seems unlikely that any of the snails was initially quite uninhabitable. There
remains the possibility that the presence of one species or a group of species in a snail
makes it uninhabitable by other species, or at least reduces the chance that they will
occupy it. However, in comparisons between ten of the commoner species, there were
only two species pairs which never occurred together in any snail, and in neither case was
the lack of association significant. Thus it seems preferable to include zero counts in the
analysis where snails were uninhabited.

PATTERNS OF ABUNDANCE
Some of the basic parameters of the collections are shown in Table 1. When the number
of species in the community is small, the commonly used measures of species diversity
do not distinguish between different species abundance distributions. For this reason,
relative abundance curves for each collection considered as a whole are given in Fig. 1.

Table l. Communityparametersfor the Diptera and their parasites bred from Cepaea
nemoralis at different times of year; (means are given + 1 S.E.)
No. weeks Total no. Total no. Mean no. Mean no.
Date of Collection collection No. of individuals species individuals species
collection no. exposed snails bred bred bred/snail bred/snail
3 March 7 4 28 33 3 1-18?0-57 0-36?0-12
16 May 1 1 35 244 7 7-00?0-80 1-34?0-12
12 June 3 1 33 360 6 10-91+1-94 1 09+0-08
18 July 4 1 43 789 11 18-35?2-93 2-79+0-22
28 July 5 1 29 473 12 16 31?3 30 : 3-14?024
15 Sept. 6(1) 1 15 180 8 1200?288 1-93?0-27
21 Sept. 6(2) 2 15 383 11 25 53?467 407?037

Several diversity indices have been calculated, but they do not add to the interpretation
of the data and are omitted.
May (1975) has discussed the different patterns of abundance found in communities,
and shown that for large or heterogeneous sets of species, a lognormal pattern of abund-
ance is to be expected as a mathematical rather than an ecological consequence of the
size or heterogeneity of the sets. In relatively small and homogeneous sets of species, the
fdistributionmay tend towards either a logseries distribution (as the statistically realistic
expression of the ideal geometric series) or MacArthur's ( 1960) broken-stick distribution.
In the former, the pattern of abundance is significantly less even than the lognormal, and
in the latter more even than the lognormal. The distributions shown in Fig. 1 clearly tend
towards the logseries or geometric series distributions. They are characterized by the
dominance of one or two species which make up at least 63% and sometimes more than
90/%of the community (Table 2). The dominance is particularlyL evident in collections 3,
4 and 7.

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786 Non-equilibriumDipteran communities
It must be realized that a species which is dominant in terms of numbers need not
necessarily dominate the utilization of the food supply. This is because the snail usually
contains species of widely differing size. Biomass is a better basis for comparisons of
resource utilization. Data are not available for these communities, but comparisons with
species of similar size found in tropical communities in dead snails (R. A.- Beaver,
unpublished observation), suggest that the average Sarcophaga weighs about 300 times
as much as the average Philosepedon or Limosina. Thus whenever Sarcophaga species
occur in a snail, they almost invariably strongly dominate the community in terms of
biomass. The only other species approaching their size in the communities in Cepaea was

2-0 - 7
4
6 (1) 6 (2)
.5 0~~~~~~~~~
0~~~~~~~~~

~~0~
9. 0

I.o 0 0 0
0~~~~~~~~~~~
1.0

10

Speciessequence
FIG. 1. Dominance-diversitycurves for Diptera
-in collections1-7.

Table 2. Degree of dominance(d Ni/NT x 100) of the two most abundant

species oJ Diptera in collections 1-7
Collection Species d Species d
1 Sarcophaganigriventris 65 3 Philosepedonhumeralis 15-2
3 Philosepedonhumeralis 90-3 Limosinaluteilabris 3-1
4 P. humeralis 70-8 Sarcophaganigriventris 10-8
5 Limosinaluteilabris 41-4 Philosepedonhumeralis 22-0
6(1) Philosepedonhumeralis 48-3 Sarcophaganigriventris 35 0
6(2) Limosinaluteilabris 45-7 S. nigriventris 25-1
7 Megaselia tenebricola 87-9 Unidentifiedsp. 9.1

Mtuscina assimilis, and this was-relatively infrequent. Some seasonal changes are
evident from Table 1. The mean number of individuals bred per snail shows a tendency
to increase throughout the summer from a minimum in winter. A similar trend is found
in the mean number of species bred per snail. This increase occurs even though the total
number of species bred, having risen in early summer, is effectively constant through
collections 4, 5 and 6(2), and suggests an increase in species packing within the snails.
(Comparison of collections 6(1) and 6(2) will be made later.) It will be noted that the
number of snails is not the same in all collections. This could result in a species-area
effect on the total number of species bred. However, since the distribution of species
abundances tends towards the logseries distribution, increases in area (= number of

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 R. A. BEAVER 787
snails)have relativelylittle effect ongthe total numberof species(May 1975).The two
parametersare not significantlycorrelatedin. the, collections.Variationsin the total
numberof individualsbetweencollectionsalso seem unlikelyto affectthe total number
of speciesbred,since the two parametersare not significantlycorrelated.The observed
changesare perhapsthe result of regional-increasesin the population-densitiesof the
flies duringthe severalgenerationsof the summer.-
Whittaker(1972)and May (I1975)point out that most fieldexamplesof approximately
geometric.series distributionsoccurin communities*with few species,andwhich-areeither
in an earlysuccessionalstageor in a harshenvironment.The-communitiesfoundin dead
snailsand similarhabitatsshow manycharacteristicsof communitiesin the earlystages
of succession,but the successionis always halted at an early stage.due to the rapid
exhaustionof the energysupply.Comparisonsof collections6(1) and 6(2), whichwere
exposed on-the same.day, but-taken into.the laboratoryafter I and 2'weeks respec-
tively, indicatethat successionalchangesoccurduringthe periodthat the snailsremain
attractivefor oviposition,-
althoughtheyaresmallrelativeto thosefoundin largercarrion
(Fuller1934;Elton 1966;Denno & Cothran1975;Lane 1975).Duringthe secondweek,
thereis a significantincreasein the meannumberof individualspresent(P <0-02), and
of speciespresent(P<0 001). It has been,shownpreviously(Beaver1972)that thereis a
significantincreasefrom collection6(1) to 6(2) in the numberof snails attackedby the
differentspecies.Analysisof the numbersof individualspecies(Beaver1972)showsthat
Limosina luteilabris,Fannia canicularisand the two parasitic Hymetoptera tend to attack
the snailsin the secondweek.The increasein the numberof Limosinaluteilabriswas sig-
nificantand led to dominanceof collection 6(2) by this species,whereasPhilosepedon
humeralis and Sarcophaga nigriventris were dominant in collection-6(1) (Table 2).
Numbersof the lattertwo speciesremainedt approximatelyunchanged.
Oneof the characteristicsof the communitiesof temporaryhabitatssuchas deadsnails
is their heterogeneity(Fuller 1934; Cornaby1974; Papp 1975, 1976).Althoughall the
snailsexposedat one timeforman apparentlyhomogeneousgroupinitially,considerable
differencesare soon foundbetweenthe communitiesof individualsnailsboth with regard
to the speciespresentand the relativenumbersof the species.Table 1 in Beaver(1972)
showsthat no speciesoccurredin all the snailsof a collection,and most speciesoccurred
in less than one-thirdof the snails.As in the-:dungcommunitiesstudiedby Papp(1976),
the species/habitat-unitmatrixfor each collectioncontains-largenumbersof zeros.
The distributionof the numbersof speciesper snailwas furtherinvestigatedusingthe
index of dispersion(Greig-Smith1964):.'
I = S2(n-1)/m
where S2 and m are the variance=.--andmean of the.distributionand n the numberof
observations.The indexis distributedapproximatelyas chi-squaredwithn-I degreesof
freedom.The distributionof species:was :foundnot to be significantlydifferentfrom
randomexpectationin collections4, 6(1) and 7, but significantly(P< 005)more regular
than randomexpectationin collections1 3, 5 and 6(2)0.This impliesthe occurrenceof
biologicalinteractionslimitingthe numberof speciesin at least somecollections. -(Note
that the actualspeciespresentvaryconsiderablybetweensnails;it is only their number
which is relativelyconstant.)The interactionscould take place betweenadults, leading
for exampleto the avoidance-byspeciesA of snailson whicheggshadbeenlaidby species
B-,or betweenlarvae,leadingto the 'local'extinctionof certainspecies.It is likely that
both types of interactionoccur.^

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788 Non-equilibriumDipteran communities
The spatial relations of the species can also be studied by investigating the occurrence
of associations, positive or negative, between pairs of species. Since the snails form dis-
crete habitat units, this can be done using contingency tables. The numbers of snails in
collections in which both of the compared species occurred have been used to calculate
values of chi-squared. The significance of chi-squared and the positive or negative
character of the associations is shown in Table 3. Three species, Philosepedonhumeralis,
Megaselia brevicostalis and Subhylemyia longula have no significant associations with
other species and presumably distribute themselves among the snails independently of
the occurrence of other species. The interpretation of significant positive and negative
associations is difficult, because several explanations are usually possible, and not enough
is known about the behaviour of the species to distinguish between them. For this reason,
only a few associations will be discussed.
Fannia canicularisand Limosina liteilabris are positively associated (though not signi-
ficantly) with nearly all other species, and significantly positively associated with each
other (Table 3). This association probably arises because both species prefer to oviposit

Table 3. Significance of chi-squared and kind oJ association for paiirs of

species occurring in two or three of collections 4, 5 and 6
Species 1 2 3 4 5 6 7 8 9 10
Philosepedon humeralis (1)
Megaselia brevicostalis (2) NS+ . . . .
Limosina luteilabris (3) NS+ NS+ . . . .
Sarcophaga hirticrus (4) NS- NS+ NS+ . . . .
S. nigriventris (5) NS- NS- NS+ * . . .
S. teretirostris(6) NS- NS+ NS+ *
Muscinaassimilis(7) NS- NS- NS- NS- NS+ * .
Fanniacanicularis(8) NS+ NS+ **+ NS- **+ NS- NS+
Subhylemyialongula(9) NS- NS- NS+ NS- NS+ NS- NS- NS+
Lasiommaoctoguttatum(10) NS+ NS+ NS+ NS- **+ NS- NS+ NS+

*P<005; **P<001; ***P<0001; NS, not significant; + positive association; - negative

association.

on snails which have been exposed for some days, and which have already been partly
broken down by other species (Beaver 1972).
There are highly significant negative associations between Sarcophaganigriventrisand
both S. hirticrusand S. teretirostris.These are all large, ovoviviparous and fast-developing
species, and probably exploit the food in a very similar way. The few available breeding
records (Beaver 1972) suggest that all are primarily associated with dead snails. (S.
nigriventris may be capable of successful parasitisation of living snails on occasion
(Cameron & Disney 1976).) Studies on larval competition (Beaver 1973) show that com-
petitive interactions are important in the ecology of the three species. A mechanism by
which such interspecific and intraspecificcompetition might be reduced has recently been
put forward by Bryant & Hall (1975). Using Musca domestica L., they showed that
within a few hours after a batch of eggs hatches, larval conditioning of the medium
occurs. The females avoid the conditioned medium and oviposition stops. A similar
mechanism may perhaps be expected in the Sarcophaga species studied here. It would
be of advantage to species which encounter competition in almost every generation in the
snails. The mechanism could come into action quickly since the flies are viviparous, and
lay small batches of larvae, and would presumably reduce or prevent further oviposition

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 R. A. BEAVER 789

by Sarcophaga species but not by other Diptera. Such a mechanism could explain the
negative correlations observed between S. nigriventris and the other two species of
Sarcophaga,but not the barely significant (X2 = 4-34) positive association between S.
hirticrus and S. teretirostris. Other explanations, based on larval'interactions, are also
possible, and experiments are required to resolve the problem.
The coefficients of variation of the numbers of individuals of the commoner species in
each collection are shown in Table 4. They indicate that there is almost always very
considerable variation between snails. However, in each collection, coefficients calculated
for all individuals in a snail are lower than for single species, with one exception in collec-
tion 5. This suggests that if one species is absent from a snail, or present in low numbers,
"itsplace is likely to be taken by another. It also suggests an upper limit to the number of
individuals able to coexist in one snail. This might be expected, given the limited amount
of food available.
The aggregation of the individ'ualsof different species can also be shown by use of the
index of dispersion. The significance of the results for the commoner species is shown in
Table 4. It is clear that the individuals of each species are almost always significantly

Table 4. Coefficientof variation(0 O) of numberof individualsand significance of index of

dispersionfor the commonerspecies of Diptera andjfr all individualstogether in collections
1-7
Species 1 3 4 5 6(l) 6(2) 7
Philosepedonhlimeralis 363*** 119*** 151*** 159*** 169*** 211***
Megaselia brevicostalis 500*** - 247*** 156* - - -
M. tenebricola - - - - 330*** 260*** 268***
Limosina luteilabris - - 208*** 248*** 314*** 99***
Sarcophaga hirticrus - 485*** 393** 142***
S. nigriventris 75*** 292*** 106*** 270*** 117*** 82*** -

S. teretirostris - 450*** 210*** 104*** - 215*** -

Muscina assimilis - - 202*** 254**
Fannia canicularis - - 322*** - 186*
Subhylemyia longula 361*** - - - 300** 179NS
Lasiomma octoguttatum - 395*** 280NS 211**
All individuals 68*** 102*** 104*** 109*** 93*** 68*** 254***
* P<005; ** P<001; * P<0001; NS, not significant;- not calculated(speciesabsent or present
only in,one snail).

aggregated in the snails, as are the individuals of all species considered together, despite
the lower coefficients of variation of -the latter.
The observed aggregation probably results largely from aggregated oviposition be-
haviour. It may be increased or decreased by larval interactions. Many, though not all,
Diptera breeding in carrion and dung lay their eggs in groups or batches (e.g. Muirhead
Thomson 1937; Hammer 1941; Alwar & Sashiah 1958; Kamal 1958; Norris 1964;
Greenberg 1973). The contagion of the resulting distribution may be further increased if
some species prefer to lay their eggs where eggs are already present (Bryant & Hall 1975),
although counteracting tendencies might also be expected (see above). Larval predation
may increase or decrease the observed aggregation depending on its intensity and its
relationship to previously existing aggregation patterns. Mortality resulting from com-
petition is-likely to be density-dependent and hence to reduce the observed aggregation.
Parasitism will have no effect if the larvae remain alive. The effects of predation, para-
sitism and competition on the community are discussed further in the next section.

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790 Non-equilibriumDiqteran communities
EFFECTS OF PREDATION, PARASITISM AND COMPETITION
Only two species of predator were recorded, Hydrotaea occulta and Muscina assimilis.
These are facultative predators in the last instar (Skidmore 1973). The former species
occurred only once; the latter was more common, and its effect on the community can
be investigated by comparing snails in which it was either present or absent. This ignores
the fact that any effect is likely to be more pronounced the more M. assimilis larvae are
present, but insufficient data are available to analyse this effect. Comparisons have been
made within collection 4 in which M. assimilis was more abundant than in other collec-
tions and occurred in eleven out of forty-three snails. The average number of M. assimilis
in the snails was 1P9,the maximum 4. The results are shown in Table 5. It is evident that
the presence of the M. assimilis larvae is associated with a significant decrease in the
number of individuals in each snail. These changes seem to result largely from a decrease
in the number of Philosepedonhumeralislarvae in the snails containing Muscina assimilis
(Table 5). Philosepedon humeralis was the most abundant species in the snails. Up to
seventy-six pupae were found in one snail (from which Muscina assimilis was absent),

Table 5. The effects of Muscina assimilis on the comnmunities of the snails in

collection 4; the probabilitj (P) that the two valties are different is indicated
Muiscina Muscina
absent present P

No. of snails 32 11
Mean no. of individuals/snail 21-41 9 45 <0 01
Mean no. of species/snail 2 56 2-91 NS
Proportion of snails with Sarcophaga nigriventris 0 63 0 64 NS
Proportion of snails with Philosepedon hunieralis 0 63 0.55 NS
Mean no. of Sarcophaga nigriventris/snail (all snails) 2-03 1 82 NS
Mean no. of Philosepedon humeralis/snail (all snails) 16-25 3 55 <0 01

compared to a maximum of six puparia of the next most abundant, but much larger
species, Sarcophcaganigriventris.Table 5 shows that the proportion of snails occupied by
these two species is very similar whether Muscina assimilis is present or not. This and the
non-significant change in the species richness sugg,estthat M. assimilis has not generally
eliminated species from the snails, although 'local' extinctions may sometimes be expec-
ted. The significantly reduced number of Philosepedonhtumeralis (but not of Sarcophaga
nigriventris)found in snails with Muscina assimilis suggests that in these snails, the former
species provides the main food of the latter in its last instar.
Only casual observations have been made on other predators. A few snails disappeared
from the exposure sites in the dunes, presumably removed by birds. Coleopteran preda-
tors were occasionally noted, and included the silphid, Silpha obscura L.; carabids,
Asaphidionflavipes (L.), Dyschirius politus (Dejean), D. globosus (Herbst), Loricera pili-
cornis (F.), Nebria brevicollis (F.), and Notiophilus sp.; and staphylinids, Oxytelus
sculpturatus(Gravenhorst), Philonthusalbipes (Gravenhorst), Xantholinussp., and Atheta
spp. The only frequent species were Dyschirius globosus and Atheta spp.; most others
were represented only by one or two specimens. They are not considered to have had an
important effect on the communities from the general point of view, although they
probably removed some eggs and larvae particularly of the smaller Diptera from indi-
vidual snails.
Two species of parasitic Hymenoptera were recorded, Mesoleptus sp., a parasite of

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 R. A. BEAVER 791
Sarcophaga nigriventris, and Trybliographasp., a parasite of Subhylemyia longula. The
latter species was very rare (Beaver 1972). Both species attack the host larvae, but only
complete development after the host has formed its puparium. Each host produces one
parasite. The level of parasitism by Mesoleptulsin the different collections is shown in
Table 6. The level fluctuates rather irregularlythrough the year. It is evident that in most
collections, the parasite found less than 5000 of the snails containing Sarcophaga nigri-
ventris. The exception was collection 6(2) which was exposed for 2 weeks. It is possible
that longer exposure would have increased the rate of parasitism in the other collections.
In collections 4 and 6(2), in which the parasite was relatively abundant, there was some
indication that snails containing higher numbers otf S. nigriventris were attacked pro-
portionately more by the parasite, but.calculated regressions were not significant, and the
density-depen(lence of parasite attacks remains unproven.
The importance of the parasites lies in their reduction in the numbers of emerging
hosts. Neither species has any great effect on community structure within the snail. This
is because the parasitized&hostlarva continues to feed normally, and grows to a normal
size (when parasitized by Mesoleptus), or a somewhat reduced size (when parasitized by
Trybliographa).Thus the intensity of the competitive interactions between the Dipteran
larvae is essentially unchanged. This constrasts with the effect of predation on the
community.

Table 6. Levels of parasitism of Sarcophaga nigriventris by Mesoleptus sp.

in collectionts1-6 (SarcQphaganigriventris was absentfrom collection 7)1
Collection no. 1 3 4 5 6(1) 6(2)
Snails with Sarcophaganigriventris(%) 80 0 12-1 628 13-8 66.7 73.3
Snails with Mesoleptussp. (0) 143 0 27-9 6-9 267 66-7
Parasitismof Sarcophaga,nigriventris
puparia(3%) 31 0 44.7 250 127 552

It seems likely that the Diptera compete little as adults, although there may be some
interference between females (see above). Oviposition is also restricted to a relatively
short period, particularly in summer, as a result of the breakdown and liquefaction of
the snail body. Larval competition is presumably of the diffuse type (MacArthur 1972)
since the majority of species involved are feeding on essentially the same food. Its effects
on the communities studied are far more important than those of parasitism and pre-
dation.
The effects of larval competition on puparial size in Sarcophaga species have been
discussed by Beaver (1973). Competition is largely of the exploitation type, although the
effects of interferencebetween larvae can be detected. The food is relatively evenly shared
between the individuals of a species. The larvae apparently compensate for increased
crowding by reducing the final body size rather than by increasing mortality, at least until
a minimum size limit is reached. The adaptive nature of this strategy is discussed below.
Similar effects of competition on size and mortality have been recorded for other carrion
and dung-feeding Diptera (Fuller 1934; Ullyett 1950; Webber 1955; Bryant & Sokal
1967; Valiela 1969; Wasti, Hosmer & Barney 1975). The fecundity of the smaller indi-
viduals is almost certainly reduced, as in-other Sarcophagidae (Zakharova 1966) and
other carrion and dung-feeding Diptera (Mackerras 1933; Ullyett 1950; Webber 1955;
Hughes & Walker 1970). It is likely that similar effects occur in the other saprophagous

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792 Non-equilibriumDipteran communities
species present in the snails. (I have evidence of this from the tropics, but not for the
temperate zone species discussed here.)
Priority effects are likely to be important in larval competiton (Bryant 1971; Beaver
1974; Lane 1975). Species or individuals which start feeding earlier or which develop
faster than their fellows will have access to more food and a competitive advantage. This
affects the life history strategy of the species (see below).

DISCUSSION
The discussion that follows contains a good deal of speculation. However, it is hoped
that it may stimulate further experiments to confirm or deny the speculations. It also
attempts to make some generalizations which are, hopefully, applicable not only to the
communities in the dead snails but to other communities in habitats with similar eco-
logical characteristics, particularly carrion and dung.

Lije history strategies

One of the basic characteristics of the habitat types under discussion is that their
habitat stability, expressed as the ratio of generation time to the time the habitat remains
favourable (Southwood et al. 1974), is equal or close to unity. In this case, one generation
cannot affect the resources available to the next. There is no evolutionary penalty attached
to rapid population growth, and the species involved should be r-strategists (Southwood
et al. 1974; Southwood 1976). However, the selection pressures on the adults and larvae
are rather different and need to be distinguished.
To the adults, the environment is fine-grainedand unpredictable.During their dispersal,
they pass through many different habitat patches and variable physical conditions.
Mortality during dispersal is likely to be density-independentand non-competitive. These
are characters associated with r-strategists (Pianka 1970). Selection will favour early
reproduction and the allocation of as much energy as possible to reproduction (Pianka
1970). However, because the larval habitats are dispersed in space and only available for
a short time for oviposition, some resources must be diverted towards structures which
will improve the dispersive and colonizing abilities of the adults (Gadgil & Solbrig 1972),
thus reducing the energy available for reproduction. A compromise between the two
requirements must be reached by the species.
To the larvae, the environment is coarse-grained. They spend their whole life, until just
before pupation, in a single patch in relatively uniform and predictable physical condi-
tions. The idea of carrying capacity, based as it is on an equilibrium number of indi-
viduals, is of doubtful validity in such short-lived habitats, but the notional carrying
capacity of the habitat is very often exceeded. Competition is of regular occurrence and
frequently intense, and any resultant mortality or reduction in fecundity of the survivors
is likely to be density-dependent. These are characters associated with K-strategists
(Pianka 1970). In this situation, the optimal strategy is to channel all available energy
into maintenance and the production of a few very fit offspring (Pianka 1970). However,
if the breeding sites are small and scattered in space and time, the production of large
numbers of adults will give the species a greater chance of finding these sites. From this
point of view, it is better to produce many offspring with a reduced fitness. Thus there
must again be a compromise. In this case, the compromise seems to lie nearer the latter
than the former strategy. The larvae will tend to maximize their fitness by growing to the

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 R. A. BEAVER 793

maximum size, but if there is competition for food, the first result is a reduction in size
rather than an increase in mortality.
It is clear that the pattern of habitat units, their scattering in space and their short
lifetime requires efficient dispersal by the species. This requirement, in turn, has led to
compromises in the strategies of both adults and larvae. The compromises reached by
the different species in the communities in the dead snails, and indeed in other carrion,
differ from each other in some respects. I consider first the Sarcophagidae. The com-
promises reached here can be related to their relatively large size. Large size has the
advantage that strong, fast and directed flight is possible. Almost no work appears to
have been done on dispersal in Sarcophagidae, but their ability must equal that of the
Calliphoridae which have been more intensively studied (reviews in Norris (1964) and
Greenberg (1973)). The ability of both families to find even small, isolated carcases is
well known. Large size has the disadvantage that the amount of food required per larva
for development is relatively high. Thus the chance of competition between larvae in a
limited food source is increased. The offspring of individuals which arrive early at a new
habitat unit are at a competitive advantage and are more likely to get the amount of food
that they need to grow to full size and produce adults with a high fecundity. These adults
may also be stronger and have a greater dispersive ability. Thus efficient dispersal will be
strongly selected for. Rapid development will also be selected for since it helps the larvae
to get ahead of potential competitors. The viviparity of the Sarcophagidae gives them an
obvious advantage here over the other oviparous species. It helps them to overcome the
disadvantage that large size requires a longer development time, other things being equal.
However, it does mean that fecundity is reduced relative to oviparous species of com-
parable size (Kamal 1958). In view of the ways in which they have overcome these dis-
advantages of large size, it is not surprising that in terms of biomass the Sarcophagidae
dominate the communities in the snails in which they occur.
I next consider the small species, such as Philosepedonand Limosina. Small size has the
disadvantage that flight is relatively weaker and less directed. Thus, as in aphids (Taylor
1975), dispersal is less efficient. Despite this, the species are usually numerically dominant
in the snails (Table 2). The advantage of small size is clearly that large numbers of adults
can be produced from a relatively small amount of food. Even if an adult is a relatively
late colonizer, there may still be sufficient food for the development of numerous off-
spring. The production of large numbers can counteract the poor dispersive ability of the
species. Small size permits a shorter development time, although this was not evident in
the species studied here. The mean time between exposure of the snail and adult emer-
gence was similar in the Sarcophaga species, Philosepedon and Limosina (Table 3 in
Beaver 1972). However, some of the small species breeding in snails in the tropics do have
a very rapid development, and take as little as 9 days from egg to adult (R. A. Beaver,
unpublished observation). It should be rememberedin making comparisons of this kind
that the Sarcophagidae emerge with immature eggs, and there is a delay of about 7-12
days (Kamal 1958) before larviposition is possible. The adults of Philosepedon and
Limosina are capable of oviposition within 2-3 days after emergence.
Relative to the small species, the Sarcophagids show more K-selected characters. Both
groups lie towards the r-selected end of the r-K spectrum, but are not at the endpoint.
Similar conclusions have been reached by Denno & Cothran (1976).
There is a marked size gap between the large Sarcophagidae and the small Philosepedon
and Limosina. This gap is not unfilled, but the intermediate-sized species are relatively
less important in terms of numbers and biomass. This is also true in the tropics (R. A.

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794 Non-equilibriumDipteran communities
Beaver, unpublished observation). It prompts the speculation that there may be two
optimal sizes for Dipteran species breeding in this type of habitat.
Both large and small species tend to lay batches of eggs. This is probably related to the
degree of difficulty of finding new habitat units. If the chance of finding a unit is small,
it is clearly better for a female to lay a batch of eggs than to lay a single one and then
perhaps never find another unit. A secondary reason may be that it is easier for a group
of larvae to penetrate and utilize the food.
The lack of specialization in breeding habits of the majority of the Diptera found in
the dead snails, and indeed of most Diptera found in carrion and dung, can perhaps also
be related to the heterogeneity of the breeding sites in space and time. Since the habitat
stability is effectively unity, and dispersal is necessary in each generation, a specialist in
one type of carrion or dung would need very efective dispersal and a very predictable
supply of new habitats in order to survive. It seems likely that this condition is rarely
fulfilled in natural conditions.

Persistence and coexistence

The carrion/dung habitat is non-persistent. 'Local' extinction of the populations living
in a habitat unit is certain. The persistence of the species depends in part on the hetero-
geneity of the units in space and time. The probability of simultaneous extinction in all
units is the product of all the local extinction possibilities at a given time. Given the
heterogeneity, this is infinitesimally small when the number of units (and local popula-
tions) is large (MacArthur 1972; Allen 1975). A high dispersive and colonizing ability is
also essential so that the colonization rate of new units balances the local extinction rate
(MacArthur 1972; Allen 1975). The populations are locally unstable but show stochastic
persistence (Allen 1975) on a regional scale.
Almost all community studies of habitats such as carrion and dung note the large
number of species involved and the coexistence of many of them apparently feeding on
the same food. The coexistence can be at least partly explained in terms of differences in
the exploitation patterns of different species, even though there is usually extensive
overlap between species (Elton 1966; Denno & Cothran 1975). Thus there are differences
between species in the utilization of carrion of different species and sizes (Fuller 1934;
Cornaby 1974; Denno & Cothran 1975). If these two parameters are kept constant, there
are differences dependent on the season of the year, the local microclimate and the
successional stage of decay (Fuller 1934; Denno & Cothran 1975). Even when these
variables are excluded, the carrion itself is not completely homogeneous so that it may
be exploited by different species in different ways. Seasonal and successional differences
in utilisation patterns have been illustrated above for the dead snail communities. Such
differences are sometimes considered sufficient to explain the coexistence of the species
complex (e.g. Denno & Cothran 1975), but I suggest that the number of coexisting species
is further increased because some of them are fugitive species. These species are com-
petitively inferior, but able to survive because of their greater migratory and colonizing
ability and the heterogeneity of the distribution of the habitat units (Hutchinson 1953,
1965). Models (Horn & MacArthur 1972) suggest that there is no formal limit to the
number of coexisting fugitive species. However, in practice, there will be limits set by the
rate of supply of new units, the intensity of competitive interactions between species, and
the relative migration rates of the different species (Horn & MacArthur 1972). The
existence of such species might be expected in temporary habitats of the kind considered
here.

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 R. A. BEAVER 795

Heterogeneity
The importance of spatial and temporal heterogeneity in population and community
dynamics is being increasingly stressed (e.g. den Boer 1968; Smith 1972; Hassell & May
1973-;Levin 1974; Levin & Paine 1974; May 1974; Fenchel 1975; Wellington et al. 1975;
Southwood 1976; Thompson et al. 1976). For animals living in temporary habitats such
as carrion and dung, heterogeneity in the spatial and temporal distribution of habitats
and in the composition of their communities is of the utmost importance. It is one of the
basic determinants of the life history strategies adopted by the species. It is equally
important for the persi'stence,and probably the coexistence of the species on a regional
scale. The heterogeneity of species composition between individual habitat units is partly
a result of the heterogeneous distribution of the habitat units, and partly a consequence
of the short period during which colonization is possible for individual sp'ecies.During
this period, the chance arrival of particular species (Levin 1974), short-term meteoro-
logical events, and changes in the habitat itself (Valiela 1974) affect the composition of
the colonizing community. Competition and predatoryinteractions are probably relatively
unimportant at this stage (Valiela 1974). Biotic interactions, especially'competition, are
often of great importance during larval development, even though the species involved
are opportunistic colonists exploiting an initially empty habitat in each generation.
Despite the local heterogeneity, regularities are apparent on a regional scale. It was
noted above that the total numbers of species and individuals in the snails are relatively
evenly distributed in each collection, despite the strong aggregation of individuals of
particular species. In addition, although the dominant species was not the same in each
collection (Table 2), only four out of eighteen species were involved. There is relative
stability on a regional scale, although there may still be considerable fluctuations in the
relative abundance of species. It may be expected that spatial heterogeneity will have a
stabilizing effect while temporal heterogeneity will have an unstabilizing effect on the
situation (Smith 1972; May 1974).

ACKNOWLEDGMENTS
I am most grateful to Dr J. A. Mathias for his comments on an earlier draft of this paper,
and to Prof. C. P. Ramachandran for providing facilities for its completion at Universiti
Sains Malaysia. I am indebted to the Nature Conservancy for permission to work at the
Newborough Warren National Nature Reserve.

SUMMARY
(1) The communities of Diptera breeding in a series of collections of dead snails
(Cepaea nemoralis)are analysed from the aspect both of the single snail and the collection
exposed to attack at one time. The species involved are opportunist colonists exploiting
new habitat units in each generation, but biological interactions between the larvae in
each snail are very important in the determination of community structure.
(2) Species abundance distributions for the collections tend towards the geometric
series, with one or two strongly dominant species in terms of numbers and biomass.
Seasonal changes in the total and mean numbers of species and individuals are discussed.
Some evidence of successional changes in the communities is presented.
(3) The communities of individual snails show considerable heterogeneity, with indi-

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796 Non-equilibriumDipteran communities
viduals of each species strongly aggregated. Greater regularity is apparent on the level of
the collection, presumably as a result of biological interactions between species. Some
significant positive and negative interactions between species are discussed.
(4) Parasitism has little effect on community structure. Predation by Muscina assimilis
larvae was shown to reduce the numbers of Philosepedonhumeralis larvae in the snails,
but did not generally lead to local extinctions of species. Competition, probably diffuse,
between larvae is the most important biological interaction within the snails. Its effects
on the communities are discussed.
(5) Many of the ecological characteristics of the species can be related to the low
habitat stability and the dispersion of the habitat units in space and time. Priority effects
are likely to be important in the determination of the initial structure of the community
in each habitat unit.
(6) The life history strategies of the species are basically r-selected, but selection
pressures on adults and larvae differ leading to a need for compromises. The compromises
reached by different species can be related to their size and dispersive ability.
(7) Habitat heterogeneity in space and time is essential for the persistence, and probably
the coexistence of the species on a regional scale. It may also account for lack of speciali-
zation in breeding habits of most of the species.
(8) The conclusions given in (3), (5), (6) and (7) above can probably be extended to
most carrion and dung communities.

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APPENDIX
List of Diptera and Hymenoptera mentioned in the paper.

Diptera:
Psychodidae: Philosepedon humeralis (Meigen)
Phoridae: Megaselia(Megaselia)brevicostalis(Wood)
M. (M.) tenebricolaSchmitz
Sphaeroceridae: Limosina luteilabris (Rondani)
Sarcophagidae: Sarcophaga hirticrus Pandelle
S. nigriventrisMeigen
S. teretirostrisPandelle
Muscidae: Fanniacanicularis(L.)
Hydrotaeaocculta(Meigen)
Muscinaassimilis(Fallen)
Anthomyiidae: Subhylemyia longula (Fallen)
Lasiommaoctoguttatum(Zetterstedt)
Hymenoptera:
I-chneumonidae: Mesoleptus sp.
Eucoilidae: Trybliographa sp.

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