Why birds matter: from economic ornithology to ecosystem services

J Ornithol DOI 10.1007/s10336-015-1229-y REVIEW Why birds matter: from economic ornithology to ecosystem services Christopher J. Whelan1 • Çağan H. Şekercioğlu2,3 • Daniel G. Wenny4 Received: 1 January 2015 / Revised: 16 April 2015 / Accepted: 21 April 2015  Dt. Ornithologen-Gesellschaft e.V. 2015 Abstract Birds are conspicuous in many habitats, occur worldwide, are ecologically diverse, and are better known than other vertebrate groups. Birds devour pests, pollinate flowers, disperse seeds, scavenge carrion, cycle nutrients, and modify the environment in ways that benefit other species. Investigation of these ecosystem functions directly as ecosystem services has grown immensely over the last two decades and the ecological relevance of birds is well established. Birds are also observed, fed, and used as artistic and spiritual inspiration by millions of people around the globe. Yet the economic relevance of birds is not widely appreciated and the economic relevance to human society of birds’ ecological roles is even less understood. Quantifying the services provided by birds is crucial to understand their importance for ecosystems and for the people that benefit from them. In this paper, we briefly review the rise and fall of economic ornithology and call for a new economic ornithology with heightened Communicated by E. Matthysen. & Daniel G. Wenny dandroica@gmail.com Christopher J. Whelan whelanc@uic.edu Çağan H. Şekercioğlu c.s@utah.edu 1 Illinois Natural History Survey, c/o University of Illinois at Chicago, Chicago, IL, USA 2 University of Utah, Salt Lake City, UT, USA 3 College of Sciences, Koç University, Rumelifeneri, Sariyer, Istanbul 34450, Turkey 4 University of California-Berkeley, Museum of Vertebrate Zoology, Berkeley, CA, USA standards and a holistic focus within the ecosystem services approach. Birds’ ecological roles, and therefore, ecosystem services, are critical to the health of many ecosystems and to human well-being. By understanding and valuing bird services and disservices through careful natural history research, we can better assess the environmental consequences of bird declines and extinctions and communicate these findings to the public and policy makers, thereby increasing public support for the conservation of birds and their habitats. Keywords Ecosystem services
Pest control
Pollination
Ecological economics
Economic ornithology
Disservices
Natural history
Seed dispersal
Scavenging
Predation Introduction ‘Nature conservation’ is often thought as something that happens ‘‘out there’’ in reserves rather than something integral to daily life. This view reinforces the misconception that people are apart from the natural world, leading to many of the environmental issues we face today. However, protecting biodiversity and ecosystems is essential for human society, and therefore should be incorporated more directly into public policy, development plans, and daily life (Hackett 2011; Kareiva et al. 2011; Lovins et al. 1999; Whelan et al. 2010), which means we must understand the value of biodiversity for human society. In this paper, we outline a framework for investigating and assessing the value of birds for human society. One of the earliest examples of such an effort was in the USA, when the United States Department of Agriculture (USDA) started to assess the economic impact of birds and 123 J Ornithol mammals on agriculture in the late 1800s (see below). These efforts dwindled by the 1930s, as most species were found to be beneficial or not harmful. Since then, most economic aspects of wild animal ecology have been ignored, a problem exacerbated by the decline in funding for, and instruction in, natural history and organismal ecology (Tewksbury et al. 2014). More recently, growing awareness of the importance of ecosystem function to human society (ecosystem services, ES) has led to a renewed effort to assess the ecological and economic value of biodiversity and ecosystems (Hocking and Babbitt 2014; Losey and Vaughan 2006; Muscarella and Fleming 2007; Sekercioglu 2010; Wenny et al. 2011; Whelan et al. 2008). Here, we describe the roots of ES in economic ornithology of the late nineteenth and early twentieth centuries, outline the recent work on understanding ES provided by birds, and provide a framework for the redevelopment of economic ornithology research within the field of ecosystem services. Ecosystem services are defined as ‘‘the set of ecosystem functions that are useful to humans’’ (Kremen 2005). The history of ecosystem services has been explored in depth elsewhere (e.g., Daily 1997; Gomez-Baggethun et al. 2010). The number of scientific papers on ecosystem services has increased dramatically in the past two decades. The Millennium Ecosystem Assessment (MEA 2005) brought ecosystem services to the attention of governments (Gomez-Baggethun et al. 2010). The MEA (2005) aimed to evaluate the potential consequences of ecosystem change from a human well-being perspective and with an emphasis on ecosystem services, and identified four classes of ecosystem services: provisioning services, cultural services, regulating services, and supporting services. Birds contribute all four types of ecosystem services (Sekercioglu 2006a; Whelan et al. 2008). Provisioning services are provided by both domesticated (poultry) and non-domesticated species. Birds have long been important components of human diets for subsistence, consumption, and sport (Moss and Bowers 2007), particularly waterfowl (Anatidae) and terrestrial fowl (Galliformes; Peres 2001; Peres and Palacios 2007). Bird feathers provide bedding, insulation, and ornamentation (Green and Elmberg 2014). Through their unique salience for humans, birds offer a significant focus for studies of cultural services within the ES paradigm, and this is the field of ethno-ornithology (Cocker and Tipling 2013; Podulka et al. 2004; Tidemann and Gosler 2010). Bird-watching is one of the most popular outdoor recreational activities in the United States and around the world (Kronenberg 2014a; Ma et al. 2013; Sekercioglu 2002; White et al. 2014), and has direct economic benefits as well as indirect benefits through numerous citizen science programs involving bird-watchers (Greenwood 2007). Numerous bird species contribute regulating and supporting services via their foraging 123 ecology. These services include scavenging carcasses, nutrient cycling, seed dispersal, pollination, and pest control (Sekercioglu 2006a; Whelan et al. 2008). Here, we focus on regulating and supporting services because the benefits of these services are often transmitted indirectly to humans, and are thus poorly understood in terms of their contribution to human well-being. Many of the ecosystem services provided by birds arise through their ecological functions. Estimating their value thus necessitates sound knowledge of the natural history of the species involved (Sekercioglu 2006a, b; Wenny et al. 2011; Whelan et al. 2008). Most regulating and supporting services arise via top-down effects of resource consumption. With over 10,000 bird species on earth, birds consume a wide variety of resources in terrestrial, aquatic, and aerial environments. Sometimes the consumed resource is a pest of agricultural crops or forests. In other cases, bird resource consumption facilitates pollination or seed dispersal, promoting successful plant reproduction in thousands of plant species. For economically or culturally significant plants, these services benefit humans, who also benefit indirectly from the myriad ES provided by forests and other plants. Through these services, birds have a large, global, but rarely quantified impact on ecosystems. We urgently need to develop methods to quantify avian functions, services and their values, based on a thorough understanding of their natural history particularly habitat requirements, reproductive ecology, resource exploitation, and interactions with competitors, predators, and parasites. The rise and fall of economic ornithology Early efforts to understand bird impacts focused predominantly on direct interactions as crop pests or game species. Although not recognized formally as ecosystem services, the notion that humans may gain benefits from nature was accepted by students of natural history. In the US, early studies on food habits of native fauna and systematic expeditions cataloging wildlife and flora in North America and around the world grew into a burgeoning discipline known as ‘‘economic ornithology.’’ Embraced enthusiastically by naturalists at the end of the nineteenth century, economic ornithology experienced first a meteoric rise that was matched by a rapid demise. For ornithologists, important lessons can be gleaned from this history. Until fairly recently, birds and other wildlife were largely viewed in economic terms as pests, food, or irrelevant. Even today, agricultural birds are often viewed as pests, whether or not they cause any measurable impact (Lindell et al. 2012). Interest in positive and negative roles of birds spurred the US Congress to appropriate $5000.00 to the USDA to establish a section of economic ornithology J Ornithol in 1885 to investigate the diet, movements and other habits of birds in relation to both insects and plants. The section grew quickly, graduating into the Division of Biological Survey in 1896 and the Bureau of Biological Survey in 1905. Early work concentrated on bird-agriculture relationships, with an emphasis on agricultural production. A goal of the division was to supply the growing agricultural industry with useful information. Consequently, initial work concentrated on food habits of birds believed to be injurious or beneficial to agriculture. Similar efforts in the UK started at the same time (Kronenberg 2014b). Between 1885 and 1929, Bureau of Biological Survey researchers contributed hundreds of publications intended for a wide audience (Fisher 2011). Although the Bureau’s early work was generally received enthusiastically, criticism of methods and skepticism regarding conclusions grew. Three important flaws contributed to the eventual decline of economic ornithology within the Biological Survey. First, when Bureau scientists assessed diet through analysis of stomach contents, they mostly used the volumetric method to describe importance of the different components of the diet. In this method, relative bulk representation determines the importance of any component within the diet. The alternative numeric method, which ultimately gained favor in the larger ecological community, instead determined importance of items by frequency of occurrence. Second, a conclusion that a particular bird species (or group of species) was beneficial to agriculture was seldom followed up with practical advice promoting strategies aimed at enhancing the positive bird effects through some practical manipulation that farmers could implement (Evenden 1995). Third, and most importantly, presence of a prey species (arthropod or rodent) in the diet does not indicate how this affects the population dynamics of that species. Consumption of a pest by a bird consumer does not demonstrate avian control of that pest, leading some entomologists to contend that economic ornithologists over-stated the importance of birds as control agents. Paradoxically, coincident with the fall of economic ornithology and the rise of synthetic organic pesticides, studies from the 1940s through the 1960s that examined birds in relation to agriculture emphasized birds’ potential roles as pests rather than as pest control agents (Evenden 1995). As reviewed by Bruns (1960), interest in the economic importance of birds in Europe developed during the 1920s, and appears to have followed a somewhat different trajectory from that in the US. Motivated by an interest in economic bird protection, a variety of investigations sought to quantify food habits of birds. Investigators focused particularly on the relative consumption of beneficial versus detrimental insects, what quantities they consumed, and the relation of insect consumption to insect abundance. Additional work examined the ability to increase bird density through provisioning of nest boxes. A key difference in these European investigations from the earlier North American studies was a greater attempt to relate consumption to abundance. The many studies summarized by Bruns (1960) revealed that birds often consume a large percentage of available insects when insect densities are low, but that during insect irruptions the proportion consumed may be miniscule. In contrast to earlier views, Tinbergen (1949, in Bruns 1960) and others found that many insect-consuming forest bird species exhibit pronounced selectivities for certain insects. Moreover, many species besides cuckoos were found to consume hairy caterpillars, and one study (Koroljkowa 1956, as reported in Bruns 1960) found that birds preferentially consume caterpillars of the gypsy moth (Lymantria dispar) that were unparasitized. Some studies that provisioned areas with nest boxes led to surprising increases in density of some hole-nesting species, even when those areas were at already high densities. Areas with increased bird densities in response to nest box provisioning in turn were found to have decreased densities of harmful insects. Taken as a whole, Bruns (1960) concluded that the role of forest birds in ‘‘forest hygiene’’ is most effective at maintaining harmful insects at benign densities: ‘‘The birds generally are not able to break down an insect plague, but their function lies in preventing insect plagues. It is our duty to preserve birds from aesthetic as well as economic reasons…the wood is still able to defend itself biologically against insect plagues. It is our duty to further these biological forces (birds, bats, wood ants, parasites) and to conserve or create a rich and diverse community. By such a prophylactic, carrying out of ‘hygiene’ before a possible outbreak of an insect pest, the forests will be better protected than by any other means.’’ Interest in birds’ ecological roles increased again in the 1970s, owing to comprehensive studies of ecosystem energetics. Although notable investigations (Holmes and Sturges 1975; Sturges et al. 1974; Wiens 1973) suggested that birds may contribute little to overall ecosystem energy flux, exclosure studies demonstrated that bird predation significantly affected population densities (and, presumably, population dynamics) of arthropods, including some pests (Askenmo et al. 1977; Holmes et al. 1979; Solomon et al. 1977). Subsequent studies determined that predation of insectivorous birds on herbivorous insects positively affected plant performance (Atlegrim 1989; Marquis and Whelan 1994). In contrast to the methods of economic ornithology, these studies explicitly examined the trophic interactions 123 J Ornithol from the plant’s perspective, addressing whether bird predation on insect herbivores increased plant performance or fitness. These studies also ushered in renewed interest in birds as potential biological control agents in both natural and agro-ecosystems. Investigators today typically focus data collection on a direct or indirect assessment of plant performance, fitness, and in some circumstances, economic consequences for humans. For instance, Mols and Visser (2002) investigated effects of bird control of herbivorous insects in Dutch apple orchards, and reported that increasing bird density through deployment of nest boxes led to a 50 % reduction in apple damage and an increase of about 60 % in total apple crop yield. Koh (2008) attributed bird pest control to prevention of 9–26 % fruit loss in oil palm (Elaeis guineensis). Johnson et al. (2009) found birds significantly reduced damage by coffee berry-borer beetles (Hypothenemus hampei), with higher coffee yields resulting in increased income from US$44 to US$310/ha. Avian ecosystem services: a modern economic ornithology In light of modern approaches to avian ecology and renewed interest in avian ecological function and ecosystem services, economic ornithology deserves further development, with both a broader focus and more rigorous methodologies. The need for reliable quantitative assessment of bird-caused losses of agricultural production is necessary to assure that costs of damage prevention do not actually exceed the costs resulting from reduction in crop yield. In addition, potential disservices associated with provision of a service need to be more fully incorporated into modern ecosystem service research (Table 1). To date, most ES research has focused on the benefits provided and has ignored disservices (Kronenberg 2014b). Finally, quantifying the services and disservices is just one component of ES valuation. As we show below, some of the ES provided by birds have no direct market value, and even those that can be monetized may have additional nonmarket value. Reliance on market value to justify conservation policy is risky, because markets can change quickly, as seen when the development of pesticides appeared more effective than birds in pest control. On the other hand, attempts to assess non-market value are often ignored or criticized precisely because they do not have traditional assessment for market value (Johnson and Hackett 2016). Keeping in mind Bruns’ (1960) admonition that we must preserve birds for aesthetic as well as economic reasons can help guide holistic approaches to avian conservation that recognize birds as more than simple pawns of economic cost-benefit assessments. 123 Pest control A pest species decreases fitness, population size, growth rate, or economic value of a human resource, such as an agricultural crop. Many bird species may be observed in gardens and agricultural fields, leading to a perception that these species are raiding our gardens or crops as pests. For such a species to function as a pest, however, it must not only consume the crop, its consumption must be sufficiently large to reduce the resource’s value. This reduction may be quantified in a variety of ways, from the yield and/ or the monetary value earned from harvest, to the number of calories delivered to potential consumers. Pest control reduces the effect of a pest, thereby increasing fitness, population size, growth rate, or economic value of a resource important to humans. Pest control results from a direct negative effect of a pest control agent on the pest, producing a positive indirect effect on the resource consumed by the pest to an extent that is economically important to humans. Insects More than 50 % of bird species are predominately insectivorous, and nearly 75 % eat invertebrates at least occasionally (Sekercioglu 2006b; Wenny et al. 2011). Many studies have now examined top-down effects of birds on invertebrates in a wide variety of natural and agro-ecosystems (Whelan et al. 2008). Most, though not all, of these investigations have found that birds reduce population densities of invertebrates. Of these studies, many found that the top-down effects on invertebrates cascade to the level of the plants (Mantyla et al. 2011; Whelan et al. 2008). Small mammals Less studied are the potential roles of birds of prey as pest control agents of small mammals such as rodents and rabbits, and granivorous birds as pest control agents of agricultural weeds (Whelan et al. 2008). Although few studies since the early work of the Biological Survey have examined the potential of birds of prey to contribute pest control services in agro-ecosystems, current information suggests a strong potential. Birds of prey affect population dynamics of various rodent and other small mammal species in a variety of ecosystems around the world (Korpimaki and Krebs 1996), and many raptor species inhabit agricultural ecosystems (Williams et al. 2000). Furthermore, the very presence of predators in an ecosystem reduces the activity of prey species as a result of the creation of a ‘‘landscape of fear.’’ This effect has been shown to J Ornithol Table 1 Framework for ecosystem services research from an ecological perspective Ecosystem service Functional group Potential disservices Pest control (invertebrates) Insectivores Prey upon beneficial insects Pest control (small mammals and birds) Carnivores (raptors) Prey upon poultry and game species Weed seed control Granivores Crop damage Seed dispersal (fleshy fruits) Frugivores Spread invasive species Seed dispersal (aquatic) Waterbirds Dispersal of weed seeds Fruit crop damage Spread invasive species Habitat damage (tundra) Seed dispersal (nuts) Seed-caching birds Crop damage Pollination Nectarivores Pollinate invasive plants and help their spread Nutrient cycling Piscivores Prey upon game fish Plant damage in breeding or roosting colonies Waste removal Scavengers Spread disease Eutrophication of aquatic habitats Nutrient cycling Disease control Most previous research has focused on the positive benefits of ecosystem services (left column), but potential costs (right column) of the service should also be studied reduce rodent activities when barn owls are present (Abramsky et al. 1996). Deployment of hunting perches boosts populations and/or activity-density of various hawks and owls (Kay et al. 1994; Sheffield et al. 2001; Wolff et al. 1999), leading, in some cases, to decreased rodent population density (Kay et al. 1994). Existing evidence thus suggests that birds of prey have the potential to provide pest control services in agro-ecosystems, and the deployment of perches and nesting structures facilitates recruitment of those services. Agricultural weeds Since the studies of Judd (1901, 1902), almost no effort has been made to assess the role of granivorous birds in the abundance and distribution of herbaceous agricultural weeds (Holmes and Froud-Williams 2005; White et al. 2007). Numerous bird species around the globe are seasonally granivorous, and many of these species consume seeds of native forb and grass species, some of which are weeds in agro-ecosystems. Barrows (1889) and Judd (1901, 1902) suggested that native avian granivores in the U.S. may preferentially consume seeds of native herbs and forbs, even as the non-native house sparrow (Passer domesticus) prefers seeds of commercial cereal grains. This is an area that deserves careful, quantitative research. Given that many of the passerine granivores are seasonally insectivorous (during their breeding seasons) or granivorous (non-breeding season), they potentially could serve as both insect and weed seed pest control agents (e.g., Ndang’ang’a et al. 2013). Various impact studies could be usefully implemented. For instance, some bird species, such as the American goldfinch (Spinus tristis) in North America, often forage on seeds before dispersal (pre-dispersal seed predation), while others seem to forage on seeds post-dispersal. What is the relative magnitude of seed losses of these two processes? Are they additive or compensatory? Can we manipulate agricultural landscapes in ways that might encourage granivorous bird species’ habitat use without sacrificing agricultural yield and efficiency and/or facilitate their effectiveness as granivores (as has been demonstrated for granivorous insects—see Landis et al. 2010)? Disservices: crop damage Crop damage by birds is arguably their most recognized ecosystem disservice, but the economic losses resulting from birds are not well quantified. Frequently the perceived extent of crop loss or damage, as indicated by opinion surveys, is much greater than the actual losses measured in the field (Gebhardt et al. 2011). Similarly, the perception that bird presence in an agricultural field indicates crop damage by those species is often incorrect (Greene et al. 2010; Lindell et al. 2012). For instance, based on energetics and population size estimates, Weatherhead et al. (1982) estimated that damage to corn based on subjective governmental surveys over-estimated crop losses astronomically (10009). Energetics estimates were well within empirically based, replicated field estimates (Weatherhead et al.: 0.41 % of crop damaged; field 123 J Ornithol estimates: 0.25–0.80 % crop damaged). Basili and Temple (1999) estimated comparable magnitudes of regional losses of sorghum (0.37 %) and rice (0.73 %) crops owing to dickcissel (Spiza americana) wintering flocks in Venezuela, contrasting with the subjective impression among area farmers of an average loss of 25 % of either crop. Subjective impressions and estimates of crop loss are easily exaggerated due to the size of wintering bird flocks, their conspicuousness and highly localized concentrations. Overall, crop losses due to birds are probably fairly low, especially when compared with damage caused by rodents and insects. Similarly, the red-billed quelea (Quelea quelea), an abundant granivorous species widely considered a crop pest in Africa, may cause high crop damage locally, but cause \1 % loss of continental production (Elliott and Lenton 1989). For example, red-winged blackbirds (Agelaius phoeniceus) feed on pre-harvest corn kernels for a short period in the fall, causing some crop loss (Dolbeer 1990; McNicol et al. 1982). However, measured crop damage was \1 %, far below government estimates of about 20 % crop damage (Weatherhead et al. 1982), and was primarily in fields near wetlands and blackbird fall roosting sites. Most importantly, blackbirds eat substantial amounts of invertebrates, especially during the breeding season when corn kernels are developing. These invertebrates include corn insect pests that cause far more crop damage than blackbirds (Bendell et al. 1981; Tremblay et al. 2001). In the 30 years since these studies, less palatable corn varieties have been developed that likely reduce blackbird damage to corn even further, and anthraquinone-based repellent reduced blackbird damage to corn by 28 % (Carlson et al. 2013). A recent study in North Dakota showed that a mean of 0.2 % of the corn crop in randomly selected plots was damaged by blackbirds in 2009–2010 (Klosterman et al. 2013). Similar results have been found for other crops. For example, blackbirds had no effect on stink bugs on rice and caused damage themselves, but this did not result meaningful reduction in crop yield (Borkhataria et al. 2012). Nevertheless, some parts of fields can have [10 % damage (Conover 1984), and in some cases, even slight damage can prevent corn from being sold for human consumption (Dolbeer 1990). A critical research need is to examine in detail the entire life cycle of key ‘‘avian pest’’ species, quantifying both the negative and positive effects of their habit use and foraging behavior on agricultural crops. Such studies also need to account for the economic and ecological costs of avian and non-avian pest control measures. Such detailed analyses may well demonstrate that the cost of avian pests is usually less than what farmers perceive (e.g., Basili and Temple 1999), and that avian ‘‘pests’’ in fact provide benefits to the farmer. Furthermore, the invertebrates likely cause far 123 greater damage to crops than do birds, so attempts to control perceived avian pests may backfire and lead to greater crop damage by invertebrates (Becker 1996). Studies should also examine the costs and consequences of controlling the pest species. For example, efforts to control queleas with lethal means may have a short-term benefit for local crop production, but longer-term negative consequences (both direct and indirect) on non-target bird species and even on humans (Jaeger and Elliott 1989; McWilliam and Cheke 2004; Meinzingen et al. 1989). Disservices: birds feeding on beneficial insects Not all bird-insect interactions are beneficial for farmers. Insect pest populations may also increase as a result of birds feeding on predaceous insects and parasitoids (Sekercioglu 2006a). However, Hooks et al. (2003) found that excluding birds did not increase spider predation of herbivorous insects. Actually, birds alone were significantly better at controlling insects and reducing plant damage than spiders alone, with 18 % of plants showing extensive defoliation with only spiders versus 0 % with only birds. Although birds may reduce numbers of insect parasitoids (Tscharntke 1992) by feeding on infected insects, various lepidopteran parasitoids only emerge from the pupal stage and thus cannot prevent defoliation by the caterpillars (Hooks et al. 2003). Parasites may actually lead to increased foliage consumption (Coleman 1999). Various bird species often complement other natural enemies by selecting for non-parasitized individuals (Otvos 1979) and facilitating the spread of viruses (Takekawa et al. 1982). On the other hand, bell miners (Manorina melanophrys) are an unusual species that causes infestations of an insect herbivore (Loyn et al. 1983). These highly territorial birds mostly feeds on the nymphs, sugary exudates, and lerps (protective carbohydrate covers) of psyllid homopterans, the birds often being careful only to remove the lerps with their tongues without disturbing the nymph (Loyn et al. 1983). This ‘‘tending’’ behaviour, combined with bell miners’ aggressive group territorial defense, can result in psylid infestations of Eucalyptus trees, sometimes resulting in their defoliation and death (Loyn et al. 1983). Seed dispersal At least 33 % of bird species disperse seeds, primarily through fruit consumption, but also through herbivory and granivory by waterbirds, and scatter-hoarding of nuts and conifer seed crops by seed-caching birds (Sekercioglu 2006b; Whelan et al. 2008). With the exception of birds dispersing mistletoes, most bird dispersers interact with most plant species in a generalized or diffuse manner. A J Ornithol single bird species consumes fruits of many plant species, and the fruit of a single plant species is consumed by many bird species. The number of plant species dispersed by birds is not precisely known, but our working estimate is 80,000 (*30 %) species of angiosperms and 650 (*60 %) of gymnosperms (Green et al. 2016; Tomback 2016; Wenny et al. 2016). Fleshy fruits Birds are ideal seed dispersers. Frugivorous species typically swallow fruits and seeds intact. Birds are highly mobile and many migrate long distances. Birds occur nearly everywhere and provide mobile links within and among habitats. In most cases, seeds cannot germinate from within an intact fruit. An additional and frequently overlooked benefit of endozoochory is the removal of fruit skin and pulp from the seeds during the interaction (Samuels and Levey 2005; Traveset and Verdu 2002). Consequently, any bird–plant interaction involving seed handling or ingestion potentially benefits the plant. Some frugivorous bird species are considered pests of fruit crops, including grapes (Vitis), blueberries (Vaccinium), strawberries (Fragaria), among others (De Grazio 1978; Greig-Smith 1987). Other frugivorous bird species disperse invasive plant species. Like granivorous species, however, many frugivore species also eat many invertebrates during the breeding season. The relative costs and benefits of such diet switching have not been evaluated for any species in an ecosystem services context. Aquatic plants Although the role of waterfowl as seed dispersers was recognized decades ago (Ridley 1930), only recently has the ecology of this interaction been studied. Waterfowl (Anatidae; *150 species) occur worldwide, are migratory or otherwise capable of long-distance movements, and many species are largely vegetarian. Thus, waterfowl can be highly effective mobile links within and among wetland habitats (Green and Elmberg 2014). Seed caching Approximately 20 species of pines (Pinus) are dispersed by jays and nutcrackers (Corvidae; Tomback and Linhart 1990). These pines occur in western North America and across Eurasia and are distinguished from the primarily wind-dispersed species by having large seeds that lack a well-developed winged appendage for wind dispersal and cones that require seed removal by animals (Tomback and Linhart 1990). Corvids also disperse oaks and beeches (Fagaceae) by scatterhoarding. Although the presumed mutual adaptations in these species are less clear than for nutcrackers and pines, many seeds are cached in suitable sites for germination and establishment. Disservices: seed predation and dispersal of invasive species Some granivorous birds, such as finches and parrots, can be significant seed predators (Sekercioglu 2006a). Red crossbills (Loxia curvirostra) in Spain consume more than 80 % of the ripening seeds of relict Scots pines, whose regeneration is limited by the high rate of seed predation (Castro et al. 1999). Avian seed predation may increase in tropical forest fragments, since many tropical granivorous birds are more common in forest fragments and outside forests than in extensive forest (Bregman et al. 2014; Sekercioglu 2012). In the forest fragments of southeast Brazil, where rodent seed predators have declined and granivorous birds have increased, birds have become important, if not the main seed predators of Croton priscus (Euphorbiaceae) (Pizo 1997). As detailed above, although birds can be crop pests, damage estimates are often exaggerated and not collected scientifically (Weatherhead et al. 1982). Introductions of non-native species can turn avian seed dispersal service into a disservice. Avian seed dispersers can contribute to the spread of invasive species with generalized dispersal mechanisms (Renne et al. 2002). In the Usambara Mountains of Tanzania, silvery-cheeked hornbills (Ceratogymna brevis) are effective long-distance (up to four km) dispersers of the exotic Maesopsis eminii (Rhamnaceae) (Cordeiro et al. 2004), and significantly contribute to the rapid invasion of this West African species, which is also dispersed by Ceratogymna hornbills in its native habitat (Holbrook and Smith 2000). Pollination Over 920 species of birds pollinate plants, including hummingbirds (Trochilidae) in the Americas, sunbirds (Nectarinidae) in Africa, false-sunbirds (Philepittidae) in Madagascar, flowerpeckers (Dicaeidae) and white-eyes (Zosteropidae) in southern Asia, Honeyeaters (Melphagidae) lories (Loridae) in Australasia, and Hawaiian honeycreepers (Drepanididae) in Hawaii (Stiles 1981). In contrast to seed dispersal, birds pollinate a relatively small percentage of plant species (Sekercioglu 2006a; Whelan et al. 2008). However, in some parts of the world like Australia and certain oceanic islands, avian pollination reaches important levels and can exceed 15 % of the plant species in a community (Anderson et al. 2016). Compared to seed dispersal limitation, there have been far fewer studies of the importance of avian pollination limitation, 123 J Ornithol which can result in reduced seed set and long-term population declines, especially in island communities with a high proportion of avian pollinators, such as New Zealand (Kelly et al. 2010), Bahamas (Rathcke 2000) or Hawaii (Sekercioglu 2006a). ecology of both humans and wildlife, and additional research in this area is critically needed. Disservices: pollination of invasive species and nectar robbing Birds contribute to nutrient cycling in all habitats, but most impressively where aquatic birds nest colonially on islands (Anderson and Polis 1999; Polis and Hurd 1996). Seabirds often nest in dense colonies both in coastal areas and on islands, processing large amounts of food in small areas. The result is significant input of nutrients from the aquatic zone to the terrestrial zone. Such large inputs of phosphaterich guano can influence the structure and composition of plant communities (Ellis 2005), and guano has historically been of great economic value both as a fertilizer and in manufacture of munitions. Because phosphorous has no gaseous form at ambient temperatures, it does not move from aquatic to terrestrial ecosystems through atmospheric processes, and transport via piscivorous birds is thus critical over short time horizons. As is the case with seed dispersal, some birds help spread invasive plant species by pollinating them, especially in places like Hawaii where there are many introduced bird and plant species. Furthermore, some ‘‘nectar robbers’’ can access nectar without pollinating the plants (Proctor et al. 1996; Sekercioglu 2006a). The quality of an avian pollinator is often correlated with its bill length. Some of the shortest billed hummingbird species, such as the thornbills (genus Chalcostigma) and fiery-tailed awlbill (Avocettula recurvirostris), as well as passerine flowerpiercers (genus Diglossa), are mainly nectar robbers, using their sharp bills to pierce flower corollas and consume nectar without providing any pollination in return. Interestingly, nectar robbing may sometimes have little to no negative effect on plant fitness, and may even result in some pollination (see Sekercioglu 2006a for references). Scavenging The ecological importance of scavenging birds is often underappreciated. Despite the common assumption that decomposers (i.e., microbes and insects) are primarily responsible for recycling carrion biomass, DeVault et al. (2003) demonstrated that vultures and other vertebrate scavengers usually consume most available carcasses in terrestrial ecosystems. Although vultures are one of the most recognizable types of birds to non-ornithologists, this familiarity is often not accompanied by appreciation of the services they provide. By scavenging, vultures and other carnivorous vertebrates contribute to waste removal, disease regulation, and nutrient cycling (DeVault et al. 2003; Houston 1979). Disservices: spreading disease Although avian scavengers are generally found to decrease disease propagation, in some circumstances they may instead have the opposite effect (see Jennelle et al. 2009). For instance, the survival of scrapie prions of passage through the digestive system of American crows (Corvus brachyrhynchos) may facilitate proliferation of prion diseases (VerCauteren et al. 2012). However, relatively little is known about how avian scavengers influence disease 123 Nutrient cycling Disservices: eutrophication Avian nutrient transport can sometimes affect ecosystems negatively (Sekercioglu 2006a). Aquatic systems, especially ponds and wetlands, and small lakes, may experience eutrophication owing to massive inputs of nitrogen and phosphorus from bird excrement (Kerbes et al. 1990; Manny et al. 1994; Post et al. 1998). Excessive terrestrial nutrient deposition can inhibit plant growth (Gillham 1960) and even cause plant death. Abundance and species richness of invasive plant species may increase in areas of greatest intensity of bird colonies (Vidal et al. 2003), since these plants often have high disturbance tolerance and colonizing capacity. Large concentrations of ducks and geese can add excessive amounts of nutrients to wetlands, parks, and other open areas, reducing water quality, destroying vegetation, creating pollution, and even causing disease outbreaks (Post et al. 1998). Manny et al. (1994) calculated that of all outside nutrients that entered Michigan’s Wintergreen Lake, waterfowl added 69 % of carbon, 27 % of nitrogen, and 70 % of phosphorous, the last two of which can lead to eutrophication. Conclusions Keeping in mind the decline of Economic Ornithology in the early twentieth century, efforts to modernize the field today must ensure that the approach is rigorous, repeatable, and focused on tangible measures of the direct and indirect benefits to human society (Kronenberg 2014b; Whelan J Ornithol et al. 2008). Bird contributions to ecosystem service and disservice with respect to the replacement of the service by human labor or technology may be compared with costbenefit analysis (e.g., bird predation versus pesticides for pest control). Investigations or methods that permit scaling up from experimental plots to entire ecosystems (Rogers et al. 2012; Whelan et al. 2008) are critical. We have made considerable progress in building conceptual frameworks for economics of ecosystem services. Important considerations include whether the bird species responsible for the service is unique or part of a redundant network (Power et al. 1996). Regardless of redundancies, several studies indicate the importance of species richness for delivery of ecosystem services, implying that, even with redundancies, each species counts (Barbaro et al. 2014; Cordeiro and Howe 2003; Garcia and Martinez 2012; Kelly et al. 2010). Also critical is the temporal and spatial scale over which any potential service is generated (Chee 2004). Ecosystem service accounting needs to consider the intrinsic variability inherent in the production of any ecosystem service. Ecosystem processes naturally vary over time. Understanding natural variability is thus critical to the proper accounting of ecosystem services (MEA 2005). Avian ecologists have made great strides in understanding and documenting the many ecosystem services provided by birds, yet knowledge gaps persist and need filling. We know appreciably more about how birds function as consumers of arthropods and fruits than as consumers of nectar. We thus know more about how birds function as pest control agents of herbivorous insects and as seed dispersers, respectively, than as pollinators. Additional research regarding which plant species are pollinated by which bird species, and the effectiveness of birds relative to other pollinators, is critical. More research on avian granivory in agro-ecosystems, particularly with respect to seasonal switching of diet between seeds and arthropods, is also needed. When birds contribute multiple ecosystem services (e.g., reduction of weed seed in nonbreeding season and insect pest control in breeding season), we must determine the relative demographic impacts of each service. The same holds when different co-occurring species contribute such different ecosystem functions and services. Rarely if ever do we know the demographic contribution of birds for any one of these roles, let alone their synergistic (or antagonistic) effects. Cost–benefit analysis should be applied when alternative ecosystem ‘‘components’’ might be available (use of pesticides versus encouragement of bird predation). Rapidly changing climate and other types of global change are forcing shifts in the distributions of birds, plants, and other species, resulting in new ecological interactions, particularly in the understudied tropics that host most of the world’s bird species (Sekercioglu et al. 2012; Sodhi et al. 2011; Wormworth and Sekercioglu 2011). Ecologically specialized bird species are substantially more threatened with extinction and we still know little about the ecological consequences of bird extinctions. A better understanding of birds’ ecological functions and services is urgently needed for conserving bird populations and their ecological contributions. Conflict of interest of interest. The authors declare that they have no conflict References Abramsky Z, Strauss E, Subach A, Kotler B, Riechman A (1996) The effect of Barn Owls (Tyto alba) on the activity and microhabitat selection of Gerbillus allenbyi and G. pyramidum. Oecologia 105:313–319 Anderson S, Kelly D, Robertson A, Ladley JJ (2016) Pollination by birds: a functional evaluation. In: Sekercioglu CH, Wenny DG, Whelan CJ (eds) Why birds matter: avian ecological functions and ecosystem services. University of Chicago Press, Chicago (in press) Anderson WB, Polis GA (1999) Nutrient fluxes from water to land: seabirds affect plant nutrient status on Gulf of California islands. Oecologia 118:324–332 Askenmo C, Bromseen A, von Ekman J, Jansson C (1977) Impact of some wintering birds on spider abundance in spruce. Oikos 28:90–94 Atlegrim O (1989) Exclusion of birds from bilberry stands: impact on insect larval density and damage to the bilberry. Oecologia 79:136–139 Barbaro L, Giffard B, Charbonnier Y, van Halder I, Brockerhoff EG (2014) Bird functional diversity enhances insectivory at forest edges: a transcontinental experiment. Divers Distrib 20:149–159. doi:10.1111/ddi.12132 Barrows WB (1889) The English Sparrow (Passer domesticus) in North America, especially in its relation to agriculture. Bulletin 1. USDA Division of Economic Ornithology and Mammalogy, Washington, DC Basili GD, Temple SA (1999) Dickcissels and crop damage in Venezuela: defining the problem with ecological models. Ecol Appl 9:732–739 Becker J (1996) Hungry ghosts: Mao’s secret famine. The Free Press, New York Bendell BE, Weatherhead PJ, Stewart RK (1981) The impact of predation by red-winged blackbirds on European corn-borer populations. Canadian Journal of Zoology–Revue Canadienne de Zoologie 59:1535–1538 Borkhataria RR, Nuessly GS, Pearlstine E, Cherry RH (2012) Effects of blackbirds (Agelaius phoenicius) on stinkbug (Hemiptera: pentatomidae) populations, damage, and yield in Florida rice. Florida Entomologist 95:143–149 Bregman TP, Sekercioglu CH, Tobias JA (2014) Global patterns and predictors of bird species responses to forest fragmentation: implications for ecosystem function and conservation. Biol Conserv 169:372–383 Bruns H (1960) The economic importance of birds in forests. Bird Study 7:193–208 Carlson JC, Tupper SK, Werner SJ, Pettit SE, Santer MM, Linz GM (2013) Laboratory efficacy of an anthraquinone-based repellent 123 J Ornithol for reducing bird damage to ripening corn. Appl Anim Behav Sci 145:26–31. doi:10.1016/j.applanim.2013.01.011 Castro J, Gomez JM, Garcia D, Zamora R, Hodar JA (1999) Seed predation and dispersal in relict Scots pine forests in southern Spain. Plant Ecol 145:115–123 Chee YE (2004) An ecological perspective on the valuation of ecosystem services. Biol Conserv 120:549–565. doi:10.1016/j. biocon.2004.03.028 Cocker M, Tipling D (2013) Birds and people. Jonathan Cape, London Coleman R (1999) Parasitism of the herbivore Pieris brassicae by Cotesia glomerata does not benefit the host plant by reduction of herbivory. J Appl Entomol 123:171–177 Conover MR (1984) Response of birds to different types of food repellents. J Appl Ecol 21:437–443. doi:10.2307/2403420 Cordeiro NJ, Howe HF (2003) Forest fragmentation severs mutualism between seed dispersers and an endemic African tree. Proc Natl Acad Sci Unit States Am 100:14052–14056 Cordeiro NJ, Patrick DAG, Munisi B, Gupta V (2004) Role of dispersal in the invasion of an exotic tree in an East African submontane forest. J Trop Ecol 20:449–457 Daily GC (ed) (1997) Nature’s services: societal dependence on natural ecosystems. Island press, Washington, D.C De Grazio JW (1978) World bird damage problems. In: Proceedings of the 8th vertebrate pest conference, pp 9–24 DeVault TL, Rhodes OE, Shivik JA (2003) Scavenging by vertebrates: behavioral, ecological, and evolutionary perspectives on an important energy transfer pathway in terrestrial ecosystems. Oikos 102:225–234 Dolbeer RA (1990) Ornithology and integrated pest management-Red-winged blackbirds (Agelaius phoeniceus) and corn. Ibis 132:309–322. doi:10.1111/j.1474-919X.1990.tb01048.x Elliott CCH, Lenton GM (1989) The pest status of the quelea. In: Bruggers RL, Elliott CCH (eds) Quelea quelea: Africa’s Bird pest. Oxford University Press, Oxford, pp 17–34 Ellis JC (2005) Marine birds on land: a review of plant biomass, species richness, and community composition in seabird colonies. Plant Ecol 181:227–241 Evenden MD (1995) The laborers of nature: economic ornithology and the role of birds as agents of biological pest control in North American agriculture 1880-1930. Conservation history 39:172–183 Fisher RD (2011) Biological Survey Unit, USGS Patuxent Wildlife Research Center. http://www.pwrc.usgs.gov/history/bsphist2. html. Accessed 10 Dec 2014 Garcia D, Martinez D (2012) Species richness matters for the quality of ecosystem services: a test using seed dispersal by frugivorous birds. Proc Roy Soc B Biol Sci 279:3106–3113. doi:10.1098/ rspb.2012.0175 Gebhardt K, Anderson AM, Kirkpatrick KN, Shwiff SA (2011) A review and synthesis of bird and rodent damage estimates to select California crops. Crop Prot 30:1109–1116. doi:10.1016/j. cropro.2011.05.015 Gillham ME (1960) Vegetation of New Zealand shag colonies. T Roy Soc NZ Zool 88:363–380 Gomez-Baggethun E, de Groot R, Lomas PL, Montes C (2010) The history of ecosystem services in economic theory and practice: from early notions to markets and payment schemes. Ecol Econ 69:1209–1218. doi:10.1016/j.ecolecon.2009.11.007 Green AJ, Elmberg J (2014) Ecosystem services provided by waterbirds. Biol Rev 89:105–122 Green AJ, Soons M, Brochet AL, Kleyheeg E (2016) Dispersal of plants by waterbirds. In: Sekercioglu CH, Wenny DG, Whelan CJ (eds) Why birds matter: avian ecological functions and ecosystem services. University of Chicago Press, Chicago (in press) 123 Greene CD, Nielsen CK, Woolf A, Delahunt KS, Nawrot JR (2010) Wild turkeys cause little damage to row crops in illinois.Transactions of the Illinois State Academy of Sci 103:145–152 Greenwood JJD (2007) Citizens, science and bird conservation. J Ornithol 148:S77–S124. doi:10.1007/s10336-007-0239-9 Greig-Smith PW (1987) Bud-feeding by bullfinches: methods for spreading damage evenly within orchards. J Appl Ecol 24:49–62. doi:10.2307/2403786 Hackett SC (2011) Environmental and natural resource economics: theory, policy, and the sustainable society, 4th edn. M.E, Sharpe Armonk, NY Hocking DJ, Babbitt KJ (2014) Amphibian contributions to ecosystem services. Herpetological Conservation and Biology 9:1–17 Holbrook KM, Smith TB (2000) Seed dispersal and movement patterns in two species of Ceratogymna hornbills in a West african tropical lowland forest. Oecologia 125:249–257 Holmes R, Froud-Williams R (2005) Post-dispersal weed seed predation by avian and non-avian predators. Agr Ecosyst Environ 105:23–27 Holmes R, Schultz J, Nothnagle P (1979) Bird predation on forest insects: an exclosure experiment. Science 206:462–463 Holmes R, Sturges FW (1975) Bird community cynamics and energetics in a northern hardwoods ecosystem. J Anim Ecol 44:175–200 Hooks CRR, Pandey RR, Johnson MW (2003) Impact of avian and arthropod predation on lepidopteran caterpillar densities and plant productivity in an ephemeral agroecosystem. Ecol Entomol 28:522–532 Houston DC (1979) The adaptations of scavengers. In: Sinclair ARE, Norton-Griffiths M (eds) Serengeti. Dynamics of an Ecosystem University of Chicago Press Chicago, Illinois, pp 263–286 Jaeger ME, Elliott CCH (1989) Quelea as a resource. In: Bruggers RL, Elliott CCH (eds) Quelea quelea: Africa’s Bird Pest. Oxford University Press, Oxford, pp 327–338 Jennelle CS, Samuel MD, Nolden CA, Berkley EA (2009) Deer carcass decomposition and potential scavenger exposure to chronic wasting disease. J Wildl Manag 73:655–662. doi:10. 2193/2008-282 Johnson MD, Hackett SC (2016) Why birds matter economically: values, markets, and policies. In: Sekercioglu CH, Wenny DG, Whelan CJ (eds) Why birds matter: avian ecological functions and ecosystem services. University of Chicago Press, Chicago (in press) Johnson MD, Levy NJ, Kellermann JL, Robinson DE (2009) Effects of shade and bird exclusion on arthropods and leaf damage on coffee farms in Jamaica’s Blue Mountains. Agrofor Syst 76:139–148 Judd S (1901) The relation of sparrows to agriculture. Bulletin 15. USDA Division of Economic Ornithology and Mammalogy, Washington, D.C Judd S (1902) Birds of a Maryland farm. A local study of economic ornithology. Bulletin 17. USDA Division of Economic Ornithology and Mammalogy, Washington, D.C Kareiva P, Tallis H, Ricketts TH, Daily GC, Polasky S (eds) (2011) Natural Capital: Theory and practice of mapping ecosystem services. Oxford University Press, Oxford Kay BJ, Twigg LE, Korn TJ, Nicol HI (1994) The use of artificial perches to increase predation on house mice (Mus domesticus) by raptors. Wildlife research 21:95–106 Kelly D, Ladley JJ, Robertson AW, Anderson SH, Wotton DM, Wiser SK (2010) Mutualisms with the wreckage of an avifauna: the status of bird pollination and fruit-dispersal in New Zealand. New Zealand Journal of Ecology 34:66–85 Kerbes RH, Kotanen PM, Jefferies RL (1990) Destruction of wetland habitats by Lesser Snow Geese: a keystone species on the west coast of Hudson Bay. J Appl Ecol 27:242–258 J Ornithol Klosterman ME, Linz GM, Slowik AA, Homan HJ (2013) Comparisons between blackbird damage to corn and sunflower in North Dakota. Crop Prot 53:1–5. doi:10.1016/j.cropro.2013.06.004 Koh LP (2008) Birds defend oil palms from herbivorous insects. Ecol Appl 18:821–825 Korpimaki E, Krebs C (1996) Predation and population cycles of small mammals. Bioscience 46:754–764 Kremen C (2005) Managing ecosystem services: what do we need to know about their ecology? Ecol Lett 8:468–479. doi:10.1111/j. 1461-0248.2005.00751.x Kronenberg J (2014a) Environmental impacts of the use of ecosystem services: case study of birdwatching. Environ Manage 54:617–630. doi:10.1007/s00267-014-0317-8 Kronenberg J (2014b) What can the current debate on ecosystem services learn from the past? Lessons from economic ornithology. Geoforum 55:164–177. doi:10.1016/j.geoforum.2014.06.011 Landis D, Wratten S, Gurr G (2010) Habitat management to conserve natural enemies of arthropod pests in agriculture. Annu Rev Entomol 45:175–201 Lindell CA, Eaton RA, Lizotte EM, Rothwell NL (2012) Bird consumption of sweet and tart cherries. Human-Wildlife Interactions 6:283–290 Losey JE, Vaughan M (2006) The economic value of ecological services provided by insects. Bioscience 56:311–323 Lovins AB, Lovins LH, Hawken P (1999) A road map for natural capitalism. Harvard Bus Rev 77:145–158 Loyn RH, Runnalis RG, Forward GY, Tyers J (1983) Territorial Bell Miners (Manorina melanophrys) and other birds affecting populations of insect prey. Science 221:1411–1413 Ma ZJ, Cheng YX, Wang JY, Fu XH (2013) The rapid development of birdwatching in mainland China: a new force for bird study and conservation. Bird Conserv Int 23:259–269. doi:10.1017/ s0959270912000378 Manny BA, Johnson WC, Wetzel RG (1994) Nutrient additions by waterfowl to lakes and reservoirs: predicting their effects on productivity and water quality. Hydrobiologia 280:121–132 Mantyla E, Klemola T, Laaksonen T (2011) Birds help plants: a metaanalysis of top-down trophic cascades caused by avian predators. Oecologia 165:143–151 Marquis RJ, Whelan CJ (1994) Insectivorous birds increase growth of white oak through consumption of leaf-chewing insects. Ecology 75:2007–2014 McNicol DK, Robertson RJ, Weatherhead PJ (1982) Seasonal, habitat, and sex-specific food habits of red-winged blackbirds implications for agriculture. Canadian Journal of Zoology-Revue Canadienne De Zoologie 60:3282–3289. doi:10.1139/z82-415 McWilliam AN, Cheke RA (2004) A review of the impacts of control operations against the red-billed quelea (Quelea quelea) on nontarget organisms. Environ Conserv 31:130–137 MEA (2005) Millenium ecosystem assessment. Ecosystems and human well-being Synthesis. Island Press, Washington, DC Meinzingen WW, Bashir ESA, Parker JD, Heckel JU, Elliott CCH (1989) Lethal control of quelea. In: Bruggers RL, Elliott CCH (eds) Quelea quelea: Africa’s Bird Pest. Oxford University Press, Oxford, pp 293–316 Mols CMM, Visser ME (2002) Great Tits can reduce caterpillar damage in apple orchards. J Appl Ecol 39:888–899 Moss M, Bowers P (2007) Migratory bird harvest in northwestern Alaska: a zooarchaeological analysis on Ipiutak and Thule occupations from the Deering archaeological district. Artic Anthropology 44:37–50 Muscarella R, Fleming TH (2007) The role of frugivorous bats in tropical forest succession. Biol Rev 82:573–590 Ndang’ang’a PK, Njoroge JBM, Ngamau K, Kariuki W, Atkinson PW, Vickery J (2013) Avian foraging behaviour in relation to provision of ecosystem services in a highland East African agroecosystem. Bird Study 60:156–168. doi:10.1080/00063657. 2012.758228 Otvos IS (1979) The effects of insectivorous bird activities in forest ecosystems: an evaluation. In: Dickson JG, Conner EN, Fleet RR, Kroll JC, Jackson JA (eds) The role of insectivorous birds in forest ecosystems. Academic Press, New York, pp 341–374 Peres CA (2001) Synergistic effects of subsistence hunting and habitat fragmentation on Amazonian forest vertebrates. Conserv Biol 15:1490–1505 Peres CA, Palacios E (2007) Basin-wide effects of game harvest on vertebrate population densities in Amazonian forests: implications for animal-mediated seed dispersal. Biotropica 39:304–315 Pizo MA (1997) Seed dispersal and predation in two populations of Cabralea canjerana (Meliaceae) in the Atlantic Forest of southeastern Brazil. J Trop Ecol 13:559–578 Podulka S, Eckhardt M, Otis D (2004) Birds and humans: A Historical perspective. In: Podulka A, Rohrbugh R Jr, Bonney R (eds) Handbook of bird biology. Cornell Lab of Ornithology, Ithaca, pp 1–42 Polis GA, Hurd SD (1996) Linking marine and terrestrial food webs: allochthonous input from the ocean supports high secondary productivity on small islands and coastal land communities. Am Nat 147:396–423 Post DM, Taylor JP, Kitchell JF, Olson MF, Schindler DE, Herwig BR (1998) The role of migratory waterfowl as nutrient vectors in a managed wetland. Conserv Biol 12:910–920 Power ME et al (1996) Challenges in the quest for keystones. Bioscience 46:609–620. doi:10.2307/1312990 Proctor M, Yeo P, Lack A (1996) The natural history of pollination. Timber press, Portland Rathcke BJ (2000) Hurricane causes resource and pollination limitation of fruit set in a bird-pollinated shrub. Ecology 81:1951–1958 Renne IJ, Barrow WC, Randall LAJ, Bridges WC (2002) Generalized avian dispersal syndrome contributes to Chinese Tallow Tree (Sapium sebiferum, Euphorbiaceae) invasiveness. Divers Distrib 8:285–295 Ridley HN (1930) The dispersal of plants throughout the world. Reeve, Ashford Rogers H, Lambers JHR, Miller R, Tewksbury JJ (2012) ‘Natural experiment’ demonstrates top-down control of spiders by birds on a landscape level. PLoS One. e43446. doi:10.1371/journal. pone.0043446 Samuels IA, Levey DJ (2005) Effects of gut passage on seed germination: do experiments answer the questions they ask? Funct Ecol 19:365–368 Sekercioglu CH (2002) Impacts of birdwatching on human and avian communities. Environ Conserv 29:282–289 Sekercioglu CH (2006a) Ecological significance of bird populations. In: del Hoyo J, Elliott A, Christie D (eds) Handbook of the birds of the world: Old world flycatchers to old world warblers, vol 11. Lynx Edicions, Barcelona, pp 15–51 Sekercioglu CH (2006b) Increasing awareness of avian ecological function. Trends Ecol Evol 21:464–471 Sekercioglu CH (2010) Ecosystem functions and services. In: Sodhi NS, Ehrlich PR (eds) Conservation biology for all. Oxford University Press, Oxford, pp 45–72 Sekercioglu CH (2012) Bird functional diversity and ecosystem services in tropical forests, agroforests and agricultural areas. J Ornithol 153:S153–S161. doi:10.1007/s10336-012-0869-4 Sekercioglu CH, Primack RB, Wormworth J (2012) The effects of climate change on tropical birds. Biol Conserv 148:1–18. doi:10. 1016/j.biocon.2011.10.019 Sheffield LM, Crait JR, Edge WD, Wang GM (2001) Response of American Kestrels and gray-tailed voles to vegetation height and supplemental perches. Can J Zool 79:380–385 123 J Ornithol Sodhi NS, Sekercioglu CH, Barlow J, Robinson SK (2011) Conservation of tropical birds. Wiley-Blackwell, Oxford Solomon M, Glen D, Kendall D, Milsom N (1977) Predation of overwintering larvae of codling moth (Cydia pomonella L) by birds. J Appl Ecol 13:341–353 Stiles FG (1981) Geographical aspects of bird-flower coevolution, with particular reference to Central America. Ann Mo Bot Gard 68:323–351 Sturges FW, Holmes R, Likens GE (1974) The role of birds in nutrient cycling in a northern hardwood forest. Ecology 55:149–155 Takekawa JY, Garton EO, Langelier LA (1982) Biological control of forest insect outbreaks - the use of avian predators. T N Am Wildl Nat Res 47:393–409 Tewksbury JJ et al (2014) Natural History’s Place in Science and Society. Bioscience 64:300–310. doi:10.1093/biosci/biu032 Tidemann S, Gosler AG (2010) Ethno-ornithology: birds, indigenous peoples. Culture and society, Earthscan, London Tomback DF (2016) Seed dispersal by corvids—birds that build forests. In: Sekercioglu CH, Wenny DG, Whelan CJ (eds) Why birds matter: avian ecological functions and ecosystem services. University of Chicago Press, Chicago (in press) Tomback DF, Linhart YB (1990) The evolution of bird-dispersed pines. Evol Ecol 4:185–219 Traveset A, Verdu M (2002) A meta-analysis of the effect of gut treatment on seed germination. In: Levey DJ, Silva WR, Galetti M (eds) Seed dispersal and frugivory:ecology, evolution and conservation. CABI Publishing, Wallingford, pp 339–350 Tremblay A, Mineau P, Stewart RK (2001) Effects of bird predation on some pest insect populations in corn. Agr Ecosyst Environ 83:143–152 Tscharntke T (1992) Cascade effects among four trophic levels - bird predation on galls affects density-dependent parasitism. Ecology 73:1689–1698 VerCauteren KC, Pilon JL, Nash PB, Phillips GE, Fischer JW (2012) Prion remains infectious after passage through digestive system of American crows (Corvus brachyrhynchos). PLoS ONE 7:e45774 Vidal E, Jouventin P, Frenot Y (2003) Contribution of alien and indigenous species to plant-community assemblages near penguin rookeries at Crozet archipelago. Polar Biol 26:432–437 123 Weatherhead PJ, Tinker S, Greenwood H (1982) Indirect assessment of avian damage to agriculture. J Appl Ecol 19:773–782 Wenny DG, DeVault TL, Johnson MD, Kelly D, Sekercioglu CH, Tomback DF, Whelan CJ (2011) The need to quantify ecosystem services provided by birds. Auk 128:1–14. doi:10.1525/auk. 2011.10248 Wenny DG, Sekercioglu CH, Cordeiro N, Rogers HS, Kelly D (2016) Seed dispersal by fruit-eating birds. In: Sekercioglu CH, Wenny DG, Whelan CJ (eds) Why birds matter: avian ecological functions and ecosystem services. University of Chicago Press, Chicago (in press) Whelan CJ, Wenny DG, Marquis RJ (2008) Ecosystem services provided by birds. Ann N Y Acad Sci 1134:25–60. doi:10.1196/ anndis.1439.003 Whelan CJ, Wenny DG, Marquis RJ (2010) Policy implications of ecosystem services provided by birds. Synesis 1:11–20 White EM, Bowker JM, Askew AE, Langner LL, Arnold JR, English DBK (2014) Federal outdoor recreation trends: effects on economic opportunities. Working Paper Number 1. US Forest Service National Center for Natural Resources Economic Research White SS, Renner KA, Menalled FD, Landis DA (2007) Feeding preferences of weed seed predators and effect on weed emergence. Weed Sci 55:606–612 Wiens JA (1973) Pattern and process in grassland bird communities. Ecol Monogr 43:237–270 Williams CK, Applegate RD, Lutz RS, Rusch DH (2000) A comparison of raptor densities and habitat use in Kansas cropland and rangeland ecosystems. Journal of Raptor Research 34:203–209 Wolff JO, Fox T, Skillen RR, Wang GM (1999) The effects of supplemental perch sites on avian predation and demography of vole populations. Can J Zool 77:535–541 Wormworth J, Sekercioglu CH (2011) Winged sentinels: birds and climate change. Cambridge University Press, Cambridge. doi:10. 1016/j.biocon.2011.10.019