Chemical mediation of invertebrate defensive behaviors and the ability to distinguish between foraging and inactive predators

When the predatory sea star Pycnopodia helianthoides was placed upstream, the sea urchin Strongylocentrotus purpuratus responded defensively by extending and opening its globiferous pedicellariae. No pedicellaria response was given in control seawater or when the sea star was downstream. The snail Tegula funebralis responded by moving up vertical surfaces when Pycnopodia helianthoides or when Pisaster ochraceus were placed upstream. When these sea stars were introduced downstream, the snail's response was not significantly different from that in control seawater. Water collected from an aquarium containing a single sea star was sufficient to trigger the response of S. purpuratus and T. funebralis; the physical presence of the sea star was not essential. This indicated that a chemical stimulus was involved, and the lack of responses when sea stars were downstream argued strongly against the possible additional involvement of visual or vibrational stimuli. S. purpuratus gave stronger pedicellaria responses to water flowing over an active Pycnopodia helianthoides than to water flowing over the same sea star when it was inactive. The significance of the ability to distinguish between actively foraging and inactive predators is discussed, and a mechanism is proposed to explain differences in the amount of stimulatory chemicals released by active and inactive sea stars.     

Feeding ecology of a size-structured predator population,the South American sun-star Heliaster helianthus

Patterns of feeding in a population of Heliaster helianthus (Lamarck), a common and dominant species of starfish indigenous to the Pacific South American coast, were investigated in an intertidal habitat in central Peru from October 1986 to April 1987. The H. helianthus population comprised individuals of 3.5 to 30.2 cm body size (diameter) with two modal size classes. The number of rays ranged between 18 and 40, and individuals with 31 to 33 rays accounted for ca. 42% of the total population. There was a higher rate of increase in ray number with body size amongst small individuals(<13.0 cm diam). H. helianthus is capable of feeding on more than one prey item at a time (average of 5.6 to 13.2 prey items handled, with several predators observed to hold >100), and both the number of prey individuals captured and the total prey biomass were significantly correlated with predator size. Amongst a total of 1132 feeding observations, the largest number of predators (an average of 85.4% of those feeding) were preying on the mussel Semimytilus algosus whilst another mussel, Perumytilus purpuratus, ranked second with 21,9% of predators feeding. The proportion of S. algosus in the diet increased from 65.4% in the smallest predator size-group (10.9 cm diam) to 91.2% in the largest (19.0 cm). In contrast, P. purpuratus and barnacles were more highly represented in the diet of small H. helianthus. The smallest size-group (10.9 cm) had low dietary overlap with larger sizes and less specialized prey utilization. Two geographically separated populations of H. helianthus in Peru and Chile showed contrasting patterns of prey utilization. S. algosus and P. purpuratus comprised 85.5 and 6.5% by number in the diet of the Peruvian population, respectively, whilst corresponding figures for the Chilean population were 8.3 and 60.5%, with barnacles attaining a higher share (22.6%). However, the total number of prey individuals per feeding predator was almost the same in Peru and Chile, with 10.0 and 10.7 individuals, respectively. H. helianthus individuals of different sizes occupy slightly different microhabitats within the intertidal area, which, coupled with differential spatial distribution of prey species, results in the predator population being able to utilize a wide range of resources.     

Enlarged lantern size in similar-sized,sympatric, sibling species of Strongylocentrotid sea urchins: from phenotypic accommodation to functional adaptation for durophagy

Strongylocentrotus droebachiensis is a well known omnivorous sea urchin with an unrivalled capacity to destroy North Atlantic kelp forests. S. pallidus is a lesser known, morphologically similar, and closely related species with no record of destructive grazing, despite its larger lantern size. I quantify the lantern size of both species using bivariate allometric analysis, and test the hypothesis that enlarged lantern size facilitates durophagy, the consumption of hard prey, by measuring the feeding capacity of urchins with different lantern sizes when offered a hard-shelled prey, the blue mussel, Mytilus edulis. The results suggest that S. droebachiensis has a limited capacity for durophagous feeding irrespective of lantern size, whereas in S. pallidus the ability to exploit hard shelled prey is positively related to lantern size. This is apparently the first evidence of a relationship between trophic morphology and diet in regular sea urchins. The hypothesis of systematic latitudinal variation in the lantern size of S. pallidus is reappraised and rejected. S. droebachiensis had larger gonads than S. pallidus in field samples, confirming that its small lantern is not impeding nutrient acquisition in shallow habitats.     

Predators of juvenile sea urchins and the effect of habitat refuges

We evaluated the effects of potential predators from intertidal habitats on Strongylocentrotus purpuratus survival using laboratory experiments and assessed abundances of main predatory species along the Pacific coast of North America. The interactive effects of urchins’ and predators’ sizes in mediating predation were quantified. Habitat complexity (substrate pits, adult spine canopy) was manipulated to examine its effects on predation of most susceptible individuals (<14 mm). Pachygrapsus crassipes was identified as a major predator of urchins up to ≈30 mm. A positive effect of predator size on consumption of progressively larger urchins was detected, probably due to a mechanical limitation on crabs’ ability to consume large prey. Larger claws of males with respect to females of comparable sizes facilitated the handling of larger prey. Substrate refuges significantly reduced mortality on juvenile urchins. These results show that crab predation may be important in organizing intertidal communities, despite multiple ecological mechanisms promoting sea urchin survival.     

Effects of predators on sea urchin density and habitat use in a southern California kelp forest

Grazing sea urchins can reduce kelp abundance and therefore strongly affect kelp forest community structure. Despite the ecological importance of sea urchins, direct field studies on the role that urchin predators play in shaping urchin populations are rare for southern California. We conducted surveys and manipulative experiments within kelp forests near San Diego, CA, (32–51′28″N, 117–16′00″W) from 2006 to 2009 to determine whether predators such as sheephead (Semicossyphus pulcher) and spiny lobsters (Panulirus interruptus) may be linked to purple urchin (Strongylocentrotus purpuratus) and red urchin (Strongylocentrotus franciscanus) distribution and habitat use, as well as purple urchin density-dependent mortality. Purple urchins were less dense and more cryptic inside a local marine protected area (MPA) that contained high predator abundance than in nearby heavily fished areas, whereas red urchins rarely were found outside the MPA. Urchin proportional mortality was inversely density dependent during the day when sheephead were active, despite fish aggregations in plots of high urchin density, but was density independent during the night when lobsters were active. Urchin mortality was reduced under understory algal cover during the day, but not during the night. Examining whether urchin mortality from predation is density dependent and how habitat complexity influences this relationship is imperative because behavioral changes and increases in urchin populations can have vast ecological and economic consequences in kelp forest communities.     

Juvenile–adult associations in sea urchins ( Strongylocentrotus franciscanus and S. droebachiensis ): protection from predation and hydrodynamics in S. franciscanus

Juvenile red sea urchins, Strongylocentrotus franciscanus, aggregate under adult conspecifics, whereas sympatric juvenile green sea urchins, Strongylocentrotus droebachiensis, are typically more solitary and dispersed. Neither the potential advantage of juvenile sheltering nor the differences in post-settlement behavior between the two species has been demonstrated experimentally, but may be related to protection from predators and/or hydrodynamics. In predation experiments, juvenile vulnerability differed in the two species as the seastar Pycnopodia helianthoides consistently chose juvenile S. franciscanus over S. droebachiensis (100% vs. 0%). When associated with adults, juvenile mortality decreased dramatically in S. franciscanus (90% alone vs. 5% with adults), but very little in S. droebachiensis (85% vs. 75%). Not surprisingly, juvenile behavioral responses in the two species reflect this difference in vulnerability. Juvenile S. franciscanus sheltered under adults when predation risk was high, but not when risk was low (44% vs. 13%), whereas sheltering in S. droebachiensis was infrequent and not related to predation risk (7% for high risk versus 5% for low risk). From a hydrodynamic perspective, the presence of an adult led to the creation of a hydrodynamic refuge for juveniles, where average water velocities were reduced by > 60% around the adult urchin. Again, striking differences in sheltering rate were apparent in S. franciscanus (52% vs. 13% for high flow and low flow, respectively), but not S. droebachiensis (5% for high flow versus 4% for low flow). Sheltering behavior was also species-specific as juveniles did not shelter at high rates under adults of the opposite species (≤ 16%). A field survey confirmed these finding in that juvenile S. franciscanus abundance was associated with both adults and water motion (R ² = 0.80, P = 0.008, best-subsets regression). These results suggest that sheltering confers juvenile S. franciscanus with a degree of protection from predators and water motion, and that species-specific differences in this post-settlement behavior may be related to the differences in the protection afforded by adults.     

Improving escape responses of hatchery-reared scallops <Emphasis Type="Italic">Argopecten purpuratus</Emphasis>

Hatchery rearing of the scallop Argopecten purpuratus has resulted in successive generations of scallops not exposed to predators that are less sensitive to and escape more slowly from predators than wild scallops. The present study examined whether conditioning hatchery-reared A. purpuratus to its natural predator, the sea star Meyenaster gelatinosus, improved its escape responses. Both juvenile and adult A. purpuratus from Tongoy Bay, Chile, were exposed for 7 days to different conditions: (1) continuous predator odor, (2) predator contact for 30 min three times a day, (3) a combination of the two previous conditions, and (4) no exposure to the predator (control). After conditioning, we evaluated scallop’s escape responses: reaction time, total clap number, duration of the clapping response, clapping rate, and the time scallops spent closed when exhausted. Conditioning with contact and odor plus contact (i.e., high predation risk) resulted in 25 and 50% shorter reaction times of juveniles and adults, respectively. Further, these stimuli caused juveniles to increase the number of claps and clapping rate. For adults, the time spent closed after exhaustion decreased by 50 and 63% after conditioning with contact and odor plus contact, respectively. Therefore, it is shown for the first time that exposure of scallops to increasing predator stimuli enhances escape responses, evidence of threat-sensitive predator avoidance.     

Energetics of early development for the sea urchinsStrongylocentrotus purpuratus andLytechinus pictus and the crustaceanArtemia sp.

Embryos and larvae of two species of sea urchin,Strongylocentrotus purpuratus andLytechinus pictus, and larvae of the brine shrimpArtemia sp. (San Francisco brand) were cultured to investigate the contribution of dissolved organic material in seawater to the energetics of early development. When embroys ofS. purpuratus were reared in artificial seawater, a net loss in dry organic mass was observed. In contrast, when sibling embryos were reared to Day 2 under identical conditions in natural seawater, there was either a net increase in dry organic mass or no change. A net decrease in mass was observed in only one of five cultures reared in filtered natural seawater. Energy budgets for each species were determined by giving energy equivalents to the changes in carbohydrate, lipid and protein, and to the rate of oxygen consumption for each day of development. In the case ofS. purpuratus, the use of endogenous reserves accounted for either 0 or 38% of the metabolic demand for two independent cultures reared from Days 0 to 2. For larvae ofL. pictus, reared to 8 d, only 66% of the metabolic demand could be accounted for by the use of endogenous reserves. Sea urchins are capable of transporting dissolved organic material from seawater. Calculations revealed that the energy deficit during the early development of sea urchins (S. purpuratus) could be accounted for by the uptake of dissolved organic matter from seawater. However, for a species that cannot use this resource (Artemia sp.), the metabolic needs during development are supplied through the use of endogenous reserves.     

Settlement and recruitment of sea urchins (Strongylocentrotus spp.) in a sea-urchin barren ground and a kelp bed: are populations regulated by settlement or post-settlement processes?

I sampled recruitment of very small sea urchins (Strongylocentrotus spp.) by using the anesthetic magnesium chloride to remove individuals from substrata collected in sea-urchin barren grounds (barrens) and kelp beds at Naples Reef near Santa Barbara, California, USA. Preliminary sampling found low numbers of newly settled individuals(<0.6 mm test diam) from April–July in 1984 and 1985, and in April, 1986. In early May, 1986, I found many newly settled seaurchins (0.3 to 0.6 mm, 5 to 17 d old), and I compared the densities of the cohort on several types of natural substrata in barrens and kelp-bed habitats. Newly settled individuals of both purple sea urchins (S. purpuratus) and red sea urchins (S. franciscanus) were present in similar, high densities (1 000 S. purpuratus m^-2) on foliose red algal turf, a dominant substratum ofthe kelp bed, and on crustose coralline algae, the dominant substratum of an adjacent barrens. Larvae of S. purpuratus reared and tested in the laboratory showed high rates of settlement on both red algal turf and on crustose coralline algae, but significantly lower rates on rock. Larvae also settled in response to a partiallypurified extract of coralline algae. The reduced settlement on natural rock surfaces relative to either algal treatment and the significant settlement in response to the extract of coralline algae indicate that larvae discriminate between natural substrata and probably respond to a settlement cue other than, or in addition to, a simple microbial (bacterial) film. The similar densities of young recruits of S. purpuratus on dominant substrata of barrens and kelp bed show that, at least in this case, differential settlement cannot explain the high densities of sea urchins in the barrens habitat. Movement between barrens and kelp bed is unlikely given the small sizes of the newly recruited sea urchins relative to the large distances often involved. Reduced post-settlement mortality of newly settled individuals in the barrens remains the most likely mechanism leading to the higher densities of sea urchins in barrens relative to kelp-bed habitats.     

Movement patterns of the seastar Heliaster helianthus in central Chile: relationship with environmental conditions and prey availability

The rates and patterns of feeding and displacement of predators constitute two of the most important plastic behavioral responses that allow individuals to respond quickly to changes in abundance of their prey, predation risks and to rapid alterations in environmental conditions. In this study, we quantified seasonal and spatial variation in displacement (net changes in location in 12 or 24 h periods) and prey consumed of marked individuals of the keystone seastar Heliaster helianthus at six sites spanning 600 km along the coast of north-central Chile. We evaluated the hypotheses that: (1) at sites with low availability (cover) of the main prey, the mussel Perumytilus purpuratus, Heliaster displays larger displacements and consumes a greater proportion of other prey (e.g. mobile species) than at sites with high mussel cover, (2) daily displacements will be correlated with sea surface temperature (SST) and (3) increased wave action will reduce seastar daily displacement. Our results show that Heliaster displacement is higher at sites with lower availability of P. purpuratus; and at these sites, a larger proportion of Heliaster individuals are observed feeding, mostly on other prey (e.g. limpets), which could offset the higher costs associated with increased movement. In addition, wave forces affected the activity of Heliaster negatively. Contrary to our expectations, the daily displacements did not show any relationship with SST measured on the day or the previous days of the surveys, despite the fact that average displacement was generally higher in summer than in winter months. Future studies should examine Heliaster movement during single foraging excursions and determine whether these responses affect the growth and reproductive output of individuals. Such information is vital to understand how changes in prey abundance and environmental conditions alter the behavior and energy budget of this predator and its ability to control prey populations.     

Effects of grazing by two species of sea urchins (Strongylocentrotus franciscanus and Lytechinus anamesus) on recruitment and survival of two species of kelp (Macrocystis pyrifera and Pterygophora californica)

We studied the effects of grazing by two species of sea urchins on two species of kelp (Macrocystis pyrifera and Pterygophora californica) in the San Onofre kelp bed in southern California from 1978 through 1981. Both red sea urchins, Strongylocentrotus franciscanus, and white sea urchins, Lytechinus anamesus, were abundant and lived in aggregations. The purple sea urchin (S. purpuratus) was rare at the study site and was not studied. The aggregations of red urchins were either relatively small and stationary (for over 3 yr) or relatively large and motile (advancing at about 2 m mo^–1). Both stationary and moving aggregations were observed at the same time, and within 100 m of one another. Stationary aggregations of red urchins probably subsisted mainly on drift kelp and had no effect on kelp recruitment or on adult kelp abundance. In contrast, red sea urchins in large, motile aggregations or fronts ate almost all the macroalgae in their path. The condition of their gonalds indicated that red urchins in fronts were starved relative to red urchins in the small, stationary aggregations. Large, motile aggregations developed after 2 yr of declining kelp abundance (probably due largely to storms). We propose that a scarcity of drift algae for food results in a change in the behavior pattern of the red urchins and thus leads to the formation of large, motile aggregations. The aggregations of white urchins, which occurred along the offshore margin of the kelp bed, were large, but relatively stationary. The white urchins rarely ate adult kelps, but grazed extensively on early developmental stages of kelps and evidently prevented seaward expansion of the bed. The spatial distribution of both types of red urchin aggregations appeared to be unrelated to predation pressure from fishes or lobsters.Please address all requests for reprints to the senior author at his present address.     

Predation by the epipelagic heteropod mollusk Carinaria cristata forma japonica

In surface waters off Southern California (USA), Carinaria cristata forma japonica van der Spoel, 1972 feeds on a variety of zooplankton, although thaliaceans, chaetognaths, and copepods predominate numerically in the diet. Feeding intensity is greatest on the most abundant of two species of thaliaceans, depending on which one dominates in the plankton at the time. Some cannibalism occurs, with the prey being about one half the size of the predator. Feeding intensity is greatest during the day, possibly because heteropods depend on vision to locate prey and because prey species are more available by day. Comparisons of the proportion of each prey species in the diet and in the plankton indicate preferential feeding on thaliaceans, chaetognaths, and mollusks; in contrast, crustaceans and especially the copepods are non-preferred prey. These preference patterns may reflect differences among prey species in the ability to escape capture. Predator and prey size are positively correlated for Doliolum denticulatum gonozoids and oozoids, Thalia democratica aggregates, and Sagitta spp. Smaller individuals of D. denticulatum gonozoids and Sagitta spp. are selectively preyed on, resulting in size refuges for larger individuals.     

Crushing predation of the spiny star Marthasterias glacialis upon the sea urchin Paracentrotus lividus

Literature data report that only fish predators are able to crush sea urchin tests in Mediterranean rocky reefs. This experimental study showed that the spiny star Marthasterias glacialis is able to break Paracentrotus lividus tests and that the breaking event is more likely to occur for small-sized sea urchins than for big ones. Our results show that the role of M. glacialis in regulating P. lividus population density can be important in specific locations. They may have important implications, moreover, for the use of tethering techniques aimed at identifying predator types of sea urchins.     

Stomach contents and size-frequency distributions of two coexisting sea star species,Astropecten aranciacus and A. bispinosus,with reference to competition

Stomach contents of the sea star species Astropecten aranciacus (L.) and A. bispinosus (Otto) consisted of roughly the same sort of prey, mostly bivalves and irregular sea urchins. However, the two predators ingested prey of different size classes. The stomach contents of A. bispinosus reflected the size distribution of the benthic macrofauna, while larger prey was more frequent in the stomach contents of A. aranciacus. As the density of prey in the investigated area is low, A. aranciacus and A. bispinosus are likely to compete for food. Possible mechanisms reducing the effect of competition are discussed.     

Severe storm disturbances and reversal of community structure in a southern California kelp forest

Regular observations made over a period of 5 yr in four permanent transects provided data on plant, sea urchin, and fish densities which indicate that two unusually severe winter storms in 1980 (Storm I) and 1983 (Storm II) had different effects on a southern California kelp-forest community. Storm I removed all canopies of the giant kelp Macrocystis pyrifera, but spared most understory kelps, mainly Pterygophora californica. Hence, the previously large accumulation of detached drift kelp, mostly M. pyrifera, disappeared. Denied their preferred diet of drift kelp, the sea urchins Strongylocentrotus franciscanus and S. purpuratus then emerged from shelters to find alternative food. Without effective predators, they consumed most living plants, including the surviving understory kelps. This weakened the important detritus-based food chain, as indicated indirectly by declining abundances of algal turf and fish (Embiotocidae) that eat small animals living in turf. In 1983, Storm II reversed the process by eliminating exposed urchins, while clearing rock surfaces for widespread kelp settlement and growth. By summer 1984, the kelp grew to maturity to form extensive canopies despite elevated water temperatures during summer and fall of 1983. Thus, severe storms may have vastly different effects on community structure, depending on the state of the community before the disturbance.     

Turning the game around: toxicity in a nudibranch-sponge predator–prey association

Escalation theory proposes enemy-related selection as the most relevant factor of natural selection among individual organisms. When hazardous to predators, prey might be considered enemies that influence predator evolution. Opisthobranch molluscs that prey on chemically defended prey are an interesting study case on this subject. Predation on chemically defended species paved the way for opisthobranchs to enter in an arms race, developing means to detoxify and/or excrete harmful compounds, which led to the sequestration of those compounds and their self-defensive use, an escalation of defenses. Here we aim to understand whether the opisthobranch predator is better protected than its chemically defended prey, using as predator–prey model, a nudibranch (Hypselodoris cantabrica) and the sponge it preys upon (Dysidea fragilis), and from which it obtains deterrent chemical compounds. Specimens of both species were collected on the Portuguese coast, and their crude extracts were analyzed and used in palatability tests. Nudibranchs revealed a higher natural concentration of crude extract, probably due to a progressive accumulation of the compounds. Both predator and prey extracts revealed similar mixtures of deterrent metabolites (furanosesquiterpenes). Palatability tests revealed a more effective deterrence in the nudibranch extracts because significant rejection rates were observed at lower concentrations than those necessary for the sponge extracts to have the same effect. We concluded that the predator is chemically better protected than its prey, which suggests that its acquisition of chemical defenses reveals a defensive escalation.     

Foods and predators of the green sea urchin Strongylocentrotus droebachiensis in Newfoundland waters

Gut analyses of the green sea urchin Strongylocentrotus droebachiensis (O. F. Müller) demonstrated that perennial phaeophytes, mostly fucoids and Alaria esculenta, were predominant in the diet. Ephemeral species, coralline algae and animals, were consumed in smaller amounts when available. Grazing by the urchins is evidently responsible for the dearth of non-coralline sublittoral algae in Newfoundland waters. Lobsters, rock crabs, purple sea stars, other urchins, and a variety of fishes and birds feed on S. droebachiensis, but predation is apparently not effective in limiting the abundance of the urchin.Studies in Biology from the Memorial University of Newfoundland No. 234.Contribution from the Marine Sciences Research Laboratory No. 66.     

Feeding and nutritional ecology of the sea urchin strongylocentrotus drobachiensis in Maine,USA

The sea urchin strongylocentrotus drobachiensis exhibited a high degree of food selectivity, whether foods were presented singly or in combination. Foods ranked from most to least preferred were, in summer, Laminaria longicruris, Chondrus crispus, Corallina officinalis, Ascophyllum nodosum, and Agarum cribrosum, whereas in winter A. nodosum and A. cribrosum exchanged ranks. Food preference was not correlated with caloric content but, because of higher feeding rates on preferred foods, caloric intake was positively correlated with preference. Similarly, food absorption rankings were not correlated with food preference, with the exception of gravimetric efficiencies in winter. However, the absorption of L. longicruris, the most preferred alga, was highest in all measurements. Growth and reproductive development of S. drobachiensis on single species diets were positively correlated with food preference. Highest values occurred with animals fed L. longicruris. Urchins transferred from non-preferred to preferred diets showed increased somatic and reproductive growth compared to control animals on the original, non-preferred diets. Conversely, when transferred from preferred to non-preferred diets, urchins showed reduced growth compared to controls. No combination diet tested supported significantly better gonadal growth than L. longicruris: 25% C. crispus supported slightly better somatic growth than L. longicruris alone. These data support the view that S. drobachiensis has evolved a feeding strategy resulting in the maximization of growth and reproduction.     

Sequestration of dietary secondary metabolites by three species of sea hares: location,specificity and dynamics

We examined the location of squuestered secondary metabolites in three species of sea hares, Stylocheilus longicauda, Dolabella auricularia, and Aplysia californica (Opisthobranchia: Anaspidea). The sea hares ate a natural diet or were fed an artificial diet containing secondary metabolites in the laboratory. In all three species, sequestered secondary metabolites were located almost exclusively in the digestive gland, an internal organ, rather than in the exterior parts of the body, in eggs, or in ink (released when sea hares are disturbed). S. longicauda, a specialist sea hare, was able to sequester measur-able amounts of all six algal metabolites offered (caulerpenyne, halimedatetraacetate, pachydictyol A, malyingamides A and B, and ochtodene) and two (luffariellolide and Dysidea spp. brominated diphenyl ether) of three sponge metabolites offered (chondrillin was not sequestered). Malyngamides A and B, found in the host plant of S. longicauda, were sequestered at high, but not unique concentrations. D. auricularia, a generalist sea hare, was fed caulerpenyne, pachydictyol A and malyngamide B; patterns of sequestration of these three compounds did not differ markedly between S. longicauda and D. auricularia. S. longicauda did not lose measurable amounts of malyngamides after 18 d on a malyngamide-free diet. These results suggest that sea hares have generic mechanisms for sequestering algal metabolites rather than mechanisms that are tightly linked to particular compounds, that these mechanisms do not differ dramatically between species, and that sequestered secondary metabolites are not located optimally for defense.