Gall-Inducing Insect Species Richness as Indicators of Forest ... - debio

COMMUNITY AND ECOSYSTEM ECOLOGY

Gall-Inducing Insect Species Richness as Indicators of Forest Age and Health G. WILSON FERNANDES,1 EMMANUEL D. ALMADA,2

AND

MARCO ANTONIO A. CARNEIRO3

Ecologia Evolutiva and Biodiversidade/DBG, C P 486, ICB/Universidade Federal de Minas Gerais, UFMG, 31270 901 Belo Horizonte, MG, Brazil

Environ. Entomol. 39(4): 1134Ð1140 (2010); DOI: 10.1603/EN09199

ABSTRACT The changes in the plant community that occur during the process of succession affect the availability of resources for the community of herbivores. In this study, the richness of galling insects was evaluated in restored stands of Amazonian tropical rain forest of several ages (0 Ð21 yr), as well as in areas of primary forest in Brazil. The richness of gallers increased with the age of the restored stands. Fifty-eight percent of the variation in the richness of galling insects was explained by forest stand age, but an increase in richness was observed at intermediate stages of succession. The greatest similarity among groups was found between the initial successional stages and intermediate ones. The results indicate a recovery of both host plants and insect community and that succession directly affects the richness and composition of these herbivores. KEY WORDS Amazon, biodiversity, galling insects, mining, restoration ecology

The change in plant species composition during the process of succession results in the replacement of the communities through time. While a particular climax community may not be reached, the species number has been argued to increase throughout the successional process (Capers et al. 2005, Begon et al. 2006). In late successional stages, the number of trees and rare species increase, whereas the number of shrubs and lianas decrease (Guariguata et al. 1997, Pen˜ aClaros and de Boo 2002, Capers et al. 2005). Alternatively, many studies have shown that, during succession, plant species achieve higher richness at intermediate stages (Rosenzweig 1995; Gaston 1992, 2000; Molino and Sabatier 2001). A quadratic relationship between plant species richness is expected, as reported by Grime (1973) and Connell (1978), who named it the intermediate disturbance hypothesis. Indeed, this hypothesis is supported by the Þndings that disturbed or managed systems present higher plant diversity than intact forests (Nagaike 2002, Webb and Sah 2003). Variation in plant community composition and structure strongly inßuence the trophic levels above, such as herbivores and their natural enemies. Numerical and qualitative responses of insects are expected to parallel that of the plant community (Price 2005, Novotny et al. 2006). The diversity of several taxa of free-feeding insect herbivores shows a positive corCorresponding author, e-mail: [email protected]. Nu´ cleo de Estudos e Pesquisas Ambientais, Universidade Estadual de Campinas, 35400 000, Campinas SP, Brazil. 3 Instituto de Cie ˆ ncias Exatas e Biolo´ gicas, Universidade Federal de Ouro Preto, 35400 000, Ouro Preto, MG, Brazil. 1 2

relation with succession stage (Parrish and Bazzaz 1982, Davies et al. 1999, DeWalt et al. 2000, Kennard 2002, Kalacska et al. 2004, Hilt and Fiedler 2005, Barlow et al. 2007). The changes in the community structure of herbivore insects in different successional stages may be driven by disturbances that help maintain community composition across a wide variety of ecosystems. A simple increment or decrement of the frequency of disturbance can result in drastic changes in the community structure (Hobbs and Mooney 1991, Wootton et al. 1996, Floren and Linsenmair 2001, Foggo et al. 2001, Elderd 2006), although some taxa have been shown to be more or less susceptible to disturbance (Kruess and Tscharntke 2000, van Nouhuys 2005). The response of insect communities to changes in plant structure and composition has been widely studied, especially in restoration programs (Jansen 1997, McGeogh 1998, Andersen et al. 2002, Nakamura et al. 2003, Moreira et al. 2007). Among the insects, some preference has been found for the use of Hymenoptera, Lepidoptera, and Coleoptera as indicators of natural regeneration of forests, perhaps because of their high diversity, habitat Þdelity, and taxonomical knowledge (Rodrõ´guez et al. 1998, Ratchford et al. 2005). For instance, higher richness of these groups was reported on natural forest remnants than in reforested eucalyptus areas in Australia (Cunningham et al. 2005). Grimbacher and Catterall (2007) reported that forest structure had a strong effect on the community of coleopterans, whereas forest age and distance from remnant primary forest was of second order of importance.

0046-225X/10/1134Ð1140$04.00/0 䉷 2010 Entomological Society of America

August 2010

FERNANDES ET AL.: GALL-INDUCING INSECT AS BIOINDICATORS

Specialist insect herbivores should be most sensitive to plant community changes in a successional scenario because they present more Þne-tuned interactions with their host plants. Among the specialists, galling insects exhibit the most intimate relationship with their host plants (Fernandes 1990, Floate et al. 1996, Wright and Samways 1998, Shorthouse et al. 2005). Their richness is inßuenced by plant species richness (Fernandes 1992, Blanche and Westoby 1995, Wright and Samways 1998, Lara et al. 2002), density (Gonç alves-Alvim and Fernandes 2001), composition (Espõ´rito-Santo et al. 2007), architecture (Espõ´rito-Santo et al. 2007), and even plant ontogeny (Cuevas-Reyes et al. 2004, Fonseca et al. 2006). Furthermore, these interactions are mediated by the habitat. Galling species richness is higher in habitats where harsh conditions prevail (Fernandes and Price 1988, 1991; Ribeiro and Basset 2007). With the need to develop tools to aid in the monitoring of the restoration process of an evergreen equatorial moist forest in Brazil, we have been using gall-inducing insects as bioindicators. The mining company Mineraç aõ Rio do Norte began a pioneer reforestation program in 1979 for restoring the forest cover after bauxite ore extraction. The reforestation method used includes a wide variety of forest species: 80 Ð100 species of native forest species (for details, see Parrotta et al. 1997; Parrotta and Knowles 1999, 2001). Hence, there is approximately one quarter of a century of native forest plantations of several ages or succession stages. This scenario allowed us to evaluate the success of the restoration process on the galling insect community. Hence, we tested the hypothesis that the richness of the gall-inducing insect community increased in later successional stages in response to changes in the composition and richness of the vegetation. Materials and Methods This study was performed in the Trombetas bauxite mining area, located in the Floresta Nacional Saraca´ Taquera-Ibama, at an elevation of 180 m a.s.l., 65 km northwest of the town of Oriximina´ and 30 km from the Trombetas river in the State of Para´, Brazil (1⬚40⬘ S, 56⬚27⬘ W). Mean annual rainfall at Porto Trombetas (1970 Ð1994) is 2,185 ⫾ 964 (SE) mm, with distinct dry (winter) and wet (summer) seasons; mean monthly rainfall exceeds 100 mm in all months except JulyÐ October. The mean maximum and minimum temperatures are 34.6 and 19.9⬚C, respectively. Soils on the Saraca´ plateau are acidic yellow clay latosols with a thin humus layer (Ferraz 1993). The regional vegetation is evergreen equatorial moist forest, within which the forests occupying the upland mesas and surrounding slopes have average canopy heights of 20 Ð35 m, with emergent trees up to 45 m tall (Knowles and Parrotta 1995, 1997). The forests surrounding the mine were, until recently, largely inaccessible and undisturbed by hunting or forest clearing for the past 200 Ð300 yr. Forest restoration was initiated with a mix of native species of different successional stages and

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progressed through the natural recruitment of species from the seed bank (Parrotta and Knowles 2001). Gall sampling occurred during 20 consecutive d in both dry (July) and rainy (December) periods of 2002 (n ⫽ 40 sampling d). In this study, no attempt was made to separate the effects of season on the galling community, because future studies will address the effects of ontogeny and seasonality on this galling community. Otherwise, season may have minor effects on such herbivore community (Fernandes and Price 1988). Samples were taken in areas where reforestation was initiated in the years 1981 (n ⫽ 2), 1982 (n ⫽ 2), 1983 (n ⫽ 1), 1984 (n ⫽ 2), 1985 (n ⫽ 2), 1986 (n ⫽ 2), 1987 (n ⫽ 2), 1988 (n ⫽ 1), 1992 (n ⫽ 1), 1993 (n ⫽ 2), 1994 (n ⫽ 2), 1995 (n ⫽ 2), 1996 (n ⫽ 2), 1997 (n ⫽ 2), 1998 (n ⫽ 3), 1999 (n ⫽ 2), 2000 (n ⫽ 2), 2001 (n ⫽ 2), and 2002 (n ⫽ 2). Thus, we sampled galls on 26 restored areas where the process of reforestation spanned from 0 to 21 yr. The minimum distance between areas was 500 m (see Fernandes and Price 1988), whereas the most distant sites were 15 km apart in an area covering ⬇250 km2. On each restored area, we performed three Þeld samples of 1 h each per sampling period (totaling 6 h/sampled area). Seven areas of primary forest were sampled using the same protocols. For detailed Þeld sample methodology, see Price et al. (1998). Samples of insect galls and host plants were taken on trees up to 4 m high and hence did not cover the canopy or the intermediary forest layers. Galled plant material and samples of the host plants were identiÞed and taken to the laboratory for dissection of the galls, identiÞcation of the inducing organism to the order or family level whenever possible, and description of the major morphological traits of the galls. Host plants were identiÞed to the species level by N. Rosa (Museu Emilio Goeldi). We used gall morphotypes as an indicator of galling species because practically all Amazonian galling insect species are new to science, and taxonomical work is still underway. Furthermore, the use of gall morphotypes is acceptable as surrogates for the insect species because of their unique morphology and high host plant and plant-organ speciÞcity (Dreger-Jauffret and Shorthouse 1992, Floate et al. 1996, Price et al. 1998, Cuevas-Reyes et al. 2004; for a review, see Carneiro et al. 2009). The statistical analyses of the relationship between species richness and forest age were tested using lm linear models and were performed in the R2.4.1 program (R Development Core Team 2005). In the model, galling species richness (⫽total number of galls induced by the community of insects) was used as the dependent variable, whereas forest age was used as an independent variable. All analyses were followed by inspection of residuals using the Shapiro-Wilk normality test. The inßuence of the succession stage on the composition of the galling community was evaluated through similarity analyses of the galling insect morphospecies and their host plant among the different restored stands of differing ages. Stands were arbi-

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ENVIRONMENTAL ENTOMOLOGY

Vol. 39, no. 4

Table 1. Jaccard similarity index for species of host plants between stages successional

Fig. 1. Relationship between richness of galling insects and age of reforestation in an Amazonian rain forest [F(2,33) ⫽ 26,924; P ⬍0001; equation: gsr ⫽ 1,463 ⫹ 2.508age ⫺ 0.089age2, where gsr ⫽ richness of galling insects; age ⫽ age of restoration).

trarily grouped into three succession periods, initial (0 Ð5 yr), intermediate (6 Ð13 yr), and late (14 Ð21 yr), and evaluated through the similarity index of Jaccard (Krebs 1999). The primary forest was used as a control group. Although 21 yr do not correspond to the full length of the succession period the tropical rain forest presents, the restoration program started with a combination of typical species commonly found in the primary succession. Therefore, this study offered a unique and Þrst opportunity to look into the importance of succession of tropical rain forest on associated herbivores. Results We recorded 309 species of galling insects on 255 species of host plants, belonging to 44 plant families. The average number of galling species per galled host plant was 1.2. The richest host plant families were Fabaceae (87), Burseraceae (18), Malpighiaceae (17), Annonaceae (15), Clusiaceae (15), Melastomatacaeae (13), Chrysobalanaceae (12), Anacardiaceae (11), Euphorbiaceae (9), and Apocynaceae (7). For the complete list and detailed description of the gall morphotypes, see Almada and Fernandes (2010). The model that provided the best Þt for the data on the distribution of galling species richness with forest age showed a quadratic relationship. We found that galling species richness was higher at intermediate forest ages. Fifty-eight percent of the variation in the number of galling insects was explained by the quadratic model (F2,33 ⫽ 22,91; P ⬍ 0,001; R2 ⫽ 0,58; test of normality of Shapiro-Wilk W ⫽ 0.9647, P ⫽ 0.299; Fig. 1). The composition of the host plants of restored areas was distinct from the composition of host plants found in the primary forests. The similarity index of host

Stage

Primary forest

Early

Intermediate

Early Intermediate Late

0.06 0.09 0.09

Ñ 0,23 0.21

Ñ Ñ 0.24

plants was low between primary forests and restored stands (Table 1), whereas among restored areas, the similarity between late and intermediate stages was higher than either of these stages was to the initial stage. A similar trend reported for the host plants was found for the galling insect community. The primary forest presented a distinct community of galling insects compared with the restored stands (Table 2). The similarity of the galling community associated exclusively to the 19 host plant species common to all restored areas and primary forest was high (Jaccard ⫽ 0.61). Otherwise, the richness of galling insects found in the restored areas was higher (n ⫽ 36 species) than that found in the primary forest (n ⫽ 25 species; Table 3). Discussion The richness of galling insects found in this study (n ⫽ 309 species) is relatively high. In a study with galling insects near Manaus, Yukawa et al. (2001) reported 84 species, whereas Juliaõ et al. (2005a) found 236 species in the Mamiraua´ Sustainable Development Reserve in the Amazon. The high richness of galling insects in the restored areas may be caused by a synergistic combination of host plants of different succession stages and the presence of pioneer species that support a large number of herbivores (Fernandes and Price 1988, Fernandes 1992, Fernandes et al. 2005). The peak of 23 galling species found in some forest age stands (Fig. 1) can be the result of several factors acting in combination of the abundance and composition of hosts (Veldtman and McGeoch 2003, Espõ´rito-Santo et al. 2007). Long-term observations will provide further information on whether the pattern reported holds. The results presented here support the hypothesis that herbivores are richer in intermediate stages of succession (Guariguata et al. 1997, Capers et al. 2005). Disturbances can create opportunities for colonization by species that are absent in undisturbed enviTable 2. Jaccard similarity index of galling insects morphospecies between successional stages

Early Intermediate Late Restoreda

Primary forest

Early

Intermediate

Late

Primary forest

0.04 0.07 0.08 Ñ

Ñ 0.24 0.19 Ñ

Ñ Ñ 0.20 Ñ

Ñ Ñ Ñ Ñ

Ñ Ñ Ñ 0.61

a Analysis of the galling insects associated with plant species that occurred simultaneously in primary forest and restored stands.

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Table 3. Host plants that co-occurred in areas of primary native forest and restored stands and occurrence of their galling morphospecies Family Annonaceae Celastraceae Clusiaceae

Dilleniaceae Fabaceae

Flacourteaceae Humiriaceae

Lecythidaceae Melastomataceae Polygalaceae Rubiaceae Tiliaceae

Species Guatteria olivacea Guatteria olivacea Guatteria olivacea Goupia glabra Goupia glabra Goupia glabra Vismia latiflia Vismia latifolia Vismia latifolia Vismia latifolia Vismia latifolia Doliocarpus dentatus Doliocarpus dentatus Dalbergia atropurpurea Dipteryx odorata Hymenaea sp Hymenolobium pulcherrimum Inga Alba Inga alba Inga thibaudiana Peltogyne paniculata Peltogyne paniculata Platymiscium sp. Laetia procera Laetia procera Endopleura uchi Endopleura uchi Endopleura uchi Endopleura uchi Eschweilera coriacea Eschweilera coriacea Eschweilera coriacea Miconia gratissima Miconia gratissima Moutabea guianensis Palicourea guianensis Apeiba echinata Apeiba echinata Total

Gall morphotype

Primary forest

1 2 3 1 2 3 1 2 3 4 5 1 2 1 1 1 1

X X X X X

1 1 1 1 2 1 1 2 1 2 3 4 1 2 3 1 2 1 1 1 2

X X X X

X

X X X X X

X X X X X X

X X X X 25

Restored X X X X X X X X X X X X X X X X X X X X X X X X X X X X X X X X X X X X X 36

ronments such as primary forests. The greatest richness of host plants in habitats of intermediate ages may be the result of the combined presence of pioneer and late stage species, as well as shrubs that are not usually found in the primary forests (Capers et al. 2005). Shrubs support a high richness of galling insects in many vegetation types (Fernandes and Price 1988, 1991). Similarly, the high species richness of galling in restored forests of intermediate ages may be the result of many forces. First, it may be the result of more potential host plants (Fernandes 1992), as shown by Wright and Samways (1998) in the vegetation of fynbos in South Africa, by Oyama et al. (2003) in a tropical forest in Mexico, and by Cuevas-Reyes et al. (2004) in a dry forest also in Mexico. Studies of moths of the family Geometridae in the Ecuatorian Andes (Hilt and Fiedler 2005), in the tropical forests of Borneo (Beck and Khen 2007), and in Mount Kilimanjaro (Axmacher et al. 2004) also provide additional support for this contention. Second, the presence of shrubs and pioneer species with rapid growth in the areas of intermediate ages may also result in higher richness of galling insects. In this study, pioneer species such as Goupia glabra, Doliocarpus dentatus, and Vismia spp. are host of a large number of galling herbivores (Almada and Fernandes 2010). Fast-growing species generally present greater availability of meristems to be galled (Price 2005, Espõ´rito-Santo et al. 2007). A third

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possible effect for the high richness in intermediate stage is the composition of species (Veldtman and McGeoch 2003) or even the presence of super-host plants (Fernandes and Price 1988, Blanche and Westoby 1995, Veldtman McGeoch 2003). In fact, many species used in the restoration program correspond to super hosts such as Vismia spp. that may support up to 11 galling species (5 alone on V. latifolia) and Goupia glabra that supports 4 galling species. These are species associated with initial succession stages. These three nonexclusive hypotheses indicate the importance of bottom-up forces in the structure and composition of the herbivore fauna. Future studies should address the turnover in species at different stages of succession to determine whether the increase in species richness is caused by the addition of species to an existing pool or the introduction of a completely different set of species. The results of the analysis of similarity indicate that there is a parallel shift between the community of galling insects and the community of their host plants, which may be explained by the high degree of speciÞcity of the community of galling insects with their host plants. The initial and intermediate stages presented a more similar community of galling insects, possibly indicating that plant composition of such habitats is more similar compared with older successional stages. Alternatively, it could be driven by differential colonization and survival of the gallers on older successional stages independently on the occurrence of host plants. These results also indicate that the restoration of plant community is allowing an effective recolonization of these areas by the community of galling insects. The similarity of the community of galling insects associated with host species that occurred in primary forest sites and in the restored areas was high. These data indicate the following: Þrst, the galling community is being restored, and second, the galling insects might be inßuenced by the structure, quality, and succession stage of the forest. Studies on other groups of tropical insects reported similar trends (Davies et al. 1999, Andersen et al. 2002, Beck and Khen 2007). For the group of hosts common to primary and restores forests, more galling species were found in restored areas (n ⫽ 36) compared with primary forests (n ⫽ 24). This Þnding supports the hypothesis that environmental stresses may play an important role in galling success and/or perhaps host resistance to galling (Fernandes and Price 1991, Ribeiro and Basset 2007). Although the study was not designed to directly test this hypothesis, it highlights a possible and important connection of habitat stress and galling community diversity. Early succession periods would simulate the more xeric conditions, whereas later succession stages would simulate the more mesic conditions reported by Fernandes and Price (1988). During early succession stages, plant density and canopy biomass are lower, providing physical opportunities for light to penetrate in the low stature and unstructured forest. As succession progresses, habitat stress diminishes, whereas

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new ecological forces come into play, such as host plant composition and natural enemies. Because of the ease of sampling gallers (Fernandes and Price 1988) and their high sensitivity to environmental change (Fernandes and Price 1991), galling insects are an ideal group of species to use in monitoring biodiversity and habitat quality. In a pioneering assessment of the impact of iron mines, Bagatto and Shorthouse (2001) found higher concentrations of copper and nickel in the tissues of galls compared with other tissues of healthy plants. Juliaõ et al. (2005b) evaluated the importance of the type of urban habitat for a community of galling insects associated to two host plants, whereas Moreira et al. (2007) reported on the positive inßuence of the composition of host species in the community of galling insects in succession areas of the Atlantic rain forest. This study provides more support for the use of galling insects as bioindicators candidates. Because of their extremely Þnetuned physiological and phenological interactions with their hosts (Fernandes 1990, Shorthouse et al. 2005), galling insects may be sensitive to changes in plant quality and density of their host species in a variety of habitats and in a wide range of environmental conditions. The use of galling insects for monitoring the quality of the process of restoration proved to be an efÞcient tool to evaluate habitat quality in the tropical rain forests of Amazon. The galling community was sensitive to the age of the reforestation and changes in the structure and characteristics of the forests, as well as the composition of host plants. However, to better understand the factors that govern the dynamics of the community of insects galling in the process of succession, we suggest further studies on the importance of distance of forest fragments and remaining areas with edge effects. Acknowledgments We thank P. W. Price, T. P. Craig, and one anonymous reviewer for criticisms on earlier versions of the manuscript. This study was supported by Planta Tecnologia Ambiental and Mineraç aõ Rio do Norte SA. We also thank CNPq (Conselho Nacional de Desenvolvimento Cientõ´Þco e Tecnolo´ gico 30.9633/2007-9), Fapemig, and the Flona Saraca´Taquera for the facilities provided.

References Cited Almada, E. D., and G. W. Fernandes. 2010. Caracterizaç aõ e distribuiç aõ de insetos indutores de galhas em ßorestas de terra-Þrme e em reßorestamentos com espe´ cies nativas na Amazoˆ nia Oriental. Bol. Museu Paraense Emõ´lio Goeldi. (in press). Andersen, A. N., B. D. Hoffmann, W. J. Mu¨ ller, and A. D. Griffiths. 2002. Using ants as bioindicators in land management: simplifying assessment of ant community responses. J. Appl. Ecol. 39: 8 Ð17. Axmacher, J. C., H. Tunte, M. Schrumpf, K. Mu¨ ller-Hohenstein, V.M.L. Herbert, and K. Fiedler. 2004. Diverging diversity patterns of vascular plants and geometrid moths during forest regeneration on Mt Kilimanjaro, Tanzania. J. Biogeogr. 6: 895Ð904.

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Bagatto, G., and J. D. Shorthouse. 1991. Accumulation of copper and nickel in plant tissues and an insect gall of lowbush blueberry, Vaccinium angustifolium, near an ore smelter at Sudbury, Ontario, Canada. Can. J. Botany 69: 1483Ð1490. Barlow, J., W. L. Overal, I. S. Arau´ jo, T. A. Gardner, and C. A. Peres. 2007. The value of primary, secondary and plantation forests for fruit-feeding butterßies in the Brazilian Amazon. J. Appl. Ecol. 44: 1001Ð1012. Beck, J., and C. V. Khen. 2007. Beta-diversity of geometrid moths from northern Borneo: effects of habitat, time and space. J. Anim. Ecol. 76: 230 Ð237. Begon, M., C. R. Townsend, and J. L. Harper. 2006. Ecology: from individuals to ecosystems, 4nd ed. Blackwell Publishing, London, United Kingdom. Blanche, K. R., and M. Westoby. 1995. Gall-forming insect diversity is linked to soil fertility via host plant taxon. Ecology 76: 2334 Ð2337. Capers, R. S., R. L. Chazdon, A. R. Brenes, and B. V. Alvarado. 2005. Successional dynamics of woody seedling communities in wet tropical secondary forests. J. Ecol. 93: 1071Ð 1084. Carneiro, M.A.A., C.S.A. Branco, C.E.D. Braga, E. D. Almada, M.B.M. Costa, G. W. Fernandes, and V. C. Maia. 2009. Are gall midge species (Diptera: Cecidomyiidae) host plant specialists? Rev. Bras. Entomol. 53: 365Ð378. Connell, J. H. 1978. Diversity in tropical rain forest and coral reefs. Science 199: 1304 Ð1310. Cuevas-Reyes, P., M. Quesada, P. Hanson, R. Dirzo, and K. Oyama. 2004. Diversity of gall-inducing insects in a Mexican tropical dry forest: the importance of plant species richness, life forms, host plant age and plant density. J. Ecol. 92: 707Ð716. Cunningham, S. A., R. B. Floyd, and T. A. Weir. 2005. Do eucalyptus plantations host an insect community similar to remnant Eucalyptus forest? Austral. Ecol. 30: 103Ð117. Davies, R. G., P. Eggleton, L. Dibog, J. Lawtom, D. E. Bignell, A. Brauman, C. Hartmann, L. Nunes, J. Holt, and C. Rouland. 1999. Successional response of a tropical forest termite assemblage to experimental habitat perturbation. J. Appl. Ecol. 36: 946 Ð962. DeWalt, S. J., S. A. Schnitzer, and J. S. Denslow. 2000. Density and diversity of lianas along a chronosequence in a central Panamanian lowland forest. J. Trop. Ecol. 16: 1Ð19. Dreger-Jauffret, F., and J. D. Shorthouse. 1992. Diversity of gall-inducing insects and their galls, pp. 8 Ð33. In J. D. Shorthouse and O. Rohfritsch (eds.), Biology of insectinduced galls. Oxford University Press, Oxford, United Kingdom. Elderd, B. D. 2006. Disturbance-mediated trophic interactions and plant performance. Oecologia 147: 261Ð271. Espı´rito-Santo, M. M., F. S. Neves, F. R. Andrade-Neto, and G. W. Fernandes. 2007. Plant architecture and meristem dynamics as the mechanisms determining the diversity of gall-inducing insects. Oecologia 153: 353Ð364. Fernandes, G. W. 1990. Hypersensitivity: a neglected plant resistance mechanism against insect herbivores. Environ. Entomol. 19: 1173Ð1182. Fernandes, G. W., and P. W. Price. 1988. Biogeographical gradients in galling species richness. Oecologia 76: 161Ð 167. Fernandes, G. W. 1992. Plant historical and biogeographycal gradients effect on insular gall-forming species richness. Global Ecol. Biogeogr. Lett. 2: 71Ð74. Fernandes, G. W., and P. W. Price. 1991. Comparison of tropical and temperate galling species richness: the roles of environmental harshness and plant nutrient status, pp. 91Ð115. In P. W. Price, T. M. Lewinsohn, G. W. Fernandes,

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and W. W. Benson (eds.), Plant-animal interactions: evolutionary ecology in tropical and temperate regions. John Wiley, New York. Fernandes, G. W., S. J. Gonç alves-Alvim, and M.A.A. Carneiro. 2005. Habitat-driven effects on the diversity of gall-inducing insects in the Brazilian Cerrado Biology, ecology and evolution of gall-inducing arthropods, pp. 693Ð708. In A. Raman, C. W. Schaefer, and T. M. Withers (eds.), Biology, ecology, and evolution of gall-inducing arthropods. Science Publishers, Washington, DC. Ferraz, J.B.S. 1993. Soil factors inßuencing the reforestation on mining sites in Amazonia, pp. 47Ð52. In H. Lieth and M. Lohrann (eds.), Restoration of tropical forest ecosystems. Kluwe, Academic Publishers, Doidrecht, The Netherlands. Floate, K. D., G. W. Fernandes, and J. A. Nilsson. 1996. Distinguishing intrapopulational categories of plants by their insect faunas: galls on rabbitbrush. Oecologia 105: 221Ð229. Floren, A., and A. Linsenmair. 2001. The inßuence of anthropogenic disturbances on the structure of arboreal arthropod communities. Plant Ecol. 153: 153Ð167. Foggo, A., C.M.P. Ozanne, M. R. Speight, and C. Hambler. 2001. Edge effects and tropical forest canopy invertebrates. Plant Ecol. 153: 347Ð359. Fonseca, C. R., T. Fleck, and G. W. Fernandes. 2006. Processes driving ontogenetic succession of galls in a canopy. Biotropica 38: 514 Ð521. Gaston, K. J. 1992. Regional numbers of insect and plant species. Funct. Ecol. 6: 243Ð247. Gaston, K. J. 2000. Global patterns in biodiversity. Nature 405: 220 Ð227. Gonç alves-Alvim, S. J., and G. W. Fernandes. 2001. Comunidades de insetos galhadores (Insecta) em diferentes Þsionomias do cerrado em Minas Gerais, Brasil. Rev. Brasileira Zool. 18: 289 Ð305. Grimbacher, P. S., and C. P. Catterall. 2007. How much do site age, habitat structure and spatial isolation inßuence the restoration of rainforest beetle species assemblages? Biol. Conserv. 135: 107Ð118. Grime, J. P. 1973. Control of species density in herbaceous vegetation. J. Environ. Manage. 1: 151Ð167. Guariguata, M. R., R. L. Chazdon, J. S. Denslow, J. M. Dupuy, and L. Anderson. 1997. Structure and ßoristics of secondary and old-growth forest stands in lowland Costa Rica. Plant Ecol. 132: 107Ð120. Hilt, N., and K. Fiedler. 2005. Diversity and composition of Arctiidae moth ensembles along a successional gradient in the Ecuadorian Andes. Divers. Distribut. 11: 387Ð398. Hobbs, R. J., and H. A. Mooney. 1991. Effects os rainfall variability and gopher disturbance on serpentine annual grassland dynamics. Ecology 72: 59 Ð 68. Jansen, A. 1997. Terrestrial invertebrate community structure as indicator of the success of a tropical rainforest restoration project. Restoration Ecol. 5: 115Ð124. Julia˜ o, G. R., E. M. Venticinque, and G. W. Fernandes. 2005a. Richness and abundance of gall-forming insects in the Mamiraua´ Varzea, a ßooded Amazonian forest. Uakari 1: 39 Ð 42. Julia˜ o, G. R., G. W. Fernandes, D. Negreiros, L. Bedeˆ, and R. C. Arau´ jo. 2005b. Insetos galhadores associados a duas espe´ cies de plantas invasoras de a´reas urbanas e peri-urbanas. Rev. Bras. Entomol. 49: 97Ð106. Kalacska, M., G. A. Sanchez-Azofeifa, J. C. Calvo-Alvarado, M. Quesada, B. Rivard, and D. H. Janzen. 2004. Species composition, similarity and diversity in three successional stages of a seasonally dry tropical forest. Forest Ecol. Manage. 200: 227Ð247.

1139

Kennard, D. K. 2002. Secondary forest succession in a tropical dry forest: patterns of development across a 50-year chronosequence in lowland Bolivia. J. Trop. Ecol. 18: 53Ð 66. Knowles, O. H., and J. A. Parrotta. 1995. Amazonian forest restoration: an innovative system for native species selection based on phenological data and performance indices. Commonwealth For. Rev. 74: 230 Ð243. Knowles, O. H., and J. A. Parrotta. 1997. Phenological observations and tree seed characteristics in an equatorial moist forest at Trombetas, Para´ State, Brazil, pp. 67Ð 84. In H. Lieth and M. D. Schwartz (eds.), Phenology in seasonal climates. Backhuys, Leiden, The Netherlands. Krebs, C. J. 1999. Ecological methodology, 2nd ed. Benjamin Cummings, Menlo Park, CA. Kruess, A., and T. Tscharntke. 2000. Species richness and parasitism in a fragmented landscape: experiments and Þeld studies with insects on Vicia sepium. Oecologia 122: 129 Ð137. Lara, A.C.F., G. W. Fernandes, and S. J. Gonç alves-Alvim. 2002. Tests of hypotheses on patterns of gall distribution along an altitudinal gradient. Trop. Zool. 15: 219 Ð232. McGeoch, M. A. 1998. The selection, testing and application of terrestrial insects as bioindicator. Biol. Rev. 73: 181Ð 201. Molino, J. E., and D. Sabatier. 2001. Tree diversity in tropical rain forests: a validation of the intermediate disturbance hypothesis. Science 294: 1702Ð1704. Moreira, R. G., G. W. Fernandes, E. D. Almada, and J. C. Santos. 2007. Galling insects as bioindicators of land restoration in an a´rea of Brazilian Atlantic Forest. Lundiana 8: 107Ð112. Nagaike, T. 2002. Differences in plant species diversity between conifer (Larix kaempferi) plantations and broadleaved (Quercus crispula) secondary forests in central Japan. Forest Ecol. Manage. 168: 111Ð123. Nakamura, A., H. Proctor, and C. Catterall. 2003. Using soil and litter arthropods to assess the state of rainforest restoration. Ecol. Manage. Restoration 4: 20 Ð28. Novotny, V., P. Drozd, S. E. Miller, M. Kulfan, M. Janda, Y. Basset, and G. D. Weiblen. 2006. Why are there so many species of herbivorous insects in tropical rainforests? Science 313: 1115Ð1118. Oyama, K., M. A. Perez-Perez, P. Cuevas-Reyes, and R. LunaReyes. 2003. Regional end local species richness of gallinducing insects in two tropical rain forest in Me´ xico. J. Trop. Ecol. 19: 595Ð598. Parrish, J.A.D., and F. A. Bazzaz. 1982. Responses of plants from three successional communities to a nutrient gradient. J. Ecol. 70: 233Ð248. Parrotta, J. A., and O. H. Knowles. 1999. Restoration of tropical moist forests on bauxite-mined lands in the Brazilian Amazon. Restoration Ecol. 7: 103Ð116. Parrotta, J. A., and O. H. Knowles. 2001. Restoring tropical forests on lands mined for bauxite: examples from the Brazilian Amazon. Ecol. Eng. 17: 219 Ð239. Parrotta, J. A., O. H. Knowles, and J. M. Wunderle. 1997. Development of ßoristic diversity in 10-year-old restoration forests on a bauxite mined site in Amazonia. Forest Ecol. Manage. 99: 21Ð 42. Pen˜ a-Claros, M., and H. de Boo. 2002. The effect of forest successional stage on seed removal of tropical rain forest tree species. J. Trop. Ecol. 18: 261Ð274. Price. P. W. 2005. Adaptive radiation of gall-inducing insects. Basic Appl. Ecol. 6: 413Ð 421. Price, P. W., G. W. Fernandes, A. C. Lara, J. Bran, H. Barrio, M. G. Right, S. P. Ribeiro, and N. Rothcliff. 1998. Global

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patterns in local number of insect galling species. J. Biogeogr. 25: 581Ð591. Ratchford, J. S., S. E. Wittman, E. S. Jules, A. M. Ellison, N. J. Gotelli, and N. J. Sanders. 2005. The effects of Þre, local environment and time on ant assemblages in fens and forests. Divers. Distribut. 11: 487Ð 497. R Development Core Team. 2006. R: a language and environment for statistical computing. R Foundation for Statistical Computing, Vienna, Austria. Ribeiro, S. P., and Y. Basset. 2007. Gall-forming and freefeeding herbivory along vertical gradients in a lowland tropical rainforest: the importance of leaf sclerophylly. Ecography 30: 663Ð 672. Rodrı´guez, J. P., D. L. Pearson, and R. Barrera. 1998. A test for the adequacy of bioindicator taxa: are tiger beetles (Coleoptera: Cicindelidae) appropriate indicators for monitoring the degradation of tropical forests in Venezuela? Biol. Conserv. 83: 69 Ð76. Rosenzweig, M. L. 1995. Species diversity in space and time. Cambridge University Press, Cambridge, United Kingdom. Shorthouse, J. D., D. Wool, and A. Raman. 2005. Gall-inducing insects - natureÕs most sophisticated herbivores. Basic Appl. Ecol. 6: 407Ð 411.

Vol. 39, no. 4

van Nouhuys, S. 2005. Effects of habitat fragmentation at different trophic levels in insect communities. Ann. Zool. Fenn. 42: 433Ð 447. Veldtman, R., and M. A. McGeoch. 2003. Gall-forming insect species richness along a non-scleromorphic vegetation rainfall gradient in a South Africa: the importance of plant community composition. Austral. Ecol. 28: 1Ð13. Yukawa, J., M. Tokuda, N. Uechi, and S. Sato. 2001. Species richness of galling arthropods in Manaus, Amazon and the surroundings of the Iguassu Falls. Esakia 41: 11Ð15. Webb, E. L., and R. N. Sah. 2003. Structure and diversity of natural and managed sal (Shorea robusta Gaertn. f.) forest in the Terai of Nepal. Forest Ecol. Manage. 176: 337Ð353. Wootton, J. T., M. E. Power, and M. S. Parker. 1996. Effects of disturbance on river food webs. Science 273: 1558 Ð 1561. Wright, M. G., and M. J. Samways. 1998. Insect species richness tracking plant species richness in a diverse ßora: gall-insects in the Cape Floristic Region, South Africa. Oecologia 115: 427Ð 433. Received 15 July 2009; accepted 1 April 2010.