Ecosystem Services Provided by Birds
Christopher J. Whelan,aDaniel G. Wenny,b
and Robert J. Marquisc
aIllinois Natural History Survey, Midewin National Tallgrass Prairie,
Wilmington, Illinois, USA
bLost Mound Field Station, Illinois Natural History Survey, Savanna, Illinois, USA
cDepartment of Biology, University of Missouri-St. Louis, St. Louis, Missouri, USA
Ecosystem services are natural processes that beneﬁt humans. Birds contribute the
four types of services recognized by the UN Millennium Ecosystem Assessment—
provisioning, regulating, cultural, and supporting services. In this review, we con-
centrate primarily on supporting services, and to a lesser extent, provisioning and
regulating services. As members of ecosystems, birds play many roles, including as
predators, pollinators, scavengers, seed dispersers, seed predators, and ecosystem en-
gineers. These ecosystem services fall into two subcategories: those that arise via be-
havior (like consumption of agricultural pests) and those that arise via bird products
(like nests and guano). Characteristics of most birds make them quite special from the
perspective of ecosystem services. Because most birds ﬂy, they can respond to irrup-
tive or pulsed resources in ways generally not possible for other vertebrates. Migratory
species link ecosystem processes and ﬂuxes that are separated by great distances and
times. Although the economic value to humans contributed by most, if not all, of the
supporting services has yet to be quantiﬁed, we believe they are important to humans.
Our goals for this review are 1) to lay the groundwork on these services to facilitate
future efforts to estimate their economic value, 2) to highlight gaps in our knowledge,
and 3) to point to future directions for additional research.
Key words: birds; ecosystem engineering; ecosystem services; excavation; guano; nests;
pest control; pollination; reciprocal nutrient ﬂuxes; scavenging; seed dispersal
Birds are both visually and acoustically con-
spicuous components of ecosystems. Birds at-
tract attention. But ecologically, do birds mat-
ter? We know from two classic studies in the
1970s that birds may contribute rather little
to overall ecosystem productivity (Wiens 1973;
Holmes & Sturges 1975). Do birds therefore
live off the fat of the land, contributing little to
ecosystem function (Wiens 1973)? Or, despite
their small contribution to productivity, could
their place within food webs allow birds to im-
Address for correspondence: Christopher J. Whelan, Illinois Natural
History Survey, Midewin National Tallgrass Prairie, 30239 South State
Highway 53, Wilmington, IL 60481 Voice: +1-815-423-6370-250; fax:
pact ecosystem function, and often in surprising
ways (Holmes & Sturges 1975; Holmes 1990)?
In the intervening decades many studies have
examined various roles of birds in ecosystems
throughout the world. We now have a much
greater appreciation of the ways that birds func-
tion within numerous ecosystems. As members
of ecosystems, birds play many roles, includ-
ing as predators, pollinators, scavengers, seed
dispersers, seed predators, and ecosystem engi-
neers (Sekercioglu 2006).
“Ecosystem services” are natural processes
that beneﬁt humans. For instance, honeybees
pollinating orchards provide a service that ben-
eﬁts humans through the production of ap-
ples. In contrast, native bees pollinating milk-
weeds provide a service for the milkweed—they
facilitate its reproduction. Both are services,
Ann. N.Y. Acad. Sci. 1134: 25–60 (2008). C
2008 New York Academy of Sciences.
doi: 10.1196/annals.1439.003 25
Annals of the New York Academy of Sciences
but only the former can reasonably be argued
to have a direct or extrinsic beneﬁt for hu-
mans. Wallace (2007) reviews problems con-
cerning the classiﬁcation of ecosystem ser-
vices. Here, we follow the United Nations
Millennium Ecosystem Assessment (2003; see
also Kremen & Ostfeld 2005), which dis-
tinguishes four principal types of ecosystem
•Provisioning services, such as production
of ﬁber, clean water, and food;
•Regulating services, obtained through
ecosystem processes that regulate climate,
water, and human disease;
•Cultural services, such as spiritual enrich-
ment, cognitive development, reﬂection,
recreation, and aesthetics;
•Supporting services, which include all
other ecosystem processes, such as soil for-
mation, nutrient cycling, provisioning of
habitat, and production of biomass and
Birds contribute all four types of services.
Provisioning services are provided by both
domesticated (poultry) and nondomesticated
species. Nondomesticated birds have been im-
portant components of human diets historically
(Moss & Bowers 2007), and many are still to-
day (Peres 2001). In developed countries, many
are hunted for consumption and sport (Ben-
nett & Whitten 2003). Bird feathers provide
bedding, insulation, and ornamentation. Scav-
engers contribute regulating services, as efﬁ-
cient carcass consumption helps regulate hu-
man disease. Via art, photography, religious
custom, and bird watching, birds contribute
cultural services. Bird watching, or birding, is
one of the most popular outdoor recreational
activities in the United States and around the
world. In the United States, in 2001, 45 mil-
lion bird watchers spent $32 billion in retail
stores, generating $85 billion in overall eco-
nomic impact, and supporting over 860,000
jobs (LaRouche 2001; see also Sekercioglu
2002). Birds contribute supporting services, as
their foraging, seed dispersal, and pollination
activities help maintain ecosystems throughout
In this paper, we concentrate primarily on
supporting services, and to a lesser extent, pro-
visioning and regulating services. Because we
are interested primarily in the ecological impact
of birds, we will not consider cultural services.
Supporting services arise through the myriad
functional roles that birds play in ecosystems.
These ecosystem services fall into two subcat-
egories: those that arise via behavior (like con-
sumption of agricultural pests) and those that
arise via bird products (like nests and guano).
Currently, the economic value to humans con-
tributed by most, if not all, of the supporting
services has yet to be quantiﬁed. Nevertheless
we believe that these services are important,
in some cases vitally important, to the human
enterprise. One goal of this paper is to lay the
groundwork on these services that may facil-
itate future efforts to estimate their economic
value. A second goal is to highlight gaps in our
knowledge and point to future directions for
Why Birds Are Unique
Characteristics of most birds make them
quite special from the perspective of ecosys-
tem services. Most birds ﬂy, so most are highly
mobile, with high mass-speciﬁc metabolic rates
(and, hence, high metabolic demands). These
characteristics allow birds to respond to irrup-
tive or pulsed resources in ways generally not
possible for other vertebrates. Their mobility
also allows them to leave areas in which re-
sources are no longer sufﬁcient. Because many
species are migratory, birds link ecosystem pro-
cesses and ﬂuxes that are separated by great
distances and times. Different bird species ex-
hibit a wide range of social structure during any
given phase of the annual cycle. For example,
many species are territorial when breeding, but
others breed colonially. Finally, in many bird
species, social structure changes drastically be-
tween breeding and nonbreeding phases of the
annual cycle. For many such species, breeding
Birds and Ecosystem Services
communities are composed of individual pairs
of relatively low density owing to intraspe-
ciﬁc (and sometimes, interspeciﬁc) territorial-
ity. In the nonbreeding season, these species
may form heterospeciﬁc ﬂocks that can attain
extremely high densities. Such differences in so-
cial structure can lead to very large differences
in avian impact on the environment.
Most of the ecosystem services we consider
here result from bird behavior, speciﬁcally, for-
aging behavior. Among the nearly 10,000 bird
species on the planet, we ﬁnd species that con-
sume virtually every imaginable resource, in
aquatic, terrestrial, and aerial environments,
from remote oceanic islands to every continent.
Many services and ecosystem functions are thus
the consequence of resource consumption.
A pest-control agent must do more than
simply consume the pest species. The control
species must affect the population of the pest
species sufﬁciently that there is a positive impact
on the resource that the pest itself consumes.
The impact should be evident either through
some measure of the abundance and/or the
ﬁtness of the resource, or, when the resource
is an agricultural crop, as an increased yield
and/or economic proﬁt derived from the crop.
Bird–crop interactions fall under the domain of
Economic ornithology launched in the
United States in 1885 with a small Congres-
sional appropriation within the USDA for “the
study of the interrelation of birds and agricul-
ture, an investigation of the food, habits, and
migrations of birds in relation to both insects
and plants” (Henderson & Preble 1935). Early
efforts focused on food habits of species pre-
sumed to be either beneﬁcial or detrimental
to agriculture, including granivorous and in-
sectivorous songbirds as well as birds of prey
(Fisher 1893; Weed & Dearborn, 1903; Erring-
ton 1933; McAtee 1935; Martin et al. 1951).
Such food habit studies, while informative, can-
not reveal the functional signiﬁcance of bird
diets, because they do not measure impacts on
either the prey population itself or the resources
of the prey.
Interest in the economic role of birds as pest-
control agents receded as agriculture became
more mechanistic, large scale, and dependent
upon the rapidly growing availability of effec-
tive pesticides (see Kirk et al. 1996). Current
interest in the functional roles of birds arose
from two complementary concerns. First, de-
bate over factors, such as food competition
and predation, as structuring mechanisms of,
ecological communities (see Amer Nat 122,
1983: A Round Table on Research in Ecology
and Evolutionary Biology) spurred renewed in-
terest on impacts of birds (and other animals)
on their food resources (Rodenhouse & Holmes
1992). Second, concern over declining popula-
tions (Ambuel & Temple 1983; Robbins et al.
1989; Terborgh 1989; Askins et al. 1990) in-
creased interest in the potential consequences
of those declines (Askins 1995; Whelan & Mar-
quis 1995; Martin & Finch 1995; Sekercioglu
et al. 2004).
Quantifying the impact of bird predation
on arthropods typically involves cages that ex-
clude birds from their foraging substrates, or
less commonly, deploying perches and nest
boxes to increase their abundance. Askenmo
et al. (1977) used net exclosures to determine
that bird predation decreased densities of over-
wintering spiders in northern spruce forests.
Solomon et al. (1977) placed logs containing
coddling moth (Cydia pomonella) cocoons in ap-
ple orchards. They found that logs caged in
wire netting to exclude birds experienced al-
most no losses of cocoons over winter and
spring, but losses on uncaged logs accessible
to birds exceeded 90%. Holmes et al. (1979)
used experimental exclosures to assess the im-
pact of birds on arthropods during the breed-
ing season. They found that birds signiﬁcantly
Annals of the New York Academy of Sciences
reduced densities of Lepidoptera larvae on for-
est understory vegetation. The largest impacts
coincided with nestling and ﬂedgling periods of
the nest cycle. Joern (1986) demonstrated exclu-
sion of birds in grasslands increased densities
and diversity of grasshoppers (Orthoptera).
These early exclosure experiments presented
compelling evidence that birds can depress
abundance of at least some arthropod prey.
But they assessed only the predators (birds) and
their prey (arthropods, especially herbivorous
insects). Insect pest predators need not be insect
pest control agents, as reductions in pests may
not translate into reductions in pest damage.
Atlegrim (1989) documented the effect of
birds on plant performance: leaf damage to bil-
berry (Vaccinium myrtillus) increased signiﬁcantly
in their absence. Bock et al. (1992), however,
found that birds signiﬁcantly reduced grasshop-
per densities in Arizona grassland, but those ef-
fects did not cascade measurably to the plants
fed upon by them. In contrast, Marquis and
Whelan (1994), working in Missouri oak forest,
found that excluding birds from sapling white
oak (Quercus alba) signiﬁcant increased density of
leaf-damaging insects and leaf damage, which
in turn decreased production of new biomass
in the subsequent growing season.
We now know that such top-down effects
are widespread though not universal. Although
most studies of impacts of birds on arthro-
pods are still restricted to those two trophic
levels, there are now investigations of all three
trophic levels in a variety of both natural and
agro-ecosystems, and in both terrestrial and
aquatics habitats (Table 1). Studies in agri-
cultural systems vary from coffee plantations
(Greenberg et al. 2000; Philpott et al. 2004) to
ephemeral Brassica (broccoli, cauliﬂower) ﬁelds
(Hooks et al. 2003). Perhaps the most exciting
example comes from Dutch apple orchards.
Mols and Visser (2002) reported that emplace-
ment of nesting boxes to attract great tits (Parus
major) reduced caterpillars and fruit damage
and increased fruit yield. The increase in yield
was striking, from 4.7 to 7.8 kg apples per tree,
an astonishing increase of 66%.
Owing to mobility, many bird species can re-
spond to temporally and/or spatially disjunct
bonanzas of arthropods. An early case was re-
ported by Mormon pioneers newly settling near
the Great Salt Lake in Utah in 1848 (Schwarz
1998). In late May, their crops were attacked
by “millions” of crickets, which “took every-
thing clean.” Near disaster was averted when,
in answer to the Mormon’s prayers, “...sea
gulls have come in large ﬂocks” and destroyed
the crickets. In their review, Kirk et al. (1996)
mention several additional anecdotal reports
of birds responding to “outbreak” situations.
They conclude (p. 227) that, “while the amount
of detail included in some of the reports makes
it difﬁcult to dismiss them,” the frequency and
effectiveness for control or regulation remains
Nonetheless, numerical responses to high
arthropod populations are well known. Stewart
and Aldrich (1951) attempted to remove birds
from an experimental area in Maine undergo-
ing an outbreak of the spruce budworm moth
(Choristoneura fumiferana Clem). Despite consid-
erable effort, birds continually repopulated the
experimental area, leading the authors to con-
clude that a large number of nonterritorial
birds (ﬂoaters) were available in the surround-
ing area. Alternatively, birds may have gradu-
ally moved into this area of outbreaking bud-
worms. MacArthur (1958) and Morse (1978)
also noted movements in response to spruce
Gale et al. (2001) examined response of birds
to outbreaks of gypsy moth (Lymantria dispar)
in some eastern states. Yellow-billed cuckoos
(Coccysus americana), black-billed cuckoos (C.ery-
thropthalmus), and indigo buntings apparently
responded positively to the outbreaks, but few
other responses were observed. Similarly, Bar-
ber et al. (2008) found that gypsy moth defolia-
tion events in eastern United States and adja-
cent Canada affect regional movements and
distribution of yellow-billed and black-billed
cuckoos, drawing them in from long distances.
How cuckoos detect local defoliation events is
unknown, but they may rely on postmigration
Birds and Ecosystem Services
TABLE 1. Investigations of top-down effects
of birds on herbivorous insects by habitat
Habitat effects? effects?
Perfecto et al. (2004) yes NT
Jones et al. (2005) yes NT
Philpott et al. (2004) yes NT
Hooks et al. (2003) yes yes
Mols and Visser (2002) yes yes
Greenberg et al. (2000) yes NT
Boyer et al. (2003) yes no
Sipura (1999) yes yes
Bailey and Whitham (2003) yes yes
Bailey et al. (2006) yes yes
Mooney (2007) yes yes
Mooney (2006) yes yes
Mooney and Linhart (2006) yes yes
Gonzalez-Gomez et al. (2006) yes yes
Recher and Majer (2006) yes NT
Cornelissen and Stiling (2006) no no
Mantyla et al. (2004) yes NT
Mazia et al. (2004) yes variable
Medina and Barbosa (2002) yes NT
Lichtenberg and yes no
Sanz (2001) yes yes
Jantti et al. (2001) yes NT
Strong et al. (2000) yes no
Murakami and Nakano (2000) yes yes
Forkner and Hunter (2000) yes no
Murakami (1999) yes no
Gunnarsson and Hake (1999) yes NT
Gunnarsson (1996) yes NT
Boege and Marquis (2006) yes yes
Terborgh et al. (2006) yes yes
Van Bael and Brawn (2005) yes variable
Gruner (2004) yes no
Van B a e l et al. (2003) yes NT
Strengbom et al. (2005) yes NT
Tanhuanpaa et al. (2001) yes NT
Habitat effects? effects?
Hori and Noda (2007) yes NT
Ellis et al. (2007) yes likely
Snellen et al. (2007) yes likely
Hargrave (2006) yes likely
Wootton (1997) yes NT
Wootton (1995) yes yes
Wootton (1992) yes yes
Ellis et al. (2005) yes yes
Hamilton et al. (2006) yes no
Hamilton and Nudds (2003) yes (weak) NT
Hori and Noda (2001) yes NT
Hamilton (2000) yes no
Coleman et al. (1999) yes NT
Investigations were identiﬁed by using Web of Science
to ﬁnd published studies that cited Wootton (1992) and
Marquis and Whelan (1994). NT, not tested.
nomadic movements in spring (Hughes 1999,
2001). Studies showing local aggregation in re-
sponse to insect outbreaks or defoliation events
do not themselves provide evidence for control
or regulation of the insect. They do illustrate
the ability of some specialized bird species to re-
spond to the outbreaks, demonstrating at least a
potential to reduce insect outbreaks. At least in
some places or times, such numerical responses
may also help regulate those pest populations.
Fayt et al. (2005) reviewed the considerable
literature on response and predation of wood-
peckers on bark beetles (Coleoptera, Scolyti-
dae) infecting spruce (Picea). They conclude,
based on the trifecta of empirical observa-
tion, exclosure experiments, and modeling,
that woodpeckers are capable of regulating
these important forest pests. Many studies
show both strong numerical and functional
responses of woodpeckers to bark beetle in-
festations that reduce bark beetle outbreaks
and contribute to regulation of bark beetle
populations. Although all Picoides woodpeckers
Annals of the New York Academy of Sciences
studied show such responses, the three-toed
woodpecker (Picoides tridactylus) appears most
responsive. Budworm outbreak effects range
from reduction in growth of individual trees
to death of vast forest stands. Affected trees
often succumb to secondary infestations of in-
sects and diseases. Infested trees, regardless of
survival, often suffer growth abnormalities that
reduce their value as timber. Consequently, the
economic impact of defoliation by pests, such as
budworms, from loss of timber yields and costs
of control measures may exceed a billion dol-
lars per year (Ayres & Lombardero 2000). Al-
though we know of no estimate of the economic
value of woodpeckers in the budworm–forest
interaction, by regulating budworm popula-
tions and reducing the frequency of outbreaks,
woodpeckers must contribute substantially to
the economic value of timber harvested from
spruce-ﬁr forest ecosystems around the world.
Bird-driven, top-down trophic cascades are
not restricted to terrestrial systems. Woot-
ton (1992) excluded avian predators from a
rocky intertidal community. In the absence of
avian predation, abundance of one herbivo-
rous limpet species increased, which in turn
decreased foliose algae. Algal cover was also
indirectly related to abundance of competitors
for space. Hence birds affect abundance of al-
gae via two different interaction chains (her-
bivory and space competition). Other studies
have found top-down effects of birds in rocky
intertidal communities and in intertidal mud-
ﬂats (Table 1). Although these studies demon-
strate top-down effects, as none of the species is
considered a pest, these studies do not demon-
strate pest control. In sum, many investigations
in terrestrial and aquatic habitats, both natu-
ral and human-dominated, ﬁnd that bird pre-
dation decreases invertebrate prey populations.
Most studies that examined cascading effects of
birds on plants found them, in some cases, with
positive economic consequences for humans. In
stark contrast, bird persecution may have dev-
astating consequences. Although information
is only anecdotal, apparently the “war against
the sparrows,” part of a pest-control campaign
launched in China during Mao Zedong’s Great
Leap Forward, led to massive increases in pest
insects and, thus, crop damage, ultimately con-
tributing to a catastrophic famine from 1958–
1962 in which 30 million Chinese died from
starvation (Becker 1996).
In the late nineteenth century, many peo-
ple believed that birds of prey were detrimental
to agriculture through predation of poultry or
game birds (Allen 1893). Early reports from
the USDA Division of Ornithology and Mam-
malogy on food habits of the common hawks
and owls of the United States (e.g., Fisher 1893)
helped to change that perception: most hawks
and owls were far more helpful than injurious
to the farmer or “poulterer.” Rodents, rabbits,
hares, snakes, and insects were vastly more im-
portant prey items than chickens or game.
Given the preponderance of rodents in the
diets of many raptors (both hawks and owls), it
seems reasonable to assume that these birds
beneﬁt agriculture. Moreover, several raptor
species readily occur in agricultural landscapes
(Williams et al. 2000). However, few studies
have directly assessed effects of birds of prey
as agricultural rodent-control agents, and the
results are somewhat ambiguous. In fact, al-
though rodent-control measures (such as ro-
denticides and integrated pest management)
are used widely, surprisingly few studies have
assessed effects of rodents on agricultural pro-
duction (Brown et al. 2007). Nonetheless, there
are examples of rodents having strong effects
in agricultural crops (Brown et al. 2007), nat-
ural plant communities (Ostfeld & Canham
1993; Cote et al. 2003; Lopez & Terborgh 2007),
and newly established synthetic prairie gardens
(Howe & Brown 1999, 2001; Howe et al. 2002).
Wood and Fee (2003) reviewed rat-control
efforts in Malaysian agriculture, including de-
ployment of nest boxes to boost populations
of barn owls (Tyto alba). They concluded that
the evidence is inconsistent and the effect of
owls warrants further investigation. Marti et al.
(2005) concur: barn owls clearly eat many
Birds and Ecosystem Services
rodent agricultural pests, but whether this
consumption is sufﬁcient to beneﬁt agricultural
production remains unknown. They cite Marsh
(1998), who, in a data-free paper, “rejected the
idea that attracting nesting barn owls offered
any hope of rodent control.” In contrast, Kay
et al. (1994) found that placing perches around
soy bean ﬁelds in Australia increased the num-
ber of diurnal raptors around and over the
ﬁelds, which in turn decreased mouse (Mus do-
mesticus) population growth rate and the maxi-
mum mouse population density attained in the
ﬁelds. The effect was greater when perches
were placed 100 m apart than 200 m apart.
Other studies demonstrated that provisioning
artiﬁcial perches attracts other birds of prey
(Wolff et al. 1999; Shefﬁeld et al. 2001), including
kestrels (Falco sparverius), suggesting again that
this method may enhance or concentrate forag-
ing in potentially beneﬁcial ways. Clearly, pro-
visioning with nest boxes and artiﬁcial perches
to attract and facilitate birds of prey deserves
careful experimentation in agricultural settings.
Such measures could also potentially enhance
early plant community restorations (Howe et al.
Most investigations of predation by raptors
on rodents center on the predators’ potential
role in cyclic population dynamics. From these
studies we know much about the predator–
prey interactions of many raptor species and
many rodent species. For instance, European
kestrels (Falco tinnunculus), short-eared owls (Asio
ﬂammeus), and long-eared owls (Asio otus)ex-
hibit strong numerical and functional responses
to Microtus (M. agrestis and M.epiroticus)voles
(Korpimaki & Norrdahl 1991). The number
of breeding pairs of each species ﬂuctuated
in concordance with spring vole density, and,
via rapid immigration and emigration, they
tracked vole population ﬂuctuations without
time lags. Spring density of Microtus was pos-
itively correlated with the percentage of Mi-
crotus in the raptors’ diet. Such results suggest
the potential for raptor regulation of Microtus
in this system. Yet other studies have found
that predator exclusion can reverse the decline
phase in the microtine population cycle (Kor-
pimaki & Norrdahl 1998). Indeed, in contrast
to the ambiguous results from efforts to boost
raptor numbers or foraging with nest boxes or
perches, predator exclusion generally produces
clear and dramatic effects. On predator-free is-
lands created by a hydroelectric impoundment
in Venezuela, densities of rodents, howler mon-
keys, iguanas, and leaf-cutter ants were 10 to
100 times greater than on the nearby main-
land, and seedlings and saplings of canopy trees
were severely reduced, evidence of a trophic
cascade (Terborgh et al. 2001, 2006). These
and many other studies present strong evidence
that avian (and other) predators can have strong
and density-dependent effects on rodent popu-
lations, which further suggests further the po-
tential to exert population control or regulation.
Avian and terrestrial rodent predators may
facilitate each other. Kotler et al. (1992, 1993)
demonstrated predator facilitation between
owls and desert diadema snakes (Spalerosophus
diadema) feeding on gerbils (Gerbillus allenbyi and
G. pyramidum). Owls drive gerbils to cover, the
preferred habitat of the snake. Such effects lead
to predation on rodents even though the raptor
itself is not directly responsible for it. Similarly,
Korpimaki et al. (1996) found predator facilita-
tion between least weasel (Mustela nivalis)and
European kestrel, suggesting that “the assem-
blage of predators subsisting on rodent prey
may contribute to the crash of the four-year
vole cycle.” To paraphrase Kotler et al. (1992):
rodents shifting habitat to avoid an owl may
wind up in the fangs of a snake (and vice versa).
Taken together, available evidence thus sug-
gests that raptors exert strong and regulat-
ing predation on rodents under some circum-
stances. Various management activities can
likely increase their effectiveness as rodent
predators in cultivated and natural landscapes.
These include provisioning of nesting boxes or
platforms to increase potential nesting oppor-
tunities to boost breeding populations, provi-
sioning perches to increase or concentrate for-
aging activities, and elimination of persecution
(Kirkpatrick & Elder 1951; Van Maanen et al.
Annals of the New York Academy of Sciences
2001). These propositions are each amenable
to empirical veriﬁcation or rejection, and pro-
vide numerous avenues for applied ecological
Many bird species are granivores. As anyone
with a backyard bird feeder knows, daily and
seasonal seed consumption can be prodigious.
Could bird granivores contribute to control of
weedy plant species by virtue of seed consump-
tion? To date, most investigations approach the
interaction from a different perspective: What
habitat characteristics attract granivorous bird
species to agro-ecosystems (e.g., Robinson &
Sutherland 1999; Wilson et al. 1999; Moorcroft
et al. 2002; Gibbons et al. 2006)?
Several studies quantiﬁed consumption of
weed seeds by a number of consumers, includ-
ing granivorous birds, in agricultural settings.
Small mammals and invertebrates appear to
be the most important consumers of seeds in
these ecosystems. However, Holmes and Froud-
Williams (2005) found substantial consumption
of weed seeds by avian granivores, especially in
cropped areas of cereal ﬁelds, and in spring.
Still, avian consumption was signiﬁcantly less
than that of mammals. However, avian and
mammalian seed consumption were additive,
totaling almost 100% of the seeds at the soil
surface. These studies indicate a need for fur-
ther investigation of the roles of granivorous
birds as potential pest control agents of weedy
plant species in cultured ecosystems. For in-
stance, Howe and Brown (1999) found positive
density-dependent seed consumption. How fre-
quently is avian seed consumption density de-
pendent? Does density-dependent seed con-
sumption vary with bird species, habitat type,
and seed species available?
Holmes and Froud-Williams (2005) suggest
that recruitment of avian granivores into inte-
grated weed-management programs would re-
duce the need for herbicides, chemicals that
carry their own costs and potential negative
environmental effects. Research now needs to
investigate practical steps that would accom-
plish such recruitment. Obvious and critical
processes are habitat selection (Whittingham
et al. 2007), diet selection (Wilson et al. 1999;
Holland et al. 2006), and harvest rate—the
functional response (Whittingham & Markland
2002). In addition, many bird species once
common in agricultural landscapes have un-
dergone population declines in recent decades
(U.S.: Valiela & Martinetto 2007; Europe: Don-
ald et al. 2001; Japan: Amano & Yamaura 2007).
We need to know, ﬁrst, how these declines
may affect aggregate weed seed consumption
by avian granivores, and second, how we can
halt or even reverse such declines (Wilson et al.
Current research shows, unsurprisingly, that
different suites of bird species found in agro-
environments are favored by different aspects
of the habitat. In general, these afﬁnities seem
to reﬂect attraction to or avoidance of relatively
open versus closed habitats. The key factor is
how different species trade off food and safety
(safety may include safety from nest preda-
tors). Lima and Valone (1991) provide a use-
ful framework, pointing out that some species
are “cover-dependent” while others are “cover-
independent.” With this framework, can we
manipulate agro-environments in ways that
provide for a diversity of granivorous birds
while maintaining vigorous agricultural pro-
duction? Milsom et al. (1998) consider related
issues with respect to wading birds inhabiting
coastal grasslands in England.
In contrast to patterns found in agro-
ecosystems, some research on granivory in nat-
ural ecosystems found relatively greater con-
sumption of seeds by birds than by either small
mammals or by insects. These include the
Monte Desert in Argentina (Lopez De Case-
nave et al. 1998; Saba & Toyos 2003), miombo
woodland in Zimbabwe (Linzey & Washok
2000), and coastal steppe chaparral in north-
ern Chile (Kelt et al. 2004). Research in these
systems may point to environmental factors
that enhance the relative importance of avian
granivores. Identiﬁcation of such factors may
suggest habitat modiﬁcations or manipulations
Birds and Ecosystem Services
that may enhance avian granivory in agro-
Additional research should identify the
importance of avian granivores in agro-
ecosystems. How does prevalence of weeds in
areas with known recent reductions of avian
abundance and diversity compare with areas
containing abundances and diversities typical
of pre-decline? Many avian “granivores” are
only seasonally so: many species switch between
consuming predominantly seeds in the non-
breeding season to consuming predominantly
arthropods in the breeding season. It would be
of great interest to determine if attraction of
such species contributes to control of herbiv-
orous insects (when consuming predominantly
arthropods) in the growing season even if con-
trol of weed seeds is minimal in winter (when
consuming predominantly seeds).
Many plants depend on pollination by ani-
mals for successful seed set. Over 920 species of
birds pollinate plants, including hummingbirds
(Trochilidae) in the Americas, sunbirds (Nec-
tarinidae) in Africa, false-sunbirds (Philepitti-
dae) in Madagascar, ﬂowerpeckers (Dicaeidae)
and white-eyes (Zosteropidae) in southern Asia,
honeyeaters (Melphagidae) and lories (Lori-
dae) in Australasia, and Hawaiian honeycreep-
ers (Drepanididae) in Hawaii (Stiles 1981).
In southwestern Spain, three species of war-
blers (Sylvidae) pollinate the only native species
of bird-pollinated plant known in Europe
(Ortega-Olivencia et al. 2005), although some
non-native plant species may be pollinated by
birds (Burquez 1989). Most bird pollination
should be considered supporting services (Kre-
men & Ostfeld 2005).
In neotropical rainforests the proportion of
nectarivores in the avifauna ranges from 7.4%
in Costa Rica to 4% in Brazil and Peru (Karr
et al. 1990). Within Costa Rica, nectarivores
comprise 6% of avifauna in tropical dry for-
est and 10% in montane forests (Stiles 1985).
The majority of agricultural crops are polli-
nated by insects, but birds pollinate approx-
imately 5.4% of 960 cultivated plant species
with known pollinators (Nabhan & Buchmann
1997). Among noncultivated plants, most bird-
pollinated species are shrubs and epiphytes, but
some tree species are bird pollinated, especially
in Australasia. The number of plant species pol-
linated by birds is typically 5% of a region’s
ﬂora and up to 10% on islands (Stiles 1985;
Kato & Kawakita 2004; Anderson et al. 2006;
Bernardello et al. 2006). In New Guinea, Brown
and Hopkins (1995) found approximately 20%
of tree species in a 3 ha site were visited by
nectar-feeding birds, and 13% of the avifauna
visited ﬂowers, suggesting that nectarivorous
bird species may be more prominent locally
than regionally (Brown & Hopkins 1995).
Like seed dispersal mutualisms, pollination
interactions are characterized by much over-
lap and redundancy; examples of plant species
entirely dependent on only one species of pol-
linator are rare (Feinsinger 1983). Neverthe-
less, pollination mutualisms are more tightly
coevolved than those in seed dispersal (Wheel-
wright & Orians 1982; Johnson & Steiner
2003). Indeed much of the extensive litera-
ture on pollination is on the evolutionary as-
pects of specialization and adaptation of plants
and their pollinators (Castellanos et al. 2004;
Hingston et al. 2004; Anderson et al. 2005;
Medan & Montaldo 2005; Goldblatt & Man-
ning 2006; Micheneau et al. 2006). One re-
sult of such specialization is that morpholog-
ical matching of ﬂowers and pollinators results
in better pollination service. Many exclusion
experiments have shown greater fruit and/or
seed set from bird than from insect pollination
(Carpenter 1976; Waser 1978; Waser 1979;
Bertin 1982; Collins & Spice 1986; Ramsey
1988; Celebrezze & Paton 2004; Hargreaves
et al. 2004; Anderson et al. 2006). These stud-
ies show that even in plants apparently special-
ized for pollination by birds, insects also provide
some pollination. Thus, in the absence of birds,
plants may not suffer total reproductive failure
if insects are present. For example, Campsis radi-
cans, a hummingbird-pollinated plant native to
Annals of the New York Academy of Sciences
North America, is pollinated (rarely) by bees
in Poland where nectarivorous birds are absent
(Kolodziejska-Degorska & Zych 2006).
Natural disasters and human decimation of
native bird species can provide clues regard-
ing the role of birds as pollinators. A hurri-
cane in the Bahamas virtually eliminated two
bird species that pollinated the shrub Pavonia
bahamensis, resulting in a decline in fruit set of
74% (Rathcke 2000). The effects of pollinator
declines and extinctions are best known from
New Zealand. Most native bird pollinators have
been extirpated from the main islands and per-
sist only on small offshore islands. Many plant
species are pollen limited because of declines of
bird pollinators (Montgomery et al. 2001; Mur-
phy & Kelly 2001). Even in areas where popu-
lations of the pollinators occur, pollination was
the limiting step in plant reproduction because
there are simply not enough birds to pollinate
all ﬂowers during the relatively short time they
are available (Robertson et al. 1999; Kelly et al.
2004). The breakdown of bird pollination in
New Zealand is apparently widespread and in-
cludes plant species previously thought to be
insect pollinated (Anderson et al. 2006, 2007).
Similarly, many bird-pollinated tree species in
the Hawaiian Islands may be at risk (Sakai et al.
2002), but, as in New Zealand, what little pol-
lination does occur is by insects (Cox 1983).
The substitution of insects for birds as pollina-
tors of “bird pollinated” plants will likely lead
to a substantial reduction of plant reproduction
and subsequent population decline (Robertson
et al. 1999) but may avert plant extinction (Bond
1994; Robertson et al. 2005).
In some areas the substitution of insects
for birds results from the spread of the intro-
duced honeybee rather than declines of avian
pollinators. Consequences of this recent phe-
nomenon are not well understood (Hansen et al.
2002; Celebrezze & Paton 2004; Dupont et al.
2004a,b). In one example, honeybees may have
taken over pollination duties from birds because
they visit more frequently (England et al. 2001).
Effects of habitat fragmentation tend to be
more severe for avian insectivore species than
nectarivore species (Borgella et al. 2001), al-
though the overall number of individual nec-
tarivores declines with fragmentation (Seker-
cioglu et al. 2002). How those effects impact
pollination has rarely been studied. An agri-
cultural landscape in Costa Rica had fewer
species of hummingbirds (Daily et al. 2001)
and lower abundance of bird-pollinated plants
(Mayﬁeld et al. 2006) in fragments than in a
large forest, but neither study examined pol-
lination. Aizen and Feinsinger (1994) found
no effect of fragmentation on fruit or seed set
in two hummingbird-pollinated plants in Ar-
gentina. In southern Chile pollinator visits were
higher in pasture trees than in forest because a
main visitor was territorial in forest but absent
from pasture. Consequently, more species vis-
ited pasture trees (Smith-Ramirez & Armesto
2003). Similarly, bird visitation in New Zealand
was higher on forest edges than in forest inte-
rior, leading to higher fruit set for edge plants
(Montgomery et al. 2003). The most detailed
study on pollination in habitat fragments is
from Australia. Bird pollinators were present
and active in smaller fragments. Although they
transported pollen long distances, they trans-
ferred pollen among fewer plants, leading to in-
breeding and lower seed set in fragments than
in intact forest (Byrne et al. 2007; Yates et al.
Seed dispersal is among the most important
ecosystem services provided by birds. Seed dis-
persal by birds is geographically widespread;
both the bird and plant participants are taxo-
nomically diverse. Plants and their avian dis-
persers form part of a complex mutualistic
network fundamental to maintaining biodiver-
sity and community structure (Bascompte &
Jordano 2007). Ecological and evolutionary as-
pects of seed dispersal have been reviewed sev-
eral times (van der Pijl 1972; Howe 1986; Will-
son 1986; Jordano 2000; Willson & Travaset
2000; Herrera 2002). Most bird dispersal activ-
ities likely fall into the category of supporting
Birds and Ecosystem Services
services. When birds disperse seeds of plants of
economic signiﬁcance (lumber and landscape
species, Table 2), their activities may represent
Birds disperse seeds by various mechanisms.
In the most common, endozoochory, the bird
consumes a ﬂeshy fruit (or analogous structure)
and regurgitates or defecates the seed(s). One
variation of endozoochory is waterfowl and
shorebirds dispersing aquatic plants and inver-
tebrates, many of which are ingested inadver-
tently. Another variation is when raptors sec-
ondarily disperse seeds ingested by their prey
(Nogales et al. 2002). Birds also cache seeds
(synzoochory), primarily pines (Pinus spp.), and
oaks (Quercus spp.) in the north temperate zone.
Less frequently birds disperse seeds by adhe-
sion (epizoochory) to feathers or in mud ad-
hered to the legs or bill, but virtually nothing
is known about the extent and consequences of
At the ecosystem level, seed dispersal is but
one stage in plant reproductive cycles, but dis-
persal by birds has a large role in shaping
plant community composition in many habitats
(Herrera 1985). Seed dispersal beneﬁts plants
through one or more of the following: gene
ﬂow (Godoy & Jordano 2001), escape from ar-
eas of high mortality (Harms et al. 2000), colo-
nization of new sites (Neeman & Izhaki 1996;
Shanahan et al. 2001; Richardson et al. 2002;
Laurance et al. 2006), and directed dispersal to
especially favorable sites (Wenny & Levey 1998;
Tewksbury et al. 1999). Because the chance of a
given seed surviving the entire cycle from seed
to reproductive adult is so small, any move-
ment away from the parent plant (under which
survival is almost always nil) is likely beneﬁcial
(Howe & Miriti 2004). Resulting patterns of
seed dispersion tend to be aggregated or “con-
tagious.” Seeds are more likely to be deposited
in some places than in others as a result of dis-
perser behavior. This pattern is known as dis-
persal limitation and plays a key role in recruit-
ment limitation (the failure of plants to establish
recruits in all suitable locations). Contagious
dispersal often leads to recruitment limitation-
that is a major factor in maintaining biodiver-
sity (Schupp et al. 2002; Kwit et al. 2004).
The importance of seed dispersal can of-
ten be seen clearly in its absence. For exam-
ple, in Tanzania, frugivorous birds are rare or
absent from small forest fragments (Cordeiro
& Howe 2003). Consequently, foraging vis-
its to the tree Leptonychia usambarensis were
much less frequent, and seedling recruitment
in suitable sites was much lower (Cordeiro &
Howe 2003). More broadly, seedling recruit-
ment of the guild of animal-dispersed tree
species was 3–40 times lower in fragments than
in larger forests, while seedling recruitment
among wind-dispersed species was unaffected
by fragmentation (Cordeiro & Howe 2001).
Extrapolations of such disperser declines
and extinctions suggest substantial loss of
plant species richness (da Silva & Tabarelli
2000; Webb & Peart 2001). New Zealand
and south Paciﬁc islands have already suffered
wholesale extinctions of frugivorous birds and
widespread dispersal failure is suspected, par-
ticularly among large-seeded plant species (Mc-
Conkey & Drake 2002; Meehan et al. 2002).
However, as in pollination systems, total extinc-
tion of a plant species in the absence of its main
dispersers may be averted although seedling
recruitment may be drastically reduced. (e.g.,
Witmer & Cheke 1991). Through much of the
neotropical rainforests, hunting of large verte-
brates is likely to lead to increased dispersal and
abundance of species dispersed by small birds,
bats, and wind (Peres & Palacios 2007; Wright
et al. 2007).
Birds are ideal endozoochorus seed dis-
persers. Frugivorous species typically swallow
fruits and seeds intact. Birds are highly mo-
bile 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 and an additional, and frequently over-
looked, beneﬁt of endozoochory is the removal
of fruit skin and pulp from the seeds during the
Annals of the New York Academy of Sciences
TABLE 2. Genera of trees, shrubs, and
lianas of North America of ornamental, tim-
ber, or other (agricultural, medicinal) eco-
nomic value, in which at least one species
produces fruits or seeds dispersed by birds
Family Genus Ornamental Timber Other
Perse a X
Family Genus Ornamental Timber Other
aMalus refers to crabapple, not domestic apple.
interaction (Traveset & Verdu 2002; Samuels
& Levey 2005). Consequently, any bird–plant
interaction involving endozoochory potentially
beneﬁts the plant.
With the exception of birds dispersing mistle-
toes (see Box 1), the interaction of most bird dis-
persers with most other plant species is rather
generalized. A single bird species consumes
fruits of many plant species, and the fruit of a
single plant species is consumed by many bird
species. “Bird fruits” of many species are also
consumed by mammals (Herrera 1989; Willson
1993). Together, these diffuse interactions result
in diffuse coevolution (Janzen 1983; Herrera
1984). Because of the overlap between birds
and mammals as consumers and dispersers of
many plants, on the one hand, and the variety
of ways in which birds disperse seeds on the
other, it is difﬁcult to state precisely how many
Birds and Ecosystem Services
Birds and Mistletoes: A Specialized Mutualism
The relationship between mistletoes and seed-dispersing birds is perhaps the most specialized and tightly
coevolved dispersal interaction and perhaps best illustrates the importance of bird seed dispersal. Mistletoes
in the families Viscaceae, Loranthaceae, and Eremolepidaceae occur worldwide, with highest diversity in the
tropics and subtropics (Watson 2001). Mistletoes require dispersal to stems or branches of other plants for
establishment. Because mistletoes are parasitic and only establish as seedlings on branches, seeds in fruits of
these plants not eaten by birds and those dispersed to the ground have no chance of survival. As a result,
successful dispersal is provided almost entirely by passerine birds. Mistletoe fruits contain a sticky substance
called viscin that is not digested during gut passage and, after deposition by birds, enables the seeds to cling to
a branch until germination and connection with the host xylem.
Birds often disperse mistletoes nonrandomly (Sargent 1995; Botto-Mahan et al. 2000). In some cases dispersal
is directed to the most suitable establishment sites, which can be certain host species or a speciﬁc range of branch
sizes. In Australia, Amyema quandang mistletoes establish best on 1–6 mm diameter twigs, and mistletoebirds,
Dicaeum hiruninaceum, were more likely to deposit seeds on these twigs than were honeyeaters, Acanthagenys
rufogularis (Reid 1989). In Costa Rica, Phoradendron robustissimum established best on 10–14 mm twigs, and
euphonias tended to perch on this size branch (Sargent 1995). For both Amyema and Phoradendron, within tree
establishment is on a nonrandom set of the available branches and is dependent upon a restricted set of
dispersers. Nonrandom distribution of mistletoes among the available host plants (host preferences) has been
shown in other studies (Monteiro et al. 1992; Mart´
ınez del Rio et al. 1995; Larson 1996; de Buen & Ornelas
2002). In most areas, mistletoe populations are aggregated because birds preferentially forage in, and therefore
deposit more seeds on, already infected host plants, or perch in trees with certain characteristics (de Buen &
Ornelas 1999; Aukema & Mart´
ınez del Rio 2002; Medel et al. 2004; Carlo 2005; Ward & Paton 2007). In New
Zealand, several mistletoe species are rare or declining because, at least in part, of loss and rarity of their avian
pollinators and dispersers (Anderson et al. 2006; Ward & Paton 2007).
plant species are dispersed by birds and how
many bird species are effective dispersers. The
frequency of vertebrate-dispersed plant species
in regional ﬂoras ranges from 22% in Aus-
tralian scrubland to 89.5% in tropical rain-
forest, with dispersal of trees more common
in the tropics and New Zealand and dispersal
of shrubs and vines more important in north
temperate forests (Snow 1981; Howe & Small-
wood 1982; Willson et al. 1990; Jordano 2000).
Many birds eat fruits. Some of the important
families include trogons (Trogonidae), hornbills
(Bucerotidae), toucans (Ramphastidae), cotin-
gas (Cotingidae), manakins (Pipridae), birds-
of-paradise (Paradesidae), waxwings (Bom-
bycillidae), bulbuls (Pycnonotidae), thrushes
(Turdidae), and tanagers (Thraupidae).
Many birds are territorial and sing from
perches to maintain the territory and attract
a mate. Some species have taken such displays
to the extreme, including many tropical frugiv-
orous birds with lek breeding systems in which
the males have display perches where they
spend the majority of the day during the breed-
ing season. Wenny and Levey (1998) showed
that display perches of three-wattled bellbirds
(Procnias tricarunculata) enhance early seedling
establishment of species they disperse. Fifty-
two percent of the seeds dispersed by bellbirds
landed in canopy gaps (under display perches),
compared to only 3% of the seeds dispersed by
four other species. Seedlings in gaps had almost
twice the chance of surviving one year subse-
quent compared to seedlings in closed canopy
forest. In leks of the Guianan cock-of-the-rock
(Rupicola rupicola), 77% of the plants present as
seedlings and saplings were likely dispersed by
Rupicola, while only 11.5% of the species in a
Annals of the New York Academy of Sciences
forest understory site were shared with the lek
ery & Larpin 1993). Thus, the Rupicola leks
greatly impact vegetation structure and may
contribute to clumped and patchy distributions
of fruiting plants. Even though the plants in
these examples beneﬁt from directed disper-
sal to suitable sites, they also are dispersed by
other bird species providing colonization, es-
cape, and gene-ﬂow beneﬁts. This overlap and
redundancy is a key part of mutualistic net-
works (Bascompte & Jordano 2007). Neverthe-
less, these examples also show that dispersal
services differ among disperser species, often
with a subset of species providing the majority
of dispersal to a particular area or range of dis-
tances (Jordano et al. 2007; Spiegel & Nathan
Birds often exhibit nonrandom movement
following a foraging bout, resulting in differ-
ential movement of seeds. In forests, many
birds either feed in or move to forest gaps fol-
lowing feeding. Fruiting plants produce larger
crops in gaps (Levey 1988a,b; Levey 1990;
ınez-Ramos & Alvarez-Buylla 1995), and
frugivorous birds are also especially active in
and around gaps (Thompson & Willson 1978;
Schemske & Brokaw 1981; Willson et al. 1982;
Levey 1988b; Malmborg & Willson 1988). In
deciduous forest in eastern North America,
Hoppes (1988) found a bimodal pattern of seed
rain, with most seeds landing near parent plants
and a second smaller peak at gap edges. Over-
all, 50% of bird-dispersed seeds landed in gaps
and gap edges, which comprised 16.8% of the
study area (Hoppes 1988). The importance of
gaps in forest dynamics can likely be scaled up
to the landscape level for which forest edges and
corridors are areas of high-seed input resulting
from bird dispersal (Harvey 2000; Levey et al.
In arid and semiarid habitats the pattern of
bird dispersal is in some ways the opposite of
that in forests. Here, the shaded areas beneath
shrubs and trees provide the critical recruit-
ment sites for many plant species. Such “nurse
plants” shelter seedlings from heat stress. Soil
moisture levels and nutrient availability are of-
ten higher there than in the surrounding soil
(Valiente-Banuet et al. 1991; Fulbright et al.
1995; Callaway et al. 1996; Tewksbury et al.
1999). Nurse plants in arid and semiarid ecosys-
tems are often the only perches available and
thus provide both high seed input in a non-
random pattern and a favorable microclimate
for bird-dispersed species. Several studies re-
port higher seedling emergence under certain
post-foraging perches than others (Herrera &
Jordano 1981; Tester et al. 1987; Izhaki et al.
1991; Chavez-Ramirez & Slack 1994). Chilies
(Capsicum annum) dispersed by birds in Arizona
provide an exemplary case. Most chili plants
grow under other ﬂeshy-fruited species, espe-
cially two Celtis species. Not only were Celtis
trees used preferentially as perches by the main
dispersers, but survival of transplanted chilies
was higher under Celtis than under other nurse
plants (Tewksbury et al. 1999).
The importance of avian seed dispersal in
both forest and arid environments led to the
realization that birds could contribute to the
restoration of deforested land. High rates of
seed dispersal by birds to perches in pastures,
oldﬁelds, or other human-disturbed landscapes
have been documented many times. Perches
added by land managers to act as recruitment
foci range from artiﬁcial structures (McDon-
nell 1986; McClanahan & Wolfe 1993; Holl
1998; Shiels & Walker 2003; Zanini & Ganade
2005) to trees or shrubs (Robinson & Han-
del 1993; Robinson & Handel 2000; Martinez-
Garza & Howe 2003). Other foci include ex-
isting shrubs (Nepstad et al. 1996; Holl 2002;
Lozada et al. 2007), remnant trees (Guevara &
Laborde 1993; Debussche & Isenmann 1994;
da Silva et al. 1996; Toh et al. 1999; Slocum &
Horvitz 2000; Slocum 2001; Martinez-Garza
& Gonzalez-Montagut 2002 ;Pausas et al. 2006;
Zahwai & Augspurger 2006), and fences, wires,
or other existing structures (Holthuijzen &
Sharik 1985; Neeman & Izhaki 1996). The
suitability of such sites for growth and sur-
vival is less clear. Seedlings of woody species
may face grazing animals, frequent ﬁres, or
competition from thick grass cover (Duncan
Birds and Ecosystem Services
& Duncan 2000; Duncan & Chapman 2002).
Nevertheless, once woody species are estab-
lished above the existing matrix, recruitment
of additional bird-dispersed species is likely to
increase (Hatton 1989; Li & Wilson 1998; Toh
et al. 1999; Holl 2002). Seed dispersal by birds
is likely to play a key role in restoration and re-
covery of degraded lands (Duncan 2006; Neilan
et al. 2006; Lozada et al. 2007).
Although the role of waterfowl as seed dis-
persers was recognized decades ago (Ridley
1930), only recently has the ecology of this in-
teraction been studied. Waterfowl (Anatidae;
∼150 species) occur worldwide, are migratory
or otherwise capable of long-distance move-
ments, and many species are largely vegetarian.
Thus, waterfowl can be highly effective mobile
links within and among wetland habitats. Al-
though some waterfowl act as typical frugivores
(Willson et al. 1997), more often waterfowl for-
age actively as herbivores or granivores. Seeds
are ingested inadvertently by herbivores, and a
few escape digestion (e.g., Janzen 1984). Inter-
estingly, in addition to plant seeds, waterfowl
also disperse aquatic invertebrates (Figuerola &
Green 2002a,b; Charalambidou & Santamaria
The ﬁeld of seed dispersal by waterfowl is
largely unexplored (Santamaria & Klaassen
2002). The majority of research in this area
has focused on whether seeds and other propag-
ules survive gut passage, and many of these
studies have used mallard ducks (Anas platyrhyn-
chos) as subjects (Charalambidou & Santamaria
2002). Shorebirds (Charadriidae, Scolopaci-
dae) also disperse seeds and invertebrates, but
the extent and ecological importance of these
interactions is almost completely unknown
(Green et al. 2002). Given the migratory routes
of many waterbirds and shorebirds and the
widespread distributions of many aquatic or-
ganisms (Santamaria 2002), long-distance dis-
persal (20–1000 km) must occur, but its fre-
quency relative to local dispersal is unknown
(Clausen et al. 2002). At a waterfowl migra-
tory stopover and wintering site in southwest-
ern Spain, over 65% of nearly 400 fecal sam-
ples contained seeds and aquatic invertebrates,
suggesting the widespread occurrence of dis-
persal during migration (Figuerola et al. 2003).
Waterfowl also play a role in upstream disper-
sal along rivers for plants that would otherwise
be dispersed passively only downstream (Pollux
et al. 2005).
Future research should investigate the full
range of waterfowl species that engage in seed
dispersal and their relative effectiveness. Fur-
ther, in addition to waterfowl and some shore-
birds, other taxa, most likely herons and allies
(Ardeidae), may also disperse both seeds and
invertebrates. The signiﬁcance of invertebrate
transport by aquatic birds remains largely un-
known. Although this transport appears inad-
vertent or accidental, it need not be so. Investi-
gation of this interaction could use the study of
hummingbird transport of mites (e.g., Colwell
1986) as a model.
Approximately 20 species of pines (Pinus;
most in the subgenus Strobus) are dispersed
by jays and nutcrackers (Corvidae; Tomback
& Linhart 1990). These pines occur in west-
ern 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 re-
moval by animals (Tomback & Linhart 1990).
Two species of Nucifraga nutcrackers are the
most specialized dispersers. Nutcrackers have
a sublingual pouch (unique among birds), in
which they carry up to 90 seeds (Vander
Wall & Balda 1977; Tomback 1982). They
bury 1–4 seeds in the ground in shallow sur-
face caches. Presumably they disperse seeds
considerable distances (Lanner 1996). Each
nutcracker caches thousands of seeds each year,
exceeding its dietary requirements by 2–5 times
(Vander Wall & Balda 1977; Tomback 1982).
Several other corvids, including pinyon jays
(Gymnorhinus cyanocephalus), western scrub
Annals of the New York Academy of Sciences
jays (Aphelocoma californica), and Steller’s jay
(Cyanocitta stelleri), cache pine seeds and are
important dispersers. These birds have highly
developed spatial memory (Balda and Kamil
1989; Kamil and Jones 1997) but do not re-
trieve all caches every year (Lanner 1996). Most
seeds that are not taken by birds and fall be-
neath adult Pinus monophylla trees are harvested
by rodents that are less effective dispersers than
corvids because they larder-hoard seeds in bur-
rows (Vander Wall 1997). Most of the corvid-
dispersed pine species are found in xeric habi-
tats, where burial protects seeds from desicca-
tion (Lanner 1996). In addition, some of the
pines are early successional species (pioneers),
and the birds, nutcrackers and pinyon jays in
particular, are known to make frequent caches
in open areas (Lanner 1996).
Corvids also disperse oaks and beeches (Fa-
gaceae) by scatterhoarding. Although the pre-
sumed mutual adaptations in these species are
less clear than for nutcrackers and pines, many
seeds are cached in suitable sites for germina-
tion and establishment (Darley-Hill & Johnson
1981; Johnson & Adkisson 1985; Johnson et al.
1997; Pons & Pausas 2007). Dispersal by jays
likely aided the rapid post-Pleistocene north-
ward spread of oaks and other species (John-
son & Webb 1989; Wilkinson 1997; Clark et al.
1998). A variety of other birds hoard seeds
(Paridae, Sittidae, Picidae), but their roles as
seed dispersers are not well known and deserve
Seed dispersal by adhesion to birds is much
less frequent than by mammals and has re-
ceived very little attention. In eastern North
America 75% of four waterfowl species had
seeds of up to 12 plant species, mostly attached
to feathers, with a few in mud on the feet
(Viviansmith & Stiles 1994). In southwestern
Spain 35–100% of six species of waterbirds car-
ried seeds or invertebrate eggs. Up to 12 species
were found on an individual, with 22 species
overall. Plant seeds were more commonly at-
tached to feathers, and invertebrate eggs were
more common in mud on feet (Figuerola &
Green 2002a,b). Dispersal by adhesion was a
major source of the Hawaiian ﬂora, and the di-
versity of species dispersed adhesively by birds is
not found in any other terrestrial habitat (Price
& Wagner 2004). The most extreme case of
adhesive seed dispersal involves Pisonia grandis,
found among seabird colonies on oceanic is-
lands. Pisonia is one of the few woody plants that
can survive in the highly acidic guano-derived
soils associated with these colonies. A variety of
seabirds nest in Pisonia trees. Birds can become
entangled within entire infructescences and die.
Seeds cannot survive prolonged immersion in
seawater, so they depend upon seabirds for dis-
persal. Effective dispersal then depends on ad-
hesion to birds that do not become entangled
in plant parts (Burger 2005).
Animals die, and when they do, their car-
casses become available to scavengers. Scav-
engers here refer to microbes, invertebrates,
and vertebrates. Among the birds, the New
World (Ciconiiformes) and Old World (Falconi-
formes) vultures are essentially obligate scav-
engers, but many bird species in many orders
are known to scavenge facultatively or oppor-
tunistically (DeVault et al. 2003). DeVault et al.
(2003) argued that, contrary to conventional
wisdom, most scavenging is accomplished not
by microbes and invertebrates, but by verte-
brates. In contrast to early human perceptions
of birds of prey (predatory Falconiformes), vul-
tures were traditionally viewed as beneﬁcial—
Cathartes, the genus of the New World turkey
vulture, means “puriﬁer” (Kirk & Mossman
1998). Some persecution did occur in the
twentieth century owing to a mistaken be-
lief that vultures occasionally attacked livestock
or spread disease (Parmalee 1954; Mossman
1991; both in Buckley 1999).
Based on energetics, Ruxton and Houston
(2004) argue that obligate scavengers (the New
and Old World vultures) must be generally
large-bodied birds that locomote primarily by
Birds and Ecosystem Services
soaring ﬂight. Their models predict that soaring
ﬂight and large size (allowing infrequent feed-
ing and maintenance on body reserves) give
birds a competitive advantage over terrestrial
mammals, and thus, even precluded the evo-
lution of obligate scavenging in the mammals.
On the other hand, obligate avian scavengers
have lost the agility needed to kill prey. Mam-
mals and facultative avian scavengers have re-
tained the ability to ﬂexibly kill their own prey
and scavenge carrion, but neither can live ex-
clusively on carrion. Shivik (2006) developed
empirically based models of competition be-
tween microscavengers and macroscavengers
and concluded that evolution of macroscav-
engers will favor traits, such as ﬂight, that
maximize rapid carrion detection. These two
modeling approaches, though quite different
conceptually, both conclude that obligate ver-
tebrate scavengers are most likely to be large
Numerous sources of mortality cause non-
predatory death. Historically, these would have
included natural death due to old age, mal-
nutrition, disease, parasites, accidents, expo-
sure, and catastrophic events like storms and
wildﬁres. Today we can add collisions with
human-built structures (buildings, especially
glass; power lines and transmission towers; and
causeways), collisions with automobiles, poi-
soning, and pollution (e.g., oil spills). In the
absence of carcass removal or consumption by
scavengers, the extent of nonpredatory mor-
tality (and the accumulation of carcasses that
would accrue), may be surprising. For example,
Houston (1979) estimated that most large un-
gulate deaths (64%, representing 26 million kg
annually) on the African savanna are due
to nonpredatory causes. One hundred million
to 1 billion birds are conservatively estimated to
die annually within the United States from col-
lisions with glass alone (Klem 1990 & Dunn
1993; both in Klem et al. 2004). Clearly, in
the absence of consumption (whoever the con-
sumer), such deaths would quickly accumulate.
Studies quantifying carcass removal by scav-
engers indicate rapid removal or consumption
(Houston 1986; DeVault et al. 2004; Antworth
et al. 2005). These rapid removal rates may
mask the true extent of carcass production
through nonpredatory death. Consequences of
near extirpation of Gyps vultures due to sec-
ondary consumption of the pharmaceutical di-
clofenac in south Asia (Oaks et al. 2004) un-
derscore the vital services performed by these
scavengers. Following the collapse of popula-
tions of Indian white-backed (Gyps bengalensis),
long-billed (G. indicus), and slender-billed (G.
tenuirostris) vultures, accumulation of putrefying
carcasses led to apparent increases in feral dog
and rat populations (Pain et al. 2003; Prakash
et al. 2005). Uneaten carcasses become infested
with potentially pathogenic bacteria, and they
may be foci for diseases like anthrax (Pain et al.
2003). Increasing populations of dogs and rats,
which serve as reservoirs and vectors of diseases
like canine distemper virus, canine parvovirus,
Leptospira spp. bacteria, and rabies, can lead
to increased rates of transmission of these and
other diseases to humans and domesticated and
natural animal populations. The vulture de-
cline in south Asia has also devastated the Parsi
(Zoroastrian) tradition “sky burial,” in which
their dead are made available for vultures, who
consume the corpses (Pain et al. 2003; Watson
et al. 2004).
The swift and catastrophic decline of the
Gyps vultures in south Asia underscores a
growing concern in environmental toxicology:
widespread presence of pharmaceuticals in the
environment (Dorne et al. 2007). To date, the
suspected pathways by which pharmaceuticals
enter the environment include municipal waste
treatment systems, use of sludge as agricultural
fertilizer, manure from medicated animals, or
through excretion directly from medicated ani-
mals into grasslands (Carlsson et al. 2006). The
poisoning of vultures feeding on carcasses in
south Asia points to yet another potent path-
way. How common pharmaceuticals enter food
webs via this pathway needs further research.
Many bird species are facultative scavengers.
The diversity of documented avian taxa is
impressive: herons, Ardeidae (Hiraldo et al.
Annals of the New York Academy of Sciences
1991); rails, Rallidae (Zembal & Fancher 1988);
skuas, Stercorariidae (Norman et al. 1994); wil-
let and turnstone, Scolopacidae; gulls, Lari-
dae; plovers, Charadriidae (Gochfeld & Burger
1980); raptors, Accipitridae (Selva et al.2003,
2005; Selva & Fortuna 2007); woodpeckers, Pi-
cidae (Servin et al. 2001); and passerines, such
as crows, Corvidae, and tits, Paridae (Selva
& Fortuna 2007). Unlike vultures, whose di-
gestive systems may destroy ingested bacteria
and viruses (Houston & Cooper 1975) or pos-
sess a gut microﬂora that may confer resis-
tance to pathogenic microorganisms and their
toxins (Carvalho et al. 2003), these faculta-
tive scavengers appear frequently to harbor
such pathogens (Blanco et al. 2006). Unsurpris-
ingly, vultures also appear to possess elevated
immunocompetence against many pathogens
widely encountered in carcasses (Ohishi et al.
1979; Apanius et al. 1983; P´
erez de la Las-
tra and de la Fuente 2007). Many facultative
scavengers, including gulls, crows, and starlings,
feed extensively at landﬁlls (Burger & Gochfeld
1983; Belant et al. 1995; Baxter & Allen 2006),
where they may either contract pathogens and
toxins or spread them (Ortiz & Smith 1994).
These facultative scavengers are known carriers
of pathogens, including Salmonella (Monaghan
et al. 1985), and toxins, such as botulinum (Ortiz
& Smith 1994), and they may pose hazards to
human health and water quality. Where land-
ﬁlls are located near airports, collisions with
aircraft are common (Baxter & Allen 2006).
Opportunistic scavenging among birds
reaches its zenith with marine birds that as-
sociate with commercial ﬁsheries, feeding on
discards and offal. Large quantities of un-
wanted ﬁsh and invertebrate by-catch are dis-
carded overboard, providing a rich food source
for ship-following birds. These are typically
large seabirds, including albatross, gulls, and
skua (Furness 2003; Gonz´
alez-Zevallos & Yorio
2006). Association of seabirds with ﬁsheries can
affect breeding success, species interactions,
and distribution (Tasker et al. 2000; Furness
2003; Votier et al. 2004; Gonz ´
Yorio 2006). Although we know of no identiﬁ-
able ecosystem service resulting from scaveng-
ing ﬁsheries discard, there are many potential
ecological consequences. Fisheries discard can
attract and support great numbers of seabirds
(Furness 2003; Valeiras 2003). It is unknown
how this scavenging affects transport of nutri-
ents (e.g., Payne & Moore 2006) and contami-
nants (e.g., mercury; Monteiro & Furness 1995;
Furness & Camphuysen 1997). Reducing dis-
card is encouraged by the food and Agriculture
Organization of the United Nations and the
International Council for the Exploration of
the Sea (FAO 1995; Furness 2003). Decreas-
ing discard rates may affect not only scaveng-
ing species themselves, but entire seabird com-
munities (e.g., Furness 2003; Votier et al. 2004,
2007), as large scavenger species switch to prey-
ing on smaller species (but see Oro & Mart´
Further research is needed on the ecolog-
ical (e.g., predation on nearby nests; Husby
2006) and epidemiological consequences of
large numbers of facultative scavengers feed-
ing at landﬁlls. Research must also address how
to minimize negative consequences, either by
improved landﬁll siting and night landﬁlling
(Burger 2001), or by altering their availabil-
ity to and/or use by generalist and faculta-
tive scavengers via integrated bird management
strategies that may employ avian predators, dis-
tress calls, blank shot, pyrotechnics, gas can-
nons, and other techniques (Baxter & Allen
Additional research should address the eco-
logical conditions that favor macro- versus mi-
croscavengers. For instance, are there certain
areas or conditions in which macroscavengers,
particularly the obligate avian scavengers, are
rare or absent? J.S. Brown (personal commu-
nication) suggests that avian scavengers may
be totally absent from the island of New
Guinea, possibly because environmental con-
ditions (constant high humidity and warm tem-
perature) there so favor microbial decomposers
as to preclude vertebrate scavengers. If so,
then how do we explain the occurrence of
macroscavengers throughout the wet areas of
Birds and Ecosystem Services
Central and South America and West Central
Africa? Such studies would elucidate the situ-
ations in which avian scavengers are relatively
more (and relatively less) important contribu-
tors of these ecosystem services.
Honeyguides (Indicator indicator Sparrman), as
their name implies, guide humans to trees hous-
ing bee nests (Isack & Reyer 1989). Humans, in
the process of harvesting the honey for them-
selves, make this rich resource available to the
birds. The symbiosis between honeyguides and
the Boran people of northern Kenya was stud-
ied by Isack and Reyer (1989) over a 3-year pe-
riod. Honeyguides use distinct behaviors and
vocalizations to attract humans, and the Boran
honey gatherers use whistles and other sounds
to attract honeyguides to them. By following
honeyguides to bee nests, Boran honey gath-
erers conservatively increase their hunting ef-
ﬁciency approximately threefold. We know of
no other example of similar services provided
by birds for humans.
A variety of bird species engage in an in-
teraction known as “beaters and followers.”
The beater species “stirs” a substrate, which
in turn enhances prey availability for the fol-
lower species. Various bird species interact this
way, including waders, Ardeidae; kites, Ac-
cipitridae; kingﬁshers, Alcedinidae; woodpeck-
ers, Picidae; grackles, Icteridae; and drongos,
Dicruridae (Meyerriecks & Nellis 1967; Ben-
nets & Drietz 1997; King & Rappole 2000;
Styring & Ickes 2001). One interpretation is
that the beater species purposefully provides
an ecosystem service for the follower species,
much as honeyguides and humans. However,
it is also possible, and perhaps more likely,
that the follower is simply taking advantage of
an unintentional consequence of the foraging
or locomotor behavior of the beater. Beater–
follower interactions can also lead to surprising
opportunities. Antird (Formicariidae) follow-
ers of army ant (Eciton burchelli, Hymenoptera)
swarms are themselves followed by females
of three species of Ithomiinae (Lepidoptera:
Nymphalidae; Ray & Andrews 1980). The fe-
male butterﬂies feed upon the droppings of the
antbirds, possibly as a predictable resource nec-
essary for prolonged egg production.
Many bird species modify their environ-
ment by activities like nest construction, and,
hence, act as ecosystem engineers (Jones et al.
1994). These product-driven services include
both provisioning and supporting services.
Many bird species construct nests, which dis-
play a great range of complexity, size, longevity,
and usefulness to other organisms. Bird nests
come in many varieties (see Ehrlich et al. 1988),
but most nests fall into one of three categories:
excavated cavities or burrows, cup nests, and
In at least one case, bird nests contribute pro-
visioning services. Some species of cave swifts
(Apodidae) are renowned for their edible nests
(Gausett 2004), which are constructed predom-
inantly from their saliva. These nests are pro-
duced by a number of cave-dwelling species
from the Malaysian and Indonesian region: pri-
marily the white-nest swiftlet (Aerodramus fuci-
phagus) and the black-nest swiftlet (Aerodramus
man exploitation. The nests were used medic-
inally in the Tang (618–907 AD) and Sung
(960–1279 AD) dynasties in China (Koon &
Cranbrook 2002, in Marcone 2005). Today
they are a globally consumed delicacy, known as
the “Caviar of the East” (Marcone 2005). Peak
annual harvest from a single cave, the Niah
Cave of Malaysia, produced around 18,000 kg
of black swiftlet nests around 1931 (Gausslet
2004). Today, bird’s nest soup is one of the
most expensive foods sold. We found an on-
line retailer who today (12 October 2007) sells
grade AAA “swallow nest” at $725.00 (US)
Annals of the New York Academy of Sciences
for 303 g (approximately equivalent to $2400
per kilogram). Hong Kong and North Amer-
ica constitute the world’s two largest importers,
with estimated annual harvest of 17–20 mil-
lion nests (approximately 2 metric tons; Mar-
cone 2005). Harvest is of sufﬁcient magnitude
to cause conservation concern for the swift-
let species whose nests are harvested (Gausset
2004). Swiftlet husbandry may be one method
of alleviating the stress placed on natural swift-
let populations from nest harvest.
Woodpeckers (Picidae) are the most familiar
group of cavity-excavating birds. Woodpeckers
are found on all continents except Antarc-
suitable habitats (e.g., cactus) are available.
Twenty-ﬁve genera comprise about 180
species, ranging in size from about 30 g (e.g.,
the NA downy woodpecker, Picoides pubescens)
to over 500 g (e.g., the endangered imperial
woodpecker, Campephilus imperialis). Cavity size
varies with the size of the species. As primary
cavity excavators, woodpeckers are important
ecosystem engineers. Their cavities are used
by a large number of other animal species,
including birds, mammals, amphibians, and
arthropods (Connor et al. 1997; Neubig &
Smallwood 1999; Monterrubio-Rico &
Escalante-Pliego 2006). Akin to woodpeckers,
citreoline trogons (Trogon citreslus) exca-
vate nesting cavities in arboreal termitaria
(Valdivia-Hoeﬂich & Vega-Rivera 2005). After
abandonment, these cavities are colonized
by secondary users, including various mam-
mals and arthropods (Valdivia-Hoeﬂich &
Vega-Rivera 2005). Primary excavators like
woodpeckers and trogons are keystone species
that help maintain diversity in many areas
(Daily et al. 1993; Connor et al. 1997; Duncan
Burrows are excavated by many taxa of
birds, including penguins (Sphenisciformes),
various seabirds (Procellariiformes, Charadri-
iformes), parrots (Psittaciformes), owls (Strigi-
formes), kingﬁshers (Coraciiformes), and song-
birds (Passeriformes). These burrows alter soil
properties (see below) and, in some cases,
provide homes for numerous other organisms.
Burrow excavators provide roughly analogous
supporting ecosystem services as the woodpeck-
ers. For instance, Casas-Crivill´
(2005) found at least 19 vertebrate species
(12 birds, 2 snakes, 4 mammals, and 1 am-
phibian) using burrows excavated by the Eu-
ropean bee-eater (Merops apiaster). Markwell
(1997) and Newman (1987) report on the
use of burrows dug by fairy prions (Pachyp-
tila turtur) by the endangered tuatara (Sphenodon
Wandering albatrosses (Diomedea exulans),
which nest on oceanic islands of the Southern
Ocean, build elevated nests upon which they in-
cubate eggs and raise chicks (Sinclair & Chown
2006). The chicks occupy the nest through
winter. The nests support high invertebrate
biomass, including larvae of the ﬂightless moth
Pringleophaga marioni. Sinclair and Chown (2006)
suggest that the moth larvae select albatross
nests as habitat due the elevated thermal envi-
ronment provided by the nests, which increases
survival and food exploitation.
Open cup and domed nests are the most
common nest types (Collias & Collias 1984;
Collias 1997). These nests are constructed of
a wide variety of materials, including plants,
lichens, and spider webs. These nests are some-
times taken over by small mammals after the
original occupants ﬁnish nesting and subse-
quently abandon them, but on occasion, an
active nest may be usurped before nesting
is completed (Gates & Gates 1975). Otzen
and Schaefer (1980) report that some over-
wintering spiders exhibit preferences for com-
plex structures, such as bird nests, likely both for
predator avoidance and insulation from cold
temperatures. Abandoned bird nests are also
used by various insects, including ants (per-
sonal observation) and bumble bees (Public
Health Pesticide Applicator Training Manual;
http://vector.ifas.uﬂ.edu 2007). Remsen (2003)
reports that many animals, including insects
like beetles and social wasps, rodents, lizards,
snakes, frogs, and even other bird species, use
nests of the tropical ovenbirds (Furnariidae),
Birds and Ecosystem Services
which build domed nests generally located on
Some breeding bird communities contribute
little to nutrient ﬂuxes (shrubsteppe, Wiens
1973; northern hardwoods, Holmes & Sturges
1975). In contrast, other avian communities
or aggregations may contribute substantially
to nutrient ﬂuxes (Manny et al. 1975; McColl
& Burger 1976; Hicks 1979; Hayes & Caslick
1984). The differences reﬂect the greatly dif-
ferent sorts of aggregations that birds attain at
different phases of the annual cycle or due to
different social structures. Migrants of many
taxa form large monospeciﬁc or heterospeciﬁc
ﬂocks that can attain extremely large densities.
Some species nest or roost colonially and like-
wise attain very high densities. Large aggrega-
tions of birds contribute sizable nutrient ﬂuxes.
The impact of birds on nutrient ﬂuxes, in some
cases, represents provisioning services, but in
others, supporting services.
Seabirds congregate to nest colonially on
many oceanic islands, typically within regions
of oceanic upwelling, which support very rich
ﬁsheries. Here their excreta, or guano, accumu-
lates over many years if not centuries, and can
attain great depths. Guano became extremely
valuable in the 19th century because of its rich
concentration of nitrates and phosphates and
their importance for fertilizer, gunpowder, and
the explosives and chemical industries (Wilkin-
son 1984; Skaggs 1994). The United States
passed the Guano Islands Act of 1856, allow-
ing U.S. citizens to claim uninhabited oceanic
islands for the mining of guano (Skaggs 1994).
Some claimed islands still remain possessions
of the United States. In 1864, Spain seized
the guano-rich Chincha Islands from Peru,
provoking the Spanish–Peruvian and Spanish–
Chilean Wars, which ended with Spain’s with-
drawal in 1866. The “Guano Wars” or the
War of the Paciﬁc, waged by Chile against joint
forces of Peru and Bolivia from 1879–1883, re-
sulted in annexation of the Peruvian province of
Ta ra pa c ´
a and the Bolivian province of Litoral,
areas rich with guano deposits. Conﬂicts also
arose between the governments of the United
States, Great Britain, and Venezuela, over Aves
Island in the Caribbean Sea (Cordle 2007). An-
nual importation of guano into Britain peaked
at over 200,000 tons—worth over 2,700,000
British pounds—in the late 1850s (Mathew
1970, 1976; Cordle 2007). Most imported
guano came from Peru, for which this was the
main export commodity from 1840 through
the early 1880s (Mathew 1970). Demand for
guano declined with the advent of alternative
fertilizers, such as superphosphate (the mineral
apatite treated with sulfuric acid), in the late
1800s. Once commercial processes, such as the
Haber–Busch process for making atmospheric
guano industry all but ceased to exist (Skaggs
1994). An interesting and largely contemporary
account can be found in Lotka (1924).
Bird aggregations affect nutrient ﬂuxes, and
nutrient cycling and availability in many other
situations, including near-shore islands (Gill-
ham 1956; Bosman et al. 1986), coastal ma-
rine communities (Wooton 1991; Pﬁster et al.
2007), wildlife refuges (Kitchell et al. 1999),
terrestrial marine ecosystems (S´
& Polis 2000), and isolated urban forest frag-
ments (Fujita & Koike 2007). Importation
of nutrients has both direct effects, favoring
some primary producers over others, and in-
direct effects, as bottom-up forces cascade to
primary consumers (Wootton 1991) and detri-
nero & Polis 2000). Burrow-
ing seabirds also affect soil nutrient character-
istics (Bancroft et al. 2004; Fukami et al. 2006)
through nutrient addition (via guano) and biop-
erturbation (disturbance and soil turnover) and
can be major ecosystem drivers (Fukami et al.
Birds can also ﬁgure importantly in re-
ciprocal nutrient ﬂuxes between contiguous
habitats in heterogeneous landscapes (Nakano
& Murakami 2001). Such reciprocal nutrient
ﬂuxes directly and indirectly affect food-web
dynamics (Baxter et al. 2005), sometimes in
Annals of the New York Academy of Sciences
ways contrary to theoretical expectation. For
instance, Polis et al. (1997) predicted that al-
lochthonous prey inputs should result in neg-
ative indirect effects on in situ prey species.
Nakano et al. (1999), studying reciprocal ﬂows
between a river and adjacent terrestrial forest,
instead found decreased consumption of in situ
prey in presence of allochthonous input, but
once discontinued, in situ prey consumption in-
creased. At the ecosystem level, allochthonous
inputs sustain greater densities and diversities of
consumers (Nakano & Murakami 2001). Effects
of cross-habitat subsidies may vary seasonally
(Nakano & Murakami 2001). Power (2001) and
Fausch et al. (2002) provide commentaries on
the work of Nakano, who died tragically in an
accident in 2000. Many questions remain re-
garding such aquatic–terrestrial reciprocal en-
ergy ﬂows (Baxter et al. 2005). For instance, is
this sort of reciprocal ﬂow restricted to aquatic–
terrestrial systems, or could it also occur in dif-
ferent types of adjacent terrestrial habitats, such
as grassland–forest, or, say, forest–agricultural
ﬁeld? Do such reciprocal ﬂows between adja-
cent, heterogeneous habitats vary with climate
or with latitude?
Although we typically think of humming-
birds feeding on ﬂower nectar, some hum-
mingbirds feed and even defend sap trees of
woodpeckers or sapsuckers. Sapsuckers and
woodpeckers, in their foraging activities, pro-
duce wells of sap. These wells provide rich re-
sources, and other species use them. Species
like hummingbirds acquire both sap (a source
of carbohydrate) and insects (a source of pro-
tein), which are attracted to the wells. Ex-
amples include the ruby-throated humming-
bird (Archilochus colubris) and the yellow-bellied
sapsucker (Sphyrapicus varius)ineasternNorth
America (Southwick & Southwick 1980), and
the buff-tailed coronet (Boissonneaua ﬂavescens)
and acorn woodpecker (Melanerpes formicivorus)
in South America (Kattan & Murcia 1985).
Rufous hummingbirds (Selasphorus rufus) de-
fend sap trees (Sutherland et al. 1982). Al-
though many other species, including passer-
ines, insects, and mammals, are known to feed
at sap wells created by sapsuckers (Kilham
1953; Foster & Tate 1966), only humming-
birds appear to have strong dependencies on
Synthesis and Future Directions
An extensive literature examines techniques
and challenges of determining the economic
value of ecological services to humans. A good
starting point is the UN Millennium Ecosystem
Assessment (2003). Additional sources include:
Tu r ne r et al. (2003), Barbier (2007), Boyd
(2007), Croitoru (2007), Kroeger and Casey
(2007), and references therein. Important con-
siderations include the temporal and spatial
scale over which any potential service is gen-
erated (Chee 2004). Also critical is whether the
agent(s) responsible for the service is unique or
part of a redundant network (Power et al. 1996).
A ﬁnal aspect we feel important is the intrin-
sic variability inherent in the production of the
ecosystem service. Ecosystem processes natu-
rally vary over time. Understanding natural
variability is critical to the proper accounting of
any ecosystem service (Millennium Ecosystem
We believe a number of gaps in knowledge
regarding bird services need to be addressed.
We know considerably more about how birds
function as consumers of arthropods and fruits,
and hence as control agents of herbivorous in-
sects and as seed dispersers, respectively, than
we know about birds as pollinators. Additional
research regarding which plant species are pol-
linated by which bird species, and the effective-
ness of birds relative to other pollinators would
be extremely useful. More research on avian
granivory in agro-ecosystems is also warranted,
particularly with respect to seasonal switching
of diet between seeds and arthropods. Does the
interaction of beaters and followers represent
simple exploitation by followers, or might the
Birds and Ecosystem Services
follower species provide a return service, per-
haps predator detection, for the beater species?
Do other species create feeding opportunities
analogous to the sap wells of sapsuckers?
Perhaps the important ruler with which we
should measure the contribution of birds to the
economic output of a particular plant species
(and thus the economic contribution of the
birds themselves) is their impact on plant yield
in more managed systems and the demography
of plant populations in natural systems. When
birds play more than one role, we could de-
termine their relative demographic impacts as
pollinators, seed dispersers, and seed predators,
and so on. Rarely if ever do we know the de-
mographic contribution of birds for any one of
these roles, let alone their synergistic (or an-
tagonistic) effects. Cost–beneﬁt analysis could
be applied when alternative ecosystem “com-
ponents” might be available (use of pesticides
versus encouragement of bird predation).
As this review indicates, experimental ex-
clusion of birds is a powerful tool for assess-
ing ecosystem function. However, these exper-
iments are not always feasible, and an inherent
problem of interpretation is how best to extrap-
olate from the scale of the experiment to that
of an ecosystem. In light of such difﬁculties,
ecologists should be poised to take advantage
of “natural” experiments that may arise, for
instance, from geographically local declines of
certain species or groups of species or from epi-
zootics like that of West Nile Virus (e.g., Caffrey
2005). Such declines may allow efﬁcient detec-
tion of a concomitant decline of important bird
We thank the editors for the invitation to
contribute this review. Cagan Sekercioglu re-
viewed the manuscript and offered many useful
Conﬂicts of Interest
The authors declare no conﬂicts of interest.
Aizen, M.A. & P. Feinsinger. 1994. Forest fragmentation,
pollination, and plant reproduction in a chaco dry
forest, Argentina. Ecology 75: 330–351.
Allen, J.A. 1893. Our hawks and owls in relation to agri-
culture. Auk 10: 199–201.
Amano, T. & Y. Yamaura. 2007. Ecological and life-
history traits related to range contractions among
breeding birds in Japan. Biol. Cons. 137: 271–282.
Ambuel, B. & S.A. Temple. 1983. Area-dependent
changes in the bird communities and vegetation
of southern Wisconsin forests. Ecology 64: 1057–
Anderson, B., W.W. Cole & S.C.H. Barrett. 2005. Spe-
cialized bird perch aids cross-pollination. Nature 435:
Anderson, S.H., D. Kelly, A.W. Robertson, et al. 2006.
Birds as pollinators and dispersers: a case study from
New Zealand. Acta Zool. Sinica 52: 112–115.
Anderson, S.H., D. Kelly, A.W. Robertson & J.J. Ladley.
2007. Widespread failure of bird-pollination mutu-
alisms on the New Zealand mainland. N. Z. J. Bot.
Antworth, R.L., D.A. Pike & E.E. Stevens. 2005. Hit and
run: effects of scavenging on estimates of roadkilled
vertebrates. Southeast. Nat. 4: 647–656.
Apanius, V., S.A. Temple & M. Bale. 1983. Serum pro-
teins of wild turkey vultures (Cathartes aura). Comp.
Biochem. Phys. B 76: 907–913.
Askenmo, C., A. Bromssen, J. von Ekman & C. Jans-
son. 1977. Impact of some wintering birds on spider
abundance in spruce. Oikos 28: 90–94.
Askins, R.A. 1995. Hostile landscapes and the decline of
migratory songbirds. Science 267: 1956–1957.
Askins, R.A., J. Lynch & R. Greenberg. 1990. Population
declines in migratory birds in eastern North Amer-
ica. Curr. Ornith. 1: 1–57.
Atlegrim, O. 1989. Exclusion of birds from bilberry
stands— impact on insect larval density and damage
to the bilberry. Oecologia 79: 136–139.
Aukema, J.E. & C.M. del Rio. 2002. Where does a fruit-
eating bird deposit mistletoe seeds? Seed deposition
patterns and an experiment. Ecology 83: 3489–3496.
Ayres, M.P. & M.J. Lombardero. 2000. Assessing the con-
sequences of climate change for forest herbivore and
pathogens. Science Total Environ. 262: 263–286.
Bailey, J.K. & T.G. Whitham. 2003. Interactions among
elk, aspen, galling sawﬂies and insectivorous birds.
Oikos 101: 127–134.
Bailey, J.K., S.C. Wooley, R.L. Lindroth & T.G. Whitham.
2006. Importance of species interactions to commu-
nity heritability: a genetic basis to trophic-level in-
teractions. Ecol. Lett. 9: 78–85.
Annals of the New York Academy of Sciences
Balda, R.P. & A.C. Kamil. 1989. A comparative study of
cache recovery by three corvid species. Animal Behav-
ior 38: 486–495.
Bancroft, W.J., M.J. Garkaklisb & J.D. Roberts. 2004. Bur-
row building in seabird colonies: a soil-forming pro-
cess in island ecosystems. Pedobiologia 49: 149–165.
Barber, N.A., R.J. Marquis & W.P. Tori. 2008. Invasive
prey impacts regional distribution of native preda-
tors. Ecology (in press).
Barbier, E.B. 2007. Valuing ecosystem services as produc-
tive inputs. Econ. Policy 22: 177–229.
Bascompte, J. & P. Jordano. 2007. Plant-animal mutual-
istic networks: The architecture of biodiversity. Ann.
Rev. Ecol. Syst. 38: 567–593.
Baxter, A.T. & J.R. Allen. 2006. Use of raptors to reduce
scavenging bird numbers at landﬁll sites. Wildlife Soc.
Bull. 34: 1162–1168.
Baxter, C.V., Fausch, K.D. & W.C. Saunders. 2005. Tan-
gled webs: reciprocal ﬂows of invertebrate prey link
streams and riparian zones. Freshw. Biol. 50: 201–
Becker, J. 1996. Hungry Ghosts. Mao’s Secret Famine.The
Free Press. New York, NY.
Belant, J.L., T.W. Seamans, S.W. Gabrey & R.A. Dolbeer.
1995. Abundance of gulls and other birds at landﬁlls
in northern Ohio. Amer. Midl. Nat. 134: 30–40.
Bennets, R.E. & V.J. Drietz. 1997. Possible use of wading
birds as beaters by snail kites, boat-tailed Grackles,
and Limpkins. Wilson Bull.,109: 169–173.
Bennett, J. & S. Whitten. 2003. Duck hunting and wet-
land conservation: compromise or synergy? Canad.
J. Agric. Econ. 51: 161–173.
Bernardello, G., G.J. Anderson, T.F. Stuessy & D.J. Craw-
ford. 2006. The angiosperm ﬂora of the Archipelago
Juan Fernandez (Chile): origin and dispersal. Canad.
J. Bot. 84: 1266–1281.
Bertin, R.I. 1982. Floral biology, hummingbird pollina-
tion and fruit production of trumpet creeper (Campsis
radicans, Bignoniaceae). Am.J.Bot.69: 122–134.
Bock, C. E, J.H. Bock, & M.C. Grant. 1992. Effects of bird
predation on grasshopper densities in an Arizona
grassland. Ecology 73: 1706–1717.
Blanco, G., J.A. Lemus & J. Grande. 2006. Faecal bacteria
associated with different diets of wintering red kites:
inﬂuence of livestock carcass dumps in microﬂora
alteration and pathogen acquisition. J. Appl. Ecol.
Boege, K. & R.J. Marquis. 2006. Plant quality and preda-
tion risk mediated by plant ontogeny: consequences
for herbivores and plants. Oikos 115: 559–572.
Bond, W.J. 1994. Do mutualisms matter — assessing
the impact of pollinator and disperser disruption on
plant extinction. Philosophical Transactions of the Royal
Society of London – Series B: Biological Sciences.344: 83–
Borgella, R., A.A. Snow & T.A. Gavin. 2001. Species
richness and pollen loads of hummingbirds using
forest fragments in southern Costa Rica. Biotropica
Bosman, A.L., J.T. Dutoit, P.A.R. Hockey & G.M.
Branch. 1986. A ﬁeld experiment demonstrating
the inﬂuence of seabird guano on intertidal pri-
mary production. Est. Coastal Shelf Sci. 23: 283–
Botto-Mahan, C., R. Medel, R. Ginocchio & G. Mon-
tenegro. 2000. Factors affecting the circular distribu-
tion of the leaﬂess mistletoe Tristerix aphyllus (Loran-
thaceae) on the cactus Echinopsis chilensis.Rev. Chile.
Hist. Nat. 73: 525–531.
Boyd, J. 2007. Nonmarket beneﬁts of nature: what should
be counted in green GDP?. Ecol Econ. 61: 716–
Boyer, A.G., R.E. Swearingen, M.A. Blaha, et al. 2003.
Seasonal variation in top-down and bottom-up pro-
cesses in a grassland arthropod community. Oecologia
Brown, E.D. & M.J.G. Hopkins. 1995. A test of pollina-
tor speciﬁcity and morphological convergence be-
tween nectarivorous birds and rainforest tree ﬂowers
in New Guinea. Oecologia 103: 89–100.
Brown P.R., N.I. Huth, P.B. Banks & G.R. Singleton.
2007. Relationship between abundance of rodents
and damage to agricultural crops. Agric. Ecos. Env.
Buckley, N.J. 1999. Black Vulture (Coragyps atratus). In The
Birds of North America, No. 411. A. Poole & F. Gill,
Eds. The Birds of North America, Inc. Philadelphia,
Burger, A.E. 2005. Dispersal and germination of seeds of
Pisonia grandis, an Indo-Paciﬁc tropical tree associ-
ated with insular seabird colonies. J. Tro p. Ec o l . 21:
Burger, J. 2001. Landﬁlls, nocturnal foraging and risk to
aircraft. J. Tox ic. E n v. 64: 273–290.
Burger, J. & M. Gochfeld. 1983. Behavior of nine avian
species at a Florida garbage dump. Col. Waterbirds 6:
Burquez, A. 1989. Blue Tits, Parus caeruleus, as pollinators
of the crown imperial, Fritillaria imperialis,inBritain.
Oikos 55: 335–340.
Byrne, M., C.P. Elliott, C. Yates & D.J. Coates. 2007.
Extensive pollen dispersal in a bird- pollinated shrub,
Calothamnus quadriﬁdus, in a fragmented landscape.
Mol. Ecol. 6: 1303–1314.
Caffrey, C. 2005. West Nile virus devastates an American
crow population. Condor 107: 128–132.
Callaway, R.M., E.H. DeLucia, D. Moore, et al. 1996.
Competition and facilitation: contrasting effects of
Artemisia tridentata on desert vs montane pines. Ecology
Birds and Ecosystem Services
Carlo, T.A. 2005. Interspeciﬁc neighbors change seed
dispersal pattern of an avian-dispersed plant. Ecol-
ogy 86: 2440–2449.
Carlsson, C., A.K. Johansson, G. Alvan, et al. 2006. Are
pharmaceuticals potent environmental pollutants?
Part I: Environmental risk assessments of selected ac-
tive pharmaceutical ingredients. Sci. Total Env. 364:
Carpenter, F.L. 1976. Plant-pollinator interactions in
Hawaii: Pollination energetics of Metrosideros collina
(Myrtaceae). Ecology. 57: 1125–1144.
Carvalho, L.R. de, L.M. Farias, J.R. Nicoli, et al. 2003.
Dominant culturable bacterial microbiota in the di-
gestive tract of the American black vulture (Coragyps
atratus Bechstein 1793) and search for antagonistic
substances. Braz. J. Microbiol. 34: 218–224.
e, A. & F. Valera. 2005. The European bee-
eater (Merops apiaster) as an ecosystem engineer in
arid environments. J. Arid Env. 60: 227–238.
Castellanos, M.C., P. Wilson & J.D. Thomson. 2004. ‘Anti-
bee’ and ‘pro-bird’ changes during the evolution of
hummingbird pollination in Penstemon ﬂowers. J. Ev o l.
Biol. 17: 876–885.
Celebrezze, T. & D.C. Paton. 2004. Do introduced honey-
bees (Apis mellifera, Hymenoptera) provide full polli-
nation service to bird-adapted Australian plants with
small ﬂowers? An experimental study of Brachyloma
ericoides (Epacridaceae). Aust. Ecol. 29: 129–136.
Charalambidou, I. & L. Santamaria. 2002. Waterbirds
as endozoochorus dispersers of aquatic organisms: a
review of experimental evidence. Acta Oecologia 23:
Charalambidou, I. & L. Santamaria. 2005. Field evidence
for the potential of waterbirds as dispersers of aquatic
organisms. Wetlands 25: 252–258.
Chavez-Ramirez, F. & R.D. Slack. 1994. Effects of avian
foraging and post-foraging behavior on seed disper-
sal patterns of Ashe juniper. Oikos 71: 40–46.
Chee, Y.N. 2004. An ecological perspective on the valua-
tion of ecosystem services. Biol. Cons. 120: 549–565.
Clark, J.S., C. Fastie, G. Hurtt, et al. 1998. Reid’s para-
dox of rapid plant migration: dispersal theory and
interpretation of paleoecological records. Bioscience
Clausen, P., B.A. Nolet, A.D. Fox & M. Klaassen.
2002. Long-distance endozoochorous dispersal of
submerged macrophyte seeds by migratory water-
birds in northern Europe — a critical review of
possibilities and limitations. Acta Oecologica 23: 191–
Coleman, R.A., J.D. Goss-Custard, S.E.A.L. Durell & S.J.
Hawkins. 1999. Limpet Patella spp. consumption by
oystercatchers Haematopus ostralegus: a preference for
solitary prey items. Marine Ecol.-Progress Series 183:
Collias, N.E. 1997. On the origin and evolution of nest
building by passerine birds. Condor 99: 253–278.
Collias, N.E. & E.C. Collias. 1984. Nest Building and Bird
Behavior. Princeton University Press. Princeton, NJ.
Collins, B.G. & J. Spice. 1986. Honeyeaters and the polli-
nation biology of Banksia prionotes (Proteaceae). Aust.
J. Bot. 34: 175–185.
Colwell, R.K. 1986. Community biology and sexual se-
lection: lessons from hummingbird ﬂower mites. In
Community Ecology. J.R. Diamond & T.J. Case, Eds.:
406–424. Harper and Row. New York, NY.
Cordeiro, N.J. & H.F. Howe. 2001. Low recruitment of
trees dispersed by animals in African forest frag-
ments. Cons. Biol. 15: 1733–1741.
Cordeiro, N.J. & H.F. Howe. 2003. Forest fragmentation
severs mutualism between seed dispersers and an
endemic African tree. Proc. Natl. Acad. Sci. USA 100:
Connor, R.N., C. Rudolph, D. Saenz & R.R. Schae-
fer. 1997. Species using red-cockaded woodpecker
cavities in eastern Texas. Bull. Texas Ornith. Soc. 30:
Cordle, C. 2007. The guano voyages. Rural Hist. 18: 119–
Cornelissen, T. & P. Stiling. 2006. Responses of differ-
ent herbivore guilds to nutrient addition and natural
enemy exclusion. Ecoscience 13: 66–74.
Cote, M., J. Ferron & R. Gagnon. 2003. Impact of seed
and seedling predation by small rodents on early
regeneration establishment of black spruce. Can. J.
For. Re s. 33: 2362–2371.
Cox, P.A. 1983. Extinction of the Hawaiian avifauna re-
sulted in a change of pollinators for the ieie, Freycinetia
arborea.Oikos 41: 195–199.
Croitoru, L. 2007. Valuing the non-timber forest products
in the Mediterranean region. Ecol. Econ. 63: 768–
Daily, G.C., P.R. Ehrlich, & N.M. Haddad. 1993. Double
keystone bird in a keystone species complex. Proc.
Natl. Acad. Sci. USA 90: 592–594.
Daily, G.C., P.R. Ehrlich & G.A. Sanchez-Azofeifa.
2001. Countryside biogeography: Use of human-
dominated habitats by the avifauna of southern
Costa Rica. Ecol. Appl. 11: 1–13.
da Silva, J.M.C. & M. Tabarelli. 2000. Tree species im-
poverishment and the future ﬂora of the Atlantic
forest of northeast Brazil. Nature 404: 72–74.
da Silva, J.M.C., C. Uhl & G. Murray. 1996. Plant succes-
sion, landscape management & the ecology of fru-
givorous birds in abandoned Amazonian pastures.
Cons. Biol. 10: 491–503.
Darley-Hill, S. & W.C. Johnson. 1981. Acorn dispersal by
the blue jay (Cyanocitta cristata). Oecologia 50: 231–232.
de Buen, L.L. & J.F. Ornelas. 1999. Frugivorous birds,host
selection and the mistletoe Psittacanthus schiedeanus,
Annals of the New York Academy of Sciences
in central Veracruz, Mexico. J. Trop. Eco l . 15: 329–
de Buen, L.L. & J.F. Ornelas. 2002. Host compatibility
of the cloud forest mistletoe Psittacanthus schiedeanus
(Loranthaceae) in central Veracruz, Mexico. Am. J.
Bot. 89: 95–102.
Debussche, M. & P. Isenmann. 1994. Bird-dispersed seed
rain and seedling establishment in patchy Mediter-
ranean vegetation. Oikos 69: 414–426.
DeVault, T.L., O.E. Rhodes & J.A. Shivik. 2003. Scav-
enging by vertebrates: behavioral, ecological, and
evolutionary perspectives on an important energy
transfer pathway in terrestrial ecosystems. Oikos 102:
DeVault, T.L., I.L. Brisbin & O.E. Rhodes. 2004. Factors
inﬂuencing the acquisition of rodent carrion by ver-
tebrate scavengers and decomposers. Can. J. Zoo. 82:
Donald, P.F., R.E. Green & M.R. Heath. 2001. Agri-
cultural intensiﬁcation and the collapse of Europe’s
farmland bird populations. Proc. R. Soc. Lond. Ser. B
Biol. Sci. 268: 25–29.
Dorne, J.L.C.M., L. Skinner, G.K. Frampton, et al. 2007.
Human and environmental risk assessment of phar-
maceuticals: differences, similarities, lessons from
toxicology. Analyt. Bioanalyt. Chem. 387: 1259–1268.
Duncan, R.S. 2006. Tree recruitment from on-site ver-
sus off-site propagule sources during tropical forest
succession. New For. 31: 131–150.
Duncan, R.S. & Chapman, C.A. 2002. Limitations of ani-
mal seed dispersal for enhancing forest succession on
degraded lands. In Seed dispersal and frugivory: Ecolog y,
evolution and conservation. D.J. Levey, W.R. Silva & M.
Galetti, Eds.: 437–450. CABI Publishing. Walling-
Duncan, R.S. & V.E. Duncan. 2000. Forest succession
and distance from forest edge in an Afro-tropical
grassland. Biotropica 32: 33–41.
Duncan, S. 2003. Coming home to roost: the pileated
woodpecker as an ecosystem engineer. Science Findings
Dunn, E.H. 1993. Bird mortality from striking residential
windows in winter. J. Field Ornith. 64: 302–309.
Dupont, Y.L., D.M. Hansen, J.T. Rasmussen & J.M. Ole-
sen. 2004a. Evolutionary changes in nectar sugar
composition associated with switches between bird
and insect pollination: the Canarian bird-ﬂower ele-
ment revisited. Funct. Ecol. 18: 670–676.
Dupont, Y.L., D.M. Hansen, A. Valido & J.M. Olesen.
2004b. Impact of introduced honey bees on native
pollination interactions of the endemic Echium wild-
pretii (Boraginaceae) on Tenerife, Canary Islands.
Biol. Cons. 118: 301–311.
Ehrlich, P.R., D.S. Dobkin & D. Wheye. 1988. The Bird-
watcher’s Handbook: A Field Guide to the Natural History
of North American Birds. Simon & Schuster. New York,
Ellis, J.C., W. Chen, B. O’Keefe, et al. 2005. Predation by
gulls on crabs in rocky intertidal and shallow subtidal
zones of the Gulf of Maine. J. Exp. Marine Biol. Ecol.
Ellis, J.C., M.J. Shulman, M. Wood, et al. 2007. Reg-
ulation of intertidal food webs by avian predators
on New England rocky shores. Ecology 88: 853–
England, P.R., F. Beynon, D.J. Ayre & R.J. Whelan. 2001.
A molecular genetic assessment of mating-system
variation in a naturally bird-pollinated shrub: contri-
butions from birds and introduced honeybees. Cons.
Biol. 15: 1645–1655.
Errington, P.L. 1933. Food habits of southern Wisconsin
raptors: part II. hawks. Condor 35: 19–29.
FAO. 1995. Code of Conduct for Responsible Fisheries.FAO.
Fausch, K.D., M.E. Power & M. Murakami. 2002. Link-
ages between stream and forest food webs: Shigeru
Nakano’s legacy for ecology in Japan. TREE 17:
Fayt, P., M.M. Machmer, & C. Steeger. 2005. Regulation
of spruce bark beetles by woodpeckers — a literature
review. For. Ecol. Manage. 206: 1–14.
Feinsinger, P. 1983. Coevolution and pollination. In Co-
evolution. D.J. Futuyma & M. Slatkin, Eds.: 282–310.
Sinauer Associates. Sunderland, MA.
Figuerola, J. & A.J. Green. 2002a. Dispersal of aquatic
organisms by waterbirds: a review of past research
and priorities for future studies. Freshw. Biol. 47: 483–
Figuerola, J. & A.J. Green. 2002b. How frequent is ex-
ternal transport of seeds and invertebrate eggs by
waterbirds? A study in Do˜
nana, SW Spain. Archiv f¨
Hydrobiologie 155: 557–565.
Figuerola, J., A.J. Green & L. Santamaria. 2003. Passive
internal transport of aquatic organisms by waterfowl
nana, south-west Spain. Global Ecol. Biogeogr.
Fisher, A.K. 1893. The hawks and owls of the United
States and their relation to agriculture. U.S. Dept.
Agric., Div. Ornith. Mamm. Bull. 3: 402–422.
Forkner, R.E. & M.D. Hunter. 2000. What goes up must
come down? Nutrient addition and predation pres-
sure on oak herbivores. Ecology 81: 1588–1600.
Foster, W.L. & J. Tate, Jr. 1966. The activities and coac-
tions of animals at sapsucker trees. Living Bird 5:
Fujita, M. & F. Koike. 2007. Birds transport nutrients to
fragmented forests in an urban landscape. Ecol. Appl.
Fukami, T., D.A. Wardle, P.J. Bellingham, et al. 2006.
Above- and below-ground impacts of introduced
Birds and Ecosystem Services
predators in seabird-dominated island ecosystems.
Ecol. Lett. 9: 1299–1307.
Fulbright, T.E., J.O. Kuti & A.R. Tipton. 1995. Effects
of nurse-plant canopy temperatures on shrub seed
germination and seedling growth. Acta Oecologia 16:
Furness, R.W. 2003. Impacts of ﬁsheries on seabird com-
munities. Scientia Marina 67(Suppl. 2): 33–45.
Furness, R.W. & C.J. Camphuysen. 1997. Seabirds as
monitors of the marine environment. ICES Journal of
Marine Science 54: 726–737.
Gale, G.A., J.A. DeCecco, M.R. Marshall, et al. 2001.
Effects of gypsy moth defoliation on forest birds: an
assessment using breeding bird census data. J. Field
Ornith. 72: 291–304.
Gates, J.E. & D.M. Gates. 1975. Nesting indigo buntings
displaced by Peromyscus.Wilson Bull. 87: 422–423.
Gausset, Q. 2004. Chronicle of a foreseeable tragedy:
birds’ nests management in the niah caves (Sarawak).
Human Ecol. 32: 487–507.
Gibbons, D.W., D.A. Bohan, P. Rothery, et al. 2006. Weed
seed resources for birds in ﬁelds with contrasting
conventional and genetically modiﬁed herbicide-
tolerant crops. Proc.R.Soc.BBiol.Sci.273: 1921–
Gillham, M.E. 1956. Ecology of the Pembrokeshire Is-
lands: IV. Effects of treading and burrowing by birds
and mammals. J. Ec o l . 44: 51–82.
Gochfeld, M. & J.Burger. 1980. Opportunistic scavenging
by shorebirds: feeding behavior and aggression. J.
Field Ornith. 51: 373–375.
Godoy, J.A. & P. Jordano. 2001. Seed dispersal by animals:
exact identiﬁcation of source trees with endocarp
DNA microsatellites. Mol. Ecol. 10: 2275–2283.
Goldblatt, P. & J.C. Manning. 2006. Radiation of pollina-
tion systems in the Iridaceae of sub- Saharan Africa.
Ann. Bot. 97: 317–344.
Gonzalez-Gomez, P., C.F. Estades & J.A. Simonetti. 2006.
Strengthened insectivory in a temperate fragmented
forest. Oecologia 148: 137–143.
alez-Zevallos, D. & P. Yorio. 2006. Seabird use of
discards and incidental captures at the Argentine
hake trawl ﬁshery in the Golfo San Jorge, Argentina.
Marine Science-Progress Series 316: 175–183.
Green, A.J., J. Figuerola & M.I. Sanchez. 2002. Implica-
tions of waterbird ecology for the dispersal of aquatic
organisms. Acta Oecologia 23: 177–189.
Greenberg, R., P. Bichier, A.C. Angon, et al. 2000. The im-
pact of avian insectivory on arthropods and leaf dam-
age in some Guatemalan coffee plantations. Ecology
Gruner, D.S. 2004. Attenuation of top-down and bottom-
up forces in a complex terrestrial community. Ecology
Gunnarsson, B. 1996. Bird predation and vegetation
structure affecting spruce-living arthropods in a tem-
perate forest. J. Anim. Ecol. 65: 389–397.
Gunnarsson, B. & M. Hake. 1999. Bird predation affects
canopy-living arthropods in city parks. Canad. J. Zoo.
Guevara, S. & J. Laborde. 1993. Monitoring seed disper-
sal at isolated standing trees in tropical pastures —
consequences for local species availability. Vegetatio
Hamilton, D.J. 2000. Direct and indirect effects of preda-
tion by Common Eiders and abiotic disturbance in
an intertidal community. Ecol. Monog. 70: 21–43.
Hamilton, D.J., A.W. Diamond & P.G. Wells. 2006. Shore-
birds, snails, and the amphipod (Corophium volutator)
in the upper Bay of Fundy: top-down vs. bottom-
up factors, and the inﬂuence of compensatory inter-
actions on mudﬂat ecology. Hydrobiologia 567: 285–
Hamilton, D.J. & T.D. Nudds. 2003. Effects of predation
by common eiders (Somateria mollissima) in an inter-
tidal rockweed bed relative to an adjacent mussel
bed. Marine Biol. 142: 1–12.
Hansen, D.M., J. M. Olesen & C.G. Jones. 2002. Trees,
birds and bees in Mauritius: exploitative competi-
tion between introduced honey bees and endemic
nectarivorous birds? J. Bi o g eog. 29: 721–734.
Hargrave, C.W. 2006. A test of three alternative pathways
for consumer regulation of primary productivity. Oe-
cologia 149: 123–132.
Hargreaves, A.L., S.D. Johnson & E. Nol. 2004. Do ﬂo-
ral syndromes predict specialization in plant pol-
lination systems? An experimental test in an “or-
nithophilous” African Protea. Oecologia 140: 295–
Harms, K.E., S.J. Wright, O.,Calderon, et al. 2000.
Pervasive density dependent recruitment enhances
seedling diversity in a tropical forest. Nature 404:
Harvey, C.A. 2000. Windbreaks enhance seed dispersal
into agricultural landscapes in Monteverde, Costa
Rica. Ecol.Appl..10: 155–173.
Hatton, T.J. 1989. Spatial patterning of sweet briar (Rosa
rubiginosa) by two vertebrate species. Aust.J.Ecol.14:
Hayes, J.P. & J.W. Caslick. 1984. Nutrient deposition in
cattail stands by communally roosting blackbirds and
starlings. Am. Midl. Nat. 112: 320–331.
Henderson, W.C. & E.A. Preble. 1935. 1885 – Fiftieth
anniversary notes — 1935. The Survey 16: 59–65.
Herrera, C.M. 1984. A study of avian frugivores, bird-
dispersed plants, and their interaction in Mediter-
ranean scrublands. Ecol. Monog. 54: 1–23.
Herrera, C.M. 1985. Determinants of plant-animal co-
evolution: the case of mutualistic dispersal of seeds
by vertebrates. Oikos 44: 132–141.
Annals of the New York Academy of Sciences
Herrera, C.M. 1989. Frugivory and seed dispersal by car-
nivorous mammals and associated fruit character-
istics, in undisturbed Mediterranean habitats. Oikos
Herrera, C.M. 2002. Seed dispersal by vertebrates. In
Plant-Animal Interactions. An Evolutionary Approach.C.M.
Herrera & O. Pellmyr, Eds.: 185–208. Blackwell Sci-
Herrera, C.M. & P. Jordano. 1981. Prunus mahaleb and
birds: the high-efﬁciency seed dispersal system of
a temperate fruiting tree. Ecol. Monog. 51: 203–
Hicks, R.E. 1979. Guano deposition in an Oklahoma
crow roost. Condor 81: 247–250.
Hingston, A.B., B.D. Gartrell & G. Pinchbeck. 2004.
How specialized is the plant-pollinator association
between Eucalyptus globulus ssp globulus and the
swift parrot Lathamus discolor? Aust. Ecol. 29: 624–
Hiraldo, F., J.C. Blanco & J. Bustamante. 1991. Unspe-
cialized exploitation of small carcasses by birds. Bird
Study 38: 200–207.
Holl, K.D. 1998. Do bird perching structures elevate seed
rain and seedling establishment in abandoned trop-
ical pasture? Rest. Ecol. 6: 253–261.
Holl, K.D. 2002. Effect of shrubs on tree seedling estab-
lishment in an abandoned tropical pasture. J. Ec o l.
Holland, J.M., M.A.S. Hutchison, B. Smith, et al. 2006.
A review of invertebrates and seed-bearing plants as
food for farmland birds in Europe. Annals Appl. Biol.
Holmes, R.J. & R.J. Froud-Williams. 2005. Post-dispersal
weed seed predation by avian and non-avian preda-
tors. Agric. Ecosystems Env. 105: 23–27.
Holmes, R.T. 1990. Ecological and evolutionary impacts
of predation on forest insects: an overview. Studies
Avian Biol. 13: 6–13.
Holmes, R.T., J.C. Schultz & P. Nothnagle. 1979. Bird
predation on forest insects: an exclosure experiment.
Science 206: 462–463.
Holmes, R.T. & F.W. Sturges. 1975. Bird community
dynamics and energetics in a northern hardwoods
ecosystem. J. Anim. Ecol. 44: 175–200.
Holthuijzen, A.M.A. & T.L. Sharik. 1985. The red cedar
(Juniperus virginiana L.) seed shadow along a fenceline.
Am. Midland Nat. 113: 200–202.
Hooks, C.R., R.R. Pandey & M.W. Johnson. 2003. Impact
of avian and arthropod predation on lepidopteran
caterpillar densities and plant productivity in an
ephemeral agroecosystem. Ecol. Ent. 28: 522–532.
Hoppes, W.G. 1988. Seedfall pattern of several species of
bird-dispersed plants in an Illinois woodland. Ecology
Hori, M. & T. Noda. 2001. Spatio-temporal variation of
avian foraging in the rocky intertidal food web. J.
Anim. Ecol. 70: 122–137.
Hori, M. & T. Noda. 2007. Avian predation on wild and
cultured sea urchin Strongylocentrotus intermedius in a
rocky shore habitat. Fisheries Sci. 73: 303–313.
Houston, D.C. 1979. The adaptations of scavengers. In
Serengeti, Dynamics of An Ecosystem. A.R.E. Sinclair &
M.N. Grifﬁths, Eds.: 263–286. University Chicago
Press. Chicago, IL.
Houston, D.C. 1986. Scavenging efﬁciency of turkey vul-
tures in tropical forest. Condor 88: 312–232.
Houston, D.C. & J.E. Cooper. 1975. The digestive tract of
the whiteback griffon vulture and its role in disease
transmission among wild ungulates. J. Wildl. Dis. 11:
Howe, H.F. 1986. Seed dispersal by fruit-eating birds and
mammals. In Seed Dispersal. D.R. Murray, Ed.: 123–
189. Academic Press. Sydney, Australia.
Howe, H.F. & M.N. Miriti. 2004. When seed dispersal
matters. Bioscience 54: 651–660.
Howe, H.F. & J.S. Brown. 1999. Effects of birds and ro-
dents on synthetic tallgrass communities. Ecology 80:
Howe, H.F. & J.S. Brown. 2001. The ghost of granivory
past. Ecol. Lett. 4: 371–378.
Howe, H.F., J.S. Brown & B. Zorn-Arnold. 2002. A rodent
plague on prairie diversity. Ecol. Lett. 5: 30–36.
Howe, H.F. & J. Smallwood. 1982. Ecology of seed dis-
persal. Ann. Rev. Ecol. Syst. 13: 201–228.
Hughes, J.M. 1999. Yellow-billed Cuckoo (Coccyzus ameri-
canus). In The Birds of North America, No. 418. A. Poole
& F. Gill, Eds. The Birds of North America, Inc.
Hughes, J.M. 2001. Black-billed Cuckoo (Coccyzus ery-
thropthalmus). In The Birds of North America, No. 587. A.
Poole & F. Gill, Eds. The Birds of North America,
Inc. Philadelphia, PA.
Husby M. 2006. Predation rates on bird nests by predatory
birds and mammals around refuse dumps. J. Ornith.
Isack, H.A. & H.-U. Reyer. 1989. Honeyguides and honey
gatherers: interspeciﬁc communication in a symbi-
otic relationship. Science 243: 1343–1345.
Izhaki, I., P.B. Walton & U.N. Safriel. 1991. Seed
shadows generated by frugivorous birds in an
eastern Mediterranean scrub. J. E c ol. 79: 575–
Jantti, A., T. Aho, H. Hakkarainen, et al. 2001. Prey de-
pletion by the foraging of the Eurasian treecreeper,
Certhia familiaris, on tree-trunk arthropods. Oecologia
Janzen, D.H. 1983. Seed and pollen dispersal by ani-
mals: convergence in the ecology of contamination
and sloppy harvest. Biol. J. Linnean Soc. 20: 103–
Birds and Ecosystem Services
Janzen, D.H. 1984. Dispersal of small seeds by big herbi-
vores: foliage is the fruit. Am. Nat. 123: 338–353.
Joern, A. 1986. Experimental-study of avian predation
of coexisting grasshopper populations (Orthoptera,
Acrididae) in a sandhills grassland. Oikos 46: 243–
Johnson, S.D. & K.E. Steiner. 2003. Specialized polli-
nation systems in southern Africa. S. Afr. J. Sci. 99:
Johnson, W.C. & C.S. Adkisson. 1985. Dispersal of beech
nuts by blue jays in fragmented landscapes. Am. Mid-
land Nat. 113: 319–324.
Johnson, W.C., C.S. Adkisson, T.R. Crow & M.D. Dixon.
1997. Nut caching by blue jays (Cyanocitta cristata L.):
implications for tree demography. Am. Midland Nat.
Johnson, W.C. & T. Webb. 1989. The role of blue jays
(Cyanocitta cristata L.) in the post-glacial dispersal of
fagaceous trees in eastern North America. J. B i og e o g r.
Jones, C.G., J.H. Lawton & M. Shachak.1994. Organisms
as ecosystem engineers. Oikos 69: 373–386.
Jones, G.A., K.E. Sieving & S.K. Jacobson. 2005.
Avian diversity and functional insectivory on north-
central Florida farmlands. Cons. Biol. 19: 1234–
Jordano, P. 2000. Fruits and frugivory. In Seeds: The Ecology
of Regeneration in Plant Communities.M.Fenner,Ed.:
125–165. CABI Publishing. New York, NY.
Jordano, P., C. Garcia, J.A. Godoay & J.L. Garc´
Castano. 2007. Differential contribution of frugi-
vores to complex seed dispersal patterns. Proc. Natl.
Acad. Sci. USA104: 3278–3282.
Kamil, A.C. & J.E. Jones. 1997. The seed storing corvid
Clark’s nutcracker learns geometric relationships
among landmarks. Nature 390: 276–279.
Karr, J.R., S.K. Robinson, J.G. Blake & R.O. Bierre-
gaard.1990. Birds of four Neotropical forests. In Four
Neotropical Forests. A.H. Gentry, Ed.: 237–269. Yale
University Press. New Haven, CT.
Kato, M. & A. Kawakita. 2004. Plant-pollinator inter-
actions in New Caledonia inﬂuenced by introduced
honey bees. Amer. J. Bot. 91: 1814–1827.
Kattan, G. & M. Murcia. 1985. Hummingbird association
with acorn woodpecker sap trees in Colombia. Condor
Kay, B.J., L.E. Twigg, T.J. Korn & H.I. Nicol. 1994.
The use of artiﬁcial perches to increase predation
on house mice (Mus domesticus)byraptors.Wildl. Res.
Kelly, D., J.J. Ladley & A.W. Robertson. 2004. Is dispersal
easier than pollination? Two tests in new Zealand
Loranthaceae. New Zeal. J. Bot. 42: 89–103.
Kelt, D.A., P.L. Meserve & J.R. Gutierrez. 2004. Seed
removal by small mammals, birds and ants in semi-
arid Chile, and comparison with other systems. J.
Biogeog. 31: 931–942.
Kilham, L. 1953. Warblers, hummingbird, and sapsucker
feeding on sap of yellow birch. Wilson Bull. 65: 198.
King, D.I. & J.H. Rappole. 2000. Winter ﬂocking of insec-
tivorous birds in montane Pine-oak forests in middle
America. Condor 102: 664–672.
Kirk, D.A., M.D. Evenden & Mineau. 1996. Past and Wr-
rent attempts to evaluate the role of birdsas predators
of insect pests in temperate agriwitur. Curr. Ornith. 13:
Kirk, D.A. & M.J. Mossman. 1998. Turkey Vulture
(Cathartes aura). In The Birds of North America, No. 339.
A. Poole & F. Gill, Eds. The Birds of North America,
Inc. Philadelphia, PA.
Kirkpatrick, C.M. & W.H. Elder. 1951. The persecu-
tion of predaceous birds. Wilson Bull. 63: 138–
Kitchell, J.F., D.E. Schindler, B.R. Herwig, et al. 1999.
Nutrient cycling at the landscape scale: the role of
diel foraging migrations by geese at the Bosque del
Apache National Wildlife Refuge, New Mexico. Lim-
nol. Oceanog. 44: 828–836.
Klem, D., JR. 1990. Collisions between birds and win-
dows: mortality and prevention. J. Field Or nith. 61:
Klem, D., D.C. Keck, K.L. Marty, et al. 2004. Effects of
window angling, feeder placement, and scavengers
on avian mortality at plate glass. Wilson Bull. 116:
Kolodziejska-Degorska, I. & M. Zych. 2006. Bees sub-
stitute birds in pollination of ornitogamous climber
Campsis radicans (L.) Seem. in Poland. Acta Societatis
Botanicorum Poloniae 75: 79–85.
Koon, L.C. & Earl of Cranbrook. 2002. Swiftlets of Borneo
— Builders of Edible Nests. Natural History Publication
(Borneo) SDN., B.H.D. Sabah, Malaysia.
Korpimaki, E., V. Koivunen & H. Hakkarainen. 1996.
Microhabitat use and behavior of voles under weasel
and raptor predation risk: predator facilitation? Be-
hav. Ecol. 7: 30–34.
Korpimaki E. & K. Norrdahl. 1991. Numerical and
functional-responses of kestrels, short-eared owls,
and long-eared owls to vole densities. Ecology 72:
Korpimaki E. & K. Norrdahl. 1998. Experimental reduc-
tion of predators reverses the Crash phase of small-
rodent cycles. Ecology 79: 2448–2455.
Kotler, B.P., J.S. Brown, R.H. Slotow, et al. 1993. The in-
ﬂuence of snakes on the foraging behavior of gerbils.
Oikos 67: 309–316.
Kotler B.P., L. Blaustein & J.S. Brown. 1992. Predator
facilitation — the combined effect of snakes and owls
on the foraging behavior of gerbils. Ann. Zoo.Fenn. 29:
Annals of the New York Academy of Sciences
Kremen, C. & R.S. Ostfeld. 2005. A call to ecologists:
measuring, analyzing, and managing ecosystem ser-
vices. Front. Ecol. Environ. 3: 540–548.
Kroeger, T. & F. Casey. 2007. An assessment of market-
based approaches to providing ecosystem services on
agricultural lands. Ecol. Econ. 64: 321–332.
Kwit C., D.J. Levey & C.H. Greenberg. 2004. Con-
tagious seed dispersal beneath heterospeciﬁc fruit-
ing trees and its consequences. Oikos 107: 303–
Lanner, R.M. 1996. Made for Each Other: A Symbiosis of Birds
and Pines. Oxford University Press, New York.
LaRouche, G.P. 2001. Birding in the United States: a
demographic and economic analysis. Report 2001-
1, U.S. Fish and Wildlife Service, Washington, DC.
Larson, D.L. 1996. Seed dispersal by specialist versus gen-
eralist foragers—the plant’s perspective. Oikos 76:
Laurance, W.F., H.E.M. Nascimento, S.G. Laurance,
et al. 2006. Rain forest fragmentation and the pro-
liferation of successional trees. Ecology 87: 469–
Levey, D.J. 1988a. Spatial and temporal variation in Costa
Rican fruit and fruit-eating bird abundance. Ecol.
Monog. 58: 251–269.
Levey, D.J. 1988b. Tropical wet forest treefall gaps and
distributions of understory birds and plants. Ecology
Levey, D.J. 1990. Habitat-dependent fruiting behaviour of
an understorey tree, Miconia centrodesma and tropical
treefall gaps as keystone habitats for frugivores in
Costa Rica. J. Trop. Ecol . 6: 409–420.
Levey, D.J., B.M. Bolker, J.J. Tewksbury, et al. 2005. Effects
of landscape corridors on seed dispersal by birds.
Science 309: 146–148.
Li, X. & S.D. Wilson. 1998. Facilitation among woody
plants establishing in an old ﬁeld. Ecology 79: 2694–
Lichtenberg, J.S. & D.A. Lichtenberg. 2002. Weak trophic
interactions among birds, insects and white oak
saplings (Quercus alba). Am. Midl. Nat. 148: 338–349.
Lima, S.L. & T.J. Valone. 1991. Predators and avian com-
munity organization – an experiment in a semidesert
grassland. Oecologia 86: 105–112.
Linzey, A.V. & K.A. Washok. 2000. Seed removal by ants,
birds and rodents in a woodland savanna habitat in
Zimbabwe. African Zoo. 35: 295–299.
Lopez, L. & J. Terborgh. 2007. Seed predation and
seedling herbivory as factors in tree recruitment fail-
ure on predator-free forested islands. J. Tr op. E c ol. 23:
Lopez de Casenave, J., V.R. Cueto & L. Marone. 1998.
Granivory in the Monte desert, Argentina: is it less
intense than in other arid zones of the world? Global
Ecol. Biogeog. Lett. 7: 197–204.
Lotka, A.J. 1924. Elements of Physical Biology. Williams
and Wilkins Company. Baltimore.
Lozada, T., G.H.J. de Koning, R. Marche, et al. 2007.
Tree recovery and seed dispersal by birds: comparing
forest, agroforestry and abandoned agroforestry in
coastal Ecuador. Perspect. Plant Ecol. Evol. Syst. 8: 131–
MacArthur, R.H. 1958. Population ecology of some war-
blers of northeastern coniferous forests. Ecology 39:
Malmborg, P.K. & M.F. Willson. 1988. Foraging ecology
of avian frugivores and some consequences for seed
dispersal in an Illinois woodlot. Condor 90: 173–186.
Manny, B.A., R.G. Wetzel & W.C. Johnson. 1975. Annual
contributions of carbon, nitrogen, and phosphorus
by migrant Canada Geese to a hardwater lake. Int.
Ver. Theor. Angew. Limnol. Verh. 19: 949–957.
Mantyla, E., T. Klemola & E. Haukioja. 2004. Attrac-
tion of willow warblers to sawﬂy-damaged mountain
birches: novel function of inducible plant defences?
Ecol. Lett. 7: 915–918.
Marcone, M. 2005. Characterization of the edible bird’s
nest the “Caviar of the East”. Food Res. Int. 38: 1125–
Markwell, T.J. 1997. Video camera count of burrow-
dwelling fairy prions, sooty shearwaters, and tuatara
on Takapourewa (Stephens Island), New Zealand.
New Zeal. J. Zool. 24: 231–237.
Marquis, R.J. & C.J. Whelan. 1994. Insectivorous birds
increase growth of white oak through consumption
of leaf-chewing insects. Ecology 75: 2007–2014.
Marsh, R.E. 1998. Barn Owl nest boxes offer no solution
to pocket gopher damage. Proc. 18th Vertebr. Pest
Conf. Univ. Calif., Davis, CA.
Martin, A.C., H.S. Zim & A.L. Nelson. 1951. American
Wildlife and Plants. A Guide to Wildlife Food Habits.Dove.
New York, NY.
Marti, C.D., A.F. Poole & L.R. Bevier (2005). Barn Owl
(Tyto alba). In The Birds of North America. A. Poole, Ed.
Cornell Laboratory of Ornithology. Ithaca, NY.
Martin, T.E. & D.M. Finch. 1995. Ecology and Management
of Neotropical Migratory Birds: A Synthesis and Review of
Critical Issues. Oxford University Press. New York,
ınez-Garza, C. & R. Gonzalez-Montagut. 2002.
Seed rain of ﬂeshy-fruited species in tropical pastures
in Los Tuxtlas, Mexico. J. Tro p. Ec o l . 18: 457–462.
ınez del Rio, C., M. Hourdequin, A. Silva
& R. Medel. 1995. The inﬂuence of cac-
tus size and previous infection on bird deposi-
tion of mistletoe seeds. Aust. J. Ecol. 20: 571–
ınez-Garza, C. & H.F. Howe. 2003. Restoring trop-
ical diversity: beating the time tax on species loss. J.
Appl. Ecol. 40: 423–429.
Birds and Ecosystem Services
ınez-Ramos, M. & E.R. Alvarez-Buylla. 1995. Seed
dispersal and patch dynamics in tropical rain forests:
a demographic approach. Ecoscience 2: 223–229.
Mathew, W.M. 1970. Peru and the British guano market,
1840–1870. Econ. Hist. Rev. 23: 112–128.
Mayﬁeld, M.M., D. Ackerly & G.C. Daily. 2006. The di-
versity and conservation of plant reproductive and
dispersal functional traits in human-dominated trop-
ical landscapes. J. Ec o l . 94: 522–536.
Mathew, W.M. 1976. A primitive export sector: guano
production in mid-nineteenth century Peru. J. Latin
Amer. Stud. 9: 35–57.
Mazia, C.N., T. Kitzberger & E.J. Chaneton. 2004. In-
terannual changes in folivory and bird insectivory
along a natural productivity gradient in northern
Patagonian forests. Ecography 27: 29–40.
McAtee, W.L. 1935. Food Habits of Common Hawks.U.S.
Dept. of Agr., Circular 370.
McClanahan, T.R. & R.W. Wolfe. 1993. Accelerating for-
est succession in a fragmented landscape: the role of
birds and perches. Cons. Biol. 7: 279–288.
McColl, J.G. & J. Burger. 1976. Chemical inputs by a
colony of Franklin’s Gulls nesting in cattails. Am.
Midl. Nut. 96: 270–280.
McConkey, K.R. & D.R. Drake. 2002. Extinct pigeons
and declining bat populations: Are large seeds still
being dispersed in the tropical Paciﬁc? In Seed Dis-
persal and Frugivory: Ecology, Evolution and Conservation.
D.J. Levey, W.R. Silva & M. Galetti, Eds.: 381–395.
CABI Publishing. Wallingford, UK.
McDonnell, M.J. 1986. Old ﬁeld vegetation height and
the dispersal pattern of bird-disseminated woody
plants. Bull. Torrey Bot. Club 113: 6–11.
Medan, D. & N.H. Montaldo. 2005. Ornithophily in the
Rhamnaceae: the pollination of the Chilean endemic
Colletia ulicina.Flora 200: 339–344.
Medina, R.F. & P. Barbosa. 2002. Predation of small and
large Orgyia leucostigma (J.E. Smith) (Lepidoptera: Ly-
mantriidae) larvae by vertebrate and invertebrate
predators. Env. Ent. 31: 1097–1102.
Meehan, H.J., K.R. McConkey & D.R. Drake. 2002. Po-
tential disruptions to seed dispersal mutualisms in
Tonga, Western Polynesia. J. Bi o geog. 29: 695–712.
Meyerriecks, A.J. & D.W. Nellis. 1967. Egrets serving as
“beaters” for Belted Kingﬁshers. Wilson Bull. 79:
Micheneau, C., J. Fournel & T. Pailler. 2006. Bird polli-
nation in an angraecoid orchid on Reunion Island
(Mascarene Archipelago, Indian Ocean). Ann. Bot.
Millennium Ecosystem Assessment. 2003. Ecosystems and
Human Well-being: A Framework for Assessment.Island
Press. Washington, DC.
Milsom, T.P., D.C. Ennis, D.J. Haskell, et al. 1998. Design
of grassland feeding areas for waders during winter:
the relative importance of sward, landscape factors
and human disturbance. Biol. Cons. 84: 119–129.
Mols, C.M.M. & M.E. Visser. 2002. Great tits can reduce
caterpillar damage in apple orchards. J. Appl. Ecol.
Monaghan, P., C.B. Shedden, K. Ensor, et al. 1985.
Salmonella carriage by herring-gulls in the Clyde area
of Scotland in relation to their feeding ecology. J.
App. Ecol. 22: 669–680.
Monteiro, L.R. & R.W. Furness. 1995. Seabirds as mon-
itors of mercury in the marine environment. Wat er
Air Soil Poll. 80: 851–870.
Monteiro, R.F., R.P. Martins & K. Yamamoto. 1992. Host
speciﬁcity and seed dispersal of Psittacanthus robustus
Loranthaceae in south-east Brazil. J. Trop. Ecol . 8:
Monterrubio-Rico, T.C. & P. Escalante-Pliego. 2006.
Richness, distribution and conservation status of cav-
ity nesting birds in Mexico. Biol. Cons. 128: 67–78.
Montgomery, B.R., D. Kelly & J.J. Ladley. 2001. Pollina-
tor limitation of seed set in Fuchsia perscandens (On-
agraceae) on Banks Peninsula, South Island, New
Zealand. New Zeal. J. Bot. 39: 559–565.
Montgomery, B.R., D. Kelly, A.W. Robertson & J.J.
Ladley. 2003. Pollinator behaviour, not increased re-
sources, boosts seed set on forest edges in a New
Zealand Loranthaceous mistletoe. New Zeal. J. Bot.
Mooney, K.A. 2006. The disruption of an ant-aphid mu-
tualism increases the effects of birds on pine herbi-
vores. Ecology 87: 1805–1815.
Mooney, K.A. 2007. Tritophic effects of birds and ants on
a canopy food web, tree growth, and phytochemistry.
Ecology 88: 2005–2014.
Mooney, K.A. & Y.B. Linhart. 2006. Contrasting cas-
cades: insectivorous birds increase pine but not
parasitic mistletoe growth. J. Anim. Ecol. 75: 350–
Moorcroft, D., M.J. Whittingham, R.B. Bradbury, et al.
2002. The selection of stubble ﬁelds by wintering
granivorous birds reﬂects vegetation cover and food
abundance. J. Appl. Ecol. 39: 535–547.
Morse, D.H. 1978. Populations of bay-breasted and Cape
May warblers during an outbreak of the spruce bud-
worm. Wilson Bull. 90: 404–413.
Moss, M.L. & P.M. Bowers. 2007. Migratory bird harvest
in northwestern Alaska: a zooarchaeological analysis
of Ipiutak and Thule occupations from the Deering
archaeological district. Arctic Anthrop. 44: 37–50.
Mossman, M.J. 1991. Black and turkey vultures. In Pro-
ceedings of the Midwest Raptor Management Symposium and
Work s h o p : 3–22. Natl. Wildl. Fed. Washington, DC.
Murakami, M. 1999. Effect of avian predation on survival
of leaf-rolling lepidopterous larvae. Res. Pop. Ecol. 41:
Annals of the New York Academy of Sciences
Murakami, M. & S. Nakano. 2000. Species-speciﬁc bird
functions in a forest-canopy food web. Proc. Royal Soc.
London B. 267: 1597–1601.
Murphy, D.J. & D. Kelly. 2001. Scarce or distracted?
Bellbird (Anthornis melanura) foraging and diet in an
area of inadequate mistletoe pollination. New Zeal. J.
Ecol. 25: 69–81.
Nabhan, G.P. & S. Buchmann. 1997. Services provided
by pollinators. In Nature’s Services: Societal Dependence of
Natural Ecosystems. G.C. Daily, Ed.: 133–150. Island
Press. Washington, DC.
Nakano S. & Murakami M. 2001. Reciprocal subsidies:
dynamic interdependence between terrestrial and
aquatic food webs. Proc. Natl. Acad. Sci. USA 98: 166–
Nakano, S., H. Miyasaka & N. Kuhara. 1999. Terrestrial-
aquatic linkages: riparian arthropod inputs alter
trophic cascades in a xxxxxxx food web ecology 80:
Neeman, G. & I. Izhaki. 1996. Colonization in an aban-
doned East-Mediterranean vineyard. J. Veg . Sc i . 7:
Neilan, W., C.P. Catterall, J. Kanowski & S. McKenna.
2006. Do frugivorous birds assist rainforest succes-
sion in weed dominated oldﬁeld regrowth of sub-
tropical Australia?. Biol Conserv. 129: 393–407.
Nepstad, D.C., C. Uhl, C.A. Pereira & J.M.C. da Silva.
1996. A comparative study of tree establishment
in abandoned pasture and mature forest of eastern
Amazonia. Oikos 76: 25–39.
Neubig, J.B. & J.A. Smallwood. 1999. The “signiﬁ-
cant others” of American kestrels: cohabitation with
arthropods. Wilson Bull. 111: 269–271.
Newman, D.G. 1987. Burrow use and population den-
sities of tuatara (Sphenodon punctatus) and how they
are inﬂuenced by fairy prions (Pachyptila turtur)on
Stephens Island, New Zealand. Herpetologica 43:
Nogales, M., V. Quilis, F.M. Medina, et al. 2002. Are
predatory birds effective secondary seed dispersers?
Biol. J. Linn. Soc. 75: 345–352.
Norman, F.I., R.A. Mcfarlane & S.J. Ward. 1994. Car-
casses of adelie penguins as a food source for south
polar skuas: some preliminary observations. Wilson
Bull. 106: 26–34.
Oaks, J.L., M. Gilbert, M.Z. Virani, et al. 2004. Diclofenac
residues as the cause of vulture population decline in
Pakistan. Nature 427: 630–633.
Ohishi, I., G. Sakaguchi, H. Rieman, et al. 1979. Antibod-
ies to Clostridium botulinum toxins in free-living birds
and mammals. J. Wildl. Dis. 15: 3–9.
Oro, D. & A. Mart´
ın. 2007. Deconstructing
myths on large gulls and their impact on threat-
ened sympatric waterbirds. Anim. Cons. 10: 117–
Ortiz, N.E. & G.R. Smith. 1994. Landﬁll sites, botulism
and gulls. Epidem. Inf. 112: 385–391.
Ortega-Olivencia, A., T. Rodriguez-Riano, F.J. Valtuena,
et al. 2005. First conﬁrmation of a native bird-
pollinated plant in Europe. Oikos 110: 578–590.
Ostfeld, R.S. & C.D. Canham. 1993. Effects of meadow
vole population-density on tree seedling survival in
old ﬁelds. Ecology 74: 1792–1801.
Otzen, W. & M. Schaefer. 1980. Hibernation of arthro-
pods in bird nests: contribution to winter ecology.
Zool. Jahrb. Abt. Syst. Oekol. Geogr. Tiere 107: 435–448.
Pain, D., A.A. Cunningham, P.F. Donald, et al. 2003.
Causes and effects of temporospatial declines of Gyps
vultures in Asia. Cons. Biol. 17: 661–671.
Parmalee, P.W. 1954. The vultures: their movements, eco-
nomic status, and control in Texas. Auk 71: 443–453.
Pausas, J.G., A. Bonet, F.T. Maestre & A. Climent. 2006.
The role of the perch effect on the nucleation process
in Mediterranean semi-arid oldﬁelds. Acta Oecologia
Payne, L.X. & J.W. Moore. 2006. Mobile scavengers cre-
ate hotspots of freshwater productivity. Oikos 115:
Peres, C.A. 2001. Synergistic effects of subsistence hunt-
ing and habitat fragmentation on Amazonian forest
Vertebrates. Cons. Biol. 15: 1490–1505.
Peres, C.A. & E. Palacios. 2007. Basin-wide effects
of game harvest on vertebrate population densi-
ties in Amazonian forests: implications for animal-
mediated seed dispersal. Biotropica. 39: 304–315.
erez de la Lastra, J.M. & J. de la Fuente. 2007. Molecular
cloning of the griffon vulture (Gyps fulvus) toll-like
receptor. Dev. Comp. Immun. 31: 511–519.
Perfecto, I., J.H. Vandermeer, G.L. Bautista, et al. 2004.
Greater predation in shaded coffee farms: the role of
resident neotropical birds. Ecology 85: 2677–2681.
Pﬁster, C.A., J.T. Wootton & C.J. Neufeld. 2007.
Chemical characteristics of an intensively sampled
nearshore system. Lim. Ocean. 52: 1767–1775.
Philpott, S.M., R. Greenberg, P. Bichier & I. Perfecto.
2004. Impacts of major predators on tropical agro-
forest arthropods: comparisons within and across
taxa. Oecologia 140: 140–149.
Polis G.A., Anderson W.B. & Holt R.D. 1997. Toward an
integration of landscape and food web ecology: the
dynamics of spatially subsidized food webs. Ann. Rev.
Ecol. Syst. 28: 289–316.
Pollux, B.J.A., L. Santamaria & N.J. Ouborg. 2005. Differ-
ences in endozoochorous dispersal between aquatic
plant species, with reference to plant population per-
sistence in rivers. Fresh. Biol. 50: 232–242.
Pons, J. & J.G. Pausas. 2007. Acorn dispersal estimated by
radio-tracking. Oecologia 153: 903–911.
Power, M.E. 2001. Prey exchange between a stream and
its forested watershed elevates predator densities in
Birds and Ecosystem Services
both habitats. Proc. Natl. Acad. Sci. USA 98: 14–
Power,M.E.,D.Tilman,J.A.Estes,et al. 1996. Challenges
in the quest for keystones. Bioscience 46: 609–620.
Prakash, V., D.J. Pain, A.A. Cunningham, et al. 2005.
Catastrophic collapse of Indian white-backed Gyps
bengalensis and long-billed Gyps indicus vulture popu-
lations. Biol. Cons. 109: 381–390.
Price, J.P. & W.L. Wagner. 2004. Speciation in Hawaiian
angiosperm lineages: cause, consequence and mode.
Evol. 58: 2185–2200.
Ramsey, M.W. 1988. Differences in pollinator effective-
ness of birds and insects visiting Banksia menziesii (Pro-
teaceae). Oecologia. 76: 119–124.
Rathcke, B. J. 2000. Hurricane causes resource and pol-
lination limitation of fruit set in a bird-pollinated
shrub. Ecology 81: 1951–1958.
Ray, T.S. & C.C. Andrews. 1980. Antbutterﬂies: butter-
ﬂies that follow army ants to feed on antbird drop-
pings. Science 210: 1147–1148.
Recher, H.F. & J.D. Majer. 2006. Effects of bird predation
on canopy arthropods in wandoo Eucalyptus wandoo
woodland. Aust. Ecol. 31: 349–360.
Reid, N. 1989. Dispersal of mistletoes by honeyeaters and
ﬂowerpeckers: components of seed dispersal quality.
Ecology 70: 137–145.
Remsen, J. 2003. Family Furnariidae (Ovenbirds). In
Handbook of the Birds of the World.J.DelHoyo,A.
Elliott & D. Christie, Eds.: 162–357. Lynx Edicions.
Richardson, B.A., S.J. Brunsfeld & N.B. Klopfenstein.
2002. DNA from bird-dispersed seed and wind-
disseminated pollen provides insights into postglacial
colonization and population genetic structure of
whitebark pine (Pinus albicaulis). Mol. Ecol. 11: 215–
Ridley, H.N. 1930. The Dispersal of Plants throughout the
Wo rl d .Reeve.Ashford,UK.
Robbins, C.S., D.K. Dawson & B.A. Dowell. 1989. Habi-
tat area requirements of breeding forest birds of the
middle Atlantic states. Wildl. Monog. 103: 1–34.
Robertson, A.W., D. Kelly, J.J. Ladley & A.D. Sparrow.
1999. Effects of pollinator loss on endemic New
Zealand mistletoes (Loranthaceae). Cons. Biol. 13:
Robertson, A.W., J.J. Ladley & D. Kelly. 2005. Effective-
ness of short-tongued bees as pollinators of appar-
ently ornithophilous New Zealand mistletoes. Aust.
Ecol. 30: 298–309.
Robinson, G.R. & S.N. Handel. 1993. Forest restoration
on a closed landﬁll—rapid addition of new species
by bird dispersal. Cons. Biol. 7: 271–278.
Robinson, G.R. & S.N. Handel. 2000. Directing spatial
patterns of recruitment during an experimental ur-
ban woodland reclamation. Ecol. Appl. 10: 174–188.
Robinson, R.A. & W.J. Sutherland. 1999. The winter dis-
tribution of seed-eating birds: habitat structure, seed
density and seasonal depletion. Ecography 22: 447–
Rodenhouse, N.L. & R.T. Holmes. 1992. Results of ex-
perimental and natural food reductions for breeding
black-throated blue warblers. Ecology 73: 357–372.
Ruxton, G.D. & D.C. Houston. 2004. Obligate vertebrate
scavengers must be large soaring ﬂiers. J. T he o r. B io l .
Saba S.L. & A. Toyos. 2003. Seed removal by birds, ro-
dents and ants in the Austral portion of the Monte
Desert, Argentina. J. Arid Env. 53: 115–124.
Sakai, A.K., W.L. Wagner & L.A. Mehrhoff. 2002. Pat-
terns of endangerment in the Hawaiian ﬂora. Syst.
Biol. 51: 276–302.
Samuels, I.A. & D.J. Levey. 2005. Effects of gut passage on
seed germination: do experiments answer the ques-
tions they ask? Funct. Ecol. 19: 365–368.
nero, F. & G.A. Polis. 2000. Bottom-up dy-
namics of allochthonous input: direct and indirect
effects of seabirds. Ecology 81: 3117–3132.
Santamaria, L. 2002. Why are most aquatic plants widely
distributed? Dispersal, clonal growth and small-scale
heterogeneity in a stressful environment. Acta Oecolo-
gia 23: 137–154.
Santamaria, L. & M. Klaassen. 2002. Waterbird-
mediated dispersal of aquatic organisms: an intro-
duction. Acta Oecologia 23: 155–119.
Sanz, J.J. 2001. Experimentally increased insectivorous
bird density results in a reduction of caterpillar den-
sity and leaf damage to Pyrenean oak. Ecol. Res. 16:
Sargent, S. 1995. Seed fate in a tropical mistletoe—the
importance of host twig size. Funct. Ecol. 9: 197–204.
Schemske, D.W. & N.V.L. Brokaw. 1981. Treefalls and the
distribution of understory birds in a tropical forest.
Ecology 62: 938–945.
Schupp, E.W., T. Milleron & S.E. Russo. 2002. Dispersal
limitation in tropical forests: consequences for species
richness. In Frugivores and Seed Dispersal: Ecology, Evo-
lution and Conservation. D.J. Levey, W.R. Silva & M.
Galetti, Eds.: 19–34. CABI Publishing. Wallingford,
Schwarz, F.D. 1998. Miracle of the birds. Am. Her. 149:
Sekercioglu, C.H. 2002. Impacts of birdwatching on hu-
man and avian communities. Env. Cons. 29: 282–289.
Sekercioglu, C.H. 2006. Increasing awareness of avian
ecological function. Tre n d s E c o l. Evol. 21: 464–471.
Sekercioglu, C.H., P.R. Ehrlich & G.C. Daily. 2004.
Ecosystem consequences of ecosystem declines. Proc.
Natl. Acad. Sci. USA 101: 18042–18047.
Sekercioglu, C.H., P.R. Ehrlich, G.C. Daily, et al. 2002.
Disappearance of insectivorous birds from tropical
Annals of the New York Academy of Sciences
forest fragments. Proc.Natl.Acad.Sci.USA99: 263–
Selva, N. & M.A. Fortuna. 2007. The nested structure of
a scavenger community. Proc. R. Soc. Lond. B 274:
Selva, N., B. Jedrzejewska, W. Jedrzejewski & A. Wajrak.
2003. Scavenging on European bison carcasses in
Białowiezla Primeval Forest (eastern Poland). Eco-
science 10: 303–311.
Selva, N., B. Jedrzejewska, W. Jedrzejewski & A. Wajrak.
2005. Factors affecting carcass use by a guild of
scavengers in European temperate woodland. Can.
J. Zool. 83: 1590–1601.
Servin, J., S.L. Lindsey & B.A. Loiselle. 2001. Pileated
woodpecker scavenges on a carcass in Missouri. Wil-
son Bull. 113: 249–250.
Shanahan, M., R.D. Harrison, R. Yamuna, et al. 2001.
Colonization of an island volcano, Long Island,
Papua New Guinea & an emergent island, Motmot,
in its caldera lake. V. Colonization by ﬁgs (Ficus spp.),
their dispersers and pollinators. J. Biog e o g. 28: 1365–
Shefﬁeld, L.M., J.R. Crait, W.D. Edge & G.M. Wang.
2001. Response of American kestrels and gray-tailed
voles to vegetation height and supplemental perches.
Can. J. Zool. 79: 380–385.
Shiels, A.B. & L.R. Walker. 2003. Bird perches increase
forest seeds on Puerto Rican landslides. Rest. Ecol.
Shivik JA. 2006. Are vultures birds, and do snakes have
venom, because of macro- and microscavenger con-
ﬂict? Bioscience 56: 819–823.
Sinclair, B.J. & S.L. Chown. 2006. Caterpillars beneﬁt
from thermal ecosystem engineering by wandering
albatrosses on sub-Antarctic Marion Island. Biol. Lett.
Sipura, M. 1999. Tritrophic interactions: willows, herbiv-
orous insects and insectivorous birds. Oecologia 121:
Slocum, M.G. 2001. How tree species differ as recruit-
ment foci in a tropical pasture. Ecology 82: 2547–
Slocum, M.G. & C.C. Horvitz. 2000. Seed arrival under
different genera of trees in a neotropical pasture.
Plant Ecology 149: 51–62.
Skaggs, J.M. 1994. The Great Guano Rush. Entrepreneurs and
American Overseas Expansion. St. Martin’s Press. New
Yo r k , N Y .
Smith-Ramirez, C. & J.J. Ar mesto. 2003. Foraging be-
haviour of bird pollinators on Embothrium coccineum
(Proteaceae) trees in forest fragments and pastures in
southern Chile. Aust. Ecol. 28: 53–60.
Snellen, C.L., P.J. Hodum & E. Fernandez-Juricic.
2007. Assessing western gull predation on pur-
ple sea urchins in the rocky intertidal using op-
timal foraging theory. Canad. J. Zoo. 85: 221–
Snow, D.W. 1981. Tropical frugivorous birds and their
food plants: a world survey. Biotropica 13: 1–14.
Solomon, M.E., D.M.Glen, D.A. Kendall, & N.F. Milsom.
1977. Predation of overwintering larvae of codling
moth (Cydia pomonella (l.)) by birds. J. Appl. Ecol. 13:
Sork, V.L. 1983. Mammalian seed dispersal of pignut
hickory during 3 fruiting seasons. Ecology 64: 1049–
Southwick, E.E. & A.K. Southwick. 1980. Energetics
of Feeding on Tree Sap by Ruby-throated Hum-
mingbirds in Michigan. Amer. Midl. Nat. 104: 328–
Spiegel, O. & R. Nathan. 2007. Incorporating dispersal
distance into the disperser effectiveness framework:
frugivorous birds provide complementary dispersal
to plants in a patchy environment. Ecol. Lett. 10:
Stewart, R.E. & J.W. Aldrich. 1951. Removal and re-
population of breeding birds in a spruce-ﬁr forest
community. Auk: 68: 471–482.
Stiles, F.G. 1981. Geographical aspects of bird-ﬂower co-
evolution, with particular reference to Central Amer-
ica. Ann. Mo. Bot. Gard. 68: 323–351.
Stiles, F.G. 1985. On the role of birds in the dynamics
of Neotropical forests. In Conservation of Tropical Birds,
Vol. ICBP Technical Publication No. 4. A.W. Di-
amond & T.E. Lovejoy, Eds.: 49–59. International
Council for Bird Preservation. Cambridge, UK.
Strengbom, J., J. Witzell, A. Nordin & L. Ericson. 2005.
Do multitrophic interactions override N fertiliza-
tion effects on Operophtera larvae? Oecologia 143: 241–
Strong, A.M., T.W. Sherry & R.T. Holmes. 2000. Bird
predation on herbivorous insects: indirect effects on
sugar maple saplings. Oecologia 125: 370–379.
Sutherland, G.D., C.L. Gass, P.A. Thompson & K.P.
Lertzman. 1982. Feeding territoriality in migrant ru-
fous hummingbirds – defense of yellow-bellied sap-
sucker (Sphyrapicus varius) feeding sites. Can. J. Zool.
Styring, A.R. & K. Ickes. 2001. Interactions between the
Greater Racket-tailed Drongo Dicrurus paradiseus and
woodpeckers in a lowland Malaysian rainforest. Fork -
tail 17: 119–120.
Tanhuanpaa, M., K. Ruohomaki & E.Uusipaikka. 2001.
High larval predation rate in non-outbreaking pop-
ulations of a geometrid moth. Ecology 82: 281–289.
Tasker, M.L., C.J. Camphuysen, J. Cooper, et al. 2000.
The impacts of ﬁshing on marine birds. ICES J. Ma-
rine Sci. 57: 531–547.
Terborgh, J. 1989. Where Have all the Birds Gone? Princeton
University Press. Princeton, NJ.
Birds and Ecosystem Services
Terborgh, J., K. Feeley, M. Silman, et al. 2006. Vegetation
dynamics of predator-free land-bridge islands. J. Ec o l.
Terborgh, J., L. Lopez, P. Nunez, et al. 2001. Ecological
meltdown in predator-free forest fragments. Science
Tester, M., D.C. Patton, N. Reid & R.T. Lange. 1987.
Seed dispersal by birds and densities of shrubs under
trees in arid south Australia. Trans.RoyalSoc.S.Aust.
Tewksbury, J.J., G.P. Nabhan, D. Norman, et al. 1999.
In situ conservation of wild chilies and their biotic
associates. Con. Biol. 13: 98–107.
ery, M. & D. Larpin. 1993. Seed dispersal and veg-
etation dynamics at a cock-of-the-rock’s lek in the
tropical forest of French Guiana. J. Trop. Ecol. 9:
Thompson, J.N. & M.F. Willson. 1978. Disturbance and
the dispersal of ﬂeshy fruits. Science 200: 1161–1163.
Toh, I., M. Gillespie & D. Lamb. 1999. The role of iso-
lated trees in facilitating tree seedling recruitment at
a degraded sub-tropical rainforest site. Rest. Ecol. 7:
Tomback, D.F. 1982. Dispersal of whitebark pine seeds by
Clark’s nutcracker: a mutualism hypothesis. Journal
of Ecology 51: 451–467.
Tomback, D.F. & Y.B. Linhart. 1990. The evolution of
bird-dispersed pines. Evol. Ecol. 4: 185–219.
Traveset, A. & M. Verdu. 2002. A meta-analysis of the
effect of gut treatment on seed germination. In Seed
Dispersal and Frugivory: Ecology, Evolution and Conserva-
tion. D.J. Levey, W.R. Silva & M. Galetti, Eds.: 339–
350. CABI Publishing. Wallingford, UK.
Turner, R.K., J. Paavola, P. Cooper, et al. 2003. Valuing
nature: lessons learned and future research direc-
tions. Ecol. Econ. 46: 493–510.
Valdivia-Hoeﬂich, T. & J.H. Vega Rivera. 2005. The cit-
reoline trogon as an ecosystem engineer. Biotropica
Valeiras, J. 2003. Attendance of scavenging seabirds at
trawler discards off Galicia, Spain. Scientia Marina
Valiela, I. & P. Martinetto. 2007. Changes in bird abun-
dance in eastern North America: urban sprawl and
global footprint? Bioscience 57: 360–370.
Valiente-Banuet, A., A. Bolongaro-Crevenna, O. Briones,
et al. 1991. Spatial relationships between cacti and
nurse shrubs in a semi-arid environment in central
Mexico. J. Ve g. S c i . 2: 15–20.
Van Bael, S.A. & J.D. Brawn. 2005. The direct and indi-
rect effects of insectivory by birds in two contrasting
Neotropical forests. Oecologia 143: 106–116.
Van Bael, S.A., J.D. Brawn & S.K. Robinson. 2003. Birds
defend trees from herbivores in a Neotropical forest
canopy. Proc. Natl. Acad. Sci. USA 100: 8304–8307.
Van Der Pijl, L. 1972. Principles of Dispersal in Higher Plants,
2nd edn. Springer-Verlag. Berlin.
Vander Wall, S.B. 1997. Dispersal of singleleaf pi ˜
(Pinus monophylla) by seed-caching rodents. J. Mamm.
Vander Wall, S.B. & R.P. Balda. 1977. Coadaptations
of the Clark’s nutcracker and the pi˜
non pine for
efﬁcient seed harvest and dispersal. Ecol. Monog. 47:
Van Maanen, E., I. Goradze, A. Gavashelishvili & R.
Goradze. 2001. Trapping and hunting of migratory
raptors in western Georgia. Bird. Cons. Int. 11: 77–92.
Viviansmith, G. & E.W. Stiles. 1994. Dispersal of salt
marsh seeds on the feet and feathers of waterfowl.
Wetlands 14: 316–319.
Votier, S.C., R.W. Furness, S. Bearhop, et al. 2004.
Changes in ﬁsheries discard rates and seabird com-
munities. Nature 427: 727–730.
Votier, S.C., S. Bearhop, J.E. Crane, et al. 2007. Seabird
predation by great skuas Stercorarius skua—intra-
speciﬁc competition for food? J. Avian Biol. 38: 234–
Wallace, K.J. 2007. Classiﬁcation of ecosystem ser-
vices: problems and solutions. Biol. Con. 139: 235–
Ward, M.J. & D.C. Paton. 2007. Predicting mistletoe seed
shadow and patterns of seed rain from movements
of the mistletoebird, Dicaeum hirundinaceum.Aust. Ecol.
Waser, N.M. 1978. Competition for hummingbird pol-
lination and sequential ﬂowering in two Colorado
wildﬂowers. Ecology 59: 934–944.
Waser, N.M. 1979. Pollinator availability as a determi-
nant of ﬂowering time in ocotillo (Fouquieria splendens).
Oecologia 39: 107–121.
Watson, D.M. 2001. Mistletoe—A keystone resource in
forests and woodlands worldwide. Ann. Rev. Ecol. Syst.
Watson, R.T., M. Gilbert, J.L. Oaks & M. Virani. 2004.
The collapse of vulture populations in south Asia.
Biodiversity 5: 3–7.
Webb, C.O. & D.R. Peart. 2001. High seed dispersal rates
in faunally intact tropical rain forest: theoretical and
conservation implications. Ecol. Lett. 4: 491–499.
Weed, C.M. & N. Dearborn. 1903. Birds in their Relations
to Man. A Manual of Economic Ornithology for the United
States and Canada. J.B. Lippincott Company. Philadel-
Wenny, D.G. & D.J. Levey. 1998. Directed seed dispersal
by bellbirds in a tropical cloud forest. Proc. Natl. Acad.
Sci. USA 95: 6204–6207.
Wheelwright, N.T. & G.H. Orians. 1982. Seed dispersal
by animals: contrasts with pollen dispersal, problems
of terminology, and constraints on coevolution. Am.
Nat. 119: 402–413.
Annals of the New York Academy of Sciences
Whelan C.J. & R.J. Marquis. 1995. Songbird
ecosystem function and conservation. Science 268:
Whittingham, M.J., J.R. Kreb, R.D. Swetnam, et al. 2007.
Should conservation strategies consider spatial gen-
erality? Farmland birds show regional not national
patterns of habitat association. Ecol. Lett. 10: 25–35.
Whittingham, M.J. & H.M. Markland. 2002. The inﬂu-
ence of substrate on the functional response of an
avian granivore and its implications for farmland
bird conservation. Oecologia 130: 637–644.
Wiens, J.A. 1973. Pattern and process in grassland bird
communities. Ecol. Monog. 43: 237–270.
Wilkinson, D.M. 1997. Plant colonization – are wind dis-
persed seeds really dispersed by birds at larger spatial
and temporal scales. J. Biog e o g. 24: 61–65.
Wilkinson, N.B. 1984. Lammot Du Pont and the American
Explosives Industry, 1850–1884. University of Virginia
Press. Charlottesville, VA.
Williams, C.K., R.D. Applegate, R.S. Lutz & D.H. Rusch.
2000. A comparison of raptor densities and habitat
use in Kansas cropland and rangeland ecosystems.
J. Rapto r. R e s. 34: 203–209.
Willson, M.F. 1986. Avian frugivory and seed dispersal in
eastern North America. Curr. Ornith. 3: 223–279.
Willson, M.F. 1993. Mammals as seed-dispersal mutualists
in North America. Oikos 67: 159–176.
Willson, M.F., E.A. Porter & R. Condit. 1982. Avian fru-
givore activity in relation to forest light gaps. Carib.
J. Sci. 18: 1–6.
Willson, M.F., B.L. Rice & M. Westoby. 1990. Seed disper-
sal spectra: a comparison of temperate plant com-
munities. J. Veg. Sci . 1: 547–562.
Willson, M.F. & Travaset, A. 2000. The ecology of seed
dispersal. In Seeds: The Ecology of Regeneration in Plant
Communities. M. Fenner, Ed.: 85–110. CAB Interna-
tional. Wallingford, UK.
Willson, M.F., A. Traveset & C. Sabag. 1997. Geese as
frugivores and probable seed-dispersal mutualists. J.
Field Ornith. 68: 144–146.
Wilson, J.D., M.J. Whittingham & R.B. Bradbury. 2005.
The management of crop structure: a general ap-
proach to reversing the impacts of agricultural in-
tensiﬁcation on birds? Ibis 147: 453–463.
Wilson, J.D., A.J. Morris, B.E.Arroyo, et al. 1999. A review
of the abundance and diversity of invertebrate and
plant foods of granivorous birds in northern Europe
in relation to agricultural change. Agricul. Ecosyst. Env.
Witmer, M.C. & A.S. Cheke. 1991. The dodo and the
tambalacoque tree: an obligate mutualism reconsid-
ered. Oikos. 61: 133–137.
Wolff, J.O., T. Fox, R.R. Skillen & G.M.Wang. 1999. The
effects of supplemental perch sites on avian predation
and demography of vole populations. Can. J. Zool. 77:
Wood, B.J. & C.G. Fee. 2003. A critical review of the
development of rat control in Malaysian agriculture
since the 1960s. Crop Prot. 22: 445–461.
Wootton, J.T. 1991. Direct and indirect effects of nutrients
on intertidal community structure: variable conse-
quences of seabird guano. J. Exp. Mar. Biol. Ecol. 151:
Wootton, J.T. 1992. Indirect effects, prey susceptibility,
and habitat selection: impacts of birds on limpets
and algae. Ecology 73: 981–991.
Wootton, J.T. 1995. Effects of birds on sea urchins and
algae: a lower-intertidal trophic cascade. Ecoscience
Wootton, J.T. 1997. Estimates and tests of per capita
interaction strength: diet, abundance, and impact
of intertidally foraging birds. Ecol. Monog. 67: 45–
Wright, S.J., A. Hernandez & R. Condit. 2007. The bush-
meat harvest alters seedling banks by favoring lianas,
large seeds, and seeds dispersed by bats, birds, and
wind. Biotropica 39: 363–371.
Yates, C.J., D.J. Coates, C. Elliott & M. Byrne. 2007a.
Composition of the pollinator community, pollina-
tion and the mating system for a shrub in fragments
of species rich kwongan in south-west Western Aus-
tralia. Biodiv. Cons. 16: 1379–1395.
Yates, C.J., C. Elliott, M. Byrne, D.J. Coates & R. Fair-
man. 2007b. Seed production, germinability and
seedling growth for a bird-pollinated shrub in frag-
ments of kwongan in south-west Australia. Biol. Cons.
Zahwai, R.A. & C.K. Augspurger. 2006. Tropical for-
est restoration: tree islands as recruitment foci in
degraded lands of Honduras. Ecol. Appl. 16: 464–
Zanini, L. & G. Ganade. 2005. Restoration of Arau-
caria forest: the role of perches, pioneer vegeta-
tion, and soil fertility. Restoration Ecol. 13: 507–
Zembal, R. & J.M. Fancher. 1988. Foraging behavior and
foods of the light-footed clapper rail. Condor 90: 959–