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«A Dissertation Presented by Michael Samuel Rosenberg to The Graduate School in Partial Fulfillment of the Requirements for the Degree of Doctor of ...»

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THE COMPARATIVE CLAW MORPHOLOGY, PHYLOGENY, AND

BEHAVIOR OF FIDDLER CRABS (GENUS UCA)

A Dissertation Presented

by

Michael Samuel Rosenberg

to

The Graduate School

in Partial Fulfillment of the

Requirements

for the Degree of

Doctor of Philosophy

in

Ecology and Evolution

State University of New York

at Stony Brook

May 2000

State University of New York

at Stony Brook

The Graduate School

Michael Samuel Rosenberg We, the dissertation committee for the above candidate for the Doctor of Philosophy degree, hereby recommend acceptance of this dissertation.

____________________________________________

Jeffrey S. Levinton, Dissertation Advisor Professor, Department of Ecology and Evolution, SUNY at Stony Brook ____________________________________________

Geeta Bharathan, Chairperson of Defense Professor, Department of Ecology and Evolution, SUNY at Stony Brook ____________________________________________

F. James Rohlf Professor, Department of Ecology and Evolution, SUNY at Stony Brook ____________________________________________

Alan W. Harvey Professor, Department of Biology, Georgia Southern University This dissertation is accepted by the Graduate School.

__________________________________

Dean of the Graduate School ii

Abstract

of the Dissertation

THE COMPARATIVE CLAW MORPHOLOGY, PHYLOGENY, AND

BEHAVIOR OF FIDDLER CRABS (GENUS UCA)

by Michael Samuel Rosenberg Doctor of Philosophy in Ecology and Evolution State University of New York at Stony Brook 2000 Fiddler crabs (Ocypodidae, Uca) are a well known group of small, intertidal Brachyuran crabs, characterized by strong sexual dimorphism and male asymmetry. Male fiddler crabs exhibit one of the most extreme levels of body asymmetry of any organism, having a large major claw containing a third to half of the animal’s body mass and a small minor claw. The morphology of major and minor claws varies tremendously across species. These studies are concerned with understanding the phylogenetic history of the genus, describing patterns of claw shape withinand across species, and exploring the relationship of claw morphology with behavior and ecology.

The systematic and phylogenetic history of the genus is explored in some detail before a morphological phylogenetic analysis was performed on 88 of the 97 recognized species. These results were compared to a molecular study of 16S ribosomal DNA for 28 species. The results resolve most of the subgeneric taxonomic conflicts and allow one to perform interspecific analyses in a comparative methodological framework.

iii Geometric morphometrics was used to study claw shape across the genus.

Within species, major claws show allometric growth in both shape and size;

minor claw growth is isometric. Both major and minor claws are isometric for size and allometric for shape across species; accounting for phylogenetic dependence has little effect on the analyses. There is evidence for evolutionary allometry explaining some of the diversity of claw forms seen within the genus.

Four behaviors are associated with claw use: visual signaling, acoustic signaling, combat, and feeding. The first three are examined with respect to major claw morphology; the later with minor claw morphology. Only combat can explain a significant amount of variation in major claw morphology.

Differences in habitat choice are able to explain some variation in minor claw morphology. Species in sandy habitats have minor claws with wider gapes and longer chela than those in muddy habitats.

–  –  –

List of Figures

List of Tables

Acknowledgments

Chapter 1. Introduction

1.1 What are Fiddler Crabs?

1.2 Overview of Study

Literature Cited

Chapter 2. The Systematics and Taxonomy of Fiddler Crabs: A Phylogeny of the Genus Uca

2.1 Abstract

2.2 Introduction

2.3 History

The Genus Uca

The Subgenera of Uca

The Species of Uca

The Phylogeny of Uca

2.4 Materials and Methods

2.5 Results

2.6 Discussion

2.7 Conclusions

Literature Cited

Chapter 3. Evolution of Shape Differences Between the Major and Minor Chelipeds of Uca pugnax (Decapoda: Ocypodidae)

3.1 Abstract

3.2 Introduction

3.3 Materials and Methods

3.4 Results

3.5 Discussion

Literature Cited

vi Chapter 4. Fiddler Crab Claw Shape Variation: A Geometric Morphometric Analysis Across the Genus Uca

4.1 Abstract

4.2 Introduction

4.3 Materials and Methods

Data Acquisition

Analysis

4.4 Results

4.5 Discussion

4.6 Conclusions

Literature Cited

Chapter 5. Behavioral Variation and Morphology: Claw Evolution and Specialization in Fiddler Crabs

5.1 Abstract

5.2 Introduction

5.3 Materials and Methods

5.4 Behaviors

Visual Display





Acoustic Display

Combat

Feeding

5.5 Conclusions

Literature Cited

Appendix I. Specimens Examined

Appendix II. Character List

Appendix III. Data Matrix

–  –  –

Figure 3.1 Diagram of a cheliped with the six morphological landmarks labeled

Figure 3.2 Generalized Least-Squares superimposition of all 126 chelipeds showing variation at each landmark after the specimens have been scaled, translated, reflected, and rotated

Figure 3.3 Bivariate plot of Relative Warp 1 scores versus Relative Warp 2 scores

Figure 3.4 Overall deformation of shape along the first Relative Warp for all 126 specimens

Figure 3.5 Overall deformation of shape along the second Relative Warp for all 126 specimens

Figure 3.6 Relationship between length and shape of chelipeds of Uca pugnax

Figure 3.7 Predicted cheliped shapes

Figure 4.1 Examples of major claws from different species of Uca.

............. 71 Figure 4.2 Diagrammatic representation of the morphological features of fiddler crabs described in the text

Figure 4.3 The shape data collected from each claw

Figure 4.4 Elliptical Fourier reconstructions of an Uca vocans claw, illustrating how increasing the number of summed harmonics more accurately reproduces the original shape.

....... 77 Figure 4.5 Regression of centroid size on carapace breadth for the species means

viii Figure 4.6 Regression of slope of major claw regression slope on mean centroid size

Figure 4.7 Relative warps 1 and 2 for the species means of the major claws

Figure 4.8 Relative warps 1 and 3 for the species means of the major claws

Figure 4.9 Relative warps 1 and 2 for the species means of the minor claws

Figure 4.10 Relative warps 1 and 3 for the species means of the minor claws

Figure 4.11 Plot of relative warps for the species means of major and minor claws

Figure 4.12 Plot of interspecific multiple regression of partial warp scores on centroid size

Figure 4.13 Variant claw forms of Uca borealis

Figure 5.1 Diagrammatic representation of claw morphology

Figure 5.2 The landmark data collected from each claw

Figure 5.3 Basic vertical wave

Figure 5.4 Basic lateral wave

Figure 5.5 Variations on basic waving patterns

Figure 5.6 Acoustic specializations of Uca musica and Uca terpsichores.

....... 123 Figure 5.7 Outer view of right major claw of Uca saltitanta

Figure 5.8 The shape of the major claw of drumming and nondrumming species

Figure 5.9 Major claw morphology as it relates to combat

Figure 5.10 Illustration of the manus rub during male-male combat.

........... 132 Figure 5.11 Illustration of the dactyl slide during male-male combat........... 132 Figure 5.12 Illustration of interlocking claws and some related morphological features

Figure 5.13 Buccal cavity of Uca

Figure 5.14 Examples of spoon-tipped setae found on the second maxilliped of Uca

Figure 5.15 Minor claws of four species, representing some of the variation in specialized feeding structures

Figure 5.16 The relationship between minor claw variation and habitat.

..... 145

ix List of Tables

Table 2.1 Subdivisions of the genus Uca according to Crane (1975).

........... 18 Table 2.2 Divisions of the genus Uca according to Bott (1973)

Table 2.3 Changes to the species level taxonomy of the genus Uca since since Crane (1975)

Table 2.4 Species of Uca not included in the phylogenetic analysis.

............ 30 Table 2.5 Suites of characters which were inapplicable for some taxa......... 32 Table 2.6 Reassessment of Uca subgeneric nomenclature

Table 2.7 Number of changes required under different scenarios of frontbreadth evolution, treating front-breadth as a single character.

... 44 Table 3.1 Results of a two-way MANOVA of nonuniform (W-matrix) and uniform (affine) shape variables, comparing the effects of major versus minor cheliped and individuals

Table 3.2 Results of MANOVAs on nonuniform (W-matrix) and uniform (affine) shape variables, using major and minor cheliped as categorical variables and centroid size as the covariates.

.............. 63 Table 4.1 Results of the linear regression of ln centroid size onto ln carapace breadth for individual species (n ≥ 9)

Table 4.2 Results of the partial least squares analysis for the relationship between the landmark and outline data for individual species (n ≥ 15)

Table 4.3 Results of the multiple regression of partial warp scores (including the uniform components) onto carapace breadth for individual species (n ≥ 15)

Table 5.1 Fiddler crab species studied at each of five field sites in and around the Pacific entrance of the Panama canal

–  –  –

While the path to a dissertation can be fraught with blood, sweat, and tears, it is also filled with learning, friendship, and fun. Though it be the road less traveled, one quickly learns they are not traveling alone, and it is those traveling companions who deserve praise and thanks and who, in the end, make the trip worthwhile.

First, I would like to thank Jeff Levinton for all he has done as my advisor, for his advice, his support (both moral and financial), his indelible sense of humor, and for putting up with me as a graduate student. I suspect I have been neither a typical nor (perhaps) model student in many ways, and it took a special kind of advisor to see me through the long haul.

Thanks to Jim Rohlf for providing a wonderful framework of statistics and morphometrics and for putting up with my continual questions and comments about various “features” inherent in the invaluable software he has written.

Thanks also for his suggestions and help with the written work presented here, as well as to my other committee members: Geeta Bharathan and Alan Harvey.

Special thanks must also go to Robert Sokal for all of the support and teaching he provided over the years. So much of what I have learned as a graduate student comes directly from working with him and in his lab.

My success (if any) in maintaining sanity while a graduate student would have been impossible without the help and friendship of so many people in and out of the department. Their aid ranged from science to social to personal, but was all certainly invaluable. It would be impossible to list everyone, but some deserve special mention. Dean Adams turned out to be as good a friend as one could wish for; he helped push me in directions I would probably not have dreamed of going. Maureen Olmsted was wonderful down the final stretch, putting up with my stress and foibles, and forcing me to try to relax and enjoy myself, even as the pressure of the impending defense continued to build. Jo Kurdziel, Shirley Baker, and Lisa Suatoni were wonderful, invaluable labmates.

Ehab Abouheif, Barbara and James Thomson, Dennis Slice…thank you all.

While in Panama, John Christy and Pat Backwell provided much needed support, help and advice. Suzanne Williams, Dewayne Shoemaker, and Jeff Hunt deserve special praise for their participation in the perpetual quest for entertainment and food.

Specimens were kindly provided by the US National Museum and Diana Jones of the Western Australian Museum, as well as a number of researchers around the world who had donated specimens to Jeff Levinton for other studies.

Furthermore, the Smithsonian Tropical Research Institute and Recursos Marinos must be thanked for their help and permission to collect and export specimens of a number of Panamanian fiddler crab species.

Funding for this research came from a variety of sources, including Sigma Xi, the Smithsonian Tropical Research Institute, and an NSF grant to Jeff Levinton, as well as smaller pools of money from the Ecology and Evolution Department and Graduate Student Organization at Stony Brook. Support in the

form of research and teaching assistantships also came from a variety of sources:

Robert Sokal, Manuel Lerdau, and the Ecology and Evolution Department.

Last, but by no means least, research and survival expenses were provided by the Albert and Deborah Rosenberg Graduate School Research Contingency Fund. Without their love and support the author would never have survived the trials and travails of graduate school. Thank you for everything you have done for so many years.

CHAPTER 1

INTRODUCTION



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