Differential Post-settlement Mortality Research Articles

Thermal tolerance of Crepidula fornicata (Gastropoda) life history stages from intertidal and subtidal subpopulations

MEPS Marine Ecology Progress Series Contact the journal Facebook Twitter RSS Mailing List Subscribe to our mailing list via Mailchimp HomeLatest VolumeAbout the JournalEditorsTheme Sections MEPS 486:173-187 (2013) - DOI: https://doi.org/10.3354/meps10355 Thermal tolerance of Crepidula fornicata (Gastropoda) life history stages from intertidal and subtidal subpopulations Casey M. Diederich*, Jan A. Pechenik Biology Department, Tufts University, Medford, Massachusetts 02155, USA *Email: casey.diederich@tufts.edu ABSTRACT: The ability to withstand high summer temperatures is an extremely important determinant of species distributions in the intertidal zone; most marine organisms cannot live intertidally because of the harsh conditions experienced during aerial emersion. The members of some species, though, live both intertidally and subtidally, and their physiological tolerance to stressors may differ depending on their genetic connectivity, acclimatization, and differential postsettlement mortality. Furthermore, tolerances of organisms at different life-history stages within both habitats may differ and will play an important role in determining adult distributions. To determine the effect of habitat and life-history stage on physiological tolerance and the likely contribution of upper thermal tolerance limits to the native distribution of an important invasive species, the slippershell snail Crepidula fornicata, we compared the thermal tolerance of intertidal and subtidal embryos and adults in relation to conditions that they experience in the field. We found C. fornicata living both intertidally and subtidally in Bissel Cove, Rhode Island, where they experienced drastically different thermal conditions. Intertidal individuals achieved body temperatures as high as 42°C, more than 15°C higher than those recorded in subtidal conspecifics. However, subtidal individuals had remarkably high thermal tolerances that were nearly identical to those of intertidal conspecifics (lethal range = 33-37°C following a 3 h exposure). Furthermore, embryos were even more tolerant to high thermal stress than adults. These results are surprising: the few previous studies that have compared thermal tolerances among individuals at different life-history stages have found differences among them, and early stages are generally more sensitive than adults. Interestingly, the markedly higher temperatures that intertidal animals experienced in this study had little effect on their thermal tolerance. Intertidal (but not subtidal) slippershell snails are now living dangerously close to their upper thermal limits and will almost certainly be relegated to the subtidal as global temperatures rise. KEY WORDS: Intertidal · Subtidal · Crepidula · Thermal stress · Physiological tolerance Full text in pdf format PreviousNextCite this article as: Diederich CM, Pechenik JA (2013) Thermal tolerance of Crepidula fornicata (Gastropoda) life history stages from intertidal and subtidal subpopulations. Mar Ecol Prog Ser 486:173-187. https://doi.org/10.3354/meps10355 Export citation RSS - Facebook - Tweet - linkedIn Cited by Published in MEPS Vol. 486. Online publication date: July 12, 2013 Print ISSN: 0171-8630; Online ISSN: 1616-1599 Copyright © 2013 Inter-Research.

Cannibalism and inter-specific predation in early stages of intertidal crab species that compete for refuges

Most benthic species with dispersive life stages suffer high mortality rates in hours to days following settlement. Predation exerted by other species and predation by self (cannibalism) are commonly the chief sources of post-settlement mortality and can profoundly influence population dynamics and adult spatial distribution. In Chile, two predatory crab species (Acanthocyclus gayi and Acanthocyclus hassleri) coexist in the intertidal zone. Both settle preferentially in mussel beds, but adults show remarkable spatial segregation, apparently as a result of asymmetric competition for refuges. Although early recruits of A. gayi are an order of magnitude more abundant than A. hassleri, late juveniles are similarly abundant. Recruits of A. gayi are probably subjected to higher mortality before competition for refuges intensifies. Here, through laboratory experiments, we quantified the strength of intra and inter-cohort cannibalism and inter-specific predation as probable sources of differential post-settlement mortality. Intra-cohort cannibalism (among recruits of same size) accounted for the mortality of up to 30% of recruits in both species, with no evidence of density-dependent effects on mortality. Rates of cannibalism between juveniles and recruits (inter-cohorts) were also similar between the two species. Both species exhibit type III functional responses of juvenile predators with a tendency to consume heavily upon the most abundant recruits (A. gayi in the field), which could potentially provide A. hassleri recruits with a “virtual refuge” from the inter-cohort predation in the field. The combination of these different sources of mortality might contribute to the large reduction in abundance of A. gayi recruits by the time they reach juvenile stages. Our results illustrate the complexity of mechanisms that can underlay patterns of distribution and relative abundances among competitors through different life stages, especially among coexisting species in which attacking peers can provide higher rewards later in development than just the energy obtained from other food.

The importance of larval supply, larval habitat selection and post-settlement mortality in determining intertidal adult abundance of the invasive gastropod Crepidula fornicata

Understanding the processes that drive the recruitment of invasive non-native species is of critical importance in evaluating their potential to colonise previously unoccupied habitats. The slipper limpet Crepidula fornicata has spread rapidly into most European waters since its first introduction from the North West Atlantic in the late 19th century. Its invasion success is thought to have been aided by its long larval phase and its tolerance towards a wide range of environmental conditions. The Milford Haven Waterway in Wales, U.K. supports a population with highly variable densities in the intertidal as well as the subtidal zone. In the present study, we tested a series of existing models to investigate the roles of larval supply, larval habitat selection and post-settlement mortality in determining the final distribution of C. fornicata in the intertidal zone of the Milford Haven Waterway. During the main reproductive season of 2011, data on total settlement rates and recruitment were collected by deploying slate panels for varying durations in the low intertidal zone, and data on larval abundances were obtained by taking frequent plankton samples at two sites with contrasting adult densities: Beggars Reach (~15±13indm−2) and Pennar (~343±360indm−2). Total larval densities were much higher at Pennar, but densities of late-stage larvae (i.e. larval supply) were similar at both sites, indicating that local hydrodynamics may have resulted in the spatial homogenisation of supply of late-stage, metamorphically competent larvae, despite the higher larval production at the high adult abundance site. Settlement rates also did not differ between sites. Seasonal recruitment was overall low, indicating that post-settlement mortality, likely as a consequence of exposure to intertidal conditions, is very high. The lack of a relationship between adult abundance and settlement rates indicates that the final distribution of C. fornicata in the intertidal may be a result of differential post-settlement mortality. Understanding recruitment patterns in non-native species is essential for developing management strategies for potentially harmful invaders such as C. fornicata.

Larval habitat selection, not larval supply, determines settlement patterns and adult distribution in two chthamalid barnacles

Summary 1. Two common species of acorn barnacle, Chthamalus montagui and C. stellatus , with similar resource needs, occur together on rocky shores of NW Europe but differ in their adult distribution over two environmental gradients, wave exposure and vertical height on the shore. 2. A sampling programme was undertaken over 2 years to determine the causal mechanisms of this differential distribution. Three alternative, although not mutually exclusive, models were tested: first, adult distribution is determined at settlement as a direct result of differential larval supply; secondly, adult distribution is determined at settlement as a result of larval choice rather than differential larval supply; and thirdly, settlement occurs homogeneously over the two gradients and the adult pattern is set by differential post-settlement mortality. 3. Near-shore larval abundance in the water column over the gradient of wave exposure was determined at eight dates during the main settlement period in 2003. Larval production was assessed by quantifying early-stage larvae, while the supply of competent settlers to the adult habitat was determined by quantifying late-stage cyprid larvae. 4. The pattern of settlement of the two species was determined over both environmental gradients by daily sampling of the proportional abundance of C. stellatus and C. montagui settled cyprids at three tidal heights at exposed and sheltered shores. Differential post-settlement mortality was determined by quantifying day-old, week-old and up to 3 months-old metamorphosed individuals. 5. Larval production reflected the distribution of adults, with early-stage larvae of C. montagui predominating in shelter and C. stellatus in exposure. However, the supply of late-stage cyprid larvae to the near-shore area showed no difference in the proportion of each species over the wave-exposure gradient; differential larval supply was not responsible for dictating adult distribution. 6. Despite no differential supply of larvae, the pattern of settlement of the two species differed over both environmental gradients, with C. stellatus settling in greater proportions low on the shore and in exposure and C. montagui settlement predominating higher on the shore and in shelter. This pattern directly matched the distribution of adults. Postsettlement mortality accentuated, but did not change, the pattern set at settlement. 7. The implications of the results, and the usefulness of the technique employed, to understanding the degree of ‘openness’ in populations of marine benthic invertebrates are discussed.

Recruitment in the intertidal limpet Lottia digitalis (Patellogastropoda: Lottiidae) may be driven by settlement cues associated with adult habitat

The ribbed limpet, Lottia digitalis, is found high in rocky intertidal habitat throughout its geographic range. In order to identify likely natural settlement locations for larvae of this species, laboratory-reared larvae were settled onto substrata collected from within and near an adult L. digitalis habitat. Of larvae exposed to rock chiseled from within high-intertidal adult habitat, 31.0% and 23.3% underwent metamorphosis during two separate experiments. Similarly, an unidentified filamentous green alga that was isolated from this rock induced metamorphosis in 26.6% and 8.7% of larvae during additional experiments. In contrast, larvae did not metamorphose upon bare rocks or upon rocks encrusted with a crustose corraline alga (CCA) that were collected from lower intertidal zones, nor did they metamorphose upon the macroalgae Ulva sp., Enteromorpha contorta, Alaria marginata, or Polysiphonia sp. The presence of mucus from adult conspecifics during these experiments did not enhance metamorphosis onto rock taken from adult habitat, but it did induce metamorphosis in an average of 13.5% and 7.0% of larvae introduced to the mid-intertidal bare rock and CCA substrata, respectively. Finally, 38.0% and 34.4% of larvae from two experiments underwent metamorphosis when exposed to the high-intertidal barnacle Pollicipes polymerus. These results suggest that larval settlement, rather than differential post-settlement mortality and/or migration, drives recruitment of L. digitalis in high-intertidal habitats.

Modelling processes that generate and maintain coral community diversity

This study addresses why adjacent sites on coral reefs are different, why some places support so few coral species, and how human impacts are affecting coral community dynamics and ultimately diversity. The paper includes a brief review outlining what theory tells us and how that theory relates to empirical data. A metapopulation and a metacommunity model are introduced. The metapopulation model can be used to predict a species' probability of site occupancy and the metacommunity model can be used to predict the number of species supported at any one site. The models identify the primary mechanisms that generate and maintain local (10s m2–10s km2) coral diversity based on a regional (100s km2) perspective. Local diversity appears regulated by differential post-settlement mortality that in turn leads to local extinction of some species. Indeed, harsh local environments cause high levels of local extinction and these environments support few coral species.

Are vertical distribution patterns of scleractinian corals maintained by pre- or post-settlement processes? A case study of three contrasting species

Vertical zonation of hard corals in tropical coral reef systems is a well documented and predictable pattern in the organisation of tropical coral communities. However, the mechanisms that underly vertical zonation of hard corals are poorly understood. Two alternative conceptual models for the maintenance of vertical zonation are considered; depth-dependent settlement of larvae, or indiscriminant settlement of larvae with distributions determined by differential post-settlement mortality with depth. These alternative models were evaluated by undertaking field translocation experiments using 10 d old juveniles of 3 species with contrasting adult distributions: Goniastrea aspera (Verrill)-restricted to shallow reef fiat habitats; Oxypora lacera (Verrill)-restricted to low light, lower slope habitats; and Platygyra daedalea (Ellis and Solander)-a species with a broad depth range. Laboratory-raised larvae of each species were settled onto terracotta settlement plates and the plates translocated to 3 depths in the field: reef flat (0 m), mid slope (5 m), lower slope (10 m). Survival of the laboratory-settled juveniles was monitored at 3, 6 and 12 mo after settlement. For each of the 3 species, juveniles survived equally well at all 3 depths over the 12 mo study period. The pattern of survivorship of G. aspera and P. daedalea among depths, however, was dependent on plate surface (top, bottom). Given the absence of depth-dependent survival of juveniles from the 2 zone-specific species G. aspera and O. lacera, we reject the hypothesis that adult distribution patterns of these 2 species is determined by indiscriminant settlement of larvae followed by differential early post-settlement mortality with depth.

The Importance of Larval Choice and Hydrodynamics in Creating Aggregations of Hydroides elegans (Polychaeta: Serpulidae)

The Importance of Larval Choice and Hydrodynamics in Creating Aggregations of Hydroides elegans (Polychaeta: Serpulidae)

Enhanced settlement on microtopographical high points by the intertidal red alga Halosaccion glandiforme

The early colonization patterns of the red alga Halosaccion glandiforme (Gmel.) were examined on artificial substrata cast from molds of both real (e.g. barnacles) and model surfaces with and without surface “roughness” at the scale of 100–1,200 µm. Settlement over a 3‐d period was always at least 35 times higher on rough substrata than on smooth substrata. This difference was due to the high (84–98%) settlement of spores on the tips of individual small‐scale surface projections (i.e. the roughness elements). An outplanting experiment suggested that the greater abundance of sporelings on the tips of surface projections resulted from settlement processes rather than differential postsettlement mortality. When sporeling densities were compared at larger spatial scales (e.g. areas near the base of the substrata vs. areas near the top), they varied greatly on smooth substrata, with highest densities found near surface transitions (e.g. corners and edges). On rough surfaces, the sporelings were more evenly distributed among the various areas. Thus, smaller scale features (i.e. 100–1,200 µm) of the surface appear to be more important than larger scale features (1–2 cm) in determining the settlement of H. glandiforme.

Settling barnacle larvae avoid substrata previously occupied by a mobile predator

Settlement by the larvae of the barnacle Balanus glandula (Darwin) in the field is decreased on slate tiles that have been previously occupied by a predator of postmetamorphic stages, the whelk Nucella lamellosa (Gmelin). Settlement by another barnacle species, Semibalanus cariosus (Pallas), was not as greatly influenced by the same treatment. The effect on B. glandula also occurs when the substratum is treated with traces of the whelk by either forcing the foot over the plate or rubbing the plate with crushed individuals. This reduction in settlement can persist up to 3 wk after treatment of the substratum. A similar but lesser effect occurs after treatments with traces of a potential biological disturber of settling larvae, the limpet Tectura scutum (Rathke), but also occurs with mucus from the brown alga Fucus distichus (L.), which is not a demonstrated hazard to the barnacles. Mucus is naturally released by all of the above organisms and may be the cause of the reduced settlement. Control manipulations using a nonraucus-producing animal tissue, the pectoral muscle of the chicken Gallus gallus (L.), produced only a slight decrease in barnacle settlement. Mucus could reduce settlement either by acting as a cue for avoidance of high-risk areas, altering other settlement cues, or physically inhibiting attachment. However, not all mucus inhibits settlement: another investigator demonstrated that prior occupation by another predatory whelk induced greater settlement by another barnacle species; and we found that mucus from the dorid nudribranch Archidoris montereyensis (Cooper) increased settlement by B. glandula. Thus, our results suggest that the mucus might possibly act as a cue to the larvae, and we conclude that traces of mobile animals can influence the settlement of sessile animals. Since the threat of whelks to barnacles is delayed until some time after settlement, we hypothesize that the barnacle may be taking into account the long-term future risks (i.e., “the ghost of predation future”) when making the decision to settle. The avoidance response of the barnacle to the traces of limpets and macroalgae offers an alternative explanation (differential settlement) to patterns often attributed to biological disturbance (differential postsettlement mortality).

Interactions between the vermetid Serpulorbis squamigerus (Carpenter) and several species of encrusting bryozoans

Along the southern California coast the vermetid gastropod Serpulorbis squamigerus (Carpenter) frequently recruits onto encrusting cheilostome bryozoans. On experimental substrates 93% of 599 individuals observed recruited onto either the five dominant cheilostome species or the shells of resident juvenile Serpulorbis. Serpulorbis recruitment also varied significantly among the dominant bryozoans. These recruitment patterns were found to result from differential postsettlement mortality as well as from selective settlement of larvae. The longevity of vermetids was also found to differ among substratum types, principally from an increase in the probability of surviving to 3 months of age on bryozoan substrates. No positive or negative effects of this relationship could be found for the bryozoans. By differentially recruiting onto bryozoans the vermetid: (1) aggregated for reproduction while avoiding competition for food with adult conspecifics; and (2) decreased juvenile mortality possibly by an avoidance of competition or by being camouflaged from predators. This relationship was judged to be facultative commensalism.