Learn About Seastars: Population & community ecology

Keystone predator

Topics on population community ecology include KEYSTONE PREDATOR, considered here, and COMPETITION, GENETICS, and POPULATION BIOLOGY dealt with in other sections.

photograph of ochr star creating a patch among barnacles, mussels, and seaweeds

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

Research study 1

photograph of Bob Paine, University of Washington

In 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 rosario.wallawalla.edu.

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

NOTE3 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, andtheir 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 threads

A 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 1°C 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 3.4°C (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

Research study 8

Food webs may consist of direct interactions, such as a predatory sea star eating an herbivorous snail, and indirect interactions which, in the example just noted, might be represented by seaweeds that are now freed from being eaten by the snail. When the snail is not actually eaten by the predator, but is simply driven off, say, by behavioral flight reactions to the predator’s scent, the indirect interaction may still be the same, with the seaweeds still freed from being consumed. These kind of interactions are termed trait-mediated ones, the trait being, of course, the snails’ behaviour to the scent. The authors of the study, a consortium of west-coast researchers, comment that while the behaviour can readily be demonstrated in the laboratory with sea stars Pisaster ochraceus and Leptasterias hexactis using herbivorous black-turban snails Tegula funebralis as the reacting species, the trait has apparently not previously been described for inhabitants of rocky-shore tidepools. This is not altogether true. The escape response1 of Tegula funebralis to the scent of predatory sea stars such as Pisaster ochraceus has been known for at least 6 decades. When the herbivore crawls away from its seaweed foods in response to the predator, it would have been self-evident to an early viewer that the consequences must be the sparing of seaweed life, for that is what the snails eat in the tidepools. So, what the authors really mean by their inference is that the interaction has never previously been described using TMII jargon, or Trait-Mediated Indirect Interactions. Some findings in this nicely planned and interesting laboratory and field study are: 1) snails will respond to water-borne cues from Pisaster that are 75cm away, indicating potential for long-range TMII effects, 2) responses of 7d food-deprived snails to sea-star scent are “marginally” (but not statistically2 significant) less than fed ones (suggesting to the authors that TMII effects may be less), and 3) comparison of similar-sized3 individuals of the 2 sea-star species show that Leptasterias may be more effective at inducing TMIIs than Pisaster owing to its faster attack speed. However, with regard to the last, as the smaller Leptasterias is unable to prey upon large-sized snails, in the end, Pisaster may out-perform its “rival” in degree of TMII induction. In fact, laboratory data in the study show that the presence of Pisaster reduces the number of snails grazing by 90-fold as compared with when they are absent, accompanied by an approximate 8-fold reduction in grazing on algae (Ulva). The study is an interesting and provocative contribution to our understanding of TMII food-web interactions in tidepool habitats; now, all the researchers need to do is get out to the tidepools and test their ideas in situ. Morgan et al. 2016 Mar Ecol Prog Ser 552: 31.

NOTE1 there are at least 3 types of responses exhibited by black-turban snails in tidepools: simple fleeing, crawling upwards out of the water, and release of attachment leading to dropping to the bottom of the tidepool. The first 2 behaviours are used in the study; not the third

NOTE2 the p value for this particular comparison in the study is 0.065, which is just beyond the normally accepted confidence level of 0.05 and, when results get this close, scientists sometimes get sloppy in their thinking. in fact, non-significance in stastical-test results does not usually allow this kind of fudging, as the authors are well aware. If two means are "non-significantly" different, then they DO NOT differ...full stop! “Non-significance” in science can arise from several causes, including poor experimental design (not in this case), use of an inappropriate statistical test, or (most commonly) too small a sample size. In this case, he problem may arise from having an arbitrary cut-off at p=0.05. For scientists that use this approach, what do they do when they get a value for p of 0.051? Does that mean the results are useless? Or do they reduce the number of significant figures to 0.05 to solve it? Some scientists will not accept significance differences at confidence levels greater than 0.001, or even lower, but ultimately it may depend upon the nature of the study. For a crystallographer measuring angles of a crystal, p levels greater than, say, 0.0000000001 may be considered non-significant, while animal behaviorists might be more content with something like 0.10. For this reason, many researchers do not use the commonly accepted, but still arbitrary, rejection level of p=0.05; instead, they let the reader make his or her own conclusions. After a test result of 0.065, the authors could easily have performed a “power” test which, among other things, would tell them what the sample size would need to have been at the same level of variance to obtain “significance” at whatever p value they choose. If a sample size of 20 would do the trick, then another week’s experiments at Bodega wouldn’t be much of a burden (especially if assigned to a grad student), and especially since the study at the time of publication had already been going on for 10yr!

photograph of black-turban snails Tegula funebralis in a tidepool with an ochre star Pisaster ochraceusNull-hypothesis testing and statistical probabilities have been under criticism for many decades. For an up-to-date and coherent account of the misuses and misunderstandings of significance testing in science read Gerrodette, NOAA National Marine Fisheries Service 2011 Mar Ecol 32 (3): 404

NOTE3 sizes used in this part of the study may have been “similar” to the researchers, but at diameters of 20mm and +66mm (the central disc diameter is for some reason not included in Pisaster"s measurement) for Leptasterias and Pisaster, respectively, the latter is actually more than 4X larger in diameter than the former

Typical disposition of turban snails Tegula funebralis in a west-coast tidepool in the presence an ochre star Pisaster ochraceus. One wonders if anyone has ever compared snails in and out of water, with and without an ochre star present, under such natural conditions as in a tidepool with no experimental manipulations?

Research study 9

Two researchers at Bodega Bay Laboratory and co-authors of RS81 above are one step ahead of the ODYSSEY, in the sense that they have already published a follow-up study on TMIIs (Trait-Mediated Indirect Interactions) in black-turban snails Tegula funebralis conducted, where else?, in the tidepools featured in their first study. Their aim in the present well-designed study is to investigate in more detail food-satiation and body-size effects on intensity of TMIIs, using in this case water-borne scent of predatory sea stars Leptasterias2 spp. - species that routinely prey on Tegula in tidepools in the Bodega Bay region. Results confirm that both freshly collected (presumably well-fed) and well-fed laboratory snails exhibit strong TMIIs when exposed to water-borne scent of Leptasterias. In other words, the snails crawl quickly away, thereby removing grazing pressure from the seaweeds normally eaten. In contrast, snails that have been starved for 1wk in the laboratory and then tested in the tidepools show no TMIIs because they continue to graze3 even in the presence of sea-star scent. With respect to body-size effects, the researchers discover a new “wrinkle” to the already complex TMII trophic cascade. First, small snails newly collected and presumably well-fed, run from the scent but eat so little seaweeds that any TMII effect that they might exert is hardly measureable. Next, newly collected (well-fed) large snails, despite being in size-refuge from predation by the tiny Leptasterias, may still run away, thus creating measureable TMII effects. Finally, some of these large (“safe in size-refuge”) individuals do not run; rather, they stay put and, here comes the wrinkle, continue to graze, but they feed quicker than they would otherwise have done. This becomes is a negative TMII effect, which is a novel and unexpected discovery for the researchers. The authors provide an interesting discussion of the possible significance these findings in the context of the TMII sphere of work. Gravem & Morgan 2016 Funct Ecol 30: 1574; photograph courtesy Sarah Gravem.

NOTE1 for some reason, possibly that their other paper was not yet published, the authors don’t mention it herephotograph of tidepool in Bodega Bay with sea star Leptasterias and prey turban snails Tegula funebralis

NOTE2 species used may be one or other or both of L. aequalis and L. hexactis, a hard-to-distinguish sister-species complex

NOTE3 food in this study is not seaweeds growing naturally on rocks; rather, the experimenters use diatom films that they grow on porcelain tiles in outdoor flow-through tanks. This enables easy and accurate assessment of food consumed. Although they don’t discuss it, the authors would be aware that such tasty nutritious algal food is likely preferred by Tegula over macroalgae. Might this have influences the snails’ choice of whether to stay or leave?

Six-arm sea star Leptasteris sp. in a tidepool with prey black-turban snails Tegula funebralis. Most if not all of the snails and sea mussels Mytilus californianus are in size-refuge from predation by the sea star 0.6X