BiologicalJournal ofthe Linnean Socieg (1981),16: 293-301. With 5 figures
Microdistribution and habitat selection
in Drosophila subobscura Collin
BRYAN SHORROCKS AND LOREDANA NIGRO*
Department of Pure and Applied ,Zoology, The Universip, Leeds LS2 9JT
Accepted for publication Jub 1981
Microdistribution and habitat selection were investigated in a population of Drosophifa subobscura near
Leeds, Yorkshire. Microdistribution was examined along a transect running through a deciduous
woodland. Two main types of habitat were recognized, those with dry soil and a closed canopy of
mature trees (dry and dark) and those with wet soil and an open canopy of mature trees (wet and
light). Flies were much more frequent, judged by their attendance at baited traps, in the dry/dark
habitat. Flies taken from both habitat types, marked with different coloured fluorescent dust and
released at a point mid-way between the original habitats, tended to return to their area of initial
capture.
KEY WORDS :-Drosophifa
-
microdistribution - habitat selection - fluorescent dust.
CONTENTS
Introduction . .
Study area
. .
Methods . . .
Traps and baits
Fluorescent dust
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Results . . . .
Microdistribution .
Habitat selection .
Discussion. . . .
Acknowledgements. .
References. . . .
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INTRODUCTION
Natural environments are spatially heterogeneous and a number of workers
have recently demonstrated that Drosophilu species respond to this microgeographic
variation both genetically and behaviourally. Microgeographic genetic
differentiation (gene arrangements and allozyme frequencies) has been shown to
exist in populations of D. melunogaster (Stalker, 1976) and D . persimilis at Mather,
California (Taylor & Powell, 1976).By using mark, release, recapture experiments,
* Present address: Istituto di Biologia Animale, Universita Deglin Studi di Padova, Via Loredan, 10, 35100
Padova, Italy.
0024-4066/81/080293+09 $02.00/0
19
293
0 1981 The Linnean Society of London
294
B. SHORROCKS AND L. NIGRO
Taylor & Powell (1978) have shown that D . persirnilis and D . pseudoobscuru tend to
return to their area of origin, or to an ecologically similar area, when transplanted
away. Such local responses by individuals would have important consequencies for
population studies. In particular, if the phenomenon of habitat choice, by
individual flies, was of wide occurrence it would have important implications for
the maintenance of genetic variation in natural populations. Spatial variation in
selection coefficients, particularly when coupled with habitat preference (Taylor,
1976) is a potentially important mechanism for the maintenance of high levels of
genetic variation known to be present in many species, including Drosophilu (Nevo,
1978). In the laboratory, Jones & Probert (1980) have demonstrated the
considerable efficiency with which habitat selection can maintain genetic
polymorphism.
The experiments described in the present paper, investigate habitat choice in a
British population of D. subobscuru along with some associated problems of
experimental technique and microdistribution.
STUDY AREA
The experiments and collections described below were carried out in Adel Dam,
an area of mixed deciduous woodland 8 km north of the city of Leeds, England
(Shorrocks, 1975). It occupies an area of 50 ha surrounding a former mill pond, set
in a shallow valley. The Leeds historian, Ralph Thoresby, refers to Adel Mill in
1715 as a corn mill so it is reasonable to suppose that the original dam was built
prior to this date. Since that time the area of clear water has gradually been
reduced due to extensive silting and the growth of reedmance ( Tjphu lutifoliu L.).
The general location of the woodland and its environs are shown in Fig. 1. Like
many English woodlands, the quantity and quality of vegetation in Adel Dam
-
Deciduous
woodland
h /Darn
Figure 1. Adel Dam showing experimental area and environs.
HABITAT SELECTION IN DROSOPHILA
Figure 2. Experimental area showing position of traps
after marking the R i a (*).
295
(a),main vegetation and the point of release
varies over quite short distances. Figure 2 shows a simplified map of that part of the
woodland chosen for the present study. The area is bounded on three sides by a
fence and open ground. As indicated in Fig. 2, the two ends of the experimental
area comprise mature woodland on very dry soil. Here the canopy formed by the
many trees reduces the light intensity at ground level. Illumination was measured
as reflected light, 10 cm above a white sheet placed on the ground. Measurements
taken throughout the day while collecting was in progress gave a range of values of
80-180 lux for the area of beech (Area IV) and 110-280 lux for the area of
sycamore (Area I ) . Between these two areas, the ground falls several feet, is very
much wetter and contains a decidedly different flora. Trees, mainly Willow (Sulix)
and alder (Alnus) are very much fewer in number resulting in a very open canopy
and much more light at ground level. Here the range of illumination values were
400-600 lux for Area I1 and 800-1500 lux for Area 111.
METHODS
Traps and baits
The traps comprised plastic buckets containing cotton-wool soaked in ‘Guinness’,
a commercially produced bottled beer. Prior to conducting the experiments,
preliminary tests were carried out to examine the effect of ‘ageing’ upon the
attractiveness of this convenient Drosophila bait. New bait was always made by
pouring ‘Guinness’ from a newly opened bottle onto the cotton-wool. Traps were
first placed in the wood on the next day (called one day old bait). Twenty traps,
with bait ofdifferent ages (one day old to ten day old) were put out at two different
sites. Each day, for five consecutive days, the oldest traps were removed and
replaced by ones of one day old. This ensured the same range of bait ages during
the five day test period. In this and all subsequent experiments, flies were removed
from the traps at regular intervals throughout the day using a net and pooter. The
results are shown in Fig 3. the original collection data were subjected to a square
root transformation and the means and confidence limits then back transformed to
produce Fig. 3. There is a large amount of variation from day to day in the number
of Drosophila actually flying and therefore available for capture. This is reflected in
the large confidence limits in Fig. 3. However, in a two way analysis of variance
296
B. SHORROCKS AND L. NIGRO
50
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Age of boit (days)
Figure 3. Numbers of Drosophila subobscura coming to baits of different age. Data are daily
means f 95% confidence limits.
(age of bait x days) the effect of bait age is just significant (F9.36= 2.17,
P=0*05).The effect of days is very significant (F4.36=12.55, P < 0.01).
Although the age of the ‘Guinness’bait does appear to have some effect upon the
numbers of D. subobscuru attracted, catches on day 1 and 2 are in the highest group.
Bait of age one day is also the most convenient so far as the experimenter is
concerned. Because of both these facts fresh ‘Guinness’ was used for the
experiments reported below.
Fluorescent dust
In recent years, micronized fluorescent dust has been used by a number of
workers to mark wild flies for dispersal and density studies (Crumpacker &
Williams 1973; Begon 1976; Dobzhansky et ul., 1979). The effectiveness of such
dusts in marking the flies over several days has been tested by Crumpacker (1974)
on D. pseudoobscura and Moth & Barker (1975) on D. sirnulam. We carried out a
similar test on D. subobscuru, in which, however, the process of identifying marks
was similar to that in a field experiment.
Four colours of dust were tested (Heffner Co. Ltd., Redhill, Surrey, U.K.) on
both males and females. The experimental flies, F, progeny of wild caught females
from Adel Dam, were marked by rolling in a 75 x 25 mm glass vial thinly coated
with dust. The marked flies (25 male and 25 female for each colour of dust) were
placed into perspex cages in an outdoor insectary and examined each day for
visibility of marks. For examination, the marked flies were placed individually into
glass vials and examined under a binocular microscope with UV illumination in a
dark room. An equal number of unmarked flies, also in glass vials, were mixed with
the experimental animals. Thus, the person scoring marks had to separate marked
and unmarked flies as in a field experiment.
The results are shown in Fig. 4. There was no significant difference between
male and female data and these have been combined for each colour of dust. For
three days after marking almost 100% of the marked flies could be recognized.
HABITAT SELECTION IN DROSOPHILA
297
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Days after initial marking
Figure 4. Percentage of Drosophila subobscura with marks still visible on different days after initial
marking. A, Blue dust; 0 ,green dust; 0 ,red dust; *,yellow dust.
Even by day ten, 80% of the marks were still visible. There appears to be no
significant difference in marking ability between colours of dust.
There seems little doubt that for the periods of time required by the experiments
which follow, micronized fluorescent dusts are a suitable marking agent for D.
subo bscura.
RESULTS
Microdistribution
An examination of microdistribution is an important preliminary to many kinds
of field investigation, including habitat selection, dispersal studies and density
estimates. The collections described in this section provide the background for the
study of habitat selection which was the major objective of the work. The
collections were carried out during July 1980 in Adel Dam. A transect of 15
traps, each 10 m apart, was put out across the study area (Fig. 2). Traps were
opened in the morning and collections made, all day, for five consecutive days.
The results are shown in Fig. 5. There are quite marked differences in the numbers
of D.subobscura coming to traps, even a short distance apart. On the basis of
vegetation, amount of light at ground level and soil moisture the study area had
already been divided into four zones (Fig. 2). In general, the flies appear to prefer
the ‘dark and dry’ habitats (Areas I & IV) and to avoid those that are ‘light and
wet’ (Areas I1 & 111). These findings confirm the results of Taylor & Powell
(1978) on D.pseudoobscura. Area I11 is so unfavourable that it is unlikely to support
a resident population of any kind. We feel this is an important finding and may
help to explain why Atkinson & Miller (1980) had difficulty in demonstrating
habitat selection. Reference will be made to this area again in the Discussion.
B. SHORROCKS AND L. NICRO
298
400-
l:
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Trap site
Figure 5. Total number of Drosophila mbobscura caught at the 15 trap sites over a five day period.
There was also an interesting difference in sex ratio between the two
microhabitat types. In the ‘dark and dry’ areas there were 50% females while in
the ‘light and wet’ areas.it was 70%. Inglesfield (1979) has suggested that in D.
~ubobscuru,presence of females in a trap influences the number of males attracted. If
true, this could well be a complicating factor in any attempt to investigate habitat
selection using the two different microhabitats outlined above. We therefore
carried out an experiment in which four different types of ‘Guinness’ baited traps
were used. Each type of trap contained a small plastic cage (5 cm diameter) with a
fine mesh roof. In some traps these cages were empty and those served as controls.
The remaining types contained either males, virgin females or mature, egg laying
females. These four types of trap were used for seven days at three different sites
and the attracted D . subobscuru recorded. The data analysed was percentage of
males (transformed to arcsines). Table 1 shows the mean values over seven days for
each type of trap, and Table 2 shows an analysis of variance. There appears to be
significant effects over both days and traps. However, mature females and males,
the major part of the adult Drosophilu population, do not appear to influence the
attraction of males. We do not believe, therefore, that this will be a disturbing
factor in the habitat selection experiments.
Table 1. Percentage males coming to four types of ‘Guinness’ trap
(see text). Confidence limits are asymmetrical because the
original computation was carried out on transformed
percentages
Treatment
Virgin 99
Mature 99
C3d
Contml
O/,
males
48.01
57.18
59.16
54.01
(95% confidence limits)
(39.50 - 56.58)
(50.03- 64.19)
(46.01 - 71.68)
(42.97 - 64.85)
HABITAT SELECTION IN DROSOPHILA
299
Table 2. Analysis of variance carried out on percentage of males coming to four
types of trap (see text) over seven days. The three sites are used as replicates
Source of
variation
ss
d.f.
type of trap
days
interaction
residual
585.7
2150.6
690.7
4178.3
3
6
18
56
Total
7605.4
83
P
F
MS
195.2
358.4
38.4
74.6
2.62
4.80
0.51
< 0.05
< 0.01
n.s.
Habitat selection
Two experimental areas, 100 m apart, were chosen. One habitat (Area IV in
Fig. 2) was rather dark and the soil dry and consisted mainly of mature beech trees.
The second habitat (Area I1 in Fig. 2) was light and the ground wet, with a few
alder trees. Flies were collected from both areas, marked with fluorescent dust of
different colours and released midway between both areas (marked by an asterisk
in Fig. 2). On the following two days, flies were recaptured from both Areas I1 &
IV and from a third area (I in Fig. 2), which was also dark and dry like Area IV
although the trees were mature sycamore. These latter collections from Area I
were carried out because Taylor & Powell (1978) observed that flies also returned
to ecologically ‘similar’ areas. The experiment was repeated on three different
occasions during July and August 1980. A heterogeneity chi-square test was not
significant (xi = 9.0) and therefore in the contingency tables shown in Tables 3
and 4 the data from the three experiments have been pooled.
The first comparison between site IV and I1 (Table 3) indicates a significant
tendency (xy=9.58, P<O-Ol) for flies to return to their area of first capture.
Table 4 shows that flies also show a tendency to return to an ecologically similar
area as that in which first captured. Proportionately more flies originally caught in
Area IV were recaptured in Area I than in area I1 (x:=3.51, P=0.05).
Table 3. Contingency table showing recaptured flies according to area of original
capture and recapture. Figures in brackets indicate numbers expected if random
movement occurred
Site of recapture
B. SHORROCKS AND L. NIGRO
300
Table 4. Contingency table showing recaptured flies according to area of original
capture and recapture. Figures in brackets indicate numbers expected if random
movement occurred. Areas IV and I are ecologically similar
Site of recapture
w
iij
44
114
I
158
DISCUSSION
The results of our experiments on habitat selection are very similar to those of
Taylor & Powell (1978) carried out with D . persirnilis at Mather, California.
Drosophilu subobscuru at Adel Dam appear to return to their area of origin, or to an
ecologically similar area, when transplated away. Also, in both the Californian
and Yorkshire experiments, light level or moisture or both appear to be important
cues which enable the flies to select the correct habitat.
Although habitat selection by individuals was demonstrated in a Yugoslavian
population of D.subobscuru (Kekic et ul., 1980), a previous study on this species in
Adel Dam (Atkinson & Miller, 1980) failed to find such selection. There could be a
number of reasons for this negative result. Flies may change their response as their
density and environment in general changes. The experiments of Atkinson and
Miller were carried out in different years (one after a severe winter when summer
populations were low) and in different months May and September). However,
our study of microdistribution suggests that at one of their sites the habitat was
rather unsuitable for Drosophilu. They also used the area depicted in Fig. 2. Their
‘dark’ site (habitat A) corresponded to the area around our site 14. Their ‘light’
site (habitat B) corresponded to the area around our site 9. It is clear from our
trapping results (Fig. 5) that their ‘light’ area produced very few flies. If this area is
so unattractive for Drosophilu subobscuru then such flies that are caught here may
simply be passing through. Such non-resident flies would not be expected to show
habitat selection.
There appears to be little doubt that under the appropriate circumstances the
European species D.subobscuru does show individual habitat selection. That is,
individual flies show a tendency to return to their area of initial capture. This
tendency may have a heritable component since female flies, and their F, progeny,
from light habitats are more photopositive than those from dark areas (Kekic et ul.,
1980). In addition to this individual response there is a more general selection of
habitats such that more flies are found in dark shaded areas compared with light
open ones. Both levels of response will contribute to a population structure which
has been largely ignored by population biologists. Environments are heterogeneous
and this will have an effect upon population processes.
ACKNOWLEDGEMENTS
We would like to thank Professor R. McN. Alexander for the provision of
laboratory facilities. L.N. would like to thank the Accademia Nazionale dei Lincei
HABITAT SELECTION IN DROSOPHILA
30 1
(linked to the Royal Society by the European Science Exchange Programme) and
the British Council for financial support.
REFERENCES
ATKINSON, W. D. & MILLER, J. A., 1980. Lack of habitat choice in a natural population of Dmsophila
subobscura. Heredig, 44: 193-199.
BEGON, M., 1976. Dispersal, density and microdistribution in Drosophila subobscura Collin. Journal of Animal
Ecology, 4.5: 44-456.
CRUMPACKER, D. W., 1974. The use of micronized fluorescent dusts to mark adult Drosophila psnrdoobscura.
American Midland Naturalist, 91: 118-129.
CRUMPACKER, D. W. & WILLIAMS, J. S., 1973. Density, dispersion and population structure in Drosophila
pseudoobscura. Ecological Monographs, 43: 499-538.
DOBZHANSKY, Th., POWELL, J. R., TAYLOR, C. E. & ANDREGG, M., 1979. Ecological variables
affecting the dispersal behavior of Drosophila Pseudoobscura and its relatives. American Naturalist, 114: 325-334.
INGLESFIELD, C., 1979. Migration and Mitrodutribulion in Drosophila subobscura Collin. Ph. D. Thesis,
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JONES, J. S. & PROBERT, R. F., 1980. Habitat selection maintains a deleterious allele in a heterogeneous
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KEKIC, V., TAYLOR, C. E. & ANDJELKOVIC, M., 1980. Habitat choice and resource specialization by
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NEVO, E., 1978. Genetic variation in natural populations: Patterns and theory. Thcorctical Population Biology, 13:
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SHORROCKS, B., 1975. The distribution and abundance of woodland species of British Drosophila (Diptera:
Drosophilidae). J o u m l of Animal Ecology, 44: 851-864.
STALKER, H. D., 1976. Chromosome studies in wild populations of D . mclanogastn. Genetics, 82: 323-347.
TAYLOR, C. E., 1976. Genetic variation in heterogeneous environments. Genetics, 83: 887-894.
TAYLOR, C. E. & POWELL, J. R., 1976. Microgeographic differentiation of chromosomal and enzyme
mlvmomhisms in Drosobhila bersimilis. Genetics. 85: 681-695.
TAGLOR, k. E. & POWEiL, J: R., 1978. Habitat choice in natural populationsofDrosophiln. Occologia (Berlin),
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