The Need to Quantify Ecosystem Services Provided by Birds

Abstract

WHAT ARE BIRDS worth—what is their actual dollar value to human society? To most of us in the ornithological community, birds are invaluable. But in these times we need more specific rationales to convince policy makers and business leaders to include bird conservation in land-use and development decisions. Over the past two decades, awareness of our dependence on a variety of ecosystem services (natural ecological processes that benefit human society) and of their importance and prevalence has progressed toward the goal of making conservation a mainstream value (Ehrlich and Kennedy 2005, Perrings et al. 2010, Rands et al. 2010, Sodhi and Ehrlich 2010). Building strategies for the protection of ecosystem services into conservation and land-use planning is essentially the promotion of human survival, although many policy makers misinterpret conservation efforts as luxury. Several previous reviews have identified ecosystem services that benefit human society (Costanza et al. 1997, Daily 1997, Pimentel et al. 1997, Sekercioglu 2010). The challenge, however, is to calculate the value of ecosystem services in meaningful and relevant ways that can be used to justify the protection of ecosystem services in land-use recommendations and policy decisions (Daily et al. 2000, 2009). As the case studies below illustrate, recent work on the ecosystem services provided by birds has made good progress toward this goal, but much remains to be done. Our objectives here are to describe the ecosystem services provided by birds, highlight recent steps toward quantifying those services, and, finally, suggest directions for future research. Overall, we emphasize that global efforts to conserve bird populations and sustain avian biodiversity also preserve the diverse ecosystem services provided by birds, thus contributing to human well-being. Ecosystem services are divided into four categories (Millenium Ecosystem Assessment 2003). Provisioning services refer to natural products that are directly used by humans for food, clothing, medicines, tools, or other uses. Cultural services provide recreational opportunities, inspiration for art and music, and spiritual value. Regulating services include pest control and carcass removal. Supporting services, such as pollination, seed dispersal, water purification, and nutrient cycling, provide processes essential for ecological communities and agricultural ecosystems. The Millennium Ecosystem Assessment's description of ecosystem services (Millenium Ecosystem Assessment 2003) is widely cited, but considerable debate continues on what constitutes an ecosystem service and how each should be quantified (Boyd 2007, Boyd and Banzhaf 2007, Matero and Saastamoinen 2007, Nijkamp et al. 2008, Bartelmus 2010, Farley and Costanza 2010, Kontogianni et al. 2010, Norgaard 2010, Wainger et al. 2010). The main issues include how to value nonmarket services, how to avoid double counting a process and its end product, and how to incorporate ecosystem valuation into policy and land-use decisions. We do not advocate any particular method of valuation here, but we argue that a consistent methodology for calculating units of ecosystem services is needed (as with any system of weights and measures; Boyd 2007). Birds are the best-known class of vertebrate animals, occur world-wide in nearly all habitats, and provide many services (Sekercioglu 2006a, b; Whelan et al. 2008). Thus, they are an ideal group to examine for ecosystem service valuation. Yet, surprisingly, little ornithological research has been done in an ecosystem-services context. Much ecosystem-services work has been focused on watersheds and insect pollination, perhaps because market value can readily be assigned to both fresh drinking water and agricultural crops that require pollination (Kremen et al. 2007, Brenner et al. 2010). Similarly, economic aspects of some cultural and provisioning services such as bird watching and hunting have been quantified (Sekercioglu 2002, LaRouche 2003, Leonard 2008, Carver 2009). Other historical and cultural aspects of birds have been reviewed and quantified in a general way (Diamond and Filion 1987, Podulka et al. 2004, Mynott 2009). Most of the important ecological roles that birds fill, however, involve supporting and regulating services, such as insect pest control and seed dispersal, and these types of services are the most difficult to quantify (Farber et al. 2006; Sekercioglu 2006a, b; Whelan et al. 2008, 2010). As we describe below, many of the most important ecosystem services that birds provide result from their foraging behavior. Through their foraging, birds act as mobile links that transfer energy both within and among ecosystems, and thus contribute to ecosystem function and resilience (Lundberg and Moberg 2003). We know that birds are important ecologically; the challenge is to quantify that importance in terms that are currently meaningful to humans. Pest control.—The regulating and supporting services provided by birds result mostly from foraging (i.e., consuming and processing resources; Table 1). The prime example is insectivory, which can provide the ecosystem service of pest control. More than 50% of bird species are predominantly insectivorous, and nearly 75% eat invertebrates at least occasionally (Sekercioglu 2006b; Table 1). The beneficial role of birds in consuming arthropods, and especially their responses to and influence on insect outbreaks (e.g., spruce budworms [Choristoneura spp.], cicadas [Magicicada spp.], and Mormon Crickets [Anabrus simplex]), is well documented (U.S. Biological Survey reports, summarized by Whelan et al. 2008). Furthermore, numerous studies in both natural and agricultural habitats show not only that birds reduce herbivorous insect populations, but also that plants respond with higher growth rates or crop yields (see Whelan et al. 2008: Table 1), a classic “trophic cascade” (Terborgh and Estes 2010). To cite an anecdotal example, the 1958 extermination campaign in China against the Eurasian Tree Sparrow (Passer montanus) ultimately contributed to insect pest outbreaks rather than rice yield increases, demonstrating indirectly that the sparrows' control of insects benefited the crop (Suyin 1959, Becker 1996). Other trophic cascades that involve birds potentially benefit agriculture, but they have seldom been studied. For example, although many raptors (both hawks and owls) consume rodents, we know of no study that has examined this predator-prey interaction from the perspective of economic value or trophic cascades. A few studies have directly assessed birds of prey as agricultural rodent-control agents, and the results are somewhat ambiguous. Wood and Fee (2003) reviewed measures to control rats in Malaysian agroecosystems, including deployment of nest boxes to raise populations of Barn Owls (Tyto alba). They concluded that the evidence was inconsistent and that the effect of owls warrants further investigation. Kay et al. (1994) reported that perches placed around soybean fields in Australia increased the number of diurnal raptors around and over the fields, which in turn decreased House Mouse (Mus musculus) population growth rate and maximum population density in the fields. Perches placed 100 m apart were more effective than those placed 200 m apart. Other studies demonstrated that providing artificial perches attracts various birds of prey, including American Kestrels (Falco sparverius), which also suggests that this method may enhance or concentrate foraging in potentially beneficial ways (Wolff et al. 1999, Sheffield et al. 2001). Clearly, more research is needed on the potential for birds of prey to drive trophic cascades in natural and agricultural ecosystems. The role of granivorous birds in control of agricultural weeds is essentially unknown, but one example is suggestive. In New Zealand, a granivorous bird introduced for aesthetic reasons, the European Goldfinch (Carduelis carduelis), destroyed 10× more seeds of the than a that was introduced to provide control of and In the of seed destroyed by at that to the seed to at the insect provided effective control and is that most species of avian are beneficial in agroecosystems, especially because most species also eat considerable of invertebrates the the most studies of are those on birds as agricultural et al. and and 1999, et al. and and 2004, and 2005, et al. 2008). research should examine more the and of avian in agricultural of pollination and seed have potentially on ecosystems. of bird species but also of and seed crops Sekercioglu is difficult to the number of species by birds, because of with and of many In the (i.e., and New of are species are to have the is for example, in New Zealand, are in of et al. and of all species but in only of the et al. a and which are in the and 2001). the most species and are and and et al. Thus, of all species have many of of species benefit from bird in terms of of from to or and and and and 2000, importance of categories among avian important an or at within on and from importance of categories among avian important an or at within on and from Birds the seeds of many species with value to humans for food, or other the dependence of these plants on birds for and the on the are in many The in of birds and have directly or indirectly from human and some have been from or have and 2003, Sekercioglu et al. 2004, and 2007, et al. 2008). plants are most at because they require which are more to and et al. 2009). As a the number of plants with few or no is especially on which have and ecological than (e.g., et al. 2010). of may a of the which can result in or in more the plants and 2003, et al. 2008, et al. and et al. and 2010). result in in rather than the of species and and et al. b; et al. et al. 2009). is how these populations, or that are important to humans. More work is needed to the ecological processes and their bird and species are in bird species and of and but recent evidence suggests that important The to be more than with seed dispersal, and the of a is to et al. For some plants in New Zealand, insects were as effective for birds, but do not this et al. et al. for some species with 2003). As with seed dispersal, may not of but we have few good measures of such especially in birds have rather than recent study a et al. a trophic in New of birds, in an in seed of the and a in The that have been made within a plants to be more than the of may be and for than for et al. 2004, 2010). pollination is by seed is the more at 2007). and nutrient ecological importance of birds is the that (i.e., and are for et al. (2003) demonstrated that and other vertebrate consume most in ecosystems. are one of the most types of birds to this is not by of the services they and other contribute to and nutrient et al. 2003). In to many other bird species at least including and et al. 2003). in are on and and and American and the most et al. 2003). More research is needed on the ecological of and on how these processes are by human such as and 2003, et al. and and which many and for Birds contribute to nutrient in all habitats, but most birds nest on and and nest in both in and on they process of in In this from the to the of can influence the and of communities of birds of a the et al. 2005, et al. 2010). Birds as ecosystem is the one supporting service provided by birds that not result from foraging but of that are used by many other in and to other include or and (see Ehrlich et al. and the most nest types and are over by and and and et al. animals, including insects and rodents, and other bird the of 2003). are used by other birds and by many other including and et al. 1997, and 1999, and are by many bird including and and thus nutrient (see and, they are used by many other including birds, and and are occur many ecological and respond to As in the bird provide links within and and can have on other The ecosystem services that birds provide are and or enhance other For example, insectivory, pollination, seed dispersal, and nutrient benefit plants that food, and and other for human Birds may act as that on which can result in prey population pest and in in the of ecosystem services, population among birds may to that and in to humans. the services are birds their services are in birds are only of any conservation by economic an of conservation in which a of species or other are the for conservation planning and land-use decisions. may be for bird conservation in some but to the has inconsistent in and of other species et al. 2008, et al. et al. 2010). that valuation of bird services the of ecosystem valuation and efforts as well as the to humans. the efforts to valuation research on many and important ecological The goal of the value of ecosystem services can be divided into is the need to describe and quantify the services at and The goal of ecosystem services is (Sekercioglu 2006a, b; Whelan et al. and we know considerable that are relevant to many ecosystem But we need more at from a variety of to global in this way we can the with (i.e., that value from one are to those at a et al. et al. 2010). from also an of the and of in ecosystem the in services among to more of the value of ecosystem services and more effective conservation we need to quantify the or of ecosystem services and to these with case we need to the from ecosystem services to a or of to how ecosystem services can be land-use or policy We need this of because a service (e.g., seed not be by but rather as of a conservation Several some ecological have been (Daily and 2008, et al. 2008, Daily et al. et al. 2009). Most of the supporting and regulating ecosystem services are not in and in that they are with the and value to all the value of some ecosystem services or may with of For example, at a may the birds to the that they or their thus the or for et al. As ecosystem services are to such as from other of a For example, by one may pollination or pest control for an is that the economic value in that are by (e.g., those by the and is not by or the value to the end as in the value. For all of these reasons, market (i.e., the of market value to is more the than the for ecosystem raise the of economic to issues et al. 2000, 2003, and in that ecosystem valuation is a toward the and natural A variety of have been used in valuation of ecosystem services (Farber et al. 2002, we the that are for quantifying services provided by of these are in that the is an economic value and the are to for an or valuation such as or have for but they have not been to the services The value of birds in pest control can be as the by birds of have been for et al. and insects and for this include the (e.g., crop from and on and natural of both insects and an of the that occur with no birds that the function of birds and yield the crop in the of birds, the of that of is the and an of the value of avian pest control. that this method well for agricultural crops or species for which we have both market and (e.g., and but not for most plants (e.g., et al. 2009). that this is no responses of the to the has that to et al. et al. but have not to do to birds because birds also but one that some of the market value of an end product, is valuation in which value is assigned on the of the economic that results from in For example, the value of of seeds by be on the value of the species they (see case study Similarly, the value of or a ecosystem The which an artificial system and human this to an or can yield that are essentially the to for an ecosystem service and with and are used to the economic of and other recreational uses. For example, in the more than for and 2003, Carver and be to to for 2003). pest control in can be habitats for birds, especially species that do not on and 2004, et al. foraging within is in the that over the and The are and in insect et al. many birds also to some on insects on the and have that bird foraging insect on in et al. et al. et al. et al. and et al. 2009). The is the most insect pest of in that birds reduce pest populations, and et al. 2008, et al. 2010). of the provided were by pest in the and of bird foraging and higher crop yields in the of birds into a dollar crop market Birds by on et al. and by on a et al. here and below, are in As of ecosystem services, birds are mobile and of the of ecosystem services by birds in some may on and To economic for conservation of birds and their habitats in agricultural not only the economic value of the ecosystem services provided by birds, but also bird and among agricultural and natural Several are for ecosystem services over a such as (Daily et al. and and studies have that an important pest the from diurnal foraging within to within natural et al. and foraging to and of within and results links the provisioning of an ecosystem service and natural both within and bird to of and of services, a can how in can the of services and be used by conservation to the economic value of habitats within agricultural and to provide economic of ecosystem services land-use for the services of Eurasian in were by et al. The of one of the in The as species that communities of and as well as birds and et al. In the of many of the and are more than of the in the most result from dispersal, by Eurasian that an of is and that most of the in the are currently et al. that the natural services of the be especially important for natural over The the value of one of two the of and the of They used from to quantify by Eurasian and the number of that from each and the of the concluded that the value of a of Eurasian was from on are and are the by in the these a value of to for and example is the economic value of seeds of by The of do not this on for and are important and with for but they contribute little or no seed and 2008, et al. 2009). an that and outbreaks of have in nearly this is currently for as a or species and 2010). The has that involve the of from seeds from (e.g., et al. 2010, and 2010). The of these efforts essentially the valuation of natural the of the the of from two the of with a density of a of the of seeds that be and in to from the seeds and from and in to the were by that of seeds for a be from only one although efforts require more Other such as and the of each from were the of and were services the a of in two this be within one used a study of the to the number of that from natural seed et al. 2001). concluded that a of to in the for to this is over may yield by over (e.g., of in a higher by including in that the both and by way of in of the recent of in because of the role that in et al. 2003, et al. 2004, et al. In the of on the for and were to other As a populations of and other and to humans and et al. that human to population of in over the cultural to the which on for et al. 2008). The of ecosystem services and case studies to some specific research that are More we on all the ways that birds contribute to ecosystem services that ultimately benefit humans. we know in general the types of ecosystem services that birds we of bird and to of ecosystem valuation in a relevant to human well-being. In to the more specific research below, a that has little in the ecosystem-services is the economic of some bird For example, some birds may be crop and and seeds or 1999, et al. or and in and research birds as agricultural has that can be than actual and or that the can be with also have beneficial such as and research on potential pest species to examine all the ecological roles that a bird in to the economic and a few bird species economic at the ecosystem the services provided by birds are (Sekercioglu 2006a, Whelan et al. 2008). More for ecosystem services are increased in and (e.g., 2008, Farley and Costanza 2010, et al. and the of ecosystem is also more et al. 2008, 2010, 2010). little of that however, has been focused on of services and and is important for to contribute to this of research in the Pest control.—The of pest control in need of further study is the to which trophic cascades have economic in terms of increased growth or agricultural We know that of bird foraging are but most studies are to two trophic birds and their More all trophic (e.g., and Whelan and 2002, et al. are especially in Similarly, et al. concluded that can populations of insect of but no studies have examined the economic to the of this the of bird of or for crop yield or be within agricultural to and is a prime example of an of research at the of rather than at or to be by of pest control that avian should be to is on natural avian population in from et al. 2007). on potential (e.g., in human by of those population on ecosystem function and of ecosystem services be and Other for research involve the and of that populations of avian pest (e.g., nest or their as pest (e.g., providing perches for of should be a of any pest we need of the of such at least in agroecosystems, and of bird control control with (i.e., studies that examine the of such incorporate from the of of et al. 2001). For example, perches may the of their increased thus their foraging, population not A few studies have that avian but these studies need to examine the on an agricultural crop or other are needed to seed in a variety of from natural communities to to In birds are (e.g., and of trophic function be for example, consume seeds of but may of pest and and pollination are to We need more on the from over the of the include how various including and seed and to how and seed and are both in the and in the and because these dependence on the of in services and its at the such as or other the of seed which pollination et al. and more studies to the importance of bird pollination to plants with that are to insect pollination in New et al. in other Birds seeds of and species and in some a role in the of plants and et al. 2002, et al. 2004, et al. 2005, and et al. 2007, and 2007). is not species may provide ecosystem services, such as control or The the of seed their The is further plants are by birds such as European in and European in New More work is needed on of species in an ecosystem-services As with other ecological we the we be to valuation the value provided by ecosystem services is most their The ecological and by the recent of populations in et al. have the importance of ecosystem services provided by is that in some ecosystem function is in on the of by or is a process by an for among and et al. 2003, et al. and and 2009). carcass of the vertebrate community, and other and all influence for et al. 2003). In some the for is from birds, toward insects and (e.g., et al. or (e.g., research at the which various consume be work links ecosystem and the population of various such as the system in into the of birds also our of et al. nutrient ecosystem types et al. and the of and their prey et al. Birds provide many ecosystem services, which by and are and Several of such services (e.g., in pest control in China were pollination in New provide a of the should such services be We suggest that ecosystem services be and to that humans to the and that birds to provide The case studies here show of but much work remains to be done. the role of birds as little research has been done on in an ecosystem-services and most of what has been done is on pest control in Similarly, the ecosystem service of seed has been quantified only for of plants by and of plants by have not been We are not of any ecosystem-services valuation research on the role of birds in nutrient or as ecosystem research to the economic value of birds policy and and justify bird conservation and ultimately the among human ecosystems, and the of avian is in on a at the in in We the of that for supporting our at the to and the group of for many on the is for from the New for and and of and for providing the with for to past research and on ecosystem the for