6
Strategies for Maintaining Pollinators and Pollination Services

Although information on the status of most pollinators is incomplete, much can be done to maintain commercial and wild pollinator populations and to prevent future shortages of pollination services. The sustainability of the European or western honey bee (Apis mellifera), the principal managed pollinator in North America, could be buttressed through the development and adoption of parasite- and pathogen-resistant stocks of bees. Several developments could help the bee industry reach this goal: use of modern molecular techniques for identifying superior Apis stocks, effective methods for the preservation of honey bee germplasm, a suitable infrastructure for maintenance and use of resistant stocks, and adoption of practices by commercial queen producers and beekeepers that are consistent with these goals.

The development of mite- and pathogen-resistant stocks, however, is a long-term solution, one that will require extensive collaboration among researchers, extension personnel, and the queen-and-package industry. In the meantime, beekeepers require immediate relief. Other pest management strategies include programs that mitigate the effects of pesticide resistance in mite populations and cultural and other nonchemical techniques for disease management in commercial hives. Management techniques also must be implemented to reduce the impact of Africanized honey bees, which have begun to colonize areas of the United States critical to the beekeeping industry. The development of methods that support the commercialization of non-Apis pollinator species is also a high priority.

For wild, unmanaged pollinators, the most important goals involve conservation and restoration of habitat. Many pollinators can survive in small habitat patches and use the resources in natural areas, wildlands,



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Status of Pollinators in North America 6 Strategies for Maintaining Pollinators and Pollination Services Although information on the status of most pollinators is incomplete, much can be done to maintain commercial and wild pollinator populations and to prevent future shortages of pollination services. The sustainability of the European or western honey bee (Apis mellifera), the principal managed pollinator in North America, could be buttressed through the development and adoption of parasite- and pathogen-resistant stocks of bees. Several developments could help the bee industry reach this goal: use of modern molecular techniques for identifying superior Apis stocks, effective methods for the preservation of honey bee germplasm, a suitable infrastructure for maintenance and use of resistant stocks, and adoption of practices by commercial queen producers and beekeepers that are consistent with these goals. The development of mite- and pathogen-resistant stocks, however, is a long-term solution, one that will require extensive collaboration among researchers, extension personnel, and the queen-and-package industry. In the meantime, beekeepers require immediate relief. Other pest management strategies include programs that mitigate the effects of pesticide resistance in mite populations and cultural and other nonchemical techniques for disease management in commercial hives. Management techniques also must be implemented to reduce the impact of Africanized honey bees, which have begun to colonize areas of the United States critical to the beekeeping industry. The development of methods that support the commercialization of non-Apis pollinator species is also a high priority. For wild, unmanaged pollinators, the most important goals involve conservation and restoration of habitat. Many pollinators can survive in small habitat patches and use the resources in natural areas, wildlands,

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Status of Pollinators in North America and even human-dominated areas including appropriately managed farms, urban parks, and golf courses. Small changes could produce substantial benefits, but basic information on the resource requirements of a wider variety of pollinator species is needed to improve habitat management. Also, economic and policy incentives would encourage the stewards of a wide range of urban and rural areas to adopt pollinator-friendly practices and also to encourage information exchange and outreach. The most effective and sustainable route to stability in pollination services is to identify and implement practices that promote the availability of diverse commercial and wild pollinators. MAINTAINING COMMERCIAL POLLINATORS Apis mellifera: Problems and Solutions The beekeeping industry is at a critical juncture as it faces a suite of challenges that defy easy solution. The parasitic honey bee mite Varroa destructor, now ubiquitous in North America, is the single greatest threat to a sustainable supply of healthy and affordable honey bee colonies worldwide (DeJong, 1990; DeJong et al., 1982a, 1984). Major wintertime losses of honey bees in the United States every few years since 1993 (Burgett, 1994; Caron and Hubner, 2001; Finly et al., 1996; Lumkin, 2005) are almost certainly attributable to varroa mite infestation, which was exacerbated by the evolution of resistance to standard miticides. The tracheal mite Acarapis woodi also contributes to the periodic catastrophic winter losses, but reliable data on its prevalence in North America are not available. There are effective treatments for management of tracheal mites, including trachealmite-resistant stocks of bees (Chapter 3). Problems with tracheal mites, to the extent that they exist, can most likely be ameliorated by improved detection and control among beekeepers. Another serious challenge to the beekeeping industry is the Africanized honey bee, which has colonized several regions of the United States that are important to the commercial queen-and-package bee industry (northern California and the southeastern United States). The bees also migrate with beekeepers to hospitable wintering grounds. Because the Africanized bees have several traits that are undesirable for beekeeping (Chapter 3), it is imperative that the genotype be prevented from coming to predominance in the United States and Canada. The bees’ presence in the southeast—an important area of queen-and-package production for the rest of the United States and a primary wintering ground for beekeepers (Chapter 3)—makes this objective paramount.

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Status of Pollinators in North America Resistant Honey Bee Breeding A long-term solution to the problems of parasitic mites and honey bee pathogens is the development of resistant stocks of bees. Several traits associated with varroa mite resistance are heritable (that is, available for selection) (Camazine, 1986; Camazine and Morse, 1988; DeJong, 1996; Harbo, 1992, 1993; Harbo and Harris, 1999a,b; Harbo and Hoopingarner, 1995; Harbo et al., 1997; Moritz, 1985; Moritz and Hanel, 1984; Rinderer et al., 2003). Similarly, tracheal mite resistance is a heritable trait (Gary et al., 1990; Page and Gary, 1990). A varroa-resistant stock of honey bees was developed at the U.S. Department of Agriculture (USDA) Agricultural Research Service (ARS) honey bee research laboratory in Baton Rouge, Louisiana (Harbo and Harris, 1999a), and is available commercially as SMR (suppressing mite reproduction) or SMART stock. Related efforts also have focused on identifying honey bee populations with a long history of exposure to V. destructor as a potential source of resistant stock (Rinderer et al., 1999, 2001, 2003). ARS began to import bees from the Primorsky region in far-eastern Russia beginning in the early 1990s (Rinderer et al., 2005). The Russian bees were quarantined on an island off the coast of Louisiana, and they have been subject to further selection. The Russian bees exhibit a high degree of varroa mite resistance (Rinderer et al., 2003, and references therein), and they are now available commercially. Resistance to American foulbrood and other bee pathogens was shown to be heritable in the 1930s (Park, 1936). Although other traits contribute to foulbrood resistance (Spivak and Gilliam, 1998a,b), the principal mechanism is hygienic behavior (Rothenbuhler, 1964). Stocks that exhibit hygienic behavior have been developed at least three times since the 1930s (Park et al., 1937, 1939; Rothenbuhler, 1964; Spivak and Reuter, 2001). Hygienic behavior also could operate in mite resistance (Boecking et al., 2000; Harbo and Harris, 2005; Spivak and Rueter, 2001), and the University of Minnesota has developed hygienic stocks that are available commercially. Another challenge to the bee industry is the synthesis of results from federal and academic research into sustainable commercial queen-and-package operations. There are well-developed methods for quantifying resistance to mites and pathogens (Harbo and Harris, 1999a; Harbo et al., 1997; Spivak and Downey, 1998; Spivak and Gilliam, 1998a,b) and for breeding and maintaining resistant stocks (Harris et al., 2002; Page and Laidlaw, 1982a,b; Page et al., 1983, 1985). Perusal of trade journals reveals beekeepers’ interest in mite-resistant stocks of bees and the low availability of such stock: Several suppliers advertise Russian, SMR, or hygienic bee stocks, but there are no data on the number or quality of queens available. It is not clear why resistant stocks have not yet been widely adopted (Sheppard, 2006), but it is possible that the impediments include the difficulty of maintaining inbred

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Status of Pollinators in North America lines, the negative consequences of selecting one trait over others that are commercially important (Page and Laidlaw, 1992), and the time and effort involved in replacing queens (Laidlaw, 1992). Of particular importance is the lack of locally adapted stocks. Typically, although not universally, southern queen producers use stocks that perform well in the warmer south but that might not do well in the north, where winters are more severe. This is especially problematic for stocks that are affected by tracheal mites or diseases such as chalkbrood, both of which affect bees more in the cooler, damper regions of the north (Flores et al., 1996). Establishing locally adapted populations of bees is difficult because more than 500,000 queens are shipped each year throughout the country from southern production sites (Schiff and Sheppard, 1995, 1996). Instrumental insemination (Laidlaw, 1992) is ideal for bee-breeding programs (development and maintenance), although it is more costly than is natural mating. Moreover, the honey bee mating behavior presents a challenge to the development and maintenance of selected lines of honey bees. Honey bee queens are naturally polyandrous (Winston 1987), mating with 7–17 drones on 1–5 mating flights, usually within the second week of life. Queens and drones fly to discrete spaces in drone congregation areas, located some distance above the ground and away from their nests. Mating takes place as the queen flies through one or more drone congregation areas, where the sources of drones are uncontrolled. It is not clear whether some percentage of mating with a specific desired stock is necessary to ensure a mite- or pathogen-resistant colony (Box 6-1) and likely depends on the genetic mechanisms involved (dominance, additive, epistasis). Most commercial queen producers probably do not use resistant stocks, and most queens shipped throughout the United States apparently still come from susceptible stocks of bees. Susceptible queens also produce drones that flood local mating areas, so it is difficult to establish a sustainable resistant population. Genetic Solutions to Problems with Mites and Pathogens Genomics and germplasm preservation could be used to facilitate the development and maintenance of selected honey bee stocks. The traditional breeding process could be augmented through the use of genetic markers (expressed sequence tags and quantitative trait loci) for desirable traits. Markers already have been identified for defensive behavior (Hunt et al., 1998) and for hygienic behavior (Lapidge et al., 2002), and more research could facilitate development of commercially viable selected stocks of honey bees. The recent sequencing of the honey bee genome by the Baylor College of Medicine (The Honeybee Genome Sequencing Consortium, 2006) and

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Status of Pollinators in North America BOX 6-1 Development and Maintenance of Selected Stocks: Controlled Mating The development and maintenance of selected stocks and breeder queens require controlled mating, generally through instrumental insemination (Laidlaw, 1992). Breeder queens (selected queens inseminated with semen from selected drones) are transferred or sold to commercial queen producers who use them to produce large numbers of production queens for sale to beekeepers. The parentage of the production queens is controlled through the use of breeder queens. Before a production queen is sold to a beekeeper, it is first mated to several drones, and the mating of production queens is invariably natural. Because commercial queen producers cannot completely control the sources of the drones that mate with their production queens (Laidlaw and Page, 1998), the queens often mate with drones from unselected stocks of local wild bees or from colonies belonging to other beekeepers. Thus, production queens will often produce hybrid workers that do not exhibit the desired traits or that do not exhibit those traits to the desired extent, depending on the genetic basis of the variation under selection (for example, dominance, additive, epistasis). The percentage of matings that must occur with a specific desired stock to ensure a mite or pathogen resistance in a colony is not known and could depend on the trait. Some work suggests that open-mated queens from selected stocks can produce colonies with useful—but incomplete—mite resistance (Harbo and Harris, 2001; see also Spivak and Reuter, 1998, and Spivak et al., 1995, for response to American foulbrood), but another report suggests that both male and female parents should be from selected stocks (Harris and Rinderer, 2004). Although instrumental insemination is currently complicated for use in commercial queen production, there are other options for controlling commercial mating—drone saturation and isolation (Laidlaw and Page, 1998). The former achieves varying degrees of controlled natural mating by stocking mating areas with large numbers of drone source colonies from the desired selected source (Hellmich, 1986, 1991; Hellmich et al., 1988). The latter uses isolated mating yards to control mating. The opportunity to employ isolation is limited because a separation of several kilometers from other sources of drones is required.

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Status of Pollinators in North America related developments in honey bee genomics (Robinson et al., 2005) provide outstanding resources for these efforts. Maintaining selected stocks of honey bees is difficult because of the generally uncontrolled mating behavior of queens and because queens have relatively short and unpredictable lives of 1–3 years (Seeley, 1985). Given the ephemeral nature of honey bee stocks, honey bee germplasm (sperm, eggs, embryos) is an ideal candidate for preservation, which would allow stakeholders an economical way to maintain large quantities of desirable germplasm from a nearly unlimited number of sources. The benefit seen in the increased access to resources would well justify the investment required to identify or develop the germplasm. This work would fit within the mission of the USDA National Animal Germplasm Program (http://www.ars-grin.gov/animal/), which coordinates and supports the cryopreservation of U.S. animal genetic resources (Blackburn, 2002). Preservation of honey bee germplasm has been attempted, so far with limited success (Collins, 2000, 2004). Transition to Resistant Stocks Converting the current U.S. honey bee population to one that is resistant to parasites and pathogens is an enormous challenge that would require unprecedented cooperation among queen producers and consumers, federal and university research facilities and extension programs, and, most important, beekeepers. A successful transition would require improved identification methods, including the use of genetic markers in mass screening for desirable traits; new stocks that are viable in several regions; an industry infrastructure that maintains superior stocks; and a mechanism for third-party certification of new product lines. Certification of breeder stock, mating technology, production methods and facilities, and commercially produced bees and queens would be necessary. Managing Miticide Resistance Pesticide resistance has become the major problem for the management of parasitic mites. Populations of V. destructor that exhibit resistance to fluvalinate (Baxter et al., 1998; Elzen et al., 1998, 1999a,b,c,d; Hillesheim et al., 1996; Macedo et al., 2002), coumaphos (Elzen and Westervelt, 2002; Milani and Della Vedova, 1996; Pettis et al., 2004), or amitraz (Elzen et al., 1999c, 2000) are widespread. Resistance management programs would provide beekeepers with a significant tool for mite management. Such programs could be built around results from several areas of research, including projects on the mechanisms and management of resistance to various pesticides (Gerson et al. 1991; Ting et al. 2003; Wang et al. 2002; Wu et al. 2003), the identification of genetic

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Status of Pollinators in North America correlations among resistance mechanisms, determination of the fitness consequences of pesticide resistance, and determination of optimal intervals for pesticide rotation (Hall et al. 2004). The industry also could benefit from the development of synergists to inhibit enzyme-based resistance in mite populations, thereby restoring the effectiveness of existing miticides. And the identification of new, less toxic pesticide compounds derived from natural products would provide beekeepers with still more options. In particular, the work should focus on improving the efficiency and reliability of such commercial products as Mite-Away II and other soft chemicals (Apiguard and Api-Life VAR). The design of resistance management programs could follow up results from research projects outlined above. Although there are no comprehensive programs for beekeepers, there is considerable literature that could be used as a starting point for research on pests of bees (see Batabyal and Nijkamp, 2005; Benting et al., 2004; Comins, 1986; Elzen et al., 1999b; Georghiou, 1980; Green et al., 1990; Hall et al., 2004; MacDonald et al., 2003; Phillips et al., 1989; Thompson, 2003; Walker-Simmons, 2003; Williamson et al., 2003). The tracheal mite has dropped into relative obscurity over the past decade, overshadowed by problems with varroa mites. The current effects of tracheal mites on honey bee populations are not known. Fortunately, several remedies are available for control of tracheal mites, including “grease patties” (made from vegetable shortening and granulated or powdered sugar) (Baxter et al., 2000; Calderone and Shimanuki, 1995; Liu and Nasr, 1993; Wilson et al., 1989), formic acid (Baxter et al., 2000; Feldlaufer et al., 1997; Hoppe et al., 1989), and menthol (Baxter et al., 2000; Duff and Furgala, 1993; Wilson et al., 1989, 1990). Amitraz, although not currently marketed, also can be effective against tracheal mites under some circumstances (Duff and Furgala, 1993; Wilson and Collins, 1993). Treatment results have been mixed (Duff and Furgala, 1993; Scott-Dupree and Otis, 1992), and honey bee populations have evolved resistance to tracheal mites (Gary et al., 1990; Page and Gary, 1990), an attribute that likely has contributed to a reduction in concern about this pest. There is an additional economic benefit to deploying mite-resistant bees and reducing pesticide use—over and above the savings realized from eliminating the need to purchase chemical pesticides. The use of resistant stocks allows beekeepers to eliminate pesticide use, and some beekeepers could potentially sell their products at a premium (NRC, 2000). Other Methods of Managing Parasites and Pathogens Nonchemical control methods—such as cultural methods or biological control—offer many advantages for beekeepers. Combined with third-party

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Status of Pollinators in North America certification of honey (as pesticide-free or organic, for instance), those methods expand the beekeepers’ options in the marketplace, enabling them to take advantage of the more lucrative trade in natural foods. Among the cultural methods for mite control, drone brood removal, which exploits mite preference for drone brood, can be effective albeit labor-intensive (Calderone, 2005). The Beltsville screen insert, a piece of wire mesh inserted 3–5 cm between a hive’s bottom and its bottom board, traps the mites that typically fall to the bottom of the hive as bees groom to rid themselves of mites. The insert prevents the mites from climbing back up to reinfest the bees. The screen insert has yielded mixed and generally disappointing results (Ellis et al., 2001; Harbo and Harris, 2004; Pettis and Shimanuki, 1999; Rinderer et al., 2003), but it could become an effective management tool if it were combined with pesticides that have a rapid knockdown effect for application during honey-producing months. The fungal pathogens Hirsutella thompsonii and Metarhizium anisopliae have shown promise as potential biological control agents for varroa mites (Kanga et al., 2003a,b), but problems with the pathogens’ sensitivity to temperature and spore distribution within hives remain unsolved. If these could be overcome, biological control could become a viable option for managing parasitic mites. Perhaps even more important than developing new treatments for bee diseases and parasites is reinforcement of regulations aimed at prevention. Protection of North America against invasive pests and diseases from abroad is the cornerstone of pollinator protection on the continent, but existing regulations should be strictly enforced and strengthened to remain effective. The Federal Honey Bee Act of 1922 “prohibits the entry of honey bees from countries where diseases and parasites harmful to honey bees are known to exist” (USDA-APHIS, 2002). The act authorizes the Animal and Plant Health Inspection Service (APHIS) to regulate importation of honey bees in the United States. In 2004, APHIS changed the regulation to allow honey bee packages from Australia and New Zealand to be imported to pollinate California almond groves (USDA-APHIS, 2004). Although honey bee colonies from Australia and New Zealand can offer a short-term benefit in the pollination marketplace, great care must be exercised to ensure that they do not carry new pests, parasites, pathogens, and predators. APHIS and corresponding agencies in Canada and Mexico should conduct periodic, coordinated monitoring of honey bee populations to determine whether specific pests are present. Target species for monitoring should include Tropilaelaps clareae (parasitic mite), Hyplostoma fuligineus (large hive beetle), Varroa spp. and V. destructor haplotypes that are not present in North America, Apis mellifera scutellata (African honey bee), Apis mellifera capensis (another potentially invasive subspecies of honey bee from South Africa), and other Apis species. APHIS could coordinate the

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Status of Pollinators in North America efforts with cognate agencies in Mexico and Canada. State departments of agriculture should be included in the development of monitoring programs and could provide valuable personnel. Shipments of bees from countries or territories that have pests that are not already present throughout North America should not be permitted if long-term safeguarding of North American pollination capacity is a priority. APHIS should carefully assess the integrity of inspection in countries interested in supplying bees to North America, and it should collect and analyze samples of adult and immature honey bees from producers who wish to ship to North America. Sampling in the countries of origin is necessary because the bees could have pests that are currently unidentified and therefore not on the list of target species. Also, North American countries should proceed with research on honey bee pests in the potential source countries that have not yet arrived in North America to prepare the countries’ beekeeping industries for possible or eventual introductions. Africanized Honey Bees The consequences of the Africanized honey bee (AHB) infiltration of U.S. and Canadian honey bee populations are difficult to predict. However, uncertainty and precedent in other nations suggest that it is prudent to prepare for the worst. There are three general methods for managing AHBs: eradication, genetic isolation, and breeding (http://www.ces.ncsu.edu/depts/ent/notes/Bees/ahbactionplan2001.pdf). Several states, including North Carolina, have developed action plans that include recommendations for best management practices for beekeepers, and procedures for abatement, quarantine, outreach, and first-responder training. Other states should develop similar plans, and much of the information they need is available from existing resources. Eradication is most effective against confirmed or suspected founder colonies that are inadvertently imported by truck or ship, but before the Africanized bees can become established. Genetic isolation is achieved through various controlled-mating techniques—such as geographic isolation, instrumental insemination, and drone saturation (Laidlaw and Page, 1998). Geographic isolation requires European honey bee production apiaries to be established at a distance from AHB colonies that is sufficient to prevent mating of the European queens with the Africanized drones. Queen-and-package producers might be able to use this method to a limited degree by placing operations in places that are so far free of Africanized bees: the northern United States, Hawaii, Canada, Australia, and New Zealand. Northern U.S. and Canadian operations could be of limited use, however, because the colder weather prevents production of queens and packages until late in the season. The United States began to import honey

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Status of Pollinators in North America bee packages from Australia and New Zealand for early-season pollination after winter losses in 2004–2005 (Sumner and Boriss, 2006). Australia, New Zealand, and Hawaii could be important sources of uncontaminated germplasm in the future, but extreme vigilance would be needed to ensure that additional invasive diseases or pests not be introduced. A second way to control mating is through instrumental insemination (Laidlaw, 1977), which allows for control of male and female sources of germplasm and for maintenance of a secure, closed breeding population. Instrumental insemination is a highly effective tool in the hands of qualified practitioners and it is effective for the maintenance of domestic supplies of germplasm that is free of AHB traits. However, it is impractical for the production of commercial queens for sale to beekeepers: it is too time-consuming and labor-intensive to be profitable (Laidlaw and Page, 1998). The final method for controlling mating is drone saturation: flooding an area with enough drones from a desired source to enhance the probability that young queens will mate with them. More research is required, however, to determine the degree of mating control required to produce behaviorally acceptable colonies (Guzmán-Novoa and Page, 1994a). Beekeepers are aware of liability issues that could result from stinging incidents that involve Africanized bees. Guzmán-Novoa and Page (1994b, 1999) have reported that selective breeding within Africanized populations can result in a reduction in defensive behavior. However, continuous breeding selection could be necessary to suppress defensive behavior, especially where AHB stocks are prevalent. Integrated Pest Management Integrated pest management (IPM; Kogan, 1998) provides a unifying framework for the management of many agricultural pests, including those of honey bees. IPM coordinates the use of several pest control methods for sustainable, economically feasible management. Whenever possible, IPM uses reliable pest-sampling methods and economic injury thresholds to guide treatment decisions. IPM is desirable because it allows beekeepers to use pest information to avoid economically unnecessary applications of pesticides and antibiotics, thereby extending the long-term utility of those products by reducing the rate at which resistance evolves. It also allows beekeepers to reduce or eliminate pesticide residues in hive products. Each sector of the beekeeping industry will require an IPM program to fit its size (the number of colonies) and its marketing goals (commercial or natural foods). American foulbrood is one disease that is effectively treated with IPM approaches. The combination of cultural methods with inspection programs and the proper use of antibiotics provides good results for control (Goodwin and Van Eaton, 1999). Continued extension efforts should be en-

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Status of Pollinators in North America couraged to widen acceptance of IPM of parasitic mites, especially by large commercial operators. The future of IPM’s application in the industry will depend on the development of additional treatments and on the creation of economic incentives to compensate for the additional costs involved. Extension activities provide a primary mechanism for informing bee-keepers about pest management options and the best ways to implement them. Extension apiculturists should encourage the use of IPM whenever possible, and extension personnel should encourage beekeepers to demand third-party certification of resistant stock from commercial queen producers. Extension efforts directed toward queen breeders and commercial queen producers should emphasize methods for stock development and maintenance and the use of controlled mating, primarily through geographic isolation and drone saturation. ARS Honey Bee Research Much of the applied research on honey bees in the United States is conducted in ARS honey bee laboratories. Research funding has increased from $5.6 million in 1996 to $9.2 million in 2006, although the number of fulltime scientists has declined since 2003 (Table 6-1). Some of the approaches to preventing or reversing pollinator decline outlined in this chapter depend on strong ARS involvement in honey bee research. Maintaining current research support and restoring lost scientist positions—with a special focus on honey bee pollination—at ARS is critical to pollinator conservation and restoration. TABLE 6-1 Funding and Staffing ARS Bee Research Fiscal Year Funding ($ U.S.) Full-Time Permanent Staff Scientists 1996 5,574,000 23 1997 5,913,000 23 1998 6,380,000 23 1999 6,599,000 26 2000 7,009,000 26 2001 7,629,000 27 2002 8,037,000 25 2003 8,450,000 28 2004 8,844,000 27 2005 8,861,000 27 2006 9,227,000 24 SOURCE: USDA-ARS.

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Status of Pollinators in North America From a site in Israel that had high pollinator biodiversity (Mt. Carmel), Potts and colleagues (2003) discovered that fire initially was catastrophic to plant and bee communities, but that recovery was rapid. Within 2 years of the fires there was a peak in plant and bee diversity that was followed by a long and steady decline over the next 50 years. They reported that bee pollinator communities closely matched the plant community in recovery and regeneration (Potts et al., 2001, 2003). Like mowing and grazing, fire is an important management tool that can be used to reset the successional sequence and maintain the diverse and heterogeneous mosaic landscapes that include early successional stages (oldfields) and late primary stages (climax forests). Resetting the successional sequence provides resources for a wider array of species (Pickett and White, 1985; Smallidge and Leopold, 1997). More information is needed on the short- and long-term effects of fire—and its use as a management technique—on diverse North American plant and pollinator communities. Nesting Habitat Although solid expanses of grasses and forbs are not productive nesting habitats for bees, they do provide nest sites (larval host plants) for a variety of Lepidoptera. Thus, grassland management protocols that are well adapted for Lepidoptera also should consider provisions for bee-nesting sites. Nesting sites can be provided by creating patches of bare ground or sand-loam mixes for ground-nesting bees; by maintaining a landscape mosaic of wooded and grassy areas, protecting some dead wood and standing snags and drilling holes in some dead wood; putting out trap nests for twig-nesting bees; and putting out bumble bee nest boxes, buried or above ground (Box 6-4). Large-scale herbicide applications, such as are applied in the southwestern United States to remove undesirable scrub and brush (mesquite and Prosopis plants), should be discouraged because they remove not only nesting sites and refuges, but also pollen and nectar sources for native bees, honey bees, and other pollinators (Buchmann and Nabhan, 1996). MAINTAINING POLLINATION SERVICES Maintaining commercial pollinator stocks and the diversity of wild pollinator communities differs from maintaining pollination services provided by pollinators, because pollination services could be enhanced without an increase in pollinators. This section presents strategies for maintaining pollination services to crops by commercial pollinators and pollination services to crops and wild native plant populations by wild pollinators.

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Status of Pollinators in North America BOX 6-4 Golf Courses and Other Urban and Suburban Green Spaces Traditionally, golf courses have been inhospitable areas for pollinating birds, bats, and insects because of the large amounts of fertilizers, herbicides, and pesticides used and their close-cropped mowing. The U.S. Golf Association has adopted pollinator-friendly practices (Shepherd, 2002; Shepherd and Tepedino, 2000; Shepherd et al., 2001) for out-of-play areas (roughs), where wildflowers are planted, nesting domiciles (drilled bee boards) are provided, and few or no pesticides and herbicides are applied. Some golf courses have combined to form an association of organic golf courses (http://www.usga.org/turf/green_section_record/2005/jan_feb/Inorganic.html; http://www.epa.gov/oppbppd1/PESP/strategies/2005/ogmd05.htm). Similar techniques could be applied in urban parks and greenbelts, on large corporate campuses, and at a smaller scale in home gardens, to improve habitat for pollinators in urban and suburban areas. The abundant floral resources in backyard gardens in some urban areas already support diverse communities of bees and nest sites for twig-nesters in wooden fences or houses (Cane et al., 2006; Frankie et al., 2005). Commercial Pollinators Crops that require or are improved by animal pollination benefit from the services of commercially managed honey bees or other commercially managed bees. The supply of commercial honey bee colonies can be stabilized by reducing bees’ vulnerability to pests, parasites, pathogens, and pesticides. If honey bee colonies are in short supply, a new and potentially useful compensation is to increase the available colonies’ efficiency. Honey bee brood pheromones have been identified that temporarily increase the proportion of a colony’s foragers that collect pollen (Pankiw, 2004). Hormone manipulations also can advance the age at which bees switch from working in the hive to foraging and increase the proportion of a colony’s foraging-worker force (Robinson and Ratnieks, 1987). These pheromones and hormones could be developed into slow-release stimulants to increase a colony’s pollinator force in a grower’s field, although possible negative effects on bee hives also should be explored. The supply of alternative commercial pollinators requires caution to reduce losses to pathogens and parasites, as happened to the alfalfa leafcutter bee, for example. Intensified research and technology transfer will be required for development of new species of alternative pollinators.

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Status of Pollinators in North America Commercially managed pollinators can be brought to the crops that need their services, ensuring service delivery. Thus, growers of commodities that require pollination follow recommendations for pollinator stocking. For example, hybrid sunflower production requires two colonies of honey bees per hectare (Delaplane and Mayer, 2000). Although some improvements could be made to maximize benefits by altering the spacing of colonies in fields and the spacing of self-incompatible cultivars (Chapter 4), in general, the great advantage of using commercially managed pollinators is that service delivery can be controlled, or at least manipulated, by relative placement of pollinators and cultivars. Wild Pollinators It is far more difficult to ensure that services from wild pollinators are delivered to crops. Because the mechanisms are not still well understood, managing wild pollinators requires a better understanding of foraging ecology and population biology and how they are influenced by landscape properties (Kremen and Ostfeld, 2005). The few existing studies, however, suggest that healthy (diverse and abundant) pollinator communities could provide enhanced pollination services for a wider array of crops, and ensure stability of services within seasons and across years (Klein et al., 2003; Kremen and Chaplin, in press; Kremen et al., 2002a). Because pollinators are mobile and they collect resources within the foraging range of a nest, roost, or territory (for example, hummingbirds), environmental qualities of the immediate site (local) and the surrounding area (landscape) affect their population sizes, densities, and persistence. Many pollinator species use a variety of floral and nesting resources that can be distributed across different habitat types at different times of the year (Westrich, 1996). Some pollinators use native plant resources that occur only in natural habitats in season, and weedy resources that occur in agricultural habitats in the summer (Kremen et al., 2002a). Mass-flowering resources provided by crops can also be important for selected species in a landscape (Westphal et al., 2003). Evidence suggests that the character of a landscape is important in determining the richness, abundance, and composition of pollinator communities on farms. Pollinator species differ in their ability to provide services to different crops (for example, Free, 1993; Kremen et al., 2002b), and their effectiveness could vary with the community context in which they exist (Greenleaf and Kremen, 2006b; Thomson and Goodell, 2001; Thomson and Thomson, 1992). Therefore, alterations in the composition of pollinator communities due to landscape change influence both the quantity and quality of pollination services to crops—although local site characteristics also influence pollinator communities and services (reviewed in Kremen

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Status of Pollinators in North America and Chaplin, in press). In California’s Mediterranean climate environment, landscape factors (the proximity or proportional area of natural habitat within a site) are the dominant factors for pollinator richness, composition, abundance, and services (Greenleaf, 2005; Greenleaf and Kremen, 2006b; Kremen et al., 2002b, 2004), although site characteristics (conventional or organic management of farm sites) modulate these responses at the population level (Kim et al., 2006; Williams and Kremen, in press). In tropical rainforest biomes of Central and South America and Indonesia and in temperate grassland biomes in Germany and Canada, pollinator richness, abundance, and services also respond primarily to proximity to natural or seminatural habitat at the landscape level (Chacoff and Aizen, 2006; Klein et al., 2002, 2003a; Morandin and Winston, 2005; Ricketts, 2004; Ricketts et al., 2004; Steffan-Dewenter and Tscharntke, 1999; Steffan-Dewenter et al., 2001, 2002), but local factors, such as light (Klein et al., 2002, 2003b) and the abundance and richness of weedy floral resources (Morandin and Winston, 2005), also have statistically significant effects. Pollination services for wild plants that depend on or benefit from animal pollination are generally provided exclusively by wild pollinator populations, although managed honey bees often forage on wild plants and, thus, provide some services (Kremen et al., 2002). Managing wild pollinator communities is needed to ensure pollination function for natural plant communities. Pollination services to wild plants in habitat fragments can be influenced by the size and isolation of the fragment, the characteristics of the surrounding human-modified matrix, and the resulting population responses of plants and pollinators (Bronstein, 1995; Ghazoul, 2005c). Small fragments tend to have small plant populations (MacArthur and Wilson, 1967), which can be less attractive to pollinators (Brody and Mitchell, 1997; also reviewed in Kunin, 1997), and thus become pollinator limited (Box 4-1; Groom, 2001). Smaller fragments often also contain smaller populations and fewer pollinator species (MacArthur and Wilson, 1967; Miller et al., 1995; Ricketts, 2001; Steffan-Dewenter, 2003) thus reducing pollinator visitation (Aizen and Feinsinger, 1994; Cresswell and Osborne, 2004). Empirical studies, however, have revealed positive, negative, and neutral effects of fragment size on pollinator abundance, richness, and services (Aizen and Feinsinger, 1994; Cane et al., 2006; Danielsen et al., 2005; Miller et al., 1995; Tonhasca et al., 2002; Winfree et al., 2006). The variability in response is probably attributable to differences in habitat specificity and dispersal ability among pollinator species (Law and Lean, 1999; Saville et al., 1997; Steffan-Dewenter, 2003). Geographic isolation also can affect pollination services to wild plants (Ghazoul, 2005c). Plant populations in isolated fragments could be self-limited by the amount of compatible pollen available (Duncan et al., 2004). Isolated fragments contain smaller populations and fewer pollinator and

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Status of Pollinators in North America plant species (MacArthur and Wilson, 1967) thus reducing pollinator visitation and fruit set (Cunningham, 2000; Steffan-Dewenter and Tscharntke, 1999). Corridors that link habitat fragments have been shown to increase movement of selected pollinator species and enhance pollination of target plants (Tewksbury et al., 2002; Townsend and Levey, 2005). Isolation also can reduce pollinator visitation and seed set (Jennersten, 1988), but in some cases, even highly isolated plants are known to receive sufficient out-crossed pollen to reproduce (Nason and Hamrick, 1997; Schulke and Waser, 2001; White et al., 2002). All of the fragment-specific factors are likely to be modulated by the type of human-dominated matrix that surrounds natural fragments (Ricketts, 2001). If the surrounding matrix is hospitable to wild plants (Mayfield and Daily, 2005) or contains nesting or floral resources for some pollinator species (Klein et al., 2002; Westphal et al., 2003), the effects of fragment size and isolation can be alleviated. Relatively few studies of pollinator communities and pollination function in fragmented landscapes consider matrix effects (Cane et al., 2006; Dauber et al., 2003; Hirsch et al., 2003; Steffan-Dewenter et al., 2006; Williams and Kremen, in press; Winfree et al., 2006). Clearly, managing landscapes and sites will be important for restoring, preserving, or maintaining diverse pollinator communities and ecological service functions to crops and wild plants. How much natural habitat is sufficient in the landscape for pollinator maintenance is an open question. Kremen and colleagues (2004) observed a log-linear relationship between the amount of pollination services provided to a watermelon crop and the proportional area of natural habitat within several kilometers of a farm. Full pollination services could be provided by wild bee communities at 30 percent or more natural habitat cover. Morandin and Winston (2006) determined that removing 30 percent of land from canola seed production would actually increase profits to canola farmers, because of the resulting increased diversity, abundance, and services provided by wild bees. Ricketts and colleagues (2004) suggested that fragments of at least 20 hectares of tropical rainforest provide valuable services to coffee from wild bees that are comparable to other land use values. Equivalent studies of native plants in natural habitat fragments are lacking. How patches of habitat should be configured to deliver pollination services into the surrounding agricultural matrix (in the case of crops) or to maintain gene flow and population persistence for isolated populations of wild plants that are confined to fragments also is poorly understood. If wild pollinators in an area indeed depend on natural habitat fragments for nesting sites and critical floral resources, then crop pollination can benefit from a “service halo” around the habitat fragment corresponding to the foraging ranges of individual pollinator species (Ricketts, 2001; Ricketts

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Status of Pollinators in North America et al., 2004). Dispersing small fragments extensively throughout an area seems logical but leaves open the question of how to configure large parcels to allow pollinator populations to persist. Both metapopulation theory (reviewed in Hanski and Ovaskainen, 2000; Harrison and Fahrig, 1995) and empirical data (Harrison et al., 1988) suggest that some larger patches are needed to support larger sized populations that are more resistant to extinction (see also Berger, 1990; Zayed and Packer, 2005). Larger areas also will, in theory, contain more diverse assemblages of pollinators (MacArthur and Wilson, 1967; Simberloff and Wilson, 1969) that might provide more services, more consistently, and contribute to pollination of a wider variety of crops (Kremen and Chaplin, in press) and other plants (Memmott, 1999; Memmott et al., 2004). More research is needed to determine the optimal configuration of landscape fragments and their connectedness to maintain pollinator populations, communities, and functions. PUBLIC POLICY AND POLLINATOR POPULATIONS U.S. Endangered Species Act The Endangered Species Act (ESA) of 1973 is the broadest and most powerful U.S. law for the protection of endangered species and their habitats (NRC, 1995). The act lists species of plants and animals (vertebrate and invertebrate) as endangered or threatened according to assessments of their risk of extinction (Congressional Research Service [CRS], 2006). Once a species is listed, ESA’s strict substantive provisions become legal tools to assist in the species’ recovery and the protection of its habitat. Endangered species and their critical habitats are entitled to strong protections. It is illegal, for example, to take any endangered species in the United States or its territorial waters, and any federal action that will jeopardize the future of an endangered species is prohibited, including any action that threatens to destroy or damage critical habitat. At press time for this volume, in the fall of 2006, 1879 U.S. and foreign animals and plants were listed as endangered or threatened (U.S. Fish and Wildlife Service [USFWS], 2006). ESA’s major goals include the recovery of endangered and threatened species to the point at which protection is no longer needed. As this volume went to press, USFWS (2006) had cataloged 17 U.S. and foreign species that had been recovered and removed from the list. The populations of other listed species have increased, and some appear to have stabilized even though they remain on the list. A species is placed on the Endangered Species List on the initiative of the secretary of the interior or of the secretary of commerce. The decision is based on the best available scientific and commercial information and a

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Status of Pollinators in North America lengthy procedure that ensures public participation and the collection of relevant information. Because Congress directed that listing have a scientific foundation for the label of threatened or endangered, economic factors are not considered in the listing decision. In June 2006, there were 282 “candidate” species for which no decision had been made. The status of those species is to be monitored and, if any emergency poses a significant risk to their continued existence, they must be listed promptly. Modifications of ESA and other recently proposed changes could make it more difficult to list pollinators than some other animals. A 1981 congressional revision specifically exempted any “species of the Class Insecta determined by the Secretary to constitute a pest whose protection under the provisions of this Act would present an overwhelming and overriding risk to man.” Any species that has caused economic damage or could do so is less likely to be protected. The larvae of some lepidopteran pollinators, for example, and the adults of some hymenopteran pollinators can under some circumstances cause economic damage. Securing endangered status for them could prove problematic. Recent efforts to amend ESA also could add new barriers to listing pollinators. H.R. 3824, passed by the House of Representatives in 2005, “To amend and reauthorize the Endangered Species Act of 1973 to provide greater results conserving and recovering listed species, and for other purposes” replaces the criterion of “best scientific and commercial data available” with “best available scientific data.” More important, unlike ESA itself, H.R. 3824 for the first time defines “best available scientific data” as “scientific data, regardless of source, that are available to the Secretary at the time of a decision or action for which such data are required by this Act and that the Secretary determines are the most accurate, reliable, and relevant for use in that decision or action.” The secretary is directed to issue regulations that establish criteria for “best available scientific data” and must ensure that the information consists of empirical data or data found in sources that have been subjected to peer review by people recognized by the National Academy of Sciences [NAS] as qualified to independently review a covered action in a manner that is in compliance with the Data Quality Act (44 USC 3516) (Congressional Research Service, 2006). According to CRS, “Some contend that the specification of empirical data in H.R. 3824 would exclude estimates derived from models and limit the type of data available for use…. However, estimates derived from modeling could be allowed under H.R. 3824, if it meets the NAS peer-review conditions set forth in the bill.” Because of the paucity of data available for many pollinator species (Chapter 2), assessments of species status often are based on information derived from population models or from genetic studies, which could be excluded if ESA is amended as proposed.

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Status of Pollinators in North America Incentives for Stewardship The public benefits provided by wild pollinators justify public policy that encourages stewardship of wild pollinators. Given the importance of habitat, land stewardship policies constitute the majority of relevant mechanisms. However, consumer-oriented measures also have a role in pollinator conservation policies. For agricultural lands, there are four voluntary programs that can be used or adapted to create or maintain pollinator habitat. The Farm Security and Rural Investment Act of 2002 (the Farm Bill) authorized them: The Wildlife Habitat Incentives Program (WHIP) (NRCS, 2006a) provides cost sharing and incentive payments to eligible farmers for planting native and nonnative plants that could enhance wildlife habitat (including pollinators) through early successional habitat development, riparian herbaceous cover, tree and shrub establishment, and upland and wetland habitat management. The Environmental Quality Incentives Program (EQIP) (NRCS, 2006b) also provides money to eligible farmers who focus on soil and water conservation. The program can be customized to include pollinator habitat through improvements in hedgerows, riparian buffer strips, tree and shrub planting, and wildlife habitat management. The Conservation Reserve Program (CRP) (USDA-FSA, 2006) pays eligible farmers to convert agricultural land to conservation uses under a 10-year contract. Farmers make bids that describe their land management plans and the annual payments they would require. The Farm Service Agency (FSA) evaluates the bids in light of technical advice from NRCS. The evaluation is based on state priorities, and points are awarded for expected conservation benefits from plans that include native species, especially flowering shrubs and forbs. Currently, no points are assigned explicitly for pollinator habitat. The Conservation Stewardship Program (CSP) (NRCS, 2006c) awards 10-year contracts to eligible farmers according to the farmers’ proposed intensity of stewardship and their proposed practices. CSP payments for pollinator habitat are available as “resource enhancements” under the rubric of “wildlife habitat management.” In 2005, North Dakota’s state NRCS program covered pollinator habitat under three CSP enhancements involving native herbaceous cover plots, unharvested tame hay land, and native woody cover plots (NRCS-North Dakota, 2005). WHIP, EQIP, and CRP are available to farmers who have traditionally raised wheat and feed grains eligible for federal price supports. Because of the tightening federal budget, access to payments for conservation practices is rationed through priorities established by state technical committees and

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Status of Pollinators in North America according to the characteristics of individual conservation plans submitted by landowners. Many states do not assign points for enhancing pollinator habitat or provide guidance for doing so. In the states that do provide points, such as Michigan, very few landowners had enrolled as of December 2005. CSP eligibility is further restricted to farmers in a limited number of watersheds in each state on a list that rotates annually, with the goal of making each watershed eligible every 7–10 years (A. Herceg, NRCS, personal communication, December 2005). Although the four U.S. farm environmental stewardship programs provide a sound vessel for encouraging landowners to enhance pollinator habitat, interest among farmers has been limited. The research base for NRCS to estimate the on-farm and external conservation benefits from pollinator habitat also is limited. Development of a national monitoring program for pollinator species would provide a remedy (Chapter 5). For nonfarm, private landowners—homeowners, public utilities, or businesses—investments in pollinator habitat could be encouraged through income tax deductions. Public agencies involved in land management, such as the U.S. Forest Service, the U.S. Department of the Interior, and the U.S. Department of Transportation, could include provisions for pollinator protection or enhancement in their guidelines. The inclusion of pollinator protection in the criteria for federal land leases for grazing and timber harvest also could encompass large areas of land. Some interstate highways already have wildflower plantings, which could be enhanced by purposeful selection of appropriate native plant species favored by wild pollinators. Volunteer networks also could encourage creation or restoration of pollinator habitats much as they have done for pollinator monitoring in the Audubon Society’s annual Christmas Bird Counts and the North American Butterfly Association’s Fourth of July counts (Chapters 2 and 5). Monarch Watch’s Monarch Waystation program has already resulted in the creation and registration of more than 600 butterfly-friendly habitats with nectar resources and host plants. A private, nongovernmental organization interested in pollinators might establish a “friends of pollinators” network that could be diffused through school programs and public service announcements. Interest could be sparked through activities such as a landscape architecture competition for designs that invite and support pollinator populations. Even consumers can engage in pollinator protection. Following the successful ecolabeling campaigns for dolphin-safe tuna and shade-grown coffee, a label could be used to certify pollinator-safe fruits and vegetables. With the important exception of the USDA organic label, most food certification labelling is done by private organizations. Currently, however, there are no known organizations that are both interested in and capable of developing and providing certification for a pollinator-protector label.

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Status of Pollinators in North America ADAPTIVE MANAGEMENT AND POLLINATOR MONITORING Different management strategies can be used across landscapes, including public and private lands, working lands, and natural areas, to improve conditions for pollinators and to maintain pollination function in crops and wild plants. Strategies range from site-specific management that could be performed by private landowners, to landscape and regional actions that would require coordination by county, state, or regional authorities and nongovernmental organizations. Although management actions can be guided by a body of existing scientific knowledge, all are experimental; therefore, concurrent monitoring of pollinator status and of pollination function is needed (Chapter 5) to determine the efficacy of different strategies and to adapt measures to provide even better performance (Kremen et al., 1993; Margoluis and Salafsky, 1998; Walters and Holling, 1990). CONCLUSIONS This chapter presents various actions that could be taken to maintain commercial pollinators, wild pollinator species and communities, and pollination function. The committee suggests the following as priorities. Apis Develop and refine both traditional and molecular methods for identifying bees with economically desirable traits for inclusion in honey bee breeding programs. Select model populations of honey bees with economically desirable traits for adoption by the beekeeping industry. Develop educational materials and programs to enable private-sector queen producers to develop and maintain pest, parasite, and pathogen resistant stocks of honey bees and to serve as reliable sources of quality production queens that produce colonies expressing useful levels of economically important traits. Develop sustainable methods for ensuring that Africanized bees do not degrade the commercial value of existing stocks of honey bees. Develop resistance management programs to mitigate the adverse effects of pesticide and antibiotic resistance in honey bee pest, parasite, and pathogen populations. Develop methods for the preservation of honey bee germplasm. Other Commercial Species Identify commercially viable solutions to the problem of chalkbrood in the alfalfa leafcutter bee, Megachile rotundata.

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Status of Pollinators in North America Identify non-Apis bees with the potential to be developed into economically useful pollinators. Develop commercially viable methods for culturing economically important species of bumble bees and solitary bees for use as crop pollinators. Wild Bees Inform the public—in particular, the agricultural community and managers of golf courses, urban parks, and other large urban-suburban areas such as industrial and academic campuses—about current knowledge of actions (such as creating pollinator habitat) that can be taken to manage pollinators. Conduct field studies in different regions of North America to determine the suites of key floral resources for use in restoration protocols in each region. Conduct additional studies that can be used to improve existing restoration protocols, including monitoring the influence of restoration activities on population and community dynamics of pollinators and understanding land managers’ willingness to adopt restoration practices. Define land-management practices (by NRCS state offices) that encourage pollinator populations that are eligible for federal payments under existing Farm Bill conservation programs such as EQIP, WHIP, CRP, and CSP. Integrate land management practices that encourage pollinator populations at the state level into existing Farm Bill conservation programs such as EQIP, WHIP, CRP, and CSP. Conserve existing natural habitats in human-dominated landscapes.