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«This dissertation is submitted in partial fulfillment of the requirements for the degree of Doctor of Philosophy Lance P. Garrison Approved ...»

-- [ Page 1 ] --

This dissertation is submitted in partial fulfillment of

the requirements for the degree of

Doctor of Philosophy

Lance P. Garrison

Approved September, 1997

Romuald N. Lipcius, Ph. D.

Committee Co-Chair/ Co-advisor

Fu-lin E. Chu, Ph. D.

Committee Co-Chair/Co-advisor

Roger Mann, Ph. D.

Jacques van Montfrans

John Boon, Ph. D.

Anson H. Hines, Ph. D.

Smithsonian Environmental Research Center

Edgewater, MD

Dedicated to Kimberly with grateful thanks for her constant love and support.

“Why is the sea king of a hundred streams ?

Because it lies below them.

Therefore, it is the king of a hundred streams.” Lao Tsu Tao Te Ching

TABLE OF CONTENTS

ACKNOWLEDGEMENTS......................................... vi FUNDING....................................................... vii LIST OF TABLES................................................ viii LIST OF FIGURES............................................... x

Abstract

.................................................... xii INTRODUCTION................................................ 2 Literature Cited.............................................. 14 CHAPTER 1..................................................... 17 Abstract.................................................... 18 Introduction................................................. 19 Materials and Methods........................................ 21 Results.................................................... 31 Discussion.................................................. 64 Acknowledgments............................................ 69

–  –  –

Funding for the plankton sampling in Chapters 1 and 4 and the development of the larval transport procedures in the HEM3d in Chapter 2 was provided by the NOAA Office of Sea Grant, U.S. Department of Commerce, Grant No. NA-90AA-D-SG-45 to the Virginia Graduate Marine Science Consortium and Virginia Sea Grant College Program.

Funding for biochemical supplies and equipment for Chapters 3 and 4 was provided by the Jefress Memorial Trust Grant No. J352 to Dr. Fu-Lin Chu. Additional funding was provided by a College of William and Mary Minor Research Grant and a VIMS Faculty Minor Research Grant to the author.

Financial support for the author was provided by a VIMS Graduate Fellowship for two years. During the last three years I have been supported by the Willard A. Van Engel Fellowship Corporation. I wholeheartedly thank the members of the Board of Directors and in particular Dr. W.A. Van Engel for their generosity.

–  –  –

CHAPTER 3 1 A-B. Mean percent composition of neutral and polar lipid classes......... 140

2. Analysis of Variace tables for Uca minax........................... 141

3. Partial correlations from error matrix for Uca minax................... 142 4 A-B. Multivariate analysis of variance tables for Uca minax............. 143

5. Canonical variate coefficents and correlations for Uca minax............ 144

6. Canonical variate coeffiecients and correlations for Uca minax.......... 145 7 A-B. Analysis of variance tables for Dyspanopeus sayi................. 146

8. Partial correlations from error matrix for Dyspanopeus sayi............. 147 9 A-B. Multivariate analysis of variance tables for Dyspanopeus sayi........ 148 10 A-B. Canonical variate coefficients and correlations for Dyspanopeus sayi. 149

11. Partial correlations matrix for Dyspanopeus sayi..................... 150

12. Mutilvariate analysis of variance tables for Dyspanopeus sayi........... 151 13 A-B. Canonical variate coefficients and correlations for Dyspanopeus sayi..152

–  –  –

In estuarine systems, the brachyuran crabs exhibit a diversity of larval development and dispersal strategies. There is a gradient of dispersal ranging from strong retention within hatching habitats to rapid export of larvae from the estuary to the continental shelf.

This dissertation examined the mechanisms by which physical transport and nutritional stress influence recruitment success in species with different larval dispersal strategies.

The first portion of the study examined how larval behaviors influence advective transport. Larval vertical migration patterns were examined within the York River, VA.

Larvae from different families exhibited tidally and light driven vertical migration behaviors that promote different patterns of advective transport. The degree to which vertical migration is selected for by large scale processes is likely associated with the constraint on larval recruitment success imposed by factors within the estuary.





The transport patterns of vertically migrating larvae were examined using a threedimensional hydrodynamic model of the York River. This study compared the distribution and dispersal of vertically migrating larvae to those of non-migrating particles.

Differences in the phase of tidal vertical migration and light limited behaviors influenced the rate and direction of dispersal. Tidal shear fronts appear to strongly effect the distribution of larvae and may play an important role in determining the strength of biotic interactions such as predation and nutritional stress.

The role of nutritional stress was examined in a combined field and laboratory study. The laboratory study examined the impact of starvation and food quality on the survival and biochemical composition of larvae with different dispersal strategies. Larvae that develop on the continental shelf generally had greater resistance to starvation than those that develop in the estuary. This study examined the biochemical mechanisms underlying differences in nutritional resilience. Larvae that develop on the continental shelf showed more efficient utilization of essential biochemical constituents during nutritional stress. In particular, phospholipid metabolism appeared to be an important aspect of the starvation response of brachyuran zoeae.

The biochemical composition of larvae in the natural habitat was examined to assess variability in nutritional condition over short time scales associated with the tidal cycle. Larvae collected from the field were larger and had higher contents of important energetic lipids than those in laboratory studies. These data suggest that nutritional stress is relatively rare in the estuary and feeding conditions in the natural habitat promote the accumulation of energetic reserves. There was a large degree of short term variability in phospholipid composition of larvae in the plankton. These changes are likely associated with small scale physical factors that determine the contact rates between zoeae and their prey.

The results from this dissertation highlight the importance of small scale and ephemeral physical features in the recruitment success of crab zoeae. While large scale gradients play an important role in selecting for dispersal strategies, small scale physical processes on scales of hours strongly influence the variability in recruitment success of crab zoeae.

–  –  –

Thorson (1950) broadly categorized larval development strategies among marine benthic invertebrates. This classification system has undergone modification, but remains an important framework for examination of reproductive strategies (Grahame and Branch, 1985). Thorson classified larval types based upon the mode of feeding and development.

These broad categories are: Long-lived Planktotrophic larvae that remain in the plankton for extended periods and rely upon dietary energy sources, Short-lived Planktotrophic larvae that are in the plankton for short periods ( 1 week) with fully developed guts and are capable of developing in the absence of food, and Lecithotrophic larvae that have large amounts of maternally supplied reserves and generally short planktonic duration on the order of hours (Grahame and Branch, 1985; Thorson, 1950). These modes of development were thought to be selected primarily by the trade-off between larval mortality in the plankton and adult energy investment in offspring. Vance (1973a, b) formalized these selective pressures in models that predicted that only the extremes of development patterns (i.e., complete planktotrophy or lecithotrophy) are evolutionarily stable, and egg size, as a measure of adult energy investment per larva, should show a bimodal distribution among related taxa. While there continues to be considerable debate on appropriate measures of fitness (Caswell, 1981), the relationship between egg size and energy investment (Underwood, 1974; Hines, 1986a), and the importance of energy considerations relative to mortality rates (Underwood, 1974), these models continue to find general support within specific taxa (e.g., echinoderms; Strathman, 1986).

The planktonic larval form arose in response to strong selective pressures in the adult habitat such as predation and resource limitation that promoted the movement of early juvenile forms to the plankton as a refuge (Strathman, 1986). Larval physical and behavioral traits subsequently arose as adaptations to selective pressures in the planktonic habitat (Strathman, 1986). The planktotrophic larvae is considered to be the most primitive; therefore, derived states such as lecithotrophy and vivaparity are responses to selective pressures in the planktonic habitat that favor the reduction of larval duration.

Since these strategies involve the loss of feeding structures, they are generally considered a uni-directional adaptation (Strathman, 1986). The rate of mortality in the planktonic habitat is particularly important in determining larval development strategy. Predation, nutritional stress, and adverse physical transport in the plankton are considered the primary processes that select for larval type (Thorson, 1950; Morgan, 1995).

The larval type and the associated length of residence in the plankton has strong implications for the rates of evolution and population dynamics of the adult population.

The extent of both dispersal and spread of larvae is determined by the duration of larvae in the plankton and the strength and direction of prevailing currents (Palmer and Strathman, 1981; Scheltema, 1986). Lecithotrophic larvae with durations on the scales of hours may be limited to dispersal scales on the order of hundreds of meters, while long-lived “teleplanic” larvae with extended durations (1 year) may have potential dispersal scales of thousands of kilometers (Day and McEdward, 1984). Local habitat quality and the frequency of local extinctions may place an additional constraint on the evolution of shortlived lecithotrophic larvae. Species with long-lived widely dispersing planktotrophic larvae have enhanced gene flow rates, are less susceptible to local extinction, and have longer duration times in the geological record (Palmer and Strathman, 1981; Strathman, 1986). These advantages are the byproduct of the larval type rather than selective factors that promote planktotrophy (Strathman, 1986; Palmer and Strathman, 1981). Factors in the plankton that select for a particular larval type play a strong indirect role in determining the overall rates of speciation and gene flow in benthic invertebrates.

Larval type and subsequent recruitment patterns can also have an important impact upon the demographic characteristics of benthic invertebrates. Large fluctuations in recruitment are generally more likely with planktotrophic larval development. Physical transport processes in particular tend to be highly variable, resulting in large variation in the delivery of larvae to suitable settlement sties and subsequent recruitment (Jackson, 1986). In contrast, lecithotrophic larvae with short planktonic periods are less likely to experience adverse physical transport and thus promote consistent recruitment patterns which are more sensitive to local variations in parental fecundity and space availability (Levin et al., 1987; Palmer and Strathman, 1981). The consequences of these differing patterns were explored in a polychaete with both types of larval development. Populations employing lecithotrophic larvae had more stable population growth rates and produced cohorts that were consistently effective colonizers of local substrates, resulting in consistent patterns of strong recruitment. Those with planktotrophic larvae were characterized by a more opportunistic lifestyle with the ability to rapidly invade habitats following local disturbance, but they were less adapted to local conditions (Levin et al., 1987). The type of larval development has a strong impact on determining the population growth rates, the degree of fluctuation in population size, and the age structure of invertebrate populations. The factors that determine the mortality rate of larvae in the plankton again have a strong influence on the characteristics of the adult population. They are important not only because they drive the selection of larval types, but also because they determine the degree of variability in recruitment success.

While it is apparent that the rate of larval mortality in the plankton plays a strong role in determining the overall life history and evolutionary patterns in marine invertebrates, estimates of the magnitude and variability in larval mortality are lacking. In particular, there is very little data which directly measures rates of larval mortality associated with the three primary selective factors in the plankton: predation, nutritional stress, and physical transport (Morgan, 1995; Eckman, 1996; Hines, 1986a). Thorson (1950) originally hypothesized that the vast majority of larvae would die in the plankton.



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