Blackwell Science, LtdOxford, UKBIJBiological Journal of the Linnean Society0024-4066The Linnean Society of London, 2006? 2006
87?
233247
Original Article
RELATIONSHIPS BETWEEN DROSOPHILIDS AND THE ENVIRONMENT
R. TIDON
Biological Journal of the Linnean Society, 2006, 87, 233–247. With 5 figures
Relationships between drosophilids (Diptera,
Drosophilidae) and the environment in two contrasting
tropical vegetations
ROSANA TIDON*
Instituto de Biologia, GEM, Universidade de Brasília CP 04457, 70919–970, Brasília, Brazil
Received 20 September 2004; accepted for publication 9 March 2005
Although natural populations of drosophilid flies have been the subject of ecological studies, the population ecology
of these insects in the tropics is still poorly known. This paper discusses aspects of the relationship between drosophilids and their environment, based on 28 monthly collections made in two contrasting vegetations of the Brazilian
Cerrado biome: gallery forest and savanna. Exotic species were found in both types of environment; but 14 of the 30
captured Neotropical species occurred exclusively in the gallery forests, probably because of their climatic stability
and greater environmental heterogeneity. Even though some endemic species were more abundant in the dry and
cold months, most populations exhibited peaks of abundance in the wet season. The species diversity indexes (H′ and
D), higher in the dry season, were probably affected by increased evenness at this time of year, when the populations
of practically all the species are greatly reduced. As species richness in the savanna vegetation clearly decreased in
the dry season, increasing again in the wet season, it is suggested that some drosophilids migrate to the forests when
climatic conditions are too stressful in the savannas. © 2006 The Linnean Society of London, Biological Journal of
the Linnean Society, 2006, 87, 233–247.
ADDITIONAL KEYWORDS: biodiversity – Brazil – Cerrado biome – Drosophila – gallery forest – savanna –
South America – temporal distribution – Zaprionus.
INTRODUCTION
Many factors affect the ability of a species to survive
and reproduce in sufficient numbers in order to persist
in a locality. Biotic and abiotic factors may vary in
space and time, and for a mobile organism spatial
variation often becomes temporal variation (Futuyma,
1998). The belief that organisms are remarkably well
suited to the world they live in predates scientific biology; metaphors used to explain the relation between
organism and environment usually invoke an external
world that has acquired its properties independently
of the organism (Lewontin, 2000). However, this view
has been questioned since species in practically all
kingdoms participate actively in building their environment, and changes caused by them often result in
selective pressures acting not only on a particular species, but also on those that share the area (Mayr, 1963;
*E-mail: [email protected]
Gould & Lewontin, 1979; Lewontin, 1982; Levins &
Lewontin, 1985).
According to Odling-Smee, Laland & Feldman
(2003), organisms can change environmental factors
in their niches by two ways. Perturbation is when they
physically change one or more factors in their environment at specified locations and times. Relocation is
when they actively move, choosing the direction and
or distance in space through which they travel, and
sometimes also choosing the time. In the process of
relocation, they expose themselves to alternative habitats, at different times, and thus to different environmental factors. Odling-Smee et al. (2003) consider that
the question of niche construction has been neglected,
and suggest studies to investigate the relationship
between organism and environment.
Of the millions of species that inhabit the Earth,
biological research tends to concentrate on relatively
few organisms; among them, none has received as
much attention as Drosophila. This genus played a
© 2006 The Linnean Society of London, Biological Journal of the Linnean Society, 2006, 87, 233–247
233
234
R. TIDON
major role in the development of genetics and evolutionary theory, and more recently in the study of development and molecular biology (Brookes, 2001). If
Drosophila has a weakness as a model, it has been on
the ecological level, due more to a lack of attention
than to any inherent inappropriateness for such studies (Powell, 1997). Drosophilids are small, numerous,
with a short life cycle, easily collected and manipulated, besides being extremely sensitive to changes in
their habitat conditions. There is a consensus that full
understanding of evolutionary patterns and mechanisms requires relating the genetics of the organism to
the environment in which it lives; that is, genetic
knowledge needs to be placed in an ecological context.
A better understanding of the ecology of drosophilids
will certainly add meaning to the available genetic
information about these insects.
Drosophilids interact with the environment in both
the ways described by Odling-Smee et al. (2003). They
promote perturbation in the substrates where they
feed and breed, usually decaying plants and fungi,
intervening in the succession of the microorganisms
involved in the fermentation process (Begon, 1982).
They also move actively in the environment, congregating in feeding and breeding sites when temperature, light, humidity and time of day are appropriate.
Although natural tropical populations of drosophilid
flies have been the subject of ecological studies
(Dobzhansky & Pavan, 1950; Pavan, 1959; TidonSklorz & Sene, 1992), especially in the Sonoran desert
(Heed & Mangan, 1986; Pfeiler & Markow, 2001;
Gibbs, Perkins & Markow, 2003), knowledge of the
population ecology of most of the Neotropical species is
still limited (Brncic, Budnik & Guinez, 1985; Saavedra
et al., 1995) compared to that of Paleartic species of
this group. In a review of Neotropical Drosophila, Val,
Vilela & Marques (1981) concluded that ‘there is a surprising lack of information on the environmental situation in which the species are found.’ This statement
holds true for tropical South America.
The Cerrado biome is a complex of seasonal savannas that covers most of the interior of Brazil and
includes a few small contiguous areas in Bolivia and
Paraguay. Extending over approximately 2 million
km2, it is the second largest South American biome
(Ratter, Ribeiro & Bridgewater, 1997; Oliveira & Marquis, 2002), and one of the 25 ecological hotspots of the
world – areas with great endemism and less than 30%
remaining of the natural vegetation (Myers et al.,
2000). This biome is a mosaic of physiognomic vegetetational forms, ranging from dense grassland, usually with a sparse covering of shrubs and small trees,
to woodland that is almost closed, with a canopy
height of 12–15 m (Ratter et al., 1997). The typical
landscape of the Cerrado biome consists of savanna of
very variable structure, on the well-drained inter-
fluves, with gallery forests or other moist vegetation
following the watercourses (Oliveira-Filho & Ratter,
2002). These two basic types of vegetation have different structures and species composition, and the transition between them is usually sharp. According to the
Koeppen classification system the climate in the Cerrado is tropical dry winter Aw in 95% of the biome,
changing to cooler Cw at higher altitudes; precipitation is highly seasonal, characterized by a well-defined
dry season from May to September.
Although the peculiar characteristics of the Cerrado, i.e. its heterogeneity and seasonality, makes it of
special interest to those studying the complexities of
tropical communities, little is known about its insect
communities (Diniz & Kitayama, 1998; Pinheiro et al.,
2002). A few collections of drosophilids were made in
this area in previous studies: three samples in the late
1940s (Dobzhansky & Pavan, 1950), five between 1976
and 1978 (Sene et al., 1980) and, more recently, a survey aimed at investigating the impact of the recently
introduced species Zaprionus indianus in the region
(Tidon, Leite & Leão, 2003). Currently, about 60 species are known from this biome.
In this study, some aspects of the spatial and temporal distribution of drosophilids are discussed, based
on 28 monthly collections made in two contrasting
vegetations of the Cerrado biome. The specific purposes of the project were: (1) to compare drosophilid
assemblages at different vegetations, (2) to investigate
the monthly fluctuations in the abundance of common
species, relating them to climatic factors, and (3) to
explore connections between spatial and temporal distributions of drosophilids.
MATERIAL AND METHODS
Monthly collections of drosophilids were made in two
areas close to the city of Brasília, capital of Brazil: the
ecological reserve of IBGE (RECOR) and the National
Park of Brasília (NP). RECOR, located 35 km south of
Brasília (15°56′S, 47°53′W), is part of an environmental protection area with an extent of 10 000 ha. In
addition, it is part of the Reservation Nucleus for the
Cerrado Biosphere, created in 1993 by UNESCO. NP
is located 10 km north-west of Brasília (15 °40′S,
47°54′W) and covers an area of 30 000 ha. It was created in 1961 with the intent of preserving samples of
typical ecosystems of the central plateau of Brazil. In
RECOR, collections were made between December
1998 and June 2000 (except during the period between
March and May 1999). In NP, the collections took
place between July 2000 and June 2001. Climatic
data, collected daily, were obtained from meteorological stations in RECOR and NP. Figure 1 shows
climatic variation based on these data, from 1999 to
2000.
© 2006 The Linnean Society of London, Biological Journal of the Linnean Society, 2006, 87, 233–247
RELATIONSHIPS BETWEEN DROSOPHILIDS AND THE ENVIRONMENT
235
Figure 1. Variation of precipitation, relative humidity (RH), light intensity and temperature at the studied sites.
Two different vegetation types were sampled in
each area: a savanna-like vegetation, termed cerrado
sensu stricto (or cerrado), and gallery forest. The cerrado is one of the most characteristic physiognomies of
the Cerrado biome, showing a predominantly grassy
ground layer with scattered herbs and a woody layer
of trees and shrubs with thick husks and coriaceous
leaves (Eiten, 1972). The gallery forests occur where
humidity conditions and appropriate soils foster the
development of an arboreal community, and are classified as evergreen tropical forest.
In each of the four sites, ten traps were placed 20 m
apart along a 200 m-long transect. Care was taken to
have them placed always at the same points. The traps
contained fermented banana bait and remained in
place for 3–4 days. Flies were captured with entomological nets and the collected individuals were trans-
ported live to the laboratory. The drosophilid
specimens captured were identified by identification
keys, descriptions, and in some cases, by the analysis
of the male terminalia (Freire-Maia & Pavan, 1949;
Frota-Pessoa, 1954; Val, 1982; Vilela, 1983; Vilela &
Baechli, 1990; Vilela, 1992; Chassagnard & Tsacas,
1993). Although the cryptic species of the willistoni
subgroup were not fully determined, samples identified by Dr Marlucia Martins (Goeldi Museum) have
revealed only D. willistoni. References to species
descriptions (Appendix) can be consulted online in the
database TaxoDros (Bächli, 2004).
The species were then classified into three categories: (1) endemic species of the Neotropical region (2)
exotic species from Drosophila and Scaptodrosophila
subgenus, and (3) Zaprionus indianus. The last species was placed in a separate group due to its abun-
© 2006 The Linnean Society of London, Biological Journal of the Linnean Society, 2006, 87, 233–247
236
R. TIDON
each season (June to September for the dry season,
November to February for the wet season).
RESULTS
In total, 47 415 specimens were collected in the
present study, 59% of which were from the savanna
vegetation. Table 1 shows the abundance of the identified species from the four collection sites as well as
their preference for a vegetation type. The unidentified specimens (about 0.5%) occurred mainly in the
gallery forests.
Fourteen of the 30 captured Neotropical species
occurred exclusively in the gallery forests, besides four
others that showed a preference for this type of vegetation. On the other hand, only D. mercatorum,
D. mesostigma and D. aragua showed preference for
the savanna. The last two species were captured exclusively in this phytophysiognomy. Nine endemic species
did not demonstrate preference for either type of vegetation. In contrast, all exotic species were found in
savannas and gallery forests. D. immigrans was the
only exotic species that demonstrated preference for
D
ec
-9
8
Ja
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9
Fe
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M
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Ap
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M 9
ay
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9
Ju
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Ju
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Au 9
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dance and recent introduction in South America
(Vilela, 1999). Figure 2 reveals the relative abundance
of each category, dividing the total number of individuals from each category by the total number of drosophilids of that collection.
Mann–Whitney tests were used for comparing the
abundance of species that occur simultaneously in cerrados and gallery-forests. Regressions of abundance of
predominant species (N = 30) on climatic variation
were also carried out.
Indexes of species diversity were calculated by using
the formulae proposed by Shannon and Weaver (H′ =
– (∑pi ln pi)), and by Simpson (D = 1 – ∑pi), where
pi = frequency of species i, S = number of species,
n = sample size and H′ and D are measures of community species richness that take into account the frequencies of the species that form the community
(Huston, 1994). An index of equitability or evenness, j′,
was also obtained in order to provide data on the regularity of different species’ contributions to the samples: j′ = H′/ln S′, where H′ is the Shannon-Weaver and
S the number of species in the sample. All indexes
were calculated for the second to the fifth months of
Figure 2. Temporal variation, in cerrado sensu stricto (savanna) and gallery forest, of the proportion of individuals
belonging to the three categories of drosophilids: (1) Neotropical species from Drosophila; (2) exotic species from Drosophila
and Scaptodrosophila, and (3) Zaprionus indianus.
© 2006 The Linnean Society of London, Biological Journal of the Linnean Society, 2006, 87, 233–247
RELATIONSHIPS BETWEEN DROSOPHILIDS AND THE ENVIRONMENT
237
Table 1. Species collected in savannas and gallery forests at two sites: RECOR and NP. Preference for vegetation type
was evaluated by the Mann–Whitney test
Savanna
RECOR
NEOTROPICAL SPECIES
D. ararama
D. arauna
D. atrata
D. bandeirantorum
D. bocainensis
D. cardinoides
D. fuscolineata
D. guaru
D. mediopunctata
D. onca
D. paraguayensis
D. paramediostriata
D. paranaensis
D. schildi
D. maculifrons
D. ornatifrons
D. pallidipennis
Sgr. willistoni
D. aragua
D. mesostigma
D. mercatorum
D. austrosaltans
D. cardini
D. mediostriata
D. nebulosa
D. neocardini
D. nigricruria
D. polymorpha
D. prosaltans
D. sturtevanti
EXOTIC SPECIES
D. immigrans
D. hydei
S. latifasciaeformis
Z. indianus
D. malerkotliana
D. simulans
D. busckii
Gallery forest
NP
0
0
0
0
0
0
0
0
0
0
0
0
0
RECOR
NP
0
2
5
3
6
0
14
1
13
3
31
1
0
2
34
50
0
6437
0
0
105
0
230
8
119
0
1
3
0
375
1
2
5
3
7
24
16
4
17
3
266
1
3
3
41
149
5
9477
1
7
1626
21
499
19
840
19
15
744
8
3000
only in
only in
only in
only in
only in
only in
only in
only in
only in
only in
only in
only in
only in
only in
mainly
mainly
mainly
mainly
only in
only in
mainly
both
both
both
both
both
both
both
both
both
forest
forest
forest
forest
forest
forest
forest
forest
forest
forest
forest
forest
forest
forest
in forest **
in forest **
in forest **
in forest **
savanna
savanna
in savanna **
310
0
0
153
29
2206
3
535
106
269
19509
1083
8820
48
mainly
mainly
mainly
mainly
both
both
both
in
in
in
in
0
0
0
0
0
0
0
0
0
0
0
0
0
0
0
10
1
206
1
7
751
8
70
8
401
5
4
507
3
1121
1
0
0
109
0
0
632
0
149
2
233
0
4
5
2
465
1
0
0
0
1
24
2
3
4
0
235
0
3
1
6
89
4
2725
0
0
138
13
50
1
87
14
6
229
3
1039
34
93
212
10035
299
2191
30
10
2
12
9179
49
822
8
181
11
45
142
706
3601
7
Total
Preference
forest **
savanna *
savanna **
savanna **
*P = 0.05, **P = 0.01.
forest; D. hydei, Scaptodrosophila latifasciaeformis
and Zaprionus indianus were more abundant in the
savanna, and D. simulans, D. malerkotliana and
D. busckii did not show any pattern of preference.
Figure 2 depicts the temporal changes in the relative frequencies of the Neotropical species, Zaprionus,
and the other exotic species, in the four studied areas.
In the gallery forests, the endemic species predomi-
nated from January to July, whereas exotic species
(dominated by D. simulans) were more abundant from
August to December In the savannas, this pattern was
altered by the massive presence of Z. indianus
between November and March.
Most of the species had some temporal population
fluctuation. The first two columns in Tables 2 and 3
show, for species which had an abundance equal to or
© 2006 The Linnean Society of London, Biological Journal of the Linnean Society, 2006, 87, 233–247
238
R. TIDON
greater than 30 individuals in at least one site, the
total number of individuals and number of collections
in which the species was captured. In the RECOR
gallery forest, for example, D. maculifrons and
S. latifasciaeformis were captured in just two of the 16
sampled months. In contrast, D. simulans and
D. sturtevanti were found in 13 collections during this
period. Species not present in these tables were considered rare (N = 30) in the collection sites. Most of
them are endemic to the Neotropical region and
occurred in just one or few collections.
The temporal fluctuation in numbers, not proportions, of the most abundant species is shown in Figure
3. All species from the savannas have a peak of abundance in the wet season. Although this has also
been the rule in the gallery forest, some of the
forest-restricted rare species (D. ararama, D. atrata,
D. bocainensis, D. fuscolineata, D. mediopunctata,
D. paraguayensis, D. onca) showed the opposite pattern being more abundant in the dry season (data not
shown).
The regression of estimated abundance of drosophilid species on climatic factors is also presented in
Tables 2 and 3. Although the majority of the associations were not significant, some species apparently
responded to environmental fluctuations. As a rule,
drosophilid populations decreased with light intensity
and increased with precipitation, relative humidity
and temperature. Figure 4 illustrates, using the total
samples of the National Park savanna, the patterns
obtained for the significant regressions. Table 4 presents the measures of diversity and abundance for
savannas and gallery forests, for RECOR and NP, during the middle of the wet (November to February) and
dry (June to September) seasons. Although all communities had more species in the wet season, the diversity is usually higher in the dry season (Fig. 5).
DISCUSSION
DROSOPHILID
RICHNESS IN SAVANNAS AND
GALLERY FOREST
Of the 30 endemic drosophilid species identified in the
current study, 14 had been found exclusively in the
gallery forests, and four others also showed a preference for this type of environment. In contrast, only
three species were found exclusively or preferentially
in the savannas. The preference for forests has already
been recorded for vespids in the Cerrado biome (Diniz
& Kitayama, 1998), and for drosophilids in other
regions (Basden, 1954; Parsons, 1982; van Klinken &
Walter, 2001).
It is well known that drosophilids avoid environments that are too dry, bright or too hot (Grossfield,
1978). Certainly, these conditions in savannas are
more extreme than they are in gallery forests. Kanegae, Brás & Franco (2000) evaluated the degree of
shade at different heights from the ground, in two
environments in an area located in the same region,
very similar to the ones studied here. In the open vegetation environment, which is about 50 cm in height,
the shade effect quickly diminished with an increase
of the distance from the ground. In the forest formation known as cerradão, on the other hand, this phenomenon was less extreme: at 50 cm from the ground,
this vegetation received just 22–65% of the light intensity that reaches the open vegetation at the same
height. In fact, the crowns of the trees in the gallery
forests form a closed canopy (80–100%) that hampers
the passage of light. Although climatic differences
between the different types of vegetation were
notevaluated in this report, since we used data supplied by meteorological stations, such measurements
could have been useful to help improve our understanding of the microclimates associated with different environments. Future studies should focus on
localizing and characterizing the microhabitats used
by flies; it is a difficult but necessary task.
Forests tend also to be more floristically diverse
than open vegetation (Felfili & Silva, 1992). In NP, the
numbers of tree/large shrub species in the gallery forests and savannas are 260 and 109, respectively, while
in RECOR there are 193 and 84 (Oliveira-Filho & Ratter, 2002). In northern Australia, Parsons (1982) refers
to a mosaic of soil-type variations where the richest
habitats are associated with forests, and presumably
with Drosophila resource heterogeneities. Vertical
stratification of the vegetation is one aspect of this
complexity. The gallery forests where we made the collections are about 15–20 m high, probably supporting
a variety of microhabitats for insects.
Detailed studies of vertical distribution of drosophilids have been conducted in temperate regions in
various parts of the world, including Japan (Beppu,
1985; Tanabe, 2002), Canada (Toda, 1985) and Western Europe (Shorrocks, 1975; Lumme et al., 1979). In
each case, flies were commonly found well above the
forest floor, with some species even restricted to the
canopy. Tropical and subtropical regions, on the other
hand, have been less studied. Tidon-Sklorz & Sene
(1992) collected drosophilids in a forest near the city of
Sertãozinho, Brazil, at 0, 2, 6 and 10 m above ground
level, and found that the Drosophila populations are
distributed in aggregates that vary in size and location over the year. Van Klinken & Walter (2001)
described the vertical distribution (0–20 m) of drosophilids in five different vegetation types in subtropical
eastern Australia, and concluded that the vertical
structure of the drosophilid ‘community’ differed with
vegetation type. This vertical stratification of drosophilid populations in forests has been associated with
© 2006 The Linnean Society of London, Biological Journal of the Linnean Society, 2006, 87, 233–247
RELATIONSHIPS BETWEEN DROSOPHILIDS AND THE ENVIRONMENT
239
Figure 3. Monthly population fluctuation (absolute numbers) of the most abundant drosophilid species, from December
1998 to June 2001.
the vertical diversity of microhabitats, resources for
feeding and ovipositing, and should be taken in
account when conducting and interpreting studies
aimed at understanding the relationship between
drosophilids and their environment. In open, generally shorter, vegetation, the heterogeneity of niches is
certainly lower.
All the exotic species occurred in the two types of
environments, confirming their versatility. Cosmopolitan D. immigrans was the only exotic drosophilid species more frequent in forests, confirming what had
already been verified in Chile (Brncic, 1970), Japan
(Toda, 1973) and Australia (Parsons & Bock, 1979). It
is interesting to point out that this species, considered
© 2006 The Linnean Society of London, Biological Journal of the Linnean Society, 2006, 87, 233–247
30/5
70/3
93/9
34/6
299/9
751/14
401/14
507/14
2191/14
1121/13
206/7
212/7
10035/12
16065/16
D. busckii
D. cardini
D. hydei
D. immigrans
D. malerkotliana
D. mercatorum
D. nebulosa
D. polymorpha
D. simulans
D. sturtevanti
D. willistoni
Scaptodrosophila
Zaprionus
Total
Significance: * P = 0.05; ** P = 0.01.
RECOR/16
Taxon
N/N COL.
11687/12
8/3
149/12
2/1
10/5
49/3
632/11
233/11
5/3
822/12
465/10
109/5
12/5
9170/10
PN/12
0.238
0.073
0.013
0.021
0.073
0.004
0.149
0.214
0.180
0.127
0.013
0.007
0.001
0.152
RECOR
0.573**
–
0.043
–
–
0.350*
0.358*
0.220
–
0.822**
0.096
0.035
–
0.488**
NP
Precipitation
0.336*
0.007
0.084
0.020
0.126
0.124
0.218
0.046
0.191
0.171
0.144
0.097
0.060
0.191
RECOR
0.417**
–
0.131
–
–
0.361*
0.212
0.313
–
0.305
0.259
0.156
–
0.348*
NP
Rel. humidity
0.280*
0.079
0.121
0.001
0.089
0.015
0.324*
0.047
0.171
0.188
0.072
0.033
0.012
0.158
RECOR
Light
0.372*
–
0.170
–
–
0.305
0.460*
0.468*
–
0.583**
0.122
0.105
–
0.284
NP
0.069
0.107
0.004
0.098
0.017
0.185
0.010
0.005
0.008
0.065
0.160
0.136
0.160
0.026
RECOR
0.404*
–
0.001
–
–
0.261
0.145
0.033
–
0.080
0.451*
0.168
–
0.367*
NP
Temperature
0.201
0.363
0.353
0.488
0.130
0.834**
0.556*
0.388
0.232
0.210
0.489
0.436
0.616*
0.356
RECOR
Multiple R2
0.737**
–
0.387
–
–
0.440
0.646
0.654
–
0.906**
0.498
0.357
–
0.690
NP
Table 2. Regression values for number of individuals collected in cerrado vegetation (N = 30) and climatic variables at two sites: RECOR and NP. N, abundance;
NCOL, number of monthly collections
240
R. TIDON
© 2006 The Linnean Society of London, Biological Journal of the Linnean Society, 2006, 87, 233–247
50/2
181/9
6/2
776/8
138/12
87/8
89/12
235/10
229/15
3601/13
1039/13
2725/13
45/2
142/9
9407/16
D. cardini
D. immigrans
D. maculifrons
D. malerkotliana
D. mercatorum
D. nebulosa
D. ornatifrons
D. paraguayensis
D. polymorpha
D. simulans
D. sturtevanti
D. willistoni
Scaptodrosophila
Zaprionus
Total
Significance: * P = 0.05; ** P = 0.01
RECOR/16
Taxon
N/N COL.
10256/12
230/8
310/11
34/10
29/3
105/10
119/10
50/12
31/4
3/3
2206/10
365/9
6437/10
–
153/11
PN/12
0.002
0.006
0.000
–
0.003
0.032
0.387**
0.220
0.036
0.002
0.001
0.000
0.004
0.000
0.188
RECOR
0.227
0.201
0.567**
0.083
–
0.645**
0.247
0.047
0.268
–
0.691**
0.155
0.043
–
0.004
NP
Precipitation
0.050
0.080
0.026
–
0.046
0.087
0.162
0.254*
0.000
0.055
0.031
0.102
0.046
0.016
0.124
RECOR
0.057
0.191
0.275
0.003
–
0.154
0.286
0.002
0.049
–
0.277
0.229
0.128
–
0.058
NP
Rel. humidity
0.019
0.109
0.010
–
0.005
0.100
0.074
0.254*
0.045
0.055
0.019
0.020
0.012
0.002
0.217
RECOR
Light
0.213
0.374*
0.272
0.036
–
0.294
0.422*
0.008
0.181
–
0.432*
0.112
0.038
–
0.008
NP
0.070
0.011
0.055
–
0.067
0.064
0.000
0.067
0.011
0.031
0.056
0.176
0.061
0.048
0.025
RECOR
0.518**
0.004
0.124
0.007
–
0.133
0.023
0.040
0.167
−0
0.041
0.535**
0.466*
–
0.332*
NP
Temperature
0.231
0.344
0.173
–
0.303
0.164
0.631*
0.287
0.145
0.191
0.158
0.700**
0.225
0.191
0.252
RECOR
Multiple R2
0.562
0.486
0.907**
0.251
–
0.931**
0.504
0.276
0.462
–
0.922**
0.542
0.508
–
0.444
NP
Table 3. Regression values number of individuals collected in gallery forest vegetation (n = 30) and climatic variables at two sites: RECOR and NP. N, abundance;
NCOL, number of monthly collections
RELATIONSHIPS BETWEEN DROSOPHILIDS AND THE ENVIRONMENT
© 2006 The Linnean Society of London, Biological Journal of the Linnean Society, 2006, 87, 233–247
241
Abundance
R. TIDON
Abundance
242
Total light intensity (°c)
Abundance
Abundance
Relative humidity (%)
Precipitation (mm)
Temperature (°C)
Figure 4. Correlation between environmental attributes in a savanna of National Park of Brasília and the overall sample
abundance of drosophilids.
Table 4. Estimates of species-diversity index (ShannonWiener H′ and Simpson D), evenness (j′), abundance (N)
and species number (S) from communities of drosophilid
species collected from the Cerrado biome at different vegetations and seasons
cerrado wet RECOR
cerrado dry RECOR
cerrado wet NP
cerrado dry NP
forest wet RECOR
forest dry RECOR
forest wet NP
forest dry NP
Figure 5. Diversity of drosophilid species collected in the
Cerrado biome from different vegetations and during
different seasons, measured by the Shannon-Weaver
index (H′) and species number (S). F = forest; S = savanna;
W = wet season, D = dry season; Re = Ecological Reserve
of IBGE, NP = National Park of Brasília.
H′
D
j′
N
S
0.78
1.85
0.64
1.17
1.86
1.77
1.13
1.72
0.31
0.81
0.26
0.55
0.77
0.74
0.53
0.65
0.26
0.80
0.25
0.56
0.66
0.65
0.38
0.61
11424
146
9774
258
1122
327
8496
366
20
10
13
8
17
15
19
17
as commensal with humans (Cooper & Dobzhansky,
1956), has been collected in high frequencies in the
city of Brasília (Ferreira & Tidon, 2005), which has
more climatic similarities with the savanna than with
the forest. Three exotic species have a demonstrated
preference for open vegetation; the African
S. latifasciaeformis and Z. indianus (Wheeler, 1981),
© 2006 The Linnean Society of London, Biological Journal of the Linnean Society, 2006, 87, 233–247
RELATIONSHIPS BETWEEN DROSOPHILIDS AND THE ENVIRONMENT
and D. hydei, which probably originated in Mexico
(Val et al., 1981). The species of the melanogaster
group (D. simulans and D. malerkotliana), as well as
D. busckii, were found in both forests and savannas.
TEMPORAL
DISTRIBUTION OF DROSOPHILIDS
Insect abundances can vary over time for a number of
reasons, including macroclimatic and microclimatic
changes, and variation in the availability of food
resources (Wolda, 1988). In temperate zones, climatic
seasons tend to translate into seasonal activity patterns in living organisms; the higher the latitude, the
shorter the growing season. In the tropics, where seasonal changes in temperature tend to be minimal and
the seasons reflect variations in rainfall or sunshine,
seasonality patterns are poorly known and less understood (Wolda, op cit.). To comprehend how tropical
insect populations respond to seasonal variations, it is
fundamental to clarify their phenological patterns and
life history (Braby, 1995; Pinheiro et al., 2002).
Collecting temperate Drosophila species in the
same locality at different seasons usually reveals that
the abundance of the different species changes greatly
with time and often depends upon the prevailing climatic conditions (Patterson, 1943; Pipkin, 1952; Basden, 1953; Cooper & Dobzhansky, 1956; Mather, 1956;
Paik, 1957; Shorrocks, 1975; Kimura, 1976; Jaenike,
1978a, 1978b; Franck & Valente, 1985; Valente et al.,
1989; Valente & Araujo, 1991; Benado & Brncic, 1994;
Saavedra et al., 1995; Kim, 1996; Rohde & Valente,
1996; Goñi, Martinez & Daguer, 1997).
Tropical forests are considered as systems of great
complexity that may have interesting properties not
present in simpler systems found in temperate climates (Dobzhansky & Pavan, 1950). Studies investigating the seasonality of tropical drosophilids
(Dobzhansky & Pavan, op. cit.; Pipkin, 1953; Heed,
1957; Pavan, 1959; Hunter, 1966; Hunter & Navarro,
1969; Gupta, 1974; Dasmohapatra et al., 1982; Martins, 1987; Tidon-Sklorz & Sene, 1992) do not show
consistent patterns regarding the relationship
between fly abundance and climatic factors. It seems
that in these areas the availability of breeding and
feeding sites plays a decisive role on the population
fluctuation of drosophilids.
Our data on the temporal distribution of drosophilids showed large population fluctuations for most
captured species. Although the majority presented
population peaks in the wet season, some species
restricted to the gallery forest were more abundant in
the dry and cold months. This phenomenon occurred
only in forests, probably because they are more stable
than the savanna, and presents new opportunities for
niches in the dry season due to a population decline of
most drosophilid species. The species diversity (H′ and
243
D) in the dry season was usually higher, and this temporal fluctuation of the drosophilid assemblage probably contributes to the maintenance of biodiversity in
this region.
Despite the negative correlations eventually
observed between the populations of some species
(D. sturtevanti, Sgr. willistoni, S. latifasciaeformis and
Z. indianus) and temperature, there does not appear
to be a limiting climatic factor for the temporal distribution of the drosophilids, since the region usually
does not present extremes that would compromise
their development. Activity of Drosophila species
occurs within certain limits of temperature (Grossfield, 1978), and more extreme values (below 12 °C or
above 32 °C) can be tolerated if applied for a period
shorter than the total development time (David et al.,
1983). Some desert species of Drosophila, however, are
able to survive even stronger heat stress (Stratman &
Markow, 1998). Although the extremes of temperature
observed during this study were 7.8 °C and 33.4 °C,
the minimum and maximum monthly average temperatures (10.6 °C and 29.7 °C) appear to allow survival
and reproduction.
Relative humidity is one of the factors that serve as
a boundary condition for maintaining the activity of
drosphilids, and this factor interacts with temperature and light to control voluntary movements of flies
in the field (Grossfield, 1978). According to Tauber
et al. (1998), moisture is one of the major physical factors that influence insect seasonal ecology, but its
importance has been neglected in phenological
studies.
Even though the majority of the species showed
population growth in the wet season, variations in
precipitation or relative humidity seem to affect
the temporal distribution of the exotic species
more effectively, since the distribution of most of
them (D. malerkotliana, D. immigrans, D. simulans
and Z. indianus) correlated significantly with these
parameters. Amongst the Neotropical species, this
effect was observed only in D. mercatorum and
D. ornatrifrons, which showed low but significant correlations with monthly precipitation and humidity,
respectively. These results, added to the fact that some
endemic species showed peaks of abundance in the dry
season, suggest that the species that evolved in the
region are better adapted to local conditions.
Light intensity is considered a major factor in determining flight activity. Bright light has been reported
to inhibit activity and prevent flight, and avoidance of
bright light in the field has been noted for many
species (Grossfield, 1978). Although the abundance
of all species was inversely proportional to the light
intensity, these correlations were significant only
for D. cardini, D. mercatorum, D. nebulosa and
D. simulans.
© 2006 The Linnean Society of London, Biological Journal of the Linnean Society, 2006, 87, 233–247
244
R. TIDON
These results need to be approached with caution,
because correlations between drosophilid abundance
and climate were found to be, in general, low, with
inconsistencies between RECOR and NP. It is possible
that our data would have been different had they been
taken directly from the microhabitats where the
drosophilids actually live.
A factor that was not controlled for in this work, but
that is usually used to explain temporal fluctuations of
drosophilids, is the peculiar availability of breeding
and feeding sites during the year (Pipkin, 1953; Birch
& Battaglia, 1957; Rohde & Valente, 1996). Pipkin
(1964) investigated the influence of breeding and feeding sites for 62 species of Neotropical forest-dwelling
Drosophila in Panama, and found that populations of
species that use small drier fallen fruits and blossoms
expand during the wet season, when these sites suffer
less from desiccation, while those that use fleshy fruits
may expand in the dry season, since their substrate
resists drought during this period. This hypothesis
should be tested in the Cerrado biome.
HABITAT
SELECTION AND MIGRATION
There is some evidence that habitat choice is occurring
on a fine scale in Drosophila (Shorrocks & Nigro,
1981), and that it is genotype-dependent (Powell,
1997). In Brazil, Valente & Araujo (1985) showed that
different second and third chromosome karyotypes of
D. willistoni were differentially attracted to different
types of fruits, and that different proportions of karyotypes emerge from different substrates. The search
for favourable habitats may also involve dispersal,
which occurs when conditions are too dry, wet, bright,
dim, hot or cold or when food is absent.
Species richness in the savanna clearly diminished
in the dry season, rising again in the wet season (Fig.
5). It is possible that some drosophilids migrate from
this open vegetation to the forests in the dry season,
since climatic conditions should then be less stressful.
The magnitude of dispersal among drosophilid species
is highly variable, and it appears that the species with
the greatest oligophagy show the greatest effective
mobility (Powell, 1997). In unfavourable territory like
deserts, adults may travel several kilometers in a few
days (Jones et al., 1981; Coyne et al., 1982; Coyne,
Bryant & Turelli, 1987; Markow & Castrezana, 2000).
Since the Cerrado biome is a mosaic of vegetation
types relatively close to each other, it should be possible for drosophilids to migrate among them.
The argument that gallery forests ‘act as nucleus
for re-colonization of deciduous habitat’ has been
already proposed for vespids (Forsyth, 1980; Diniz &
Kitayama, 1998), for which foraging habitats seem to
vary temporally; during the dry season these insects
are more diverse and abundant in gallery forests. Sev-
eral experiments with drosophilids suggest that
demes regularly connected by migration may become
extinct in the stressful season, being re-established
later by migrants (Bryant, 1976; Moore, Taylor &
Moore, 1979; Jones et al., 1981; Moore & Moore, 1984;
Kimura & Beppu, 1993). This population structure
may homogenize neutral genetic variation among populations, reducing the possibility that well-known
morphological, inversion, and allozyme clines are
caused by historical accidents or genetic drift (Coyne
& Milstead, 1987).
Hoffmann et al. (2003) showed that the Australian
tropical rainforest fly D. birchii exhibits clinal variation in desiccation resistance, but the most resistant
population lacks the ability to evolve further resistance even after intense selection for over 30 generations. In the Cerrado biome, most species from the
savanna-like vegetation were also present in forests,
although the reverse was not true, suggesting the lack
of ability of some species to explore the drier neighbourhoods of the latter. We would do well to heed Diniz
& Kitayama (1998), who warn of ‘the extreme importance of the moist habitats for the maintenance of
vespid colonies during the long dry season in the cerrado area’, and advocate ‘therefore, it is necessary to
preserve all kinds of habitats in the Cerrado (biome),
mainly due to the faunal spatial and temporal variation’. These recommendations will surely help to
preserve both the drosophilid flies and many other
organisms of the region.
ACKNOWLEDGEMENTS
This article was written during sabbatical leave at
Harvard University. I am grateful to R. C. Lewontin,
A. C. Franco and R. Henriques for their comments on
the manuscript, and to D. F. Leite and B. D. F. Leão for
their valuable help in the field and laboratory work.
Parque Nacional de Brasília, Reserva Ecológica do
IBGE, and Universidade de Brasília provided logistic
support. This work was financially supported by the
Conselho Nacional de Desenvolvimento Científico e
Tecnológico (CNPq).
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APPENDIX: AUTHORITIES FOR THE
MENTIONED SPECIES
Drosophila ararama Pavan and Cunha
Drosophila aragua Vilela and Pereira
Drosophila arauna Pavan and Nacrur
Drosophila atrata Burla and Pavan
Drosophila austrosaltans Spassky
Drosophila bandeirantorum Dobzhansky and Pavan
Drosophila bocainensis Pavan and Cunha
Drosophila buskii Coquillett
Drosophila cardini Sturtevant
Drosophila cardinoides Dobzhansky and Pavan
Drosophila fuscolineata Duda
Drosophila guaru Dobzhansky and Pavan
Drosophila hydei Sturtevant
Drosophila immigrans Sturtevant
Drosophila maculifrons Duda
Drosophila malerkotliana Parshad and Paika
Drosophila mediopunctata Dobzhansky and Pavan
Drosophila mediostriata Duda
Drosophila mercatorum Patterson and Wheeler
Drosophila mesostigma Frota-Pessoa
Drosophila nebulosa Sturtevant
Drosophila neocardini Streisinger
Drosophila nigricruria Patterson and Mainland
Drosophila onca Dobzhansky and Pavan
Drosophila ornatifrons Duda
Drosophila pallidipennis Dobzhansky and Pavan
Drosophila paraguayensis Duda
Drosophila paramediostriata Townsend and Wheeler
Drosophila paranaensis Barros
Drosophila polymorpha Dobzhansky and Pavan
Drosophila prosaltans Duda
Drosophila schildi Malloch
Drosophila simulans Sturtevant
Drosophila sturtevanti Duda
Drosophila willistoni Sturtevant
Zaprionus indianus Gupta
D. latifasciaeformis is currently included in the genus
Scaptodrosophila latifasciaeformis (Duda)
© 2006 The Linnean Society of London, Biological Journal of the Linnean Society, 2006, 87, 233–247