Tree species richness and density affect parasitoid diversity in cacao agroforestry

Abstract

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 1 ha 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 to 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.

Zusammenfassung

In Brasilien wird Kakao meist unter Schattenpflanzen angepflanzt. Die Diversität der Schattenbäume variiert von monospezifischen bis zu äußerst diversen Kronendächern, die charakteristisch für ursprüngliche atlantische Wälder sind. Diese Studie bewertet die Beziehung zwischen dem Familienreichtum der Hymenoptera-Parasitica sowie Chrysidoidea und der Baumartenzahl und -dichte, der Artenzahl des krautigen Unterwuchses sowie der Fläche und dem Alter des Kakao-Waldfeldbausystems. In 16 Kakao-Waldfeldbausystemen mit einer Variation der Kronendachdiversität von einer bis 22 Arten pro Hektar nahmen wir in drei Jahreszeiten Proben: Sommer (März), Winter (August) und Frühjahr (November). Die Parasitoide wurden unter Verwendung von acht Malaise-Townes-Fallen pro Probefläche gesammelt. Die Baumartenzahl und -dichte wurden innerhalb eines Hektars für jede Probefläche gezählt und die Artenzahl der krautigen Pflanzen wurde über acht 1 m²–Probeflächen innerhalb des Hektars berechnet. Die Zahl der Parasitoidenfamilien stieg mit der Baumartenzahl und -dichte im Frühjahr und Sommer, nahm im Winter jedoch ab. Weder die Artenzahl der krautigen Pflanzen noch die Größe oder das Areal des Systems beeinflusste die Zahl der Parasitoidenfamilien. Wir schlagen vor, dass die Zunahme der Parasitoidendiversität mit der Baumartenzahl und -dichte in den wärmeren Jahreszeiten die zunehmende Heterogenität und Verfügbarkeit der Ressourcen wiederspiegelt. Die Abnahme der Anzahl der Parasitoidenfamilien mit der Baumdichte im Winter könnte auf die lokale Verarmung der Ressourcen zurück zu führen sein, die zu einer Emigration der Parasitoide in benachbarte Waldreste führt. Diese Ergebnisse zeigen, dass eine höhere Diversität der Schattenbäume besonders in den warmen Jahreszeiten helfen wird, hohe Bestände von Parasitoiden und als Konsequenz höhere Bestände natürlicher Feinde der Kakaoschädlinge aufrecht zu erhalten. Diese Vorhersage wird von der Erfahrung der Kakaoproduzenten getragen. Das richtige Management der Schattenbaumdiversität wird eine wichtige Rolle bei der Aufrechterhaltung der Nachhaltigkeit des Kakao-Waldfeldbaus in den Tropen spielen und gleichzeitig hohe Biodiversitätswerte an diesen Orten aufrecht erhalten.

Introduction

Tropical landscapes are dominated by agroecosystems, but the potential value of such agroecosystems for the conservation of species is often overlooked (Klein, Steffan-Dewenter, & Tscharntke, 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 minimised 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, Harper, & Townsend, 1996). It is expected that diversity will increase with habitat heterogeneity (Strong, Lawton, & Southwood, 1984). Levels of parasitism may increase with landscape complexity (Kruess, 1994; Marino & Landis, 1996; Thies & Tscharntke, 1999; Menalled, Marino, Gage, & Landis, 1999), and ant species richness has been shown to increase with tree species richness (a surrogate for ‘habitat heterogeneity’) (Ribas, Schoereder, Pic, & Soares, 2003).

The highest priority areas for conservation have been designated ‘biodiversity hotspots’ (Myers, Mittermeyer, Mittermeyer, Fonseca, & Kent, 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 Espı́rito Santo (Thomas, Carvalho, Amorim, Garrison, & Arbeláez, 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, Ramos, & Hori, 1976; Rosand, Santana, & Zevallos, 1987). In Brazil most 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 (Janzen (1989), Wolda (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.