Limited impact of a bioeroding sponge, Cliona sp., on Ostrea chilensis from Foveaux Strait, New Zealand.

Bioeroding sponges can cause extensive damage to aquaculture and wild shellfish fisheries. It has been suggested that heavy sponge infestations that reach the inner cavity of oysters may trigger shell repair and lead to adductor detachment. Consequently, energy provision into shell repair could reduce the energy available for other physiological processes and reduce the meat quality of commercially fished oysters. Nevertheless, the impacts of boring sponges on oysters and other shellfish hosts are inconclusive. We studied the interaction between boring sponges and their hosts and examined potential detrimental effects on an economically important oyster species Ostrea chilensis from Foveaux Strait (FS), New Zealand. We investigated the effect of different infestation levels with the bioeroding sponge Cliona sp. on commercial meat quality, condition, reproduction, and disease susceptibility. Meat quality was assessed with an index based on visual assessments used in the FS O. chilensis fishery. Meat condition was assessed with a common oyster condition index, while histological methods were used to assess sex, gonad stage, reproductive capacity, and pathogen presence. Commercial meat quality and condition of O. chilensis were unaffected by sponge infestation. There was no relationship between sex ratio, gonad developmental stage, or gonad index and sponge infestation. Lastly, we found no evidence that sponge infestation affects disease susceptibility in O. chilensis. Our results suggest that O. chilensis in FS is largely unaffected by infestation with Cliona sp. and therefore reinforces the growing body of evidence that the effects of sponge infestation can be highly variable among different host species, environments, and habitats.

Global change scenarios trigger carry-over effects across life stages and generations of the intertidal limpet, Siphonaria australis.

For organisms with complex life histories, carry-over effects (COEs) can manifest between life stages, when conditions experienced by one stage influence the next, as well as trans-generationally, when the parental environment affects offspring. Here we used multiple global change-associated stressors to examine both forms of COE simultaneously in an intertidal limpet with mixed development (i.e. planktonic larvae hatch from benthic egg masses). Adult Siphonaria australis were subjected to four treatments over four weeks: an ambient control, a treatment featuring elevated water temperature (25°C) and UVB (1.7 W m-2), a copper pollution treatment (5.0 µg L-1), and a treatment incorporating all three stressors. Egg masses laid by these adults were then redistributed among the same four treatments (producing 16 adult-to-egg treatment histories) and stressed until hatching. Finally, hatching larvae were reared under ambient conditions for 24 days. While adult survivorship was unaffected by treatment, embryonic viability in egg masses responded strongly to egg mass treatment, as well as parental stress exposure, therefore displaying trans-generational COEs. These trans-generational COEs interacted with COEs originating in egg masses to produce highly context-dependent hatching sizes and larval growth. This demonstrates that the performance of a given organism at a given time reflects not only conditions experienced during embryonic development, but also those of the parental generation, and suggests that COEs play an important but underestimated role in responses to global change scenarios.

A dose-dependent relationship between copper burden in female urchin gonads and developmental impairment of their offspring.

We examined transgenerational effects of exposure to copper on early development of offspring in the urchin Evechinus chloroticus, and whether parental exposure mediated offspring response to a further low level exposure to copper during early development. Month-long exposure to elevated copper (25 µgL-1) in the laboratory increased copper in gonads of both males and females and reduced gonad size by almost half. There was a negative relationship between adult size and copper burden. Normal larval development and larval size four days after fertilization were both strongly, negatively related to the amount of copper in female gonads in a dose-dependent manner, but fertilization success was unaffected. This demonstrates a transgenerational effect of maternal exposure to copper pollution on offspring performance that is mediated by individual traits of females, but no evidence of strong paternal effects, nor of a low level of copper in the water in which early development occurs.

Maternal Lipid Provisioning Mirrors Evolution of Reproductive Strategies in Direct-Developing Whelks.

The energetic input that offspring receive from their mothers is a well-studied maternal effect that can influence the evolution of life histories. Using the offspring of three sympatric whelks: Cominella virgata (one embryo per capsule); Cominella maculosa (multiple embryos per capsule); and Haustrum scobina (multiple embryos per capsule and nurse-embryo consumption), we examined how contrasting reproductive strategies mediate inter- and intraspecific differences in hatchling provisioning. Total lipid content (as measured in µg hatchling(-1) ± SE) was unrelated to size among the 3 species; the hatchlings of H. scobina were the smallest but had the highest lipid content (33.8 ± 8.1 µg hatchling(-1)). In offspring of C. maculosa, lipid content was 6.6 ± 0.4 µg hatchling(-1), and in offspring of C. virgata, it was 21.7 ± 3.2 µg hatchling(-1) The multi-encapsulated hatchlings of C. maculosa and H. scobina were the only species that contained the energetic lipids, wax ester (WE) and methyl ester (ME). However, the overall composition of energetic lipid between hatchlings of the two Cominella species reflected strong affinities of taxonomy, suggesting a phylogenetic evolution of the non-adelphophagic development strategy. Inter- and intracapsular variability in sibling provisioning was highest in H. scobina, a finding that implies less control of allocation to individual hatchlings in this adelphophagic developer. We suggest that interspecific variability of lipids offers a useful approach to understanding the evolution of maternal provisioning in direct-developing species.

Carry-over effects of multiple stressors on benthic embryos are mediated by larval exposure to elevated UVB and temperature.

Damaging effects of UVB in conjunction with other stressors associated with global change are well-established, with many studies focused on vulnerable early life stages and immediate effects (e.g., mortality, developmental abnormalities). However, for organisms with complex life cycles, experiences at one life stage can have carry-over effects on later life stages, such that sublethal effects may mediate later vulnerability to further stress. Here, we exposed embryos in benthic egg masses of the New Zealand intertidal gastropod Siphonaria australis to treatments of either periodic stress (e.g., elevated UVB, salinity, and water temperature mimicking tidepool conditions in which egg masses are commonly found during summer) or control conditions (low UVB, ambient salinity, and water temperatures). Although there was high mortality from stressed egg masses, 24% of larvae hatched successfully. We then exposed the hatching larvae from both egg mass treatments to different combinations of water temperature (15 or 20 °C) and light (high UVB or shade) 12 h per day for 10 days. The most stressful larval conditions of 20 °C/high UVB resulted in low survival and stunted growth. Carry-over effects on survival were apparent for shaded larvae exposed to elevated temperature, where those from stressed egg masses had 1.8× higher mortality than those from control egg masses. Shaded larvae were also larger and had longer velar cilia if they were from control egg masses, independent of larval temperature. These results demonstrate that previous experience of environmental stress can influence vulnerability of later life stages to further stress, and that focus on a single life stage will underestimate cumulative effects of agents of global change.

Effects of temperature on hatching time and hatchling proportions in a poecilogonous population of Haminoea zelandiae.

Poecilogony is a relatively uncommon life-history strategy that results in the production of two different larval forms from the same egg mass (e.g., free-swimming lecithotrophic larvae and post-metamorphic, crawling juveniles). In this study, a population of the opisthobranch gastropod Haminoea zelandiae from Pauatahanui Inlet, New Zealand, was found to exhibit poecilogony. Further, differences in development, hatching times and proportion of hatchlings that were veligers or juveniles were examined for egg masses in two temperature regimes in the laboratory: cool (15-17 °C), and warm (21-23 °C). Hatching proportions were also examined for egg masses collected from the field (where temperatures ranged from 21-23 °C) for varying lengths of time (1 d, 5 d, and 10 d post-spawning). Hatchlings from egg masses in warmer temperatures developed faster and hatched earlier than those in cool temperatures. In the laboratory, egg masses in warm conditions hatched a greater proportion of post-metamorphic juveniles (45.4%) compared to egg masses in cool conditions (24.6%) Further, egg masses that had been in the field 10 d before hatching (i.e., more days at warmer temperatures) exhibited a greater proportion of post-metamorphic juveniles (67.9%) than those that were collected after only 1 d in the field (25.1%). Together these results suggest that temperature may have an important role in mediating dispersal strategies in this poecilogonous species.

Life history and matrix heterogeneity interact to shape metapopulation connectivity in spatially structured environments.

Metapopulation models have historically treated a landscape as a collection of habitat patches separated by a matrix of uniformly unsuitable habitat. This perspective is still apparent in many studies of marine metapopulations, in which recruitment variation is generally assumed to be primarily the result of variability in ocean currents and interactions with disperser behavior, with little consideration of spatial structure that can affect disperser viability. We use a simple model of dispersal of marine larvae to demonstrate how heterogeneity in dispersal habitat (i.e., the matrix) can generate substantial spatial variation in recruitment. Furthermore, we show how this heterogeneity can interact with larval life-history variation to create alternative patterns of source-sink dynamics. Finally, we place our results in the context of spatially structured matrix population models, and we propose the damping ratio of the connectivity matrix as a general and novel measure of landscape connectivity that may provide conceptual unification to the fields of metapopulation biology and landscape ecology.

Relative effects of maternal and juvenile food availability for a marine snail.

The relative importance of maternal vs. juvenile food environment on juvenile performance is poorly understood, particularly for marine organisms. Here, we use a manipulative experiment to compare the influence of maternal and juvenile nutrition on early juvenile performance for a marine gastropod (Cominella virgata) with completely benthic development. Adult whelks adjusted growth and capsule volume to food availability, but there was no effect on the initial size or number of their hatchlings, which varied greatly within and among females. Although hatchling survivorship was also unaffected by maternal nutrition, juveniles fed lower food showed decreased survivorship. By contrast, growth of C. virgata hatchlings in the month after hatching was higher for hatchlings from high-food mothers, suggesting important carry-over effects of maternal nutrition on early juveniles, mediated by a trait other than offspring size. This maternal effect faded in the second month after hatching, as the hatchling environment became more important.

Evolutionary and experimental change in egg volume, heterochrony of larval body and juvenile rudiment, and evolutionary reversibility in pluteus form.

Heterochronic developmental plasticity of the juvenile rudiment and larval body of sea urchin larvae occurs in response to supply of food. Evolutionary increase in egg size can also be associated with earlier development of the juvenile rudiment. We examined effects of egg volume of feeding larvae on this heterochrony and other changes in larval form. (1) Evolutionary and experimental enlargements of egg volume did not accelerate formation of the rudiment relative to the larval body. Development of the larval body and juvenile rudiment was compared for the echinoids Strongylocentrotus purpuratus (with an egg of 78-82 microm) and Strongylocentrotus droebachiensis (with an egg of 150-160 microm diameter). Development of both larval body and rudiment were accelerated in S. droebachiensis relative to S. purpuratus but with greater acceleration of the larval body, so that the rudiment of S. droebachiensis was initiated at a later larval stage even though at an earlier age. Also, experimentally doubling the egg volume of S. purpuratus did not accelerate development of the juvenile rudiment relative to the larval body. (2) Both species exhibited similar plasticity in timing of rudiment development in response to food supplies. (3) Doubling egg volume of S. purpuratus produced a larval form more similar to that of S. droebachiensis. This result mirrors previous experiments in which larvae from half embryos of S. droebachiensis were more similar to larvae of S. purpuratus. Many of the effects of egg volume on larval form are similar against either species' genetic background and are thus evolutionarily reversible effects on larval form.

High variability in egg size and energetic content among intertidal mussels.

Maternal investment is a fundamentally important parameter in life-history theory and models, yet the scales at which it varies (among individuals vs. among populations) is rarely reported. In this study, variability in attributes of eggs and early larvae of Mytilus californianus was examined from four sites spanning Point Conception, California, in June and September 2001. The effects of female, site, and month were examined for the following variables: egg volume (microl), egg energy content (microg carbon per egg), and initial larval size (microm). The only significant effect on both egg traits was that of female. Females differed by up to 57% in mean egg volume and 116% in mean egg energetic content. Although there were significant effects of rearing environment, female, site, and month on initial larval size, variability in larval length was small compared to the egg traits. Mean larval length was maximally 11% different among females. Neither female body weight nor length was correlated to mean offspring traits, and there were also no significant relationships between egg traits and initial larval size. The primary source of variation in maternal investment in this system appears to be among individual females rather than over space or time.

Natural variability in size and condition at settlement of 3 species of marine invertebrates.

Experimental studies have demonstrated that for many marine invertebrate species, variability in larval condition or quality at settlement may have important effects on post-settlement, early juvenile performance. Relatively few studies, however, explicitly examine natural variability in larval condition at settlement. This study examines natural variability in larval attributes (size and lipid index) at settlement for terminal-stage larvae of intertidal mussels (Mytilus sp.) and barnacles (Pollicipes polymerus and Chthamalus dalli) from southern California. Despite significant differences among cohorts in larval attributes, for all 3 species a greater percentage of the variance in larval length (80-100%) and lipids (58-83%) occurred among individuals within a cohort, rather than among cohorts. For all 3 species, coefficients of variation within a cohort for length were much smaller (3-8%) than those for lipid index (30-93%), suggesting that lipid storage is a much more plastic attribute than size for larvae. For mussels, settlement intensity and larval attributes were decoupled, such that average larval condition of a cohort was not related to the number of larvae that settled. At the cohort level, Mytilus and Pollicipes settling together across 3 dates showed similar trends of decreasing lipid index over time, suggesting that environmental conditions may influence co-occurring planktonic larvae similarly across species. This work highlights the need for further experiments in the field on the effects of larval history on recruitment success in natural populations, and further studies to determine what factors influence larval attributes for planktonic larvae in the field.