versión impresa ISSN 1519-566X
Neotrop. Entomol. v.34 n.3 Londrina mayo/jun. 2005
ECOLOGY, BEHAVIOR AND BIONOMICS
Population dynamics of the invasive species Zaprionus indianus (Gupta) (Diptera: Drosophilidae) in communities of drosophilids of Porto Alegre City, Southern of Brazil
Dinâmica de populações da espécie invasora Zaprionus indianus (Gupta) (Diptera: Drosophilidae) em comunidades de drosofilídeos da cidade de Porto Alegre, RS
Norma M. da SilvaI; Carina da C. FantinelI; Vera L.S. ValenteI; Victor H. ValiatiI, II, III
IDepto. Genética, Instituto de Biociências, Univ. Federal do Rio Grande do Sul, C. postal 15053 Av. Bento Gonçalves, 9500, 1501-970, Porto Alegre, RS
IILab. Biologia Molecular, Centro de Ciências da Saúde Univ. do Vale do Rio dos Sinos, C. postal 275, 93022-000, São Leopoldo, RS
IIICentro de Ciências da Saúde Univ. Luterana do Brasil, Canoas, RS
Population studies of invasive species allow us to understand how invaders react to new biotic and abiotic conditions, and how native species react to invasion. We evaluated the colonisation efficiency of the invader Zaprionus indianus (Gupta), in the urban area of Porto Alegre city, southern of Brazil. Samples of flies were taken from three urban parks, and ecological indexes were used based on the frequency of the sampled species. The indexes were calculated for breeding and feeding sites separately. The highest frequencies of Z. indianus compared to the other drosophilids were registered during seasons of highest mean temperatures, both for the feeding and the breeding sites. The highest values for the dominance index (D) and the lowest values for diversity (H') were found at the same seasons and for both components. An analysis of the values for Morisita similarity index shows that the Botanical Garden and Farroupilha Park had higher similarity in terms of diversity of the breeding sites. For the feeding sites the highest similarity was between Farroupilha Park and Gabriel Knijnik Park. Despite the three parks have some particularities, the ease with which Z. indianus became established at these places seem to be the same. The arrival of this invader seems to be promoting adjustments in the survival strategies of the resident species, at least at certain periods when the frequency of the populations of the invader increases significantly. However, most of species seem to be able to coexist with the invader.
Key words: Biological invasion, ecological index, urban park
Estudos em populações de espécies invasoras permitem entender como os invasores reagem às novas condições bióticas e abióticas, e como espécies nativas reagem à invasão. Avaliou-se a eficiência de colonização da invasora Zaprionus indianus (Gupta), na área urbana da cidade de Porto Alegre, RS. Amostras de moscas foram tomadas de três parques urbanos, e índices ecológicos foram usados baseados na freqüência das espécies amostradas. Os índices foram calculados para sítios de oviposição e alimentação separadamente. A maior freqüência de Z. indianus comparada aos outros drosofilídeos foi registrada nas estações de temperaturas médias maiores, tanto para o componente sítio de alimentação como o de oviposição. Nessas mesmas estações, e para ambos os componentes, foram encontrados os maiores valores do índice de dominância (D) e os menores valores de diversidade (H'). Uma análise dos valores do índice de similaridade de Morisita mostrou que o Jardim Botânico e o Parque Farroupilha apresentam maior similaridade em termos de diversidade para o componente sítio de oviposição. Para o componente sítio de alimentação a maior similaridade foi entre Parque Farroupilha e Parque Gabriel Knijnik. Apesar de os três parques apresentarem algumas particularidades, a facilidade de estabelecimento de Z. indianus nesses locais parece ter sido a mesma. A chegada da invasora parece estar promovendo ajustes nas estratégias de sobrevivência das espécies residentes, pelo menos em certos períodos quando a freqüência das populações da invasora aumenta significantemente. Entretanto, pelo menos a maioria das espécies parece ter condições de coexistir com a invasora.
Palavras-chave: Invasão biológica, índice ecológico, parque urbano
Recognition of the impact of biological invasions on the Earth's ecosystems has received ample attention from researchers to try to understand the factors that affect them (Vitousek et al. 1997). Recent reviews have considered invasions from a variety of viewpoints, including biological characteristics of invaders (Kolar & Lodge 2001), ecological characteristics of invaded communities (Lonsdale 1999, Tsutsui et al. 2000), interference of the invader in resources availability (Sher & Hyatt 1999, Davis et al. 2000) and presence of natural enemies and occupancy of space (Keane & Crawley 2002). Moreover, some studies "suggest that the invasion success of many species might depend more heavily on their ability to respond to natural selection than on broad physiological tolerance or plasticity" (Lee 2002). Accordingly, these findings emphasize the utility of genomic approaches for determining invasion mechanisms, through analysis of gene expression, gene interactions, and genomic rearrangements that are associated with invasion events. As these issues are not independent, it is essential to find ways of considering them jointly (Shea & Chesson 2002). For D'Antonio & Kark (2002), the key challenge in invasion biology is to understand the interaction of species traits and ecosystem properties in determining which species will become invasive and where.
Species of drosophilids (and other animals) that are generalists in respect to trophic resource use and tolerance to variable climatic conditions are good candidates to be invasive on new territories, frequently far from their centres of origin (Brncic et al. 1985). The majority of the drosophilids feeds fundamentally on bacteria and yeasts participating in the fermentation of carbohydrate-rich substrates, specially decomposing fruits. Volatile substances originating in the fermentation of these substrates work as the main attractive for the flies (Carson 1971, Vilela et al. 2001). Some species are more restricted ecologically, using only one species as feeding and reproduction sites; others are more versatile, being able to exploit different kinds of resources (Throckmorton 1975). Moreover, there are many drosophilid species occurring along with or very close to human habitations, as gardens, orchards and waste deposits, ending up being spread with the creation of such habitats (Parsons 1987).
Zaprionus indianus (Gupta) is an afrotropical drosophilid that recently invaded South America (Vilela 1999) and quickly expanded its area of distribution, attaining the status of plague on fig crops in the Brazilian State of São Paulo. Since then, this fly invaded other Brazilian States (Castro & Valente 2001, De Toni et al. 2001, Tidon et al. 2003) and the Uruguayan territory (Goñi et al. 2001), in which it has been found, in the same period, as one of the most abundant members of local communities of Drosophilidae.
This work evaluates some possible colonisation strategies of this alien species and its impact in the local diversity of drosophilids. The urban area of the city of Porto Alegre, southern of Brazil, have been studied in terms of its drosophilid communities by researchers from our laboratory for the last twenty years, with regular field collections and research on the ecology, genetics and behaviour of the flies (Valente et al. 1989, Valiati & Valente 1996, 1997).
Material and Methods
Samples of flies were collected from three places in Porto Alegre city (30º02'S-51º14'W) with different urbanisation levels (Farroupilha Park (FP), high urbanisation level; Botanical Garden (BG), intermediate level; and Gabriel Knijnik Park (GKP), low urbanisation level) according to a classification by Ruszczyk (1986/1987). Sampling was done during seven seasons from February 2001 to September 2002, one sample per season for each place, in the period between 9 a.m. and 12 a.m.
Two sampling methods were employed: 1. adult flies were netted as they were flying over a variety of rotten fruits (both native and exotic), and during periods when fruits were not available, conventional banana baits were used; 2. pre-adult stages were collected from field collected fermenting fruits and kept in bottles containing vermiculite in the laboratory in chambers with controlled temperature and humidity (25 ± 1ºC, 60% R.H.). Adult specimens were identified (and counted) using keys of Freire-Maia & Pavan (1949) and Chassagnard & Tsacas (1993). The sibling cryptic species Drosophila melanogaster (J.W. Meigen) and D. simulans (A.H. Sturtevant), D. willistoni (A.H. Sturtevant) and D. paulistorum (T. Dobzhansky & C. Pavan) were joined together as subgroups (melanogaster and willistoni, respectively).
For the description of the communities, we used the following parameters: 1. relative abundance: the number of individuals of the species i divided by the total number of individuals in the sample; 2. species diversity index (H'), according to Shannon & Weaver (1949), modified by Hutcheson (1970): H' = - (Spi ln pi) - (S - 1)/2N, were pi = frequency of species i; S = number of species and N = sample size; 3. species richness (S): the number of different species found in the sample; 4. evenness index (J'), according to Pielou (1974): J' = H'/Hmax, were H' = diversity index observed and Hmax = maximum diversity of the sample, found when all species are equally abundant (= ln S), were S is the total number of species; 5. dominance index (D), according to Simpson (1949): D = ni (ni -1)/ N ( N - 1); were, ni is number of individuals of the species i and N is the total number of the samples; 6. Morisita-Horn (quantitative) similarity index, according to Morisita (1959), modified by Horn (1966): CMH = 2S(ani X bni)/ (da+db)aN X bN, where aN is the number of individuals at place A; bN is the number of individuals at place B; ani is the number of individuals of species i at place A; bni is the number of individuals of species i no place B; da = Sani2/aN2; and db = Sbni2/bN2 .
The above indexes were calculated using the frequency of individuals flying over the fruits (feeding sites), and of imagoes emerging from fruits took to the laboratory (breeding sites), separately.
Temperature data were obtained from the Instituto Nacional de Metereologia of the Oitavo Distrito de Metereologia (INMET), in Porto Alegre, RS, Ministério da Agricultura, Pecuária e Abastecimento (MAPA).
Results and Discussion
We collected 48,609 drosophilids along the whole sample period in the three parks, with Z. indianus (19,146 individuals), subgroup willistoni (11,381 individuals) and subgroup melanogaster (9,495 individuals) the more abundant entities (Table 1). Together they represent 82.3% of the sample. Despite considering D. melanogaster and D. simulans as subgroup melanogaster and D. willistoni and D. paulistorum as subgroup willistoni, our previous experience (Valente et al. 1989; Santos & Valente 1990; Valiati & Valente 1996,1997) suggests that these subgroups correspond mostly to individual contributions from D. simulans and D. willistoni, respectively, the dominant species before the Z. indianus invasion.
The relative frequencies of Z. indianus compared to the other drosophilids collected across the seven seasons at the three sample places, both for adult feeding sites and breeding sites are showed in the Figs. 1 to 3. For some of the seasons and in some places, no drosophilids were found flying over fruits, or there were no fermenting fruits to be brought back to the laboratory. Independently of place, drosophilid community composition, or even substrate type (fruits) used as feeding and breeding sites, the highest frequencies of Z. indianus were obtained during seasons with higher mean temperatures (summer and spring) (Figs.1 to 4). Even though Z. indianus frequencies suffer a sharp drop during autumn and winter, they increase again in spring, especially for breeding sites, that demonstrates the invasive ability of this species (Figs. 1 and 2).
Da Cunha & Magalhães (1965) argued that the observed oscillations in species frequencies across the seasons would be reflecting differences in tolerance of the various species at a same local to the variable climatic conditions. Seasonal oscillations in the frequency of Drosophila subobscura (J.E. Colling), a colonizing species in Chile, were registered by Brncic et al. (1985). During three sampled years, this species had its highest frequencies between August and December. The authors suggest that changes in temperature and humidity affect vital parameters as: viability, crosses, fertility, development time from egg to adult, life span and other factors that influence survival of populations of species of genus Drosophila. The same could be happening with local populations of Z. indianus in Porto Alegre city.
The dominance affects species diversity significantly, both for the feeding sites component (r = -0.9701; P < 0.0001), and breeding sites (r = -0.9294; P < 0.0001). For example, the highest value of dominance (0.848), at Farroupilha Park, during summer of 2001, for the feeding sites component, was accompanied by the lowest value of H' (0.59) (Table 2). Similar results were seen for the breeding sites component, so that at Gabriel Knijnik Park, during the summer of 2001, the highest value of D (0.753) accompanied the lowest H'(0.77).
In general, the highest values of D were found during seasons with higher mean temperatures (summer and spring) (Table 2), when Z. indianus (at the three sample places, both flying over and emerging from fruits), had its highest frequencies, usually above 50%. At Farroupilha Park, for example, during the summer of 2001, the frequency of Z. indianus reached 92.0%, for feeding sites (Fig. 3a). However in autumn and winter, when mean temperatures fall, there is also a decrease in the frequency of Z. indianus and, consequently, an increase in the number and frequency of other species. Such fact is ratified by the negative correlation between dominance and richness, in terms of adult feeding sites (r = -0.5518; P < 0.05) as in breeding sites (r =-0.6402; P < 0.01).
The clear seasonal pattern in community structure is observed in an association between the higher values of evenness index and effective number of species (r = 0.769; P < 0.01), in seasons with lower mean temperatures (autumn and winter) whereas both indices are lower in summer and spring, periods of higher mean temperatures and highest frequencies of Z. indianus.
Saavedra et al. (1995), studying communities in Rio Grande do Sul State, southern of Brazil, showed that the lowest estimates for evenness index and effective number of species, were influenced by the strong dominance of D. willistoni, apparently similar to the effect of Z. indianus in the structure of communities of Drosophilidae in Porto Alegre.
We analysed the influence of some variables that may contribute to diversity and were able to explain only 19.9% of the diversity levels found (80.11% were not explained, see Table 3). This value is quite less than those obtained by Shorrocks (1975) and Brncic et al. (1985), for communities of Drosophila in England (82.4%) and Chile (63.3%), respectively. However, for both authors as well as for our work, the component contributing more to the explanation of diversity was the seasonal one (14.1%, see Table 3). Even thus, using similar components to the other authors, we could not explain much of the diversity in our drosophilid communities. That could stem from the methodology contemplating only one sample per season, differently from the monthly samples of the cited papers, so that for us a single sample represents a period of three months. Furthermore we would consider that the rest of the variation may be attributed to other variables not studied here, as microclimatic variations and fruit kinds available across the seasons.
The dendrograms presented in these work were generated from Morisita (1959) similarity indexes (Fig. 5). The latter represent the similarity between the places sampled during the seven seasons, both for breeding and feeding sites. The similarity index was calculated based on the number and frequency of sampled species at the three places. Botanical Garden and Farroupilha Park had a higher similarity among their diversities when the breeding sites component was considered (Fig.5a), while for feeding sites, similarity was higher between Farroupilha Park and Gabriel Knijnik Park (Fig.5b). All sites studied here are urban parks, though Gabriel Knijnik Park is located in what is considered a low urbanisation area. Even though the parks have different size, species number (S) and varied resources availability across the seasons, three parks had similarity above 83% (Fig. 5). Also, the places showed the mean of diversities (H') closed, oscillating between 1.59 and 1.76 to breeding sites, and 1.95 and 2.18 to feeding sites (Table 2), as well as the absent of significant differences among the species richness (c2 = 9.672; P = 0.974).
There are many variables that could cause environments to differ, relative to the dynamics of drosophilid communities. Among these variables affecting species relationships in such communities we could have: (I) number and kind of resources available across seasons, correlated to the availability (or not) of different kinds of yeast and bacteria (participating in the process of fermentation of fruit substrates), to be used by different species; (II) differences in species composition across seasons, which is particularly true for regions with well defined seasons as in southern of Brazil; (III) environmental differences typical of each place, as the presence of forest patches; (IV) microclimatic conditions; (V) presence of predators; (VI) human action. Besides, the study of tropical communities is usually complex, since tropical environments have considerable ecological richness, with many species living in sympatry in very diverse habitats (Valente & Araújo 1991).
In spite of any differences among the three parks sampled (different dimensions, varied resources availability along the seasons and urbanisation level), the ease with which Z. indianus became established in each of those seem to be the same. This establishment seem to be responsible for promoting adjustments in the survival strategies of the resident species, at least for certain periods when the frequency of the populations of the invader increases significantly but, it is probable that many of the resident species are able to coexist ecologically with the invader.
Considering its possible colonisation strategies, our data suggest that, together with the ability to live in environments associated to humans, its capacity to recover high population levels, under favourable conditions, contribute to its competence for expansion and colonisation of new areas. However, we do not know how the species survives cold periods, whether there is diapause or the populations recuperate by reintroduction. Another hypothesis for further studies is the formation of heat islands in the Porto Alegre city, as a phenomenon associated to urbanisation (Danni 1980). These thermic islands could then be used as refuges for urban populations of insects during unfavorable periods.
Besides, the availability and diversity of substrates on the urban area opens up niches to explore and Z. indianus showed the ability to explore different substrates for feeding and breeding in the three parks. An important aspect to test is whether Z. indianus is good competitor in exploring the feeding substrates as a larva as it seems to be when in adult form.
The monitoring of Drosophilidae communities at these places, for longer time spans, will allow us to confirm or not these conclusions and will contribute to clarify the dynamics of the interactions between the populations of the invasive species with resident ones.
We are grateful to Dr. Milton Mendonça Jr., of the Departamento de Zoologia, Instituto de Biociências, Universidade Federal do Rio Grande do Sul, for reviewing this manuscript. This research was supported by grants and fellowships from CNPq, CAPES, FAPERGS and PROPESQ-UFRGS.
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Received 05/IV/04. Accepted 13/I/05.