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

NOTE 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

In classic studies at Mukkaw Bay, Washington, removal of all ochre sea stars over a 10-yr period 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. Paine 1974 Oecologia 15: 93.  Photograph courtesy Dave Cowles, Walla Walla University, Washington rosario.wallawalla.edu.

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

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.

Ideas 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, and 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

When 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

A 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 mussels 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

Ochre 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