Managing genetic variation in tropical trees: linking knowledge with action in agroforestry ecosystems for improved conservation and enhanced livelihoods

Tree species in agroforestry ecosystems contribute to the livelihoods of rural communities and play an important role in the conservation of biodiversity. Unless agroforestry landscapes are productive, however, farmers will not maintain or enhance the range and quality of tree species in them, and both income opportunities and biodiversity will be lost. Productivity depends on both tree species diversity and genetic (intra-specific) variation, but research on the latter has until recently not received the recognition it deserves. Worse, when knowledge on tree genetic variation in agroforestry systems has become available, it has not generally been linked in any systematic way with management, indicating a disjunction between research and field-level practice. In this essay, we attempt to bridge this gap by considering three questions: why is genetic diversity important in tree species? What is our current state of knowledge about intra-specific variation in trees in agroforestry systems? And, finally, what practical interventions are possible to support the conservation of this diversity in agricultural landscapes, while enhancing farmers’ livelihoods? A wide genetic base in agroforestry trees is essential to prevent inbreeding depression and allow adaptation to changing environmental conditions and to altering markets for tree products. Recent evidence shows, however, that many species are subject to poor germplasm collection practice, occur at low densities in farmland, and are found in highly aggregated distributions, all of which observations raise concerns about productivity and sustainability. A range of germplasm-access based interventions is necessary to improve current management, including the enhancement of community seed- and seedling-exchange networks, and the development of locally based tree domestication activities. Equally necessary, but more difficult to address, is the development of markets that support genetic diversity in tropical tree species; we discuss approaches by which this may be undertaken.     

Biodiversity conservation in cocoa production landscapes: an overview

Cocoa agroforests that retain a floristically diverse and structurally complex shade canopy have the potential to harbour significant levels of biodiversity, yet few studies have documented the plant and animal species occurring within these systems or within landscapes dominated by cocoa production. In this special issue, we bring together nine studies from Latin America, Africa and Asia that document the contribution of cocoa agroforestry systems to biodiversity conservation, and explore how the design, management and location of these systems within the broader landscape influence their value as habitats, resources and biological corridors. Tree diversity within the cocoa production systems is variable, depending on management, cultural differences, location and farm history, among other factors. Animal diversity is typically highest in those cocoa agroforests that have high plant diversity, structurally complex canopies, and abundant surrounding forest cover. In general, both plant and animal diversity within cocoa agroforests is greater than those of other agricultural land uses, but lower than in the original forest habitat. There are several emerging threats to biodiversity conservation within cocoa production landscapes, including the loss of remaining forest cover, the simplification of cocoa shade canopies and the conversion of cocoa agroforestry systems to other agricultural land uses with lower biodiversity value. To counter these threats and conserve biodiversity over the long-term, land management should focus on conserving native forest habitat within cocoa production landscapes, maintaining or restoring floristically diverse and structurally complex shade canopies within cocoa agroforests, and retaining other types of on-farm tree cover to enhance landscape connectivity and habitat availability.     

Relative contribution of agroforestry,rainforest and openland to local and regional bee diversity

Due to increasing human modification of tropical landscapes, the relative importance of natural habitats and agricultural systems has become a major conservation topic to counteract global species loss. We investigated the contribution of tropical primary forest, cacao agroforestry systems of varying management practices and openland to the temporal and spatial variation of diversity of native bee communities in the herb layer (Apidae, Hymenoptera) in Sulawesi (Indonesia). Local bee density and diversity were highest in openland, followed by agroforestry systems and were lowest in primary forests, revealing the importance of herbaceous food resources in the understorey. In contrast, highest regional bee richness was found in agroforestry systems, because of high community dissimilarity. Multidimensional scaling supported these findings with openland habitats showing more compactly clustered bee species communities than agroforestry habitats. In conclusion, the herb associated bee community profited from the opening of the landscape as a result of agricultural activities, while agroforestry systems increased bee species richness especially on a regional scale due to high management diversity.     

From Forest to Farmland: Species Richness Patterns of Trees and Understorey Plants along a Gradient of Forest Conversion in Southwestern Cameroon

Vegetation surveys were carried out at 24 sampling stations distributed over four land use types, namely near-primary forest, secondary forest, agroforestry systems and annual crop lands in the northeastern part of the Korup region, Cameroon, to assess the impact of forest conversion on trees and understorey plants. Tree species richness decreased significantly with increasing level of habitat modification, being highest and almost equal in secondary and near-primary forests. Understorey plant species richness was significantly higher in annual crop lands than in other land use types. The four land use types differed in tree and understorey plant species composition, the difference being smaller among natural forests. Tree and understorey plant density differed significantly between habitat types. Density was strongly correlated with species richness, both for trees and understorey plants. Five tree and 15 understorey plant species showed significant responses to habitat. A 90% average drop in tree basal area from forest to farmland was registered. Our findings support the view that agroforestry systems with natural shade trees can serve to protect many forest species, but that especially annual crop lands could be redesigned to improve biodiversity conservation in agricultural landscapes of tropical rainforest regions.     

Predator–prey ratios on cocoa along a land-use gradient in Indonesia

Tropical landscapes are dominated by agroecosystems, but the potential value of agroecosystems for the survival of species is often overlooked. In agroecosystems, species conservation is especially important when functional groups such as predators are affected. In Central Sulawesi, we sampled arthropods on cocoa in a gradient of land-use intensity from extensively used forest gardens to intensively used agroforestry systems. The abundance and diversity of all arthropods did not correlate with land-use intensity, so human impact was not followed by high species losses. However, the number of species and abundance of the phytophagous arthropods increased and that of the entomophagous arthropods decreased with land-use intensity. The reduced predator–prey ratio in intensified systems can be related to their reduced species richness of shade trees and the changed microclimate (increased temperature, decreased humidity and canopy cover). In conclusion, transformation of traditional into intensified agroforestry systems had a great impact on arthropod community structure on cocoa. Since predator–prey ratios decreased with increasing land-use intensity, local farmers should have least pest problems in the traditionally diversified agroforestry systems.     

A conceptual framework and experimental design for analysing the relationship between biodiversity and ecosystem functioning (BEF) in agroforestry systems

There is compelling evidence for positive effects of plant diversity on the functioning of forests and agroecosystems. This information is increasingly used to optimize production systems that provide a wide range of ecosystem services. While agroforestry is actively promoted for the sustainable intensification of agriculture and restoration of degraded landscapes, there is a paucity of knowledge on Biodiversity Ecosystem Functioning (BEF) relationships in agroforestry systems. Since BEF-relationships in agroforestry might be shaped by combinations of different life-forms (e.g. trees, shrubs, herbs) and their interactions, experiences from grassland and forest experiments cannot be readily transferred to agroforestry. This highlights the need for a new type of experiments in agroforestry to advance our understanding of the role of biodiversity for the functioning of these systems. Therefore, our aim was to develop a conceptual framework for analysing BEF-relationships in agroforestry systems and to present an exemplary design for this purpose, which we placed in a (sub)tropical context. Based on designs used in tree diversity experiments, we suggest four major design principles: 1) a trait-based approach for selecting tree and crop species, 2) the integration of trees and crops along a gradient of functional diversity, 3) maintaining constant density across different combinations of life-forms in agroforests through the concept of “growing-patch-density”, and 4) disentangling a priori the effects of species diversity on ecosystem functioning from those of structural and functional diversity, defined here as the variation in structural attributes such as plant dimensions and in plant functional traits, respectively. Our conceptual design and the embedded principles offer a promising avenue to identify important drivers of specific BEF-relationships and to quantify management influences on these. This design can support new research projects that aim at improving ecosystem functioning of agroforestry with the view of optimizing the provision of ecosystem services and facilitation of ecosystem restoration.     

Dung Beetle and Terrestrial Mammal Diversity in Forests, Indigenous Agroforestry Systems and Plantain Monocultures in Talamanca, Costa Rica

In order to explore the importance of indigenous agroforestry systems for biodiversity conservation, we compared the abundance, species richness and diversity of dung beetles and terrestrial mammals across a gradient of different land use types from agricultural monocultures (plantains) to agroforestry systems (cocoa and banana) and forests in the BriBri and Cabécar indigenous reserves in Talamanca, Costa Rica. A total of 132,460 dung beetles of 52 species and 913 tracks of 27 terrestrial mammal species were registered. Dung beetle species richness and diversity were greatest in the forests, intermediate in the agroforestry systems and lowest in the plantain monocultures, while dung beetle abundance was greatest in the plantain monocultures. The number of mammal tracks per plot was significantly higher in forests than in plantain monocultures, whereas mammal species richness was higher in forests than in either cocoa agroforestry systems or plantain monocultures. Species composition of both terrestrial mammals and dung beetles also varied across the different land use types. Our study indicates that indigenous cocoa and banana agroforestry systems maintain an intermediate level of biodiversity (which is less than that of the original forest but significantly greater than that of plantain monocultures) and provide suitable habitat for a number of forest-dependent species. Although the agroforestry systems appear to serve as favorable habitats for many terrestrial mammal species, their potential positive contribution to mammal conservation is being offset by heavy hunting pressure in the reserves. As in other agricultural landscapes, the conservation of biodiversity in Talamanca will depend not only on maintaining the existing forest patches and reducing the conversion of traditional agroforestry systems to monocultures, but also on reducing hunting pressure.     

Exploring the Ecological History of a Tropical Agroforestry Landscape Using Fossil Pollen and Charcoal Analysis from Four Sites in Western Ghats,India

Contrary to expectations, some human-modified landscapes are considered to sustain both human activities and biodiversity over the long-term. Agroforestry systems are among these landscapes where crops are planted under native shade trees. In this context, ancient agroforestry systems can provide insight into how farmers managed the landscape over time. Such insight can help to quantify the extent to which tropical forests (especially habitat-specialist trees) are responding to local and landscape-level management. Here, we extracted fossil pollen (indicator of past vegetation changes) and macroscopic charcoal (indicator of biomass burning) from four forest hollows’ sedimentary sequences in an ancient agroforestry system in Western Ghats, India. We used a mixed-modelling approach and a principal components analysis (PCA) to determine past trajectories of forest change and species composition dynamics for the last 900 years. In addition, we reconstructed the long-term forest canopy dynamics and examined the persistence of habitat-specialist trees over time. Our results show that the four sites diverged to a surprising degree in both taxa composition and dynamics. However, despite these differences, forest has persisted over 900 years under agricultural activities within agroforestry systems. This long-term analysis highlights the importance of different land-use legacies as a framework to increase the effectiveness of management across tropical agricultural lands.     

Agroforestry coffee soils increase the insect‐suppressive potential offered by entomopathogenic fungi over full‐sun soils: A case proposing a “bait survival technique”

Entomopathogenic fungi are important natural enemies of insects. However, there is little information on the insect‐suppressive potential of these fungi and possible effects of farming management on this. Meanwhile, changes in natural landscapes due to agricultural intensification have caused considerable biodiversity loss and consequent decay of ecosystem services. However, the adoption of practices such as agroforestry in agroecosystems can foster abiotic and biotic conditions that conserve biodiversity, consequently restoring the provision of ecosystems services. Here, we assessed the effect of management systems (agroforestry or full‐sun) on the pest‐suppressive potential of entomopathogenic fungi in Brazilian coffee plantations. We used the insect bait method coupled with survival analyses to assess the speed of kill by entomopathogenic fungi and their presence in soil samples from both farming systems. We found that insects exposed to agroforestry soils died more quickly than insects exposed to full‐sun soils. Of the fungi isolated from the bait insects, Metarhizium was found most frequently, followed by Beauveria. Meanwhile, Fusarium was frequently isolated as primary or secondary infections. We propose that the differential survival of insects is indicative of a greater suppressive potential by entomopathogenic fungi in agroforestry, and that this could be promoted by the diversified landscape, microclimatic stability, and reduced soil disturbance in agroforestry systems. Furthermore, our results provide a useful demonstration of the potential use of the insect bait method to investigate pest‐suppressive potential through bait insect mortality, and we term this the “bait survival technique.”     

Seasonal contrasts in the response of coffee ants to agroforestry shade-tree management

In many tropical landscapes, agroforestry systems are the last forested ecosystems, providing shade, having higher humidity, mitigating potential droughts, and possessing more species than any other crop system. Here, we tested the hypothesis that higher levels of shade and associated humidity in agroforestry enhance coffee ant richness more during the dry than rainy season, comparing ant richness in 22 plots of three coffee agroforestry types in coastal Ecuador: simple-shade agroforests (intensively managed with low tree species diversity), complex-shade agroforests (extensively managed with intermediate tree species diversity) and abandoned coffee agroforests (abandoned for 10-15 yr and resembling secondary forests). Seasonality affected responses of ant richness but not composition to agroforestry management, in that most species were observed in abandoned coffee agroforests in the dry season. In the rainy season, however, most species were found in simple-shade agroforests, and complex agroforestry being intermediate. Foraging coffee ants species composition did not change differently according to agroforestry type and season. Results show that shade appears to be most important in the dry seasons, while a mosaic of different land-use types may provide adequate environmental conditions to ant species, maximizing landscape-wide richness throughout the year.     

Interactions between changes in land cover and potential of ecosystem services in Lithuania at temporal and spatial scale

The growing interest in ecosystem services is mainly related to land use changes. The aim of the study is to analyse spatial-temporal changes in the capacity to supply of ES in Lithuania based on land use changes in 1990–2018. The results show some balance between loss and gains of ecosystem services capacity due to land use changes. Decrease in heterogenous agricultural areas had negative impact on provision of ecosystem integrity and services. Considerable increase in scrubland and herbaceous vegetation areas significantly increased the ecosystem service potential. The conversion of former agricultural land to less intensively managed ecosystems enhance the potential of valuable habitats for biodiversity and ecosystem services associated with natural grasslands, moors and heathland, transitional woodland shrubs. The urbanization process along with increase in urban fabric areas had little effect on ESs potential since artificial vegetated areas had compensated the loss of ESs due to increased areas of urbanized ecosystems. Despite the area of open spaces slightly increased, this led to decrease of provision of ESs. Temporal changes in overall ESs capacity indicated an increase in Lithuania over the last two decades. Given the observed dynamic context of land cover, the structure of ecosystem services may face potential threats from land use change due to urban development and agricultural activities.     

The conservation value of cacao agroforestry for bird functional diversity in tropical agricultural landscapes

Cacao agroforestry have been considered as biodiversity‐friendly farming practices by maintaining habitats for a high diversity of species in tropical landscapes. However, little information is available to evaluate whether this agrosystem can maintain functional diversity, given that agricultural changes can affect the functional components, but not the taxonomic one (e.g., species richness). Thus, considering functional traits improve the understanding of the agricultural impacts on biodiversity. Here, we measured functional diversity (functional richness‐FD, functional evenness‐FEve, and functional divergence‐Rao) and taxonomic diversity (species richness and Simpson index) to evaluate changes of bird diversity in cacao agroforestry in comparison with nearby mature forests (old‐growth forests) in the Brazilian Atlantic Forest. We used data from two landscapes with constraining areas of mature forest (49% Una and 4.8% Ilhéus) and cacao agroforestry cover (6% and 82%, respectively). To remove any bias of species richness and to evaluate assembly processes (functional overdispersion or clustering), all functional indices were adjusted using null models. Our analyses considered the entire community, as well as separately for forest specialists, habitat generalists, and birds that contribute to seed dispersal (frugivores/granivores) or invertebrate removal (insectivores). Our findings showed that small cacao agroforestry in the forested landscape sustains functional diversity (FD and FEve) as diverse as nearby forests when considering the entire community, forest specialist, and habitat generalists. However, we observed declines for frugivores/granivores and insectivores (FD and Rao). These responses of bird communities differed from those observed by taxonomic diversity, suggesting that even species‐rich communities in agroforestry may capture lower functional diversity. Furthermore, communities in both landscapes showed either functional clustering or neutral processes as the main driver of functional assembly. Functional clustering may indicate that local conditions and resources were changed or lost, while neutral assemblies may reveal high functional redundancy at the landscape scale. In Ilhéus, the neutral assembly predominance suggests an effect of functional homogenization between habitats. Thus, the conservation value of cacao agroforestry to harbor species‐rich communities and ecosystem functions relies on smallholder production with reduced farm management in a forested landscape. Finally, we emphasize that seed dispersers and insectivores should be the priority conservation targets in cacao systems.     

Use of agroecosystem matrix habitats by mammalian carnivores (Carnivora): a global‐scale analysis

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Large climate mitigation potential from adding trees to agricultural lands

While improved management of agricultural landscapes is promoted as a promising natural climate solution, available estimates of the mitigation potential are based on coarse assessments of both agricultural extent and aboveground carbon density. Here we combine 30 meter resolution global maps of aboveground woody carbon, tree cover, and cropland extent, as well as a 1 km resolution map of global pasture land, to estimate the current and potential carbon storage of trees in nonforested portions of agricultural lands. We find that global croplands currently store 3.07 Pg of carbon (C) in aboveground woody biomass (i.e., trees) and pasture lands account for an additional 3.86 Pg C across a combined 3.76 billion ha. We then estimate the climate mitigation potential of multiple scenarios of integration and avoided loss of trees in crop and pasture lands based on region‐specific biomass distributions. We evaluate our findings in the context of nationally determined contributions and find that the majority of potential carbon storage from integration and avoided loss of trees in crop and pasture lands is in countries that do not identify agroforestry as a climate mitigation technique.     

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What is the relevance of smallholders’ agroforestry systems for conserving tropical tree species and genetic diversity in circa situm, in situ and ex situ settings? A review

Smallholders’ agroforests may be valuable for conserving tropical trees through three main mechanisms. First, trees planted and/or retained by farmers in agricultural landscapes where wild stands were once found may be circa situm reservoirs of biodiversity. Second, farmland trees may support conservation in situ by providing an alternative source of product to reduce extraction from forest, and by acting as ‘corridors’ or ‘stepping stones’ that connect fragmented wild stands. Third, the additional value that planting assigns to trees may result in greater interest in including them in seed collections, field trials and field ‘genebanks’ that support ex situ conservation. Here, we critically review the evidence for these mechanisms, and highlight areas for research and for intervention so that agroforestry practices can better support conservation in each setting, with an emphasis on often neglected genetic-level considerations. Based on current global challenges to diversity, conservation will need to rely increasingly on a smallholder-farm circa situm approach, but concerns on long-term effectiveness need to be properly quantified and addressed. Connectivity between widely dispersed, low density trees in agricultural landscapes is an important factor determining the success of the circa situm approach, while improving farmers’ access to a diversity of tree germplasm that they are interested in planting is required. The circumstances in which agroforestry plantings can support in situ conservation need to be better defined, and research on the stability of active tree seed collections (how long are species and populations retained in them?) as ex situ reservoirs of biodiversity is needed.     

Agroforestry: a refuge for tropical biodiversity?

As rates of deforestation continue to rise in many parts of the tropics, the international conservation community is faced with the challenge of finding approaches which can reduce deforestation and provide rural livelihoods in addition to conserving biodiversity. Much of modern-day conservation is motivated by a desire to conserve 'pristine nature' in protected areas, while there is growing recognition of the long-term human involvement in forest dynamics and of the importance of conservation outside protected areas. Agroforestry -- intentional management of shade trees with agricultural crops -- has the potential for providing habitats outside formally protected land, connecting nature reserves and alleviating resource-use pressure on conservation areas. Here we examine the role of agroforestry systems in maintaining species diversity and conclude that these systems can play an important role in biodiversity conservation in human-dominated landscapes.     

Ecological outcomes of agroforests and restoration 15 years after planting

Large‐scale forest restoration relies on approaches that are cost‐effective and economically attractive to farmers, and in this context agroforestry systems may be a valuable option. Here, we compared ecological outcomes among (1) 12–15‐year‐old coffee agroforests established with several native shade trees, (2) 12–15‐year‐old high‐diversity restoration plantations, and (3) reference old‐growth forests, within a landscape restoration project in the Pontal do Paranapanema region, in the Atlantic Forest of southeastern Brazil. We compared the aboveground biomass, canopy cover, and abundance, richness, and composition of trees, and the regenerating saplings in the three forest types. In addition, we investigated the landscape drivers of natural regeneration in the restoration plantations and coffee agroforests. Reference forests had a higher abundance of trees and regenerating saplings, but had similar levels of species richness compared to coffee agroforests. High‐diversity agroforests and restoration plantations did not differ in tree abundance. However, compared to restoration plantations, agroforests showed higher abundance and species richness of regenerating saplings, a higher proportion of animal‐dispersed species, and higher canopy cover. The abundance of regenerating saplings declined with increasing density of coffee plants, thus indicating a potential trade‐off between productivity and ecological benefits. High‐diversity coffee agroforests provide a cost‐effective and ecologically viable alternative to high‐diversity native tree plantations for large‐scale forest restoration within agricultural landscapes managed by local communities, and should be included as part of the portfolio of reforestation options used to promote the global agenda on forest and landscape restoration.     

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