Keystone Species

By: Stephen C. Wagner (Department of Biology, Stephen F. Austin State University) 2010 Nature Education
Citation: Wagner, S. C. (2010) Keystone Species. Nature Education Knowledge 3(10):51

A keystone in an arch's crown secures the other stones in place. Keystone species play
the same role in many ecological communities by maintaining the structure and integrity
of the community.
Aa Aa Aa

Paine's Milestones
The term keystone species was first coined by Robert Paine (1966) after extensive studies examining the interaction
strengths of food webs in rocky intertidal ecosystems in the Pacific Northwest. One of his study sites, located at Mukkaw
Bay, contained a community consistently dominated by the same species of mussels, barnacles, and the starfish, Pisaster
ochraceus, which preys upon the other species as a top predator (Figure 1).
Paine (1966) had observed that the diversity of organisms in rocky intertidal ecosystems declined as the number of
predators in those ecosystems decreased. He hypothesized that some of these consumers might be playing a greater role
than others in controlling the numbers of species coexisting in these communities. He tested his hypothesis in an experiment
that involved selecting a "typical" piece of shoreline at Mukkaw Bay, about 8 meters long by 2 meters wide, that was kept
free of starfish. This area was compared to an adjacent, undisturbed control area of equal size.

Figure 1: Food web of species present in temperate intertidal ecosystem

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Paine observed dramatic changes in the temperate intertidal ecosystem after Pisaster was artificially removed compared
with the control area that remained unchanged in its species number and distribution. The intertidal area where Pisaster had
been removed was characterized by many changes. Remaining members of the ecosystem's food web immediately began
to compete with each other to occupy limited space and resources. Within three months of the Pisaster removal, the
barnacle, Balanus glandula, occupied 60 to 80% of the available space within the study area. Nine months later,Blanus
glandula had been replaced by rapidly growing populations of another barnacle Mitella and the mussel Mytilus. This
phenomenon continued until fewer and fewer species occupied the area and it was dominated by Mytilus and a few
adult Mitella species. Eventually the succession of species wiped out populations of benthic algae. This caused some
species, such as the limpet, to emigrate from the ecosystem because of lack of food and/or space. Within a year of the
starfish's removal, species diversity significantly decreased in the study area from fifteen to eight species (Figure 2).

Figure 2: Effect of removal of top predator on total species number in intertidal ecosystem
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In his seminal paper that followed this work, Paine (1969) derived the term keystone species to describe the starfish in these
intertidal ecosystems. Of these species he commented: "The species composition and physical appearance were greatly
modified by the activities of a single native species high in the food web. These individual populations are the keystone of
the community's structure, and the integrity of the community and its unaltered persistence through time."
Paine went on to describe the criteria for a keystone species. A keystone species exerts top-down influence on lower trophic
levels and prevents species at lower trophic levels from monopolizing critical resources, such as competition for space or
key producer food sources. This paper represented a watershed in the description of ecological relationships between
species. In the twenty years that followed its publication, it was cited in over ninety publications. Additionally, the original
paper describing the intertidal areas was cited in over 850 papers during the same time period (Mills et al. 1993).

Other Keystone Species

There are a number of other well-described examples where keystone species act as determinate predators. Sea otters (i)
regulate sea urchin populations, which in turn feed upon kelp and other macroalgae (Duggins 1980). The otters keep the sea
urchin populations in check, thus allowing enough kelp forests to remain as a habitat for a variety of other species. As a
result, the entire ecosystem is kept in balance. In terrestrial environments, fire ants function as keystone predators by
suppressing the numbers of individuals and species of arthropods that could be harmful to agriculture.
Keystone species also play important roles in many other ecosystems (Mills et al. 1993). For example, hummingbirds are
sometimes referred to as keystone mutualists because they influence the persistence of several plant species through
pollination. On the other hand, keystone modifiers, such as the North American beaver (Casor candensis), determine the
prevalence and activities of many other species by dramatically altering the environment (Figure 3). Species like the
Saguaro cactus (Carnegiea gigantea) in desert environments and palm and fig trees in tropical forests are called keystone

hosts because they provide habitat for a variety of other species. Keystone prey are species that can maintain their numbers
despite being preyed upon, therefore controlling the density of a predator.

Figure 3: A dam built by beavers as keystone modifiers

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Gray Wolves: A Case Study of Keystone Species Removal and Restoration

Gray wolves (Canis lupus, Figure 4) once roamed the western portions of North America from Alaska to Mexico. During the
latter part of the nineteenth century, most of the important prey for wolves bison, deer, elk, and moose were severely
depleted by human settlers. The wolves soon became the enemies of the ranchers and farmers when they turned to preying
upon sheep and other livestock (Grooms 1993, Breck & Meier 2004, Outland 2010).

Figure 4: The gray wolf (Canis lupus), a keystone species in Yellowstone National Park
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When the federal government set aside the Greater Yellowstone Ecosystem (GYE) as a national park in 1872, about three to
four hundred wolves were present, preying mostly upon large hooved ungulates such as elk (Cervus canadensis, Figure 5)
and bison (Yellowstone Association 1996). Fearing the wolves' impact on elk and bison herds as well as livestock owned by
area ranchers, the federal government began eradicating the wolf population. Bounty programs that continued until 1965
offered as much as $50 per wolf. Wolves were trapped, shot, dug from their dens, hunted with dogs, and poisoned. In
Yellowstone National Park, park rangers killed the last two remaining pups in 1924. By the 1930s wolves had been
effectively eliminated from the contiguous 48 States and Mexico and only remained in high numbers in Alaska.

Figure 5: The elk (Cervus canadensis), principal prey of gray wolves (Canis lupus)
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With their primary predator eliminated, elk populations exploded, leading to the overgrazing of plants, especially those found
in riparian zones (Laliberte & Ripple 2004). Significant declines in the populations of many plant species (e.g., aspen, willow)
resulted, which in turn influenced other wildlife, such as beaver and songbird populations (Ripple & Breschetta 2004,
Hallofsky & Ripple 2008). Intensive browsing of aspen (Populus tremuloides) stands, for example, led to a rapid decline in
the number of seedlings and root sprouts growing into saplings and trees. For many stands of these trees, only large
diameter trees (i.e., those that had matured before the wolves were eradicated) remained.
Disappearance of these and other plant species not only caused the loss of habitat for many other animals but also
influenced other ecological factors (Smith et al. 2009), including stream bank stability, the deposition of organic matter and
fine sediment in riparian zones, water temperature regulation via shading, and nutrient cycling. The removal of wolves thus
led to the instability of riparian and other environmentally sensitive areas.

Figure 6: Map of wolf pack territories in Yellowstone National Park in 2009

Public Domain National Park Service.
After the United States Congress passed the original Endangered Species Preservation Act in 1966, the gray wolf made the
original Endangered Species List. The subsequent Endangered Species Act of 1973 called for their restoration.
Consequently, the National Park Service changed their policy to restore natural conditions within Yellowstone National Park,
including the reintroduction of the gray wolf (Smith & Bangs 2009). In 1995, the federal government began reintroducing
gray wolves into the GYE. Initially, fourteen wolves were captured in Canada and relocated to one-acre acclimation pens
where they were held for ten weeks before being released into the GYE. This process was repeated in 1996 and 1997 with
an additional seventeen wolves from Canada and ten pups from Montana (Smith et al. 2009). For the most part, wolf
populations have continued to grow at a rapid rate, averaging 17% per year (Smith & Bangs 2009). At the end of 2009, there
were between 96 and 98 wolves in Yellowstone, with 14 packs, 1 non-pack grouping, and 2 loners (Figure 6). Park staff
recorded 365 prey animals killed by wolves, most of which were elk (302).
Despite some setbacks (e.g., disease outbreaks within the fledgling wolf packs), recovery efforts in the GYE have greatly
surpassed expectations. Since their reintroduction, wolves have overwhelmingly targeted elk over other prey. This has
coincided with an increase in willow heights in several areas. This may indicate that a wolf-elk-willow trophic cascade has
been reestablished within the GYE. Furthermore, investigators believe that restoration of willow populations has led to a tenfold increase in beaver populations (Smith 2004) as well as a significant songbird rebound (Baril & Hansen 2007).
Halofsky & Ripple (2008) found that aspen browsing by elk had ceased in areas burned during the historic 1988 fires but
continued in unburned areas. These results were attributed to the increased risk of wolf predation in burned areas. The
authors proposed that a recoupling of fire with increased predation risk from wolves may help improve aspen restoration.
The results also suggest that much more research needs to be conducted to determine the effects of wolf reintroduction into
the GYE.

Summary
The concept of keystone species was first proposed and demonstrated in the 1960s by the dominance of top-predator
starfish in intertidal ecosystems. Keystone species are species that play a disproportionately large role in the prevalence and
population levels of other species within their ecosystem or community. The recovery of the gray wolf after its eradication

from Yellowstone National Park, almost ninety years ago, demonstrates how crucial keystone species are to the long-term
sustainability of the ecosystems they inhabit. Most importantly, the preservation and restoration of keystone species is
essential for maintaining and/or reestablishing the historic structure and function of the ecosystems they inhabit.

References and Recommended Reading

Baril, L. & Hansen, A. Avian response to willow height growth in Yellowstone's Northern range. Report to Yellowstone
National Park, 2007.
Beck, S. & Meier, T. Managing wolf depredation in the United States: past, present, and future. Sheep and Goat Research
Journal 19, 4146 (2004).
Duggins, D. O. Kelp beds and sea otters: an experimental approach. Ecology 61, 447453 (1980).
Grooms, S. Return of the Wolf. Minocqua, WI: Northword Press, 1993.
Halofsky, J. & Ripple, W. Recoupling fire and aspen recruitment after wolf reintroduction in Yellowstone National
Park. Forest Ecology and Management256, 10041008 (2008).
Laliberte, A. S. & Ripple, W. J. Range contractions of North American carnivores and ungulates. BioScience 54, 123138
(2004).
Mills, L. S. et al. The keystone-species concept in ecology and conservation. BioScience 43, 219224 (1993).
Outland, K. Who's afraid of the big bad wolf? The Yellowstone wolves controversy. Journal of Young
Investigators 11, (2010).
Paine, R. T. Food web complexity and species diversity. American Naturalist 100, 6575 (1966).
Paine, R. T. A note on trophic complexity and community stability. American Naturalist 103, 9193 (1961).
Yellowstone Association. The Yellowstone Wolf: A Guide and Sourcebook. Edited by P. Shullery. Winnipeg: Red River
Books, 1996.
Ripple, W. J. & Breschetta, R. L. Wolves, elk, willows, and trophic cascades in the upper Gallatin Range in Southwester
Montana, USA. Forest Ecology and Management 200, 161181 (2004).
Smith, D. W. 2003 Beaver Survey. Internal Memorandum. Yellowstone National Park, 2004.
Smith, D. W. & Bangs, E. E. "Reintroduction of wolves to Yellowstone National Park: history, values and ecosystems."
In Reintroduction of Top-Order Predators, eds. M. W. Hayward & M. J. Somers (Oxford, UK: Wiley-Blackwell, 2009), 92125.
Smith, D. W. et al. "Wolf recolonization of the Madison Headwaters Area in Yellowstone." In The Ecology of Large Mammals
in Central Yellowstone, eds. R. A. Garrott et al. (New York, NY: Academic Press, 2009), 283304

Keystone Species and the Diversity-Stability Hypothesis

Not all species are equal with respect to their [effects on other species. Starfish feeding in the intertidal zone
clean an area free of barnacles and mussels. These barnacles and mussels, without predation by the
starfish, would come to dominate the community. In a classic 1966 study, Robert Paine removed starfish
from enclosures. In those enclosures where the starfish were removed, the number of species in the
community dropped from fifteen to eight. Paine called starfish a keystone species, one whose presence
has a dramatic effect on species diversity.
Prior to 1973 most ecologists thought that more diverse ecosystems would be more stable than would ones
with fewer species. This general belief, what has become known as the diversity-stability hypothesis,
was based on a variety of observations but not really tested. One such observation was that cultivated land
that had simplified ecological communities was more subject to species invasions than similar areas that
hadn't had human influence. In addition, insect outbreaks are much more common in the less diverse boreal
forests than they are in tropical forests.
In 1973 Robert May published a theoretical study that challenged the intuitive ideas that ecologists had
about the diversity-stability hypothesis. May analyzed randomly constructed communities and found that
communities with more species tended to be less, not more, stable. May's study, like more theoretical
studies of the 1970s, assumed that population numbers of each species were at equilibria. This assumption
was made, not because it reflected reality, but because it made the mathematics more tractable. More
recent studies have shown that if there is some degree of flux in the population numbers, the community
can maintain more species than in equilibrium. This variability may allow different species to respond
differently to the environment, and can result in fewer species being lost due to competitive exclusion. When
theoretical ecologists relax the equilibrium assumption and allow for population fluxes, they have found
results consistent with the diversity-stability hypothesis: communities with more species are more stable.
Several lines of evidence now support the diversity-stability hypothesis. The studies conducted by David
Tilman and his colleagues provide some of the strongest evidence for the hypothesis. In 1982 Tilman divided
grassland fields in Minnesota's Cedar Creek National History Area into more than 200 plots. He and his
colleagues monitored the species richness and community biomass (the total mass of all plants) in each of
those fields over the next two decades. They found that diversity within a community is positively correlated
with plant community stability, as defined by the extent of variation in community biomass. Various other
studies at different scales have found similar results: stability increases with diversity.4

Keystone Species Hypothesis

From chilly Alaska to sunny Baja California, on the exposed rocky shores between
low and high tide, lives a group of marine organisms in delicate balance with one
another. But one organism, the starfish Pisaster ochracues, is the pillar of the
community on which the stability of the entire system depends.
If that single predator is removed, dramatic changes result in the varieties and
population densities of all the other species in the community. Interestingly, no
comparable changes appear when other "consumers" are removed from the biological
fabric. That starfish is the "keystone" species governing biological diversity in the
entire intertidal zone.
The keystone species concept has been a mainstay of the ecological and conservation
biology literature since its introduction by UW zoology professor Robert T. Paine in
1969. His seminal paper extended the conclusions of a field experiment published
three years earlier. The research resulting in the keystone species concept was done on
Makah Tribal lands on the outer coast of Washington State, with the Makahs'
permission. It involved the sustained removal of a single predator species over a threeyear interval and documentation of the resultant changes.
Keystone species are usually noticed when they are removed or they disappear from
an ecosystem, resulting in dramatic changes to the rest of the community. The
phenomenon has been observed in a wide range of ecosystems and for a wide range of
organisms.
Put another way, a keystone species is one whose impacts on its community or
ecosystem are large and greater than would be expected from its relative abundance or
total biomass, explains Paine. Species that are known to play this role, besides the
starfish mentioned above, include the sea otter, the freshwater bass, and the predatory
whelk Concholepas (a kind of elongated sea snail). By contrast, trees, giant kelp,
prairie grasses, and reef-building corals all have impacts that are large but not
disproportionate to their total biomass, and therefore they are not keystone species.
A good illustration of Paine's keystone species concept is provided by the sea otter,
which formerly occupied a range extending from the northern Japanese archipelago,
through the Aleutian Islands, down the coast of North America as far south as Baja
California. The return of the sea otter to southern California, for example, is restoring

kelp beds and associated marine life there. That's because one of the favorite
delicacies of the otter is the large sea urchin, which in turn feeds on kelp. As the sea
otter returns to its native territories, scientists expect the population of invertebrates,
like urchins and abalone, for example, to decrease as marine plant biomass increases.
In fact, a decrease in sport and commercial abalone fisheries was reported following
an influx of sea otters into areas of California, causing a controversy there.
Paine's work has been cited by hundreds of researchers over the years, and it has been
proposed as a foundation for management efforts to protect the biological diversity of
the world's ecosystems.
"Its importance," says Paine, "is that it convinced managers and conservationists alike
that the ecological impact of single species matters. That is, in order to manage,
understand, and restore ecological assemblages, the roles of individual species have to
be understood and considered."
The concept has provided a powerful model for understanding the forces that organize
ecological communities, and it has influenced the thinking of managers and policy
makers as they set priorities in their efforts to conserve species and habitats. Over the
years, controversy in scientific circles has grown up around the term keystone species
as a result of "overly expansive usage." Through a United Nations Environmental
Programme workshop held in 1994, prominent researchers in the field reached a new
consensus about a definition of the term and new guidelines for its expanding
applications in the future.

1.

"The Keystone-Species Concept in Ecology and Conservation," L. Scott Mills, Michael E. Soule, and
Daniel F. Doak, BioScience, 43 (4), 219 (1993).

2.

"Sea Otters: Their Role in Structuring Nearshore Communities," Science, 185, 1058 (1974).

3.

"The Keystone Cops Meet in Hilo," Mary E. Power and L. Scott Mills, TREE, 10 (5), 182 (1995).