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Larval Behavior and Natural Trace Element Signatures as Indicators of Crustacean Population Connectivity

Abstract

In an era of increasing governmental protection of marine resources and accelerating climate change, knowing how benthic populations of marine organisms are connected is of paramount importance. However, little is known about connectivity in the nearshore environment, particularly at ecologically and demographically relevant scales. Because the dispersive larval stage is the key to understanding population connectivity, my dissertation focused on developing a new technique for tracking larvae and determining how larval swimming behaviors can influence their cross-shelf distributions in the dynamic upwelling environment of northern California. This information is relevant not only to the applied fields of invasive species management, stock assessment, and marine protected area establishment, but also to the academic pursuit of understanding how life evolved in the sea.

In Chapters 1 and 2, I focused on investigating the role of swimming behavior in regulating larval transport in upwelling regimes. I observed in the laboratory the larvae of four crab species from open coast and estuarine habitats that develop either nearshore or offshore. Larval vertical positions in acrylic columns were recorded for up to three days, and I determined whether (1) depth preferences differed for the four species, (2) larvae undertook tidal and diel vertical migrations, (3) vertical migrations were timed endogenously or exogenously, and (4) maternal habitat influenced larval swimming behavior. Regardless of light or tidal phase, larvae of three species (Hemigrapsus oregonensis, Lophopanopeus bellus bellus, and Pachygrapsus crassipes) that develop offshore stayed high in the water column, where they would be transported seaward in the field. In contrast, larvae of one species (Petrolisthes cinctipes) that develop nearshore stayed low in the water column, where they would remain in shoreward-flowing bottom waters. None of the species from the open coast exhibited tidal or diel vertical migrations, but one estuarine species (H. oregonensis) exhibited reverse tidal vertical migrations that would expedite their transport to the open ocean. Furthermore, larvae hatched from estuarine populations of P. crassipes exhibited tidal swimming behaviors, while larvae hatched from coastal populations showed no tidally based behavior. Thus, larvae of species that hatch in different locations and develop different distances from shore exhibited diverse larval swimming behaviors that regulate transport, and these behaviors are phenotypically plastic.

In Chapters 3 and 4, I determined the utility of using trace element signatures in larval soft tissues as natural tags to track larval dispersal and population connectivity. As larvae develop as embryos and then pass through water masses throughout their development, they incorporate natural trace element signatures into their bodies. Many previous studies have successfully used the signatures in calcified structures, such as mollusc shells or fish otoliths, so my research instead concentrated on determining the utility of trace element signatures in larval soft tissues. The ability to track larvae based on trace element signatures in soft tissues would dramatically increase the diversity of taxa that could be investigated using this established tool.

A successful trace element study requires a natal site atlas with high reclassification success, but selecting sites to create an atlas is time consuming and expensive, with no guarantee that trace element signatures will differ among sites and remain consistent over time. In Chapter 3, I determined whether natal site atlases could be used repeatedly and identified site characteristics that yielded the best results by building atlases in five consecutive years using crab embryos from 15 sites that spanned 190 km of the northern California coast. I analyzed the elemental composition of embryos using a discriminant function optimization procedure to determine the suite of elements that resulted in the best reclassification success for individual sites and groups of sites each year. No element or group of elements was useful in discriminating the origins of embryos every year, and the reclassification success of the atlas varied at all spatial scales among years. Average reclassification success at the site level ranged annually from 39.5% to 54.3% correct, and combining sites into three areas or two regions improved overall reclassification success to 72.5% to 97.7% correct. Sites with unique geology, consistent freshwater runoff, or high anthropogenic influences had the highest individual reclassification success (up to 86.7% correct), and variation in these factors helped account for the variability in reclassification success among sites. Targeting differences in these factors when selecting sites in future trace element studies will increase the resolution of population connectivity estimates and infoinform explorations on the usefulness of these types of studies in a given area.

Finally, Chapter 4 focused on whether or not trace element signatures were retained in larval soft tissues throughout their pelagic development, to determine whether trace element analysis could be applied to larvae of the vast majority of species that do not retain larval calcified structures. To determine whether natal signatures are retained in soft tissues throughout larval development, I collected embryos of the porcelain crab, Petrolisthes cinctipes, from two to four locations along the coast of northern California in two years and reared larvae in a common water source for 6-8 weeks until they metamorphosed to postlarvae. Twenty elements were analyzed in extractions of soft tissues from embryos for the two larval and one postlarval stages. Elemental signatures of these planktonic stages were compared to those of embryos from the different collection sites using discriminant function analysis to determine if they could be accurately assigned to their site of origin. Overall reclassification success of postlarvae was poor (average 39.7% correct), though individual site success ranged from 86.2% correct to 0% correct. Reclassification success improved to 81.7% correct overall (ranging from 35.7% correct to 94.4% correct) when using each larval stage as a training set for the same larval stage. Thus, the same trace element signatures were not consistently maintained from embryos to postlarvae, but differences in signatures among natal sites were maintained. Trace element signatures in soft tissues could be useful in tracking dispersal from one stage to the next and determining how many sites, rather than which sites, contributed to a cohort of settlers.

These studies, taken as a whole, reveal new insights on larval behavior in upwelling regimes and highlight new approaches to determining population connectivity. Larvae from the open coast of northern California have evolved simple swimming behaviors in the face of complex oceanography, while estuarine species exhibit complex swimming rhythms based on the tidal stage; these differences persist even between populations of the same species. This finding reinforces the importance of understanding how populations are connected through their larval stage, and stokes the discussion about the importance of phenotype versus genotype in determining the success of larvae.

Finally, my work provides novel information about the utility of soft tissue trace element signatures and how to incorporate them into future studies. Marine ecologists constantly seek new and better tools to help determine larval dispersal patterns and population connectivity, and trace element signatures are an important component of the ecologist’s tool box. By determining the best way to utilize trace element signatures in soft tissues, my work opens the door to employing this tool on a whole new suite of taxa and dramatically broadens its utility. Investigators will now be able to use trace element signatures in soft tissues to inform the placement of marine reserves based on source/sink dynamics and an understanding of the locations of larval nursery areas, as well as determine how populations of invasive species are spreading from their points of introduction. Beyond these applied uses, my findings broaden our knowledge of the complexities of larval life in the ocean and inform our understanding of the persistence of sedentary and sessile populations in the sea.

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