Keystone SpeciesBy:Stephen C. Wagner(Department of Biology, Stephen F. Austin State University)2010Nature Education

Citation:Wagner,S.C.(2010)Keystone Species.Nature Education Knowledge3(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.AaAaAa

Paine's MilestonesThe 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 2010Nature EducationAll rights reserved.Paine observed dramatic changes in the temperate intertidal ecosystem afterPisasterwas artificially removed compared with the control area that remained unchanged in its species number and distribution. The intertidal area wherePisasterhad 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 thePisasterremoval, the barnacle,Balanus glandula, occupied 60 to 80% of the available space within the study area. Nine months later,Blanus glandulahad been replaced by rapidly growing populations of another barnacleMitellaand the musselMytilus. This phenomenon continued until fewer and fewer species occupied the area and it was dominated byMytilusand a few adultMitellaspecies. 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 2010Nature EducationAll rights reserved.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 (Millset al. 1993).Other Keystone SpeciesThere 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 (Millset 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 2010Nature EducationAll rights reserved.Gray Wolves: A Case Study of Keystone Species Removal and RestorationGray 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 2010Nature EducationAll rights reserved.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) 2010Nature EducationAll rights reserved.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 (Smithet 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 2009Public DomainNational 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 (Smithet 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 ten-fold 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.SummaryThe 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 Journal19,4146 (2004).Duggins, D. O. Kelp beds and sea otters: an experimental approach.Ecology61,447453 (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.BioScience54,123138 (2004).Mills, L. S.et al. The keystone-species concept in ecology and conservation.BioScience43,219224 (1993).Outland, K.Who's afraid of the big bad wolf? The Yellowstone wolves controversy.Journal of Young Investigators11,(2010).Paine, R. T. Food web complexity and species diversity.American Naturalist100,6575 (1966).Paine, R. T. A note on trophic complexity and community stability.American Naturalist103,9193 (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.ForestEcology and Management200,161181 (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." InReintroduction 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." InThe Ecology of Large Mammals in Central Yellowstone, eds. R. A. Garrottet 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 akeystone 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 thediversity-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 starfishPisaster 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 three-year 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 whelkConcholepas(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).