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  Population & community ecology
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Keystone predator


Topics on community interactions include keystone predator, considered here, and COMPETITION and POPULATION BIOLOGY dealt with in other sections.


photograph of ochr star creating a patch among barnacles, mussels, and seaweedsNOTE a keystone predator is one of high trophic status that through its feeding activities exerts a disproportionate influence on community structure.  Visualise a classic feeding pyramid, where a top predator eats another predator and this predator eats an herbivore, and so on.  Removal of the top predator can cause repercussions throughout the ecosystem.  The importance of a keystone predator is most evident when its principal prey is a species that monopolises a basic resource, such as space, and out-competes or excludes other species.  The concept in its marine context originally applies to the ochre sea star Pisaster ochraceus eating its preferred prey, the sea mussel Mytilus californianus, but has since been used to describe other marine predators, such as sea otters, spiny lobsters, sharks, and so on


An ochre star Pisaster ochraceus creates
a patch among a community of barnacles,
mussels, and seaweeds 0.15X

Research study 1

photograph of Bob Paine, University of WashingtonIn classic studies1 at Mukkaw Bay, Washington, removal of all ochre sea stars Pisaster ochraceus over a 10yr period by Robert Paine2, a University of Washington scientist, produces marked changes in zonation patterns.  Most notable is a downward shift in the lower limit of mussel distribution of about 2m through redistribution of adults and normal settlement of larvae.  In the absence of Pisaster the new lower limits of mussel distribution are set mainly by predation by whelks Nucella spp. on juvenile mussels, and by other factors.  Accompanying the mussel-bed expansion is a severe alteration in community structure.  Where previously about 25 species of barnacles and algae occupy most of the free space on the rock, this changes over time to a virtual 100% monoculture of sea mussels.  Accompanying this is occupation of the new 3-dimensional space within the bed by numerous species of worms, crabs, snails, and other small invertebrates. From these modest beginnings grew a groundswell of interest in marine ecological science, and the author’s influence in the field has been inestimable3. Paine 1966 Am Nat 100: 65; Paine 1969 Ecology 50: 950; Paine 1969 Am Nat 103 (929): 91; Paine 1974 Oecologia 15: 93.  Photograph of Bob Paine courtesy Anne Paine, Seattle, Washington, Ed Yong, and Nature magazine; photograph of mussel bed courtesy Dave Cowles, Walla Walla University, Washington

NOTE1 the seastar-removal experiment continued for about 10yr and, while the author discusses the results and their implications in several research publications up until 1974, it wasn’t until 1969 in two publications that he actually mentions the term keystone, and then more as an afterthought. It was only later that it became the ecological “buzzword” that it is today, used (and overused) to describe foodweb status of carnivores such as eagles, killer whales, grizzly bears, snails, and sea otters, and even such things as fire ants, termites, and herbivorous sea urchins and beavers. Some prey species, such as snowshoe hares, have been termed keystone prey species. For a good, easily readable, review of the strengths and shortfalls of the concept as it is used in contemporary science see Mills et al. 1993 Bioscience 43 (4): 219.

NOTE2 Bob Paine was a man of his time, a marine-ecology tour de force, who left a legacy of his own brilliance and a dynasty of over 40 doctoral and countless masters students, most of whom carried on their own unique research programmes in marine science. For an informal history of Bob Paine, his research, and his legion of marine-ecology students, see a review written for Nature magazine in 2013. Yong 2013 Nature 493: 286.photograph of ochre stars Pisaster ochraceus eating a mussel bed from below courtesy Dave Cowles, Walla Walla University, Washington

in tribute to the 50th anniversary of the publication in 1966 of Paine’s seastar-removal work in the journal The American Naturalist in and, coincidentally, of the author’s death in 2016, two University of California scientists laud the work as perhaps “the most influencial ecological paper ever”. In noting that the paper has been, and continues to be, the most cited article in the journal’s 150yr history (from March 1867), these authors note that even “after 50 years it continues to influence ecological theory and (now) conservation biology”. Lafferty & Suchanek 2016 Am Nat 188 (4): 365.

The sea stars attack from lower in the intertidal zone, moving up when the tide comes in and wrenching the mussels free from their attachment. They then crawl downwards with their prey to digest them. The sea stars effectively set the lower limits of distribution of the mussels. Note the dominance of mussels in the higher zone, and their replacement by algae in the lower zone

Research study 2

Interestingly, and perhaps unsurprisingly in view of the complexity of marine intertidal ecosystems, repeat experiments on sea-star removal may fail to produce the same results as the original on which the keystone-predator concept was first erected.  Questions have therefore arisen as to the general applicability of the “keystone” concept and to the inter-relationships of this kind of “top-down” influence on community dynamics with other “bottom-up” effects, such as nutrient availability.  For example, what are the conditions under which the keystone effect occurs? what is its generality in space and time? and what are the interactive effects of nutrient availability for primary production?  Pisaster’s feeding activities exemplify the effects of “strong” predation from a single source, but what about strong predation from multiple sources?  This consideration provides a new concept of diffuse predation, defined as strong predation by several predators, but with each predator alone having little measurable effect on patterns of community structure.  In view of these considerations, one author has proposed a re-definition of the keystone concept, that is, that communities may be affected by strong or weak predation, and that those with strong predation may be under the influence of either keystone or diffuse predation.  Ideas and concepts from Menge et al. 1994 Ecol Monogr 64: 249; for detailed discussion of top-down and bottom-up concepts see Menge 1992 Ecology 73: 755.

Zones are well defined in this photograph of a moderately wave-exposed island shore in Barkley Sound, British Columbia. Major groups of organisms are listed on the Left. Note the large barren area above the sea anemones and below the mixed mussels/barnacles/Endocladia zone. Potentially, this area could be inhabited by mussels and other species favoured by ochre stars Pisaster ochraceus. At high tide the sea stars crawl upwards to feed primarily on mussels at the lower limit of their distribution. Note the difference between this photo and the one above in Research Study 1 that features a more protected shore in Puget Sound, Washington
photograph of zonation in Barkley Sound, British Columbia
Research study 2.1

photograph of mussels Mytilus californianus showing epibiotic organisms growing on the shells and living within the byssus threadsA study that relates to the keystone-predator concept is done by a University of California, Santa Barbara scientist on epibionts on sea mussels Mytilus californianus at 16 sites along the coast from Oregon to mid-California. A basic tenent of the Pisaster-Mytilus interaction described above is that predation by the seastar on the mussel frees up primary space on the rock that may now be occupied by species otherwise excluded by the mussels. Thus, in the absence of mussels the diversity of species inhabiting primary rock space should theoretically be increased. But is it? The researcher finds, in fact, that almost all of the newly recruited species to the rock surface are ones that formerly lived epibiotically on the shells of the mussels, so diversity of these species is basically unchanged. What does this finding do to our understanding of the keystone-predator concept? Nothing, for the original premise involves diversity changes on the primary rock surface, not on the secondary surfaces represented by mussel shells. It does, however, draw attention to the vague definition of some of the elements, such as diversity, inherent in the original concept. Lohse 1993 J Exp Mar Biol Ecol 166: 1.

NOTE out of a total of 59 major taxa identified in the study, 56 are able to inhabit both substrata (rock and shell)

A few of the epibionts inhabiting shells of mussels Mytilus californianus 0.75X

Research study 3

photograph of cluster of mussels Mytilus trossulusmocked-up photo of whelks Nucella ostrina and N. canaliculata courtesy Linda Schroeder, Northwest Shell ClubIdeas relating to the keystone-predator concept are tested on the central Oregon coast where the bay mussel Mytilus trossulus inhabits both wave-exposed and wave-protected habitats.  In these locations the mussels may cover greater than 70% of the rocky substratum by mid- to late-spring.  Principal predators of the mussels are ochre stars Pisaster ochraceus, and whelks Nucella ostrina and N. canaliculata.  The authors transplant clumps of mussels to wave-exposed and wave-protected areas at 2 sites (Boiler Bay and Strawberry Hill).  At each site the predator species are either removed (one or other, or both), or left undisturbed.  Survival of the mussels is monitored over a 60-d period.  The chief research questions being addressed are: 1) what is the sensitivity/predictability of a keystone predator's activity in the presence of other predators? and 2)  what is the degree of importance of other predators in the presence and absence of a keystone species?  Replicate groups of mussels (each comprising 50 individuals) are transplanted in spring to the experimental areas by pressing them onto the shore under plastic mesh “blankets”, the blankets themselves being fastened to the rocks.  After 4wk the mesh blanket is removed and numbers of sea star and whelk predators adjusted to create 3 experimental treatments and a control: 1) both Pisaster and Nucella spp. removed, 2) only Pisaster removed, 3) only Nucella spp. removed, graph showing survival of mussels Mytilus trossulus in the presence or absence of sea-star and whelk predatorsand 4) both Pisaster and Nucella spp. left undisturbed (control).

After a 60d, the results show (see sample graph on Right) that where both predators are removed (Treatment 1) the mussels survive well. Where Nucella spp. are present but Pisaster absent (Treatment 2) the whelks eat the mussels and progressively reduce their numbers. In the absence of Pisaster in this treatment there is an increase in whelk density and evidence of size increase in individual whelks.  Whether this owes to a release from predation by, or competition with, Pisaster is not known. Finally, where Pisaster is present, whether whelks are present or not (Treatments 3, 4), the mussels are quickly eaten, and there is no significant difference between the 2 treatments. In other words, Pisaster is the dominant predator and the whelks have little or no effect on Pisaster's predatory activities. In Treatment 4 (control) the whelks are implicated as predators because of the evidence of drilled shells. The effect is the same in both wave-exposed and wave-protected conditions, and at both geographical sites. 

Overall, the effect of Pisaster is 2-3 orders of magnitude greater than the effect of Nucella spp.  The authors conclude that in a keystone predator-dominated system, other invertebrate predators may have small or no effects on community structure and may be considered “redundant”.  However, in the absence of the keystone species, such “redundant” predators may adopt larger roles in the dynamics of the community and may at least partially compensate for the absence of the keystone species.  The authors note that the keystone concept, originally used for a Pisaster-dominated system, has seen such broad application that it risks becoming a “label”, and they caution that it be used only under clearly defined conditions.  The study is especially important in that it is the first rigorous test of the generally accepted idea that the effect of a keystone predator is independent of the presence of other predator species.  Navarrete & Menge 1996 Ecol Monogr 66: 409. Photographs of whelks courtesy Linda Schroeder, Pacific Northwest Shell Club, Seattle, Washington PNWSC.

NOTE  the mussels are small in size (2.5-5.0 cm shell length) to ensure that both sea stars and whelks can prey on them

NOTE  the predators are removed from fairly wide areas surrounding the treatment clumps of mussels.  However, in addition to the removals, some mussel clumps are enclosed in plastic-mesh cages, either dome-shaped or “top-plus-two-sides”, to protect the clumps against re-invading predators during periods when the experiments are not being monitored and to assess cage effects, respectively

Research study 4

graph showing interactive effects of predators and prey on numbers of predatory whelks Nucella in OregonWhen a top predator Pisaster ochraceus preys on intermediate predators such as Nucella ostrina and N. canaliculata,  and they all prey on a common resource such as Mytilus trossulus, it is known as intraguild predation. In the previous Research Study 3 the mechanisms responsible for negative effects of Pisaster on the whelks, whether competition or predation, are not conclusively identified.  However, based on results of this earlier study, if competition occurs, it is expected to favour greatly the sea stars.  A follow-up study by the same research group investigates these interactions through manipulation of sea-star and mussel densities on mussel-patch areas containing known densities of whelks. 

First, replicate plots for each of the combinations of predators (Pisaster) and prey (Trossulus) are created and maintained for 14mo. Any re-invading sea stars and mussels are removed during each site-visit (daily to fortnightly intervals) over the duration of the study. The experimental approach used allows the separation and quantification of top-down effects of predation by sea stars versus the bottom-up effects of competition and food limitation.  Results support a model of indirect (exploitative) competition between the sea stars and whelks, and additionally reinforces the idea that food-chain “omnivory” is the most important trophic interaction in this particular Oregon intertidal community, and one that dominates its dynamics.   Note in the summary histogram presented here the relatively large direct effect of Mytilus trossulus (the prey) on whelk density in comparison with the smaller non-significant effects of predation by Pisaster ochraceus and the small but significant effects of exploitative competition with Pisaster.  Navarrete et al. 2000 Ecology 81: 2264.

NOTE  use of open “manipulation plots”, rather than cages, removes possible caging artifacts from the analysis

NOTE  this describes consumers that feed on more than one trophic level, such as sea stars eating both mussels and whelks

Research study 5

graph showing effects on mussel population of manipulating densities of sea stars Pisaster ochraceusA recent study on predator/prey interactions between ochre stars Pisaster ochraceus and sea mussels Mytilus californianus confirms that distributional boundaries of shore organisms are maintained by complex spatial equilibria. In other words, prey refuges are not static.  The experiments, conducted in Barkley Sound, British Columbia and at the Bamfield Marine Sciences Centre, involve removal of sea stars in some plots, addition of sea stars in other plots, and no manipulation in control plots.  After 30mo the results are as shown in the accompanying graph, with a downward extension of the lower mussel boundary in the sea-star removal plots, an upward extension in the sea-star additon plots, and little overall change in the control plots.  Although the results seem predictable based on what is already known of the effects of Pisaster presence on sea-mussels, a critical point is that in the second treatment, that of increased densities of sea stars, the lower boundary of mussels actually moves well up into the zone usually thought to be one of spatial refuge for the mussels from sea-star predation.  In the addition-plots, as small mussel prey are depleted over time, so correspondingly larger mussels are attacked, including the largest individuals that  otherwise would represent the lower boundary of their distribution. The study is valuable in not only confirming that disributional limits of photograph of ochre stars Pisaster ochraceus crawling up the shore at high tidemussels move down in the absence of a chief predator, but also in demonstrating that they move up in the presence of the predator, not just to “control levels”, but beyond.  Thus, the “lower boundary does not delimit an impenetrable refuge”.  Robles et al. 2009 Ecology 90: 985.

NOTE  the authors’ premise is that current understanding of shore zonation is founded on concepts of static prey refuges, that is, that distributional limits are essentially unchanging over time.  This notion would surely be dismissed by any shore biologist familiar with seasonal and other fluctuations in zonational levels.  The argument therefore seems contrived, but certainly not unwelcome. In effect, the authors are erecting a “straw-man”-type scenario that leads to an informative discussion of “refuge hypothesis” versus “equilibrium process”


At high tide ochre stars Pisaster ochraceus move upwards,
beyond the lower limit of distribution of the prey mussels

Research study 5.1

graph showing sites along the shores of Strait of Juan de Fuca used in study of global warminggraphs showing historical records of intertidal distributions of mussels and barnacles in the Strait of Juan de Fuca, along with mean summer air temperaturesWhat changes in composition and distribution of intertidal communities are expected as a result of global warming?  This is an important question and a difficult one to answer because of the long timeline involved.  Partly for this reason most studies on the subject have involved observing acute effects of temperature in laboratory settings.  However, a University of British Columbia researcher has approached the problem in a  uniquely more direct way, using sea stars Pisaster ochraceus and their mussel and barnacle prey at field sites along the Strait of Juan de Fuca (see map on Left) as indicator species.  Additionally, the historical sites noted in orange on the map provide a 5-decade-old history of intertidal levels occupied by prey mussel and barnacle speces1, with historical air temperatures for one of the stations (Victoria) being provided by Canadian government climatological services (see red graph top Right).  In general, seawater temperatures are cooler at sites closer to the Pacific Ocean and warmer at sites closer to the Gulf of graphs showing intertidal zonation patterns for selected sessile invertebrates and the ochre star Pisaster ochraceusGeorgia and Puget Sound at the eastern end of the Strait (see map).  The author first records intertidal heights of the 4 prey species and Pisaster at the 6 research sites (blue boxes on map), along with mean summer rock temperatures (numbers in red on map). Results show, as expected, a depression of height with increasing temperatures for all prey species but not for the predator (see graphs on Left for barnacles S. cariosus and mussels M. californianus) .  Similarly, records of intertidal distributions obtained from earlier researchers show a depression of intertidal heights occupied by mussel and barnacle species from 1958 onwards, considered by the author to be responses to increased seawater2 temperature of about 1oC estimated for this period (see graphs on Right).  At the cooler, more wave-exposesd sites at the western end of the Strait, sessile prey species can occupy shore levels well above the foraging range of sea-star predators.  In contrast, at the eastern warmer and wave-protected sites, this high-shore refuge is unavailable because of temperature and desiccation stresses.  With respect to beds of mussels M. californianus, space freed up by downward movement of this dominant space-inhabiting species can be occupied by other species, such as barnacles, but only if predators are experimentally removed3.  Under these predator-free conditions, species richness more than doubles.  The study provides an excellent overview of the complexity of interactions to be confronted in this era of global warming.   Harley 2011 Science 334 (1124): 1124.

NOTE1  prey species are mussels Mytilus californianus and M. trossulus, and barnacles Balanus glandula and Semibalanus cariosus

NOTE2   during the same 52yr period air temperatures at Victoria, British Columbia rose by 3.4oC (see graph on Right)

NOTE3   these results are presented by the author, but not shown here

Relationship between zonation patterns and rock temperatures for 2 selected sessile
invertebrate species and the predatory sea star Pisaster ochraceus. The ordinate axes
represent relative intertidal heights, where 0 represents extreme low water and 1
represents extreme high water levels for the year in which the data were collected

Research study 6

histogram showing inhibitory effects of sea-star effluent on growth in whelks Nucella emarginataOchre stars Pisaster ochraceus not only exert strong effects on community diversity directly, but at the same time can exert such effects indirectly, by “intimidating” the predatory behaviour of nearby whelks Nucella emarginata.  Laboratory studies by researchers at the University of California, Santa Barbara show that this happens through perception by the whelks of water-borne substances emitted by Pisaster.  The affected whelks not only eat less, digest less, and thus grow/reproduce less over the 8wk period of study (see accompanying figure), but their feeding preferences are significantly altered.  The sea stars are not eating more of the whelks, just causing them to go off their regular diets.  The authors remark that this may explain why whelks eat fewer sea mussels Mytilus californianus in the presence of Pisaster than in their absence.  By drawing attention to such clandestine influences of P. ochraceus, the study offers new insight into the already large role that these keystone predators play in regulating intertidal community dynamics.  Gosnell & Gaines 2012 Mar Ecol Progr Ser 450: 107.

NOTE  see Research Study 3 above

NOTE  a question that immediately comes to mind is whether whelks tend to avoid the presence of the sea stars in the field

Research study 7

Sea stars in the area of Attu Island at the extreme western end of the Alaska archipelago are also involved in a food web with mussels Mytilus trossulus as their prey and sea otters Enhydra lutris as their predators.  A comparison of sea-star species before(1983) and after (1994) sea otters reinhabited the area reveals significant declines in biomass.  Mussels translocated on rocks from intertidal to subtidal locations also show lower mortality from sea-star predation after the return of the sea otters.  Asteroids not seem like suitable food for sea otters and apparently only constitute some 1-3% of their regular diet (based on reports of other researchers), so it is actually unclear whether otters are entirely responsible for the large decline in asteroid numbers.  The authors do not indicate the extent to which outer skin and ossibles are eaten, or only the internal organs (gonads and digestive glands).  The authors liken the trophic pathway in this Alaskan system to the well-known sea otter-sea urchin-kelp pathway in California (see LEARNABOUT/SEA URCHIN/POPULATION & COMMUNITY ECOLOGY/INTERACTION WITH KELPS & SEA OTTERS).  Vicknair & Estes 2012 Mar Biol 159: 2641.

NOTE  there are 5 dominant sea-star species or species groups in the Attu Island area of Alaska, including Evasterias retifera, Leptasterias spp.,  Lethasterias nanimensis, Henricia spp. and Crossaster papposus.  Two species Pisaster ochraceus and Pycnopodia helianthoides, important predators in other areas of the northeast Pacific, are absent in these Alaskan islands

NOTE  also eaten by the sea stars are barnacles Semibalanus cariosus, data not included in this synopsis