Why is the World Green?:

The Role of Large Terrestrial Carnivores in Ecosystem Functioning

Robert GilsonPractical Research Methods

Spring 2011

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Why is the World Green?:

The Role of Large Terrestrial Carnivores in Ecosystem Functioning

Introduction

The world we inhabit is composed of many complex systems with even more finely

interwoven relationships within those systems. If one delves deeply enough into this fascinating

place called Earth, one can see powerful connections between seemingly unrelated objects. It is

the intention of this essay to explore some of those unseen connections through a brief look into

the history of top-down regulation research leading to an examination of the important role large

terrestrial predators play in maintaining overall healthy ecosystems. With the exception of

Terborgh, Feeley, Silman, Nuñez, and Balukjian (2006) all of the studies cited within this essay

will pertain to ecosystems of North America. The United States government, after many years of

predator removal, has started to recognize the importance of apex predators, as is illustrated by

the reintroduction of the Gray wolf (Canis lupus) in Yellowstone National Park, The Mexican

wolf (Canis lupus baileyi) in Arizona and New Mexico, and the Red wolf (Canis rufus) in North

Carolina (Parker and Phillips 1991). Despite this slow recognition of the significant role of large

carnivores in ecosystem functioning a more complete understanding will be essential in future

conservation efforts the world over.

Such was the case for ecologist Charles Elton, one of the two ecologists credited with the

development of modern animal ecology (Smith and Smith, 2006), with the “intertwined,

crisscrossing, and connecting” (Stolzenburg, 2008, p. 12) chains of his food cycle. Elton came to

recognize that certain organisms were inherently connected to other organisms based on the

relationship between producers and consumers. His food cycle was based on a large foundation

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of plants and photosynthetic plankton. From the large green base the cycle continues, upward

and increasingly narrowing, moving to herbivorous animals, and then on to smaller predators,

and finally to the smallest group of them all: the apex predator (Stolzenburg, 2008). This idea

soon emerged as one of the “tenants of Ecology” (Stolzenburg, 2008, p. 12) and would later be

referred to in the literature as the Eltonian pyramid.

Elton published his famed text Animal Ecology in 1927, in which he explained his

pyramidal approach to the food chain, where each trophic level was limited by the level it rested

upon. In the 1960s the focus of the Eltonian pyramid shifted from a bottom-up perspective to a

top-down perspective. Terborgh, Holt, and Estes explained that “bottom-up processes determine

the flow of resources into the system, whereas top-down processes influence how the resources

are distributed among trophic levels” (2010, p.4). The scientific community of the 1960s began

to view the traditional Eltonian pyramid from both directions with some surprising results: the

top level of the pyramid, where all of the large carnivores rest, seemed to exhibit an

unexplainable power, despite its relatively small size compared to the bottom trophic level, over

the processes that govern ecosystem dynamics. It is the intention of this essay to provide a brief

synopsis of the history of top-down regulation research and to explore the importance of large

terrestrial predators in maintaining overall healthy ecosystems. With the exception of Terborgh

(2006) all of the studies cited will pertain to ecosystems of North America. The United States

government, after many years of predator removal, has started to recognize the importance of

apex predators, as is illustrated by the reintroduction of the Gray wolf (Canis lupus) in

Yellowstone National Park, The Mexican wolf (Canis lupus baileyi) in Arizona and New

Mexico, and the Red wolf (Canis rufus) in North Carolina (Parker and Phillips 1991). Despite

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this slow recognition of the significant role of large carnivores in ecosystem functioning a more

complete understanding will be essential in future conservation efforts the world over.

The green world hypothesis proposed by Nelson G. Hairston, Frederick E. Smith, and

Lawrence B. Slobodkin in their article published in The American Naturalist entitled

“Community structure, population control, and competition,” suggested proposed the notion that

the world remained green because of the limits placed upon herbivores by their predators and

that herbivores have evolved multiple characteristics that allow them to coexist without

competing for the same food source (1960). For example, grazers feed on leafy material;

browsers consume woody material; frugivores eat fruit; and granivores feed on seed (Smith and

Smith, 2006). Some authors dispute this claim, contending that much of the world is green due

to the varying complexity and edibility of plants, (Polis and Strong, 1996; Polis, 1999)

diminishing the role of the predator. Polis, Sears, Huxel, Strong, and Maron also argue that

herbivores can limit themselves through inter- and intra- specific competition (2000). The

science since Hairston et al. published their paper does support Polis’s premise that herbivores

can restrict their growth through inter- and intra- specific competition. However, the science has

also progressed regarding the importance of the apex predator’s role in shaping ecosystems. The

hypothesis proposed by Hairston et al.SS was based largely on assumptions (Ehrlich and Birch,

1967) rather than proof, sparking thean impassioned debate amongst ecologists of the 1960s that

continues to this day.

The Big Three

The debate over top-down versus bottom-up regulation spawned by Hairston et al.SS’s

paper raised many questions about the role of the predator in its environment. Answers to these

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questions started to emerge with the 1966 publication of Robert T. Paine’s American Naturalist

article “Food Web Complexity and Species Diversity”. Paine’s article finally provided some

empirical data on the role of an apex predator. Paine stated, “Local species diversity is directly

related to the efficiency with which predators prevent the monopolization of the major

environmental requisites by one species” (1966, p. 73). In 1963 Paine visited Mukkaw Bay on

the Olympic Peninsula in Washington where he set about testing his hypothesis in one of two

tidal pools. His experiment was quite simple: he used one tidal pool as a control and the other as

an experimental pool from which he removed the top predator, a large orange and purple starfish

(Pisaster ochraceous). Over the period of a year he physically removed Pisaster from his

experimental pool and documented the results of diversity in that pool compared to the control.

The results were staggering: out of the fifteen species present at the beginning of the experiment

seven were missing (Paine, 1966). Out of the eight remaining species, the California mussel

(Mytilus californianus) was the only one increasing in population (Paine, 1966). In the absence

of Pisaster it seemed that Mytilus was taking over at the expense of the rest of the species that

normally inhabited the tidal pool. Paine coined the term “keystone species” to describe Pisaster

as the “keystone of the community’s structure and the integrity of the community, and its

unaltered persistence through time, that is, stability, are determined by their activities and

abundances” (Paine, 1969, p. 92).

Paine’s discovery provided more questions than answers. How commonplace was the

keystone predator? Are there some predators that matter more than others? As Stolzenburg

noteds, it is around this time that a “new generation of ecologists” (2008, p. 26) emergedis up

and coming, and to these young ecologists “Paine’s predator-free rock was writing on the wall”

(Stolzenburg, 2008, p. 26).

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One of those up and comers rising ecologists was the young James Estes. In 1970 Estes

traveled to the island of Amchitka in the Aleutians to take up a new post studying the Sea Otters

(Enhydra lutris) of the area and went about his assignments without any clear sense of direction

or purpose. This all changed; however, when in 1971 he had a chance meeting with Robert

Paine and finally gained some insight into the relevance of what he was studying (Stolzenburg,

2008). With Paine’s inspiration behind him, a single question soon emerged: Does “predation on

sea urchins by sea otters…affect vegetation associations, and consequently the dynamics of the

entire nearshore community[?]” (Estes, Smith, and Palmisano, 1978, p. 823). Estes had the

opportunity to conduct a study within the “natural laboratory” of the Aleutians on a potential

keystone predator, Enhydra lutris, the sea otter. Immediately, Estes set about conducting

exacting surveys of islands that supported communities of sea otters and those that did not (Estes

et al. 1978) and an unmistakable pattern was revealed:

On otter patrolled reefs…there were forests of brown kelp, with fish swimming

among the rising fronds, and a colorful diversity of sponges and hydrocorals,

muscles, and barnacles populating the sea floor. In the otterless reef… the

seafloor had been reduced to a pavement of pink coralline algae, pocked with

spiny green blobs of enormous sea urchins (Stolzenburg, 2008, p. 61).

In this marine near-shore community the sea otter is the keystone predator controlling the

population of sea urchins, thereby allowing the kelp forest to flourish.

Top-down regulation of ecosystems was an idea that was gaining traction, and the

scientific community was finding prime examples of how keystone predators, or the lack thereof,

affect those ecosystems. In 1993 famed ecologist, John Terborgh, found himself in Lago Guri,

Venezuela anxious to explore the islands that had arisen after the flooding of a hydroelectric

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impoundment behind the Raul Leoni Dam. The islands came in all sizes, creating the perfect

outdoor laboratory to determine if the removal of predators from these islands would inexorably

lead to an increase in herbivore density, thereby ultimately affecting the biomass of the island

(Terborgh et al., 2006). Terborgh and his team documented the destruction of vegetation by the

herbivores of the small islands and the takeover by the infamous leaf-cutter ant (of the Family

Atta). The leaf-cutter populations swelled, and, as a result, the vegetation suffered immensely,

reaching the point where it could not recover fast enough from the intense grazing. This all

resulted in what the researchers of Lago Guri named as the post-Atta stage of the islands. This

post-Atta stage is described by Terborgh and his co-authors in this telling statement:

The forest canopy dies without replacement, light is appropriated by herbivore-

resistant lianas that clamber up the well-lit margins of openings until they overtop

the canopy, eventually smothering it and hastening tree mortality. The end point

of this process is a nearly treeless island buried under an impenetrable tangle of

liana stems (Terborgh et al., 2006, p. 261).

After more than a decade of research in the islands of Lago Guri it became evident to Terborgh

that in the absence of predators a terrestrial “trophic cascade,” another term coined by Robert

Paine, was undoubtedly apparent. Berger et al. have defined a trophic cascade as “predator-

related effects that result in inverse patterns of abundance or biomass across multiple trophic

levels in a food web” (2001, p.818) or as Paine, himself, later defines as the “dynamic process

unleashed whenever numbers of apex predators are decreased by exploitation, increased through

restoration, or experimentally manipulated” (2010, p.21). Simply stated, a change in the

uppermost trophic level will eventually cascade to the lowermost level in the food web. With the

revelation of these trophic cascades, the theories proposed by Hairston et al. seem all the more

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plausible. Although, the skeptics still contend that remain, largely due to scaling issues or

the lack of scientific rigor in the experimental designs of studies concerning top-down regulation

produce questionable results (Polis et al., 2000; Schmitz,, Hambäck, and Beckerman, 2000).

Creating the proper experimental settings to appropriately study large terrestrial carnivores, their

prey, and how those predator-prey interactions affect their respective ecosystems is an almost

impossible task (Terborgh and Estes, 2010). For this reason studies in this field rely on natural

laboratories, e.g.- the Lago Guri impoundment.

Missing Wolves Spells Trouble for Plants

With this brief history of three seminal studies dealing with top-down regulation of

ecosystems in mind let us narrow our focus to concentrate on the large terrestrial predators of

North America and the role they play in shaping their respective ecosystems. Large predators,

such as the wolf or cougar (Puma concolor), The large and important predators of the continent

have been relegated to small and often isolated areas of the continent. The local extirpation of

these carnivores from the vast majority of the contiguous United States has lead toleaving

irrupting herbivore populations running free without their natural checks. Many people might

consider a large herd of deer grazing in a lush meadow a wonderful sight, but to the trained

ecologist the same scene might evoke images of a degraded landscape characterized by

decreased biodiversity and reduced tree recruitment, the survival rate of seedlings that grow

above the browse line to be counted among the population of mature trees.

William Ripple and Robert Beschta ventured to Yellowstone National Park initially to

study the hydrology and lack riparian plant species recruitment in the Lamar Valley. The results

of their study produced an unlikely culprit, the Gray wolf, for the dismal state of the riparian

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vegetation (Ripple & Beschta, 2003). Further research in the valley revealed an increased

growth of woody plant species (Populus spp. and Salix spp.) after the return of the wolf from its

seventy year absence (2003). It should be acknowledged that past studies have raised doubts of a

predator’s indirect effects on plant biomass or reproductive outputs (Polis et al., 2000; Schmitz et

al., 2000). However, Ripple and Beschta’s work clearly document a reduction in biomass

following a lack of recruitment due to heavy browsing pressure in the absence of wolves (2003,

2004). They sum up their work in Yellowstone National Park with a concise statement:

the extirpation of the gray wolf [in the northern range of Yellowstone National

Park] is most likely the overriding cause of the precipitous decline and cessation

in the recruitment of aspen, cottonwood, and willow” (Ripple and Beschta, 2004,

p. 764).

In Zion National Park there are similar patterns of low recruitment of Cottonwoods (Populus

fremontii), high numbers of Mule Deer (Odocoileus hemionus), extreme river bank erosion, and

an almost nonexistent top predator (Ripple and Beschta, 2006). Beschta and Ripple discovered

the same pattern repeated over and over again of “eradications of apex predators, dying trees,

ecosystems sliding toward duller, less stable planes of simplicity” (Stolzenburg, 2008, p. 167) in

parks in the United States such as Olympic National Park, Yosemite National Park, Wind Cave

National Park, as well as Jasper National Park in Canada (2009).

Bow Valley in Banff National Park, Canada provided another setting for a natural

experiment to test a wolf driven trophic cascade. Wolves recolonized the valley in 1986 after

local extirpation in the early 1900’s. Banff town site is located in the middle of the park in the

Bow Valley creating a high human density area with low wolf usage and, conversely, the area

surrounding the town site has low human density and high wolf use. This scenario allowed

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Hebblewhite, White, Nietvelt, McKenzie, Hurd, Fryxell, and Paquet et al. to measure and

compare wolf densities, elk (Cervus canadensis) densities, recruitment, and browse intensity

(2005). Despite a few limitations of such a natural experiment (e.g., human mediated exclusion

of predators besides the wolf such as grizzly bears, Ursus arctos) the results were not surprising:

low wolf population leading to higher densities of elk leading to lower recruitment of woody

plants, and reduced beaver and songbird numbers (Hebblewhite et al., 2005).

In North America the forests in the east, for example, are being overrun with deer (Ripple

and Beschta, 2005) threatening forest plant diversity (Côté, 2004) and even the extirpation of

some plant species (Rooney and Dress, 1997). Irruptions of deer due to the removal of wolves

and cougars have been documented as far back as 1880 in Maine, 1885 in the Adirondacks, and

the early 1900s in New York, Pennsylvania, Michigan, and Wisconsin (Leopold, Sowls, and

Spencer, et al., 1947). Leopold et al. compared deer irruptions in the United States (predator

free areas) with sites in both Canada and Mexico with intact carnivore guilds and came to the

conclusion that “over-control of these predators is a predisposing cause” (1947, p.176) of the

documented irruptions. The effects of an absent guild of top predators is still being felt today in

the simplification of old growth forests of northwestern Pennsylvania as Rooney and Dress

report a seventy percent reduction in herbaceous plant species diversity over a sixty-five year

period (1997) attributable to the over-browsing of unchecked populations of White-tailed deer

(Odocoileus virginianus).

In the west the story is the same: The islands of Haida Gwaii, British Columbia, Canada

provided another opportunity for a large-scale natural experiment, as Black-tailed deer

(Odocoileus hemionus) have been introduced to only a portion of the archipelago, leaving some

islands free of unchecked deer browsing. Allombert, Stockton, and Martin et al. noted a ninety

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percent reduction of ground-dwelling invertebrate species and a diminished bird population on

the islands populated by deer in Haida Gwaii as compared to those where no deer wereare found

(2005), while Stockton et al, Allombert, Gaston, and Martin. documented a marked reduction in

herbaceous plants and an overall loss of plant diversity (twenty to fifty percent) on islands

inhabited by deer (2005). Nonetheless, Greenwald, Petit, and Waite et al. noted the inverse at

their study plot in Cuyahoga Valley National Park, Ohio, USA where an increase in herpetofauna

and invertebrate species within control plots grazed by deer compared to exclosure plots was

observed over the two year study period (2008). Greenwald et al. did, however, acknowledge

potential biases (e.g., the refuge effect) that may have skewed the documented results (2008).

Granted Greenwald et al. reported an indirect positive effect of grazing on invertebrate and

herpetofauna density; however, their results seem to be the exception rather than the rule

(Terborgh and Estes, 2010). In predator-free areas, the continent over, populations of wild

ungulates have used the forests as a free buffet. This behavior has simplified our forests,

reducing biodiversity.

William Ripple and Robert Beschta ventured to Yellowstone National Park initially to study the

hydrology and lack riparian plant species recruitment in the Lamar Valley. The results of their

study produced an unlikely culprit, the Gray wolf, for the dismal state of the riparian vegetation

(Ripple & Beschta 2003). Further research in the valley revealed an increased growth of woody

plant species (Populus spp. and Salix spp.) after the return of the wolf from its seventy year

absence (2003). It should be acknowledged that past studies have raised doubts of a predator’s

indirect effects on plant biomass or reproductive outputs (Polis et al. 2000, Schmitz et al. 2000).

However, Ripple and Beschta’s work clearly document a reduction in biomass following a lack

12

of recruitment due to heavy browsing pressure in the absence of wolves (2003, 2004). They sum

up their work in Yellowstone National Park with a concise statement:

the extirpation of the gray wolf [in the northern range of Yellowstone National Park] is most

likely the overriding cause of the precipitous decline and cessation in the recruitment of aspen,

cottonwood, and willow” (Ripple and Beschta 2004, p. 764).

In Zion National Park there are similar patterns of low recruitment of Cottonwoods (Populus

fremontii), high numbers of Mule Deer (Odocoileus hemionus), extreme river bank erosion, and

an almost nonexistent top predator (Ripple and Beschta, 2006). Beschta and Ripple discovered

the same pattern repeated over and over again of “eradications of apex predators, dying trees,

ecosystems sliding toward duller, less stable planes of simplicity” (Stolzenburg 2008, p. 167) in

parks in the United States such as Olympic National Park, Yosemite National Park, Wind Cave

National Park, as well as Jasper National Park in Canada (2009).

The Power of Fear

It is obvious at this point that large terrestrial predators provide an indirect positive effect

towards overall plant recruitment as well as the overall stability of an ecosystem, but is this

accomplished through mere predation alone? In a 2010 article “The Ecology of Fear” Brown

suggests that non-lethal effects of predation may exert more pressure on herbivores that lethal

effects alone. Prey species are forced to choose between sustenance or security (Fortin, Beyer,

Boyce, Smith, Duchesne, and Mao, 2005; Brown, 2010) and time spent browsing is reduced

when the threat of predation is increased (Brown, 2010; Eisenberg, 2010). The effects of this

can be seen in areas characterized by an increased predation risk, such as some riparian habitats

in Yellowstone National Park. Ripple and Beschta (Brown or Berger) documented increased

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willow recruitment along previously denuded river banks in areas where vision is limited,

suggesting minimal foraging in high risk areas ( ).

Fortin et al. also documented a change in habitat preference associated with predation

risk (2005) implying, as Berger pointeds out, variations of spatial and temporal foraging patterns

(2010). An example of this fear-mediated behavior is illustrated in Yellowstone National Park

through a measure of aspen recruitment, elk density, and the presence or absence of wolves.

Fortin et al. cited figures of increased elk numbers (approximately 2-3 times greater) as well as a

notable rise in aspen recruitment at the turn of the century as compared to the time period

between 1930 and 1968 (2005). This may seem somewhat counterintuitive: shouldn’t an

increase in elk numbers result in a decrease in aspen recruitment due to increased browsing

pressure? Well, no. According to Fortin et al., the reintroduction of the wolf into the park in the

mid-1990s spawned a trophic cascade that was behaviorally mediated (2005). Wolves have

changed the dynamics of the Greater Yellowstone ecosystem through a modification of habitat

use by elk and seemed to have an overall positive indirect effect on the biomass of the park. As

a cautionary, however, it is important to take into consideration that an increase in biomass in

one area of the park may not correspond to an increase within the entire ecosystem. Fortin et al.

pointed out that decreased foraging in one aspen stand may translate to an increase of foraging in

another (2005). Clearly this is an area that requires further study.

Conclusion

The facts are simple, apex predators are important to the overall health of the ecosystem

in which they inhabit. The research, up to this point, clearly identifies terrestrial trophic cascades

throughout North America caused by the absence or removal of an apex predator (Allombert et

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al. 2005 Hebblewhite et al. 2005 Stockton et al. 2005 Ripple and Beschta 2009). Predators not

only help keep the world green, as H hypothesized half a century ago, but they help stabilize

ecosystems and maintain diversity. The view that top-down regulation of ecosystems works in

concert with bottom-up forces is fast becoming less the exception and more the

rule.Unfortunately, as the body of literature supporting the need for large terrestrial carnivores

builds support in the scientific community, a vilification of these animals still exists among some

segments of our population. Ranchers see wolves as a threat to their livestock and hunters see

them as competition for elk. Recently, a measure to remove all federal protection for the wolves

in Montana and Idaho was attached, and approved, to a federal budget bill. This is the first time

in the history of the Endangered Species Act that any animal has been delisted by an act of

congress rather than a scientific review. It appears that fear-mediated behavior is not solely

reserved for elk.

The facts are simple, apex predators are important to the overall health of the ecosystem

in which they inhabit. The research, up to this point, clearly identifies terrestrial trophic cascades

throughout North America caused by the absence or removal of an apex predator (Allombert et

al., 2005; Hebblewhite et al., 2005; Stockton et al., 2005; Ripple and Beschta, 2009). Predators

not only help keep the world green, as Hairston et al. hypothesized half a century ago, but they

help stabilize ecosystems and maintain diversity. The view that top-down regulation of

ecosystems works in concert with bottom-up forces is fast becoming less the exception and more

the rule.

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