Settlement behaviour of marine invertebrate larvae measured by EthoVision 3.0

Submerged marine surfaces are rapidly colonized by fouling organisms. Current research is aimed at finding new, non-toxic, or at least environmentally benign, solutions to this problem. Barnacles are a major target organism for such control as they constitute a key component of the hard fouling community. A range of standard settlement assays is available for screening test compounds against barnacle cypris larvae, but they generally provide little information on mechanism(s) of action. Towards this end, a quick and reliable video-tracking protocol has been developed to study the behaviour of the cypris larvae of the barnacle, Balanus amphitrite, at settlement. EthoVision 3.0 was used to track individual cyprids in 30-mm Petri dishes. Experiments were run to determine the optimal conditions vis-a-vis acclimation time, tracking duration, number of replicates, temperature and lighting. A protocol was arrived at involving a two Petri dish system with backlighting, and tracking over a 5-min period after first acclimating the cyprids to test conditions for 2 min. A minimum of twenty replicates was required to account for individual variability in cyprid behaviour from the same batch of larvae. This methodology should be widely applicable to both fundamental and applied studies of larval settlement and with further refinements, to that of smaller fouling organisms such as microalgae and bacteria.     

A robotic molecular method for in situ detection of marine invertebrate larvae

Knowledge of the temporal and spatial abundance of invertebrate larvae is critical to understanding the dispersal capabilities and recruitment potential of marine and aquatic organisms. Traditional microscopic analyses are time-consuming and difficult given the diversity of larval species and a frequent lack of discriminating morphological characteristics. Here, we describe a sensitive rRNA targeted sandwich hybridization assay (SHA) that uses oligonucleotide probes to detect and enumerate the larvae of invasive green crabs (Carcinus maenas), native blue mussels (Mytilus), native barnacles (Balanus) and polychaetes (Osedax and Ophelia) that occur in the Monterey Bay National Marine Sanctuary, California. Laboratory-based assays demonstrate specificity, high sensitivity, and a quantitative response to cultured samples from three of the target organisms. Oligonucleotide probes were then printed in arrays on nitrocellulose membranes and deployed in our robotic Environmental Sample Processor (ESP) to detect larvae in situ and autonomously. We demonstrate that the SHA-detection method and ESP robot can be used for near real-time, in situ detection of larval species in the marine environment.     

Effect of mytilan on the UV-radiation resistance of marine invertebrate larvae and human lymphocytes

The effect of UV irradiation on the state of marine invertebrate larvae (a bivalve mollusk and a sea urchin) and human peripheral blood lymphocytes was investigated in the presence of mytilan, a polysaccharide isolated from the mussel Crenomytilus grayanus. This polysaccharide exhibited UV-protective activities in each of the tested model systems. The preincubation with mytilan markedly reduced the negative effects of UV irradiation: the viability of marine invertebrate larvae was enhanced, the occurrence of their morphological abnormalities decreased, the number of viable lymphocytes increased, and the basic parameters of physiological activity of lymphocytes became normal.     

Seasonal variation in the effects of hard substratum biofilming on settlement of marine invertebrate larvae

The effect of season on "biofilming";, as a cue for the settlement of marine invertebrate larvae, was investigated in a long-term field study during the years 1992-1994. The series of settlement experiments was conducted in a tidal rapid on the west coast of Scotland, and involved manipulations of artificial panels. Biofilming of substrata, whilst excluding larval settlement, was achieved by the enclosure of panels within tight-fitting (but removable) mesh screens so that the number of settlers on filmed and unfilmed substrata were counted in the initial absence of other incumbent post-larvae. Depending on larval species, the effects of biofilming were found to be either facilitatory or inhibitory. Significant within- and between-species seasonal differences in the settlement responses were detected, and a reversal of the effect of biofilming on larval settlement response, from inhibitory to facilitatory and vice versa, was noted with season in the case of some taxonomic groups and species (e.g. Tubulipora sp., Plagioecia sp., Electra pilosa (L.)). The present study emphasizes the need for extended field studies of larval responses to environmental cues, when the focus of interest is in drawing general inferences about naturally occurring behavioural patterns at settlement.     

Size-specific protection against predation by fish in swarming waterfleas,Bosmina longispina

When feeding on non-swarming waterflea prey, sticklebacks, Gasterosteus aculeatus, selected larger items. However, when feeding on swarming prey, the fish fed mainly at the edges of the swarms and smaller items were consumed. This selection of small prey items can be explained by the fact that when attacked by a stickleback the waterfleas escaped towards the centre of the swarm, larger individuals more quickly than smaller ones, thus leaving the stickleback with smaller than average prey at the edge of the swarm.     

The distribution,abundance and seasonality of pelagic marine invertebrate larvae in the maritime Antarctic

A survey of pelagic larvae was undertaken between November 1992 and February 1995 at Signy Island, Antarctica (60° 43 minutes S, 45° 36 minutes W). A diver-towed net and hand-held plankton pump were used at five sites of varying depths (6 to 30 m) and benthic substrata, in a combination of monthly and fortnightly samples. Overall larval ecological diversity was much higher than expected, with 131 morphologically distinct larval forms collected, apparently representing most of the benthic phyla present. The species richness observed is comparable with levels recorded at temperate latitudes, and higher than Arctic data and the implications for Thorson''s rule (the inferred cline of reduced pelagic larval diversity towards high latitudes) is discussed. Larval abundances were low (mean 2.6 individuals per cubic metre) which were two to six orders of magnitude lower than peaks in comparable data from temperate and tropical zones. We suggest that the low abundances recorded are a reflection of both slow developmental rates and a high dilution of larvae, reducing synchrony and spreading larvae over larger distances. Three seasonal periods, during which different larval types occur, have been identified. Summer, late summer and winter spawning strategies were discernable, and in some groups larvae occurred throughout the year.     

Foundations of gregariousness: a dispersal polymorphism among the planktonic larvae of a marine invertebrate

Theory predicts that selection should favor genotypes that can vary their tendency to disperse in habitats that are spatially or temporally variable or those that remain near their carrying capacity. Although many marine habitats appear to fit these criteria, confirmed examples of dispersal polymorphism among marine invertebrates are exceedingly rare. Competent larvae of the gregarious tubeworm, Hydroides dianthus, settle specifically in response to living conspecific worms, but a small proportion of each spawn settle nonspecifically on uninhabited substrata concurrently with their gregarious siblings. Here, using a parental half-sib analysis, we show that the proportion of a spawn settling in response to uninhabited biofilm is highly heritable. When estimated as a continuous trait based on a one-way ANOVA, heritability is estimated to be 0.83 +/- 0.31. When founder production was analyzed as a threshold trait, heritability was estimated to be 0.68 +/- 0.10 based on the breeding design experiment and 0.65 +/- 0.09 based on the artificial selection experiments. Realized heritability based on the selection experiments was considerably lower, however (0.17 per generation and 0.02 cumulative). Artificial selection was ineffectual at sequentially increasing the proportion of founder larvae among inbred family lines, but after three generations of selection, the proportion of larvae settling in response to biofilm was significantly higher among inbred lines than among the field-collected parents. The obligate planktonic larval stage common among so many marine invertebrates is thought to preclude the evolution of dispersal polymorphisms in these animals. Theoretical expectations of variable dispersal may instead be realized through individual behavioral differences resulting in differential transport or settlement preference, but this possibility remains largely unexplored among marine invertebrates.     

Uniformity in marine invertebrate ichnology

Relationships between ichnology and uniformitarianism are perhaps less complicated than those of their sister subdisciplines, paleontology and paleoecology. Trace fossils are manifestations of benthic behavior; and these traits, although evolving in significant ways, have remained stable over longer spans of time than individual species of invertebrates. The fossil record of behavior in fact originated earlier than the fossil record of invertebrate body parts. Although macroinvertebrates and their traces exhibit tremendous diversity of form and function, these fit into a relatively small number of behavioral patterns. The patterns, in turn, may correlate with prevailing environmental conditions, resulting in gradients among trace fossil assemblages, or ichnofacies. Behavioral patterns and characteristic ichnofacies therefore constitute the main basis for uniformity in ichnology. Thus, the most fundamental questions are: What is the specific function represented by the trace? How will it change as the tracemaker is influenced by other genetic, physiologic, or ecologic stimuli? In which facies will it likely occur? and what preservational biases are apt to modify the fossil record of this behavior and its environmental distribution? Approached from this standpoint, the present is indeed a key to the ichnologic past, and vice versa. In practice, however, the present has been studied considerably less than its importance would dictate.     

Seasonality of occurrence and recruitment of Arctic marine benthic invertebrate larvae in relation to environmental variables

The Arctic system is one of the regions most influenced by ongoing global climate change, but there are still critical gaps in our knowledge regarding a substantial number of biological processes. This is especially true for processes taking place during the Arctic winter but also for seasonal processes, such as the dynamics of intra-annual meroplankton occurrence. Here, we report on a 1-year study of meroplankton seasonal variability from a fjordic system in the Arctic Archipelago of Svalbard. The study combines an examination of phytoplankton, zooplankton, and hard bottom benthic settlement with measurements of environmental parameters (e.g., water temperature, particulate organic matter, and dissolved organic carbon). Samples were taken on a bi-weekly or monthly basis, and a total of 11 taxa representing six phyla of meroplankton were recorded over a 1-year period from January to December 2007. The occurrence of benthic larvae varied between the seasons, reaching a maximum in both abundance and taxon richness in late spring through early summer. Meroplanktonic larvae were absent in winter. However, settlement of benthic organisms was also recorded during the winter months (February and March), which indicates individual trade-offs related to timing of reproduction and competition. In addition, it suggests that these larvae are not relying on higher summer nutrient concentrations, but instead are dependent on alternative food sources. In parallel with meroplankton abundance, all other measured parameters, both biological (e.g., phyto- and zooplankton abundance and diversity) and physical (e.g., particulate organic matter), exhibited seasonal variability with peaks in the warmer months of the year.     

Differential susceptibility of marine invertebrate larvae: Laboratory predation of sand dollar, Dendrasterexcentricus (Eschscholtz), embryos and larvae by zoeae of the red crab, Cancer productus Randall

Predation on eggs, embryos, and larvae of the sand dollar, Dendraster excentricus (Eschscholtz) was investigated in a series of laboratory feeding experiments. Dendraster susceptibility to predation by zoea larvae of the red crab, Cancer productus Randall was strongly dependent on developmental stage and ontogenetic differences in motility. Clearance rates by C. productus were highest for eggs and averaged 0.551·zoea⁻¹·day⁻¹. Embryos and prism larvae of Dendraster were consumed at an intermediate rate, while pluteus larvae were captured at a relatively low rate. Clearance rates decreased from 0.18 to 0.031·zoea⁻¹·day⁻¹ during the transition of prism larvae into echinoplutei. Differences in Dendraster susceptibility to predation cannot be attributed to increasing prey body size because dwarf plutei were captured at the same rate as normal plutei. Reduced capture rates by Cancer productus zoeae are dependent on the development of Dendraster swimming behavior. Periodic reversals in the direction of ciliary beating and backwards swimming effectively remove Dendraster plutei from the immediate capture sphere of Cancer productus. Reversed swimming appears to function as a post-contact encounter response that reduces the mortality rates of Dendraster plutei.     

Environmental noise reduces predation rate in an aquatic invertebrate

Noise is one of a wide range of disturbances associated with human activities that have been shown to have detrimental impacts on a wide range of species, from montane regions to the deep marine environment. Noise may also have community-level impacts via predator–prey interactions, thus jeopardising the stability of trophic networks. However, the impact of noise on freshwater ecosystems is largely unknown. Even more so is the case of insects, despite their crucial role in trophic networks. Here, we study the impact of underwater noise on the predatory functional response of damselfly larvae. We compared the feeding rates of larvae under anthropogenic noise, natural noise, and silent conditions. Our results suggest that underwater noise (pooling the effects of anthropogenic noise and natural noise) decreases the feeding rate of damselflies significantly compared to relatively silent conditions. In particular, natural noise increased the handling time significantly compared to the silent treatment, thus reducing the feeding rate. Unexpectedly, feeding rates under anthropogenic noise were not reduced significantly compared to silent conditions. This study suggests that noise per se may not necessarily have negative impacts on trophic interactions. Instead, the impact of noise on feeding rates may be explained by the presence of nonlinearities in acoustic signals, which may be more abundant in natural compared to anthropogenic noise. We conclude by highlighting the importance of studying a diversity of types of acoustic pollution, and encourage further work regarding trophic interactions with insects using a functional response approach.     

The relationship between egg size and the duration of the facultative feeding period in marine invertebrate larvae

Feeding larvae of marine invertebrates fuel development from both endogenous egg energy and exogenous energy obtained from the planktonic environment. Although both sources of energy likely influence certain larval stages, only the effects of exogenous food have been well studied. Despite the lack of research on the effects of egg size on larval stages, investigators have hypothesized that egg size influences the duration of the facultative feeding stage—the stage in which larvae can feed but do not have to because development is still being fueled by egg energy. To test this hypothesis, we investigated six species of sand dollars with different sized eggs and quantified the duration of the larval facultative feeding period of each species by comparing when fed and starved larvae diverged in size. Regardless of whether phylogeny was taken into account, the duration of the facultative feeding period was positively correlated with egg size. We further determined that our conclusions were not sensitive to either our estimation of the duration of the facultative feeding period, or the branch lengths of the phylogeny we used. This relationship is likely a result of larger eggs being provisioned with more energy, and may affect how well larvae can cope with natural variability in food concentrations. Furthermore, our results support an assumption of a theoretical model developed to understand the evolution of different life-history strategies in marine invertebrate larvae, which suggests that this relationship has important evolutionary consequences.     

Evolution of marine invertebrate reproductive patterns

A simple model of the evolution of reproductive patterns in marine benthic invertebrates is presented. The aim is to discuss the dichotomous distribution of forms into those which produce a large number of small eggs with planktotrophic development, and those which produce a small number of large eggs with direct or lecithotrophic development. The fecundity of adult individuals is assumed to be inversely proportional to egg size, and the mortality of planktonic larvae is assumed to be density independent and size dependent. The growth of planktonic larvae is assumed to be sigmoid with metamorphosis occurring at a given size. The model concludes that there are at most two evolutionarily stable egg sizes. Depending on larval growth rate and death rate, the metamorphosis size, a smaller egg size, or both may be evolutionarily stable. The predictions of the model are compared to patterns observed in nature. Illustrative data are supplied mainly from prosobranch molluscs.     

Temperature- and light-mediated predation by perch on vendace larvae

The perch foraging pattern in a Finnish lake (64) N) was crepuscular and they moved into littoral areas at dusk and returned to deeper waters by dawn. Predation on vendace larvae was guided by environmental cues, mainly temperature and light periodicity, which affected the density and foraging activity of perch in the littoral area. The availability and the vulnerability of different food categories were both responsible for the perch diet. The hypothesis that perch have a generally decisive role in the regulation of vendace larval abundance through predation at the time of high vendace larvae concentration in the littoral area was not supported. We emphasize the need to evaluate biological phenomena, such as predator–prey relationships, in the light of the relevant physical variables, and to do so within appropriate time and space scales, instead of relying on indirect estimates of the predator and prey population abundance and using their reciprocity as evidence of the interaction.     

Developmental biology in marine invertebrate symbioses

Associations between marine invertebrates and their cooperative bacterial symbionts offer access to an understanding of the roots of host-microbe interaction; for example, several symbioses like the squid-vibrio light organ association serve as models for investigating how each partner affects the developmental biology of the other. Previous results have identified a program of specific developmental events that unfolds as the association is initiated. In the past year, published studies have focused primarily on describing the mechanisms underlying the signaling processes that occur between the juvenile squid and the luminous bacteria that colonize it.     

Effects of hydroperiod and predation on a Mississippi River floodplain invertebrate community

 The objective of this study was to determine if pond permanence and vertebrate predation (by fish and waterfowl) affect invertebrate community structure in the mudflat habitat of floodplain ponds. Invertebrate communities were studied for 1 year in four Mississippi River floodplain ponds with different hydroperiods. Pond 1 experienced five dry periods, pond 2 experienced four, pond 3 dried once, and standing water remained in pond 4 for the entire year. Vertebrate predator exclusion treatments (all access, no access, small-fish access and cage controls) were placed in all ponds. As pond duration increased, predatory invertebrate richness and abundance increased while overall invertebrate richness and abundance decreased. With the exception of the cladoceran Diaphanosoma, all commonly encountered taxa were strongly affected by pond permanence in terms of abundance, biomass and, generally, individual biomass. Taxa were nearly early divided between those that were more abundant in less permanent ponds and those that were more abundant in longer-duration ponds. Invertebrate taxa richness, abundance, and total biomass were lower in the all-access treatment than in the treatments that restricted predator access, and these effects were stronger in the more permanent ponds. In general, there were no significant differences in responses to the treatments with small-fish access and no access. These results support models that predict relatively weak effects of predation in frequently disturbed habitats. Received: 30 May 1995 / Accepted: 21 June 1996