he Auk
An International
Journal of Ornithology
Vol. 128 No. 1 January 2011
he Auk 128(1):1–14, 2011
he American Ornithologists’ Union, 2011.
Printed in USA.
PERSPECTIVES IN ORNITHOLOGY
THE NEED TO QUANTIFY ECOSYSTEM SERVICES PROVIDED BY BIRDS
DANIEL G. WENNY,1,8 TR AVIS L. D EVAULT, 2 M AT THEW D. J OHNSON, 3 DAVE K ELLY,4
C AGAN H. S EKERCIOGLU, 5,9 D IANA F. TOMBACK ,6 AND C HRISTOPHER J. WHELAN7
1
Jo Daviess Conservation Foundation, 126 N. Main Street, Elizabeth, Illinois 61028, USA;
U.S. Department of Agriculture, National Wildlife Research Center, Sandusky, Ohio 44870, USA;
3
Department of Wildlife, Humboldt State University, Arcata, California 95521, USA;
4
Biological Sciences, University of Canterbury, Christchurch 8140, New Zealand;
5
Center for Conservation Biology, Department of Biology, Stanford University, Stanford, California 94305, USA;
6
Department of Integrative Biology, University of Colorado Denver, P.O. Box 173364, Denver, Colorado 80217, USA; and
7
Illinois Natural History Survey, c/o Department of Biological Sciences, University of Illinois at Chicago,
845 W. Taylor Street, Chicago, Illinois 60607, USA
2
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 speciic 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 beneit
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 eforts as luxury.
Several previous reviews have identiied ecosystem services that
beneit human society (Costanza et al. 1997, Daily 1997, Pimentel
et al. 1997, Sekercioglu 2010). he 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,
8
9
highlight recent steps toward quantifying those services, and, inally, suggest directions for future research. Overall, we emphasize that global eforts to conserve bird populations and sustain
avian biodiversity also preserve the diverse ecosystem services
provided by birds, thus contributing to human well-being.
D EFINITIONS
AND
BACKGROUND
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 puriication, and nutrient cycling, provide processes essential for ecological communities and agricultural ecosystems.
he 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 quantiied (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). he main issues include
Present address: Loras College, 1450 Alta Vista, Dubuque, Iowa 52004, USA. E-mail: harrier2@mchsi.com
Present address: Department of Biology, University of Utah, 257 South 1400 East, Room 201, Salt Lake City, Utah 84112, USA.
he Auk, Vol. 128, Number 1, pages 1−14. ISSN 0004-8038, electronic ISSN 1938-4254. 2011 by he American Ornithologists’ Union. All rights reserved. Please direct all
requests for permission to photocopy or reproduce article content through the University of California Press’s Rights and Permissions website, http://www.ucpressjournals.
com/reprintInfo.asp. DOI: 10.1525/auk.2011.10248
—1—
2
— WENNY
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).
O VERVIEW
OF
E COSYSTEM S ERVICES P ROVIDED
BY
B IRDS
Birds are the best-known class of vertebrate animals, occur worldwide in nearly all habitats, and provide many services (Sekercioglu 2006a, b; Whelan et al. 2008). hus, 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 quantiied (Sekercioglu 2002, LaRouche 2003, Leonard 2008, Carver
2009). Other historical and cultural aspects of birds have been reviewed and quantiied in a general way (Diamond and Filion 1987,
Podulka et al. 2004, Mynott 2009). Most of the important ecological roles that birds ill, however, involve supporting and regulating
services, such as insect pest control and seed dispersal, and these
types of services are the most diicult 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. hrough 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.—he regulating and supporting services provided by birds result mostly from foraging (i.e., consuming and
processing resources; Table 1). he 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). he beneicial role of birds in consuming arthropods, and especially their responses to and inluence 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 beneited the crop (Suyin 1959, Becker 1996).
Other trophic cascades that involve birds potentially beneit agriculture, but they have seldom been studied. For example,
ET AL .
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AUK , VOL . 128
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). hey concluded that the evidence was inconsistent and that the efect of owls warrants further
investigation. Kay et al. (1994) reported that perches placed around
soybean ields in Australia increased the number of diurnal raptors
around and over the ields, which in turn decreased House Mouse
(Mus musculus) population growth rate and maximum population
density in the ields. Perches placed 100 m apart were more efective
than those placed 200 m apart. Other studies demonstrated that
providing artiicial perches attracts various birds of prey, including
American Kestrels (Falco sparverius), which also suggests that this
method may enhance or concentrate foraging in potentially beneicial ways (Wolf et al. 1999, Sheield et al. 2001). Clearly, more
research is needed on the potential for birds of prey to drive trophic
cascades in natural and agricultural ecosystems.
he 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 Goldinch (Carduelis carduelis), destroyed 10× more
seeds of the aggressive pasture weed Carduus nutans than a weevil
(Curculionidae: Rhinocyllus conicus) that was introduced to provide biological control of C. nutans (Kelly and McCallum 1990). In
fact, the 32% of seed destroyed by goldinches at that site compares
favorably to the highest well-documented seed losses attributed to
R. conicus (30–40%) at sites where the insect provided efective biological control (Kelly and McCallum 1995). While it is likely that
most species of avian granivores are beneicial in agroecosystems,
especially because most species also eat considerable quantities
of invertebrates during the breeding season, the most prominent studies of granivores are those on birds as agricultural pests
(Weatherhead et al. 1982, Elliott and Lenton 1989, Dolbeer 1990,
Basili and Temple 1999, Avery et al. 2001, Blackwell and Dolbeer
2001, McWilliam and Cheke 2004, Cirne and Lopez-Iborra 2005,
Hagy et al. 2008). Future research should examine more fully the
costs and beneits of avian granivory in agricultural settings.
Bird–plant mutualisms.—he bird–plant interactions of pollination and seed dispersal have potentially large efects on ecosystems. Nearly 33% of bird species disperse seeds, primarily through
fruit consumption, but also through scatter-hoarding of nuts and
conifer seed crops (Vander Wall 2001, Sekercioglu 2006b). It is dificult to estimate the number of plant species dispersed by birds,
because of overlap with seed-dispersing mammals and incomplete
knowledge of many habitats. In the temperate zone (i.e., Europe,
North America, Japan, and New Zealand), 36–55% of woody lora
are leshy-fruited (Burrows 1994). Nonwoody species are less likely
to have leshy fruit, so the average across whole loras is lower; for
example, in New Zealand, leshy fruits are found in 59% of trees
(Kelly et al. 2010) and 48% of all woody species (Burrows 1994),
but in only 12% of the whole lora (Lord et al. 2002). hese temperate-zone totals exclude dry (lacking a leshy covering), scatterhoarded tree nuts and conifer seeds, which are common in the
Northern Hemisphere (Tomback and Linhart 1990, Vander Wall
J ANUARY 2011
— P ERSPECTIVES
IN
O RNITHOLOGY —
3
TABLE 1. Relative importance of dietary categories among avian orders (+ indicates primary item, – indicates less important item, blank indicates an
item rarely or never eaten at family level within orders). List based on Gill and Donskar (2010). Diets from Harris (2009).
Terrestrial
Order
Tinamiformes
Struthioniformes
Rheiformes
Casuariiformes
Apterygiformes
Galliformes
Anseriformes
Gaviiformes
Sphenisciformes
Procellariiformes
Podicipediformes
Phoenicopteriformes
Phaethontiformes
Ciconiiformes
Pelecaniformes
Suliformes
Accipitriformes
Falconiformes
Otidiformes
Mesitornithiformes
Cariamiformes
Eurypygiformes
Gruiformes
Charadriiformes
Pteroclidiformes
Columbiformes
Psittaciformes
Opisthocomiformes
Musophagiformes
Cuculiformes
Strigiformes
Caprimulgiformes
Apodiformes
Coliiformes
Trogoniformes
Leptosomiformes
Coraciiformes
Bucerotiformes
Piciformes
Passeriformes
Families
Genera
Species
Inverts
Verts
1
1
1
2
1
5
3
1
1
4
1
1
1
1
5
4
4
1
1
1
1
2
6
19
1
1
3
1
1
1
2
4
4
1
1
1
6
4
9
120
9
1
2
2
1
83
51
1
6
26
6
3
1
6
35
8
72
11
11
2
2
2
42
94
2
42
86
1
6
32
27
21
128
2
7
1
35
17
67
1278
47
2
2
4
5
297
169
5
19
134
21
6
3
19
111
55
260
65
27
3
2
2
162
379
16
321
373
1
23
146
220
117
454
6
42
1
157
73
431
6237
+
–
–
+
+
+
+
–
–
+
–
+
+
+
+
–
+
–
–
–
+
+
+
+
+
+
+
+
Inverts
Verts
–
–
–
–
+
–
+
+
Aquatic
Carrion
–
+
–
+
+
+
+
+
+
+
+
+
+
+
+
+
+
+
+
+
Fruit
Seeds
Vegetation
–
–
–
+
–
–
+
+
–
+
+
+
+
+
–
+
–
–
+
–
–
–
+
–
+
–
–
–
–
+
+
+
–
+
–
–
–
+
+
–
+
–
–
+
–
–
–
+
+
+
+
2001). Also, the tropics hold most plant species diversity, and tropical loras are disproportionately woody and leshy-fruited (Howe
and Smallwood 1982, Willson et al. 1989, Fleming 1991). hus,
probably 30–50% of all plant species have vertebrate-dispersed
fruit (80,000–140,000 species). Certainly, many tens of thousands
of plant species beneit from bird dispersal in terms of gene low,
colonization of open sites, escape from predators, directed dispersal to favorable sites, or enhanced germination (Vander Wall and
Balda 1981, Howe and Smallwood 1982, Johnson and Webb 1989,
Tomback and Linhart 1990, Jordano 2000, Tomback 2005).
Birds disperse the seeds of many woody plant species with
direct value to humans for timber, medicine, food, or other uses;
+
–
–
+
–
–
–
+
+
+
–
–
–
–
–
Nectar
+
+
–
–
–
–
+
+
+
+
–
–
+
+
–
–
+
yet the dependence of these plants on birds for dispersal and the
anthropogenic inluences on the seed-dispersal pathways are in
many cases poorly understood. he great declines in abundance
of large frugivorous birds and mammals have resulted directly or
indirectly from human activities, and some have been extirpated
from regions or have become extinct (Cordeiro and Howe 2003,
Sekercioglu et al. 2004, Peres and Palacios 2007, Terborgh et al.
2008). Large-seeded plants are most at risk because they require
large-bodied dispersers, which are more vulnerable to anthropogenic efects (Hansen and Galetti 2009, McKinney et al. 2009). As
a result, the number of relatively large-seeded plants with few or
no dispersers is now rising, especially on islands, which have lower
4
— WENNY
diversity and less ecological redundancy than continental areas
(e.g., Kelly et al. 2010). Lower densities of frugivores may disperse
a smaller fraction of the fruit crop, which can result in fewer seedlings or in seedlings being more concentrated under the parent
plants (Cordeiro and Howe 2003, Terborgh et al. 2008, Cordeiro
et al. 2009, Sethi and Howe 2009, Sharam et al. 2009, Chimera
and Drake 2010). hese efects generally result in changes in plant
community composition rather than the local extirpation of
plant species (Wright and Duber 2001; Cordeiro and Howe 2003;
Muller-Landau 2007; Wright et al. 2007a, b; McKinney et al. 2009;
Sharam et al. 2009). It is unknown how these changes will afect
plant populations, or even entire forest communities, that are important to humans. More experimental work is needed to determine the ecological processes involved and their outcomes.
Fewer bird and plant species are involved in bird-pollination
mutualisms (~900 bird species and ~5% of regional loras; Stiles
1985, Nabhan and Buchmann 1997), but recent evidence suggests
that bird-pollination failure still poses important risks. he relationships tend to be more specialized than with seed dispersal,
and the outcome of a failed mutualism is unambiguously negative
(failure to produce seed; Kelly et al. 2004). For some plants in New
Zealand, insects were regarded as efective substitutes for missing
birds, but data do not support this belief (Kelly et al. 1996, Robertson et al. 2005), even for some temperate-zone plant species
with apparently insect-adapted lowers (Anderson 2003). As with
seed dispersal, plant extinction may not follow loss of pollinators,
but we have few good measures of such efects, especially in cases
where birds have declined rather than become extinct. One recent study provides a cautionary example: Anderson et al. (2011)
showed a terrestrial trophic cascade in New Zealand whereby
mammalian carnivores reduced densities of pollinating birds, resulting in an 84% reduction in seed output of the bird-pollinated
shrub Rhabdothamnus solandri and a 55% reduction in shrub regeneration. he authors stress that gradual plant declines might
frequently pass unrecorded. Where comparisons have been made
within a single region, bird-pollinated plants seem to be more pollen limited than dispersal limited; thus, the efects of mutualism
breakdown may be greater and faster-acting for bird-pollination
than for seed-dispersal systems (Kelly et al. 2004, 2010). However,
where pollination is primarily by insects, seed dispersal is probably the mutualism more at risk (Corlett 2007).
Scavenging and nutrient cycling.—he 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 (Houston
1979, DeVault et al. 2003).
In addition to vultures, many other bird species scavenge animal carcasses at least occasionally, including raptors, seabirds,
gulls, herons, rails, shorebirds, woodpeckers, and passerines
(DeVault et al. 2003). Seabirds, in particular, are accomplished
scavengers, often feeding on ishery discards (Hill and Wassenberg
ET AL .
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AUK , VOL . 128
1990, 2000; Wassenberg and Hill 1990; Jennings and Kaiser 1998).
Among passerines, corvids—especially American Crows (Corvus
brachyrhynchos) and Common Ravens (C. corax)—are the most
conspicuous scavengers (DeVault et al. 2003). More research is
needed on the ecological consequences of obligate and facultative scavenging, particularly on how these processes are afected
by contemporary human activities such as transportation (Dean
and Milton 2003, Antworth et al. 2005) and commercial isheries
(Britton and Morton 1994), which make many dead animals and
byproducts available for scavengers.
Birds contribute to nutrient cycling in all habitats, but most
impressively where aquatic birds nest colonially on islands (Polis and Hurd 1996, Anderson and Polis 1999). Seabirds often nest
in dense colonies both in coastal areas and on islands where they
process large amounts of food in small areas. In this manner, seabirds transport nutrients from the aquatic zone to the terrestrial
zone. Such large inputs of phosphate-rich guano can inluence
the structure and composition of plant communities (Ellis 2005).
Conversely, removal of nesting birds after introduction of a predator fundamentally alters the plant community (Croll et al. 2005,
Bellingham et al. 2010).
Birds as ecosystem engineers.—Ecosystem engineering is
the one supporting service provided by birds that does not result from foraging but involves construction of nests that are later
used by many other organisms. Nests vary greatly in building
materials, structure, complexity, size, longevity, and usefulness
to other organisms. Examples include excavated cavities or burrows, cup nests, platform nests, mud nests, and domed nests (see
Ehrlich et al. 1988). Open-cup and domed nests, the most common nest types (Collias and Collias 1984, Collias 1997), are often
taken over by small mammals (Gates and Gates 1975), overwintering spiders (Otzen and Schaefer 1980), and bumble bees (Dame et
al. 2002). Many animals, including insects like beetles and social
wasps, rodents, lizards, snakes, frogs, and even other bird species,
use the domed ground nests of tropical ovenbirds (Furnariidae;
Remsen 2003). Woodpecker cavities are used by other birds and
by many other animal species, including mammals, amphibians,
and arthropods (Conner et al. 1997, Neubig and Smallwood 1999,
Monterrubio-Rico and Escalante-Pliego 2006). Nest burrows are
excavated by many bird taxa, including penguins, seabirds, alcids,
parrots, owls, kingishers, and passerines. hese nests alter soil
properties and thus afect nutrient cycling (see above), and, like
woodpecker cavities, they are used by many other taxa, including birds, snakes, mammals, and amphibians (Casas-Criville and
Valera 2005).
Summary: Indirect services.—Birds are highly mobile, occur
globally, ill many ecological roles, and respond rapidly to environmental change. As described in the overview above, bird activities provide links within and between ecosystems and can have
large efects on other species. he ecosystem services that birds
provide are largely indirect and support or enhance other services.
For example, insectivory, pollination, seed dispersal, and nutrient cycling beneit plants that then produce oxygen, food, lumber, medicine, lood and erosion control, aesthetics, recreation,
and other beneits for human society. Birds may act as densitydependent consumers that exert strong top-down efects on food
webs, which can result in prey population regulation, pest control,
and corresponding changes in plant communities. herefore, in
J ANUARY 2011
— P ERSPECTIVES
IN
the context of ecosystem services, population decline among birds
may lead to changes that cascade through ecosystems and cause
subsequent declines in beneits to humans.
Because the services are usually indirect, neither birds nor
their services are generally included in ecosystem-valuation models. herefore, birds are only indirect beneiciaries of any conservation actions advocated by economic models. his approach
implies an indicator-species model of conservation in which a
limited subset of species or other environmental indicators are
the basis for conservation planning and land-use decisions. Such
indirect beneits may be suicient for bird conservation in some
cases, but to date, the indicator-species model has had inconsistent success in predicting abundance and diversity of other species (Roberge et al. 2008, Larsen et al. 2009, Cushman et al. 2010).
Data that enable valuation of bird services will improve the models of ecosystem valuation and increase bird-conservation eforts
as well as the beneits to humans. At the same time, eforts to establish valuation will promote additional research on many fundamental and important ecological questions.
Q UANTIFYING E COSYSTEM S ERVICES
he overall goal of determining the value of ecosystem services
can be divided into three components. First is the need to describe
and quantify the services themselves at local and regional levels.
he goal of describing ecosystem services is largely accomplished
(Sekercioglu 2006a, b; Whelan et al. 2008), and we know considerable natural-history details that are relevant to many ecosystem
services. But we need more detail at local levels from a variety of
sites to make global comparisons; in this way we can minimize
the problems associated with “beneit transfer” (i.e., assuming that
value estimates from one site are equivalent to those at a similar
habitat elsewhere; Farber et al. 2006, Plummer 2009, Eigenbrod
et al. 2010). Data from multiple sites will also allow an assessment
of the extent and sources of variation in ecosystem services. Understanding the variation in services among sites will lead to more
robust estimates of the value of ecosystem services and more effective conservation plans.
Second, we need methods to quantify the direct or indirect
values of ecosystem services provided, and to test these methods
with case studies. Finally, we need to combine the information
from multiple ecosystem services to form a metric or model of values to assess how ecosystem services can be maximized under different land-use scenarios or policy changes. We need this type of
modeling approach because a given service (e.g., seed dispersal)
will not be protected successfully by itself, but rather as part of a
comprehensive conservation strategy. Several models incorporating some ecological input have been developed (Daily and Matson 2008, Ranganathan et al. 2008, Daily et al. 2009, Nelson et al.
2009).
Most of the supporting and regulating ecosystem services are
not traded in traditional markets, and in that sense they are public
goods with approximately the same cost (usually “free”) and value
to all users. However, the value of some public ecosystem services
or resources may decline with level of use. For example, intensive
birdwatching at a given site may disturb the birds to the point that
they leave or alter their behavior, thus rendering the resource unavailable or less worthwhile for additional viewers (Blumstein et
O RNITHOLOGY —
5
al. 2005). As public goods, ecosystem services are susceptible to
“externalities,” such as uncompensated side efects from other users of a common resource. For example, extensive habitat modiication by one landowner may negatively afect pollination or pest
control for an adjacent landowner. An additional complication is
that the economic value in environmental markets that are driven
by regulations (e.g., those mandated by the Clean Water Act and
Endangered Species Act) is not determined by production functions or the value to the end users, as in traditional markets. Instead, regulators set the value. For all of these reasons, market
failure (i.e., the failure of market value to relect full social cost),
is more often the rule than the exception for ecosystem services.
hese problems raise fundamental concerns about the ability of
neoclassical economic theory to adequately address environmental issues (Hall et al. 2000, Lux 2003, Nadeau 2010), and in that
sense ecosystem valuation is a step toward bridging the divide between economics and natural sciences.
A variety of methods have been used in valuation of ecosystem services (Farber et al. 2002, 2006). Here, we briely review the
methods that are useful for quantifying services provided by birds.
All of these methods are conventional in that the output is an economic value and therefore represents the “marginal value” people
are willing to pay for an item or service. Non-monetary valuation
methods such as ranking or stakeholder analysis have promise for
community-level decisions, but they have not yet been applied to
the services discussed here.
he value of birds in pest control can be estimated as the
costs avoided by using birds instead of pesticides. hese valuations have been determined for bats (Cleveland et al. 2006) and insects (Losey and Vaughan 2006). Data necessary for this estimate
include irst the monetary loss (e.g., reduced crop yields) from
herbivory under current conditions, and then, based on diet and
natural history of both insects and insectivores, an estimate of the
additional loss that would occur with no birds present. Assuming that pesticides could accomplish the pest-control function of
birds and would yield the same crop levels in the absence of birds,
the cost of that amount of pesticides is the avoided cost and an
estimate of the value of avian pest control. Note that this method
works well for agricultural crops or timber species for which we
have both market values and natural-history data (e.g., Takekawa
and Garton 1984), but not for most wild plants (e.g., Sharam et al.
2009). Also note that this is short-term costing, assuming no evolutionary responses of the pests to the pesticides, whereas experience has shown that pests rapidly evolve resistance to pesticides
(Gassmann et al. 2009, Bourguet et al. 2010) but have not yet managed to do so to birds because birds also evolve.
An alternative, but one that still requires some estimate of the
market value of an end product, is production valuation in which
value is assigned on the basis of the economic outcome that results
from changes in services. For example, the value of scatter-hoarding of seeds by corvids could be based on the reforestation value of
the species they disperse (see case study below). Similarly, replacement costs relect the value of replacing or recreating a missing
ecosystem service. he Biosphere 2 experiment, which created an
artiicial habitable system and cost ~$9 million per human inhabitant per year, took this to an extreme (Avise 1994).
Finally, through surveys or polls, preference-based approaches can yield contingent values that are essentially the
6
— WENNY
willingness to pay for an ecosystem service (Bowker and Stoll
1988). Contingent values, along with travel and equipment costs,
are used to estimate the economic impact of tourism and other
recreational uses. For example, birdwatchers in the United States
spend more than $30 billion annually for travel and equipment
(LaRouche 2003, Carver 2009) and would be willing to spend $35
to $134 per day for birdwatching opportunities (LaRouche 2003).
C ASE STUDIES
Cofee pest control in Jamaica.—Shade-cofee farms can be highquality habitats for insectivorous birds, especially migratory generalist species that do not rely on intact understory vegetation
(Tejeda-Cruz and Sutherland 2004, Johnson et al. 2006). Bird
foraging within farms is concentrated in the shade trees that
grow over the cofee shrubs (Wunderle and Latta 2000). he coffee shrubs are naturally chemically defended and comparatively
poor in insect abundance (Lepelley 1973, Greenberg et al. 2000).
Nonetheless, many birds also forage, to some degree, on insects
on the cofee shrubs (Wunderle and Latta 2000). Bird exclosure
experiments have conirmed that bird foraging reduces overall insect biomass on cofee shrubs in Guatemala (Greenberg et
al. 2000), Mexico (Philpott et al. 2004), Panama (Van Bael et al.
2008), Puerto Rico (Borkhataria et al. 2006), and Jamaica (Johnson et al. 2009). he Cofee Berry Borer (Hypothenemus hampei) is the world’s most damaging insect pest of cofee (Damon
2000). Recent experiments in Jamaica indicate that birds reduce
pest populations, increase saleable fruit, and boost farm income
(Kellermann et al. 2008, Johnson et al. 2010). Calculations of the
beneits provided were obtained by documenting pest infestation
levels in the presence and absence of bird foraging (via exclosures)
and translating higher saleable crop yields in the presence of birds
into a dollar igure using crop market prices. Birds boosted farm
income by $75 ha–1 year–1 on high-elevation farms (Kellermann et
al. 2008) and by $310 ha–1 year–1 on a mid-elevation farm (Johnson
et al. 2010; here and below, igures are in U.S. dollars).
As agents of ecosystem services, birds are notably mobile and
capable of utilizing multiple habitats. herefore, the delivery of
ecosystem services by birds in some cases may depend strongly
on habitat coniguration and landscape composition. To harness
economic forces for conservation of birds and their habitats in
agricultural landscapes, ornithologists must not only document
the economic value of the ecosystem services provided by birds,
but also clarify bird movements and relationships among agricultural lands and surrounding natural habitats. Several models are
available for projecting ecosystem services over a changing landscape, such as InVEST (Daily et al. 2009) and individual-based
models (Grimm and Railsback 2005). Ongoing radiotelemetry
studies have shown that an important cofee pest predator, the
Black-throated Blue Warbler (Dendroica caerulescens), commutes
from diurnal foraging territories within cofee habitat to nocturnal roosting sites within natural forests (Jirinec et al. 2011) and
establishes foraging territories close to farm edges and patches
of uncultivated vegetation within farms (B. R. Campos and M. D.
Johnson unpubl. data). hese results establish links between the
provisioning of an economically valuable ecosystem service
and natural vegetation both within and outside cofee farms. By
linking bird movements to maps of landscapes and estimates of
ET AL .
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pest-control services, a spatially explicit individual-based model
can simulate how changes in landscape composition can afect the
delivery of pest-control services (M. D. Johnson and S. F. Railsback
unpubl. data). his approach could be used by conservation planners to estimate the economic value of forested habitats within
agricultural landscapes, and to provide economic estimates of
ecosystem services under proposed land-use scenarios.
Swedish oaks.—he replacement costs for the seed-dispersal
services of Eurasian Jays (Garrulus glandarius) in Stockholm National Urban Park were estimated by Hougner et al. (2006). he
National Urban Park of Stockholm features one of the largest oak
forests in Sweden. he Swedes recognize oaks as keystone species
that support unique communities of insects, lichens, mosses, and
fungi, as well as nesting birds and bats (Hougner et al. 2006). In
the National Urban Park of Stockholm, many of the oaks (Quercus robur and Q. petrea) are more than 500 years old. Nearly 85%
of the oaks in the park most likely result from acorn dispersal,
primarily by Eurasian Jays. Given that an epidemic of lethal oak
disease is spreading across Europe and that most of the oaks in
the park are currently healthy, Hougner et al. (2006) argued that
the natural seed-dispersal services of the jays will be especially
important for maintaining healthy forests through natural local
seed-dispersal over time. he authors calculated the replacement
value of one pair of territorial jays, using two approaches: the cost
of manually planting acorns and the cost of planting sapling oaks.
hey used data from several references to quantify acorn dispersal by Eurasian Jays and the number of sapling oaks that arise
from jay dispersal each year, estimating germination and survival
rates. Having computed the costs of manual reforestation, the authors concluded that the minimum replacement value of a pair of
Eurasian Jays was about $4,035 (conversion from SEK, based on
2005 values) if acorns are seeded, and about $22,560 if saplings
are planted. Given the area occupied by oak forest in the Park,
these jays represent a value of $2,115 to $9,450 per ha for forest
regeneration.
Nutcrackers and pines.—A similar example is the economic
value of scatter-hoarding (caching) seeds of Whitebark Pine (Pinus
albicaulis) by Clark’s Nutcrackers (Corvidae: Nucifraga columbiana). he cones of Whitebark Pine do not open, so this conifer obligately depends on nutcrackers for dispersal (Tomback 1978, 2001;
Hutchins and Lanner 1982). Pine squirrels (Tamiasciurus spp.) are
important conifer-seed predators and compete with nutcrackers for Whitebark Pine seeds, but they contribute little or no seed
dispersal (Siepielski and Benkman 2008, McKinney et al. 2009).
Cronartium ribicola, an invasive fungal pathogen that causes white
pine blister rust, and regional outbreaks of native pine beetles have
produced precipitous declines in Whitebark Pine nearly rangewide;
this pine is currently being evaluated for federal listing as a threatened or endangered species (Tomback and Achuf 2010). he U.S.
Forest Service has undertaken restoration programs that involve
the planting of putative pathogen-resistant seedlings, grown from
seeds harvested from screened parent trees (e.g., Schwandt et al.
2010, Tomback and Achuf 2010). he cost of these restoration efforts essentially represents the valuation of natural seed-dispersal
activities throughout the range of the pine.
On the basis of igures obtained from two U.S. national forests, D. F. Tomback (unpubl. data) calculated the costs of planting
upper subalpine terrain with a typical density of Whitebark Pine
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— P ERSPECTIVES
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seedlings (440 ha–1). Ironically, a large part of the cost of obtaining
seeds requires that trees be climbed and cones caged in early summer to prevent nutcrackers from depleting the seeds and squirrels
from cutting down cones, and then climbed again in September
to harvest the cones. hese costs were reduced by assuming that
adequate numbers of seeds for a 1-ha planting could be harvested
from only one tree, although restoration eforts would actually require more genetic diversity. Other expenses, such as materials,
travel, and the cost of protecting trees each year from pine beetles
were excluded, whereas the costs of growing seedlings, planting
seedlings, and administrative oversight were included.
Replacing nutcracker seed-dispersal services costs the U.S.
Forest Service a minimum of $2,190 ha–1 in two national forests.
Whereas this seedling planting could be accomplished within one
ield season, D. F. Tomback (unpubl. data) used a study of postire
regeneration after the 1988 Yellowstone ires to estimate the average number of new seedlings per year that germinated per hectare
from natural seed caches (Tomback et al. 2001). She concluded that
it would take a minimum of 5 to 6 years in the Yellowstone area
for nutcrackers to produce 440 Whitebark Pine seedlings per hectare. Although this is slower, spreading regeneration over several
years may yield beneits by spreading risks over time (e.g., reducing risks of failure in a dry season, higher genetic diversity by including parents seeding in diferent years). However, given that the
nutcrackers would spread both pathogen-resistant and susceptible
genotypes, establishing 440 healthy trees per hectare under current conditions by way of nutcrackers would take additional time.
Vulture decline in South Asia.—he consequences of the recent catastrophic decline of vultures (three Gyps spp.) in South
Asia because of toxic livestock chemicals vividly demonstrate the
vital role that vultures play in ecosystems (Pain et al. 2003, Green
et al. 2004, Oaks et al. 2004). In the near absence of vultures, cattle
carcasses remained on the landscape for longer periods and were
available to other scavengers. As a result, populations of feral dogs
and other human-commensal facultative scavengers increased,
and diseases spread to humans and domestic livestock. Markandya et al. (2008) estimated that human health costs attributable
to population crashes of vultures in India totaled $34 billion over
the years 1993–2006. Additional cultural costs to the Parsi sects,
which rely on vultures for corpse cleansing, totaled $1.6 million
(Markandya et al. 2008).
R ESEARCH N EEDS
he overview of selected ecosystem services and case studies discussed above point to some very speciic research needs that are
outlined below. More generally, we lack basic information on all
the ways that birds could contribute to ecosystem services that ultimately beneit humans. Although we know in general the types of
ecosystem services that birds provide, we often lack suicient details of bird behavior and ecology to formulate models of ecosystem
valuation in a broader framework relevant to human well-being.
In addition to the more speciic research subjects noted below,
a topic that has received relatively little attention in the ecosystemservices literature is the economic costs of some bird activity. For
example, some birds may be crop pests (Elliott and Lenton 1989,
Dolbeer 1990, Basili and Temple 1999), disperse weed seeds (Williams 2006), damage property or livestock (Lowney 1999, Harding
O RNITHOLOGY —
7
et al. 2007), or generate noise and droppings in residential areas
(Gorenzel and Salmon 1995). Some research regarding birds as agricultural pests has shown that perceived damage can be greater
than actual damage (Basili and Temple 1999) or that the damage
can be minimized with appropriate management (Dolbeer 1990).
Crop pests also have beneicial efects, such as insectivory (Dolbeer 1990), and research on potential pest species needs to examine all the ecological roles that a bird ills in order to evaluate the
economic costs and beneits. Although a few bird species cause
economic damage, at the ecosystem level the services provided by
birds are overwhelmingly positive (Sekercioglu 2006a, Whelan et
al. 2008). More generally, payments for ecosystem services (PES)
are receiving increased attention in natural-resource management
practice and theory (e.g., Pagiola 2008, Farley and Costanza 2010,
Sommerville et al. 2010), and the recognition of ecosystem disservices (McCauley 2006) is also becoming more formalized (Lyytimaki et al. 2008, Dunn 2010, Power 2010). Very little of that work,
however, has been focused on organismal delivery of services and
costs (but see Nelson 2009), and it is important for ornithologists
to contribute to this line of research in the future.
Pest control.—he key aspect of pest control in need of further study is the extent to which trophic cascades have measurable
economic beneits in terms of increased plant growth or agricultural production. We know that top-down efects of bird foraging
are widespread, but most studies are still restricted to two trophic
levels: birds and their prey. More experiments involving all three
trophic levels (e.g., Marquis and Whelan 1994, Mols and Visser
2002, Johnson et al. 2010) are needed, especially in agroecosystems. Similarly, Fayt et al. (2005) concluded that woodpeckers can
regulate populations of insect pests of northern temperate conifer forests, but no studies have explicitly examined the economic
beneits to the timber industry of this interaction. Research examining the consequences of bird consumption of pests (arthropod
or rodent) for either crop yield or plant demographics would be
extremely useful if conducted within multiple agricultural ecosystems to determine generality and variability. his is a prime
example of an area of research where repetition aimed at establishing the generality of research, rather than aimed at “being irst”
or “novel,” needs to be encouraged by funding agencies. Another
aspect of pest control that avian ecologists (and funding agencies) should be poised to exploit is centered on unfortunate natural “experiments” like avian population declines in eastern North
America from West Nile virus (LaDeau et al. 2007). Research on
potential consequences (e.g., increases in human diseases carried by insects) of those population declines on ecosystem function and provision of ecosystem services would be very useful and
instructive.
Other useful avenues for research involve determining the feasibility and efectiveness of habitat manipulations that boost either
populations of key avian pest consumers (e.g., deploying nest boxes)
or their efectiveness as pest consumers (e.g., providing perches
for foraging). hese sorts of manipulations should be a standard
component of any integrated pest management (IPM) plan. Additionally, we need cost–beneit analyses of the efectiveness of
such manipulations, at least in agroecosystems, and cost–beneit
comparisons of bird control versus chemical control mechanisms
with large externalities (i.e., pesticides). Moreover, studies that examine the efectiveness of such manipulations must incorporate
8
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efects from the framework of “landscapes of fear” (Laundré et al.
2001). For example, perches may alter the behavior of small rodents
through their increased fear, thus restricting their foraging, even if
rodent population size does not decline markedly.
A few studies have suggested that avian granivores exert
weed control, but these studies need to examine the efects on
an agricultural crop or other plants. Exclosure experiments are
needed to carefully document birds’ seed consumption in a variety of contexts, from natural communities to agroecosystems
to restoration projects. In areas where birds are considered pests
(e.g., Basili and Temple 1999), careful documentation of trophic
function would be useful—birds may, for example, consume seeds
of crops, but may compensate via consumption of pest insects.
Dispersal and pollination.—he key remaining questions
about dispersal and pollination are largely very hard to answer.
We need more information on the mechanisms (preferably from
manipulative experiments) over the whole life cycle of the plants.
Unresolved topics include (1) how various factors, including frugivores (birds and mammals), seed predators, pathogens, habitat
fragmentation, and plant competitors, interact to determine plant
reproductive success; (2) how widespread density- and distancedependent seed and seedling mortality efects are (so-called JanzenConnell efects), both in the tropics and in the temperate zone
(Packer and Clay 2000), because these greatly increase dependence on dispersers; (3) the level of change in dispersal services
and its impacts at the plant community level following hunting,
habitat fragmentation, disturbance such as ire, or other anthropogenic change; (4) the extent of seed limitation, which determines whether pollination limitation matters (Kelly et al. 2007);
and (5) more studies to determine whether the unexpected importance of bird pollination to plants with lowers that are apparently
suited to insect pollination in temperate New Zealand (Kelly et al.
2010) applies in other areas.
Birds disperse seeds of native and non-native plant species
and in some areas play a role in the spread of invasive plants (Sallabanks 1992, Vila and Dantonio 1998, Renne et al. 2002, Cordeiro
et al. 2004, Gosper et al. 2005, Bartuszevige and Gorchov 2006,
Milton et al. 2007, Underhill and Hofmeyr 2007). Such dispersal is
not necessarily detrimental—the non-native plant species themselves may provide ecosystem services, such as erosion control or
aesthetics. he question becomes whether the beneits of seed dispersal outweigh their detrimental efects. he situation is complicated further when non-native plants are dispersed by non-native
birds such as European Starlings (Sturnus vulgaris) in North
America and European Blackbirds (Turdus merula) in New Zealand (Williams 2006). More work is needed on dispersal of nonnative plant species in an ecosystem-services framework. As with
other ecological processes, if we understand the speciics we will
be better able to develop realistic valuation models.
Scavengers.—Unfortunately, the value provided by ecosystem
services is most apparent after their loss. he catastrophic ecological and human-health ramiications created by the recent collapse of vulture populations in India (Markandya et al. 2008) have
revealed the importance of ecosystem services provided by carrion-feeding birds. It is clear that in some areas proper ecosystem
function is dependent, in part, on scavenging birds. Even so, the
cycling of carrion biomass, whether by scavenging or decomposition, is a complex process governed by an intense competition
ET AL .
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for carcasses among vertebrates, insects, fungi, and microbes
(DeVault et al. 2003, 2004; Selva et al. 2005; Selva and Fortuna
2007; Parmenter and MacMahon 2009). Habitat type, climate,
carcass type, composition of the vertebrate community, and other
biotic and abiotic factors all inluence competition for carrion
(DeVault et al. 2003). In some situations, the competitive balance
for carrion is shifted naturally away from birds, toward insects
and microbes (e.g., DeVault et al. 2004) or facultative mammalian
scavengers (e.g., Putman 1983). Future research aimed at identifying the conditions under which various taxa consume carrion
would be beneicial. Such work would help elucidate vital links
between ecosystem health and the population status of various
vertebrates, such as the vulture–cattle carrion system in India.
Future investigations into the scavenging ecology of birds would
also improve our understanding of disease ecology (Jennelle et
al. 2009), nutrient transport across ecosystem types (Polis et al.
2004), and the distribution of predators and their prey (CortesAvizanda et al. 2009a, b).
CONCLUSIONS
Birds provide many ecosystem services, which by and large are
invisible and underappreciated. Several sudden losses of such services (e.g., carrion scavenging in India, pest control in China when
sparrows were locally exterminated, forest plant pollination in
New Zealand) provide a sense of the negative consequences should
such services be lost. We suggest that ecosystem services be better studied and valued properly to ensure that humans continue
to receive the beneits, and that birds continue to provide them.
he case studies presented here show promising lines of research,
but much work remains to be done. Despite the huge role of birds
as insectivores, very little research has been done on insectivory
in an ecosystem-services context (pest control), and most of what
has been done is on pest control in cofee plantations. Similarly,
the ecosystem service of seed dispersal has been quantiied only
for seed-caching corvids. Dispersal of woody plants by terrestrial
frugivores and dispersal of aquatic plants by waterfowl have not been
addressed. We are not aware of any ecosystem-services valuation
research on the role of birds in nutrient cycling or as ecosystem
engineers. Further research to better understand the economic
value of birds will enable better policy and restoration practices,
promote and justify bird conservation eforts, and ultimately demonstrate the vital connections among human well-being, intact
ecosystems, and the preservation of avian biodiversity.
ACKNOWLEDGMENTS
his paper is based, in part, on a symposium held at the joint AOU,
COS, CSO meeting in San Diego in February 2010. We thank the
organizers of that conference for supporting our participation
at the symposium. hanks to W. Gibbons, N. Lichti, D. Shealer,
S. Zack, and the lab group of J. Brown for many helpful comments
on the manuscript. D.K. is grateful for funding from the New
Zealand Foundation for Research, Science and Technology under
contracts CO9X0004 and CO9X0503. D.F.T. thanks M. Jenkins,
U.S. Department of Agriculture (USDA) Forest Service, Flathead
National Forest, and E. Davy, USDA Forest Service, Bridger-Teton
National Forest, for providing the costs associated with whitebark
J ANUARY 2011
— P ERSPECTIVES
IN
pine restoration projects. C.J.W. gratefully acknowledges R. Marquis
for his contributions to past research and ongoing, critical discussions on ecosystem services. C.S. thanks the Christensen Fund
for support.
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Received 29 October 2010, accepted 7 December 2010.