Behavioral Ecology Advance Access originally published online on July 21, 2004
Behavioral Ecology 2005 16(1):316-322; doi:10.1093/beheco/arh125
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Dispersal and prepupation behavior of Chilean sympatric Drosophila species that breed in the same site in nature
a Departamento de Biología, Facultad de Ciencias, Universidad de Playa Ancha, Valparaíso, Chile, and b Programa de Genética Humana, ICBM, Facultad de Medicina, Universidad de Chile, Independencia 1027, Casilla 70061, Santiago-7, Chile
Address correspondence to R. Godoy-Herrera. E-mail: rgodoy{at}machi.med.uchile.cl.
Received 10 September 2002; accepted 1 April 2004.
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ABSTRACT |
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 TOP ABSTRACT INTRODUCTIONMETHODSRESULTSDISCUSSIONREFERENCES |
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We investigated dispersal patterns of Drosophila larvae searching for pupation sites over three substrates to determine the role of spatial heterogeneity and presence of other species on prepupation behavior. We used D. melanogaster, D. hydei, and D. pavani whose parents emerged from apples collected in one orchard. Each species showed different preferences for substrates on which to pupate, particularly in the presence of another Drosophila species. Larval locomotion rate and turning behavior in D. melanogaster, D. hydei, and D. pavani were modified depending this upon the type of substrate (agar and sand) on which the larvae crawled. These two behaviors are involved in dispersal and aggregation of pupae. Distance between pupae of the same species decreases when larvae of another species pupate on the same substrate. Aggregated distributions over the substrates lead to patches with few or no individuals. These could serve as pupation sites for other Drosophila species that, in nature, also emerge from small breeding sites.
Key words: breeding sites, pupation behavior, sympatric Drosophila species.
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INTRODUCTION |
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TOPABSTRACTINTRODUCTIONMETHODSRESULTSDISCUSSIONREFERENCES |
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Dispersal is a life history trait that affects the distribution and abundance of species, with consequences for community structure (Dieckermann et al., 1999
). Dispersal may also reduce intra- and interspecific competition for food and space, contributing to coexistence of species (Shorrocks and Bingley, 1994). Research on the behavioral basis of dispersal in relation to utilization of food and space could also help to discover which behavioral patterns contribute to this coexistence in the wild (Nunney, 1990) and may reveal how local guilds that share common resources can coexist and persist through time (Martin and Martin, 2001).
In Drosophila, larval patterns of movement are central to understanding foraging strategies and selection of pupation sites (Godoy-Herrera and Silva-Cuadra, 1998; Sokolowski, 1986). However, most studies on larval prepupation behavior of Drosophila have used food vials as the substrate. Pupation site preference has been measured by the distance between the surface of the substrate and the pupa location (review in Singh and Pandey, 1993). This experimental design provides little insight into features of the environment that may regulate dispersal patterns of larvae searching for pupation sites. Wong et al. (1985), Godoy-Herrera et al. (1989), and Godoy-Herrera and Silva-Cuadra (1997, 1998) observed that larvae of Drosophila melanogaster, Drosophila pavani, Drosophila gaucha, and of the reciprocal interspecific hybrid between the latter two species react to humidity, light, and to substrate texture and consistency. Nevertheless, no studies link prepupation behavior of Drosophila with larval dispersal patterns in heterogeneous environments and coexistence of species that breed in the same sites in the wild.
Larval dispersal behavior of Drosophila has a genetic component, which is important in the colonization of new niches and the expansion of populations (de Souza et al., 1970). Aspects of choice of pupation site by Drosophila also have a genetic basis (Grossfield, 1978; Sokolowski et al., 1986). For example, pupation by D. melanogaster on dry substrates outside the food cup is dominant over pupation inside the cup; there is also additive variation (Godoy-Herrera et al., 1989). Singh and Pandey (1993) found that pupation height in shell vials in Drosophila ananassae is under polygenic control and most of the variance is additive. The type of pupation site selected by larvae also affects pupal survival of D. melanogaster (Rodriguez et al., 1992; Sokal, 1966). When placed on dry substrates, D. pavani and D. gaucha pupated both outside and inside the food cup, while the interspecific hybrid larvae did so only inside the cup (Godoy-Herrera and Silva-Cuadra, 1997). Drosophila simulans, Drosophila hydei, and Drosophila busckii, which share the same breeding sites in the Central Valley of Chile, show different substrate preferences to form puparia. For example, D. busckii larvae select humid substrates with a smooth surface for pupation, whereas D. simulans larvae select humid substrates with a rough surface (Godoy-Herrera and Silva-Cuadra, 1998).
In this work we propose that the larval movement patterns of Drosophila species observed to form puparia contribute to their coexistence. To test this hypothesis, we compared substrate preferences of larvae from of each three species that had emerged from the same rotten apples collected in one orchard in the presence and absence of another Drosophila species. We also recorded movement patterns on two substrates of larvae while searching for pupation sites. Additionally, we measured aggregation of pupae in the presence and absence of another Drosophila species. These studies enabled us to explore how habitat heterogeneity interacts with the presence of another Drosophila species to influence movement and dispersal of larvae searching for pupation sites.
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METHODS |
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Subjects
We used wild type D. melanogaster (subgenus Sophophora, melanogaster group), D. hydei (subgenus Drosophila, repleta group), and D. pavani (subgenus Drosophila, mesophragmatica group). Flies were collected in April of 1999 (Autumn in Chile) in Chillán, 420 km south of Santiago. In this season Chilean populations of Drosophila reach their peaks of abundance (Brncic, 1980
). Collections were made in an orchard of the University of Concepción (Faculty of Agronomy). This is a humid site in which ornamental plants, native vegetation, and tomatoes and grapes grow together with cherry, plum, medlar, apple, and peach trees. Once these fruits fall on the ground, Drosophila use them as breeding sites (Brncic, 1980, 1987).
We used eggs and larvae of D. melanogaster, D. hydei, and D. pavani whose parents had emerged from 10 overripe apples (Red Delicious variety) collected in an orchard. Ten of these fruits were individually deposited into 500 cc flasks kept at 22°C in the laboratory. The stock population for each of the three species was established from a mixture of 10 males and 10 females emerged from each of the 10 fruits (i.e., a total of 200 individuals). The amount of genetic variability in the stocks was not estimated. Other Drosophila species (D. simulans, D. repleta, D. immigrans, D. busckii, and D. subobscura) also emerged from the collected apples. D. melanogaster, D. hydei, and D. pavani pupae can be distinguished morphologically. The D. melanogaster pupae are brown-yellow in color and measure 3.50 ± 0.05 mm (N = 120), whereas those of D. hydei and D. pavani measure 4.50 ± 0.01 mm (N = 120) and are brown-black in color. D. hydei and D. pavani pupae can be distinguished by their horn shapes; D. hydei pupae have curved horns while D. pavani pupae have V-shaped horns. Pupae of D. simulans, D. repleta, D. immigrans, D. busckii, and D. subobscura, which also emerged from the apples, could not be distinguished morphologically from those of the species used in the present experiments. No more than four generations had elapsed between the establishment of the populations and their use in the present study. The stocks were kept in half-pint bottles containing 50 cc of Burdick's medium (1954) at 24°C.
Eggs and larvae collection
Groups of 60–70 inseminated females were allowed to lay eggs for 3–4 h on plastic spoons filled with culture Burdick's medium. Eggs were collected with a dissecting needle. For the single species experiments, 100 eggs were sown on individual 2.0 x 2.0 cm cups filled with Burdick's medium. For the experiments using two species, 50 24-h old larvae of each of the species of the following dyads were placed in the same cup: (1) D. melanogaster and D. hydei, (2) D. melangaster and D. pavani, and (3) D. hydei and D. pavani. Previous observations had shown that mortality of D. hydei and D. pavani was over 95% when their eggs were sown together with those of D. melanogaster in the same rearing cup. However, mortality decreased to 25–30% when 24-h old larvae of D. melanogaster were deposited together with 24-h old larvae of either of the other two species. This is comparable to that obtained in single species cultures. D. melanogaster egg chorion may contain some substances that increase mortality of D. pavani and D. hydei preadults.
Behavioral experiments
The experimental design was modified from de Souza et al. (1970) (Table 1). We used 10 x 10 x 10 (wide x long x high) cm transparent plastic boxes as described by Godoy-Herrera et al. (1989). All the boxes were situated in the same area of the rearing chamber to avoid variations in illumination and temperature.
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Pupation substrate preferences
Pupation substrate preferences of D. melanogaster, D. hydei, and D. pavani were tested by offering the larvae three different substrate combinations with two treatments in each. The treatments were each species alone versus presence of another Drosophila species, then the three possible pairwise substrate combinations (Table 1). Each treatment of each substrate combination contained four replicates. For each of the species, a set of eight plastic boxes were filled with 3% agar to a depth of 2 cm. Then, an area of agar measuring 10.0 x 5.0 cm was removed along one side to leave a dry surface. In the first experiment, a 2.0 x 2.0 cm food cup was placed at the bottom of four boxes. Thus, larvae could choose to pupate either on agar, plastic, or in the rearing cup (experiment 1, Table 1). In the second experiment, the plastic part of four boxes was filled with yellow dry sand forming a 2-cm thick layer (experiment 2, Table 1). The number of pupae outside (plastic, agar, and sand) and inside of the rearing cup was recorded prior to eclosion. Finally, larval preferences for two kinds of dry substrates were tested (experiment 3, Table 1). Floor measuring 10.0 x 5.0 cm of four plastic boxes was filled to a depth of 2 cm with dry yellow sand. To keep the sand to one side of the box, two pieces of the same type of plastic measuring 4.0 x 2.0 cm (length x height) were placed between the cup and each of the opposite sides of the box. The boxes were maintained for six days (D. melanogaster) and 12 days (D. hydei and D. pavani) at 24°C. These substrates allowed control of contamination by fungi and bacteria.
Larval dispersal distances
Larval dispersal activity of the three species on each of the substrates was evaluated in the presence and absence of another Drosophila species. The distance between the pupae found on the surface of the plastic, agar, and sand and the center of the cup (experiments 1, 2, and 3, Table 1) was recorded. Normality of the frequency distributions was also tested under the presumption that a departure from normality might indicate a tendency for conspecific larvae to pupate near each other.
Nearest neighbor analysis
Pupal aggregation in the substrates of each of the three species was recorded, in the presence and absence of another species. First, the position of each of the pupae on the substrates outside of the rearing cup was registered. Then, the distance to the nearest neighbor was measured using a 0.5 cm Cartesian grid. In the experiments with two species, we also recorded species identity of the nearest neighbor pupae. Pupae distributions were analyzed using the nearest neighbor method of Clark and Evans (1954). The average distance to the nearest neighbor of the same species (rA) obtained in the single species treatments was compared with the expected value (rE) for the same number of individuals randomly distributed on an area of equal size (rE = 
V–
), where is the pupal density. The ratio R = (rA/rE), reflects the form of the spatial distribution of individuals (aggregated, random, overdispersed). Its value ranges between R = 0 (maximum aggregation) and R = 2.15 (uniform). When individuals are randomly distributed then R = 1. The analysis was repeated for the mixed species treatments. Then, we compared R-values from single and mixed species treatments using ANOVA (Clark and Evans, 1954).
Searching patterns
Pupation site choice by Drosophila larvae depends on the larval patterns of movement on different substrates (Sokolowski et al., 1986). Samples of 50 late third instar larvae of D. melanogaster, D. hydei, and D. pavani were collected from the walls of the culture bottles. Larvae were individually deposited on agar or dry sand. Each larva was tested on new agar and sand. Larvae might remain motionless on the substrates. Once each larva began to move, the trail made by each larva was drawn for a period of two min using a Wild M5 camera lucida. The trail length was measured as described in Sokolowski (1980). These measurements provided an estimate of locomotion. Larval turning behavior was also estimated by counting the number of directional changes in each trail.
Statistical analysis
We used a G-test of Independence (Sokal and Rohlf, 1995) to determine whether the number of pupae inside the rearing cup in each treatment and substrate combination (Table 1) was significantly different from that found outside the cup. We examined homogeneity for replicates within substrate combinations (single and mixed species) using the R x C test of Independence (Sokal and Rohlf, 1995).
Normality of pupae distributions outside the rearing cup (plastic, agar, and dry sand) was examined using a Kolmogorov-Smirnov test, and homogeneity of variances was also determined with Bartlett's test in the single and mixed species treatments. The skewness (g1) and kurtosis (g2) of the data were also calculated. These statistics were used to estimate aggregation.
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RESULTS |
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TOPABSTRACTINTRODUCTIONMETHODSRESULTSDISCUSSIONREFERENCES |
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The replicates in each treatment and substrate combinations were not shown to be significantly different. So, the data were pooled as shown below. However, the data were not normally distributed (Kolmogorov-Smirnov test, D = 86, p < .05), although variances were homogeneous (Bartlett's test,
). Therefore, nonparametric statistics were used to analyze the data.
Larval substrate preferences
In the single species experiments, D. melanogaster larvae pupated on dry sand whereas D. hydei and D. pavani larvae pupated on agar (Figure 1, first row). The distributional pattern of D. melanogaster pupae was not modified by the presence of D. hydei or D. pavani preadults (Figure 1, first column). On dry sand, D. hydei and D. pavani pupae distributions also did not differ in the absence and presence of another Drosophila species (Figure 1; G-test of Independence values were all below critical value, 
).
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When the rearing cup was surrounded by agar and plastic (Figure 2), most D. melanogaster, D. hydei, and D. pavani pupae were observed on agar. In the presence of D. hydei and D. pavani, D. melanogaster larvae also used the plastic to pupate (G-test of Independence, presence versus absence of D. hydei and D. pavani,
2 = 20.83 and 22.18, respectively, df = 2, p < .01). In contrast, most D. hydei and D. pavani larvae left the cup in the presence of the other Drosophila species pupating (over 70 %) on agar (Figure 2). Nevertheless, in the presence of D. melanogaster larvae, about 11% of D. hydei pupae were detected on the plastic (G-test of Independence, D. hydei, presence versus absence of D. melanogaster, 2 = 10.21, df = 2, p < .05). About 30% of D. pavani pupae were also found on the plastic when D. hydei was present (Figure 2; G-test of Independence, D. pavani, presence versus absence of D. hydei, 2 = 15.22, df = 2, p < .05).
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When the cup was surrounded by dry sand and plastic (experiment 3; Table 1), most D. melanogaster and D. hydei larvae pupated in the rearing cup (Figure 3, first row). In contrast, 100% of D. pavani pupae were detected outside the cup on the sand (Figure 3, first row). This situation changed in the presence of another Drosophila species. For example, when D. hydei or D. pavani were present, most of D. melanogaster pupae were on the plastic (Figure 3, first column; G-test of Independence: (1) presence versus absence of D. hydei,
2 = 24.36, df = 2, p < .001; (2) presence versus absence of D. pavani, 2 = 32.18, df = 2, p < .01).
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In the case of D. hydei, most of the pupae were detected outside the cup on the plastic when D. melanogaster or D. pavani larvae were present (Figure 3, second column; G-test of independence: (1) presence versus absence of D. melanogaster,
2 = 31.13, df = 2, p < .01; (2) presence versus absence of D. pavani, 2 = 29.47, df = 2, p < .01).
D. pavani larvae tended to pupate in the rearing cup when D. melanogaster was present (Figure 3, third column). In the presence of D. hydei, D. pavani larvae pupated on the plastic (G-test of Independence values exceeded the critical value, 2 = 5.99, df = 2, p < .01; Figure 3).
Aggregation in the presence and absence of another Drosophila species
Outside the rearing cup (the plastic, agar, and dry sand) larvae of D. melanogaster, D. hydei, and D. pavani formed puparia near other larvae, as shown by the distributional pattern of pupae on the substrates (skewness [g1] and kurtosis [g2] values fluctuated between 10.54 and 32.14). The Z-values calculated to evaluate the goodness-of-fit of pupae distributions with respect to a normal distribution exceeded the critical two-tailed value (all Z > Z0.05 = 1.96, p < .05).
Larval aggregation behavior of D. melanogaster, D. hydei, and D. pavani on the plastic, agar, and sand was also estimated by recording distances (cm) between pupae of one species in absence or presence of Drosophila species (Table 2). The distance between the nearest neighbor pupae of the same species decreased in the presence of another Drosophila species (Kruskal-Wallis one way ANOVA values were all greater than the critical value H = 10.88, df = 2, p < .001). Nearest neighbor analysis also yielded significant values of R (Clark and Evans, 1954), indicating that the pupae are aggregated (R < 1; Kruskal-Wallis test values exceeded the critical value H = 5.99, df = 2, p < .05). In the presence of another Drosophila species, the calculated R-values were statistically lowest than the R-values yielded in the single experiments (Kruskal-Wallis one way ANOVA values were greater than the critical value H = 5.99, df = 2, p < .05).
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Larval dispersal and patterns of movement
In the absence of another Drosopohila species, the distance at which larvae of D. melanogaster, D. hydei, and D. pavani pupated varied depending on the substrate (Table 3). When another Drosophila species was present, most larvae of D. melanogaster, D. hydei, and D. pavani modified their dispersal activities. The magnitude of change in dispersal depended on the type of substrate and which of the species was present (Table 3). For instance, when alone and on agar D. melanogaster larvae tended to pupate at 4.45 ± 0.32 cm away from the rearing cup, whereas in the presence of D. pavani they pupated at a distance of 1.36 ± 0.82 cm (Table 3). In contrast, on the same substrate, in the absence of D. melanogaster most D. pavani pupae were detected at 5.63 ± 1.15 cm away from the cup, and they were detected at 5.86 ± 1.15 cm when D. melanogaster was present (Table 3). For most of the comparisons of presence versus absence of another species, the Kruskal-Wallis test values exceeded the critical value (H = 3.84, df = 1, p < .05). We conclude, therefore, that Drosophila larvae that coexist with other species in the same breeding sites respond to substrate features and to the presence of larvae of other species of the genus, modifying their dispersal patterns.
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To understand better how D. melanogaster, D. hydei, and D. pavani third instar larvae disperse over the agar and sand, we drew the trails made by the preadults on those substrates. The length of the trails was an estimation of locomotion, and mean turning behavior was calculated from number of changes in direction shown by the trails. On agar, D. hydei and D. pavani larvae exhibited similar rates of locomotion (Kruskal-Wallis test value H = 1.68, df = 1, NS); D. melanogaster larvae move slowly on this substrate (Kruskal-Wallis test values: (1) D. melanogaster versus D. hydei: H = 12.16, df = 1, p < .01); (2) D. melanogaster versus D. pavani: H = 13.11, df = 1, p < .01). On agar, turning rates of D. melanogaster and D. pavani were lower than that of D. hydei (Kruskal-Wallis test values: (1) D. melanogaster versus D. pavani: H = 2.63, df = 1, NS; (2) D. melanogaster versus D. hydei: H = 16.61, df = 1, p < .01; (3) D. hydei versus D. pavani: H = 8.37, df = 1, p < .01).
On the sand, D. melanogaster and D. pavani larvae decreased their locomotion, whereas D. hydei preadults showed an increase in this behavior (Table 4; Kruskal-Wallis test values: (1) D. melanogaster versus D. pavani: H = 1.32, df = 1, NS; (2) D. hydei versus D. melanogaster: H = 34.28, df = 1, p < .01; (3) D. hydei versus D. pavani: H = 23.91, df = 1, p < .01). All three species show less larval turning behavior on dry sand than on agar (Table 4; Kruskal-Wallis test values were nonsignificant).
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DISCUSSION |
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TOPABSTRACTINTRODUCTIONMETHODSRESULTSDISCUSSIONREFERENCES |
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Cosmopolitan D. melanogaster and D. hydei and endemic D. pavani species bred on the same orchard differ in their larval prepupation behavior. First, the larvae show different preferences for pupation substrates. Second, pupa aggregation increases in the presence of another Drosophila species. As a result of these behaviors, pupae of one species are separated from pupae of another species. In addition, late third instar larvae of D. melanogaster, D. hydei, and D. pavani collected in the same orchard pupated at differing depths in the substrate (Godoy-Herrera and Silva-Cuadra, 1997
, 1998). At 24°C, D. melanogaster has a shorter larval period (4 days) than that of D. hydei and D. pavani (7 days). This difference may mean that D. melanogaster larvae leaving the rearing cup do not encounter pupae of the other species. Why, then, did D. melanogaster larvae modify their pupation behavior when larvae of another species were present? Perhaps recognition of conspecific and alien larvae occurs when first and second instar larvae are feeding. The recognition could be expressed later through pupal aggregation. Further studies are planned to investigate this idea.
In the Central Valley of Chile, a substantial number of Drosophila species use decaying apples, plums, and grapes as breeding sites (Brncic, 1987). These abundant, discrete small breeding sites favor interactions among larvae of the same or different species. Environmental heterogeneity may favor species coexistence if D. melanogaster, D. hydei, and D. pavani larvae show different preferences for pupation substrates. Pupa aggregations of one species via recognition of conspecific and alien larvae also reduce competition for space. Thus, these two features of Drosophila species larval behavior may contribute to their coexistence.
In the wild, ecological conditions of Drosophila breeding sites change in a relatively short time (Atkinsons and Shorrocks, 1984; Shorrocks and Bingley, 1994; Shorrocks and Rosewell, 1987). In changing environments organisms may evolve diverse traits characterized by a high phenotypic plasticity (Levins, 1968). Our results show that larval prepupation behavior of D. melanogaster, D. hydei, and D. pavani exhibit such plasticity, as expected given the changing features of decaying fruits used as breeding sites.
On the other hand, genetic polymorphisms in a variable environment are possible when the populations are regulated by density dependence in each habitat (Levene, 1953). Thus, European larvae of D. melanogaster that remain in the upper layer of the substrate are more infested by a parasitic Hymenoptera than are those that dig into the medium. "Rover" larvae go deeper into the substrate than "sitter" preadults (Carton and David, 1985). In this way, the parasite helps maintain the frequencies of "rover" and "sitter" larvae of D. melanogaster in the wild (Carton and Sokolowski, 1992). In contrast, in Chile, monthly collections of D. melanogaster, D. hydei, D. pavani, and other Drosophila species for over 40 years have been unsuccessful in revealing any parasitic Hymenoptera (Brncic, 1980). Chilean Drosophila communities change through the year. This suggests that seasonal fluctuations in physical environmental factors, abundance of breeding sites, and presence of other Drosophila species could be important evolutionary pressures to regulate larval dispersal, preferences for pupation substrates and pupa aggregations. Recent field observations on the behavior of third instar larvae that have left natural decaying fruit-breeding Drosophila show that highly aggregated pupae distributions are commonly observed in the wild (unpublished data).
Dispersal and aggregation of pupae depended on larval movement patterns. Heterogeneity of the substrates can greatly modify locomotion rate and turning behavior of D. melanogaster, D. hydei, and D. pavani larvae (Table 4). In particular, on the sand, larval movement of D. melanogaster and D. pavani larvae tends to be slower than on other substrates. However, D. hydei larvae increased their locomotion on this substrate. The energetic cost of larval crawling is higher than walking, flying, or swimming (Berringam and Lighton, 1993). As larval dispersal takes place, the forces generated by surface tension over a relatively large area must be overcome, and friction is produced in contact with the surface (Casey, 1991). The frequencies of locomotion, turning, and bending behavior exhibited by Drosophila larvae (Green et al., 1983) imply a significant energetic cost. This cost should be lower when the larvae crawl on a moist surface such as agar, and it should be higher on substrates such as sand. We noted that in the case of D. melanogaster and D. pavani larvae, their movements seemed to decrease as the number of obstacles in the landscape increased. This might be expressed in an increase in larval settlement rates, and thus in pupa aggregation. In contrast, D. hydei larvae, which increase their movement on the sand, might pupate and aggregate far from D. melanogaster and D. hydei pupae.
Spatial heterogeneity influences habitat selection, foraging ecology and space utilization, and refuge from predation (Bond et al., 2000). On the other hand, the interactions between biotic and abiotic influences on habitat use have important implications for coexistence of scramble type competitors species that share common resources (Martin and Martin, 2001). This is the case for Drosophila species that appear to occupy similar ecological niches (Powell, 1997). In mixed species tests, pupae of D. melanogaster, D. hydei, and D. pavani showed aggregated distributions over the substrates, creating patches with few or no individuals. These could serve as potential pupation sites for other Drosophila species, such as those that also lived in the orchard (D. simulans, D. repleta, D. immigrans, D. busckii, and D. subobscura).
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ACKNOWLEDGEMENTS |
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This work is a part of the M. C. Medina-Muñoz Master's Thesis in Environmental Education. M.C.M.-M. thanks the Postgraduate Studies School, Universidad de Playa Ancha de Ciencias de la Educación, Valparaíso, Chile for financial support. R.G.-H. wishes to thank Kevin J. Connolly and Barrie Burnet for their warm hospitality in the Psychology Department, Sheffield University, UK and for their constructive comments and criticisms of the manuscript. We also are indebted to Susi Koref-Santibañez for all her very useful comments. We wish to thank two anonymous referees for critical commments on the manuscript. We are particularly indebted to Marlene Zuk for her splendid editorial help and for her patience with our English. R.G.-H. also thanks The Royal Society of London (UK) and CONICYT (Chile) for a Study Visit grant which made the travel to the UK possible. This work was supported by FONDECYT 1020130, and it is dedicated to R.G.-H.'s wife Alejandra Rosas-Rosas, Rosita Herrera-Sepúlveda, Raúl Godoy-Osses, and Rosita Herrera-Godoy.
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