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Small-scale patch dynamics after disturbance in litter ant communities
ARTICLE IN PRESS Basic and Applied Ecology 8 (2007) 36—43
www.elsevier.de/baae
Small-scale patch dynamics after disturbance in litter ant communities Renata B.F. Camposa, Jose ´ H. Schoerederb,, Carlos F. Sperberb Po ´s-Graduac-a ˜o em Entomologia, Departamento de Biologia Animal, Universidade Federal de Vic-osa, Vic-osa, MG 36570-000, Brazil b Departamento de Biologia Geral, Universidade Federal de Vic-osa, Vic-osa, MG 36570-000, Brazil a
Received 4 July 2005; accepted 24 March 2006
KEYWORDS Biodiversity; Formicidae; Re-colonisation; Species composition; Succession; Tropical forest
Summary The dynamics of re-colonisation of disturbed patches may aid in the understanding of spatial variation of species richness. The present study experimentally tested the hypothesis that the variation of litter ant local species richness and composition is caused by the dynamics of re-colonisation after disturbances. We were particularly interested in whether the re-colonisation was by pre-existent species or species new to the patches, and whether the succession of species evidences the existence of dominance-controlled or founder-controlled communities. Litter patches of a forest remnant in Southeast Brazil were disturbed by removing most animals through litter drying, and litter samples were returned to the same sites from where they were removed. Ant species richness and composition were compared before and 2 months after the disturbance. Dissimilarity among disturbed and non-disturbed samples was compared to infer the succession model occurring after disturbance. Ant species richness did not recover after 2 months, and species composition of the disturbed samples showed more new colonisers than pre-existent species. Dissimilarity among samples in the disturbed plots was smaller than in the control plots, indicating a directional, or dominance-controlled, succession. The changes in species composition observed were caused by a decrease of some species, particularly predators, and an increase of species that are possibly opportunistic. Patches of litter are naturally disturbed in time and space, and evidence from the present paper indicates that succession occurring in these patches would lead to different species richness and compositions. Thus the dynamics of re-colonisation contributes to explaining the diversity of litter-dwelling ant communities at larger spatial and temporal scales. In each patch the succession seems to be directional, with opportunist species re-colonising preferentially empty plots. Therefore, these communities may attain a high diversity due to a small-scale patch dynamics model. ¨ kologie. Published by Elsevier GmbH. All rights reserved. & 2006 Gesellschaft fu ¨r O
Corresponding author. Tel.: +55 31 3899 4003; fax: +55 31 3899 2549.
E-mail address: [email protected] (J.H. Schoereder). ¨ kologie. Published by Elsevier GmbH. All rights reserved. 1439-1791/$ - see front matter & 2006 Gesellschaft fu ¨r O doi:10.1016/j.baae.2006.03.010
ARTICLE IN PRESS Disturbance and patch dynamics in litter ants
37
Zusammenfassung Die Dynamik der Wiederbesiedlung von gesto ¨rten Bereichen kann helfen die ra ¨umliche Variation des Artenreichtums zu verstehen. Die vorliegende Untersuchung testete experimentell die Hypothese, dass die Variation des lokalen Artenreichtums und der Zusammensetzung von Streuameisen durch die Dynamik der Wiederbesiedlung nach einer Sto ¨rung verursacht wird. Wir interessierten uns besonders dafu ¨r, ob die Wiederbesiedlung durch schon vorkommende Arten oder durch Arten, die neu fu ¨r den Bereich waren, erfolgte und ob die Sukzession der Arten die Existenz von dominanzkontrollierten oder gru ¨nderkontrollierten Gemeinschaften belegt. Es wurden Streubereiche eines Waldrestes in Su ¨dost-Brasilien gesto ¨rt, indem die meisten Tiere durch Trocknen der Streu entfernt wurden, und sie dann an dieselben Orte zuru ¨ckgebracht wurden, von welchen sie entfernt wurden. Der Artenreichtum und die Zusammensetzung der Ameisen wurden vor und zwei Monate nach der Sto ¨rung miteinander verglichen. Es wurden die Unterschiede zwischen den gesto ¨rten und nicht-gesto ¨rten Proben verglichen um eine Sukzessionsmodell abzuleiten, das nach einer Sto ¨rung stattfindet. Der Artenreichtum der Ameisen erholte sich nach zwei Monaten nicht und die Artenzusammensetzung der gesto ¨rten Proben wiesen mehr neue Kolonisten als vorher vorhandene Arten auf. Die Unterschiede zwischen den Proben der gesto ¨rten Bereiche waren geringer als zwischen den Kontrollbereichen, und wiesen auf eine gerichtete oder dominanzkontrollierte Sukzession hin. Die beobachteten Vera ¨nderungen in der Artenzusammensetzung wurden durch die Abnahme einiger Arten verursacht, vor allem von Pra ¨datoren, und durch die Zunahme opportunistischer Arten. Bereiche mit Streu sind natu ¨rlicherweise in Zeit und Raum verteilt und die Hinweise aus der vorliegenden Vero ¨ffentlichung weisen darauf hin, dass die Sukzession, die in diesen Bereichen stattfindet, zu unterschiedlichen Artenreichtum und –zusammensetzungen fu ¨hrt. Deshalb tra ¨gt die Dynamik der Wiederbesiedlung dazu bei, die Diversita ¨t der im Streu lebenden Ameisengesellschaften auf gro ¨ßeren ra ¨umlichen und zeitlichen Skalen zu erkla ¨ren. In jedem Bereich scheint die Sukzession gerichtet zu sein, mit opportunistischen Arten, die bevorzugt leere Bereiche wiederbesiedeln. Deshalb ko ¨nnen diese Gemeinschaften aufgrund eines Dynamikmodells in Bereichen auf kleiner Skala eine hohe Diversita ¨t erlangen. ¨ kologie. Published by Elsevier GmbH. All rights reserved. & 2006 Gesellschaft fu ¨r O
Introduction Despite the unquestionable importance of identifying biodiversity patterns, the study of processes determining these patterns is essential, and merits more attention. It is necessary to know not only where biodiversity is higher, but also to understand what mechanisms are responsible for its maintenance (DeSouza, Schoereder, Brown, & Bierregaard Jr., 2001). This is especially important in hyperdiverse communities and taxonomic groups (Yoon, 1993). Forest litter is considered one frontier in biodiversity studies because it harbours an enormous biodiversity and is the stratum of several important processes in the forest, such as nutrient and soil dynamics (Copley, 2000). In tropical forests, an important and abundant fraction of litter communities is composed by ants (Levins, Pressick, & Heatwole, 1973; York, 1999), and considerable attention has recently been given to ground-dwelling ant communities, and to mechanisms determin-
ing their biodiversity. Competition (McGlynn & Kirksey, 2000), microclimate (Kaspari & Weiser, 2000; Perfecto & Vandermeer, 1996; Torres, 1984), litter abundance (Carvalho & Vasconcelos, 1999; Oliver, Nally, & York, 2000), disturbance (Kaspari, 1996), and predation (Hirosawa, Higashi, & Mohamed, 2000) are usually regarded as key factors determining litter ant biodiversity. Of these factors, some may be more important for the determination of litter ant species richness than others. For instance, there is little evidence for the importance of litter abundance (Campos, Schoereder, & Sperber, 2003; Delabie & Fowler, 1995; McGlynn et al., 2002) and competition on litter ant communities (Soares & Schoereder, 2001; Soares, Schoereder, & DeSouza, 2001; Yanoviak & Kaspari, 2000). On the other hand, there is a hypothesised higher importance of the dynamics of local communities on biodiversity, including dynamics of colonisation and extinction linked to local processes (Campos et al., 2003; Levins et al., 1973; Soares et al., 2001).
ARTICLE IN PRESS 38 Disturbance in litter communities occurs frequently, because this microhabitat receives a constant input of vegetal and animal detritus, and also because this organic material is constantly subject to decomposition and incorporation into the soil (Facelli & Pickett, 1991). Other sources of litter disturbance may include the presence of army ants and other predators (Hirosawa et al., 2000). The response of litter ant communities to disturbances may be local extinction or colony migration, and several litter ant species are known to frequently relocate their nests (Byrne, 1994; Franks & Sendova-Franks, 2000; Herbers, 1994). Disturbance may trigger an ecologic succession, because communities are altered and species richness may decrease in the short term (Kaspari, 1996). Resident species may be eliminated by disturbance and pioneer species may invade the altered patches of litter. In the course of time, the species lost by disturbance may re-enter the litter patch and the community may eventually return to the original species richness (Kaspari, 1996). Although species richness may recover, different species composition may occur, depending on which species re-invade the litter patch. Two basic models of community succession might occur depending on whether communities are dominance-controlled or founder-controlled. In dominance-controlled communities, the empty patches are colonised initially by pioneer species, which are substituted through competition by mid-succession and climax species. This model, therefore, implies a directional succession, where the final stages are predictable (Dauber & Wolters, 2004, 2005). In founder-controlled communities every species may colonise a new patch, impairing the establishment of others. The final stages of such a model are unpredictable, and this model is usually called a competitive lottery (Yu, Wilson, & Pierce, 2001). The structure of ant communities in forest litter with frequent disturbances would be determined by a mosaic of different patches of litter experiencing different successional stages, disregarding the model of succession occurring there (Andersen, 1997; Soares et al., 2001; Yanoviak, 1999). To our knowledge, this hypothesised effect of disturbance on litter ant species richness and composition has not been studied yet. The present study experimentally tested the hypothesis that the variation of litter ant local species richness and composition is caused by the dynamics of recolonisation after disturbances. We were particularly interested in whether the plots were recolonised by pre-existent species or new species, and whether the succession of species evidences
R.B.F. Campos et al. the existence of dominance-controlled or foundercontrolled communities.
Material and methods Study site The experiment was installed in a forest remnant with an area of about 300 ha, at Vic-osa, Minas Gerais, Brazil (201450 S, 421510 W). The climate is moderate subtropical moist with a rainy season from September to April and a dry season from May to August (Golfari, 1975). The annual rainfall ranges from 1500 to 2000 mm, average air relative humidity is 80% and temperature ranges from 14 to 26.1 1C (Castro, Valente, Coelho, & Ramalho 1983). This remnant has suffered periodic exploitation mainly due to coffee crops, and it is protected since 1966, when a process of natural secondary succession started. The secondary forest now occupies most of the reserve area, and we arbitrarily chose a forested area to carry out the sampling.
Experimental design Forty samples with 30 cm diameter of litter were removed in January 2001, receiving a code number indicating the sampling site. These samples were placed in modified Berlese funnels for 3 days, and then manually sorted to remove all ants (giving the initial species composition). These defaunated litter samples were returned to the forest, in the beginning of February 2001, and placed in exactly the same places from where they had been taken. After 2 months the samples were re-collected, and placed in Berlese funnels for 10 days to extract all the ants (giving the final species composition). The ants from initial and final samples were sorted, mounted and identified to genus (Bolton, 1994) and, whenever possible, to species with the help of taxonomists. The final number of species was compared with control samples. These were 40 non-disturbed samples of litter (30 cm diameter) that were collected concomitantly with treated litter at the end of the experiment. To test which mechanism of re-colonisation prevails in this community, the species before and after re-colonisation were compared, dividing them into three categories: (1) species present in the initial samples and absent from the final samples; (2) species absent from the initial but present in the final samples (new colonisers); and (3) species present in both samples (pre-existent species). If re-colonisation was
ARTICLE IN PRESS Disturbance and patch dynamics in litter ants primarily due to new colonisers, category (2) above would present higher species richness than category (3), i.e., most re-colonising species would be different from the original local set of species. While comparisons were carried out using species richness, the differences between categories gave an estimate of changes in species composition.
Statistical analyses Species richness in the re-colonised and control plots were compared by analyses of covariance (ANCOVA), using Poisson errors. Since litter weight may influence litter ant species richness (Campos et al., 2003), litter dry weight was determined and included as a continuous variable in ANCOVA. Explanatory variables were litter dry weight, treatment and the interaction between these variables, while the response variable was species richness. The complete model was fitted and nonsignificant explanatory variables were removed in turn, analysing the effect of removal on the deviance (Crawley, 2002). Species composition before and after re-colonisation was compared using analysis of variance (ANOVA using Poisson errors). The number of species that were absent in the initial samples but recorded from the final samples was compared to the number of species present in both samples. To explore the changes of species composition, we used ant species frequency, i.e. the proportion of samples in which the species occurred. Dissimilarity between samples was calculated using the Bray–Curtis method (package ‘‘vegan’’, Oksanen, 2004). The average dissimilarity of each sample with all others within a treatment was calculated, thereby producing a number of values equal to the number of samples and avoiding pseudoreplication. The same procedure was carried out for the control samples. These dissimilarity values were compared using analysis of variance with binomial models corrected for overdispersion (Crawley, 2002). All analyses were carried out using the R software (R Development Core Team, 2005), and were followed by residual analyses to check for the suitability of the models and distributions used.
Results In total, 53 species were recorded from the litter samples, belonging to five subfamilies (Table 1). Control samples together summed 33 species. Experimental samples, used to test for re-colonisation, had 34 species before removal of ants and 28
39 species after 2 months of re-colonisation (Table 1). Nine species were absent from the experimental patches, but occurred in control patches (Table 1). There were seven species that appeared only after disturbance, all of them with frequencies higher than 0.02. Eight species of Myrmicinae and five of Ponerinae disappeared after disturbance, and several species in both subfamilies decreased their frequency. The most striking examples where Pheidole sp. 1 among the Myrmicinae and Gnamptogenys striatula among the Ponerinae. Some species did not change remarkably in frequency, such as Brachymyrmex sp. 1 and Solenopsis sp. 1, while Monomorium floricola increased its frequency. In general, frequencies were lower in the treatment than in the control samples, and the species richness was significantly lower after experimental disturbance (Fig. 1). Litter weight did not influence ant species richness (F1,85 ¼ 0.17; P ¼ 0.68), nor did the interaction between litter weight and disturbance (F1,84 ¼ 0.43; P ¼ 0.52). Species richness 2 months after disturbance was significantly smaller than in control samples (non-disturbed) (F1,86 ¼ 5.12; P ¼ 0.03; Fig. 1). The number of species present both in initial and final samples (pre-existent species) was significantly smaller than the number of species that were absent in the initial samples (new colonisers) (F1,78 ¼ 14.15; P ¼ 0.0002; Fig. 2), showing that species composition was affected by disturbance. Dissimilarity among samples in the treatment plots was smaller than in the control plots (F1,86 ¼ 166.05; Po0.001; Fig. 3), indicating a directional succession.
Discussion Ant species richness did not recover 2 months after disturbance, regardless of the amount of litter present in the samples. These results indicate that the re-colonisation process was not limited by resource availability but by colonising abilities of ant species. Litter abundance has been reported as a determining factor of ant species richness by some authors (Campos et al., 2003; Carvalho & Vasconcelos, 1999; Oliver et al., 2000), while other authors did not find any relationship between ant species richness and litter weight (Delabie & Fowler, 1995; McGlynn, Carr, Carson, & Buma, 2004; McGlynn et al., 2002), or even reported a negative correlation between the variables (Lassau & Hochuli, 2004). Our results might help to explain the discrepancy of this relationship, showing that disturbance may negatively influence species
ARTICLE IN PRESS 40 Table 1. Brazil
R.B.F. Campos et al. Ant species sampled in litter at Vic-osa, MG,
Table 1. (continued ) Taxon
I
RC
I
RC
C
8 — 1
— — —
— 1 —
34
28
33
C
Myrmicinae Acanthognatus stipulosus Apterostigma complex pilosus sp. Hylomyrma reitteri Hylomyrma sp. 1 Megalomyrmex sp. 1 Megalomyrmex sp. 2 Megalomyrmex sp. 3 Monomorium floricola Octostruma jheringhi Octostruma rugifera Oligomyrmex sp. Pheidole sp. 1 Pheidole sp. 2 Pheidole sp. 3 Pheidole sp. 4 Pheidole sp. 6 Pheidole sp. 8 Pheidole sp. 11 Pheidole sp. 12 Pheidole sp. 13 Pheidole sp. 14 Pyramica subedentata Rogeria sp. Solenopsis sp. 1 Solenopsis sp. 2 Solenopsis sp. 3 Solenopsis sp. 4 Solenopsis sp. 8 Stegomyrmex vizottoi Strumygenys sp. Strumygenys sp. prox perpava Wasmannia sp.
— 1 1 1 — 1 1 3 4 — 2 6 4 3 2 1 — — — — — — — 16 2 1 8 — 1 1 3 1
1 — 1 — — — — 7 3 — 3 3 2 1 — — 1 — — 1 2 1 1 13 4 — 13 2 — 2 — 1
— — 1 — 1 — — 5 2 1 3 13 3 4 3 — 1 1 1 1 2 — — 27 11 3 9 — — — 1 6
Ecitoninae Labidus coecus
—
1
—
Formicinae Brachymyrmex sp. 1 Brachymyrmex sp. 3 Camponotus atriceps Camponotus crassus Camponotus (Myrmaphaenus) sp.
9 1 — 1 —
9 — 1 — 1
8 1 — 1 —
Ponerinae Amblyopone lurilabes Anochetus sp. Discothyrea sexarticulata Gnamptogenys sp. 1 Gnamptogenys striatula Hypoponera foreli Hypoponera sp. 1 Hypoponera sp. 3 Hypoponera sp. 4 Hypoponera sp. 5 Hypoponera sp. 6 Hypoponera sp. 7
1 — — 1 7 2 3 — 18 1 1 —
1 — — 3 1 — 1 — 13 — — —
— 1 1 1 3 — 3 1 24 — — 1
Odontomachus meinerti Pachycondyla harpax Pachycondyla striata Number of species
Initial (I), Re-colonised (RC) and Control (C) refer to frequencies of ants in each treatment (total number of samples ¼ 40).
3
Total ant species richness
Taxon
2
1
0 Control
Treatment
Figure 1. Local ant species richness in control (litter samples without disturbance) and in treatment samples (litter samples 2 months after ant removal). Species richness in the treatment samples refers to the number of re-colonisers. Bars are standard errors.
richness. Since in the tropics and subtropics litter communities might be constantly disturbed, for instance due to army ant raids (Kaspari & O’Donnell, 2004; McGlynn et al., 2004) or freshly fallen litter, the effect of litter weight on species richness may decrease in some samples. It is noteworthy that colonisation by ants, in a strict sense, implies the establishment of a nest within a habitat. In contrast, we did not differentiate between species that colonised disturbed patches by founding a colony (or by moving an existing colony into the patch) and species that just entered the patch to forage. Similarly, since we extracted ants using Berlese funnels, we could not find brood in the samples to check whether the species had nests within plots.
ARTICLE IN PRESS Disturbance and patch dynamics in litter ants
Ant species richness
2
1
0 New colonisers
Pre-existent
Figure 2. Change of local ant species composition after disturbance (treatment with ant removal). The species recorded 2 months after disturbance may be exclusive to these samples (new colonisers) or may have been found previously (pre-existent species). Bars are standard errors.
0.9 0.8
Dissimilarity among samples
0.7 0.6 0.5 0.4 0.3 0.2 0.1 0.0 Control
Treatment
Figure 3. Dissimilarity among treatment (disturbed) and among control (non-disturbed) samples. Bars are standard errors.
41 Species composition changed in treatment samples compared to controls, due to the colonisation of new species to the patches, since the number of new colonisers in the treatment samples was higher than the number of pre-existent species. However, different species reacted to disturbance in different ways, reducing, increasing or maintaining their frequencies. All species absent from the experimental patches but present in controls exhibited a low frequency (0.02), and can be taken as a measure of the spatial variability among experimental and control patches. The absence of changes in frequencies observed in some species may indicate that these species are tolerant to litter disturbance, because ant species richness is also influenced by litter quality (Armbrecht, Perfecto, & Vandermeer, 2004). Possibly, nesting and foraging habits of these species allow them to rapidly re-colonise the disturbed plots. Ants nesting in the soil would recover more rapidly, because they could re-enter the samples after disturbance from their unaffected nests in the soil. Species with a generalist habit could also be quick re-colonizers, using feeding resources that remained after the experimental disturbance, such as seeds, fungi, and arthropod carcasses. Some species of the genus Monomorium are described as generalists, which usually enter highly disturbed sites (Burbidge, Leicester, McDavitt, & Majer, 1992), and our study corroborates their finding. The subfamily Ponerinae is composed of generalist predator species, which nest and forage in the litter. Since the litter of disturbed samples was dried and animals removed, the decrease of predators could be a result of the reduction of prey items. Decrease of predators and of some of the dominant species may have allowed the occurrence of species that were neither observed in control plots nor in the initial samples. Samples disturbed at the same time, i.e., the defaunated samples, were more similar than control samples, which may have been naturally disturbed at different and unknown occasions. The experimental disturbance did not only remove animals, but also dried and fragmented the litter, and probably decreased the number of fungi and bacteria, thereby disrupting the dynamics of litter decomposition. The micro-habitat conditions of these samples were much more similar among each other than the conditions of control samples, which may have suffered natural and random disturbances. When we put the litter samples back to the original sites, some generalist species nesting in the soil and in the nearby litter could have immediately entered the litter samples to forage.
ARTICLE IN PRESS 42 With time, only species that found enough resources and suitable conditions would inhabit the samples. On the other hand, these samples would have less predators and competitors, facilitating the occurrence of opportunist species. Therefore, the experimental disturbance tended to homogenise species composition in the samples after 2 months of re-colonisation. This result evidenced that particular species occur preferentially at specific successional stages, indicating a directional succession. Re-colonisation may depend both on colony size and mobility, and it is expected that species with large colony size and high worker mobility occur more often in disturbed patches than species with small colonies and low mobility. Unfortunately, there are few data regarding biology and habits of Neotropical ant species, and these hypotheses cannot be tested with the present knowledge. Patches of litter are naturally disturbed in time and space. Evidence from the present paper indicates that succession occurring in disturbed patches can lead to different species richness and compositions. Thus the dynamics of re-colonisation could explain the diversity of litter-dwelling ant communities at larger spatial and temporal scales. In each patch, succession seems to be directional, with opportunist species re-colonising preferentially empty plots. The idea of disturbances leading to high diversity in litter communities has already been hypothesised (Campos et al., 2003; Soares et al., 2001), and our paper gave experimental evidence in support of this mechanism. In conclusion, natural disturbances followed by directional succession may be fundamental to explain local species richness in litter ant communities. Especially in the tropics, where litter falls frequently in small quantities, new habitat patches are created on a daily basis. These communities may attain a high overall diversity because disturbances render some patches to initial successional stages, while other patches remain in mid-successional and climax stages, in a small scale patch dynamics model (Yodzis, 1986).
Acknowledgements The authors are indebted to Alessandra B.F. Campos, Carla R. Ribas, Fernando Z. Vaz-de-Mello, and Harvey O. Pengel who helped at fieldwork. Ivan C. do Nascimento (Universidade Federal de Vic-osa) and Dr. Jacques H.C. Delabie (Comissa ˜o Executiva do Plano da Lavoura Cacaueira) helped us with ant identification. Og DeSouza, Angelo Pallini, Carla R.
R.B.F. Campos et al. Ribas, Tathiana G. Sobrinho, Ju ´lio N.C. Louzada and two anonymous referees read and criticised a previous version of the manuscript. R.B.F. Campos is supported by a CAPES Grant and J.H. Schoereder is supported by a CNPq Grant. The work was supported by CAPES/PROF and FAPEMIG.
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43 Oksanen, J. (2004). Vegan: R functions for vegetation ecologists. /http://cc.oulu.fi/jarioksa/softhelp/ vegan.htmlS. Oliver, I., Nally, R. M., & York, A. (2000). Identifying performance indicators of the effects of forest management on ground-active arthropod biodiversity using hierarchical partitioning and partial canonical correspondence analysis. Forest Ecology and Management, 139, 21–40. Perfecto, I., & Vandermeer, J. (1996). Microclimatic changes and indirect loss of ant diversity in a tropical agroecosystem. Oecologia, 108, 577–582. R Development Core Team. (2005). R: A language and environment for statistical computing. Vienna, Austria: R Foundation for Statistical Computing. ISBN 3900051-00-3, URL /http://www.R-project.orgS. Soares, S. M., & Schoereder, J. H. (2001). Ant-nest distribution in a remnant of tropical rainforest in southeastern Brazil. Insectes Sociaux, 48, 280–286. Soares, S. M., Schoereder, J. H., & DeSouza, O. (2001). Processes involved in species saturation of grounddwelling ant communities (Hymenoptera, Formicidae). Austral Ecology, 21, 187–192. Torres, J. A. (1984). Niches coexistence of ant communities in Puerto Rico: Repeated Patterns. Biotropica, 16, 284–295. Yanoviak, S. P. (1999). Effects of leaf litter species on macroinvertebate community properties and mosquito yield in Neotropical tree hole microcosms. Oecologia, 120, 147–155. Yanoviak, S. P., & Kaspari, M. (2000). Community structure and the habitat templet: Ants in the tropical forest canopy and litter. Oikos, 89, 259–266. Yodzis, P. (1986). Competition, mortality and community structure. In J. Diamond, & T. J. Case (Eds.), Community ecology (pp. 480–491). New York: Harper & Row. Yoon, C. K. (1993). Research News: Counting creatures great and small. Science, 260, 620–622. York, A. (1999). Long-term effects of frequent lowintensity burning on the abundance of litter-dwelling invertebrates in coastal blackbutt forests of southeastern Australia. Journal of Insect Conservation, 3, 191–199. Yu, D. W., Wilson, H. B., & Pierce, N. E. (2001). An empirical model of species coexistence in a spatially structured environment. Ecology, 82, 1761–1771.
www.elsevier.de/baae
Small-scale patch dynamics after disturbance in litter ant communities Renata B.F. Camposa, Jose ´ H. Schoerederb,, Carlos F. Sperberb Po ´s-Graduac-a ˜o em Entomologia, Departamento de Biologia Animal, Universidade Federal de Vic-osa, Vic-osa, MG 36570-000, Brazil b Departamento de Biologia Geral, Universidade Federal de Vic-osa, Vic-osa, MG 36570-000, Brazil a
Received 4 July 2005; accepted 24 March 2006
KEYWORDS Biodiversity; Formicidae; Re-colonisation; Species composition; Succession; Tropical forest
Summary The dynamics of re-colonisation of disturbed patches may aid in the understanding of spatial variation of species richness. The present study experimentally tested the hypothesis that the variation of litter ant local species richness and composition is caused by the dynamics of re-colonisation after disturbances. We were particularly interested in whether the re-colonisation was by pre-existent species or species new to the patches, and whether the succession of species evidences the existence of dominance-controlled or founder-controlled communities. Litter patches of a forest remnant in Southeast Brazil were disturbed by removing most animals through litter drying, and litter samples were returned to the same sites from where they were removed. Ant species richness and composition were compared before and 2 months after the disturbance. Dissimilarity among disturbed and non-disturbed samples was compared to infer the succession model occurring after disturbance. Ant species richness did not recover after 2 months, and species composition of the disturbed samples showed more new colonisers than pre-existent species. Dissimilarity among samples in the disturbed plots was smaller than in the control plots, indicating a directional, or dominance-controlled, succession. The changes in species composition observed were caused by a decrease of some species, particularly predators, and an increase of species that are possibly opportunistic. Patches of litter are naturally disturbed in time and space, and evidence from the present paper indicates that succession occurring in these patches would lead to different species richness and compositions. Thus the dynamics of re-colonisation contributes to explaining the diversity of litter-dwelling ant communities at larger spatial and temporal scales. In each patch the succession seems to be directional, with opportunist species re-colonising preferentially empty plots. Therefore, these communities may attain a high diversity due to a small-scale patch dynamics model. ¨ kologie. Published by Elsevier GmbH. All rights reserved. & 2006 Gesellschaft fu ¨r O
Corresponding author. Tel.: +55 31 3899 4003; fax: +55 31 3899 2549.
E-mail address: [email protected] (J.H. Schoereder). ¨ kologie. Published by Elsevier GmbH. All rights reserved. 1439-1791/$ - see front matter & 2006 Gesellschaft fu ¨r O doi:10.1016/j.baae.2006.03.010
ARTICLE IN PRESS Disturbance and patch dynamics in litter ants
37
Zusammenfassung Die Dynamik der Wiederbesiedlung von gesto ¨rten Bereichen kann helfen die ra ¨umliche Variation des Artenreichtums zu verstehen. Die vorliegende Untersuchung testete experimentell die Hypothese, dass die Variation des lokalen Artenreichtums und der Zusammensetzung von Streuameisen durch die Dynamik der Wiederbesiedlung nach einer Sto ¨rung verursacht wird. Wir interessierten uns besonders dafu ¨r, ob die Wiederbesiedlung durch schon vorkommende Arten oder durch Arten, die neu fu ¨r den Bereich waren, erfolgte und ob die Sukzession der Arten die Existenz von dominanzkontrollierten oder gru ¨nderkontrollierten Gemeinschaften belegt. Es wurden Streubereiche eines Waldrestes in Su ¨dost-Brasilien gesto ¨rt, indem die meisten Tiere durch Trocknen der Streu entfernt wurden, und sie dann an dieselben Orte zuru ¨ckgebracht wurden, von welchen sie entfernt wurden. Der Artenreichtum und die Zusammensetzung der Ameisen wurden vor und zwei Monate nach der Sto ¨rung miteinander verglichen. Es wurden die Unterschiede zwischen den gesto ¨rten und nicht-gesto ¨rten Proben verglichen um eine Sukzessionsmodell abzuleiten, das nach einer Sto ¨rung stattfindet. Der Artenreichtum der Ameisen erholte sich nach zwei Monaten nicht und die Artenzusammensetzung der gesto ¨rten Proben wiesen mehr neue Kolonisten als vorher vorhandene Arten auf. Die Unterschiede zwischen den Proben der gesto ¨rten Bereiche waren geringer als zwischen den Kontrollbereichen, und wiesen auf eine gerichtete oder dominanzkontrollierte Sukzession hin. Die beobachteten Vera ¨nderungen in der Artenzusammensetzung wurden durch die Abnahme einiger Arten verursacht, vor allem von Pra ¨datoren, und durch die Zunahme opportunistischer Arten. Bereiche mit Streu sind natu ¨rlicherweise in Zeit und Raum verteilt und die Hinweise aus der vorliegenden Vero ¨ffentlichung weisen darauf hin, dass die Sukzession, die in diesen Bereichen stattfindet, zu unterschiedlichen Artenreichtum und –zusammensetzungen fu ¨hrt. Deshalb tra ¨gt die Dynamik der Wiederbesiedlung dazu bei, die Diversita ¨t der im Streu lebenden Ameisengesellschaften auf gro ¨ßeren ra ¨umlichen und zeitlichen Skalen zu erkla ¨ren. In jedem Bereich scheint die Sukzession gerichtet zu sein, mit opportunistischen Arten, die bevorzugt leere Bereiche wiederbesiedeln. Deshalb ko ¨nnen diese Gemeinschaften aufgrund eines Dynamikmodells in Bereichen auf kleiner Skala eine hohe Diversita ¨t erlangen. ¨ kologie. Published by Elsevier GmbH. All rights reserved. & 2006 Gesellschaft fu ¨r O
Introduction Despite the unquestionable importance of identifying biodiversity patterns, the study of processes determining these patterns is essential, and merits more attention. It is necessary to know not only where biodiversity is higher, but also to understand what mechanisms are responsible for its maintenance (DeSouza, Schoereder, Brown, & Bierregaard Jr., 2001). This is especially important in hyperdiverse communities and taxonomic groups (Yoon, 1993). Forest litter is considered one frontier in biodiversity studies because it harbours an enormous biodiversity and is the stratum of several important processes in the forest, such as nutrient and soil dynamics (Copley, 2000). In tropical forests, an important and abundant fraction of litter communities is composed by ants (Levins, Pressick, & Heatwole, 1973; York, 1999), and considerable attention has recently been given to ground-dwelling ant communities, and to mechanisms determin-
ing their biodiversity. Competition (McGlynn & Kirksey, 2000), microclimate (Kaspari & Weiser, 2000; Perfecto & Vandermeer, 1996; Torres, 1984), litter abundance (Carvalho & Vasconcelos, 1999; Oliver, Nally, & York, 2000), disturbance (Kaspari, 1996), and predation (Hirosawa, Higashi, & Mohamed, 2000) are usually regarded as key factors determining litter ant biodiversity. Of these factors, some may be more important for the determination of litter ant species richness than others. For instance, there is little evidence for the importance of litter abundance (Campos, Schoereder, & Sperber, 2003; Delabie & Fowler, 1995; McGlynn et al., 2002) and competition on litter ant communities (Soares & Schoereder, 2001; Soares, Schoereder, & DeSouza, 2001; Yanoviak & Kaspari, 2000). On the other hand, there is a hypothesised higher importance of the dynamics of local communities on biodiversity, including dynamics of colonisation and extinction linked to local processes (Campos et al., 2003; Levins et al., 1973; Soares et al., 2001).
ARTICLE IN PRESS 38 Disturbance in litter communities occurs frequently, because this microhabitat receives a constant input of vegetal and animal detritus, and also because this organic material is constantly subject to decomposition and incorporation into the soil (Facelli & Pickett, 1991). Other sources of litter disturbance may include the presence of army ants and other predators (Hirosawa et al., 2000). The response of litter ant communities to disturbances may be local extinction or colony migration, and several litter ant species are known to frequently relocate their nests (Byrne, 1994; Franks & Sendova-Franks, 2000; Herbers, 1994). Disturbance may trigger an ecologic succession, because communities are altered and species richness may decrease in the short term (Kaspari, 1996). Resident species may be eliminated by disturbance and pioneer species may invade the altered patches of litter. In the course of time, the species lost by disturbance may re-enter the litter patch and the community may eventually return to the original species richness (Kaspari, 1996). Although species richness may recover, different species composition may occur, depending on which species re-invade the litter patch. Two basic models of community succession might occur depending on whether communities are dominance-controlled or founder-controlled. In dominance-controlled communities, the empty patches are colonised initially by pioneer species, which are substituted through competition by mid-succession and climax species. This model, therefore, implies a directional succession, where the final stages are predictable (Dauber & Wolters, 2004, 2005). In founder-controlled communities every species may colonise a new patch, impairing the establishment of others. The final stages of such a model are unpredictable, and this model is usually called a competitive lottery (Yu, Wilson, & Pierce, 2001). The structure of ant communities in forest litter with frequent disturbances would be determined by a mosaic of different patches of litter experiencing different successional stages, disregarding the model of succession occurring there (Andersen, 1997; Soares et al., 2001; Yanoviak, 1999). To our knowledge, this hypothesised effect of disturbance on litter ant species richness and composition has not been studied yet. The present study experimentally tested the hypothesis that the variation of litter ant local species richness and composition is caused by the dynamics of recolonisation after disturbances. We were particularly interested in whether the plots were recolonised by pre-existent species or new species, and whether the succession of species evidences
R.B.F. Campos et al. the existence of dominance-controlled or foundercontrolled communities.
Material and methods Study site The experiment was installed in a forest remnant with an area of about 300 ha, at Vic-osa, Minas Gerais, Brazil (201450 S, 421510 W). The climate is moderate subtropical moist with a rainy season from September to April and a dry season from May to August (Golfari, 1975). The annual rainfall ranges from 1500 to 2000 mm, average air relative humidity is 80% and temperature ranges from 14 to 26.1 1C (Castro, Valente, Coelho, & Ramalho 1983). This remnant has suffered periodic exploitation mainly due to coffee crops, and it is protected since 1966, when a process of natural secondary succession started. The secondary forest now occupies most of the reserve area, and we arbitrarily chose a forested area to carry out the sampling.
Experimental design Forty samples with 30 cm diameter of litter were removed in January 2001, receiving a code number indicating the sampling site. These samples were placed in modified Berlese funnels for 3 days, and then manually sorted to remove all ants (giving the initial species composition). These defaunated litter samples were returned to the forest, in the beginning of February 2001, and placed in exactly the same places from where they had been taken. After 2 months the samples were re-collected, and placed in Berlese funnels for 10 days to extract all the ants (giving the final species composition). The ants from initial and final samples were sorted, mounted and identified to genus (Bolton, 1994) and, whenever possible, to species with the help of taxonomists. The final number of species was compared with control samples. These were 40 non-disturbed samples of litter (30 cm diameter) that were collected concomitantly with treated litter at the end of the experiment. To test which mechanism of re-colonisation prevails in this community, the species before and after re-colonisation were compared, dividing them into three categories: (1) species present in the initial samples and absent from the final samples; (2) species absent from the initial but present in the final samples (new colonisers); and (3) species present in both samples (pre-existent species). If re-colonisation was
ARTICLE IN PRESS Disturbance and patch dynamics in litter ants primarily due to new colonisers, category (2) above would present higher species richness than category (3), i.e., most re-colonising species would be different from the original local set of species. While comparisons were carried out using species richness, the differences between categories gave an estimate of changes in species composition.
Statistical analyses Species richness in the re-colonised and control plots were compared by analyses of covariance (ANCOVA), using Poisson errors. Since litter weight may influence litter ant species richness (Campos et al., 2003), litter dry weight was determined and included as a continuous variable in ANCOVA. Explanatory variables were litter dry weight, treatment and the interaction between these variables, while the response variable was species richness. The complete model was fitted and nonsignificant explanatory variables were removed in turn, analysing the effect of removal on the deviance (Crawley, 2002). Species composition before and after re-colonisation was compared using analysis of variance (ANOVA using Poisson errors). The number of species that were absent in the initial samples but recorded from the final samples was compared to the number of species present in both samples. To explore the changes of species composition, we used ant species frequency, i.e. the proportion of samples in which the species occurred. Dissimilarity between samples was calculated using the Bray–Curtis method (package ‘‘vegan’’, Oksanen, 2004). The average dissimilarity of each sample with all others within a treatment was calculated, thereby producing a number of values equal to the number of samples and avoiding pseudoreplication. The same procedure was carried out for the control samples. These dissimilarity values were compared using analysis of variance with binomial models corrected for overdispersion (Crawley, 2002). All analyses were carried out using the R software (R Development Core Team, 2005), and were followed by residual analyses to check for the suitability of the models and distributions used.
Results In total, 53 species were recorded from the litter samples, belonging to five subfamilies (Table 1). Control samples together summed 33 species. Experimental samples, used to test for re-colonisation, had 34 species before removal of ants and 28
39 species after 2 months of re-colonisation (Table 1). Nine species were absent from the experimental patches, but occurred in control patches (Table 1). There were seven species that appeared only after disturbance, all of them with frequencies higher than 0.02. Eight species of Myrmicinae and five of Ponerinae disappeared after disturbance, and several species in both subfamilies decreased their frequency. The most striking examples where Pheidole sp. 1 among the Myrmicinae and Gnamptogenys striatula among the Ponerinae. Some species did not change remarkably in frequency, such as Brachymyrmex sp. 1 and Solenopsis sp. 1, while Monomorium floricola increased its frequency. In general, frequencies were lower in the treatment than in the control samples, and the species richness was significantly lower after experimental disturbance (Fig. 1). Litter weight did not influence ant species richness (F1,85 ¼ 0.17; P ¼ 0.68), nor did the interaction between litter weight and disturbance (F1,84 ¼ 0.43; P ¼ 0.52). Species richness 2 months after disturbance was significantly smaller than in control samples (non-disturbed) (F1,86 ¼ 5.12; P ¼ 0.03; Fig. 1). The number of species present both in initial and final samples (pre-existent species) was significantly smaller than the number of species that were absent in the initial samples (new colonisers) (F1,78 ¼ 14.15; P ¼ 0.0002; Fig. 2), showing that species composition was affected by disturbance. Dissimilarity among samples in the treatment plots was smaller than in the control plots (F1,86 ¼ 166.05; Po0.001; Fig. 3), indicating a directional succession.
Discussion Ant species richness did not recover 2 months after disturbance, regardless of the amount of litter present in the samples. These results indicate that the re-colonisation process was not limited by resource availability but by colonising abilities of ant species. Litter abundance has been reported as a determining factor of ant species richness by some authors (Campos et al., 2003; Carvalho & Vasconcelos, 1999; Oliver et al., 2000), while other authors did not find any relationship between ant species richness and litter weight (Delabie & Fowler, 1995; McGlynn, Carr, Carson, & Buma, 2004; McGlynn et al., 2002), or even reported a negative correlation between the variables (Lassau & Hochuli, 2004). Our results might help to explain the discrepancy of this relationship, showing that disturbance may negatively influence species
ARTICLE IN PRESS 40 Table 1. Brazil
R.B.F. Campos et al. Ant species sampled in litter at Vic-osa, MG,
Table 1. (continued ) Taxon
I
RC
I
RC
C
8 — 1
— — —
— 1 —
34
28
33
C
Myrmicinae Acanthognatus stipulosus Apterostigma complex pilosus sp. Hylomyrma reitteri Hylomyrma sp. 1 Megalomyrmex sp. 1 Megalomyrmex sp. 2 Megalomyrmex sp. 3 Monomorium floricola Octostruma jheringhi Octostruma rugifera Oligomyrmex sp. Pheidole sp. 1 Pheidole sp. 2 Pheidole sp. 3 Pheidole sp. 4 Pheidole sp. 6 Pheidole sp. 8 Pheidole sp. 11 Pheidole sp. 12 Pheidole sp. 13 Pheidole sp. 14 Pyramica subedentata Rogeria sp. Solenopsis sp. 1 Solenopsis sp. 2 Solenopsis sp. 3 Solenopsis sp. 4 Solenopsis sp. 8 Stegomyrmex vizottoi Strumygenys sp. Strumygenys sp. prox perpava Wasmannia sp.
— 1 1 1 — 1 1 3 4 — 2 6 4 3 2 1 — — — — — — — 16 2 1 8 — 1 1 3 1
1 — 1 — — — — 7 3 — 3 3 2 1 — — 1 — — 1 2 1 1 13 4 — 13 2 — 2 — 1
— — 1 — 1 — — 5 2 1 3 13 3 4 3 — 1 1 1 1 2 — — 27 11 3 9 — — — 1 6
Ecitoninae Labidus coecus
—
1
—
Formicinae Brachymyrmex sp. 1 Brachymyrmex sp. 3 Camponotus atriceps Camponotus crassus Camponotus (Myrmaphaenus) sp.
9 1 — 1 —
9 — 1 — 1
8 1 — 1 —
Ponerinae Amblyopone lurilabes Anochetus sp. Discothyrea sexarticulata Gnamptogenys sp. 1 Gnamptogenys striatula Hypoponera foreli Hypoponera sp. 1 Hypoponera sp. 3 Hypoponera sp. 4 Hypoponera sp. 5 Hypoponera sp. 6 Hypoponera sp. 7
1 — — 1 7 2 3 — 18 1 1 —
1 — — 3 1 — 1 — 13 — — —
— 1 1 1 3 — 3 1 24 — — 1
Odontomachus meinerti Pachycondyla harpax Pachycondyla striata Number of species
Initial (I), Re-colonised (RC) and Control (C) refer to frequencies of ants in each treatment (total number of samples ¼ 40).
3
Total ant species richness
Taxon
2
1
0 Control
Treatment
Figure 1. Local ant species richness in control (litter samples without disturbance) and in treatment samples (litter samples 2 months after ant removal). Species richness in the treatment samples refers to the number of re-colonisers. Bars are standard errors.
richness. Since in the tropics and subtropics litter communities might be constantly disturbed, for instance due to army ant raids (Kaspari & O’Donnell, 2004; McGlynn et al., 2004) or freshly fallen litter, the effect of litter weight on species richness may decrease in some samples. It is noteworthy that colonisation by ants, in a strict sense, implies the establishment of a nest within a habitat. In contrast, we did not differentiate between species that colonised disturbed patches by founding a colony (or by moving an existing colony into the patch) and species that just entered the patch to forage. Similarly, since we extracted ants using Berlese funnels, we could not find brood in the samples to check whether the species had nests within plots.
ARTICLE IN PRESS Disturbance and patch dynamics in litter ants
Ant species richness
2
1
0 New colonisers
Pre-existent
Figure 2. Change of local ant species composition after disturbance (treatment with ant removal). The species recorded 2 months after disturbance may be exclusive to these samples (new colonisers) or may have been found previously (pre-existent species). Bars are standard errors.
0.9 0.8
Dissimilarity among samples
0.7 0.6 0.5 0.4 0.3 0.2 0.1 0.0 Control
Treatment
Figure 3. Dissimilarity among treatment (disturbed) and among control (non-disturbed) samples. Bars are standard errors.
41 Species composition changed in treatment samples compared to controls, due to the colonisation of new species to the patches, since the number of new colonisers in the treatment samples was higher than the number of pre-existent species. However, different species reacted to disturbance in different ways, reducing, increasing or maintaining their frequencies. All species absent from the experimental patches but present in controls exhibited a low frequency (0.02), and can be taken as a measure of the spatial variability among experimental and control patches. The absence of changes in frequencies observed in some species may indicate that these species are tolerant to litter disturbance, because ant species richness is also influenced by litter quality (Armbrecht, Perfecto, & Vandermeer, 2004). Possibly, nesting and foraging habits of these species allow them to rapidly re-colonise the disturbed plots. Ants nesting in the soil would recover more rapidly, because they could re-enter the samples after disturbance from their unaffected nests in the soil. Species with a generalist habit could also be quick re-colonizers, using feeding resources that remained after the experimental disturbance, such as seeds, fungi, and arthropod carcasses. Some species of the genus Monomorium are described as generalists, which usually enter highly disturbed sites (Burbidge, Leicester, McDavitt, & Majer, 1992), and our study corroborates their finding. The subfamily Ponerinae is composed of generalist predator species, which nest and forage in the litter. Since the litter of disturbed samples was dried and animals removed, the decrease of predators could be a result of the reduction of prey items. Decrease of predators and of some of the dominant species may have allowed the occurrence of species that were neither observed in control plots nor in the initial samples. Samples disturbed at the same time, i.e., the defaunated samples, were more similar than control samples, which may have been naturally disturbed at different and unknown occasions. The experimental disturbance did not only remove animals, but also dried and fragmented the litter, and probably decreased the number of fungi and bacteria, thereby disrupting the dynamics of litter decomposition. The micro-habitat conditions of these samples were much more similar among each other than the conditions of control samples, which may have suffered natural and random disturbances. When we put the litter samples back to the original sites, some generalist species nesting in the soil and in the nearby litter could have immediately entered the litter samples to forage.
ARTICLE IN PRESS 42 With time, only species that found enough resources and suitable conditions would inhabit the samples. On the other hand, these samples would have less predators and competitors, facilitating the occurrence of opportunist species. Therefore, the experimental disturbance tended to homogenise species composition in the samples after 2 months of re-colonisation. This result evidenced that particular species occur preferentially at specific successional stages, indicating a directional succession. Re-colonisation may depend both on colony size and mobility, and it is expected that species with large colony size and high worker mobility occur more often in disturbed patches than species with small colonies and low mobility. Unfortunately, there are few data regarding biology and habits of Neotropical ant species, and these hypotheses cannot be tested with the present knowledge. Patches of litter are naturally disturbed in time and space. Evidence from the present paper indicates that succession occurring in disturbed patches can lead to different species richness and compositions. Thus the dynamics of re-colonisation could explain the diversity of litter-dwelling ant communities at larger spatial and temporal scales. In each patch, succession seems to be directional, with opportunist species re-colonising preferentially empty plots. The idea of disturbances leading to high diversity in litter communities has already been hypothesised (Campos et al., 2003; Soares et al., 2001), and our paper gave experimental evidence in support of this mechanism. In conclusion, natural disturbances followed by directional succession may be fundamental to explain local species richness in litter ant communities. Especially in the tropics, where litter falls frequently in small quantities, new habitat patches are created on a daily basis. These communities may attain a high overall diversity because disturbances render some patches to initial successional stages, while other patches remain in mid-successional and climax stages, in a small scale patch dynamics model (Yodzis, 1986).
Acknowledgements The authors are indebted to Alessandra B.F. Campos, Carla R. Ribas, Fernando Z. Vaz-de-Mello, and Harvey O. Pengel who helped at fieldwork. Ivan C. do Nascimento (Universidade Federal de Vic-osa) and Dr. Jacques H.C. Delabie (Comissa ˜o Executiva do Plano da Lavoura Cacaueira) helped us with ant identification. Og DeSouza, Angelo Pallini, Carla R.
R.B.F. Campos et al. Ribas, Tathiana G. Sobrinho, Ju ´lio N.C. Louzada and two anonymous referees read and criticised a previous version of the manuscript. R.B.F. Campos is supported by a CAPES Grant and J.H. Schoereder is supported by a CNPq Grant. The work was supported by CAPES/PROF and FAPEMIG.
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