Running title: Tree species richness increases parasitoid diversity

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Carlos Frankl Sperber1*, Kazuiyuki Nakayama2,3, Maria Júlia Valverde3 & Frederico de Siqueira Neves2


Tree species richness and density affect parasitoid diversity in cacao agroforestry

Running title:

Tree species richness increases parasitoid diversity

Words: 4846

Words in title: 11

Abstract: 290 words

1 Departamento de Biologia Geral, Universidade Federal de Viçosa, Brazil

2 Entomology Graduation Programm, Departamento de Biologia Animal, Universidade Federal de Viçosa, 36570-000, Viçosa, MG, Brazil, E-mail:

3 CEPLAC/CEPEC/SECEN, Rodovia Ilhéus–Itabuna, km. 22, CP: 7, 45.600-000, Itabuna, BA, Brazil, E-mail:
* Corresponding author: Carlos Frankl Sperber, Departamento de Biologia Geral, Universidade Federal de Viçosa, 36570-000, Viçosa, MG, Brazil, Phone: +55 31 3899 2556, Fax: +55 31 3899 2549, E-mail:


In Brazil, cacao is mostly planted beneath shade trees. The diversity of shade trees varies from monospecific to highly diverse canopies, characteristic of pristine Atlantic Forest. This study evaluates the relationships between family richness of Hymenoptera-Parasitica and Chrysidoidea, and tree species richness and density, the species richness of herbaceous understorey, and the area and age of the cacao agroforestry system. We sampled 16 cacao agroforestry systems, with canopy diversity ranging from one to 22 tree species per hectare, in three seasons: summer (March), winter (August) and spring (November). Parasitoids were sampled using eight Malaise-Townes traps per site. Tree species richness and density were enumerated within one hectare at each site, and herbaceous plant species richness was calculated in eight 1 m2 plots, within the hectare. The number of parasitoid families increased with tree species richness and density in spring and summer, but decreased in winter. Neither species richness of herbaceous plants nor area and age of the system affected parasitoid family richness. We suggest that the increase of parasitoid diversity with tree species richness and density in warmer seasons reflects increasing heterogeneity and availability of resources. The decrease in parasitoid family number with tree density in winter may be due to local impoverishment of resources, leading to parasitoid emigration to neighbouring forest remnants. This result implies that a higher diversity of shade trees will help maintain high parasitoid levels and, in consequence, higher levels of natural enemies of cacao pests, particularly in the warmer seasons. This prediction is borne out in the experience of cacao producers. The proper management of shade tree diversity will play a vital role in maintaining the sustainability of cacao agroforestry production systems in the tropics and, concurrently, will maintain high biodiversity values in these locations.

Key words: biodiversity hotspot – Brazilian Atlantic Forest – cabruca – canopy – habitat heterogeneity – LME - seasonality – wasps


[We would like to ask for German translation]

Tropical landscapes are dominated by agroecosystems, but the potential value of such agroecosystems for the conservation of species is often overlooked (Klein et al. 2002). Investigations of the determinants of biodiversity, especially in managed areas within high diversity regions, must be of high priority so that conservation values can be maximised and impacts minimized in these irreplaceable areas.
At the local spatial scale, species diversity may be influenced by area, species interactions, disturbance, resource availability, and habitat heterogeneity (Ricklefs & Schluter 1993, Begon et al. 1996). It is expected that diversity will increase with habitat heterogeneity (Strong et al. 1984). Levels of parasitism may increase with landscape complexity (Kruess 1994, Marino & Landis 1996, Thies & Tscharntke 1999, Menalled et al. 1999), and ant species richness has been shown to increase with tree species richness (a surrogate for ‘habitat heterogeneity’) (Ribas et al. 2003).

The highest priority areas for conservation have been designated ‘biodiversity hotspots’ (Myers et al. 2000). Brazil’s Atlantic Forest is one of these biodiversity hotspots, with a wealth of endemic species, and high levels of past, present and potential degradation. In two sites near Ilhéus, southern Bahia, more than 44 % of the tree species (Angiospermae) are endemic to the coastal forest and more than 26 % are endemic to southern Bahia and northern Espírito Santo (Thomas et al. 1998).

One of the most significant factors which contribute to the loss of biodiversity in forested areas is the introduction of intensive agricultural systems (Mahar 1989). One way to ameliorate such impacts while maintaining agricultural productivity is the promotion of less environmentally ‘aggressive’ agroecosystems such as those which combine elements of forestry, particularly of local tree species, with other crops (‘agroforestry’). (Altieri 1987, Nair 1993). In Brazil, cacao (Theobroma cacao L., Sterculiaceae) is mostly planted within agroforestry systems. The shade trees may be planted, or the canopy of the native forest thinned and the cacao planted as an understorey. Planted overstorey trees are most commonly Erythrina fusca Lour. (Leguminosae: Papilionoideae) and Hevea brasiliensis (Wild.) Muell.-Arg. (Euphorbiaceae). When cacao is cultivated beneath native forest trees, it is referred to as cabruca (Vinha et al. 1976; Rosand et al. 1987). In Brazil mostr cacao is grown in areas currently or once covered by Atlantic rainforest.

(Coimbra-Filho & Câmara 1996). Accordingly where cabruca systems are in place the overall agroecosystems may present high levels of tree richness and, potentially at least, be of high conservation value.

Tropical insects show accentuated seasonality (Wolda 1989, 1992), probably related to tree phenological events, such as leaf shedding and budding, flowering and fruiting (Janzen 1975, Larcher 2000). These may influence the number of parasitoid families directly or indirectly, and may well affect the relationship between parasitoid diversity and tree diversity.

In this study we evaluate whether the number of Hymenoptera families of the Parasitica series and of the Chrysidoidea superfamily, increase with the richness and density of tree species in the overstorey, herbaceous plant species richness in the understorey, and the area and age of the cacao agroforestry system. We also evaluate if these relationships are affected by season.

Materials and methods
Study area and sites
The sampling sites where located in Bahia, Brazil, in a polygon which includes remnants of Atlantic forest (bounded by: 15o17’S, 39o04’W; 15o25’S, 39o19W; 15o25’S, 39o39’W; 15o05’S, 39o20’W), in a climatic region regarded as optimal for cacao agroforestry (Sá et al. 1982). The mean annual temperature is 24 oC, with lowest temperatures (monthly mean = 20 oC) in June to August (winter) and highest temperatures (monthly mean = 26 oC) in December to March (summer). There are pronounced differences between wet and dry seasons, with total annual precipitation below 750 mm (Rosand et al. 1987).

We compared 16 cacao agroforestry systems, between seven and 55 km apart, (Table 1). The systems chosen presented levels of richness of shade trees ranging from one (Erythrina fusca or Hevea brasiliensis) to 22 species per hectare (Lauraceae, Leguminosae, Meliaceae, Moraceae, Sapotaceae, and others).


In each cacao agroforestry system we determined tree species richness, tree density and the richness of herbaceous plants. Tree species richness was determined by counting all tree species within a seingle hectare. All trees with a crown which overtopped the cacao plants, were included. Tree density was calculated by counting the number of trees in this site. Herbaceous plant species richness was calculated by counting the number of species of herbs in one square meter plot, located in the core of each one-hectare site. When in doubt, identification was confirmed by comparing field material with the herbarium collection of CEPLAC (Centro de Pesquisas da Lavoura Cacaueira) [WHAT IS THIS??]. All collected material was incorporated subsequently in the CEPLAC collection.

Sampling of parasitoids

Each agroforestry system was sampled using eight Malaise-Townes traps (Townes 1972), erected on the ground for one day, along a 100 m transect, in the core of each one hectare site. We used a total of 32 traps, manipulated by two teams. Each team used 16 traps, sampling one or two sites per day. Each site was sampled on three occasions: summer (17 to 28 March 2001), winter (5 to 14 August 2001), and spring (22 November to 2 December 2001). The whole study involved (16 sites 8 traps 1 day) - a total of 384 trap-days.

Parasitoid diversity

Parasitoid diversity was calculated as the mean number of families of Hymenoptera-Parasitica series (Terebrantia) or of the Chrysidoidea superfamily, sampled per trap in each site. The taxa involved were almost all (> 95 %) parasitoids and contain most of the known hymenopterous parasitoids (Goulet & Huber 1993). Families were identified using Goulet & Huber (1993) and Gibson et al. (1997). We chose to work at the level of the family, because the taxonomy of parasitoids in tropical regions is poorly known at the genus and species level and, because the sheer number of specimens collected in this study obviated the use of any finer taxonomic level. Higher taxon diversity may be a good surrogate of species diversity (Humphries et al. 1995, Cabeza & Moilanen 2001, Baldi 2003).


We used linear mixed effect models, with tree species richness, season, herb richness, tree density, area and age of cacao agroforestry system as explanatory variables. The analyses also generated interaction terms.

All of the explanatory variables were put into the model as fixed effects (Table 1). The site of variables related to the cacao systems wasere regarded as random effect. Mixed-effects models enable us to model correlations that may exist within grouped data (Pinheiro & Bates 2000; Buckley et al. 2003). Accordingly all the fixed effect variables were nested within the random effects of the site of the cacao agroforestry system, thus avoiding pseudoreplication (Crawley 2002).

We used the natural logarithm of the number parasitoid family numbers as the response variable within the model to normalise the count errors and so meet the demands of the linear mixed effect model (Buckley et al. 2003).

Our analysis used both categorical and continuous variables and so was analogous to a multiple regression with an associated analysis of covariance (Crawley 2002). We progressively simplified the model by removing non-significant terms in a stepwise fashion.. We did this in an hierarchical manner beginning with the removal of the highest level interaction terms, then, the non-significant explanatory variables. Finally we amalgamated non-significant factor levels, using contrasts (see Crawley 1993).We evaluated models usingf analyses of variance, F-tests of the maximum likelihood ratios within and between models. Finally we calculated and assessed the minimal adequate model (Crawley 2002, Buckley et al. 2003).

Tree species richness and density were present as explanatory variables in the adjusted minimal adequate model. We examined the correlation between these two variables with Pearson’s product-moment correlation (Crawley 2002). All analyses were done within the R statistical package, R 1.7.1 © 2003; The R Development Core Team (Ihaka & Gentleman 1996).

In total we sampled 21346 individual parasitoids (Hymenoptera Parasitica and Chrysidoidea), belonging to 33 families (Table 2). The superfamilies Platygastroidea, Chalcidoidea, and Ichneumonioidea were most abundant.
In the complete model, only season, tree species richness, and the interaction term of season with tree species richness and of season with tree density were significant (Table 3). The minimal adequate model included all these significant variables plus tree density, which could not be removed from the model because it was included as part of a significant interaction term ly realated to family richness (Table 4). Richness of herbaceous plants, the area and age of the cacao agroforestry system, and the interaction terms not included in the minimal model, did not affect the number of parasitoid families (Table 3). The numbers of parasitoid families increased with tree species richness and tree density in both spring and summer, but decreased in winter (Table 5, Fig. 1). Tree species richness and tree density were strongly correlated (Fig. 2, r = -0.89, t = 13.04, d.f. = 46, p < 0.0001).

This work showed that the abundance of parasitoids in cacao agroforestry systems is astonishingly high, when compared with other systems. For example we collected almost three times the number of individuals per unit trapping effort than did Matlock & de la Cruz (2002) in a mosaic of agriculture and forest remnants in the Caribbean..

The family taxonomic level was sensitive to the effects of variables related to the canopy of shade trees, possibly due to their high levels of specialisation. Most parasitoid families prey upon a restricted range of insect orders (Quicke 1997). It seems unlikely that the use of a lower taxonomic level for the parasitoids would show any different trend.

The taxonomic composition of the hymenopteran assemblage in our study was similar to that in natural forest of the same biome. Sampling an Atlantic forest reserve, Azevedo & Santos (2000) collected 8305 individuals, in 30 families. The number of families was almost the same in their study and ours - the most abundant super-families were the same, with the same order of abundance. Scelionidae was the most abundant family in both studies, Platygastridae, Ichneumonidae, Braconidae, and Eucoilidae were among the ten most abundant families in Azevedo & Santo’s (2000) study.

Our results showed that parasitoid family numbers are affected by the richness and density of the shade trees which form the canopy of the agroecosystem. Similar trends have been demonstrated for other predatory insects. In sclerophyllous cerrado vegetation in Brazil, ant species richness increased with tree species richness and tree density (Ribas et al. 2003). In general, tree species richness is probably a surrogate for resource heterogeneity (Tilman & Pacala 1993, Ribas et al. 2003). So, for example, Lill et al. (2002) showed that some parasitoid species are specialized with respect to tree species - each new tree species provides a different set of direct and indirect resources for parasitoids.

Direct resources include supplementary food such as pollen, nectar, and honeydew (Thompson 1999; Wackers 2001, Beach et al. 2003, Gentry 2003, enemy free space (Russell 1989), suitable microhabitats (Lawton 1983; Bell et al. 1991; Ribas et al. 2003), and herbivorous hosts associated with the trees (Hawkins 1990, Godfray 1993, Hawkins & Mills 1996, Quicke 1997).

The species richness of insect herbivores is probably positively correlated with tree species richness (Erwin 1982; Novotny et al. 2003). The greater the herbivore specialization and the faunal turnover among tree species, the stronger will be the correlation of herbivorous species richness with tree species richness (Basset et al. 1996). The percentage of monophagous herbivorous insects in the canopy may be as low as 4 % (Novotny et al. 2002) or as high as 26 % (Barone 1998); the faunal overlap among tree species canopies is generally high (Basset & Novotny 1999). Tree diversity is correlated with faunal composition (Brehm et al. 2003). The richness of herbivores on any one tree will be affected not only by the identity of the tree species itself but by the pattern of adjacent canopies (Basset & Novotny 1999). In addition, variation in plant traits among plant species may well promote the development of a characteristic functional assemblage of insect herbivores associated with each plant species (Peeters et al. 2001).

Why, then, did the number of parasitoid families increase with tree density in the warm seasons? For tropical forest figs, significant predictors of insect species richness include tree density (Basset & Novotny 1999). In experimentally manipulated agroecosystems, shade structures have a strong effect on enemy and herbivore trophic levels (Dyer & Stireman 2003). Klein et al. (2002), studying a cacao agroforestry system, showed that the abundance and species richness of entomophagous insects diminished with land-use intensity: an effect which the authors ascribed to reduced species richness of shade trees as well as increased temperature, decreased canopy cover and lower humidity. Increased tree density maintains a mesic microclimate, which Fernandes & Price (1991, 1992) have hypothesised to favour parasitoids of herbivores.

We are confident that the effect of tree species richness and density upon the numbers of families of parasitoids is not merely a spurious correlation. There was a significant correlation of tree species richness with tree density, but this was negative rather than the positive trend that has been observed in other systems (Ribas et al. 2003). This negative correlation is probably the result of human interventions within the cacao agroecosystem. Locations with the lowest tree richness have canopies composed of planted trees – in other words their minimal richness is entirely anthropogenic.

The switch in direction in the relationship between parasitoid richness and overstorey richness that we observed across seasons is probably related to differences in resource availability. In the warmer, growing seasons, there is an increased availability in new meristematic tissue, new leafs and fruits which are often preferred resources for herbivores (Wolda 1989, 1992; Novotny et al. 2003, Wagner 2001) which, in turn, are a resource for parasitoids. Flowering phenology may also be implicated. Many tropical tree species flower synchronously (Augspurger 1985; Kirmse et al. 2003), which may well be reflected in an apparent seasonality in their directly or indirectly dependent insect associates (Basset et al. 2003, Didham & Springate 2003, Itioka et al. 2003).

The negative relationship between parasitoid family numbers and tree species richness and density in the winter is more difficult to explain. The lower parasitoid diversity in the systems with monospecific shade trees may have a landscape-level explanation possibly involving the emigration of the parasitoids to neighbouring forest remnants (Ricklefs & Schluter 1993; Chesson 2000) in search of scarce resources. Natural habitat remnants may harbour most of the animal diversity of agriculturally managed systems (Duelli & Obrist 2003). In addition, in the winter, temperature is lower and rainfall less (Rosand et al. 1987), which will likely reduce plant growth and flowering, with consequent negative impacts upon populations of insect herbivores both directly (as development rates decrease) and indirectly though comparable negative impacts upon resources (Ferro 1987).

Although the traps we used were located at ground level, parasitoid diversity was unaffected by species richness of herbaceous plants. This contrasts with multiple cropping systems or crops intermingled with weeds, where parasitoid diversity is correlated to herbaceous plant diversity (Andow 1990, and references therein).

Our results showed that parasitoid diversity was not affected by the area or the age of the cacao agroforestry system and this result agrees with what previous information exists on the topic (see the results of Matlock & de la Cruz 2002, from Central Sulawesi). This may be the result of different parasitoid species responding to different spatial scales (Roland & Taylor 1997).

Our results have direct implications for herbivore regulation and sustainable management of cacao agroforestry systems. Cacao agroforestry systems using natural forest as shade trees maximize parasitoid family numbers in the warm seasons, when herbivore populations are higher (Ferro 1987) increasing the likely efficiency of natural pest control. Klein et al. (2002), studying tropical cacao agroforestry systems and natural forests, showed that the predator-prey ratio was reduced with land-use intensity. Use of insecticides and nematicides reduces species richness and abundance of parasitoids in a mosaic of agricultural habitats and forest remnants (Matlock & de la Cruz 2002). In less diverse cacao habitats, the abundance of particular herbivorous taxa, such as rhizophagous Coleoptera, is higher than in cacao under natural forest (Garcia & Silveira Neto 1980; Benton 1984). There is also evidence that cacao planted under shade trees, irrespective of tree species richness, experiences a lower frequency of pest outbreaks (Abreu 1972, Benton 1984, Medeiros et al. 1995), and requires lower levels of pesticide use (CEPLAC 1980). Therefore, vegetational diversity can lead to supression of pests via ‘top-down’ enhancement of natural enemy populations, as well as longer term benefits for sustainability of the farming system and, ultimately, broad societal benefits including aesthetics and conservation of flora and fauna (Gurr et al. 2003).

The maintenance of natural forest canopy as shade trees in the cacao agroforestry system may have conserved, or even enhanced (see Sax & Gaines 2003), the naturally occurring number of parasitoid families. This has been demonstrated in comparisons with natural systems. Accordingly the use of natural mixtures as shade for cacao is not only good sense from the point of view of reducing pest numbers but also has considerable positive implications for conservation. This is particularly important in regions such as the Atlantic forest which is recognised as a biodiversity ‘hotspot’ (Myers et al. 2000)


This work was done as part of the requisites for the PhD thesis of K. Nakayama, who was supported with a grant from CNPq (Conselho Nacional de Pesquisa). We thank Celso O. Azevedo for training in taxonomy, José Henrique Schoereder for manuscript review, Og DeSouza for the initial ideas, Carla Galbiati for helping with the statistical analyses, and Roger L. Kitching, for English revision. Two anonymous referees, gave valuable critics and suggestions which improved the manuscript substantially.

Abreu JM (1972) Flutuações de populações de coleópteros nocivos ao cacaueiro no Espírito Santo, Brasil. Revista Theobroma 2: 45-55.

Altieri MA (1987) The scientific basis of alternative agriculture. Westview Press, Boulder.

Andow DA (1990) Population dynamics of an insect herbivore in simple and diverse habitats. Ecology 71: 1006-17.

Augspurger C (1985) A cue for synchronous flowering. In: Leigh E, Rand A, Windsor D (eds) The ecology of a tropical forest: seasonal rhythms and long-term changes. Smithsonian Institution, Washington, pp 133-150.

Azevedo CO, Santos HS (2000) Perfil da fauna de himenópteros parasitóides (Insecta, Hymenoptera) em uma área de Mata Atlântica da Reserva Biológica de Duas Bocas, Cariacica, ES, Brasil. Boletim do Museu de Biologia Mello Leitão 11/12: 117-126.

Baldi, A. (2003) Using higher taxa as surrogates of species richness: a study based on 3700 Coleoptera, Diptera, and Acari species in Central-Hungarian reserves. Basic and Applied Ecology 4: 589-593.

Barone JA (1998) Host-specificity of folivorous insects in a moist tropical forest. Journal of Animal Ecology 67: 400-409.

Basset Y, Novotny V (1999) Species richness of insect herbivore communities on Ficus in Papua New Guinea. Biological Journal of the Linnean Society 67: 477-499

Basset Y, Novotny V, Miller S, Kitching R (2003) Arthropods of tropical forests: spatio-temporal dynamics and resource use in the canopy. Cambridge University, Cambridge.

Basset Y, Samuelson GA, Allison A, Miller SE (1996) How many species of host-specific insects feed on a species of tropical tree? Biological Journal of the Linnean Society 59: 201-216

Beach JP, Williams L, Hendrix DL, Price LD (2003) Different food sources affect the gustatory response of Anaphes iole, an egg parasitoid of Lygus spp. Journal of Chemical Ecology 29: 1203-1222.

Begon M, Harper JL, Townsend CR (1996) Ecology: individuals, populations and communities. 3rd ed. Blackwell Science, Oxford.

Bell SS, McCoy E D, Mushinsky HR (1991) Habitat structure: the physical arrangement of objects in space. Chapman and Hall, London.

Benton PF (1984) Abundância estacional dos coleópteros fitófagos do cacaueiro do sul da Bahia e Espírito Santo. Revista Theobroma 14: 85-102.

Brehm G, Homeier J, Fiedler K (2003) Beta diversity of geometrid moths (Lepidoptera: Geometridae) in an Andean montane rainforest. Diversity and Distributions 9: 351-366.

Buckley YM., Briese DT, Rees M (2003) Demography and management of the invasive plant species Hypericum perforatum. I. Using multi-level mixed-effects models for characterizing growth, survival and fecundity in a long-term data set. Journal of Applied Ecology 40: 481-493.

Cabeza M, Moilanen A (2001) Design of reserve networks and the persistence of biodiversity. Trends in Ecology & Evolution 16(5): 242-248.

CEPLAC (1980) Contribuições da pesquisa para atualização dos pacotes tecnológicos recomendados para a região cacaueira. Comissão Executiva do Plano da Lavoura Cacaueira, Ilhéus.

Chesson P (2000) Mechanisms of maintenance of species diversity. Annual Review of Ecology and Systematics 31: 343-366.

Coimbra-Filho AF, Câmara IG (1996) Os limites originais do bioma Mata Atlântica na Região Nordeste do Brasil. Fundação Brasileira para a Conservação da Natureza, Salvador.

Crawley MJ (1993) GLIM for ecologists. Blackwell Scientific Publications, Oxford.

Crawley MJ (2002) Statistical computing: an introduction to data analysis using S-Plus. John Wiley & Sons, Chichester.

Didham R, Springate N (2003) Determinants of temporal variation in community structure. In: Basset Y, Novotny V, Miller S, Kitching R (eds) Arthropods of tropical forests: spatio-temporal dynamics and resource use in the canopy. Cambridge University, Cambridge, pp 28-39.

Duelli P, Obrist MK (2003) Regional biodiversity in an agricultural landscape: the contribution of seminatural habitat islands. Basic and Applied Ecology 4: 129-138.

Dyer LA, Stireman JO (2003) Community-wide trophic cascades and other indirect interactions in an agricultural community. Basic and Applied Ecology 4: 423-432.

Erwin T (1982) Tropical forests: their richness in Coleoptera and other arthropod species. Coleopterists Bulletin 36: 74-75.

Fernandes G, Price PW (1992) The adaptive significance of insect gall distribution: survivorship of species in xeric and mesic habitats. Oecologia 90: 14-20.

Fernandes G, Price PW (1991) Comparison of tropical and temperate galling species richness: the roles of environmental harshness and plant environmental status. In: Price P, Lewinsohn T, Fernandes G, Benson W (eds) Plant-animal interactions: evolutionary ecology in tropical and temperate regions. John Wiley & Sons, New York, pp 91-115.

Ferro D (1987) Insect pest outbreaks in agroecosystems. In: Barbosa P, Schultz J (eds) Insect outbreaks. Academic Press, San Diego, pp 195-215.

Garcia JJS, Silveira-Neto S (1980) Estudo faunístico de coleópteros e hemípteros associados ao cacaueiro no Estado do Pará. Revista Theobroma 10: 15-23.

Gentry, G (2003) Multiple parasitoid visitors to the extrafloral nectaries of Solanum adherens. Is S. adherens an insectary plant? Basic and Applied Ecology 4: 405-411.

Gibson GAP, Huber JT, Woolley JB (eds) (1997) Annotated keys to the genera of nearctic Chalcidoidea (Hymenoptera). NRC Research, Ottawa.

Godfray HCJ (1993) Parasitoids: behavioral and evolutionary ecology. Princeton University, Princeton.

Goulet H, Huber JT (eds) (1993) Hymenoptera of the World: an identification guide to families. Agriculture Canada Research Branch, Ottawa.

Gurr GM, Wratten SD, Luna JM (2003) Multi-function agricultural biodiversity: pest management and other benefits. Basic and Applied Ecology 4: 107-116.

Hawkins BA (1990) Global patterns of parasitoid assemblage size. Journal of Animal Ecology 59: 57-72.

Hawkins BA, Mills JL (1996) Variability in parasitoid community structure. Journal of Animal Ecology 65: 501-516.

Humphries, CJ, Williams PH, Vanewright RI (1995) Measuring biodiversity value for conservation. Annual Review of Ecology and Systematics 26: 93-111.

Ihaka R, Gentleman R (1996) A language for data analysis and graphics. Journal of Computational and Graphical Statistics 5: 299-314.

Itioka T, Kato M, Kaliang H, Merdek M, Nagamitsu T, Sakai S, Mohamad SU, Yamane S, Hamid AA, Inoue T (2003) Insect responses to general flowering in Sarawak. In: Basset Y, Novotny V, Miller S, Kitching R (eds) Arthropods of tropical forests: spatio-temporal dynamics and resource use in the canopy. Cambridge University, Cambridge, pp 126-134.

Janzen DH (1975) Ecology of plants in the tropics. Edward Arnold, London.

Kirmse S, Adis J, Morawetz W (2003) Flowering events and beetle diversity in Venezuela. In: Basset Y, Novotny V, Miller S, Kitching R (eds) Arthropods of tropical forests: spatio-temporal dynamics and resource use in the canopy. Cambridge University, Cambridge, pp 256-268.

Klein AM, Steffan-Dewenter I, Tscharntke T (2002) Predator-prey ratios on cocoa along a land-use gradient in Indonesia. Biodiversity and Conservation 11: 683-693.

Kruess A (1994) Habitat fragmentation, species loss, and biological-control. Science 264: 1581-1584.

Larcher W (2000) Ecofisiologia vegetal. Rima, São Carlos.

Lawton JH (1983) Plant architecture and the diversity of phytophagous insects. Annual Review of Entomology 28: 23-39.

Lill JT, Marquis RJ, Ricklefs RE (2002) Host plants influence parasitism of forest caterpillars. Nature 417: 170-173.

Mahar DJ (1989) Government policies and deforestation in Brazil's Amazon region. The World Bank, Washington.

Marino PC, Landis DA (1996) Effect of landscape structure on parasitoid diversity and parasitism in agroecosystems. Ecological Applications 6: 276-284.

Matlock RB, de la Cruz R (2002) An inventory of parasitic Hymenoptera in banana plantations under two pesticide regimes. Agriculture Ecosystems & Environment 93: 147-164.

Medeiros MA, Fowler HG, Bueno CO (1995) Ant (Hym., Formicidae) mosaic stability in Bahian cacao plantations: implications for management. Journal of Applied Entomology 119: 411-414.

Menalled FD, Marino PC, Gage SH, Landis DA (1999) Does agricultural landscape structure affect parasitism and parasitoid diversity? Ecological Applications 9: 634-641.

Myers N, Mittermeyer RA, Mittermeyer CG, Fonseca GAB, Kent J (2000) Biodiversity hotspots for conservation priorities. Nature 403: 853-858.

Nair PR (1993). An Introduction to Agroforestry. Kluwer Academic, Dordrecht.

Novotny V, Basset Y, Kitching R (2003) Herbivore assemblages and their food resources. In: Basset Y, Novotny V, Miller S, Kitching R (eds) Arthropods of tropical forests: spatio-temporal dynamics and resource use in the canopy. Cambridge University, Cambridge, pp 40-53.

Novotny V, Basset Y, Miller SE., Drozd P, Cizek L (2002) Host specialization of leaf-chewing insects in a New Guinea rainforest. Journal of Animal Ecology 71: 400-412.

Peeters, P. J., Read, J., Sanson, G. D. 2001. Variation in the guild composition of herbivorous insect assemblages among co-occurring plant species. Austral Ecology 26: 385-399.

Pinheiro JC, Bates DM (2000) Mixed-Effects Models in S and S-Plus. Springer, New York.

Quicke DLJ (1997) Parasitic Wasps. Chapman & Hall, New York.

Ribas CR, Schoereder JH, Pic M, Soares SM (2003) Tree heterogeneity, resource availability, and larger scale processes regulating arboreal ant species richness. Austral Ecology 28: 305-314.

Ricklefs RE, Schluter D (eds) (1993) Species diversity in ecological communities: historical and geographical perspectives. University of Chicago, Chicago.

Roland J, Taylor PD (1997) Insect parasitoid species respond to forest structure at different spatial scales. Nature 386: 710-713.

Rosand PC, Santana M, Zevallos AC (1987). Associations between cacao (Theobroma cacao) and shade trees in southern Bahia, Brazil. In: Beer JW, Fassbender HW, Heuveldop J (eds) Advances in agroforestry research. Centro Agronómico Tropical de Investigacion y enseñanza (CATIE) / Deutsche Gesellschaft für Technische Zusammenarbeit (GTZ), Turrialba, pp 137-154.

Russell EP (1989) Enemies hypothesis: A review of effect of vegetational diversity on predatory insects and parasitoids. Environmental Entomology 18: 590-599.

Sá DF, Almeida HA, Silva LF, Leão AC (1982) Fatores edafo-climáticos seletivos ao zoneamento da cacauicultura no Sudoeste da Bahia. Revista Theobroma 12: 169-187.

Sax, D. F., Gaines, S. D. 2003. Species diversity: from global decreases to local increases. Trends in Ecology & Evolution 18: 561-566.

Strong DR, Lawton JH, Southwood R (1984) Insects on plants: community patterns and mechanisms. Harvard University / Blackwell Scientific Publication, Cambridge.

Thies C, Tscharntke T (1999) Landscape Structure and Biological Control in Agroecosystems. Science 285: 893-895.

Thomas WM, Carvalo W, Amorim AMV, Garrison AMA, Arbeláez J (1998) Plant endemism in two forests in Southern Bahia, Brazil. Biodiversity and Conservation 7: 33-322.

Thompson SN (1999) Nutrition and culture of entomophagous insects. Annual Review of Entomology 44: 561-592.

Tilman D, Pacala S (1993) The maintenance of species richness in plant communities. In: Ricklefs RE, Schluter D (eds) Species diversity in ecological communities: historical and geographical perspectives. University of Chicago, Chicago, pp 13-25.

Townes HA (1972) A light-weight Malaise trap. Entomological News 83: 239-247.

Vinha SG, Ramos TJS, Hori M (1976) Recursos Florestais. In: CEPLAC (ed) Diagnóstico sócio-econômico da região cacaueira. Comissão Executiva do Plano da Lavoura Cacaueira, Ilhéus, vol. 7.

Wackers FL (2001) A comparison of nectar- and honeydew sugars with respect to their utilization by the hymenopteran parasitoid Cotesia glomerata. Journal of Insect Physiology 47: 1077-1084.

Wagner T (2001) Seasonal changes in the canopy arthropod fauna in Rinorea beniensis in Budongo Forest, Uganda. Plant Ecology 153: 169-178.

Wolda H (1989) Seasonal cues in tropical organisms. Rainfall? Not necessarily! Oecologia 80: 437-442.

Wolda H (1992) Trends in abundance of tropical forest insects. Oecologia 89: 47-52.

Sperber, Nakayama, Valverde & Neves

Table 1. Locations and characteristics of the cacao agroforestry systems which were sampled.

Tree species richness

Farm name


Age (years)

Area (ha)


Bolandeira 3





Bolandeira 4





Cachoeira 1





Piruna 2





Puaia 4










São Roque 2





Bolandeira 1





Piruna 1





São Roque 1





Serra Boa





Bolandeira 2





Cachoeira 2





Puaia 2





Puaia 3







Puaia 1




Sperber, Nakayama, Valverde & Neves

Table 2. Number and percentage of Hymenoptera of the Parasitica series and the Chrysidoidea superfamily in the sampled cacao agroforestry systems.
















































































































< 0.01



















Sperber, Nakayama, Valverde & Neves

Sperber, Nakayama, Valverde & Neves

Sperber, Nakayama, Valverde & Neves

Fig. 1. Number of Hymenoptera Parasitica and Chrysidoidea families in cacao agroforestry systems with different shade tree diversity, in three seasons: Spring, Summer, and Winter. Left: parasitoid family number against shade tree species richness; right: parasitoid family number against shade tree density. Curves were based on parameters (Table 5) of the fitted minimum adequate linear mixed effect model (Table 4).
Fig. 2. Scatter-plot of shade tree species richness against tree density, in cacao agroforestry systems. Dashed line: fitted linear regression. Pearson’s product-moment correlation, r = -0.89, t = 13.04, d.f. = 46, p < 0.0001

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