title for learn-about section on whelks & relatives in A SNAIL'S ODYSSEY
  Habitat & community ecology
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  Agents of community structure
  Topics in this diverse section include agents of community structure, considered here, and SHELL MORPHOLOGY & HABITAT, SHORE-LEVEL SIZE GRADIENTS, and DEMOGRAPHY & HABITAT COMPLEXITY considered in other sections. The research studies are presented chronologically below.
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Research study 1

schematic showing predation effects of whelks on distributions of prey barnaces on west-coast shoresThe idea of refuges, that is, places or situations providing safety from predators, is developed in an early study of predation on barnacles Balanus glandula, Chthamalus dalli, and Semibalanus cariosus by whelks Nucella lamellosa, N. canaliculata, and N. ostrina in the San Juan Islands, Washington.  The whelks effectively eliminate B. glandula from the lower zone.  Upper-zone B. glandula, however, survive in spatial refuge, and this breeding population yearly provides colonisation stock for the middle and lower zones.  In effect, settlement below the refuge zone constitutes fodder for the predators, and their numbers are sufficient to eat all B. glandula from the lower shores each year.  The whelks are setting the lower limits of distribution of B. glandula. Because of the dependability of this food supply, a special niche at the upper shore levels is created for Nucella ostrina.  This species lives somewhat higher on the shore than the other 2 Nucella species. Lower limits of Nucella ostrina are set, in part, by the absence of their prey barnacles lower down the shore, likely a consequence of competition for food with the other Nucella species, but predation by sea stars and crabs is also implicated.  Nucella ostrina is smaller-sized and thinner-shelled than the other whelk species, and is more vulnerable to being eaten by red-rock crabs Cancer productus

Experiments at Friday Harbor Laboratories, Washington show that, when given a choice, these crabs overwhelmingly prefer the thinner-shelled N. emarginata to the thicker-shelled N. lamellosa.  Immature Nucella lamellosa are thin-shelled and vulnerable to predation by Cancer, so how do they survive in the lower parts of the shore where intensity of crab predation is high?  The answer may partly be that the crabs seem to ignore the small-sized whelks.  As well, the author notes that temporal and spatial fluctuations in crab numbers may provide relief. Sea stars Pisaster ochraceus also eat the whelks but, in comparison with C. productus and other crabs that prowl throughout the high-shore zone during high tides, the sea stars are mostly limited to lower-zone activities.  

Although thatched barnacles Semibalanus cariosus are eaten by Nucella spp. when the barnacles are smaller and thinner-shelled, they soon reach a refuge in size when their plates thicken beyond the ability of a whelk to drill and eat them in a single high-tide cycle.  The receding tide may leave the predator “high and dry”, and seasonal conditions of heat/drying/cold may cause it to abandon its feeding efforts and seek shelter.  Size refuge is reached by Semibalanus after only 1-2yr of growth.  The plate thickness of the barnacle is itself not the obstacle to Nucella depredation.  If whelks and Semibalanus are caged together at subtidal levels the barnacles are readily drilled and eaten.  Connell 1970 Ecol Monogr 40: 49.

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Research study 2

graph showing growth rates of whelks Nucella spp. on prey barnacles Balanus glandula over 5 months of summer/autumnAspects of interspecific competition for food are part of a later comprehensive study at Friday Harbor Laboratories, Washington on the biology of west-coast Nucella spp.  Basically, the research question follows from earlier work on the same topic (see Research Study 1 above); that is, how do 3 apparently similar whelk species coexist utilising a common food source of barnacles Balanus glandula?  In the laboratory, growth rates of N. lamellosa, N. ostrina, and N. canaliculata are similar on a diet of B. glandula, the food specimens collected from a single source population, thus demonstrating that the prey species is potentially good for growth of all Nucella spp. (see accompanying graph). The author’s thesis, however, is that B. glandula does not have the same nutritional quality at all intertidal positions.  Thus, because growth, settlement intensity, and survival of B. glandula all decrease in an upshore direction, the prey really exists in 2 forms - a higher level one used by N. ostrina and a lower level one used by N. lamellosa.  Although N. canaliculata overlaps these distributions and potentially competes with the other species, it is able to exploit another prey species, Semibalanus cariosus.  Spight 1981 Res Popul Ecol 23: 245.

NOTE the data shown for late summer/autumn may not be the best to illustrate the authors contention, as all species are actually losing weight. This is a time of gonad production leading up to copulation and egg-laying in autumn/winter

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Research study 3

photograph of mud snail Cerithidea californica courtesy Dave Cowles, Walla Walla University, WashingtonMost research on community dynamics of intertidal snails on the west coast relates to predatory whelks Nucella spp. However, introduction of the related eastern mud snail Ilyanassa obsoleta into the San Francisco Bay region of California over a century ago created a large-scale natural experiment involving an endemic mud snail Cerithidea californica.  Studies in the Palo Alto region at the south end of the Bay show that Ilyanassa is outcompeting the native mud snail in mutually preferred tidal creek and mudflat habitats, and forcing it into less desirable marsh-pan habitats.  The exclusion involves interference competition, with Cerithidea avoiding contact with Ilyanassa or remaining withdrawn as Ilyanassa crawls over them, and active predation by Ilyanassa on eggs or photograph of mud snails lyanassa obsolete eating a dead sculpinjuveniles of Cerithidea.  Other possible explanations for the exclusion, such as barriers to dispersal (unlike Ilyanassa, Cerithidea has no pelagic larval phase), and species-specific predation and parasitism, are discussed by the authors and discounted.  It appears that Ilyanassa is intolerant of the summer heat and drying on the marsh pans that are now the only refuge for Cerithidea.  Each year, following winter dormancy by both species, Cerithidea attempts to re-invade the creek habitats but is repulsed by the more dominant Ilyanassa.  The authos notes that this is the first documented case of the competitive exclusion of an endemic marine intertidal species by an introduced ecological equivalent.  Race 1982 Oecologia 54: 337. Photograph courtesy Dave Cowles, Walla Walla University www.wallawalla.edu.

NOTE  the snails are thought to have arrived in shipments of eastern oysters Crassostrea virginica during the period 1901-1907

Several mud snails Ilyanassa obsoleta
feeding on a dead sculpin 0.5X

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Research study 4

The effects of predation by whelks on intertidal community structure varies both with region and over time.  On mid-intertidal shorelines of Oregon coasts where beds of sea mussels Mytilus californianus are predominant (50-70% cover), patches within the beds and below them are inhabited by dense aggregations of whelks Nucella canaliculata and N. ostrina.  The role played by these whelks in the Oregon mid-intertidal community is assessed in a 25-mo study using predator-exclusion cagesThe experiment described here is part of a larger study which also includes experiments in which densities of whelks within cages are varied at different times.  The second part of the study is important for an understanding of how temporal changes in predation intensity affect community structure, especially with regard to spatial heterogeneity in mid-intertidal ecosystems but, unfortunately, is too detailed to include here.  Percentage cover in the cages of 7 major species is monitored at 1-2mo intervals.  Results show:



legend for graphs dealing with whelk-exclusion study in Oregon

graph showing effect of excluding whelks Nucella spp. on percentage cover of mussels Mytilus trossulus

1. a large and immediate increase in cover of bay mussels Mytilus trossulus occurs in the absence of the whelks.

graphs showing effects of excluding whelks Nucella spp. on percentage cover of mussels Mytilus californianus and goose barnacles Pollicipes2. removal of all whelks has little effect on density of sea mussels Mytilus californianus and goose barnacles Pollicipes polymerus, species not preyed upon much by whelks in this region.  Towards the end of the study, however, there is a small but unexplained increase in cover of mussels, and a larger, also unexplained, increase in cover of goose barnacles.

graph showing effects of removal of whelks Nucella spp. on percentage cover of barnacles Chthamalus
3. there are variable effects on % cover of barnacles, perhaps associated with cage effects. Shown here: C. dalli.
graph showing effect of removal of whelks Nucella spp. on percentage cover of barnacles Balanus
4. cover of Balanus glandula decreases from 60% to almost 0% by the end of the study period.
graph showing effects of removal of whelks Nucella spp. on percentage cover of thatched barnacles Semibalanus cariosus
5. effects on barnacles Semibalanus cariosus are also highly variable. Note the relatively strong cage effects seen here, as seen also for Chthamalus dalli.
graph showing effects of removal of whelks Nucella spp. on percentage cover of sea anemones Anthopleura xanthogrammica
6. cover of sea anemones Anthopleura xanthogrammica increases, an indirect effect of absence of whelks leading to more mussels, and thus to more space for the anemones to live.


food web of Oregon shore communityThe schematic on the Right shows a summary of interactive effects of selected members of the Oregon shore community, determined by path analysis of the above data. NOte that a minus value denotes negative effects, for example, barnacles eaten by the whelks, while a positive value denotes a facilitative effect, usually relating to space.  The author's summary:

Nucella spp.:  whelks eat both types of mussels and also barnacles, and thus have direct negative effects on their numbers.

Mytilus trossulus: because their byssus threads provide settling substrata for larvae of sea mussels; thus, the bay mussels facilitate the recruitment of Mytilus californianus.  Later, the larger and thicker-shelled sea mussels replace the bay mussels and come to dominate the mussel clumps.  Therefore, by removing bay mussels, M. trossulus, the whelks have an indirect negative effect on sea mussels M. californianus.
Barnacles:  because their shell plates provide sites for settling larvae of bay mussels, barnacles facilitate the recruitment of Mytilus trossulus.  And, by removing barnacles, the whelks indirectly affect numbers of both types of mussels by removing another useful settlement substratum.  Also, by removing the larger barnacle species, the whelks can potentially, and indirectly, increase the survival the smaller competitively inferior barnacle .Chthamalus dalli.

M. californianus: increase in density of sea mussels M. californianus directly provides space within the bed for sea anemones to live. In their absence, the whelks indirectly affect the recruitment of sea anemones Anthopleura xanthogrammica to the community. Navarrete 1996 Ecol Monogr 66: 301.

NOTE  the cages are 20 x 20 x 5cm in size, constructed of stainless steel bolted to the substratum, and are of 3 types:  experimental, in which all whelks are removed; control, in which the normal complement of whelks are included (densities of whelks in the area range from 10-50 individuals per sq m); and cage control, each of which consists of a roof only.  This last control attempts to monitor cage artifacts, that is, effects arising from the cages themselves, including shading, disruption of currents, effects on whelk behaviour, and so on

NOTE  as an example, percentage cover of Chthamalus dalli unexpectedly increases towards the end of the study in the cage controls

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Research study 5

photographs of horn snails Cerithidea californica and a main predator, the shor crab Pachygrapsus crassipesThe health and welfare of horn snails Cerithidea californica on mudflats in California depends upon a balance between “top-down” predation effects from shore crabs Pachygrapsus crassipes and “bottom-up” nutritional effects from amount of microalgae available as food.  The question of how these factors interact is addressed in a study by University of California, Los Angeles researchers through a series of cage experiments done on a tidal mud/sand-flat in Mugu Lagoon, California.  The researchers deploy twenty 0.5 x 0.5m  fiberglass-mesh containment cages on the flats, then populate half of them with normal densities of crabs (4 per cage), and leave the other half crabless. All cages contain normal densities of snails.  To half of all cages they add phosphate/nitrate fertilizers in pellet form (Osmocote) to stimulate growth of diatoms and cyanobacteria that comprise the snails’ main diet.  The researchers hypothesise that the crabs will have both direct and indirect effects on the snails, the first by consuming them and the second, by reducing food availability through their burrowing activities. After a period of 5wk the following results are obtained.  Where crabs and snails are present 85% of the snails are consumed, but there is no concomitant increase in benthic microalgae even in cages with augmented nutrient levels. In fact, microalgal biomasses actually decrease by 50-80%, likely because of bioturbation caused by the crabs burrowing activities.  In treatments without crabs, snails increase in size by up to 20%.  However, in cages without crabs but with added nutrients, snail mortality unexpectedly increases, possibly owing to increased growth of poor-quality/toxic cyanobacteria.  Overall, the authors conclude that top-down impacts of P. crassipes generally reduce bottom-up effects of nutrients, but  what is additionally disclosed by the experiments is a much more complex community structure than first supposed.   Armitage & Fong 2006 Mar Ecol Progr Ser 313: 205. Photographs courtesy EPA, University of California Davis, and Kevin Lafferty.

NOTE  other experiments are done to test for cage effects


Horn snails Cerithidea californica in normal density on a California
mudflat (0.3X) with shore crab Pachygrapsus crassipes (1X)

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Research study 6

photograph of oyster drill Urosalpinx cinerea courtesy Jose and Marcus Coltro - Femorale.comIf non-indigenous species are introduced into a community and are successful, does that assume they cause only nominal disruption to existing food webs, or are they more likely to disrupt things in major ways?  To investigate this, researchers based mainly at University of California, Santa Cruz compare effects on trophic cascades in Tomales Bay, California of 2 non-invasive species with effects of 2 invasive species.  In areas of the Estuary dominated by native crabs Cancer antennarius (the top consumers) and native whelks Acanthinucella spirata (the intermediate consumers), with native oysters Ostrea conchaphila as the major prey, the oysters suffer low and sustainable mortality. However, in nearby areas dominated by non-native oyster drills Urosalpinx cinerea and green crabs Carcinus maenas, basic food webs are disrupted and native-oyster mortality is high and possibly unsustainable. Field experiments involving manipulation of densities of the invasive oyster drills show that oyster mortality is causally linked to density of the drills, and not to stresses of desiccation, photograph of Acanthinucella spirata courtesy Kaustov Roytemperature, or salinity.  Other experiments in laboratory mesocosms indicate that it is interaction between native crabs and native whelks that maintains the oyster populations.  The native crabs both consume the native whelks and alter their behaviour.  Thus, when native species occupy the top and intermediate trophic levels, the oysters indirectly benefit from density- and trait-mediated cascades. In contrast, non-native oyster drills are naïve to the crabs and fail to avoid them, thus restricting their invasion into areas where native crabs are present.  If, however, native crabs are replaced in mesocosms with smaller-sized invasive crabs that have a naïve foraging strategy to either species of intermediate consumer, the snails are inefficiently consumed, and native-oyster populations are depleted.  The study is large, well-designed and analysed, and contributes greatly to our understanding of how invasive species can alter trophic interactions; this brief summary does not do justice to it. Kimbro et al. 2009 Oecologia 160: 563. Photographs courtesy Kaustov Roy (Left) and Jose & Marcus Caltro (Right).

NOTE  the direct consumption is known as density-mediated trophic cascade, while the alteration of behaviour is termed trait-mediated trophic cascade

Acanthinucella spirata 3X

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Research study 7

photograph of several Littorina sp. in an empty barnacle testgraph showing relationship between empty barnacle test and density of littorinid snails Littorina sp.Predation by whelks Nucella ostrina on acorn barnacles Balanus glandula and Chthamalus dalli leaves the empty barnacle tests as a favourable microhabitat for colonisation by other organisms, such as littorinid snails Littorina plena and various algae (see photo). Studies by researchers at Bodega Marine Laboratory, California show that humidity is higher within the barnacle tests than outside during low-tide periods, and additionally the tests may provide refuge from predators and wave action. Preference by the littorinids is for the larger tests of  B. glandula (see graph), and density of the  littorinids actually increases out of proportion with availability of empty tests because several individuals can shelter within a single test.  Field experiments involving exclusion cages (whelks, either 2 or 8mo in duration) and manipulation of empty-test availability show that littorine density is significantly increased by the whelk’s predatory activity.  Another finding by the researchers is that preferential predation by the whelk on the larger and more nutritious B. glandula permits greater settlement and survival of the smaller, less preferred, and competively inferior C. dalli.  Now, what happens to the system if whelk densities increase?  Based on other studies on whelks, one might expect the whelks to switch their preferences to the smaller Chthanalus and, when this resource becomes in short supply, to move, perhaps temporarily, to an alternative food source such as mussels.  Interestingly, a model developed by the researchers predicts that the number of available empty tests will increase with predation intensity up to a point, but then decline at an intermediate level of predation when barnacle densities become severely reduced. The non-linear effect predicted by the model represents a significant finding, and the authors discuss several possible explanations for it.  Harley & O’Riley 2011 Oecologia 166: 531.

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