POLLINATORS POLLINATION AND FOOD PRODUCTION

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THE ASSESSMENT REPORT ON POLLINATORS, POLLINATION AND FOOD PRODUCTION the food chain and those generated by loss of flowers in response to herbicide use, are not considered in the risk assessments for insect resistant or herbicide tolerant GM crops (see section 2.2.2.2.1 for assessment of these effects). mellifera) but may nevertheless be important to agricultural pollination. Nature conservation responses are commonly applied to mitigate negative impacts of land use change, such as those identified in Chapter 2. 390 6. RESPONSES TO RISKS AND OPPORTUNITIES ASSOCIATED WITH POLLINATORS AND POLLINATION Possible changes in the toxicological model have been discussed and new approaches for ERA of GM plants have been proposed to match the Cartagena Protocol guidelines (Hilbeck et al., 2011; Sensi et al., 2011; Dana et al., 2012; Sanvido et al., 2012; Andow et al., 2013; Carstens et al., 2014), but there is no consensus about the exact scope of the assessment of GM plants on non-target species. Globally, there is a clear need for comprehensive, transparent, scientific guidelines for selecting the nontarget species to be evaluated, and among those, different species of pollinators need to be considered, not only Apis mellifera. The lack of these guidelines has led to different interpretations of the risk assessment process of GM plants among stakeholders (developer companies of GM crops, governmental regulators, and scientists) (Hilbeck et al., 2011; Andow et al., 2013; see Table 1 in Carstens et al., 2014). In conclusion, there are no international specific policies for risk assessment of GM plants on pollinators and no specific mitigation action to deal with the possible risks. The Cartagena Protocol does not make a clear reference to pollinators, but they are in the legislation of many countries within the scope of non-target organisms, along with other beneficial species such as those used as biological control agents (Flint et al., 2012). Various species, among them Apis mellifera, quail and mouse have been used in the ERA of GM crops. Whether these are appropriate surrogate species for wild pollinators has been questioned for toxicological tests of synthetic pesticides (see section 6.4.2.1). 6.4.2.6.2 Knowledge responses In Brazil, a monitoring program may be required by CTNBio (National Biosafety Technical Commission, http://www. ctnbio.gov.br), based on the results of risk analysis and it is designed on a case by case basis. Until now, this committee has not required monitoring specifically for pollinators. In Europe, post-market environmental monitoring is required for all GM crops released in the environment (EFSA, 2011), but there are few specific guidelines for pollinators (Shindler et al., 2013; Dolek and Theissen, 2013). 6.4.3 Nature conservation Many pollinator species are known to be vulnerable or in decline (Chapter 3). This section examines nature conservation responses that are intended to or likely to support pollinators and pollination. The nature conservation focus means that the targets are wild pollinators rather than domesticated pollinators (e.g., the European honey bee Apis 6.4.3.1 Technical responses 6.4.3.1.1 Habitat management This area has the strongest knowledge base because it has been a focus for land management practitioners and ecological scientists. The evidence that loss of habitat has been a driver of pollinator decline is very strong (see section 2.1.1). Many studies have examined the response of pollinators to on-ground actions, which inform possibilities for the future. Possible actions range from the protection or maintenance of existing natural habitat to the creation of new habitat patches by ecological restoration. At a larger spatial scale there are also actions that relate to the planning of natural habitat networks and how they spatially relate to one another to ensure that pollinators can disperse and adapt to global change, and that there is the best benefit flow into agricultural landscapes (crop pollination). There is evidence that forage resources commonly limit wild bee populations (Roulston and Goodell, 2011), which suggests that provision of additional appropriate forage resources could have significant population effects, but most studies do not assess these, instead focusing only on activity and frequency of pollinators. Planted forage resources might be focused on native plant species, and therefore be considered part of a nature conservation strategy, but because these plantings are generally integrated into agricultural practice, we have reviewed them in section 6.4.1.1 as agricultural responses. Forest management practices also influence bee communities, and planted forests have been shown to host significant bee communities in the early stages, but declining as a more closed forest environment develops (Taki et al., 2013). In New Jersey, USA, bees were more diverse and abundant when there was less closed forest in the surrounding landscape (Winfree et al., 2007). In tropical forest successional communities in Kenya, pollinator abundance and diversity actually increased across a gradient from natural forests to cultivated areas (Gikungu, 2006). Greater generalization was found among the bee communities in more mature forests, and more specialized and rare bee species were found in the earlier successional and more open habitats. In general, bees benefit from native plants and non-farmed habitats, but increasing cover of forests with closed canopies is less likely to favour rich bee communities. In addition to the potential to improve crop pollination (Garibaldi et al., 2014), restored patches might re-establish pollination networks of wild plant species and their
THE ASSESSMENT REPORT ON POLLINATORS, POLLINATION AND FOOD PRODUCTION pollinators (Menz et al., 2011). Some studies have shown that restored patches compare well with remnant patches in terms of diversity and identity of dominant pollinators (Forup et al., 2008; Williams, 2011; Hopwood, 2008) but the flower visitation rate for native plant species (Williams, 2011) and interactions with insect parasites (Henson et al., 2009) may take longer to recover. Bees often require specific nesting resources that can be enriched in a nature conservation strategy. For Osmia bicornis (formerly rufa), a stem-nesting bee in Europe, the provision of nesting material (reeds) in habitat patches in an agricultural landscape led to a local population increase (Steffan-Dewenter and Schiele, 2008) and many other trials establish that appropriate artificial nesting materials are used by a range of solitary bee species (Dicks et al., 2010). In contrast, the provision of boxes intended to host bumble bees has had highly variable outcomes (Dicks et al., 2010; Williams and Osborne, 2009) with average occupation of boxes low (Lye et al., 2011). Honey bees and stingless bees prefer to nest in large old trees, so protection of such trees is important. For example, the stingless bee species Melipona quadrifasciata was shown to nest selectively in the legally protected cerrado tree Caryocar brasilense (Atonini and Martins, 2003) (further discussion of nest sites for social bees is in 6.4.4.1.9 and 6.4.4.4.). 6.4.3.1.2 Landscape planning and connectivity Landscape planning for better pollinator outcomes has been the subject of theory and discussion (e.g., Menz et al., 2011; Viana et al., 2012) and a component of large-scale research projects, such as LEGATO (http://www.legato-project.net/). Although landscape planning has aided conservation of some species, little information is available to demonstrate the effectiveness of landscape planning strategies for pollinators and pollination specifically. Studies of existing fragmented landscapes have shown that in some biomes, the edge environments that predominate in small or linear patches tend to favour only certain pollinators (Girão et al., 2007; Lopes et al., 2009). An important theme in landscape planning is the maintenance of landscape connectivity for animal movement and gene flow. Several recent studies imply that the configuration of landscape features (the way they are arranged in the landscape) have only weak effects on bee populations or population persistence (Franzen and Nilsson, 2010; Kennedy et al., 2013, for example). However, in a review of studies examining landscape effects on the pollination, Hadley and Betts (2012) indicated that it had been very difficult to distinguish effects of landscape configuration (i.e., the shapes and position of habitat fragments) from the more general impact of habitat loss (i.e., direct effects of land clearing). Strategically-placed replanted vegetation might increase connectivity for ecological processes, which could benefit species in fragmented landscapes and support the ability for species to move in response to climate change. There is experimental and modelling evidence that pollen flow occurs between remnant and replanted vegetation (Cruz Neto et al., 2014) and that linear features linking patches of floral resource promote movement of bees and other pollinators through landscapes (Cranmer et al., 2012; Hodgson et al. 2012), thereby enhancing pollen transfer between plants in those patches (Townsend and Levey, 2005; Van Geert et al., 2010). These patterns provide some documentation of the benefits that habitat connectivity can provide. The role habitat connectivity has in maintaining pollinator populations remains unclear, but theory and observations for other taxa suggest that when the amount of natural habitat in the landscape declines below approximately 20% populations risk becoming isolated and connectivity may play an important role in their conservation (Hanski, 2015). Increased connectivity can be achieved by making the matrix (i.e., land between the habitat patches) more hospitable to dispersing organisms (Mendenhall et al. 2014), as well as by preserving or creating “stepping stones” and corridors of habitat connection. Climate change can impact populations in many ways, and in some cases species are expected to shift in distribution (i.e., populations move) generally poleward or to higher elevations, so that they remain within a climatically suitable environment (Chen et al., 2011). This kind of movement is only possible if suitable habitat for the species occurs at the new locations. Further, for migration to occur naturally, connectivity of habitat for the species in question may be important, keeping in mind that species vary greatly in their capacity to move long distance or cross inhospitable environments. With this in mind, adaption to climate change could include habitat improvements and increasing connectivity across landscapes, but currently there is limited evidence regarding effectiveness of this strategy. 6.4.3.1.3 Non-timber forest products Pollinators might also be important to the productivity and maintenance of non-timber forest products (NTFPs) (Rehel et al., 2009). For example, Brazil nut is primarily harvested from wild sources (Clay, 1997) and the production of nuts depends on pollination by large-bodied wild bees (Motta Maués 2002). Another interesting example showed that Yucatec Mayan people in Central America relocate honey bees into maturing stands of secondary forest, aged 10–25 years, to aid pollination and take advantage of the many flowering plant species for honey production (Diemont et al., 2011). While there are, no doubt, many other examples of NTFP’s that are animal pollinated (e.g. guarana, Krug et al., 2014; Euterpe palm, Venturieri, 2006), little is known of the extent to which sustainable yield depends on pollination rates or pollinator conservation and there is little scientific knowledge available regarding the effectiveness of 391 6. RESPONSES TO RISKS AND OPPORTUNITIES ASSOCIATED WITH POLLINATORS AND POLLINATION
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POLLINATORS POLLINATION AND FOOD PRODUCTION

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