Benefits of biotic pollination for non-timber forest products and cultivated plants

Biodiversity supplies multiple goods and services to society and is critical for the support of livelihoods across the globe. Many indigenous people depend upon non-timber forest products (NTFP) and crops for a range of goods including food, medicine, ﬁ bre and construction materials. However, the dependency of these products on biotic pollination services is poorly understood. We used the biologically and culturally diverse Nilgiri Biosphere Reserve in India to characterise the types of NTFP and crop products of 213 plant species and asses their degree of dependency on animal pollination. We found that 80 per cent of all species bene ﬁ ted from animal pollination in their reproduction, and that 62 per cent of crop products and 40 per cent of NTFP bene ﬁ ted from biotic pollination in their production. Further we identi ﬁ ed the likely pollinating taxa documented as responsible for the production of these products, mainly bees and other insects. A lower proportion of indigenous plant products (39 per cent) bene ﬁ ted from biotic pollination than products from introduced plants (61 per cent). We conclude that pollinators play an important role in the livelihoods of people in this region.


INTRODUCTION
Non-timber forest products (NTFP) are defi ned here as goods other than timber and fi rewood, of plant origin and derived from forests (De Beer & McDermott 1996).Crops and NTFP produce may be used directly, such as food, fi bre, medicine and construction materials or processed further to yield oils, soap substitutes and other commodities, and these products may be traded for money or bartered for other goods and services (De Beer & McDermott 1996, Muraleedharan et al. 1997).The plant parts used are diverse and include, fruits, seeds, nuts, leaves, bark, roots, stems, gums and resins (Durst et al. 1994, Lopez & Shanley 2004).
Human populations have harvested NTFP for thousands of years, for subsistence and trade (Ticktin 2004).Recent meta-enhancing fruit / seed quantity / quality, enhancing population viability and / or persistence, or by greater genetic diversity through outbreeding.Products from crops and NTFP may benefi t from animal pollination in their production (e.g., fruits, seeds, pods) or the plant species itself may benefi t from animal pollination in reproduction, even though the product itself may not result directly from pollination services (e.g., bark, roots, stems, etc.).Approximately 75 per cent of the global crops that are used directly as human food depend, at least in part, on animal-mediated pollination (Klein et al. 2007); and the majority of wild plants also require biotic pollination (Allen-Wardell et al. 1998, Kearns et al. 1998).In a study of tropical monsoon forests in Southeast Asia , Kato et al. 2008, found that 51 per cent (68 / 134) species were reported to be pollinated by bees.Despite the recognition of the general importance of animal pollination for crops and NTFP production, there is little systematic documentation of the proportion of crops and NTFP benefi ting from the pollinators and the identity of the pollinators themselves (Ahmed et al. 2005, Klein et al. 2007).
The most important pollinators around the world are bees, but other insects (fl ies, butterfl ies, beetles, etc.), bats and birds also make signifi cant contributions to biotic pollination (Buchman & Nabhan 1996).These pollinators provide an essential ecosystem service by contributing to human nutrition and welfare, however, the extent of this service is poorly understood.It is estimated that globally, pollination services to cultivated crops are worth €153 billion per annum, yet we have no similar estimate of the contribution to non-cultivated plants from which NTFP are derived (Gallia et al. 2009).Given the central role of pollinators in supporting livelihoods, and the fact that in many places around the world pollinators are under increasing threat from global change (Biesmeijer et al. 2006, Natural Research Council 2006), it is essential to understand and document the role of pollinators as a basis to conserve this component of biodiversity and ensure its continued contribution to indigenous livelihoods (Ahmed et al. 2005).
Ensuring linkages between conservation and the livelihoods of forest-dependent people and the biodiversity components they utilise, necessitates a good understanding of the natural resources.This is of special importance in regions like the Nilgiri Biosphere Reserve (NBR) in South India, which supports exceptional levels of both biological and cultural diversity.The NBR is home to more than 14 different Adivasi communities who harvest and depend on a wide variety of NTFP for subsistence and commercial use, and many of them also practise subsistence agriculture (Keystone 2007).As logging and hunting are prohibited within the NBR, NTFP and crops are the most important natural resources used in this area.
As a fi rst step towards better understanding the linkages between biodiversity, NTFP and the crops, we have used the NBR in India as a model system to explore the role of pollinators in relation to crops and NTFP.We aim to characterise the proportion of crops and NTFP which benefi t from biotic pollination, identify their probable pollinators and describe the plant parts and use of the products.Specifi cally we test the hypotheses: (1) cultivated crop products benefi t more from biotic pollination than NTFPs, as has been found in other studies (Klein et al. 2007;Kato et al. 2008); (2) introduced crops and NTFPs benefi t more from pollinators than indigenous plants, as reported elsewhere (James and Pitts-Singer 2008); (3) bees are the most important pollinator taxa responsible for crop and NTFP pollination in NBR, as they are in other regions of the tropics (Roubik 1995).

MATERIALS AND METHODS
The Nilgiri Biosphere Reserve (NBR) lies between 10° 45'N to 12° N and 76° E to 77° 15' E with a total area of 5,520 km 2 , spread across the three southern states of Karnataka, Kerala and Tamil Nadu.Altitude within the NBR varies from 250 m to 2650 m, and presents a diversity of vegetation types, ranging from tropical evergreen to thorny scrub.At least four of the major rivers of South India originate from this region -the Bhavani, Moyar, Kabini and Chaliyar rivers.
A database for the NBR was compiled by Shiny Rehel using the species lists of crops and NTFP listed in K e ystone Foundation ( 2006), Keystone Foundation (2007), Manivasakam (2003) & Rajendran et al. (2008).For each species additional information was included for the type of product(s) used by local people, what the product(s) were used for, whether they were traded, whether production of the plant product benefi ted from biotic pollination, whether the plant species itself benefi ted from biotic pollination for reproduction, whether the species was indigenous to NBR or introduced, and the documented pollinators for the species.For the pollinators, we included both direct empirical studies demonstrating that visitors were the pollinators, and also those studies reporting that observed visitors were the possible pollinators; some caution was needed, as not all observed visitors were pollinators, but for our broad scale study we included the best available evidence at the time.Details of the categories used are summarised in Table 1, and the database is available as supplementary online material.Where information was not available for a particular species it was assigned as unknown.The database was analysed by summing counts and calculating percentages for different categories, and comparisons between counts for cultivated versus NTFP species and indigenous versus introduced species were tested using an χ 2 test in Minitab v15.

RESULTS
For the NBR, in our database, we identifi ed 74 cultivated species and 139 NTFP species.Overall 47.9 per cent of the plant products used by local people benefi ted from biotic pollination (62.2 per cent of the cultivated products and 40.3 per cent of the NTFP products); products from cultivated plants more often benefi ted from biotic pollination than products from NTFP (χ 2 = 32.51,d.f.= 2, P < 0.001; Figure 1a).Irrespective of whether the plant product benefi ted from insect pollination or not, 80.3 per cent of all the species were reported as being biotically pollinated (Figure 1b; 82.4 per cent of the cultivated species and 79.1 per cent of the NTFP species), but there was no signifi cant difference in the numbers of cultivated and NTFP species benefi ting from pollination (χ 2 = 5.21, d.f.= 2, P = 0.074).Considering only the fruit products, most cultivated plants (88.2 per cent) and NTFP (89.4 per cent) benefi ted from biotic pollination, with no evidence that the plant type and degree of benefi t were related (χ 2 = 0.02, d.f.= 1, P = 0.874).
In our study, among the plants, 128 were indigenous to the NBR and 85 were introduced.Most of the NTFP were indigenous to the area (117 / 139 species), while most of the Benefi ts of pollinators for NTFP and crops / 215

Benefit
No benefit Unknown

Figure 2 (a) The proportions of indigenous and introduced products benefi ted, at least in part, by biotic pollination; (b) the proportions of indigenous and introduced species benefi ted, at least in part, by biotic pollination
cultivated species were introduced (63 / 74 species); these two factors, plant type and origin, were strongly related (χ 2 = 96.73,d.f.= 1, P < 0.001).Among the indigenous plants, 39.1 per cent of the products and 79.7 per cent of the species benefi ted from biotic pollination, whereas, among the introduced plants 61.2 per cent of the products and 81.2 per cent of the species benefi ted from biotic pollination (Figure 2).On the whole, introduced plant products benefi ted more from pollinators than the indigenous products (χ 2 = 17.10, d.f.= 2, P < 0.001), while the indigenous and cultivated species benefi ted equally from pollinators (χ 2 = 0.09, d.f.= 2, P = 0.955).
The plant species which benefi ted from pollination utilised a wide range of pollinator taxa (Table 2).Cultivated plants and NTFP were most commonly pollinated by bees and other insects, but rarely by birds and bats.Honeybees (Apis spp.) and solitary bees were the most frequent bee pollinators for both cultivated crops and NTFP, although both taxa are more commonly reported for crops.The overall pollinator community for cultivated plants and NTFP were different (χ 2 = 26.62,d.f.= 2, P = 0.002).For those species where fruit products were used, most cultivated plants (79.5 per cent) and about half of the NTFP (53.1 per cent) were recorded as having bee pollinators and these two factors, plant type and frequency of bee pollination, were related (χ 2 = 6.47, d.f.= 1, P = 0.010).Indigenous and introduced plants were fairly similar in the spectrum of the pollinating taxa associated with them (χ 2 = 16.97,d.f.= 2, P = 0.049), again being dominated by bees and other insects, however, introduced plants appear to be more often associated with honeybees and solitary bees than indigenous plants.
The types of products collected or harvested from plants benefi ting from pollinators are diverse (Table 3) and included: fruits, seeds, nuts, pods, bark, shoots, stems, leaves, fl owers, gum or resin, bulbs, roots, tubers, or rhizomes and the whole plant.Fruits were the most commonly cultivated and harvested products (33 / 66), while fruits (46 / 122) and leaves (32 / 122) were the most commonly collected NTFP.Most pollinatorbenefi ting crops were used as food (Table 4: 56 / 61), whereas, NTFP yielded a wider array of use for products, the most common being food (45 / 109) and medicine (56 / 109).Nearly all cultivated products that benefi ted from biotic pollination were traded (52 / 61) while only about half of the NTFP were commonly traded (65 / 110).

DISCUSSION
This is the first study we know of, which attempts to systematically assess the level of benefi ts for both crops and non-timber forest products (NTFP) from biotic pollination, in an ecologically important area.Within the NBR we identifi ed 213 plant species important to the local people, a third of which were cultivated and two-thirds of which were NTFP.Both crops and NTFP had a signifi cant proportion of their products which benefi ted directly from pollinators, although crops (60 per cent) benefi ted more than NTFP (42 per cent).Even greater proportions of the species themselves benefi ted from biotic pollination (~80 per cent, even though the harvested products themselves did not rely directly on the pollinators as such).We can therefore conclude that the majority of products collected from the forests or those grown as crops in the NBR, greatly benefi t from the provision of pollinator services.Similarly a great proportion of the world's crops also depend, at least in part, on biotic pollination (e.g., Klein et al. 2007), although a greater proportion of our NTFP benefi ted from biotic pollination than the plant species assessed in the tropical monsoon forests in Southeast Asia (Kato et al. 2008).
The majority of NTFP in our study were indigenous to the NBR, while most of the cultivated species had been introduced.The cultivated plants had a greater association with honeybees, which were usually considered as generalist pollinators and can readily use novel fl oral resources (Itioka et al. 2001, Thomas et al. 2009).Honeybees may have played an important role in ensuring that newly introduced crop species were productive, and may continue to contribute in the same way if further species are brought to the NBR.Of the indigenous plants ~40 per cent of the products benefi ted from pollinators, whereas, more than 60 per cent of the crop products benefi ted from Benefi ts of pollinators for NTFP and crops / 217 pollination by animals.This suggested that more cultivated products would be sensitive to the loss of pollination services rather than those obtained from the forests.
Insects were the most important taxa providing pollination services, and bees in particular were linked to the reproduction of many species.Honeybees and solitary bees were the most commonly documented pollinators, but stingless bees were also listed for several species.Many studies have observed bees to be key pollinators of a wide range of crops and wild fl owers and the continued availability of bees is therefore essential in the NBR to ensure that crop and NTFP products are produced and continue to contribute to the livelihoods in the NBR.
Pollinators contributed to the availability of a wide range of products which are important components of local diets and provide a variety of medicines.Bees and other insects are therefore contributing directly to the nutrition, health and livelihoods of many indigenous people of the NBR.Bees and other insects must therefore be considered as a crucial component of biodiversity, delivering essential services to society.
Given that in many regions of the world pollinator declines have been observed and land use changes and climate changes are impacting the NBR, it is essential to understand the conservation needs of bees in the NBR and to ensure that suitable forage and nesting resources are made available to them, now and in the future.Only by managing bee habitats can the provision of pollinator-related products be ensured and the livelihoods of indigenous people be protected.
Figure 1 (a) The proportions of cultivated and NTFP products benefi ted, at least in part, by biotic pollination; (b) the proportions of cultivated and NTFP species benefi ted, at least in part, by biotic pollination

Table 1 Categories in the database, defi nition of terms and resources used
Studies on Non Timber Forest Products in the Eastern region of The Biosphere Reserve.MSc thesis, Tamil Nadu Agricultural University.Keystone Foundation (2006) Forest plants of the Nilgiris, an illustrated fi eld guide.Studies on Non Timber Forest Products in the Eastern region of The Biosphere Reserve.MSc thesis, Tamil Nadu Agricultural University.
ProductThe part of the plant that is harvested or collected for human use or consumption: fruits, seeds, nuts, pods, bark, shoots or stems, leaves, fl owers, gum or resin, bulbs or roots or tubers, rhizomes and the whole plant.Manivasakam S. (2003) Studies on Non Timber Forest Products in the Eastern region of The Biosphere Reserve.MSc thesis, Tamil Nadu Agricultural University.Use The use of the product as: food, medicine, construction material, fi bre, fumigation, oil extraction, perfumes or soap.Manivasakam S. (2003) Studies on Non Timber Forest Products in the Eastern region of The Biosphere Reserve.MSc thesis, Tamil Nadu Agricultural University.