Diptera) in Northern Finland

Larval niche differences between the sibling species, Drosophila montana and D. littoralis (Diptera) in northern Finland

JouniAspi

Aspi, J. 1996: Larval niche differences between the sibling species, Dro sophila montana and D. littoralis (Diptera) in northern Finland. - Entomol. Fennica 7:29-38. Differences in larval substrate, or in the spatial and temporal occurrence of larvae between two closely related and ecologically similar Drosophila spe cies were investigated. Vials containing homogenised tissue of water lily stems or birch phloem wetted with sap were exposed for oviposition in two habitats during two time periods. A logit analysis of the field emergence data suggested significant niche differences between the species. The logit model best explaining the species composition among emerging adults included an interaction between habitat and substrate, and also an interaction between habitat and exposure period. The differences between the species were, however, small and the species overlapped broadly with respect to each of the studied niche dimensions. The distribution of emerging flies among the yellow water lily vials appeared to fulfill the assumptions of a theoretical model for aggregation-mediated coexistence, i.e. the distribution of flies was aggregated among vials in both species, and there was no interspecific corre lation in the numbers of flies emerging from the vials. Jouni Aspi, University of Oulu, Oulanka Biological Station, Liikasenvaarantie 134, FIN-90570 Kuusamo, Finland, e-mail: [email protected]

Received 22 December 1994, accepted 16 February 1996

1. Introduction Although there are only slight differences among these species in their adult ecology (Lumme et al. The boreal Drosophila virilis species association 1978, 1979, Aspi et al. 1993), they may differ in consists of four closely related sibling species other life stages. In Drosophila the major specificity (D. lummei Hackman, D. littoralis Meigen, D. of the ecology seems to relate to the breeding sites ezoana Takada & Okada and D. montana Stone, in the larval stage (e.g. Carson 1971, Krebs et al. Griffen & Patterson). The phenology and spatial 1993). There is only scanty information available distribution of adults of these species in the field about female oviposition and on larval feeding sites is very similar, and they form a compact group among these species. In general the species of the distinct from the other drosophilids in northern D. virilis group are classified as sap breeders, the Scandinavia (Lumme et al. 1978, 1979, Aspi et known breeding sites being sap and the decaying al. 1993). phloem tissue of some deciduous tree species (e.g., 30 Aspi: Larval niches between Drosophila species • ENTOMOL. FENNICA Vol. 7

Carson 1971, Spieth 1974, Shorrocks 1982, Watabe source patches, and if intraspecific aggregation ex & Peng 1991). During the previous fieldwork in the ceeds interspecific aggregation. Under these condi boreal area (As pi et al. 1993) we have been able to tions interspecific competition is more intense breed a few adults of D. littoralis and D. montana among the superior species than among the inferior from the phloem tissue of birch and yeast growing one. Since earlier observations indicate that the on birch sap fluxes, and also from the rotting stems natural breeding sites of D. virilis group species are of yellow water lily, Nuphar lutea. At least these discrete and ephemeral (i.e. wounds in birch bark two species seem to share the breeding substrates. and rots in stems of yellow water lily), the aggrega Drosophila species using identical breeding re tion-mediated competition model may allow their sources may differ in the spatial or temporal use of coexistence even if the breeding niches are similar. these resources (Kaneshiro et al. 1973, Lachaise et The aim of this paper is to examine whether D. al. 1982, Nunney 1990). The distribution of adult littoralis and D. montana have a different oviposition flies during the breeding season may provide indi preference for the two known breeding substrates, rect evidence about spatial differences in breeding and in spatial and temporal distribution of larvae in sites of Drosophila. Among the boreal D. virilis the field. The aggregation model of coexistence is group there seem to be, however, no large differ also considered in light of the distribution of larvae ences in the spatial distribution of ovipositing fe among resource items. males (Lumme et al. 1979, Aspi et al. 1993). All these species feed and mate in close proximity to water. Only D. montana is not as strictly restricted 2. Material and methods to habitats with high humidity as the other species (Lumme et al. 1979, Aspi et al. 1993). The main 2.1. Substrate preparation breeding season of boreal species of D. virilis group is in early spring, and is very short, limiting the Baits from decaying plant material were prepared to re possibility of temporal niche differentiation (Lumme semble the natural breeding substrate of the species (see e.g. Offenberger & Klarenberg 1992). The plant materials et al. 1978, Aspi et al. 1993). However, Aspi et al. used were: I) phloem tissue of birch (Betula pubescens) (1993) reported differences in the seasonal mating peeled from young trees, dried, homogenised and mois schedules between the three most common species tened with birch sap, and 2) tissue of underwater stems of of the D. virilis group, which may in tum also indi the yellow water lily (Nuphar lutea) homogenised into a cate temporal differences in occurence of larvae. pulp. After a period of rotting and fermenting, each substrate The use of similar breeding substrates can lead batch was mixed thoroughly and frozen. For the field study, 10 ml of thawed birch phloem tissue or 5 ml of to interspecific competition and exclusion of com yellow water lily pulp was dispensed directly into plastic peting species. Coexistence of competing Dro vials (75 mm deep, 27 mm diameter). Different volumes of sophila species in spatially homogenous environ the two substrates were used to keep the carbohydrate ments may sometimes be promoted by differences content of the vials similar. in life-history (Sevenster & van Alphen 1993a, 1993b; see also Davis & Hardy 1994). However, there seem to be no large differences in life-history 2.2. Exposure of substrate vials for oviposition characters among the boreal D. virilis group spe in the field cies (Lumme et al. 1978, Aspi et al. 1993). The fieldwork was carried out near Kemi, Finland, along the The exclusion of competing species will not River Iso-Ruonaoja (E27 Grid number 7292:394, 65.40 'N, always occur if the resources are patchy and ephem 23 • 35'E; see As pi et at. 1993 for a detailed description). In eral. Several authors have suggested theoretical earlier trappings all members of the riparian guild have been models (Shorrocks et al. 1979, Atkinson & found, with D. littoralis the most common followed by Shorrocks 1984, Hanski 1981, 1983, Ives & May D. montana, D. lummei, and D. ezoana respectively. 1985; see Hanski [1987] and Shorrocks [1990] for The oviposition vials were placed in white 2-litre plastic buckets (14.5 em deep, 15.5 cmdiameter) containing a 5 em reviews) in which an inferior competitor can coex layer of moistened sand. Two vials of birch phloem and two ist with a superior one if the competing stages are of yellow water lily were randomly half-submerged in a aggregated among the discrete and ephemeral re- square in the sand layer. The buckets were placed in two ENTOMOL. FENNICA Vol. 7 • Aspi: Larval niches between Drosophila species 31 habitats: on the river shore, or in a forest five metres from the a yellow lily vial river bank (Fig. 1) . !0.\ a birch phloem vial Substrate vials were exposed for oviposition (and also ~ for natural microbe contamination) for two different peri · a bucket ods: 12 replicates between 12 May and 31 May (early season), and 12 replicates between 22 May and 5 June (late season) in 1992. These time limits covered the whole reproductive period of overwintered females (Aspi et al. 1993). Although the latter period was shorter, the accumu lated temperature sum above Y C (below which the activ 0 ity of flies ceases) was rather similar for both, 91.5 daily Sm degrees in the early season and 115.7 in the late season. 0 0 lo I- 10m -j Overlapping periods were used to increase the number of flies per vial, since in preliminary experiments the number of flies emerging per vial had been fairly low. After exposure, the vials containing the substrate were Fig. 1. Schematic representation of the experimental plugged and taken back to the laboratory. The vials were design. kept outside in a ventilated cage, where the ambient tem perature was quite similar to that of the original breeding This measure of overlap ranges from 0 (no resources site. The contents of the vials were moistened regularly used in common) to 1.0 (total overlap). with distilled water. All emerging flies were collected and Morisita's index was calculated for uncombined data identified to species. using each vial as a different "resource" category, and also for each measured niche dimension (habitat, substrate and exposure period). For this analysis the twelve replicates 2.3. Niche metrics and aggregation analysis within habitats (i .e. shore and forest) were combined, as were the data from the two vials containing the same substrate within the buckets. Emergence data was used to calculate niche breadth for different niche dimensions and niche overlap between spe The significance of niche differences was analysed cies. All niche metric calculations were carried out on statistically by subjecting the emergence data to a logit Krebs' (1989) NICHE program. Niche breadth for substrate, analysis (Christensen 1990), where the species of an emerg season and habitat usage for each species was estimated ing fly was the response variable, and substrate (birch vs. using Levins' standardised niche breadth (scale from 0 to yellow water lily), exposure period (early vs. late), and 1.0) formula (e.g. Krebs 1989): habitat (shore vs. forest) were the explanatory variables. Logit regression was further used to analyse the temporal eq. I. BA = (B-1)/(n-1), difference in emergence dates between the species. For this analysis, the two exposure periods were pooled, emer where: BA =Levin's standardized niche breadth, B =Levin's gence data from all vials was combined within sixteen original measure of niche breadth, n =number of possible two-day periods, and curve-fitting for the number of resource states. emerged flies in each species was carried out by the least [ Levin~' original measure of niche breadth is calcu square principle (Jongman et al. 1987) and the date (Julian lated from the formula: day from the beginning of the experiment) as the explana eq. 2. B = li(L,pj2), tory variable. The GLIM statistical package (e.g. Aitkin et al. 1990) was used to fit the logit models and to determine where: B =Levin's measure of niche breadth, pj = Propor the parameters for least square regression. tion of individuals found in resource state j]. If the distribution of flies among the resource items is Niche overlap between the species was calculated us random, the distribution of emerging adults should follow a ing Morisita's index of overlap (e.g. Krebs 1989): Poisson distribution. Departure from the Poisson distribution was tested using the index of dispersion test (Krebs 1989, p. eq. 3. C= (2Spijpik)I(I.npij[(nij-l)I(Nj-l)] + I.npik[(nik-1)/(Nk-1)]) 76). The aggregation pattern of the larvae among the vials where: C= Morisita's index of niche overlap between spe was further analysed by using comparable measures of both cies} and k, pi}= Proportion resource i is the total resources intraspecific and interspecific aggregation as suggested by used by species j, pik = Proportion resource i is the total Ives (1988, 1991). These measures are based on the mean resources used by species k, nij =Number of individuals of and variance of the larvae in the vials as censused by the species j that use resource category i, nik = Number of number of emerging adults. Intraspecific aggregation is meas individuals of species k that use resource category i, Nj, Nk = ured by 1, the proportionate increase in the number of Total number of individuals of each species in sample, (i.e. conspecific competitors experienced by random individual Enii= Nj, Snik= Nk). relative to a random distribution. It is calculated by: 32 Aspi: Larval niches between Drosophila species • ENTOMOL. FENNICA Vol. 7

eq. 4. Ji =[(Vi/xi) - 1)/xi)], and exposure period (i.e. model {HS} {HP} (SP}) where: Ji =measure of intraspecific aggregation for species did not significantly improve the explanatory power i, xi= mean of the number oflarvae pervial in species i, Vi= of the model (.1 G< 1J = 0.849;p > 0.1). variance of the number of larvae per vial in species i. The total niche overlap between species esti When individuals are randomly distributed, Ji = 0, mated by using each vial as a different "resource" whereas a value of Ji = 0.5 indicates a 50% increase in the category was fairly high (0.631). The univariate number of conspecifics expected in a vial (e.g. Shorrocks niche statistics showed an even broader overlap & Sevenster 1995). Interspecific aggregation is measured by C, which measures the proportionate increase in the than that with respect to each studied niche dimen number of heterospecific competitors relative to a random sion (Table 2). Both species had a lower niche association (Ives 1988, 1991). It is calculated by: breadth for breeding substrate than for other factors. D. littoralis exhibited a more variable breeding-site eq. 4. Cij = Covijlxixj, niche than D. montana. Although yellow water lily where: Cij = measure of interspecific aggregation between pulp produced more specimens of both species, species i and j, Covij = covariance between species i and j, D. littoralis was relatively more abundant in birch xi= mean of the number of larvae per vial in species i, phloem pulp than D. montana. Overlap between xj =mean ofthenumberoflarvae per vial in speciesj. When Cij = 0 then species i and j are independently species by substrate was, however, high. The inter distributed across vials, when Cij > 0 then species are action between substrate and habitat (Table 1) was positively associated and when Cij < 0 then species are due to fact that two species appeared to have the negatively associated. minimum substrate niche breadth in different habi For estimating the relative strength of intra- and tats (Fig. 2). The niche widths of D. littoralis in interspecific aggregation on the number of competitors with shore and in forest were 0.600 and 0.498, and those which a larva shares a resource, Ives (1991) has proposed a quantity A, calculated by: of D. montana 0.127 and 0.242, respectively (Fig. 3). The adult emergence data indicated that eq. 5. Aij = [(Ji + l)(Jj + 1)]/CCW. D. montana larvae were almost equally abundant where: Aii is a measure of relative strengths of intra- and interspecific aggregations for species i andj, and Ji, Jj, and Table 1. Logit analysis of the factors influencing the Cij as above. When intra- and interspecific aggregations overall species composition. The abbreviations for are equal then Aij = 0, and when Aij > 0 then intraspecific the factors are: H = habitat (shore vs. forest), S = aggregation is stronger than interspecific aggregation (e.g. substrate (birch phloem tissue vs. water lily) and P = Jaenike & James 1991, Shorrocks & Sevenster 1995, exposure period (early vs. late). Sevenster 1996). Model G df p

{HS}{HP}{SP} 4.943 1 0.026 3. Results {HS}{HP} 5.792 2 0.055 {HS}{SP} 0.843 2 0.004 3.1. Niche metrics for D. montana andD.littoralis {HP}{SP} 9.238 2 0.010 {P}{HS} 11.562 3 0.009 Adults of only two species, D. littoralis and D. {S}{HP} 9.611 3 0.022 montana were obtained from the vials exposed for {H}{SP} 14.894 3 0.002 {H}{S}{P} ovipositing in the field. The mean number of flies 15.818 4 0.003 per vial was 0.656 (Median= 0) for D. littoralis and 2.23 (Median = 0) for D. montana. Table 2. Niche metrics for the dimensions studied between two boreal Drosophila virilis group species. Species composition was not independent with respect to the explanatory variables (i .e. exposure Breadth Overlap period, habitat and substrate) (Table 1). The best fitting logit model included an interaction between Dimension D. montana D. Jittoralis habitat and substrate, and also an interaction be tween habitat and exposure period ( {HS}{HP}). Exposure period 0.880 0.833 0.999 Habitat 0.991 0.728 0.909 This model was the only adequate representation of Substrate 0.204 0.684 0.976 the data, as adding an interaction between substrate

2 ENTOMOL. FENNICA Vol. 7 • Aspi: Larval niches between Drosophila species 33

Shore Forest 100 D D. rrwntan D D. montana E;:ssJ D. littoralis ~ D. littoralis 80 .-- ~ --:>-. 60 C) ~ (l) ;::::l 0' 40 (l) 1-< ~ 20

0 Water lily Birch Water lily Birch

Fig. 2. Percentage of adults emerged from the two substrates in the two habitats studied. N = 63 for 0. littora/is, N = 214 0. montana. in both habitats, whereas D. littoralis was relatively observed daily frequencies of inseminated females more abundant on the river bank. The narrower did not differ significantly from the values given by habitat niche of D. littoral is caused the lowest de the fitted curves (goodness of fit tests gave gree of niche overlap in this dimension. The inter G01 l = 13.28 in D. littoralis, Gc 12l = 16.36 in action between habitat and exposure period ap D. montana: p > 0.1 in both cases). The Gaussian peared to be almost solely caused by D. littoralis response curve parameter t, which is a measure of (Fig. 3), which was concentrated on the river bank the emergence amplitude (range of emergencies is during the early exposure period (niche breadth about 4t; see e.g. Jongman et al. 1987) was quite 0.198). In the late exposure period, when this spe similar for both species: 4.4 for D. montana and 4.6 cies was more abundant, it was also found in the for D. littoralis, indicating no large differences in forest (niche breadth 0.943). No large differences the amplitude of adult emergences. On the other were detected in the relative abundance of hand, the parameter u, i.e. the day that gives the D. montana in different habitats in the two expo maximum (see e.g. Jongman et al. 1987) for sure periods (niche breadths 0.995 and 0.989 for D. montana was 25.0 and for D. littoralis 29.9 early and late exposure periods, respectively). revealing a difference of about five days in the Niche overlap of the species on the basis of the mean times of emergence. To test whether this two exposure periods was large. The degree of difference between the species was significant, the temporal overlap between the species was also as emergence data from both species was pooled, and sessed for the sixteen two-day emergence periods, species was also used as an explanatory variable as and this niche overlap showed a lower value (0.718). well (together with the day of emergence) in a logit This distribution of emerging adults differed sig regression model with a Gaussian response curve. nificantly between the species (G(7) = 49.39; Excluding species variable, this model significantly p < 0.001), and in the least-square analysis Gaussian decreased the explanatory power of the model response curve gave a good fit for the number of (GoJ = 103.26; p < 0.001) and confirmed that the emerged flies with respect to emergence day both difference in emergence dates between species was in D. littoralis and in D. montana (Fig. 4). The significant. 34 Aspi: Larval niches between Drosophila species • ENTOMOL. FENNICA Vol. 7

Early season Late season 100 D D. rnontan D D. montana t;SSl D. littoralis ~ D. littoralis 80 .....--._ .._.,~ :>-. 60 (.) ~ Q) ;:::l 0"' 40 Q) J.. ~ 20

0 Shore Forest Shore Forest

Fig. 3. Percentage of individuals emerging from the two habitats during the two exposure periods. Number of specimens as in Fig. 2.

3.2. Intra-and interspecific aggregation N = 27; p > 0.1 ), indicating that the vials producing many D. montana were not the same as those yield Because the birch phloem produced a low number ing many D. littoralis (see Fig. 5). The interspecific of flies in both species, the aggregation pattern of aggregation parameter (C) was smaller than either larvae among vials was only analysed for yellow of the intraspecific aggregation parameters, and the water lily vials. The early exposure period samples measure of the relative strength of intra- and did not allow goodness-of-fit tests due to low number interspecific aggregation (A) was 2.454, indicating of flies emerged, and the data from both periods that the effect of intraspecific aggregation on the was combined. To avoid spurious positive covariance number of competitors a larva shares a resource between species due to double zero vials (i.e. vials with was stronger than the effect of interspecific in which both species were absent), these vials were aggregation. excluded from the analysis (see e.g. Worthen & McGuire 1988, Shorrocks et al. 1990). The larvae appeared to be aggregated among 4. Discussion the yellow water lily vials. Distribution of the emerg ing adults differed significantly from the Poisson The number of flies emerging per vial was low distribution in both D. montana (X2<26J = 143.4; compared with the number of mature females col p < 0.001) andD.littoralis (X2<26J= 140.1;p < 0.001) lected in the study site (see e.g. Aspi et al. 1993, (separate tests for the late exposure period gave Aspi & Lankinen 1992). There are several possible similar conclusions in both species and were not reasons for the low number of emerging adults. reported).The intraspecific aggregation parameter First, this may reveal that the principal breeding (J) was positive in both species, and it was some sites of these species are not birch phloem or yel what larger in D. littoralis (J = 2.487) than in low water lily. However, extensive rearing attempts D. montana (J = 0.628). have been made in the study area, and only the ones The interspecific aggregation parameter was used in this study have produced emerging adults. slightly positive (C = 0.521), but not statistically A more probable reason for the low number of significant (Spearman rank correlation: rs = 0.040; emerging adults may be that the females may have ENTOMOL. FENNICA Vol. 7 • Aspi: Larval niches between Drosophila species 35

60,------, had problems with fmding the vials, since the amount DTosophila montana of substrate used in the field experiment was rather '0 40 small. Yet another possibility is that the imitated Q.) substrates did not support larval development as ...011 Q.) well as their natural breeding substrates do. 8 2 0 The observed differences in the adult spatial Q.) rn and temporal distribution of D. littoralis and Q.) D. montana (Lumme et al. 1979, Aspi et al. 1993) DTosophila litto1·alis were also reflected in the temporal and spatial oc currence oflarvae. With respect to the proximity of water, adults of D. montana have a wider niche ,. than D. littoralis (Lumme eta[. 1979, Aspi et al. o I ' ' ' '., D 1993). Correspondingly, the larvae of D. montana ' appeared to be more abundant than D. littoral is in 20 the less moist habitats. In northern Finland June D. montana females tend to copulate about one week earlier than D. littoralis females (Aspi et al. Fig. 4. Number of individuals emerging from the field kept vials during the season. The solid and broken 1993). The difference in the adult emergence lines represent the fitted number given by logit maxima in the present experiment appears to be regression. Number of specimens as in Fig. 2. about the same, D. montana emerging about five days earlier than D. littoralis. Some interactions between habitat and the other that for separate niche dimensions (0.999-D.909). explanatory variables affecting the species compo This may be partly due to random effects, since sition among emerged flies were confirmed during vials were nested units within the studied niche the study. The interactions may be due to differ dimensions. On the other hand, it may also indicate ences in environmental conditions between the habi that the egg-laying females may perceive the 'habi tats and also between the exposure periods. Krebs tat' on a much finer scale than that of forest or river & Barker (1992) and Arthur & Cassey (1992) have bank. This explanation is also supported by the fact described how such changes in temperature or rela that the probability of the best fitting logit model tive humidity and wetness of substrate may affect (including interaction between habitat and substrate, competitive relationships of other closely related and also an interaction between habitat and expo Drosophila species under laboratory conditions. sure period) was low (p = 0.055). Accordingly, The present results confirm that at least two more detailed studies on the environmental require species belonging to this species group (D. littoralis ments of egg-laying females among boreal D. virilis and D. montana) partially share the same breeding group species are needed. niche, and may be potential competitors. I was not, In their survey of Drosophila studies Rosewell however, able to show that there is competition et al. (1990), Shorrocks et al. (1990), and Shorrocks between the species. Despite overlapping resources, & Sevenster ( 1995) found that individual species environmental factors may well keep the popula almost without exemption exhibit aggregated dis tion densities at such a low level that there is no tributions, and that associations between species competition at the larval stage at all. In fact, compe were generally low. However, Worthen & McGuire tition in Drosophila has been demonstrated in only (1988), Nunney (1990) andJaenike &James (1991) a few cases in natural conditions in the wild reported that the numbers of emerging adults are (Grimaldi & Jaenike 1984, Atkinson 1985, Jaenike often correlated between species belonging to the & James 1991). same species group. The level of niche partitioning seems to be low D. montana and D. littoralis belong to the same with respect to any of the studied niche dimensions species group (D. virilis species group). However, between D. littoralis and D. montana. However, on the basis of emerging adults the species distribu the estimate for niche overlap using each vial as a tions were aggregated, and the effect of intraspecific different resource category was smaller (0.631) than aggregation on the number of competitors the lar- 36 Aspi: Larval niches between Drosophila species • ENTOMOL. FENNICA Vol. 7

40 40 D. montana D. littoralis k=0.338±0.096 k=0.179±0.070 30

'0 20 20 h Q) .D E 1 o 10 z;:J

0 0 0 6.5 14.5 22.5+ 0 2.5 6,5 10.5+ N. of flies emerged N. of flies emerged

Fig. 5. Association between the numbers of flies emerging from the yellow water lily substrate vials in Drosophila montana and D. littoralis. vae shared a resource which appeared to be stronger aggregations may not be randomly dispersed among than the effect of interspecific aggregation. Given the resource items. In D. virilis species group, Bartelt that the distribution of the emerging adults repre et al. (1986) have described existence of special sented the original distribution of eggs, the require aggregation pheromones, which attract both sexes ments of aggregation models of coexistence seemed of these species, and may accordingly cause non to be fulfilled in the present case. This mechanism random courtship aggregations. Because leaving promotes coexistence of these two species even in a an aggregation and searching a new breeding site is competitive situation . costly, Drosophila females may tend to lay their The observed clumped distribution of individu eggs at the same sites where they have mated. Even als within the species over the resource items seems though laying eggs in these sites may be costly in to be problematic, because this can cause food com terms of intraspecific competition, it may still cost petition among siblings. Several reasons for aggre less than leaving the site and possibly losing a gated distributions of individuals have been sug suitable feeding or ovipositing resource. gested. Firstly, clumping can be initially advanta Thirdly, Shorrocks et a!. (1979; see also geous to larvae (for a survey of advantages, see Atkinson & Shorrocks 1984, Shorrocks & Rosewell Stamp 1980): for example, chewing into food item 1987) have proposed a model, in which ovipositing may be more successful in groups. Sjerps et al. females visit breeding sites randomly, lay eggs at a ( 1993) have recently suggested a theoretical model, constant rate while on a site, and have a constant in which clumping is advantageous during the ini probability of leaving the site. This kind of egg tial growth of larvae, but disadvantageous later. laying behaviour would lead to independent and They showed that several factors, like the size of aggregated distribution of species among resource eggs supply and the patchiness of suitable oviposition items. This was the pattern observed in D. littoralis items, can contribute towards egg clumping. and D. montana on the basis of adult emergences. Secondly, in Drosophila the mating behaviour However, it have been questioned whether this may have some importance on the aggregation of mechanism of aggregation can lead to coexistence eggs. In general drosophilid mating takes place in of the competing species (Green 1986, 1988; fly aggregations on suitable feeding and breeding Sevenster 1996; see also Shorrocks & Rosewell sites (Spieth 1974, Spieth & Ringo 1983). These 1988). ENTOMOL. FENNICA Vol. 7:99. 20.1X.l996

Errata

Vol. 7, No 1, 1996, p. 36

In "Larval niche differences between the sibling species, Drosophila montana and D. littoralis (Diptera) in northern Finland" by Jouni Aspi (Entomologica Fennica 7: 36) the figure 5 was incorrect. The correct figure is reproduced below.

14 ,------.

'0 12 • Q) ~ Q) 10 E • Q) :1Q 8 g~ ""' 6 • .!!! :.t: • g. 4 e(/) • • Cl 2 • • • zci .. .. . 0 ..... • •

0 5 10 15 20 25 30 No. Drosophila montana emerged

Fig. 5. Association between the numbers of flies emerging from the yellow water lily substrate vials in Drosophila montana and D. littoralis. ENTOMOL. FENNICA Vol. 7 • Aspi: Larval niches between Drosophila species 37

Acknowledgments: I would like to express my thanks - 1991. Aggregation and coexistence in a carrion fly to Ary Hoffmann, Robert Krebs, Jaakko Lumme, Timo community. -Ecol. Monogr. 61:75-94. Muotka, Jan Sevenster and an unknown referee for their Ives, A. R. & May, R. M. 1985: Competition within and valuable comments on the manuscript. between species in a patchy environment: relations be tween microscopic and macroscopic models. -J. Theor. Bioi. 115: 65-92. Jaenike, J. & James, A. C. 1991: Aggregation and the References coexistence of mycophagous Drosophila. - J. Anim. Ecol. 60:913-928. Aitkin, M., Anderson, D., Francis, B. & Hinde, J. 1990: Jongman, R. H. G., ter Braak, C. J. F. & Tongeren, 0 . F. R. Statistical modeling in GLIM. Oxford statistical sci 1987: Data analysis in community and landscape ecol ence series 4. - Oxford Science Publications, Ox ogy.- Pudoc, Wageningen, Netherlands, 299 pp. ford, 374 pp. Kaneshiro, K. Y., Carson, R. E., Clayton, R. E. & Heed, W. Arthur, W. & Cassey, S. 1992: Variability of a niche differ B. 1973: Niche separation in a pair of homosequential ence between Drosophila hydei and D. melanogaster. Drosophila species for the island of Hawaii. - Am. Ecol. Entomol. 17:354-358. Nat. 107:766-774. Aspi, J. & Lankinen, P. 1992: Frequency of multiple in Krebs, C. J. 1989: Ecological methodology.- Harper & semination in a natural population of Drosophila Row, Cambridge, 654 pp. montana. - Hereditas 117: 169-177. Krebs, R. A. &Barker, J. S. F. 1993: Coexistence of ecologi Aspi, J., Lumme, J., Hoikkala, A. & Heikkinen, E. 1993: cally similar colonising species. II. Population differen Reproductive ecology of the boreal riparian guild of tiation in Drosophila aldrichi and D. buzzatii for com Drosophila. - Ecography 16:65-72. petitive effects and responses at different temperatures Atkinson, W. D. 1985: Coexistence of Australian rainfor and allozyme variation in D. aldrichii.- J. evol. Bioi. est Diptera breeding in fallen fruit. -J. Anim. Ecol. 6:281-298. 54:507-518. Lachaise, D., Tsacas, L. & Couturier, G. 1982: The Atkinson, W. D. & Shorrocks, B. 1984: Aggregation of Drosophilidae associated with tropical African figs. larval diptera over discrete and ephemeral breeding -Evolution 36:141-151. sites: the implications of coexistence. - Am. Nat. Lumme, J., Muona, 0. & Orell, M. 1978: Phenology of boreal 124:336-351. drosophilids.- Ann. Entomol. Fennici 44:73-85. Bartelt, R. J., Schaner, A. M. & Jackson, L. L. 1986: Lumme, J., Lakovaara, S., Muona, 0. & Jarvinen, 0. 1979: Aggregation pheromones in five taxa of the Drosophila Structure of boreal community of drosophilids virilis group.- Physiol. Entomol. 11 :367-376. (Diptera). - Aquilo Ser. Zool. 20:65-73. Carson, H. 1971: The ecology of Drosophila breeding Nunney, L. 1990: Drosophila on oranges: colonization, com sites.- Harold L. Lyon Arboretum Lecture 2:1-28. petition, and coexistence. -Ecology 71 : 1904-1915. Christensen, R. 1990: Log-linear models. - Springer Offenberger, M. & Klarenberg, A. J. 1992: Attractiveness Verlag, New York, 408 pp. and exploitation of decaying herbage by Drosophila in Davis, A. & Hardy, I. 1994: Hares and tortoises in Dro temperate woodland. - Oecologia (Berl.) 92: 183-187. sophila community ecology. -TREE 9:119-120. Rosewell, J., Shorrocks, B. & Edwards, K. 1990: Competi Green, R. F. 1986: Does aggregation prevent competitive tion on a divided and ephemeral resource: testing the exclusion? A response to Atkinson and Shorrocks. assumptions. I. Aggregation.- J. Anim. Ecol. 59:977- Am. Nat. 128:301-304. 1001. 1988: Reply to Shorrocks and Rosewell.- Am. Nat. Sevenster, J. G. 1996. Aggregation and coexistence. I. 128:301-304. Theory and analysis. - J. Anim. Ecol. (in press.). Grimaldi, D. & Jaenike, J. 1984: Competition in natural Sevenster, J. G. & van Alphen, J. J. M. 1993a: Coexistence population of mycophagous Drosophila. - Ecology in stochastic environments through a life history trade 65:1113-1120. off in Drosophila.- Lect. Notes Biomath. 98: 155-172. Hanski, I. 1981 : Coexistence of competitors in patchy - 1993b: A life history trade-off in Drosophila species environment with and without predation. - Oikos and community structure in variable environments. 37:306-312. J. Anim. Ecol. 62: 720-736. 1983: Coexistence of competitors in patchy environ Shorrocks, B. 1982: The breeding sites of temperate wood ment. -Ecology 64:493-500. land Drosophila, pp. 385-428. - In Ashburner, M., 1987: Colonization of ephemeral habitats, pp. 155-185. Carson, H. L. & Thompson, J. N. (eds), The genetics -In: Gray, A. J., Crawley, M. J. & Edwards, P. J. (eds.), and biology of Drosophila. Vol 3b. Academic Press, Colonization, succession and stability. 26th symposium London, 428 pp. of the British Ecological Society. Blackwell, Oxford, 1990: Coexistence in a patchy environment. pp. 91- 482pp. 106. - In Shorrocks, B. & Swingland, I. R. (eds), Ives, A. R. 1988: Aggregation and the coexistence of com Living in patchy environment. Oxford University Press, petitors.- Ann. Zoo!. Fenn. 25:75-88. Oxford, 246 pp. 38 Aspi: Larval niches between Drosophila species • ENTOMOL. FENNICA Vol. 7

Shorrocks, B., Atkinson, W. D. & Charlesworth, P. 1979: problem for insects. - Theor. Popul. Bioi. 43:337- Competition on a divided and ephemeral resource. 367. J. Anim. Ecology. 48:899-908. Spieth, H. T. 1974: Courtship behaviour in Drosophila. Shorrocks, B. & Rosewell, J. 1987: Spatial patchiness and Ann. Rev. Entomol. 19:385-405. community structure: coexistence and guild size of Spieth, H. T. & Ringo, J. M. 1983. Mating behavior and drosophilids on ephemeral resources, pp. 29-51.- In sexual isolation in Drosophila, pp. 224-284. - In Gee, J. H. R. & Giller, P. S. (eds), Organization of com Ashbumer, M., Carson, H. L. and Thompson, J. L. munities, past and present. The 27th symposium of the (eds), The genetics and biology of Drosophila, Vol3c. British Ecological Society. Blackwell, Oxford, 576 pp. Academic Press, London, 428 pp. 1988: Aggregation prevents competitive exclusion: a Stamp, N. 1980: Egg deposition patterns in butterflies: response to Green.- Am. Nat. 131:765-771. why do some species cluster their eggs rather than Shorrocks, B., Rosewell, J. & Edwards, K. 1990: Compe deposit them singly?- Am. Nat. 115:367-380. tition on a divided and ephemeral resource: testing the Watabe, H. & Peng, T. X. 1991: The Drosophila virilis assumptions. II. Association. - I. Anim. Ecol. section (Diptera: Drosophilidae) from Guandong Prov 59:1003-1017. ince, Southern China. -Zoo!. Sci. 8:147-156. Shorrocks, B. & Sevenster, J. 1995: Explaining local spe Worthen, W. B. & McGuire, T. R. 1988: A criticism of the cies diversity.- Proc. R. Soc. Lond. B. 260:305-309. aggregation model of coexistence. non-independent Sjerps, M., Haccou, P., Meelis, E. & van der Meijden, E. distribution of dipteran species on ephemeral resources. 1993: Egg distribution within patches: an optimality -Am. Nat. 131:453-458.