Abstract
Sand dollars (Fellaster zelandiae) are a common sight at many sandy subtidal locations throughout Aotearoa (New Zealand). Their distinctive flattened purplegrey round tests and/or fragments are often washed up onto beaches. Sightings of live organisms or shell fragments have been recorded from Cape Reinga at the top of the North Island/Te Ika-a-Maui to Papatowai at the bottom of the South Island/Te Wahipounamu and even in Post Office Bay of Ulva Island/Te Wharawhara in Stewart Island/Rakiura. Specific details and focused scientific research on this species are, however, fragmented at best. There are few publications on this endemic New Zealand species and unpublished data has yet to make an impact on either the scientific community or the general public. Since its discovery in 1855 by Gray and subsequent reclassification as a species endemic to New Zealand in 1955 by Durham, new educational and academic information has yet to reveal a complete story of this species. Understanding Fellaster zelandiae is especially imperative as this species is an important benthic-pelagic coupler and bioturbator in nearshore Aotearoa. Fellaster can be used an indicator of the health of the marine environment; changes in populations can signal environmental changes such as pollution or disease.
This research aimed to characterise Fellaster zelandiae in as many aspects as possible: highlighting the life cycle of this species, its role in the environment, looking back at the extent of research performed thus far, and looking forward answering new questions about this endemic species. Research was performed in three major disciplines: genetics, ecology, and mineralogy, to create a multidisciplinary approach to a marine invertebrate species.
Investigating the biogeography of a marine species using genetic analysis can reveal the physical environmental processes that shape spatial biodiversity. New Zealand occupies its own biogeographic realm, where deep bathymetric features and oceanographic characteristics act as physical barriers to the influx of species and lineages from the rest of the world. Marine species often have dispersive larval stages, but might not be well connected over large distances; sand dollars, for example, often show regional isolation but local connectivity. Fellaster zelandiae was shown to have an extremely low amount of genetic diversity between locations around the country (0.2% difference across 40,725 SNPs). The genetic homogeneity of the sand dollar matches other species from New Zealand with high larval dispersal potential, such as Jasus edwardsii and Evechinus chloroticus. The most distinct population differences between Fellaster occur between the geographic break of the North Island’s Northeast and the rest of the country. Small-scale genetic variation between northern and southern populations, however, appears consistent with biogeographic patterns seen in other coastal species in New Zealand and is probably driven by isolation of some regions by oceanographic features including the East Auckland Current, East Cape Current and Southland Current. Hydrology has created discrete but shallow population breaks, but at the same time has allowed for larval dispersal and gene flow around the entire country, keeping Fellaster as a well-connected single species.
Multi-stressor experiments are a common tool to investigate echinoderm larvae development. Here, the importance of local adaptation from geographically distinct populations of a single species is highlighted. Fellaster larvae from four populations across a range of latitudes (37° S to 46° S) were tested in temperature and food treatments to measured developmental responses. While high-food treatment larvae had greater growth compared to low-food treatment larvae and larval development was accelerated with increasing temperature, the lineage of Fellaster influenced the magnitude of these effects. Larvae from warmer lineages (35 to 40 °S, summer mean SST = 18-23 °C) increased in size by as much as 100% in high-food conditions compared to low-food conditions. Larvae grew faster as temperature increased in both high- and low-food treatments by a minimum of 3 days and an average of 6 days. Colder lineages (41 to 46 °S, summer mean SST = 13-17 °C) meanwhile only showed a maximum of a 50% increase in development between high-food and low-food conditions. Temperature was not a significant factor for cold populations, where elevated temperatures did not accelerate development as was seen in the two warm-populations. For a genetically homogeneous species, Fellaster zelandiae exhibited surprisingly different developmental responses based on the lineage of the parents. The four different populations of Fellaster displayed different morphological plasticity to future ocean conditions, and thermally-influenced phenotypes mostly arose from warm populations.
Fellaster zelandiae resembles other echinoderms in biomineralizing Mg-calcite. Their skeletons, however, show mineralogical variation at different levels of scale: nanostructure, body part, individual, and population. Teeth, the deepest internal skeletal structures in the individual and vital for feeding, showed the greatest compositional variation at the nanoscale, whereas tests and spines were both more consistent in Mg concentrations. Mg incorporation is, approximately, a function of proximity to seawater, with levels highest in layers further away from the marine environment. Body part variation within individuals of a populations was relatively low (Maximum SDx = ± 0.19 wt% MgCO3, n = 9) while average variation was ± 0.14 wt% MgCO3 (n = 670), reflecting low genetic variability. Populations across the country showed that external parts (spines) were most affected by temperature and classical environmental factors, while internal parts (Aristotle’s lanterns) were not as affected by abiotic factors. Intermediate structures (tests) were unexpectedly influenced by wave energy, where increases in Mg content among populations were correlated to higher wave-energy beaches. While intrinsic, phylogenetic, and extrinsic factors can individually influence skeletal carbonate mineralogy, accounting for the cumulative individual and population-level factors affecting mineralogy provides an extremely nuanced understanding of biomineralization within a single species. In future ocean conditions, skeletal composition will change in the spines of adults, while other mineral components may retain the same composition, but at an increase to the energetic cost.
The environmental characteristics that drive Fellaster populations around New Zealand are typical of other irregular echinoids: saline, nearshore, and siliceous sediment of a grain size between 100-700 µm. Sediment grain size along the coast predicts the presence/absence of Fellaster better than many other variables. In the imminent future, changes to the sediment type in locations of sand dollar beds is the most direct threat to sand dollar habitat. Increases in nearshore sedimentation and silt buildup from runoff and changing terrestrial landscapes affects the microphytobenthos community which in turn affects the food availability for adult sand dollars. Changes to grain size in environments will force migrations of adults as silt destroys the habitat of current populations.
Other characteristics of the environment, such as temperature and average wave energy, do not currently limit the range of the species, but rather seem to affect other biological processes, including developmental plasticity and morphological differences. Fellaster zelandiae currently occurs across a broad latitudinal range (35° S – 48° S), experiencing a range of temperature (5 – 24 °C) and primary productivity (200 – 700 mg m2 d-1). Environmental conditions of future oceans are predicted to have uneven spatial changes. The current larval dispersal time for Fellaster (28 days) provides ample time for gene flow and creates high population connectivity. This intergenerational connectivity gives the current populations of Fellaster a good ability to adapt with phenotypic plasticity to future ocean conditions. While the strong connectivity of many contemporary populations is likely the result of a long-lived larval stage, gene flow may reduce in the future as larval development times decrease in future ocean conditions. Larval development times are set to accelerate in Fellaster in warmer populations in the north, while densities of settled juveniles will decrease. Warmer populations may experience range contractions and increasing genetic isolation as larvae travel less distance. Based on prevailing hydrology and thermally-indifferent larval development, I hypothesis that colder populations of Fellaster will retain their development timing with no adverse morphology as primary productivity is slated to increase in the southeast. Southern populations may increase their range and create one-way gene flow northwards as larval dispersal remain the same and high density create dispersal pressure into the warm population areas. This thesis research has shown that novel combinations of multidisciplinary research can be a great tool to answer questions pertaining to marine ecological changes in the face of future ocean conditions.