Download Ecosystem Services Provided by Birds

Ecosystem Services Provided by Birds
Christopher J. Whelan,a Daniel G. Wenny,b
and Robert J. Marquisc
a
Illinois Natural History Survey, Midewin National Tallgrass Prairie,
Wilmington, Illinois, USA
b
Lost Mound Field Station, Illinois Natural History Survey, Savanna, Illinois, USA
c
Department 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 concentrate 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 engineers. These ecosystem services fall into two subcategories: those that arise via behavior (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 irruptive 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
Introduction
Birds are both visually and acoustically conspicuous components of ecosystems. Birds attract attention. But ecologically, do birds matter? 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:
+1-815-423-6376. [email protected]
Ann. N.Y. Acad. Sci. 1134: 25–60 (2008).
doi: 10.1196/annals.1439.003
C
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 function within numerous ecosystems. As members
of ecosystems, birds play many roles, including as predators, pollinators, scavengers, seed
dispersers, seed predators, and ecosystem engineers (Sekercioglu 2006).
“Ecosystem services” are natural processes
that benefit humans. For instance, honeybees
pollinating orchards provide a service that benefits humans through the production of apples. In contrast, native bees pollinating milkweeds provide a service for the milkweed—they
facilitate its reproduction. Both are services,
2008 New York Academy of Sciences.
25
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Annals of the New York Academy of Sciences
but only the former can reasonably be argued
to have a direct or extrinsic benefit for humans. Wallace (2007) reviews problems concerning the classification of ecosystem services. Here, we follow the United Nations
Millennium Ecosystem Assessment (2003; see
also Kremen & Ostfeld 2005), which distinguishes four principal types of ecosystem
services:
•
•
•
•
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 enrichment, cognitive development, reflection,
recreation, and aesthetics;
Supporting services, which include all
other ecosystem processes, such as soil formation, nutrient cycling, provisioning of
habitat, and production of biomass and
atmospheric oxygen.
Birds contribute all four types of services.
Provisioning services are provided by both
domesticated (poultry) and nondomesticated
species. Nondomesticated birds have been important components of human diets historically
(Moss & Bowers 2007), and many are still today (Peres 2001). In developed countries, many
are hunted for consumption and sport (Bennett & Whitten 2003). Bird feathers provide
bedding, insulation, and ornamentation. Scavengers contribute regulating services, as efficient carcass consumption helps regulate human 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 million bird watchers spent $32 billion in retail
stores, generating $85 billion in overall economic 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
the world.
In this paper, we concentrate primarily on
supporting services, and to a lesser extent, provisioning 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 subcategories: those that arise via behavior (like consumption of agricultural pests) and those that
arise via bird products (like nests and guano).
Currently, the economic value to humans contributed 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 facilitate future efforts to estimate their economic
value. A second goal is to highlight gaps in our
knowledge and point to future directions for
additional research.
Why Birds Are Unique
Characteristics of most birds make them
quite special from the perspective of ecosystem 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 irruptive or pulsed resources in ways generally not
possible for other vertebrates. Their mobility
also allows them to leave areas in which resources are no longer sufficient. Because many
species are migratory, birds link ecosystem processes and fluxes that are separated by great
distances and times. Different bird species exhibit 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 between breeding and nonbreeding phases of the
annual cycle. For many such species, breeding
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Whelan et al.: Birds and Ecosystem Services
communities are composed of individual pairs
of relatively low density owing to intraspecific (and sometimes, interspecific) territoriality. In the nonbreeding season, these species
may form heterospecific flocks that can attain
extremely high densities. Such differences in social structure can lead to very large differences
in avian impact on the environment.
Behavior-driven Services
Most of the ecosystem services we consider
here result from bird behavior, specifically, foraging behavior. Among the nearly 10,000 bird
species on the planet, we find species that consume 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.
Pest Control
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.”
Economic ornithology launched in the
United States in 1885 with a small Congressional appropriation within the USDA for “the
study of the interrelation of birds and agriculture, 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 presumed to be either beneficial or detrimental
to agriculture, including granivorous and insectivorous 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, cannot 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 pestcontrol agents receded as agriculture became
more mechanistic, large scale, and dependent
upon the rapidly growing availability of effective pesticides (see Kirk et al. 1996). Current
interest in the functional roles of birds arose
from two complementary concerns. First, debate over factors, such as food competition
and predation, as structuring mechanisms of,
ecological communities (see Amer Nat 122[5],
1983: A Round Table on Research in Ecology
and Evolutionary Biology) spurred renewed interest on impacts of birds (and other animals)
on their food resources (Rodenhouse & Holmes
1992). Second, concern over declining populations (Ambuel & Temple 1983; Robbins et al.
1989; Terborgh 1989; Askins et al. 1990) increased interest in the potential consequences
of those declines (Askins 1995; Whelan & Marquis 1995; Martin & Finch 1995; Sekercioglu
et al. 2004).
Herbivorous Insects
Quantifying the impact of bird predation
on arthropods typically involves cages that exclude 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 overwintering spiders in northern spruce forests.
Solomon et al. (1977) placed logs containing
coddling moth (Cydia pomonella) cocoons in apple orchards. They found that logs caged in
wire netting to exclude birds experienced almost 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 impact of birds on arthropods during the breeding season. They found that birds significantly
28
reduced densities of Lepidoptera larvae on forest understory vegetation. The largest impacts
coincided with nestling and fledgling periods of
the nest cycle. Joern (1986) demonstrated exclusion 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 bilberry (Vaccinium myrtillus) increased significantly
in their absence. Bock et al. (1992), however,
found that birds significantly reduced grasshopper densities in Arizona grassland, but those effects 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 arthropods 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 agricultural 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 emplacement 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%.
Annals of the New York Academy of Sciences
Owing to mobility, many bird species can respond to temporally and/or spatially disjunct
bonanzas of arthropods. An early case was reported 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 everything 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
unclear.
Nonetheless, numerical responses to high
arthropod populations are well known. Stewart
and Aldrich (1951) attempted to remove birds
from an experimental area in Maine undergoing an outbreak of the spruce budworm moth
(Choristoneura fumiferana Clem). Despite considerable effort, birds continually repopulated the
experimental area, leading the authors to conclude that a large number of nonterritorial
birds (floaters) were available in the surrounding area. Alternatively, birds may have gradually moved into this area of outbreaking budworms. MacArthur (1958) and Morse (1978)
also noted movements in response to spruce
budworm outbreaks.
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. erythropthalmus), and indigo buntings apparently
responded positively to the outbreaks, but few
other responses were observed. Similarly, Barber et al. (2008) found that gypsy moth defoliation events in eastern United States and adjacent 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
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Whelan et al.: Birds and Ecosystem Services
TABLE 1. Investigations of top-down effects
of birds on herbivorous insects by habitat
Habitat
Terrestrial
Agricultural
Perfecto et al. (2004)
Jones et al. (2005)
Philpott et al. (2004)
Hooks et al. (2003)
Mols and Visser (2002)
Greenberg et al. (2000)
Grassland
Boyer et al. (2003)
Riparian
Sipura (1999)
Bailey and Whitham (2003)
Bailey et al. (2006)
Temperate Forest
Mooney (2007)
Mooney (2006)
Mooney and Linhart (2006)
Gonzalez-Gomez et al. (2006)
Recher and Majer (2006)
Cornelissen and Stiling (2006)
Mantyla et al. (2004)
Mazia et al. (2004)
Medina and Barbosa (2002)
Lichtenberg and
Lichtenberg (2002)
Sanz (2001)
Jantti et al. (2001)
Strong et al. (2000)
Murakami and Nakano (2000)
Forkner and Hunter (2000)
Murakami (1999)
Gunnarsson and Hake (1999)
Gunnarsson (1996)
Tropical Forest
Boege and Marquis (2006)
Terborgh et al. (2006)
Van Bael and Brawn (2005)
Gruner (2004)
Van Bael et al. (2003)
Boreal
Strengbom et al. (2005)
Tanhuanpaa et al. (2001)
Bird–insect Tritop-down trophic
effects?
effects?
yes
yes
yes
yes
yes
yes
NT
NT
NT
yes
yes
NT
yes
no
yes
yes
yes
yes
(variable)
yes
yes
yes
yes
yes
yes
yes
no
yes
yes
yes
yes
yes
yes
yes
yes
NT
no
NT
variable
NT
no
yes
yes
yes
yes
yes
yes
yes
yes
yes
NT
no
yes
no
no
NT
NT
yes
yes
yes
yes
yes
yes
yes
variable
no
NT
yes
yes
NT
NT
Continued
TABLE 1. Continued
Habitat
Aquatic
Rocky intertidal
Hori and Noda (2007)
Ellis et al. (2007)
Snellen et al. (2007)
Hargrave (2006)
Wootton (1997)
Wootton (1995)
Wootton (1992)
Intertidal mudflat
Ellis et al. (2005)
Hamilton et al. (2006)
Hamilton and Nudds (2003)
Hori and Noda (2001)
Hamilton (2000)
Coleman et al. (1999)
Bird–insect
top-down
effects?
Tritrophic
effects?
yes
yes
yes
yes
yes
yes
yes
NT
likely
likely
likely
NT
yes
yes
yes
yes
yes (weak)
yes
yes
yes
yes
no
NT
NT
no
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 response 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 respond 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 woodpeckers on bark beetles (Coleoptera, Scolytidae) infecting spruce (Picea). They conclude,
based on the trifecta of empirical observation, 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 infestations that reduce bark beetle outbreaks
and contribute to regulation of bark beetle
populations. Although all Picoides woodpeckers
30
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 insects 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 dollars per year (Ayres & Lombardero 2000). Although we know of no estimate of the economic
value of woodpeckers in the budworm–forest
interaction, by regulating budworm populations 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. Wootton (1992) excluded avian predators from a
rocky intertidal community. In the absence of
avian predation, abundance of one herbivorous 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 algae via two different interaction chains (herbivory and space competition). Other studies
have found top-down effects of birds in rocky
intertidal communities and in intertidal mudflats (Table 1). Although these studies demonstrate top-down effects, as none of the species is
considered a pest, these studies do not demonstrate pest control. In sum, many investigations
in terrestrial and aquatic habitats, both natural and human-dominated, find that bird predation 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 devastating consequences. Although information
is only anecdotal, apparently the “war against
the sparrows,” part of a pest-control campaign
Annals of the New York Academy of Sciences
launched in China during Mao Zedong’s Great
Leap Forward, led to massive increases in pest
insects and, thus, crop damage, ultimately contributing to a catastrophic famine from 1958–
1962 in which 30 million Chinese died from
starvation (Becker 1996).
Rodents
In the late nineteenth century, many people 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 Mammalogy 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 important 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, although rodent-control measures (such as rodenticides and integrated pest management)
are used widely, surprisingly few studies have
assessed effects of rodents on agricultural production (Brown et al. 2007). Nonetheless, there
are examples of rodents having strong effects
in agricultural crops (Brown et al. 2007), natural 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 deployment 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
Whelan et al.: 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 number of diurnal raptors around and over the
fields, which in turn decreased mouse (Mus domesticus) population growth rate and the maximum 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 foraging in potentially beneficial ways. Clearly, provisioning 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.
2002).
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) exhibit 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 positively correlated with the percentage of Microtus 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
31
phase in the microtine population cycle (Korpimaki & 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 islands created by a hydroelectric impoundment
in Venezuela, densities of rodents, howler monkeys, iguanas, and leaf-cutter ants were 10 to
100 times greater than on the nearby mainland, 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 populations, which further suggests further the potential 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 facilitation between least weasel (Mustela nivalis) and
European kestrel, suggesting that “the assemblage 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 suggests that raptors exert strong and regulating predation on rodents under some circumstances. 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 opportunities to boost breeding populations, provisioning perches to increase or concentrate foraging activities, and elimination of persecution
(Kirkpatrick & Elder 1951; Van Maanen et al.
32
2001). These propositions are each amenable
to empirical verification or rejection, and provide numerous avenues for applied ecological
research.
Weeds
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 consumption? 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, including granivorous birds, in agricultural settings.
Small mammals and invertebrates appear to
be the most important consumers of seeds in
these ecosystems. However, Holmes and FroudWilliams (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 further investigation of the roles of granivorous
birds as potential pest control agents of weedy
plant species in cultured ecosystems. For instance, Howe and Brown (1999) found positive
density-dependent seed consumption. How frequently is avian seed consumption density dependent? Does density-dependent seed consumption vary with bird species, habitat type,
and seed species available?
Holmes and Froud-Williams (2005) suggest
that recruitment of avian granivores into integrated weed-management programs would reduce 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-
Annals of the New York Academy of Sciences
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 undergone population declines in recent decades
(U.S.: Valiela & Martinetto 2007; Europe: Donald 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.
2005).
Current research shows, unsurprisingly, that
different suites of bird species found in agroenvironments 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 predators). Lima and Valone (1991) provide a useful framework, pointing out that some species
are “cover-dependent” while others are “coverindependent.” With this framework, can we
manipulate agro-environments in ways that
provide for a diversity of granivorous birds
while maintaining vigorous agricultural production? Milsom et al. (1998) consider related
issues with respect to wading birds inhabiting
coastal grasslands in England.
In contrast to patterns found in agroecosystems, some research on granivory in natural ecosystems found relatively greater consumption of seeds by birds than by either small
mammals or by insects. These include the
Monte Desert in Argentina (Lopez De Casenave et al. 1998; Saba & Toyos 2003), miombo
woodland in Zimbabwe (Linzey & Washok
2000), and coastal steppe chaparral in northern 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
Whelan et al.: Birds and Ecosystem Services
that may enhance avian granivory in agroecosystems.
Additional research should identify the
importance of avian granivores in agroecosystems. 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 nonbreeding 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 herbivorous insects (when consuming predominantly
arthropods) in the growing season even if control of weed seeds is minimal in winter (when
consuming predominantly seeds).
Pollination
Many plants depend on pollination by animals for successful seed set. Over 920 species of
birds pollinate plants, including hummingbirds
(Trochilidae) in the Americas, sunbirds (Nectarinidae) in Africa, false-sunbirds (Philepittidae) in Madagascar, flowerpeckers (Dicaeidae)
and white-eyes (Zosteropidae) in southern Asia,
honeyeaters (Melphagidae) and lories (Loridae) in Australasia, and Hawaiian honeycreepers (Drepanididae) in Hawaii (Stiles 1981).
In southwestern Spain, three species of warblers (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 (Kremen & 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 forest and 10% in montane forests (Stiles 1985).
The majority of agricultural crops are polli-
33
nated by insects, but birds pollinate approximately 5.4% of 960 cultivated plant species
with known pollinators (Nabhan & Buchmann
1997). Among noncultivated plants, most birdpollinated species are shrubs and epiphytes, but
some tree species are bird pollinated, especially
in Australasia. The number of plant species pollinated 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 overlap and redundancy; examples of plant species
entirely dependent on only one species of pollinator are rare (Feinsinger 1983). Nevertheless, pollination mutualisms are more tightly
coevolved than those in seed dispersal (Wheelwright & Orians 1982; Johnson & Steiner
2003). Indeed much of the extensive literature on pollination is on the evolutionary aspects 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 & Manning 2006; Micheneau et al. 2006). One result of such specialization is that morphological 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 studies show that even in plants apparently specialized 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 radicans, a hummingbird-pollinated plant native to
34
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 regarding the role of birds as pollinators. A hurricane 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 persist only on small offshore islands. Many plant
species are pollen limited because of declines of
bird pollinators (Montgomery et al. 2001; Murphy & Kelly 2001). Even in areas where populations 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 includes 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 pollination does occur is by insects (Cox 1983).
The substitution of insects for birds as pollinators 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 introduced honeybee rather than declines of avian
pollinators. Consequences of this recent phenomenon 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
Annals of the New York Academy of Sciences
nectarivore species (Borgella et al. 2001), although the overall number of individual nectarivores declines with fragmentation (Sekercioglu et al. 2002). How those effects impact
pollination has rarely been studied. An agricultural 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 pollination. Aizen and Feinsinger (1994) found
no effect of fragmentation on fruit or seed set
in two hummingbird-pollinated plants in Argentina. 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 visited pasture trees (Smith-Ramirez & Armesto
2003). Similarly, bird visitation in New Zealand
was higher on forest edges than in forest interior, 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 transferred pollen among fewer plants, leading to inbreeding and lower seed set in fragments than
in intact forest (Byrne et al. 2007; Yates et al.
2007a,b).
Seed Dispersal
Seed dispersal is among the most important
ecosystem services provided by birds. Seed dispersal by birds is geographically widespread;
both the bird and plant participants are taxonomically diverse. Plants and their avian dispersers form part of a complex mutualistic
network fundamental to maintaining biodiversity and community structure (Bascompte &
Jordano 2007). Ecological and evolutionary aspects of seed dispersal have been reviewed several times (van der Pijl 1972; Howe 1986; Willson 1986; Jordano 2000; Willson & Travaset
2000; Herrera 2002). Most bird dispersal activities likely fall into the category of supporting
35
Whelan et al.: Birds and Ecosystem Services
services. When birds disperse seeds of plants of
economic significance (lumber and landscape
species, Table 2), their activities may represent
provisioning services.
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 invertebrates, many of which are ingested inadvertently. Another variation is when raptors secondarily 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 adhesion (epizoochory) to feathers or in mud adhered to the legs or bill, but virtually nothing
is known about the extent and consequences of
these interactions.
At the ecosystem level, seed dispersal is but
one stage in plant reproductive cycles, but dispersal 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 areas of high mortality (Harms et al. 2000), colonization 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 movement 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 “contagious.” Seeds are more likely to be deposited
in some places than in others as a result of disperser behavior. This pattern is known as dispersal limitation and plays a key role in recruitment 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 biodiversity (Schupp et al. 2002; Kwit et al. 2004).
The importance of seed dispersal can often be seen clearly in its absence. For example, in Tanzania, frugivorous birds are rare or
absent from small forest fragments (Cordeiro
& Howe 2003). Consequently, foraging visits to the tree Leptonychia usambarensis were
much less frequent, and seedling recruitment
in suitable sites was much lower (Cordeiro &
Howe 2003). More broadly, seedling recruitment 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, particularly among large-seeded plant species (McConkey & Drake 2002; Meehan et al. 2002).
However, as in pollination systems, total extinction 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 vertebrates 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).
Endozoochory
Birds are ideal endozoochorus seed dispersers. Frugivorous species typically swallow
fruits and seeds intact. Birds are highly mobile and many migrate long distances. Birds
occur nearly everywhere and provide mobile
links within and among habitats. In most cases
seeds cannot germinate from within an intact
fruit and an additional, and frequently overlooked, benefit of endozoochory is the removal
of fruit skin and pulp from the seeds during the
36
Annals of the New York Academy of Sciences
TABLE 2. Genera of trees, shrubs, and
lianas of North America of ornamental, timber, or other (agricultural, medicinal) economic value, in which at least one species
produces fruits or seeds dispersed by birds
TABLE 2. Continued
Family
Rhamnaceae
Genus
Ornamental Timber Other
Family
X
X
X
Juniperus
X
X
X
Ilex
X
Ceonothus
Frangula
X
X
Parthenocissus
Vitis
X
X
X
Sapindus
X
X
Rhus
X
Aralia
X
Callicarpa
X
Diervilla
Lonicera
Symphoricarpos
Viburnum
Sambucus
X
X
X
X
X
Sabal
Serenoa
X
Smilax
X
Vitaceae
Cupressaceae
Taxaceae
Ornamental Timber Other
Aquifoliaceae
Pinaceae
Pinus
Genus
Sapindaceae
Taxus
X
X
Magnoliaceae
Anacardiaceae
Magnolia
X
X
Lauraceae
Araliaceae
Persea
Sassafras
Lindera
X
X
X
Verbenaceae
X
Fagaceae
Caprifoliaceae
Fagus
Quercus
X
X
X
X
Celtis
X
X
Morus
X
Morella
X
Ulmaceae
Moraceae
X
Arecaceae
Myricaceae
X
X
Ericaceae
X
Smilacaceae
Gaultheria
Arctostaphylos
Vaccinium
Gaylussacia
X
X
X
X
Diospyros
X
Ribes
X
X
Rubus
Rosa
Prunus
Malusa
Photinia
Sorbus
Crataegus
Amelanchier
X
X
X
X
X
X
X
X
X
X
X
Shepherdia
X
Cornus
Nyssa
X
X
Celastrus
Euonymus
X
X
a
Malus refers to crabapple, not domestic apple.
X
Ebenaceae
X
X
Grossulariaceae
Rosaceae
X
X
Elaeagnaceae
Cornaceae
X
Celastraceae
Continued
interaction (Traveset & Verdu 2002; Samuels
& Levey 2005). Consequently, any bird–plant
interaction involving endozoochory potentially
benefits the plant.
With the exception of birds dispersing mistletoes (see Box 1), the interaction of most bird dispersers 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
37
Whelan et al.: Birds and Ecosystem Services
Box 1
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; Martı́nez 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 & Martı́nez 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 Australian scrubland to 89.5% in tropical rainforest, 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 & Smallwood 1982; Willson et al. 1990; Jordano 2000).
Many birds eat fruits. Some of the important
families include trogons (Trogonidae), hornbills
(Bucerotidae), toucans (Ramphastidae), cotingas (Cotingidae), manakins (Pipridae), birdsof-paradise (Paradesidae), waxwings (Bombycillidae), 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 frugivorous birds with lek breeding systems in which
the males have display perches where they
spend the majority of the day during the breeding season. Wenny and Levey (1998) showed
that display perches of three-wattled bellbirds
(Procnias tricarunculata) enhance early seedling
establishment of species they disperse. Fiftytwo 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 subsequent 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
38
forest understory site were shared with the lek
(Théry & 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 dispersal to suitable sites, they also are dispersed by
other bird species providing colonization, escape, and gene-flow benefits. This overlap and
redundancy is a key part of mutualistic networks (Bascompte & Jordano 2007). Nevertheless, 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 distances (Jordano et al. 2007; Spiegel & Nathan
2007).
Birds often exhibit nonrandom movement
following a foraging bout, resulting in differential movement of seeds. In forests, many
birds either feed in or move to forest gaps following feeding. Fruiting plants produce larger
crops in gaps (Levey 1988a,b; Levey 1990;
Martı́nez-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. Overall, 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.
2005).
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 recruitment sites for many plant species. Such “nurse
plants” shelter seedlings from heat stress. Soil
moisture levels and nutrient availability are of-
Annals of the New York Academy of Sciences
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 ecosystems are often the only perches available and
thus provide both high seed input in a nonrandom pattern and a favorable microclimate
for bird-dispersed species. Several studies report 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, especially 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 (McDonnell 1986; McClanahan & Wolfe 1993; Holl
1998; Shiels & Walker 2003; Zanini & Ganade
2005) to trees or shrubs (Robinson & Handel 1993; Robinson & Handel 2000; MartinezGarza & Howe 2003). Other foci include existing 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 survival is less clear. Seedlings of woody species
may face grazing animals, frequent fires, or
competition from thick grass cover (Duncan
39
Whelan et al.: Birds and Ecosystem Services
& Duncan 2000; Duncan & Chapman 2002).
Nevertheless, once woody species are established 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 recovery of degraded lands (Duncan 2006; Neilan
et al. 2006; Lozada et al. 2007).
Waterfowl
Although the role of waterfowl as seed dispersers was recognized decades ago (Ridley
1930), only recently has the ecology of this interaction been studied. Waterfowl (Anatidae;
∼150 species) occur worldwide, are migratory
or otherwise capable of long-distance movements, and many species are largely vegetarian.
Thus, waterfowl can be highly effective mobile
links within and among wetland habitats. Although some waterfowl act as typical frugivores
(Willson et al. 1997), more often waterfowl forage actively as herbivores or granivores. Seeds
are ingested inadvertently by herbivores, and a
few escape digestion (e.g., Janzen 1984). Interestingly, in addition to plant seeds, waterfowl
also disperse aquatic invertebrates (Figuerola &
Green 2002a,b; Charalambidou & Santamaria
2005).
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 propagules survive gut passage, and many of these
studies have used mallard ducks (Anas platyrhynchos) as subjects (Charalambidou & Santamaria
2002). Shorebirds (Charadriidae, Scolopacidae) 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 organisms (Santamaria 2002), long-distance dispersal (20–1000 km) must occur, but its frequency relative to local dispersal is unknown
(Clausen et al. 2002). At a waterfowl migra-
tory stopover and wintering site in southwestern Spain, over 65% of nearly 400 fecal samples contained seeds and aquatic invertebrates,
suggesting the widespread occurrence of dispersal during migration (Figuerola et al. 2003).
Waterfowl also play a role in upstream dispersal 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. Further, in addition to waterfowl and some shorebirds, 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 unknown. Although this transport appears inadvertent or accidental, it need not be so. Investigation of this interaction could use the study of
hummingbird transport of mites (e.g., Colwell
1986) as a model.
Seed-caching
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 western North America and across Eurasia and
are distinguished from the primarily winddispersed species by having large seeds that
lack a well-developed winged appendage for
wind dispersal and cones that require seed removal 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 surface 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
40
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 retrieve all caches every year (Lanner 1996). Most
seeds that are not taken by birds and fall beneath adult Pinus monophylla trees are harvested
by rodents that are less effective dispersers than
corvids because they larder-hoard seeds in burrows (Vander Wall 1997). Most of the corviddispersed pine species are found in xeric habitats, where burial protects seeds from desiccation (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 (Fagaceae) by scatterhoarding. Although the presumed mutual adaptations in these species are
less clear than for nutcrackers and pines, many
seeds are cached in suitable sites for germination and establishment (Darley-Hill & Johnson
1981; Johnson & Adkisson 1985; Johnson et al.
1997; Pons & Pausas 2007). Dispersal by jays
likely aided the rapid post-Pleistocene northward spread of oaks and other species (Johnson & 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
further study.
Adhesion
Seed dispersal by adhesion to birds is much
less frequent than by mammals and has received 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 carried seeds or invertebrate eggs. Up to 12 species
were found on an individual, with 22 species
overall. Plant seeds were more commonly attached to feathers, and invertebrate eggs were
Annals of the New York Academy of Sciences
more common in mud on feet (Figuerola &
Green 2002a,b). Dispersal by adhesion was a
major source of the Hawaiian flora, and the diversity 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 islands. 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 dispersal. Effective dispersal then depends on adhesion to birds that do not become entangled
in plant parts (Burger 2005).
Scavenging
Animals die, and when they do, their carcasses become available to scavengers. Scavengers here refer to microbes, invertebrates,
and vertebrates. Among the birds, the New
World (Ciconiiformes) and Old World (Falconiformes) vultures are essentially obligate scavengers, but many bird species in many orders
are known to scavenge facultatively or opportunistically (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 vertebrates. In contrast to early human perceptions
of birds of prey (predatory Falconiformes), vultures 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 belief 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
Whelan et al.: Birds and Ecosystem Services
soaring flight. Their models predict that soaring
flight and large size (allowing infrequent feeding and maintenance on body reserves) give
birds a competitive advantage over terrestrial
mammals, and thus, even precluded the evolution of obligate scavenging in the mammals.
On the other hand, obligate avian scavengers
have lost the agility needed to kill prey. Mammals and facultative avian scavengers have retained the ability to flexibly kill their own prey
and scavenge carrion, but neither can live exclusively on carrion. Shivik (2006) developed
empirically based models of competition between microscavengers and macroscavengers
and concluded that evolution of macroscavengers will favor traits, such as flight, that
maximize rapid carrion detection. These two
modeling approaches, though quite different
conceptually, both conclude that obligate vertebrate scavengers are most likely to be large
birds.
Numerous sources of mortality cause nonpredatory death. Historically, these would have
included natural death due to old age, malnutrition, disease, parasites, accidents, exposure, 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, poisoning, and pollution (e.g., oil spills). In the
absence of carcass removal or consumption by
scavengers, the extent of nonpredatory mortality (and the accumulation of carcasses that
would accrue), may be surprising. For example,
Houston (1979) estimated that most large ungulate 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 collisions with glass alone (Klem 1990 & Dunn
1993; both in Klem et al. 2004). Clearly, in
the absence of consumption (whoever the consumer), such deaths would quickly accumulate.
Studies quantifying carcass removal by scavengers indicate rapid removal or consumption
41
(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 secondary consumption of the pharmaceutical diclofenac in south Asia (Oaks et al. 2004) underscore the vital services performed by these
scavengers. Following the collapse of populations 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 decline 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 animals into grasslands (Carlsson et al. 2006). The
poisoning of vultures feeding on carcasses in
south Asia points to yet another potent pathway. 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.
42
1991); rails, Rallidae (Zembal & Fancher 1988);
skuas, Stercorariidae (Norman et al. 1994); willet and turnstone, Scolopacidae; gulls, Laridae; plovers, Charadriidae (Gochfeld & Burger
1980); raptors, Accipitridae (Selva et al.2003,
2005; Selva & Fortuna 2007); woodpeckers, Picidae (Servin et al. 2001); and passerines, such
as crows, Corvidae, and tits, Paridae (Selva
& Fortuna 2007). Unlike vultures, whose digestive systems may destroy ingested bacteria
and viruses (Houston & Cooper 1975) or possess a gut microflora that may confer resistance to pathogenic microorganisms and their
toxins (Carvalho et al. 2003), these facultative scavengers appear frequently to harbor
such pathogens (Blanco et al. 2006). Unsurprisingly, vultures also appear to possess elevated
immunocompetence against many pathogens
widely encountered in carcasses (Ohishi et al.
1979; Apanius et al. 1983; Pérez de la Lastra 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 landfills are located near airports, collisions with
aircraft are common (Baxter & Allen 2006).
Opportunistic scavenging among birds
reaches its zenith with marine birds that associate with commercial fisheries, feeding on
discards and offal. Large quantities of unwanted fish and invertebrate by-catch are discarded overboard, providing a rich food source
for ship-following birds. These are typically
large seabirds, including albatross, gulls, and
skua (Furness 2003; González-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; González-Zevallos &
Yorio 2006). Although we know of no identifi-
Annals of the New York Academy of Sciences
able ecosystem service resulting from scavenging 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 nutrients (e.g., Payne & Moore 2006) and contaminants (e.g., mercury; Monteiro & Furness 1995;
Furness & Camphuysen 1997). Reducing discard 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). Decreasing discard rates may affect not only scavenging species themselves, but entire seabird communities (e.g., Furness 2003; Votier et al. 2004,
2007), as large scavenger species switch to preying on smaller species (but see Oro & Martı́nezAbraı́n 2007).
Further research is needed on the ecological (e.g., predation on nearby nests; Husby
2006) and epidemiological consequences of
large numbers of facultative scavengers feeding 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 availability to and/or use by generalist and facultative scavengers via integrated bird management
strategies that may employ avian predators, distress calls, blank shot, pyrotechnics, gas cannons, and other techniques (Baxter & Allen
2006).
Additional research should address the ecological conditions that favor macro- versus microscavengers. For instance, are there certain
areas or conditions in which macroscavengers,
particularly the obligate avian scavengers, are
rare or absent? J.S. Brown (personal communication) suggests that avian scavengers may
be totally absent from the island of New
Guinea, possibly because environmental conditions (constant high humidity and warm temperature) 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
43
Whelan et al.: Birds and Ecosystem Services
Central and South America and West Central
Africa? Such studies would elucidate the situations in which avian scavengers are relatively
more (and relatively less) important contributors of these ecosystem services.
Feeding Opportunities
Honeyguides (Indicator indicator Sparrman), as
their name implies, guide humans to trees housing bee nests (Isack & Reyer 1989). Humans, in
the process of harvesting the honey for themselves, make this rich resource available to the
birds. The symbiosis between honeyguides and
the Boran people of northern Kenya was studied by Isack and Reyer (1989) over a 3-year period. 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 gatherers conservatively increase their hunting efficiency approximately threefold. We know of
no other example of similar services provided
by birds for humans.
A variety of bird species engage in an interaction known as “beaters and followers.”
The beater species “stirs” a substrate, which
in turn enhances prey availability for the follower species. Various bird species interact this
way, including waders, Ardeidae; kites, Accipitridae; kingfishers, Alcedinidae; woodpeckers, Picidae; grackles, Icteridae; and drongos,
Dicruridae (Meyerriecks & Nellis 1967; Bennets & 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) followers of army ant (Eciton burchelli, Hymenoptera)
swarms are themselves followed by females
of three species of Ithomiinae (Lepidoptera:
Nymphalidae; Ray & Andrews 1980). The female butterflies feed upon the droppings of the
antbirds, possibly as a predictable resource necessary for prolonged egg production.
Product-driven Services
Many bird species modify their environment 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.
Nests
Many bird species construct nests, which display 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
domed nests.
In at least one case, bird nests contribute provisioning services. Some species of cave swifts
(Apodidae) are renowned for their edible nests
(Gausett 2004), which are constructed predominantly from their saliva. These nests are produced by a number of cave-dwelling species
from the Malaysian and Indonesian region: primarily the white-nest swiftlet (Aerodramus fuciphagus) and the black-nest swiftlet (Aerodramus
maximus). The nests have a long history of human exploitation. The nests were used medicinally 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 online retailer who today (12 October 2007) sells
grade AAA “swallow nest” at $725.00 (US)
44
for 303 g (approximately equivalent to $2400
per kilogram). Hong Kong and North America constitute the world’s two largest importers,
with estimated annual harvest of 17–20 million nests (approximately 2 metric tons; Marcone 2005). Harvest is of sufficient magnitude
to cause conservation concern for the swiftlet species whose nests are harvested (Gausset
2004). Swiftlet husbandry may be one method
of alleviating the stress placed on natural swiftlet populations from nest harvest.
Woodpeckers (Picidae) are the most familiar
group of cavity-excavating birds. Woodpeckers
are found on all continents except Antarctica, wherever forest, woodland, or other
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) excavate nesting cavities in arboreal termitaria
(Valdivia-Hoeflich & Vega-Rivera 2005). After
abandonment, these cavities are colonized
by secondary users, including various mammals 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
2003).
Burrows are excavated by many taxa of
birds, including penguins (Sphenisciformes),
various seabirds (Procellariiformes, Charadriiformes), parrots (Psittaciformes), owls (Strigiformes), kingfishers (Coraciiformes), and songbirds (Passeriformes). These burrows alter soil
properties (see below) and, in some cases,
Annals of the New York Academy of Sciences
provide homes for numerous other organisms.
Burrow excavators provide roughly analogous
supporting ecosystem services as the woodpeckers. For instance, Casas-Crivillé and Valera
(2005) found at least 19 vertebrate species
(12 birds, 2 snakes, 4 mammals, and 1 amphibian) using burrows excavated by the European bee-eater (Merops apiaster). Markwell
(1997) and Newman (1987) report on the
use of burrows dug by fairy prions (Pachyptila turtur) by the endangered tuatara (Sphenodon
punctatus).
Wandering albatrosses (Diomedea exulans),
which nest on oceanic islands of the Southern
Ocean, build elevated nests upon which they incubate 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 environment 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 sometimes taken over by small mammals after the
original occupants finish nesting and subsequently 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 overwintering spiders exhibit preferences for complex 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 (personal 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),
Whelan et al.: Birds and Ecosystem Services
which build domed nests generally located on
the ground.
Nutrient Dynamics
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 different 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 likewise attain very high densities. Large aggregations 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, accumulates 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 (Wilkinson 1984; Skaggs 1994). The United States
passed the Guano Islands Act of 1856, allowing 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 withdrawal in 1866. The “Guano Wars” or the
War of the Pacific, waged by Chile against joint
forces of Peru and Bolivia from 1879–1883, resulted in annexation of the Peruvian province of
45
Tarapacá 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). Annual 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
N 2 available as ammonia, were invented the
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 (Gillham 1956; Bosman et al. 1986), coastal marine communities (Wooton 1991; Pfister et al.
2007), wildlife refuges (Kitchell et al. 1999),
terrestrial marine ecosystems (Sánchez-Piñero
& Polis 2000), and isolated urban forest fragments (Fujita & Koike 2007). Importation
of nutrients has both direct effects, favoring
some primary producers over others, and indirect effects, as bottom-up forces cascade to
primary consumers (Wootton 1991) and detritivores (Sánchez-Piñero & Polis 2000). Burrowing seabirds also affect soil nutrient characteristics (Bancroft et al. 2004; Fukami et al. 2006)
through nutrient addition (via guano) and bioperturbation (disturbance and soil turnover) and
can be major ecosystem drivers (Fukami et al.
2006).
Birds can also figure importantly in reciprocal 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
46
Annals of the New York Academy of Sciences
ways contrary to theoretical expectation. For
instance, Polis et al. (1997) predicted that allochthonous prey inputs should result in negative 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 increased. 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 regarding such aquatic–terrestrial reciprocal energy flows (Baxter et al. 2005). For instance, is
this sort of reciprocal flow restricted to aquatic–
terrestrial systems, or could it also occur in different types of adjacent terrestrial habitats, such
as grassland–forest, or, say, forest–agricultural
field? Do such reciprocal flows between adjacent, heterogeneous habitats vary with climate
or with latitude?
Feeding Opportunities
Although we typically think of hummingbirds feeding on flower nectar, some hummingbirds feed and even defend sap trees of
woodpeckers or sapsuckers. Sapsuckers and
woodpeckers, in their foraging activities, produce wells of sap. These wells provide rich resources, and other species use them. Species
like hummingbirds acquire both sap (a source
of carbohydrate) and insects (a source of protein), which are attracted to the wells. Examples include the ruby-throated hummingbird (Archilochus colubris) and the yellow-bellied
sapsucker (Sphyrapicus varius) in eastern North
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). Although many other species, including passerines, insects, and mammals, are known to feed
at sap wells created by sapsuckers (Kilham
1953; Foster & Tate 1966), only hummingbirds appear to have strong dependencies on
them.
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:
Turner et al. (2003), Barbier (2007), Boyd
(2007), Croitoru (2007), Kroeger and Casey
(2007), and references therein. Important considerations include the temporal and spatial
scale over which any potential service is generated (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 intrinsic variability inherent in the production of the
ecosystem service. Ecosystem processes naturally vary over time. Understanding natural
variability is critical to the proper accounting of
any ecosystem service (Millennium Ecosystem
Assessment 2003).
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 insects and as seed dispersers, respectively, than
we know about birds as pollinators. Additional
research regarding which plant species are pollinated by which bird species, and the effectiveness 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
47
Whelan et al.: Birds and Ecosystem Services
follower species provide a return service, perhaps 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 determine their relative demographic impacts as
pollinators, seed dispersers, and seed predators,
and so on. Rarely if ever do we know the demographic contribution of birds for any one of
these roles, let alone their synergistic (or antagonistic) effects. Cost–benefit analysis could
be applied when alternative ecosystem “components” might be available (use of pesticides
versus encouragement of bird predation).
As this review indicates, experimental exclusion of birds is a powerful tool for assessing ecosystem function. However, these experiments are not always feasible, and an inherent
problem of interpretation is how best to extrapolate 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 epizootics like that of West Nile Virus (e.g., Caffrey
2005). Such declines may allow efficient detection of a concomitant decline of important bird
services.
Acknowledgments
We thank the editors for the invitation to
contribute this review. Cagan Sekercioglu reviewed the manuscript and offered many useful
suggestions.
Conflicts of Interest
The authors declare no conflicts of interest.
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