Nicole E. Phillips

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.

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 (μl), egg energy content (μg carbon per egg), and initial larval size (μm). 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.

Capture of Large Particles by Suspension-Feeding Scaleworm Larvae (Polychaeta: Polynoidae)

Most of the polychaete larvae in which feeding mechanisms have been studied feed using an opposed-band mechanism, capturing particles with prototrochal and metatrochal ciliary bands and transporting them to the mouth via a food groove. However, many other planktotrophic polychaete larvae lack a metatroch and food groove and thus must feed in a different way. In this latter group are the larvae of polynoid polychaetes, which not only lack a metatroch and food groove but also bear a bundle of long cilia (the oral brush) attached near the left side of the mouth. In feeding experiments with polystyrene beads and plankton, larvae of the polynoid Arctonoe vittata ingested larger particles (up to 60 {mu}m in diameter) than those ingested by the opposed-band feeding larvae of the serpulid Serpula vermicularis (up to 12 μm in diameter). Videotaped images of feeding A. vittata larvae showed that capture behavior was elicited as particles in a feeding current driven by the prototroch approached or contacted the larval episphere. Particles on or very near the episphere were disengaged by a recoiling motion of the larva and were then moved to the mouth, probably by the oral brush. This feeding mechanism may be widespread in the polychaete superfamily Aphroditacea, which includes about 10% of extant polychaete 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.

Species-Specific Vulnerability of Benthic Marine Embryos of Congeneric Snails (Haminoea spp.) to Ultraviolet Radiation and Other Intertidal Stressors

We used field surveys and multi-factorial experiments to examine synergistic effects of ultraviolet radiation (UVR) and low tide conditions on the embryonic mortality of two bubble-shell snail species that deposit gelatinous egg masses in intertidal mudflats: Haminoea zelandiae from New Zealand, and Haminoea vesicula from Washington, USA. Egg masses of both species were predominantly found in shallow pools at low tide, and a substantial proportion of both were found in sunny as well as shaded microhabitats. Both exposure to sun and desiccation led to increased embryonic mortality for naturally deposited egg masses of H. zelandiae compared to those that were shaded or submerged. For H. vesicula, although mortality was double for embryos within desiccated egg masses, there was no additional mortality due to sun exposure. In manipulative experiments, UVR and low tide conditions increased embryonic mortality for both species; however, H. zelandiae appeared to be more vulnerable to UVR, whereas H. vesicula was particularly vulnerable to desiccation. Simulated tidal pool conditions significantly increased mortality only for H. vesicula. These results suggest an important role of species-specific differences in vulnerability to different stressors, even for ecologically similar congeners; here, these differences may be related to development time or egg mass characteristics.

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.

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.

Variation in mussel and barnacle recruitment parallels a shift in intertidal community structure in the Cook Strait region of New Zealand

Recruitment influences populations and communities of marine organisms to varying degrees and across a range of spatial scales. We hypothesised that recruitment plays a role in maintaining different intertidal invertebrate assemblages between two nearby locations in New Zealand (Wellington Harbour and the south coast), long reported to have dramatically different communities (with greater cover of sessile invertebrates in the Harbour). Sites in Wellington Harbour were hypothesised to have higher monthly recruitment rates of mussels and barnacles and greater barnacle colonisation after 1 year. Surveys were conducted to quantify community differences. In Wellington Harbour, the mid-intertidal zone was dominated by the mussel Mytilus galloprovincialis and the barnacle Chamaesipho columna and the high intertidal zone by C. columna. In contrast, on the south coast mussels were almost completely absent from both tidal heights and barnacles (predominantly Chamaesipho brunnea) were sparse. In the high zone, monthly recruitment and long term colonisation (over 1 year) of barnacles was much greater in the Harbour; in the mid-intertidal zone, mussel recruitment was up to two orders of magnitude greater in the Harbour than the south coast. Species-specific recruitment patterns differed between the locations, however and were consistent with those of adult abundance.

Acute toxicity of copper, lead, zinc and their mixtures on the sea urchin Evechinus chloroticus

ABSTRACT Coastal pollution is complex, often consisting of multiple contaminants, and it is increasingly recognised that exposure to combinations of pollutants can produce different outcomes than each does separately. This study investigates the toxicity of three major pollutants in coastal environments (copper, lead and zinc) individually and in binary mixtures on larvae of Evechinus chloroticus, a sea urchin endemic to New Zealand. Larval development assays were conducted for 72 h. Median effective concentrations (EC50) for normal larval development for individual metals were 5.4 μg/L Cu, 52.2 μg/L Pb and 27.7 μg/L Zn. Evechinus chloroticus was more sensitive to copper and zinc than most echinoid species tested to date. Effects of metal mixtures were analysed using a toxic unit (TU) approach. Cu + Zn and Cu + Pb had a less-than-additive effect on E. chloroticus larval development. By contrast, Zn + Pb was strictly additive. None of the interactions were strong, with sums of TU ranging from 1.00 to 1.85. These results support the use of criteria based on strictly-additive models to determine whether these three metals exceed water quality thresholds when occurring in a simple mixture.

Effects of microhabitat availability on estimates of density of a reef fish: implications for assessments of marine protected areas

Many estimates of ‘marine protected area (MPA) effects’ may be confounded by environmental heterogeneity between MPA and ‘Control’ sites. However, the magnitude and extent of such confounding is generally unknown. Here, the effects of microhabitat availability on estimates of MPA performance were explicitly explored. Abundance of a reef fish species, Ctenochaetus striatus (Quoy & Gaimard, 1825), available microhabitat, and, microhabitat preference for C. striatus within six ‘Ra’ui’ (traditionally managed MPAs) and six paired ‘Control’ sites on the island of Rarotonga, Cook Islands, were estimated. Response ratios accounting for available microhabitat qualitatively modified inferences of Ra’ui effectiveness for two of the six Ra’ui when contrasted with response ratios not accounting for available microhabitat. However, analysis of covariance (ANCOVA) indicated that available microhabitat accounted for significant variation in C. striatus densities between Ra’ui and Control, rather than protection. Our results suggest that adjusting for microhabitat availability may significantly alter our perception of the effects of Ra’ui on C. striatus. Our framework, in concert with our ANCOVA models, provides a stronger assessment of MPA effects. Further, we conclude that metrics of environmental heterogeneity should be incorporated into future assessments of MPA effectiveness, with our work describing one potential framework to accomplish this.