Based on the belief that marine larvae, which can spend days to months in the planktonic stage, could be transported considerable distances by ocean currents, it has long been assumed that populations of coastal species with a planktonic larval stage are demographically open and highly ''connected.'' Such assumptions about the connectivity of coastal populations govern approaches to managing marine resources and shape our fundamental understanding of population dynamics and evolution, yet are rarely tested directly due to the small size and high mortality of marine larvae in a physically complex environment. Here, we document a successful application of elemental fingerprinting as a tracking tool to determine sources of settled invertebrates and show that coastal mussel larvae, previously thought to be highly dispersed, can be retained within 20 -30 km of their natal origin. We compare two closely related and co-occurring species, Mytilus californianus and Mytilus galloprovincialis, and determine that, despite expected similarities, they exhibit substantially different connectivity patterns. Our use of an in situ larval culturing technique overcomes the previous challenge of applying microchemical tracking methods to species with completely planktonic development. The exchange of larvae and resulting connectivities among marine populations have fundamental consequences for the evolution and ecology of species and for the management of coastal resources.elemental fingerprinting ͉ in situ larval culturing ͉ larval retention ͉ larval transport ͉ Mytilus
The diverse fauna and flora of rocky intertidal ecosystems are being impacted by the activities of rapidly increasing coastal populations in many regions of the world. Human harvesting of intertidal species can lead to significant changes in body sizes of these taxa. However, little is known about the temporal trajectories of such size declines and more importantly, the long-term effects of chronic human impacts. Furthermore, it is unclear whether sizes of species not directly targeted for harvesting are also declining through indirect effects. Here we use historical (extending back to 1869) and field survey data covering 200 km of mainland southern California coast to show that human activities have led to significant and widespread declines in body sizes of rocky intertidal gastropod species over the last century. These declines, initiated several decades ago, are continuing and contrary to expectation, they are not restricted to species harvested for human consumption. Data from the only national park in this area, where conservation laws are strictly imposed, demonstrate that negative ecological impacts can be ameliorated if existing laws are enforced.
Elements incorporated into developing hard parts of planktonic larvae record the environmental conditions experienced during growth. These chemical signatures, termed elemental fingerprints, potentially allow for reconstruction of locations of larvae. Here, we have demonstrated for the first time the feasibility of this approach for bivalve shells. We have determined the spatial scale over which we are able to discriminate chemical signatures in mussels in southern California and characterized the temporal stability of these signals. Early settlers of Mytilus californianus and Mytilus galloprovincialis were collected from eight sites in southern California. Shells were analyzed for nine isotopes using laser ablation-inductively coupled plasma-mass spectrometry (LA-ICP-MS). We discriminated among mussels collected in two bays and the open coast using Mn, Pb, and Ba shell concentrations. Shell concentrations of Pb and Sr were sufficiently different to discriminate between mussels from the northern and southern regions of the open coast, each representing approximately 20 km of coastline. These signals were relatively stable on monthly and weekly time scales. These results indicate that trace elemental fingerprinting of shell material is a promising technique to track bivalve larvae moving between bays and the open coast or over along-shore scales on the order of 20 km. Identification of spatial variation in elemental fingerprints that is stable over time represents a crucial step in enhancing our ability to understand larval transport and population connectivity in invertebrates.As marine biologists began to recognize the existence of planktonic larval stages of benthic adults during the first half of the 19th century, they began to evaluate the role of early life history in determining the abundance and distribution of benthic populations (e.g., Young 1990). Over time, marine ecologists have become increasingly concerned with the role of prerecruitment processes in structuring populations (e.g., Prytherch 1929;Roughgarden et al. 1988;Caley et al. 1996). 1Corresponding author (bjbecker@ucsd.edu). AcknowledgmentsThis work was funded by the California Environmental Quality Initiative (CEQI, Graduate Research Support Fellowship), the National Science Foundation (OCE-0327209), the Office of Naval Research (N00014-00-1-0174 and N00014-01-1-0473), the Switzer Environmental Fellowship, the Link Foundation, and the Cabrillo National Monument Foundation. B.J.B is supported by the United States National Park Service. Species identification using PCRbased methods were conducted by R. Byrne in the laboratory of R. Burton. Thermistor temperature data were provided by J. Largier, who is supported by California SeaGrant, with assistance from T. Kacena. Significant laboratory and field assistance was provided by L. Fajardo, V. Cannon, T. Bernhardt, and numerous volunteers. LA-ICP-MS analyses were conducted in the Scripps Institution of Oceanography Analytical Facility; K. Walda contributed valuable assistance in ICP-MS te...
The exchange of individuals among habitat patches (connectivity) has broad relevance for the conservation and management of marine metapopulations. Elemental fingerprinting-based research conducted over the past 12 years along the open coastline and bays of San Diego County in southern California evaluated connectivity patterns for seven species: one native and two invasive mussels, an oyster, a brachyuran crab, and two fishes. The studies spanned different years and seasons but overlapped considerably in space, allowing comparisons of dispersal patterns across species, and assessment of the relative importance of location, circulation, and intra-annual and inter-annual variability. We asked whether the species exhibited commonalities in directional transport, transport distances, sources and sinks, self-recruitment, and bay-ocean exchange. Linked connectivity-demographic analyses conducted for two species of mytilid mussels and two fishes allowed evaluation of the contributions of realized connectivity to metapopulation dynamics relative to other life-history attributes. Common trends across species include average along-shore dispersal distances of 15-35 km and seasonal changes in direction of dispersal that mirrored patterns of along-shore circulation. We observed greater isolation of back-bay populations, significant exchange from front bay to ocean, and high self-recruitment in locations on the northern, open coast, and in the southern bays. Connectivity was rarely the most influential driver of growth and persistence of metapopulations, but influenced the importance of other vital rates. Several locations served consistently as sources of larvae or as nurseries for multiple species, but there were few sites in common that were sinks. For the mussels, reproductive timing guided directional transport. These results imply that local management (e.g., habitat protection, opening of the mouths of lagoons, location of aquaculture farms) may be effective along this coastline. Regional, multi-species assessments of exchange of larvae should move us closer to ecosystem-based management.
[1] Molluscan shell chemistry may provide an important archive of mean annual temperature (MAT) and mean annual range in temperature (MART), but such direct temperature interpretations may be confounded by biologic, metabolic, or kinetic factors. To explore this potential archive, we outplanted variously sized specimens of the common mussel Mytilus californianus at relatively low and high intertidal positions in San Diego, California, for 382 days with in situ recording of ambient temperature and periodic sampling of water chemistry. The prismatic calcite layer of eight variously sized specimens from each intertidal position were then serially microsampled and geochemically analyzed.
Geochemical signatures of early life stages are increasingly used to study population connectivity. This approach utilizes spatial variability in chemical signatures to predict natal or nursery origins of post-dispersal individuals by comparison with a chemical reference atlas created from individuals of known origin. To examine the relative importance of spatial, temporal, and species variation in elemental signatures, we synthesized the chemical information of otoliths, larval shells, and whole larvae from studies that employed natural geochemical signatures in San Diego County, USA between 1997 and 2009. We compared 8 elements analyzed from 4 bivalve species, 2 larval or juvenile fishes, and Stage 1 crab zoeae. Across all species, different sets of elements best discriminated among open-coast sites or within or among bays and lagoons. In mytilid mussels, which had the most complete record, all 8 elements were more variable over time than space at the site level, highlighting the need to resample the reference atlas during each study. More coarsely, however, bay and lagoon taxa maintained distinct chemical signatures both from each other and from those on the open coast, despite interannual variability. Spatially identifiable signatures for all species were likely imparted by a combination of pollution in bays and export to adjacent coastlines (copper, lead), a heterogeneous distribution of land-sourced elements (manganese, cobalt, uranium), and incorporation that may vary in response to temperature (barium, manganese, strontium) and salinity (7 elements). These results identify important elements for larval tracking of additional species depending on habitat and life history; however, source population signatures appear species-specific.
The use of geochemical tags in calcified structures of fish and invertebrates is an exciting tool for investigating larval population connectivity. Evaluating these tags over relatively short intervals (weeks) may detect environmental and ecological variability at a temporal scale highly relevant to larval transport and settlement. We collected newly settled mussels (Mytilus californianus and M. galloprovincialis) weekly during winter/spring of 2002 along the coast of San Diego, CA, USA, at sites on the exposed coast (SIO) and in a protected coastal bay (HI), to investigate temporal patterns of geochemical tags in mussel shells. Analyses of post-settlement shell via LA-ICP-MS revealed statistically significant temporal variability for all elements we examined (Mg, Mn, Cu, Sr, Cd, Ba, Pb and U). Despite this, our ability to distinguish multielemental signatures between sites was largely conserved. Throughout our 13-week study, SIO and HI mussels could be chemically distinguished from one another in 78-87% of all cases. Settlement varied between 2-27 settlers gram-byssus-1 week-1 at SIO and HI, and both sites were characterized by 2-3 weeks with "high" settlement. Geochemical tags recorded in early larval shell of newly settled mussels differed between "high" and "low" settlement weeks at both sites (MANOVA), driven by Mg and Sr at SIO (p = 0.013) and Sr, Cd, Ba and Pb at HI (p < 0.001). These data imply that shifts in larval sources or transport corridors were responsible for observed settlement variation, rather than increased larval production. In particular, increased settlement at HI was observed concurrent with the appearance of geochemical tags (e.g., elevated Cd) that suggest those larvae were retained in upwelled water near the mouth of the bay. Such shifts may reflect short-term changes in connectivity among sites due to altered transport corridors, and influence the demography of local populations.
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