A test of Brown's principle in the intertidal limpet Collisella scabra (Gould, 1846)

Aim Brown's principle predicts that a species will peak in density near its range centre, and decline gradually towards the margins of its geographical distribution. The decline is assumed to reflect a decrease in individual performance near range margins. I test this abundance–performance hypothesis by comparing patterns in density and size across the northern half of the geographical distribution of the marine patellogastropod Collisella scabra (Gould, 1846). Location Collisella scabra is a high intertidal patellogastropod species distributed along the Pacific coast of North America from Cape Mendocino (CA, USA) to southern Baja California (Mexico). I surveyed 11 research sites spanning c. 36–44° N. Methods In each of the 11 research sites I surveyed four distinct microhabitats, and compared spatial patterns in density and in the size of solitary limpets. Results Both density and size were highly variable across the species range. Density peaked near the northern range margin, and showed greater variance at small spatial scales (< 10 km) than at large scales (> 100 km). In contrast, large size occurred uniformly across the survey area, and size was strongly associated with microhabitat. Main conclusion Collisella scabra does not show spatial patterns of density or performance that are consistent with Brown's principle. The underlying assumptions of Brown's principle may conflict with specific characteristics of C. scabra's life history and/or patterns of environmental variation across its range. Because such conflicts may be common in a large number of marine and terrestrial species, the generality of Brown's principle is questioned.     

Defensive responses of gastropods to the predatory flatworms Freemania litoricola (Heath and McGregor) and notoplana acticola (Boone)

Three species of gastropods were tested in the laboraory and in the field for responses to contact with the polyclad flatworms Freemania litoricola (Heath and McGregor) and Notoplana acticola (Boone). The three limpets differed considerably in their responses to Freemania litoricola All specimens of Notoacmea scutum (Rathke) responded in some way to this flatworm, mostly by running. Fewer than half of the Collisella digitalis (Rathke) responded to Freemania litoricola, and these responded by mushrooming - elevating the shell several millimeters off the substratum. Collisella scabra (Gould) did not respond any differently to contact with Freemania litoricola than to contact with a control probe. Differences in the responses of these limpets to Freemania litoricola are discussed in relation to the characteristic intertidal distributions of this flatworm and the limpets. In contrast to Freemania litoricola, the polyclad Notoplana acticola typically did not elicit defensive responses. This difference is related to the diets of the two flatworms. Freemania litoricola was found to be a predator on limpets, whereas no evidence was found that Notoplana acticola eats limpets.     

Life at the edge: an experimental study of a poleward range boundary

Experimental studies of biogeographic processes are important, but rarely attempted because of the logistical challenges of research at large spatial scales. I used a series of large-scale transplant experiments to investigate the mechanisms controlling species abundance near a poleward range boundary. The intertidal limpet Collisella scabra experiences a 100-fold decline in abundance over the northernmost 300 km of its range. Temperature and food supply both strongly influenced individual survival, growth, and maturation. Regression analysis also revealed significant interactions among these conditions: the effect of one could not be predicted without knowing the level of the other. But these relationships could not explain geographic abundance patterns. Instead, individual limpets were highly successful at sites with relatively low abundance. These results suggest that, even though temperature is important to the success of individual C. scabra populations, the primary effect of warming temperatures under climate change may not be a shift in geographic distribution.     

The effect of a species-specific avoidance response to predatory starfish on the intertidal distribution of two gastropods

Summary The gastropodsAcmaea (Collisella) limatula andAcmaea (Notoacmea) scutum respond to water flowing over certain predatory starfish (i.e. to the scent of the starfish) by moving rapidly up a submerged, vertical surface. These limpets respond with upward movement to the scent ofPisaster ochraceus, Pisaster giganteus, Pycnopodia helianthoides, andLeptasterias aequalis. All of these starfish are predators on molluscs and at least occasionally inhabit the intertidal. In contrast, the limpets respond weakly or not at all to the scent ofPatiria miniata andPisaster brevispinus. Patiria is an omnivorous scavenger, andP. brevispinus is predaceous but strictly subtidal when it occurs on rocky shores. For the starfish tested, then, the limpets only give avoidance responses to starfish species naturally encountered as predators.The avoidance response ofA. limatula andA. scutum to predatory stafish can also be demonstrated in the field. When onePisaster ochraceus is placed beneath a population of limpets in the intertidal and confined so that contacts between the starfish and limpets are impossible, the limpet population is displaced significantly upward after one tidal cycle. In addition, the closer the limpets are to the starfish, the greater is their upward displacement.     

FACTORS GOVERNING PATTERNS OF FORAGING ACTIVITY IN LITTORAL MARINE HERBIVOROUS MOLLUSCS

Relationships of feeding activity to tidal and day/night cyclesin a variety of littoral herbivorous molluscs are reviewed.Most species are active while submerged by the tide, both byday and night. There are also many that are active only whileemersed, with variation in relation to day/night cycles dependentupon micro-habitat. The third pattern is for activity to occurwhile awash by the tide, often with continued feeding whilethe rocks remain damp. Most species in these three groups haveendogenous rhythms. The fourth type is one with no relationto tidal activity, and is confined to supra-littoral and sub-littoralspecies. Major proposed causes of the evolution of these patterns are:desiccation, together with osmotic and thermal stress whichmay have selected for nocturnal activity; dislodgement by waves;and predation by aquatic carnivores, which is often avoidedby feeding at low tide. Of these desiccation and predation arewidely regarded as most important. A study of Patella vulgata suggests that while predation anddesiccation are major factors controlling activity patterns,they do not fully explain observed activity. A discussion ofthe importance of food supply is given, and it is proposed thatwhere competition for food is low, night-time feeding shouldpredominate; where competition is high, day-time feeding shouldpredominate. This pattern fits observations on limpets at LoughHyne, but needs testing in other field situations.     

Defensive responses to predatory seastars by two specialist limpets, Notoacmea insessa (Hinds) and Collisella instabilis (Gould), associated with marine algae

The limpets Notoacmea insessa (Hinds) and Collisella instabilis (Gould), which are associated specifically with certain algae, were tested for defensive responses to seastars. Contact with predatory seastars elicited responses by both species of limpets, in contrast to previous work reporting a lack of defensive responses by specialist limpets associated with plants. Non-predatory seastars normally did not elicit defensive responses. The form of the response by Notoacmea insessa differed, depending on whether the limpet was on or off its grazing scar. When the limpet was off its grazing scar, the most common response was movement away from the point of contact. When on the scar, the limpet usually elevated its shell and rocked from side-to-side, but rarely moved from the scar. The responses of Collisella instabilis almost always involved rapid movement away from the point of contact and tended to be more vigorous than those of Notoacmea insessa.     

Studies on activity pattern of the patellid limpet Cellana toreuma (Reeve)

The habits and activity of Cellana toreuma (Reeve) have been studied in a field population. Activity is very high at ebb and flood tide, independent of the time of day, and sharply decreases during complete submergence or complete exposure. Duration of movement fluctuates with tidal amplitude; when neap tide, movement does not stop during low tide owing to continuous awash conditions. Vertical movement entirely coincides with tidal direction at day and night. In this way, the movement does not depend on light but chiefly the tide. Compared with a nocturnal limpet, C. nigrolineata (Reeve), the divergence in the behavioural patterns may be a function of the extent to which limpets are influenced by light. Duration of movement and distance increase with limpet size. Homing behaviour was not observed.     

Temporal Links in Daily Activity Patterns between Coral Reef Predators and Their Prey

Few studies have documented the activity patterns of both predators and their common prey over 24 h diel cycles. This study documents the temporal periodicity of two common resident predators of juvenile reef fishes, Cephalopholis cyanostigma (rockcod) and Pseudochromis fuscus (dottyback) and compares these to the activity and foraging pattern of a common prey species, juvenile Pomacentrus moluccensis (lemon damselfish). Detailed observations of activity in the field and using 24 h infrared video in the laboratory revealed that the two predators had very different activity patterns. C. cyanostigma was active over the whole 24 h period, with a peak in feeding strikes at dusk and increased activity at both dawn and dusk, while P. fuscus was not active at night and had its highest strike rates at midday. The activity and foraging pattern of P. moluccensis directly opposes that of C. cyanostigma with individuals reducing strike rate and intraspecific aggression at both dawn and dusk, and reducing distance from shelter and boldness at dusk only. Juveniles examined were just outside the size-selection window of P. fuscus. We suggest that the relatively predictable diel behaviour of coral reef predators results from physiological factors such as visual sensory abilities, circadian rhythmicity, variation in hunting profitability, and predation risk at different times of the day. Our study suggests that the diel periodicity of P. moluccensis behaviour may represent a response to increased predation risk at times when both the ability to efficiently capture food and visually detect predators is reduced.     

Manipulation of host behaviour by parasites: ecosystem engineering in the intertidal zone?

Understanding the influence of parasites on the community ecology of free-living organisms is an emerging theme in ecology. The cockle Austrovenus stutchburyi is an abundant mollusc inhabiting the sheltered shores of New Zealand. This species, which lives just few centimetres under the surface, plays a key role for many benthic invertebrate species, because in these habitats the cockle shell is the only available hard surface where invertebrates can establish. However, the behaviour of this cockle can be altered locally by a parasite, the trematode Curtuteria australis. Indeed, heavily infected cockles are unable to bury perfectly and typically lie entirely exposed at the surface of the mud. In this study, we investigated the ecological consequences of this behavioural alteration for two invertebrates species commonly associated with cockles, the anemone Anthopleura aureoradiata and the limpet Notoacmea helmsi. A field study first demonstrated that in both infected and non-infected populations of cockles, there was a negative relationship between the number of anemones and limpets found on cockles. In the laboratory, we showed that predation of limpets by anemones is possible when they share the same cockle shell. In a heavily infected population of cockles, limpets were significantly more frequent and more abundant on cockles manipulated by C. australis than on cockles with a normal behaviour. A colonization test conducted in natural conditions demonstrated that the predominance of limpets on manipulated cockles results from a direct habitat preference. Conversely, anemones were significantly less frequent and less abundant on manipulated cockles than on cockles manipulated by C. australis. A desiccation test revealed that, relative to limpets, they had a lower resistance to this physical stress. We discuss our results in relation to current ideas on ecosystem engineering by organisms.     

The effect of wave action on growth in three species of intertidal gastropods

Summary Populations of the limpets Collisella digitalis and C. scabra, as well as the thaidid whelk Nucella (Thais) emarginata, had greater mean shell lengths at a protected site (Tomales Bay) than at an exposed site (Mussel Point) on the California coast near the Bodega Marine Laboratory. To determine the relative importance of wave action as well as genetic differentiation among populations in explaining this pattern, tagged snails of all three species were reciprocally transferred between the two sites. For C. digitalis, total wet mass (tissue plus shell) increased by 34.4% at the protected site, but decreased by 2% at the exposed site over a two and one-half month period. For C. scabra, growth was 43.1% at the protected, and 2.7% at the exposed site, and for Nucella, 9.5% and 1%, respectively. Although some evidence of population differentiation was found, particularly for the direct-developing whelk, source differences in growth were not as large as the site effect. At least for the whelk, absolute differences in barnacle prey abundances did not occur between sites. However, all three gastropods had higher abundances at the exposed site. While factors such as genetic differentiation and competition may partially explain why gastropods are on the average smaller at exposed sites, we suggest that wave action may also play a role, possibly by limiting time available for feeding, and therefore energy available for growth. Although wave action, acting via size-specific mortality, has been suggested to limit the size that consumers can reach on exposed shores, it may also indirectly affect intertidal gastropod populations by altering foraging behavior, growth and life histories.     

Alternative Responses to Predation in Two Headwater Stream Minnows Is Reflected in Their Contrasting Diel Activity Patterns

Animals exhibit diel periodicity in their activity in part to meet energy requirements whilst evading predation. A competing hypothesis suggests that partitioning of diel activities is less important because animals capitalise on opportunity. To test these hypotheses we examined the diel activity patterns for two cyprinid minnows, chubbyhead barb Barbus anoplus and the Eastern Cape redfin minnow Pseudobarbus afer that both occur within headwater streams in the Eastern Cape, South Africa. Chubbyhead barbs exhibited consistent nocturnal activity based on both field and laboratory observations. Due to the absence of fish predators within its habitat, its nocturnal behaviour suggests a response to the cost associated with diurnal activity, such as predation risk by diving and wading birds. In contrast, redfin minnows showed high diurnal activity and a shoaling behaviour in the wild, whereas, in the laboratory, they showed high refuge use during the diel cycle. Despite their preference for refuge in the laboratory, they were diurnally active, a behaviour that was consistent with observations in the wild. The diurnal activity of this species suggests a response to the cost associated with nocturnal activity. Such a cost could be inferred from the presence of the longfin eel, a native predator that was active at night, whereas the daytime shoaling behaviour suggests an anti-predator mechanism to diurnal visual predators. The implications of these findings relate to the impacts associated with the potential invasions by non-native piscivores that occur in the mainstem sections. Diurnal activity patterns for redfin minnows, that are IUCN-listed as endangered, may, in part, explain their susceptibility to high predation by visual non-native piscivores, such as bass and trout. In contrast, the nocturnal habits of chubbyhead barbs suggest a probable pre-adaptation to visual predation. The likelihood of invasion by nocturnally-active sharptooth catfish Clarias gariepinus, however, may compromise this prior advantage.     

Positive and Negative Effects of Habitat-Forming Algae on Survival,Growth and Intra-Specific Competition of Limpets

Understanding the effects of environmental change on the distribution and abundance of strongly interacting organisms, such as intertidal macroalgae and their grazers, needs a thorough knowledge of their underpinning ecological relationships. Control of grazer-plant interactions is bi-directional on northwestern European coasts: grazing by limpets structures populations of macroalgae, while macroalgae provide habitat and food for limpets. Scottish shores dominated by the macroalga Fucus vesiculosus support lower densities and larger sizes of limpets Patella vulgata than shores with less Fucus. These patterns may be due to differences in inter-size-class competitive interactions of limpets among shores with different covers of Fucus. To examine this model, densities of small and large limpets were manipulated in plots with and without Fucus. Amounts of biofilm were measured in each plot. The presence of Fucus increased survival but hindered growth of small (15 mm TL) limpets, which were negatively affected by the presence of large limpets (31 mm TL). In contrast, large limpets were not affected by the presence of Fucus or of small limpets. This suggests the occurrence of asymmetric inter-size-class competition, which was influenced by the presence of macroalgae. Macroalgae and increased densities of limpets did not influence amounts of biofilm. Our findings highlight the role of interactions among organisms in generating ecological responses to environmental change.     

Desiccation of intertidal limpets: Effects of shell size,fit to substratum,and shape

For undisturbed, field populations of the northeast Pacific, intertidal limpet Collisella pelta (Rathke), water loss was found to be proportional to apertural circumference rather than mantle cavity surface area. This contrasts with previous laboratory measurements for other limpet species and emphasizes the importance of the fit of shell to substratum for non-homing limpets. This close fit maintained a meniscus of water between the edge of the shell and the substratum, thereby reducing evaporative surface area and increasing the advantage of large size for reducing the rate of water loss. Shell-raising behavior eliminated the meniscus, increasing the rate of desiccation, and water loss appeared to become proportional to mantle cavity surface area. Indirect evidence suggests that C. pelta may utilize shell-raising behavior for evaporative cooling under thermally stressful conditions in the field.Both shell size and shape affect the ratio of water stores (proportional to internal shell volume) to evaporative surface area (proportional to apertural circumference) and per cent water loss is, potentially, a function of this ratio. Shape, however, (when defined as volume/circumference) exhibits an average allometric increase with increasing size (volume) for C. pelta, as well as for three other sympatric limpet species: C. Paradigitalis (Fritchman), C. Digitalis (Rathke), and Notoacmea scutum (Rathke). An independent measure of shape is, therefore, required to separate shape effects on desiccation from size effects; this measure was obtained by rearranging the allometry equation. In contrast to significant size effects, no measurable effect of shape on desiccation was detected. Variation in limpet shell shape may be partially or wholly maintained by factors other than an adaptational response to desiccation.     

Demography, competitive interactions and grazing effects of intertidal limpets in southern New Zealand

Population dynamics and the effects of intraspecific competition on limpet growth and maintenance of bare patches were investigated for the intertidal limpet Cellana ornata (Dillwyn) at a boulder-dominated site and on a rocky platform near Kaikoura (South Island), New Zealand. Distribution and abundance patterns of C. ornata were described in relation to other biota and tidal height. C. ornata occurred almost exclusively in patches devoid of macroalgae, particularly in the mid-tidal zone. Both adult and juvenile limpets were most abundant on the tops of boulders, where their numbers were positively correlated with barnacle cover, which averaged 77%. The size structure and growth patterns of C. ornata were different between populations. Mark-recapture studies showed that the slopes of annual growth increments regressed on initial sizes were similar at both sites but that the annual increments on the platform were about 6 mm greater than on boulders. Growth virtually ceased at 27 mm for limpets at the barnacle-dominated boulder site and at 40 mm at the platform site. Recruiting cohorts had 20% survival on boulders and 37% on the platform during their first year. The largest size classes at both sites had around 57% annual survival. To test the effects of varying limpet densities on the growth and mortality of limpets and the maintenance of bare patches, densities of C. ornata were experimentally increased at both sites. Beyond a density of 4 per 0.25 m², sizes and survival of limpets were reduced at both sites, but the effect was more pronounced at the boulder site. Limpets at the boulder site were more effective at maintaining bare space than those on the reef platform. Enclosing limpets in plots with and without barnacles showed that C. ornata and a co-occurring species (Cellana denticulata (Martyn)) grazed more effectively and had greater growth in cleared plots. Overall, there was considerable variation in the demographics of C. ornata between populations driven by site-specific characteristics.     

Predation by small mobile aquatic predators regulates populations of the intertidal limpet Patella vulgata (L.)

Highly mobile aquatic predators are known to forage in the intertidal during periods of immersion. There is limited quantitative information, however, on the extent to which these predators influence the abundance of grazing molluscs which are known to have a key role in structuring intertidal assemblages. Our preliminary video observations revealed that crabs and small fish were abundant on shores in southwest England during high-tide. We then used manipulative experiments to quantify the effect of small mobile aquatic predators on the abundance of limpets (Patella vulgata L.). On the lower shore at two moderately sheltered rocky shores three treatments were established: complete cage, partial cage (cage control) and uncaged (natural condition). The complete cages excluded all predators. The partial cage treatment allowed full access to small predators and the uncaged treatment allowed access to all predators. After two months, limpet abundance in uncaged and partial cage treatments had declined by around 50% compared to the complete cage treatment. Population structure also changed with survival of larger individuals being greater than smaller individuals in the open and partial cage treatments compared to the complete cage treatment. The effects of excluding predators were consistent at small (meters) and large spatial scales (kilometres) and hence, it would appear that the outcomes of our research are generally applicable to similar shores in the region.To explore the mechanism behind the differential effects of predators according to prey size, we compared the detachment force required to remove limpets of differing sizes from the shore. This was around four times greater for larger individuals than for smaller ones indicating that smaller limpets were more vulnerable to predation. These effects were also consistent between locations. Subsequent laboratory observations showed that the crabs Carcinus maenas (L.), Necora puber (L.) and Cancer pagurus (L.) which are locally abundant predators of limpets, had differing handling behaviour but were all highly efficient at removing limpets from substratum. Hence, shell width and attachment force appeared to be critical factors influencing the vulnerability of limpets to predation by these crabs. Limpets are known to control the abundance of macroalgae on shores in the North-east Atlantic and so our conclusions about the role of mobile predators in regulating the abundance of these grazers are important to our broader understanding of the ecology of these shores.     

Host selection and larval interactions among three primary parasitoids ofPlathypena scabra (Lep.: noctuidae)

Three hymenopteran parasitoids that attackPlathypena scabra (F.) larvae often oviposit into consecutive instars of the host. We investigated host discrimination by adults and competitive interactions among larvae of these three parasitoid species. Avoidance of superparasitism byCotesia marginiventris (Cresson) andDiolcogaster facetosa Ashmead was tested. Females of each species were presented either withP. scabra parasitized by a different female of the same species 6 h earlier or unparasitizedP. scabra. Under these conditions,C. marginiventris attacked similar numbers of parasitized and unparasitized hosts.D. facetosa attacked 31% fewer parasitized than unparasitizedP. scabra. The avoidance of multiple parasitism byD. facetosa was studied in a similar bioassay. AlthoughD. facetosa females parasitized fewerP. scabra that had been attacked byC. marginiventris 6 h previously, the reduction in parasitism was only about 23%. In competition studies, immatureD. facetosa were better competitors than immatureC. marginiventris. Aleiodes (=Rogas) nolophanae (Ashmead) was an inferior competitor against bothC. marginiventris andD. facetosa when the duration between parasitism events was 1 h, but their competitive ability increased when they multiply parasitized hosts at least 32 h after the initial oviposition.     

Endogenous rhythms of locomotion in the American horseshoe crab, Limulus polyphemus

American horseshoe crabs (Limulus polyphemus) exhibit clear circadian rhythms of visual sensitivity in the laboratory and in the field they exhibit seasonal patterns of mating behavior that are closely associated with the tides. Recent reports suggest that Limulus locomotor activity may be controlled by endogenous circadian and/or circatidal clocks and that light:dark (LD) cycles may affect the rhythmic output of both of these clocks. In this study, we examined locomotor behavior in the laboratory to determine the extent of this endogenous activity and to examine the influence of LD cycles on these rhythms. Thirty-three L. polyphemus were captured during the breeding season and their activity was monitored with activity boxes and “running wheels” in seawater kept at constant temperature and salinity. Activity patterns were analyzed using visual inspection of actograms and Chi-square and Lomb-Scargle periodograms. Overall, 36% of the animals was significantly more active during L, while only 12% was more active during D (52% showed no preference). Circatidal rhythms were observed in LD in 67% of the horseshoe crabs. Surprisingly, LD cycles appeared to synchronize these rhythms at times. In DD, the majority of animals tested (63%) exhibited circatidal rhythms that persisted for at least seven days. Overall, the results demonstrate that an endogenously controlled tidal rhythm of locomotion operates during, and significantly after, the breeding season in this species. In addition, the present results are consistent with the presence of circalunidian oscillators controlling these rhythms.     

Antifouling activity of bioactive substances extracted from Holothuria scabra

Methanol extract of Holothuria scabrawas tested for antifouling activity using `mollusc foot adherence bioassay'. It was found that the secondary metabolites of H. scabraeffectively prevented foot adherence of P. vulgataat various concentrations. Based on the present findings it could be inferred that the bioassay guided purification and fractionation may give forth potent novel antifouling compounds.     

Video analysis of predation by polyphagous invertebrate predators in the laboratory and field

This paper describes field and laboratory time-lapse video analyses of the behavioral responses of the groups: Arachnida: Acari, Araneae, and Opiliones; Myriapoda: Chilopoda; Hymenoptera: Formicidae; Crustacea: Isopoda; and Coleoptera: Staphylinidae to live eggs of the brown blowfly, Calliphora stygia F. (Diptera: Calliphoridae), used as factitious prey in two contrasting agricultural field margins and in the laboratory. Field video results showed that predation by mites was greatest in tree-lined boundaries while centipede numbers and activity were greater in post-and-wire boundaries. All except Staphylinidae showed clear diurnal patterns of activity and egg predation rate over the 12 h recording period. Based on the number of eggs removed, number of eggs examined, predator numbers, and predator activity, three indices were formulated that allowed predator groups to be ranked according to their effectiveness as predators. Commensal interactions between the mites and harvestmen, mediated via mite-pierced eggs, were suggested from field data and confirmed in the laboratory. Phalangium opilio preferred to feed on both manually and mite-pierced compared with untreated eggs, but showed a stronger preference for manually pierced ones than mite-pierced, consuming six times as many over the same period. This is the first demonstration of a commensal interaction between two agroecosystem predators. If commensalism is common in agroecosystems it could increase the effectiveness of biological control. It may also need to be incorporated within theoretical models and may complicate the extrapolation of laboratory-based feeding studies to field situations.