Conus of the Southeastern United States and Caribbean

Conus of the Southeastern United States and Caribbean

Conus of the Southeastern United States and Caribbean

ALAN J. KOHN

PRINCETON UNIVERSITY PRESS

PRINCETON AND OXFORD

Copyright © 2014 by Princeton University Press

Published by Princeton University Press, 41 William Street, Princeton, New Jersey 08540

In the United Kingdom: Princeton University Press,

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All Rights Reserved

Library of Congress Cataloging-in-Publication Data

Kohn, Alan J.

Conus of the Southeastern United States and Caribbean / Alan J. Kohn.

pages cm

Includes bibliographical references and index.

ISBN 978-0-691-13538-0 (hardback : alk. paper) 1. Conus—Southern States—Classification.

2. Conus—Caribbean Area—Classification. I. Title.

QL430.5.C75K744 2014

594ʹ.3—dc23

2013014701

British Library Cataloging-in-Publication Data is available

This book has been composed in Palatino

Printed on acid-free paper. ∞

Printed in China

1  3  5  7  9  10  8  6  4  2

We come from halls of Academe

And, on an inspiration,

Alone, or in a learned team,

Embark on publication.

We seek to teach, or disabuse,

Where controversy rages,

And press our honest facts, or views,

On academic pages.

Then, if our theories endure,

Maintained by erudition,

Our luck and virtue should assure

A third or fourth edition.

For ultimately all should know

The fruits of our endeavour.

Though scholars come and scholars go,

Our books go on for ever.

—Ralph Lewin, The Book

Often when I do a search, what is in a book is miles ahead of what I find on a Web site.

—Sergey Brin

Study nature, not books.

—Louis Agassiz

Contents

Preface

This book explores the taxonomy and relationships of species of the marine snail Conus. Broadly considered, it is the most diverse, species-rich genus of animals in the sea and a most attractive as well as scientifically and biomedically important group of gastropod molluscs. Here I revise the taxonomy of the species that occupy the Western Central Atlantic and Caribbean region, home to arguably the least known assemblage of species in a genus whose distribution is worldwide but predominantly tropical. As the first attempt in 70 years to treat the genus as a whole in the region, this book includes accounts of nearly twice as many species as the earlier report (Clench 1942). To the extent possible, the book also addresses the roles of Conus in the ecology, evolution, and biogeography of the region; provides information to help understand an important branch on the tree of life; and contributes to documenting the diversity of life in the sea. The adverse effects on and threats to the world’s natural environments by human activities have stimulated biologists to evaluate biodiversity, particularly in places where it has been underappreciated in the past. This also motivated the research that resulted in this book.

In the less than 20 years since its predecessor on the Indo-West Pacific Conus fauna appeared (Röckel, Korn, and Kohn 1995), technological innovations have transformed the practice of systematics. The most profound changes have been new insights into both classification and phylogeny from knowledge of molecular genetics, and the burgeoning of computerized and web-based methods to more efficiently manage, present, and communicate information. I have attempted to take advantage of these advances to incorporate both molecular genetic information and quantitative morphometric methods into conclusions on the validity of described species and interpretations of their evolutionary relationships. I apply and statistically analyze morphometry of shells and of radular teeth, the hollow spears that Conus uses to inject toxic venoms in its rapid-strike, chemically aided prey-capture method. Descriptions of these traits should help readers assess differences among species and their genealogic relatedness. These are nontraditional character sets that are not usually found in books on the taxonomy of shelled molluscs. In order to link scientific research more closely with public understanding, I have attempted to explain these new approaches in order to increase their accessibility and use to nonspecialist readers. In addition, unlike earlier identification guides, this book takes advantage of the resources offered by the worldwide web to complement the printed version.

While the book adopts the general format of Röckel, Korn, and Kohn (1995), the new sources of data have begun to help unravel the especially challenging taxonomic problems of the Western Atlantic species. The Conus Biodiversity Website (http://biology.burke.washington.edu/Conus/) also serves a number of complementary functions to the book. It is an accessible repository of digital images of primary type specimens of most described species, it provides the original descriptions of most species in pdf format, and it is linked to the National Center for Biotechnology Information (NCBI) (www.ncbi.nim.nih.gov) to access gene sequences of species across the genus. Updates and corrections will be posted to the Conus Biodiversity Website as new information emerges, as they have been for the earlier book. In addition, databases listing all specimens used in the comparative morphological and molecular analyses and in establishing the geographic and bathymetric distributions are available as electronic supplementary material, accessible at http://press.princeton.edu/titles/10229.html. The electronic supplementary material also includes summarizing graphs and statistical analyses of these data that support the taxonomic conclusions reached in the text.

In the spirit of the epigrammatic epigraphs prefacing this Preface, I have sought to write a scientifically accurate yet accessible work useful to a diverse readership. However, I have intended to speak particularly to present and future biologists, especially those interested in biodiversity and its evolution. I hope this book will encourage students with fresh perspectives to make new observations and studies that will overcome the limitations of our current knowledge of the systematics, ecology, and evolutionary history of a scientifically and medically important taxon.

A number of promising research projects lurk in the unanswered broader questions raised—for example the unexplored relationships of specificity of venom actions, genetic structure of populations, evolution of life history traits, and geographic distributions of species. Others will perhaps emerge from the incidental reports of unusual events in the lives of Conus, such as pearl secretion, masculinization of females by endocrine disruptors pervasive in 21st-century environments, relations with symbionts, survival from near-fatal predator attack, and injury to humans from venom injection. Thus I also direct the book to other marine scientists, neurobiologists, natural products chemists interested in sources of pharmaceuticals from marine organisms, to nonscientist conchologists and conservationists, and to all who are attracted by the wondrous variety and elegance of molluscs and their shells. As Godfray and Knapp (2004) stated, professional and amateur biologists and naturalists alike want and need stable, informative and accessible classifications that enable easy identification. That may not have been attained, but progress along the road in that direction has been the goal.

Acknowledgments

This project originated with an invitation from José Leal to serve as the R. T. Abbott Visiting Curator at the Bailey-Matthews Shell Museum in Sanibel, Florida, in November, 2000. My research there made it clear that a systematic revision of the Western Atlantic Conus was needed, and that it was a major task that could not be undertaken without considerable external financial support.

Award of a National Science Foundation grant (No. 0316338), including a Consortium of European Taxonomic Facilities supplement, supported much of the research leading to this book. At the University of Washington, Trevor Anderson created the project’s web site and served outstandingly as research technician. Postdoctoral research associates Thomas Duda and Christopher Meyer obtained all of the molecular genetic data and carried out the phylogenetic analyses. The following University of Washington undergraduates participated in data analysis as research students and research assistants: Amanda Bruner, Kathryn Engel, Emily Evenson, Joshua Kubo, Megan Mach, Jennifer Marsh, Amber Matheny, Brenda Mathis, Daniel Okamoto, Michael Queisser, Kamila Rikhsieva, Pairin Schofield, Jessica Smith, Rachel Winstedt, Jihye Won, and Matthew Zhang, as well as a then Yale undergraduate, Kaitlin Curran. Kathy Carr, University of Washington Biological Sciences Librarian, assisted in providing access to resource materials.

This work could not have been completed without the very generous assistance of numerous colleagues in the United States, Latin America, Europe, and Japan. Danker and Elise Vink generously accommodated my study of the Vink collection in their home in Curaçao before donating it to Naturalis, the National Museum of Natural History in Leiden. Emilio Garcia was particularly helpful in providing access to specimens and supplied many images for publication. John Tucker and Manuel Tenorio generously shared specimens, images, and evidence concerning taxonomy. Others who provided helpful information and discussion, and generously made specimens and images available for reproduction in cases of scarce representation in museums and of living specimens, include Cynthia Abgarian, Carlos Afonso, Randy Allamand, Adolfo Borges, Christopher Boyko, Marcus Coltro, Juan Manuel Díaz, Gene Everson, Marien Faber, Bill Fenzan, Mike Filmer, Bill Frank, Frank Frumar, Richard Goldberg, Jon Greenlaw, Wayne Harland, Thomas Honker, Manuel Iturralde-Vinent, Afonso Jório, Paul Kersten, Lee Kremer, Harry Lee, Virginia Orr Maes, Robert Masino, Alexander Medvedev, Paula Mikkelsen, Patricia Miloslavich, Antonio Monteiro, Marc Nathanson, Bette Nybakken, Howard Peters, Richard Petit, Kenneth Piech, Andre Poremski, Colin Redfern, Dieter Röckel, Emilio Rolán, Maria Cristina Sanchez Sarasua, George and Korina Sangiouloglou, Stanley Taylor, Charlotte Thorpe, David Touitou, Amelia Tripp, Everett Turner, Roberto Ubaldi, and Robert Work.

I thank Elaina Jorgensen, who prepared the range maps, and along with Rüdiger Bieler, Elizabeth Boulding, Fabio Moretzsohn, and Gary Rosenberg also provided cogent comments that improved the text; Ursula Smith for suggesting the measure of typical shell length used; and Marla Coppolino, who assisted with preparation of some of the text-figures. Klaus Groh (Conchbooks) permitted the use of material from Röckel, Korn, and Kohn (1995).

At Princeton University Press, Dimitri Karetnikov, illustrations manager, was especially helpful in advising about and ensuring quality control of the illustrations, and Jessica Massabrook executed some of the improvements. Sheila Ann Dean, copyeditor, corrected a number of errors in the author’s manuscript. Mark Bellis, production editor, and Robert Kirk, acquisitions editor, provided assistance and discussion throughout the project.

Specialists on other animal groups who generously helped with identifications of fauna associated with Conus include Stephen Cairns, Gerhard Jarms and Wolfgang Sterrer (Cnidaria); Darryl Felder and Patsy McLaughlin (Crustacea); Harry Lee, Rüdiger Bieler, Matthew Campbell, and Lyle Campbell (Mollusca); and Theodore Pietsch, William Smith-Vaniz, David Johnson, and Ralf Britz (fishes).

Researchers and curators at the following museums and research and academic institutions generously provided access to study material:

Academia Canaria de la Lengua, Spain: Juan José Bacallado

Academy of Natural Sciences of Drexel University, Philadelphia: Gary Rosenberg, Paul Callomon, Robert Robertson

American Museum of Natural History, New York: Paula Mikkelsen, Marla Coppolino, Ross MacPhee, Bushra Hussaini, Sarfraz Lodhi

Bailey-Matthews Shell Museum, Sanibel, Florida: José Leal

Bermuda Aquarium, Natural History Museum and Zoo: Wolfgang Sterrer, Lisa Greene

Burke Museum of Natural History and Culture, University of Washington, Seattle: Robert Faucett, Ronald Eng

Carnegie Museum of Natural History, Pittsburgh: Tim Pearce

Department of Geology, San José State University, California: Jonathan Hendricks

Delaware Museum of Natural History, Wilmington: Elizabeth Shea, Leslie Skibinski

Field Museum of Natural History, Chicago: Rüdiger Bieler, Jochen Gerber

Florida Fish and Wildlife Research Institute, St. Petersburg: Sandra Farrington, Scott Woodruff.

Florida Museum of Natural History, Gainesville: Gustav Paulay, John Slapcinski, Roger Portell

Harte Research Institute, Texas A&M University, Corpus Christi: Fabio Moretzsohn, Noe Barrera

Houston Museum of Natural Science: Tina Petway

Institute of Malacology, Tokyo: Sadao Kosuge

Instituto de Oceanologia, Havana: José Espinosa

Instituto de Neurobiología, Universidad Autonóma de México: Edgar Heimer de la Cotera

Instituto Alexander von Humboldt, Bogota: Juan Manuel Díaz

Löbbecke Museum, Düsseldorf: Jürgen Jungbluth

Museu Nacional, da Universidad Federal do Rio de Janeiro: Renata dos Santos Gomes, Paolo Márcio Costa.

Museu Oceanográfico Prof. E. C. Rios, Rio Grande, Brazil: Paula Spotorno de Oliveira

Muséum d’Histoire Naturelle, Geneva: Yves Finet

Muséum National d’Histoire Naturelle, Paris: Philippe Bouchet, Rudo von Cosel, Virginie Héros

Museum of Comparative Zoology, Harvard University, Cambridge: Adam Baldinger, Murat Recevik

Museum Victoria, Melbourne: Ursula Smith

National Museum of Natural History—Naturalis, Leiden: Jeroen Goud, Frank Wesselingh, Bert Hoeksema, Willem Renema

National Museum of Natural History, Smithsonian Institution, Washington, DC: Christopher Meyer, Jerry Harasewych, Ellen Strong, Stephen Cairns, Alan Kabat, Yolanda Villacampa, Tijuana Nickens, Paul Greenhall

National Museum of Wales, Cardiff: Harriet Wood, Mary Seddon, Graham Oliver

Naturhistorisches Museum Basel: Olivier Schmidt, Felix Wiedenmeyer, Walter Etter

Naturhistorisches Museum, Vienna: Anita Eschner

North Carolina State Museum of Natural Sciences, Raleigh: Arthur Bogan, Jamie Smith

Peabody Museum of Natural History, Yale University: Eric Lazo-Wasem

Rosenstiel School of Marine and Atmospheric Sciences, University of Miami: Nancy Voss

Santa Barbara Museum of Natural History, Santa Barbara: Henry Chaney, Patricia Sedhagian, Daniel Geiger, Eric Hochberg

Senckenberg Research Institute and Natural History Museum, Frankfurt: Ronald Janssen, Rudo von Cosel

Smithsonian Tropical Research Institute, Panama: Félix Rodriguez, Biff Bermingham, Aaron O’Dea

Staatliches Museum für Naturkunde, Stuttgart: Hans-Jörg Niederhöfer, Ira Richling, Annette Schultheiss

Texas A&M University, College Station: Mary Wicksten, Heather Prestridge

Texas A&M University, Corpus Christi: Fabio Moretzsohn, Noe Barrera.

The Natural History Museum, London: Kathie Way, John Taylor, Roberto Miquez

Universidad Central de Venezuela: Adolfo Borges, Cecilia Naranjo

Universidad Nacional Autónoma de México, Querétaro: Edgar Heimer de la Cotera, Manuel Aguilar

Universidad de Cadiz, Spain: Manuel Jimenez Tenorio

Universidad de Oviedo, Spain: Jesus Ortea

Universidade do Algarve, Portugal: Carlos Afonso

Universität Hamburg, Germany: Klaus Bandel

University of Louisiana at Lafayette: Emilio Garcia, Darryl Felder, Suzanne Fredericq

University of Michigan Museum of Zoology, Ann Arbor: Thomas Duda

University of North Carolina Institute of Marine Sciences, Morehead City: Glenn Safrit

University of South Carolina Upstate, Spartanburg: Lyle Campbell

University of Utah: Baldomero Olivera, Maren Watkins

Uppsala University Museum of Evolution, Sweden: Mats Eriksson

Zoological Museum, University of Copenhagen, Denmark: Antonia Vedelsby, Kathe Jensen, Jørgen Knudsen, Ole Tendahl, Danny Eibye-Jacobsen

Zoologisch Museum, University of Amsterdam, Netherlands: Robert Moolenbeek, Bram van der Bijl

Lanna Cheng graciously permitted use of the poem The Book by her late husband Ralph Lewin, and published in Verses (Halobates Press, La Jolla, CA, 2008). The quotation from Sergey Brin appeared in an interview with Motoko Rich published in The New York Times, January 5, 2009. Louis Agassiz’s dictum was posted on the wall of the first seaside teaching laboratory, the Anderson School of Natural History. He founded the school at Penikese Island, Massachusetts, in 1873, and after its closure, the sign was moved to the new nearby Marine Biological Laboratory at Woods Hole (McMurrich 1892; Lillie 1944).

Conus of the Southeastern United States and Caribbean

Introduction

The Purposes of This Book

The main purpose of this book is to present a systematic revision and to facilitate identification of the extant species of Conus in the Southeastern United States and Caribbean region. To accomplish this goal, each species is discussed and described objectively and consistently, including estimating within-species variation, and as clearly as possible differentiating each from its most similar congeners. In biology a picture is worth far more than the proverbial thousand words, and more than 2100 color photographs of shells, on 109 plates, an average of two per species, seek to illustrate the extent of within-species variation and between-species differences. Both the images and the species accounts emphasize the characteristics of the shells of Conus, because most users of the book will probably seek to identify these most durable parts of the animals. In some cases, less commonly used characters, such as shell and radular tooth morphometry, are also described quantitatively. More than 100 text-figures illustrate these and other aspects of Conus biology, which are generally not remarked on. They include photographs of living animals of about 40% of the species covered and radular teeth of about one-third, as well as predation by and on Conus, egg capsules and larval shells, and other organisms associated with their shells.

Similarities and differences in sequences of key genes are analyzed both as taxonomic characters and to evaluate evolutionary or phylogenetic relatedness among species. The rapid advance of molecular genetics during the late 20th and early 21st centuries belies the author’s statement just 17 years ago that the application of additional character sets, e.g. from molecular biological study, awaits the next generation of researchers (Röckel, Korn, and Kohn 1995, 13). Although other attributes of Western Atlantic Conus—for example, specific habitats, feeding biology, reproduction, and geographic distribution—are far less known than for their Indo-West Pacific relatives, available information on these biological features is included.

Fossil shells of Conus in the Western Atlantic region extend back at least to the Late Eocene, about 37 million years ago (Hendricks and Portell 2008), but the geologic record of the genus still remains too poorly known to provide useful insights into the evolution of the region’s modern Conus fauna. For this reason, known fossils of extant species are mentioned, but other aspects of the geologic history of the genus are largely left to future researchers.

Surveying and evaluating the validity of all available described or nominal species proposed for the focal geographic region is a necessary but secondary purpose of the book. Valid nominal species can only be justified by documenting those that are invalid. To accomplish this, separate accounts in Chapter 5 detail each species concluded to be valid, and list and discuss its synonyms and homonyms. The chapter ends with a table summarizing the concluded dispositions of all nominal species known to occur in the region covered by the book.

Why Is Conus Important?

In addition to the fact that for centuries its shells have caught and held the attention of diverse enthusiasts—collectors, naturalists, and artists as well as biologists—Conus is important for several reasons, as discussed below.

Biodiversity. Conus is the largest genus of marine animals, with probably more than 600 species worldwide in tropical and subtropical seas. It is thus a major contributor to biodiversity in the sea. Different marine habitats support different numbers of species, and diversity gradients observed in nature have aided testing hypotheses of the factors that determine why some environments support more co-occurring species than others. Diversity of Conus is highest in the tropical Indo-West Pacific region, where more than 300 species occur. West Africa and its offshore islands constitute the next most diverse region, with 92 species (Monteiro et al. 2004). Remarkable and geologically recent adaptive radiations of Conus in the Cape Verde Islands contribute importantly to this diversity (Cunha et al. 2005; Cunha et al. 2008; Duda and Rolán 2005). The Western Atlantic and Caribbean area ranks third in diversity with at least the 53 species treated here. For reasons explained in Chapter 6, additional species are likely to be validated in the future, and others occur beyond the scope of this volume in Brazil. However, if one calculated diversity as the number of species per unit of the region’s ocean area, the Western Atlantic and Caribbean Conus fauna would probably be more diverse than that of the Indo-West Pacific. The Eastern Pacific tropics are next with 44 species according to a very recent revision (Tenorio et al. 2012), followed by South Africa with about 20 species south of the Indo-West Pacific region (Tenorio and Monteiro 2008). These figures sum to about 525 species worldwide. This is doubtless a conservative estimate, because new species continue to be discovered, including cryptic species whose shells are so similar as to be indistinguishable, but their genes show that they do not interbreed. Of all these regions, the Western Atlantic and Caribbean is taxonomically the least known. That fact most strongly dictated the need for this book.

Distribution and abundance. Conus is exceedingly widespread, occurring primarily throughout the world’s tropical and subtropical oceans. The animals are relatively large (2–10 cm in shell length in the Western Atlantic region, and to 20 cm in the Eastern Atlantic and Indo-West Pacific. In the latter region they are particularly abundant in intertidal and shallow subtidal habitats, and most diverse in depths of one to several meters of water. In the Western Atlantic and Caribbean, however, Conus is generally less abundant, less diverse and less conspicuous in intertidal and shallow subtidal environments. The preferred coral reef habitats are usually deeper, and a higher proportion of species is known only from deeper water than in the Indo-West Pacific. In all geographic regions fewer species occur on continental shelves and slopes. None is known from deeper than 1000 m, less than one-third of the world ocean’s average depth.

Some species of Conus are narrowly restricted geographically, while others are extremely widespread. In the Indo-West Pacific region, some species appear to maintain continuous populations from eastern Polynesia to the Red Sea, across an area comprising one-fourth of the entire world ocean. Many species occupy rather high proportions of this broad expanse, and a few cross the Eastern Pacific to the Pacific coast of Central America. In the Western Atlantic and Caribbean, a smaller proportion of species occupy the entire region, and many are more narrowly restricted, in some cases to one or a few islands or to narrow stretches of the continental coast.

Ecology. In addition to its importance for general marine biodiversity, Conus is notable in that several to many very similar species often co-occur in the same habitat. Up to 36 co-occurring species are known to inhabit single Indo-West Pacific coral reefs. Ecological studies of these assemblages have helped show why tropical reef-associated habitats support such high biodiversity (e.g., Kohn 1959, 2001). The reduced abundance, diversity, and accessibility of Conus populations in the Western Atlantic have impeded comparable studies.

Conus snails possess remarkable chemical expertise, and all whose diets are known are predatory carnivores. They inject potent venoms called conotoxins into their prey through a hypodermic needlelike radular tooth in a unique, rapid-strike process. The venom quickly paralyzes the prey—usually a polychaete worm, fish, or another gastropod—that is then swallowed whole. In past studies, primarily in the Indo-West Pacific and to a lesser extent in the Eastern Pacific, this has aided identification of the natural prey, led to the demonstration that different co-occurring species specialize on different food types, and enhanced understanding of coral reef ecology. As yet very few comparable data exist for Western Atlantic species.

Neurobiology and medicine. Practical applications of Conus to neurobiology and medicine are increasing rapidly. All Conus species that have been examined produce the potent conotoxins mentioned above. Several of these small peptides have been sequenced and synthesized, some are now available commercially, and their genes are also being sequenced. Because most conotoxins block the transmission of nerve impulses, they are now widely used in research on neurobiology. During the 21st century, an average of 180 scientific reports on conotoxins have appeared every year. The use of conotoxin derivatives in medicine is also expanding rapidly. At least three are in current use, and one, a painkiller, has been marketed since its approval by the US Food and Drug Administration in 2004. Several others are in clinical trials, and about 300 patents for medical uses have been awarded.

Evolution. Conus is not only the largest marine gastropod genus, but its number of species is increasing more rapidly than any other whose speciation rates have been studied. Since its origin about 55 million years ago, the fossil record indicates that the number of species has doubled on the average every 6 million years, a diversification rate at least twice that of most tropical marine gastropod genera and families. Although Indo-West Pacific Conus are currently better known, new species may well be evolving more rapidly in the Western Atlantic and Caribbean.

Conservation. Science-based knowledge of the most diverse genus of marine animals is essential for the maintenance and sustainable use of biodiversity. The most important practical applications of such information on Conus have been in neurobiology and medicine as mentioned above, but its susceptibility to very low concentrations of the endocrine disruptor tributyltin, until recently a common component of anti-fouling paints applied to ships, has been demonstrated in widely separate parts of the world. This indicates its ability to serve as an early warning system for marine pollutants.

Despite this abundant evidence of its importance, knowledge of the Conus fauna of the Western Atlantic region remains in a confused state. In fact, Todd et al. (2002, 572) noted when characterizing general molluscan taxonomy and its Neogene geological history in the modern Caribbean area, taxonomic compendia covering the whole of this time interval or region are lacking and the difficulties inherent in accurate taxonomic compilation have, to our knowledge, previously gone unmentioned. In addition, the first species-level, molecular-based phylogenetic hypotheses proposed for Conus (Duda and Palumbi 1999a, 1999b; Monje et al. 1999) appeared little more than a decade ago, and subsequent studies have expanded the coverage to about 40% of the species in the genus (Duda et al. 2001; Espiritu et al. 2001; Duda and Kohn 2005; Kraus et al. 2011; N. Puillandre, P. Bouchet, T. F. Duda, S. Kauferstein, A. J. Kohn, B. M. Olivera, M. Watkins, and C. Meyer, unpublished data¹). The time is thus appropriate for systematic revisions in the light of modern molecular genetic analyses.

Why Is Systematics Important?

Biological systematics is a rather broad term, often defined as the scientific study of diversity or, as Simpson (1961) put it even more broadly: Systematics is the scientific study of the kinds and diversity of organisms and any and all relationships among them. Taxonomy and classification are parts or subdivisions of systematics. Taxonomy is the naming, describing, and distinguishing of species, genera, and higher taxa of organisms. Classification is the hierarchical ordering of biological diversity in those categories. Taxonomy and classification are essential to enable us to understand and communicate about organisms and biodiversity. They also provide the basic data for interpreting the ecological interactions of species (e.g., Kohn 2001) and the hypotheses of phylogenetic, other evolutionary and biogeographic patterns (e.g., Duda and Kohn 2005). The species level taxonomy of Conus is also increasingly important to human health (e.g., Olivera and Teichert 2007). Conus venoms are being modified as painkillers and other medicines. Because every species has up to 100 or more active venom components, and those of every species differ, accurate documenting of source species is required. Thus taxonomy is important because it has a multitude of end users (Godfray and Knapp 2004). For Conus, these include amateurs and naturalists as well as professional biologists across the spectrum from basic physiologists, ecologists, biogeographers, and evolutionists, to more applied conservation biologists, resource managers, and natural product chemists. This book is thus directed to all with a desire to learn about the systematics of sea life.

The Geographic Scope of This Book

The region covered by this book extends from the northern limits of Conus in the western North Atlantic Ocean, along the coast of the United States from North Carolina southward, including the offshore islands of Bermuda and encompassing the Gulf of Mexico and Caribbean Sea, eastward to French Guiana. It is almost exactly the area defined by the United Nations as the Western Central Atlantic or Major Fishing Area 31: It includes the tropical and subtropical waters of the western Atlantic and is bordered by 35º north latitude corresponding to Cape Hatteras in North America, 40º west longitude, 5º north latitude corresponding to the coast of French Guiana of South America, and in the west by the corresponding coastline of South, Central, and North America (Carpenter 2002, iv; www.fao.org/fishery/area/Area31/en).

I define the southeastern United States as the Atlantic coastal region from North Carolina to southern Florida, as well as the Gulf of Mexico coastal region from southern Florida to the Texas-Mexico boundary. The Gulf of Mexico continues southward to the Yucatan Peninsula. A recent compendium also considers the north coast of western Cuba as part of the Gulf of Mexico (Felder and Camp 2009). The Caribbean region is defined as the Caribbean Sea and all of its contents, plus the facing continental margins of North, South, and Central America (Iturralde-Vinent and MacPhee 1999, 6). Although the Bahamas are geographically and geologically separate, I include them in the Caribbean region because their marine biota is closely related. The Caribbean region’s boundaries vary with different authors; Petuch (1987) defines it much more broadly (see Chapter 2 of this book). Subdivisions of the region also vary markedly among authors. I use a rather conservative system based on that of the Atlantic and Gulf Rapid Reef Assessment Program (Kramer 2003). It reflects the region’s tectonic history, so it is presented in Chapter 2 following a brief account of historical geology.

I exclude consideration of the Conus fauna of Brazil for two main reasons. First, Brazil’s marine as well as its terrestrial biodiversity is very high, and numerous species that occur there appear morphologically within the range of variation of more northerly species. Some workers have treated these as conspecifics while others have considered them distinct. However, character analyses remain very limited and molecular genetic data in particular are even sparser. A study of Brazilian reef corals that combined morphological and molecular data (Nunes et al. 2008) showed that some species considered congeneric with northern forms on morphological grounds more likely evolved from southern members of a quite different genus in striking cases of convergent evolution. Their results provide a cautionary lesson for revisionary systematics of other Brazilian marine taxa. A second reason for excluding Brazil from this treatment is its good connections with systematics institutions in richer countries and a strong program of its own (Hine 2008); better positioned Brazilian biologists are beginning to investigate the challenging problems presented by its complex, distinctive, and understudied Conus fauna (e.g., Gomes 2004, 2009, 2011; Gomes et al. 2007).

The Format of This Book

This book’s format generally follows that of an antecedent work on the Indo-West Pacific species of Conus (Röckel, Korn, and Kohn1995).

Chapter 1, Setting the Stage: Approaches, outlines the general principles and methods followed to resolve problems of determining both the species to which a specimen belongs and the classification of species of Conus. It introduces the newer methodology that has become available since the 1995 book was published and that has been incorporated in this one. Chapter 1 also explains and defends retaining all Western Atlantic species in Conus in this book, although some authors have subdivided the original genus into various numbers of other genera.

Chapter 2, Setting the Stage: The Geological Theater and the Evolutionary Play, briefly describes the complex geologic history of the focal geographic area and the evolutionary and biogeographic history of Conus worldwide and particularly in the Southeastern United States and Caribbean region. It ends with a brief history of the study of Conus in the Western Atlantic.

Chapter 3, How to Use This Book, discusses how Conus species are identified and classified, the salient features that each species account addresses, how each account is organized, and the rationale for the order of accounts that comprise Chapter 5.

Chapter 4, Behind the Scenes: Technical Aids to the Species Accounts, gives more details of the topics presented in Chapter 3. It includes glossaries of specialized terms used in shell and radular tooth descriptions and statistical analyses, and brief primers to aid in understanding the statistical methods and molecular genetic analyses.

Chapter 5, Systematic Section: Species Accounts, is the heart and most of the bulk of the book. It follows the principles discussed in the earlier chapters to present the results of the study that assesses the validity of the described extant species of Conus in the focal geographic region.

Chapter 6, Synthesis and Conclusions, summarizes and synthesizes information primarily on taxonomy, natural history, biogeography, and phylogeny, and to a lesser extent on ecology and fossil history; this is based mainly on the species accounts in Chapter 5.

A general glossary, bibliography of literature cited, and index follow.

Access to Additional Information

The Conus Biodiversity Website (http://biology.burke.washington.edu/Conus/) provides considerable important supplementary information, including PDF’s of original descriptions. It also includes videos of behavior in living animals, a format impossible to convey in a printed book. The website also periodically updates Röckel, Korn, and Kohn (1995), and updates to this book will be posted in the future as well.

A companion web site containing the data files and statistical analyses used in the research for this book has been developed and is available from the publisher’s web page (http://press.princeton.edu/titles/10229.html). The data files include collection and repository records and shell and radular tooth morphometric data for the specimens studied, and images of some that could not be included in the book. The statistical analyses summarize how the data were used to test whether characters differ between groups hypothesized as indicating different species. As Chapter 4 describes in more detail, tests of statistical significance yield values of P. The P value is the probability that if the null hypothesis (i.e., that the populations being sampled do not really differ from each other) is correct, the value of the test statistic would be as extreme or more so than the observed value. Thus, the smaller the value of P, the more strongly the test rejects the null hypothesis, and the more likely that the difference between populations is real. The supplementary material therefore presents the analyses resulting in the P values that appear in the text. It enables readers who so wish to replicate, extend, and improve the analyses of data, and it avoids cluttering the species accounts in Chapter 5 with details that not all readers will require.

¹ At the time of writing, a manuscript on species-level molecular phylogeny of Conus by these authors was being prepared for publication. Hereafter it is referred to in the text as Puillandre, et al. unpublished data.

Abbreviations Used in the Text

Abbreviations of repositories. The following is a guide to the abbreviations of museums and other institutions whose collections were used in the research leading to the species accounts in this book.

Other abbreviations used in the text. (For abbreviations of shell and radular tooth characters and statistical terms, see the specialized glossaries in Chapter 4.)

1

Setting the Stage: Approaches

The first step in wisdom is to know the things themselves; this consists in having a true idea of the objects; objects are distinguished and known by classifying them methodically and giving them appropriate names. Therefore, classification and name-giving will be the foundation of our science.

—C. Linnaeus (1735)

Natural scientists are aware that no amount of observational evidence can prove one right, whereas a single new observation may prove one wrong.

—Z. F. Danes (2008)

Scientific hypotheses, no matter how firmly established, are never proved right. They are inherently provisional. Scientists know that the door is always open for new evidence and stronger theories.

—G. Schwed (2011)

Because this book intends mainly to characterize a regional Conus fauna and to aid the identification of its species, we need to first address some general and basic questions about species: What is a species? How are species named? How are species characterized? How are species related to each other? The rest of this chapter outlines some of the methodology that allows pursuit of these questions for specific cases.

What Is a Species?

This question is really two questions, and each has more than one answer. The first is conceptual: How is species as an entity defined? For organisms that reproduce sexually, most biologists will answer that a species is a group of individual organisms and populations of organisms whose members are capable of reproducing by mating among themselves, but not with members of other such groups. A second answer, favored by evolutionary biologists who emphasize that species have an important time or historical dimension, adds that species are evolutionary lineages of ancestors and descendants with spatial and temporal boundaries.

Biologists generally accept these definitions, but they do not always make answering the second question any easier! It is the practical or operational question: How can we take Linnaeus’s first step of discovering, characterizing, delimiting, and identifying particular species? We have only to look at our own species, Homo sapiens, to appreciate that no two members of a species are exactly identical; all individual organisms vary from one another, even identical or monozygotic twins. Our task is to distinguish this within-species variation from the attributes that distinguish similar but different species from each other.

We know very well these characteristics of our own species, and the differences between Homo sapiens and the other primate species that we do not interbreed with. When we attempt to characterize species of animals that are more different from ourselves, however, our options are more limited. In most other animal groups, including gastropods, we know too little to use the breeding criterion, so we are limited to less direct approaches. Practically speaking we use other, more easily observable traits that differ among animals as stand-ins or proxies for the criterion of non-interbreeding. If we find that these traits vary continuously from individual to individual in a large sample, we usually conclude that they all can likely interbreed and share genes, and thus all belong to the same species. On the other hand, if we identify sharp discontinuities or gaps in how several of these characters are distributed among the individuals, we conclude that the sample more likely contains members of more than one species. The key word in this distinction is likely. In more formal language, we hypothesize that our sample comprises representatives of several species. Thus a classification, or an identification of a specimen as a member of a particular species, is a scientific hypothesis. And like any hypothesis in science, it is unlikely that it can ever really be proven to be correct. The best we can hope for is that the various traits of the animals we observe differ consistently among the same individuals, further supporting and strengthening our hypothesis. As in other areas of science we accept those hypotheses for which the supporting evidence is strong and contrary evidence absent or weak (see Sites and Marshall 2004).

A further complicating factor is the time dimension or history mentioned above, because all species change over time. Just as individual organisms have genetically different parents, at any given time a species or population includes members of one or more parental generations and generation(s) of offspring. All of these individuals also differ genetically (except for identical twins), so the variation in a population, and hence in a species, is dynamic, changing from generation to generation. This change of inherited characteristics in time is, by definition, a type of evolution, and it can substantially alter the appearance and other characteristics of a single species during its history.

Finally, there is another definition of the term species, as opposed to a species. Species is a category in the classification of organisms. Because classifications are nested hierarchies, species are, as noted above, groups of individual organisms and populations of individuals, but they are also members of a genus, the next more inclusive category. And genera (the Latin plural is usually used in English) are nested in the next more inclusive or higher category, the family, and so on up the scale of classification to order, class, phylum, and kingdom.

How Are Species Named and Classified?

This framework of our current systems of the nomenclature and classification of organisms dates to the pioneering work of Carl Linnaeus in the mid-18th century. Although primarily a botanist, Linnaeus (1707–1778) viewed nature as a whole and titled his seminal work the Systema Naturae per Regna Triae Naturae, (The System of Nature through the Three Kingdoms of Nature), animal, vegetable, and mineral. Although he recognized that members of all three kingdoms could grow, he distinguished the first two from the third as living, or as he put it succinctly in the first edition of the Systema Naturae (1735), there is no generation from an egg in the mineral kingdom. Today we might express this by saying that a rock lacks a genetic code that would enable it to reproduce another rock.

Linnaeus also argued cogently, first at age 28 in the epigraph of this chapter, in other writings, and in his teaching, for the importance of a uniform system of naming animals and plants. Like babies, these organisms do not come with names; people must name them in order to designate and communicate about them. As Wheeler (2008) aptly stated, Linnaeus captured the imagination of his generation with clever and provocative classifications and a sense of discovery. He opened the world of biological diversity to an ever widening audience and sparked an age of species exploration.

Taxonomists had been interested in Conus before Linnaeus, but the system of naming and classifying organisms that he finalized in the Systema Naturae (Linnaeus 1758) is now universally applied to all animals. His names are binominal and, as the page reproduced from his book shows (Text-fig. 1.1), his classification system takes the form of a nested hierarchy. Linnaeus thus solved the first bioinformatics crisis of the 18th century (Godfray 2002) by providing a single, straightforward method for both naming and classifying any type of organism, and the basic principles of his system remain in use today.

By agreement among zoologists, the tenth edition of the Systema Naturae (Linnaeus 1758) is the starting point of zoological nomenclature, and the oldest acceptable scientific names of animals date from it. In mid-18th century fashion, Carl Linnaeus wrote it and most of his other scholarly works in Latin, and his name appears on the title page as Carolus Linnaeus rather than the native Swedish form. To this day organisms are named in Latin for universality, and because it does not favor any currently used national language.

Text-fig. 1.1. Reproduction of p. 712 of the 10th edition of Systema Naturae (Linnaeus 1758), the first page of Linnaeus’s original description of the genus Conus, including his first infrageneric group ("* Truncati"), and his first three species. This illustrates how Linnaeus described the genus, infrageneric groups, and species, as well as his numbering system, descriptions comprising diagnoses and subdescriptions, and synonymy with references to prior literature. His system has of course been modified and updated over the last 250 years, but the basic framework persists as the standard in zoology.

In his book, Linnaeus (1758) introduced the genus Conus and described 35 species, including one from the Western Atlantic region. He based the genus on the rather simple conical shape of its shells. Part of his original description is Testa univalvis, convoluta, turbinata (shell univalve, spiral, conical) (Linnaeus 1758, 712) (Text-fig. 1.1). The next category lower than and within the genus was the species, and the combination of genus and species names is the scientific name of the species and hence of each individual it includes. We no longer write our books in Latin, so modern standard practice is to indicate scientific names in a font, usually italics, different from the rest of the text, and we follow Linnaeus in capitalizing the first letter of the genus name. Some Latin words, including their plurals, have become so firmly incorporated into the English language that we no longer distinguish them by italics. Commonly used in this book are species (plural: species) and genus (plural: genera), as well as taxon, originally coined in German (plural: taxa).

How Are Species Described?

The rules for introducing previously undescribed species, often referred to as new species, are now set out in the International Code of Zoological Nomenclature (ICZN 1999), specifically in its chapter 3, Criteria of Publication, and chapter 4, Criteria of Availability. Until 1999, publication meant printed on paper, but the Code specifies little about the nature of the paper and printing. New species of animals are typically described in scientific journals that require submitted manuscripts to be refereed and are deemed worthy of publication by knowledgeable experts in a process known as peer review.

While scientists, students, and serious amateurs adhere to this highly desirable principle of scientific publication, the Code does not require it. It considers anything printed on any paper to be a publication, as long as it meets a few basic requirements: its purpose must be providing a permanent and public scientific record, and it must have been produced in an edition containing simultaneously obtainable copies by a method that assures numerous identical and durable copies (Code, Art. 8.1) when it is first issued. Although the Code thus allows anyone to say essentially anything in such a document without jeopardizing its publication status, its Appendix A is titled a Code of Ethics (ICZN 1999). It urges against, but does not prohibit, offensive names and intemperate language. An 18th-century movement urged the rejection of Linnaeus’s names on the grounds that many were pornographic; his anatomical allusions in some descriptions of molluscs, but mainly bivalves, were also considered pornographic. A contemporary proponent of that effort railed, perhaps with some justification: Science should be chaste and delicate. Ribaldry at times has been passed for wit; but Linnaeus alone passes it for terms of science (Da Costa 1776, iv). However, Linnaeus’s names became universally accepted and remain so under today’s code.

Since 1999, methods other than publication on printed paper that mainly entail forms of electronic distribution are accepted as long as the relevant Code requirements are met (Code, Art. 8.6). More recently, amendment of several articles of the Code modified the rules for electronic publication of new names after 2011. The main change requires registration in ZooBank, the official registry of zoological nomenclature, of the work they appear in prior to its publication (ICZN 2012).

Regardless of the mode of publication, it is important to remember that the description of a new species is the hypothesis that the species differs from all others described in its genus, according to a biological, phylogenetic, or other species concept. Like other hypotheses in science it cannot be proven, but can potentially be refuted (see this chapter’s epigraph by Danes 2008). Much more responsibility than honor accrues to the person who describes a new species. The author’s responsibility is to present all possible relevant evidence for and against the hypothesis, and to staunchly defend his/her conclusion.

How Are Species Characterized?

Biologists usually define a species, at least among sexually reproducing animals like humans and Conus, as made up of all the populations of individuals that are capable of mating with each other to produce offspring. For most kinds of animals this interbreeding criterion of the biological species definition cannot be critically tested; one must rely on characters—usually morphological—that are observed or hypothesized to be associated with the capacity to interbreed. Taxonomists frequently use terms like describe a new species and species descriptions. In truth it is not possible to describe a species fully, especially among sexually reproducing species as noted above. And one can never hope to examine every individual of a species to know the full range of variation of all its characters. By describing species, biologists really mean that they are presenting a hypothesis and supporting it with evidence of how much its characters vary among the individuals of the species, and which characters distinguish it from the different species that are most similar to it.

Shell characters. The shell is the mollusc’s castle, and traditionally and historically the shell’s traits have exclusively been used in classifying shelled molluscs. Relatively few original descriptions of shelled marine gastropods mention anatomical features of the animal’s body. Specialists sometimes refer to the body as the soft parts. Some recommend using only shell characters, others recommend using only anatomical information. In an assessment of these disparate approaches to gastropod taxonomy, Schander and Sundberg (2001) found that the outcomes did not differ very much, and they recommended using all available data.

However, the identification and classification of Conus species has been based almost exclusively on shell characters. A good example is our earlier book on Indo-West Pacific Conus (Röckel, Korn and Kohn, 1995; hereafter cited as RKK¹). There we attempted to highlight at least two observable shell characters that differed between the most similar species. We also provided other kinds of information, including color patterns of the body, geographic distribution, habitat and habits, form of radular teeth, and characteristics of eggs and egg capsules. But shell characters determined the decisions that led to our conclusions about species identities.

The shape, sculpture, and color pattern of the durable shells of Conus provide the most easily accessible and practical characters for identification. For that reason this book also primarily emphasizes shell characters and clarifies our present understanding of their usefulness in distinguishing the Conus species of the Southeastern United States and Caribbean region. Chapter 3 defines each shell character and the terms that are used to describe their variation in the systematic accounts of each species in Chapter 5. In particular, shell shape characteristics are described and compared more objectively than in past treatments, by applying quantitative methods to fairly large samples. The section on shell morphometry in Chapter 3 presents the specific characters used, and the General Glossary defines more generally used terms.

Anatomical characters. Except for a few that depict radular teeth, all original descriptions of Conus from the Southeastern United States and Caribbean region were based only on empty shells, and many remain known only in that state to the present time. Unfortunately, the time available to this project permitted obtaining relatively few living and preserved specimens for anatomical study. Among the latter that were available, modes of fixation and preservation varied widely, rendering accurate description of anatomical features of the body impossible in most cases. Observation of living specimens proved even more challenging, but very limited field work and the generosity of several collectors provided photographs that give important information on color patterns of the exposed body in life. These are reproduced as text-figures in the species accounts.

The chitinous, hypodermic needlelike radular teeth of Conus, the animal’s key weapon in its venomaided rapid-strike predation arsenal, often remain in even poorly preserved specimens. Asymmetrical unitary structures of complex shape, the teeth are also suitable for morphometric analysis. Chapter 3 describes the radular tooth characters that are treated qualitatively and quantitatively, Chapter 4 again provides more precise definitions, and the species accounts of Chapter 5 include descriptions and comparisons from all species whose teeth could be characterized.

As was the case in RKK, the shell and animal characters defined in Chapter 3 for species determinations do not always lead to clear decisions about species-level identifications and distinctions. Likely reasons for this region include the following:

1.   The reproductive biology of many Western Atlantic species is characterized by lack of a planktonic larval stage that reduces the ability to disperse and tends to isolate populations, in striking contrast to most Indo-West Pacific species.

2.   The evolutionary history of the Caribbean region and its marine (as well as terrestrial) biota is highly complex.

3.   The accessibility of specimens for morphological study is limited, in large part because of their characteristically deeper habitats and sparser populations.

Offsetting this to some extent are recent scientific developments and the new tools derived from them. These are allowing us to assess additional characters that are likely independent of those used previously. The new procedures can thus help test our hypotheses of species identity and classification more robustly. The most important tools in this new kit are the macromolecules that parents pass to their offspring in the egg and sperm cells at reproduction. Because these new genetic characters may be unfamiliar to many readers, the next section introduces them.

Molecular characters. Recent advances in molecular genetics provide the most important of the new tools for systematics research. This revolution began only 25 years ago with the first successful application of molecular data to elucidate broad patterns of evolutionary relationships among the animal phyla (Field et al. 1988). The first publications employing molecular genetic information to help understand the classification and evolution of Conus appeared scarcely a decade later (Duda and Palumbi 1999b; Monje et al. 1999). This line of research has burgeoned in the last decade, and the species accounts of this book incorporate results to date. Thus, a brief general explanation follows that attempts to present this new information in an accessible and understandable way, so that readers unfamiliar with it will be able to appreciate its application to specific cases. The introduction and appendix of Avise (2002) provide a précis of the field and methods in a few pages. For a more general account, consult a good modern basic biology textbook.

In the mid-20th century, scientists first identified the molecules that comprise our genes and determined how their chemical structure codes genetic information. The field of molecular genetics developed rapidly, vastly increasing our understanding of how the molecular organization of genes provide blueprints for the structure and control of the development and functioning of organisms; the genetic differences among individuals, species, and higher taxa; and their evolutionary histories as well. An early remarkable finding was that whether an organism is a mushroom, mimosa, mouse, or mollusc, or even human, its genetic language is the same. Its genes are large molecules, or macromolecules, of deoxyribonucleic acid (DNA), whose function is conveying information. Although many gene sequences have been elucidated, as yet they have played little role in identification guides and monographic treatments of shelled molluscs. However as we will see, a few particular genes whose attributes make them quite helpful in determining species relationships have now been rather widely studied.

In all organisms, the genetic language in the information-carrying part of DNA macromolecules uses the same small component molecules, called nucleotides or bases, to encode its message, much as written languages employ letters of an alphabet. The sequences of nucleotides, the units or building blocks of DNA, function for the same reason that we use letters, words, and sentences to communicate complex concepts. In both cases, a relatively small number of different