Cephalopods of the Broad Caribbean: Distribution, Abundance, and Ecological Importance

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Heather L. Judkins University of South Florida

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Cephalopods of the Broad Caribbean: Distribution, Abundance, and Ecological

Importance

Heather L. Judkins

A dissertation submitted in partial fulfillment of the requirements for the degree of Doctor of Philosophy College of Marine Science University of South Florida

Co-Major Professor: Joseph Torres, Ph.D. Co-Major Professor: Michael Vecchione, Ph.D. Susan Bell, Ph.D. David Mann, Ph.D. Mark Luther, Ph.D.

Date of Approval: June 10, 2009

Keywords: mollusca, Caribbean diversity, biogeography, latitudinal gradients, coastal Atlantic Ocean

ACKNOWLEDGEMENTS

I would like to acknowledge the team of people who have helped me through this

process. Dr. Joseph Torres, Dr. Michael Vecchione, and my entire committee, Dr. Susan

Bell, Dr. David Mann, and Dr. Mark Luther, have been instrumental in terms of advice,

pathways to follow, and excellent sounding boards for my many questions. I would like to acknowledge Dr. Clyde Roper for his foresight in seeing that I had potential to add a small part of research to the cephalopod scientific community and his words of wisdom and encouragement throughout this entire venture. I would like to thank Dr. Nancy Voss for her advice and guidance in understanding of cephalopod species of the Broad

Caribbean. Her assistance in my work is beyond compare. Dr. Ronald B. Toll and Dr.

Steven C. Hess were instrumental in documenting cephalopod specimen information

from the Hourglass Cruises that were conducted from 1965 through 1967, by the Marine

Research Laboratory of the Florida Board of Conservation on the continental shelf of the

Gulf of Mexico which was included in my dissertation. I also thank Teresa Greely and

Angela Lodge for their assistance throughout the two years of my GK12 Oceans

Fellowship and the opportunity to coordinate the regional competition for the National

Ocean Sciences Bowl that I have been so excited to be a part of for the College of Marine

Science at USF. Lastly, I wouldn’t be where I am without the unfailing support and constant source of smiles from my family and friends who have been there through the ups and downs of my journey. Thank you.

TABLE OF CONTENTS

TABLE OF CONTENTS i

LIST OF TABLES iii

LIST OF FIGURES iv

ABSTRACT v

CHAPTER 1. INTRODUCTION 1 1.1 Broad Caribbean 1 1.2 Cephalopod Biology 3 1.3 Distribution of Cephalopods 4 1.4 Abundance of Cephalopods 4 1.5 Cephalopods in Food Webs 5 1.6 Overall Significance 7 1.7 Study Goals 8 1.8. Study Area 9 1.9 Materials and Methods 9 1.10 References 13

CHAPTER 2. BIOGEOGRAPHY OF CEPHALOPODS OF THE BROAD CARIBBEAN 16 2.1 Introduction 16 Broad Caribbean 16 The Cephalopods 18 Biogeography of Cephalopods 18 Abundance of Cephalopods 21 Ecological Focus 21 Study Area 24 2.2 Materials and Methods 24 Statistical analysis 26 2.3 Results 27 Rapoport’s Rule and Species Richness 27 Cephalopod Biogeography 28 Distribution and Abundance 29 Range Extensions 29 New Species to Area 38 2.4 Discussion 38 Rapoport’s Rule and Species Richness 38 Cephalopod Biogeography 41 i

Distribution and Abundance 43 Range Extensions 45 New Species 45 2.5 References 47

CHAPTER 3. CEPHALOPODA (MOLLUSCA: CEPHALOPODA) OF THE GULF OF MEXICO 52 3.1 Introduction 52 3.2 Major Systematic Revisions 56 3.3 Comparative Assessment of the Group in the Gulf of Mexico 56 3.4 Explanation of Checklist 57 3.5 Acknowledgements 60 3.6 References 61 3.7 Gulf of Mexico Checklist 66 3.8 Taxonomic Summary for Cephalopods of the Gulf of Mexico 73

CHAPTER 4. FIRST RECORDS OF Asperoteuthis acanthoderma (Lu, 1977) (CEPHALOPODA: OEGOPSIDA: CHIROTEUTHIDAE) FROM THE NORTH ATLANTIC OCEAN; STRAITS OF FLORIDA 74 4.1 Abstract 74 4.2 Introduction 75 4.3 Systematics 76 4.4 Description 76 4.5 Discussion 81 4.6 Acknowledgements 86 4.7 References 87 4.8 Figure Legends 88

CHAPTER 5. CONCLUSIONS 94 5.1 Summary 94 5.2 References 100

APPENDICES 102 Appendix A: Regional distribution point coordinates 103 Appendix B: Species richness comparison quadrats 104 Appendix C: Cephalopod distribution maps 105

ABOUT THE AUTHOR End page

LIST OF TABLES

Table 2.1 Regional cephalopod locations 20

Table 2.2 Region, species number and sample number for hotspots 33

Table 2.3 Cephalopod range extensions to Broad Caribbean 35

Table 3.1 Checklist of the Cephalopods of the Gulf of Mexico 66

Table 3.2 Taxonomic summary for cephalopods of the Gulf of Mexico 73

Table 4.1 Measurements of Asperoteuthis acanthoderma specimens 89

Table 5.1 Gulf of Mexico checklist species not included in Ch. II 95

iii

LIST OF FIGURES

Figure 1.1 Current flow through the Caribbean Sea and Gulf of Mexico 2

Figure 1.2 A summary of the role of cephalopods in the world’s oceans 6

Figure 1.3 Study Area 9

Figure 2.1 Current flow through the Caribbean Sea and Gulf of Mexico 17

Figure 2.2 Study area 24

Figure 2.3 Species richness per 5˚ latitudinal band 30

Figure 2.4 Comparison of species richness and number of individuals 30

Figure 2.5 Rapoport’s Rule- Rarefaction curve 31

Figure 2.6 Rapoport’s Rule- Chao 1 estimator graph 31

Figure 2.7 Eight study sites for richness and diversity comparisons 32

Figure 2.8 Species richness regional comparison 32

Figure 2.9 Hotspot species observed- Rarefaction curve 33

Figure 2.10 Hotspot Chao 1 estimator of regional species richness 34

Figure 2.11 Broad Caribbean sample effort map 34

Figure 4.1 Key West Asperoteuthis acanthoderma specimen 91

Figure 4.2 Marathon Asperoteuthis acanthoderma specimen 92

Figure 4.3 Internal organs of the Key West specimen 93

CEPHALOPODS OF THE BROAD CARIBBEAN SEA: DISTRIBUTION, ABUNDANCE, AND ECOLOGICAL IMPORTANCE

Heather L. Judkins

ABSTRACT

The Broad Caribbean region is defined as the Gulf of Mexico, and the coastal and marine areas of the Caribbean Sea, including the chain of islands forming the Greater and

Lesser Antilles, Turks and Caicos, the Bahamas, and the gulf coasts of the United States,

Central and South America (Stanley, 1995). The cephalopods of the Broad Caribbean were examined in terms of distribution, abundance, and ecological importance. A suite of 5190 preserved cephalopod specimens were identified and catalogued to produce regional maps of cephalopod distribution within the Broad Caribbean. Eighteen range extensions were noted for known species. Regional species richness was examined with respect to Rapoport’s Rule with an eye toward possible cephalopod hotspots in the region. Cephalopods of the Broad Caribbean within the latitudinal bands of 8˚N and

30˚N do not support Rapoport’s Rule as they exhibit increasing species richness with increasing latitude. Eight subareas were chosen to compare species richness. Regionally, species richness is patchy, with the largest concentration of cephalopods off the eastern

Florida coast. Areas of the southern Caribbean Sea are in need of more samples for accurate assemblage counts and more meaningful comparisons with other Caribbean regions. Rarefaction curves were used to normalize the variously sized samples throughout the Broad Caribbean. A checklist of the Gulf of Mexico based on literature developed a picture for the northern regions of the Broad Caribbean. This checklist v

provided an updated account of cephalopod species that were reported from smaller literature works. Lastly, the first observation in the North Atlantic Ocean of the deep-sea squid Asperoteuthis acanthoderma (family Chiroteuthidae) was described. The description is based on two nearly intact, but damaged, specimens that were found floating at the surface in the waters off Key West and Marathon, Florida in 2007. All previously known records are recorded from a few specimens scattered in the western

Pacific Ocean. There is a need for increased sampling throughout the Broad Caribbean to explore the systematics, life histories, distribution patterns, and potential fisheries for this group of organisms.

CHAPTER 1

INTRODUCTION

Cephalopods of the Broad Caribbean have not been reviewed in recent years. The unique features, currents, and coastlines of the Gulf of Mexico, Caribbean and the Straits of Florida combine as a potentially unique ecotone for cephalopod distribution, abundance, and diversity. Work conducted by G. Voss (1956), C.F. Roper (1984), N.

Voss (1998), M. Vecchione (2002), and others provide background for further exploration of cephalopods in this area. The present study focuses on over 5000 specimens collected from the area to extend cephalopod research.

1.1 The Broad Caribbean

The Broad Caribbean region is defined as the Gulf of Mexico, and the coastal and marine areas of the Caribbean Sea, including the chain of islands forming the Greater and

Lesser Antilles, Turks and Caicos, the Bahamas, and the Gulf coasts of North, Central and South America (Stanley, 1995).

The region is influenced by waters that flow through the lower Caribbean islands, originating from the Guiana Current that moves north along Brazil’s coast. The Guiana

Current is joined by the North Equatorial Current, which flows through the lower

Caribbean, veering north around western Cuba and into the Gulf of Mexico. Some upwelling occurs along the southern region of the Caribbean Sea (Longhurst, 1998). The majority of the flow moves around the Gulf coasts of the United States, flowing down along the west Florida coast before moving through the Straits of Florida to become the

Gulf Stream which moves northward through the Bahamas and along the eastern coast of

Florida. The general movement of currents in the Broad Caribbean is from east to west with gyres often spinning off the main water flow (Stanley, 1995).

Fig 1.1: Major currents of Broad Caribbean (from Carpenter et al. 2002)

The surface temperature of the ocean in the tropical half of the Broad Caribbean region is averages 27˚C with little variation throughout the year. Temperatures in the southern portion of the Gulf of Mexico also average near 27˚C but the northern Gulf of

Mexico has larger temperature fluctuations due to seasonal changes from 16˚C in winter to 28˚C in summer (Stanley, 1995).

Salinity is relatively high in the surface waters between January and May, 36.36, and lower between June and December in the region, 36.06 (Tomczak & Godfrey, 1994), mainly due to the inflow in late fall of lower-salinity waters from the Orinoco and

Amazon Rivers as well as equatorial convergence coming through the region.

Geologically, the Caribbean Sea consists of two main basins separated by a broad, submarine plateau. Two tectonic plates, the Caribbean plate and the North American 2

plate, potentially influence historical biogeography in the area. The Cayman Trench, a trench between Cuba and Jamaica, contains the Caribbean’s deepest point (7,535 m below sea level).

1.2 Cephalopod Biology

The cephalopods are molluscs with many unique features separating them from other molluscan groups including a closed circulatory system, the reduction and in most cases, absence of an external shell, a sophisticated nervous system, jet propulsion for movement, many camouflage adaptations, and a predatory lifestyle (Brusca, 2003).

Cephalopods possess a biting apparatus resembling an inverted parrot beak, and almost all have some form of radula, or rasping tongue. Food-capturing mechanisms vary from sucker-bearing arms and tentacles to hooks modified from suckers for catching prey. In particular, nektonic cephalopods are impressive predators.

Octopods are adept in stalking or hiding out to attack prey. Neritic octopods home in visually on prey and they approach by partially raising an arm and gliding in that direction. The attack is a pounce during which many of the arms and the web are thrown over the prey to immobilize it. The octopods will then bite and poison the organism

(Vecchione, 2002).

Although research is scare in terms of the life history of many cephalopod species, the consensus is that they possess a fast growth rate and relatively short lifespan.

They grow exponentially until mature and then they spawn and die. Cephalopods have various spawning methods ranging from polycyclic spawning and multiple spawning to intermittent terminal and continuous spawning. All spawning strategies end in the death of the cephalopods after the spawning period (Jereb & Roper, 2005).

1.3 Distribution of Cephalopods

Past cephalopod studies have focused on small pockets of the Broad Caribbean such as the Gulf of Mexico and Florida regions by Voss (1956), the Straits of Florida by

Cairns (1976), the eastern Gulf of Mexico, Passerella (1991), and regions surrounding

Colombia, by Gracia (2002). Cephalopods have various distribution patterns ranging from coastal species to entirely pelagic. Coastal species include the economically important lologinids and octopods. Offshore, the ommastrephids and histioteuthids are of greater importance.

Cephalopod species exhibit considerable diversity in their depth distribution as well. Squid, such as Doryteuthis are surface dwellers living within 500m of the ocean surface while chiroteuthids are deep-sea organisms with ranges down to 4000m and beyond. There are temperature tolerance patterns that exist among cephalopods; certain cephalopods thrive in the warmer waters of the Caribbean proper (Octopus zonatus,

Octopus maya) while others have an affinity for the subtropical temperatures of the northern sections of the Gulf of Mexico such as Ancistroteuthis lichensteinii.

Distribution patterns are important for researchers and fishery experts to understand as conservation measures and management practices are created for cephalopod groups.

1.4 Abundance of Cephalopods:

Since their appearance in the Cambrian, cephalopods have evolved to include some of the largest past and present invertebrates (over 20m) and to become common predators in all shallow and deep seas. For part of life’s history, over 200 million years, they were probably the top predators in the marine environment. After the Jurassic, it is believed that fishes superseded their importance as predators. While fishes and

cephalopods both evolved to cope with the same physical marine environment, much

stimulus to cephalopod evolution also came from their interaction with fish and later with

other vertebrate predators, the reptiles, seals, cetaceans, and birds (Clarke, 1996).

Cephalopod species vary in abundance in the Broad Caribbean ranging from

schools of thousands in Illex species to solitary individuals of Discoteuthis discus and

Asperoteuthis acanthoderma. Cephalopods today are not as numerous as they once were

due to the constant struggle between them and all other marine species, including other

cephalopods. Their present success is apparent in their morphological diversity,

abundance, and major role they play in the ecology of the sea (Young et al. 1998).

1.5 Cephalopods in the food web

Cephalopods are important predators on micronekton and macrozooplankton and

a major food source for nektonic fish. Diets of cephalopods change as they mature. Most begin as paralarvae preying upon small crustaceans, and as they grow, move onto larger crustaceans, fish, and other mollusca. Small, immature longfin inshore squid (Doryteuthis pealeii), for example, will feed on planktonic organisms while larger individuals feed on larger crustaceans and small fish. Studies have also shown that the immature squid will feed on euphausiids and arrow worms while adults feed on small crabs, polychaetes, and shrimp (Cargnelli, 1999). Fish species preyed on by the longfin inshore squid include silver hake, mackerel, herring, menhaden, sand lance, bay anchovy, weakfish, and silversides. As a food source for other organisms, cephalopods have been found in large

numbers in the diets of seabirds, seals, whales, and fish (Cargnelli, 1999).

Prey preference varies among species. The congeners, Doryteuthis opalescens

(Pacific) and Doryteuthis pealeii (Atlantic) are important commercial squid with

different adult sizes and prey preferences. A study by Karpov and Cailliet (1978) found that Doryteuthis opalescens fed mainly on fish, cephalopods, gastropods, and polychaetes. Doryteuthis pealeii were found to eat more equal proportions of fish and fellow squid (Amaratunga, 1983).

Figure 1.2 A summary of the role of cephalopods in the world’s oceans and seas as expressed by their position in the energetic hierarchy. (Clarke, 1996)

Cephalopods are born into the third trophic level and progress one to two stages through their life. Research has not shown them achieving top-predator status because there always seems to be some vertebrate that preys upon them (Summers, 1983). Diving birds such as penguins and murres actively search for cephalopods as part of their diet as do toothed whales and seals. Sei and Fin whales are the major baleen predators on oceanic squid. Those whales seek copepods and euphausiids, which are probably also the prey of squids. Examples of seabirds dependent on cephalopods would be the thick-

billed murres of the North Pacific and the emperor penguins of the Antarctic (Williams,

1995). Ogi lists squid as 72.6% of the diet of thick-billed murres (Summers, 1983).

1.6 Overall significance:

Cephalopods play an important role in the Broad Caribbean region in terms of

fisheries and overall biodiversity. At present, cephalopods contribute only 3% to the

tonnage of global fisheries, but their total value lies third, below only shrimps and tuna

(Clarke, 1996). Cephalopods are important as a food source for humans and well over 3

million tons are caught yearly. Fishing has become increasingly intense in the Orient and

the eastern Atlantic Ocean. Most of the cephalopods caught in the Broad Caribbean were

landed by Mexican fishermen, bringing in between 19,000 and 31,000 tons (Vecchione,

2002).

Ideally, a thorough knowledge of the systematics of a species is the required

foundation upon which all other biological and resource management studies must be

based. For example, in the Gulf of Campeche, Mexico, a traditional fishery was believed

to be based on Octopus “vulgaris” Lamarck, 1798, a ubiquitous octopus of broad

distribution. In the absence of local studies, knowledge about the biology of O.

“vulgaris” from other seas was applied to the Campeche octopus for fishery statistics

and management purposes. The discovery that the octopus was actually a new species, described as O. maya, Voss and Solis, 1966, with a very different life history, explained

the problems that had plagued biologists assigned to study the fishery and develop

recommendations. This example underscores the need for sound systematic knowledge

of species and populations if we are to regulate fisheries for these forms (Roper, 1983).

Biodiversity studies are moving from a focus on individual species to the

ecosystem level. Similarly, fisheries management has progressed from single species to

multiple target species to ecosystems (such as the large marine ecosystem approach of

Sherman et. al. 1990). For an ecosystem management effort to have any chance of success, information is needed on all abundant or ecologically important species

(Vecchione and Collette, 1996). Fisheries management is an integral part of ecosystem management practices. Changes in both targeted and bycatch species need to be

monitored. An example is the fishery for bottom fish on Georges Bank. Of the fish

caught in 1963, 67% were the prized cod, hake, and flounders, whereas 24% was made

up of unwanted species. By 1986 the dominant catch had shifted dramatically, with 14%

wanted species and 74% “junk species”. Such changes in populations of large predators

cause profound effects throughout the food web (Vecchione and Collette, 1996).

1.7 Study Goals

The goals of the present study include elements of biogeography, distribution, and

ecology of cephalopods. They are:

1. To determine the distribution and abundance of cephalopod species in the Broad Caribbean region.

2. To discern general biogeographic patterns of the group in the Broad Caribbean region.

3. To examine the distribution of the group for possible alignment to Rapoport’s Rule (RR) as studied by other authors (Macpherson 2002, Fortes 2004, Rosa et al., 2008).

4. To create a comprehensive checklist of the major species found in the Gulf of Mexico.

5. To describe new species to the region. This includes range extensions for currently known species in the area.

1.8 Study Area

The Broad Caribbean includes the Bahama Islands, Gulf of Mexico, and the

Caribbean Sea. The range for the study was between 8 ° N -30° N and 58° W – 97° W.

Figure 1.3: Study Area

1.9 Materials and Methods

The most helpful taxonomic information include examination of comparative material from a variety of locations, including from the type locality when possible

(Vecchione; Collette, 2000). Based on current cephalopod dichotomous keys, type specimens, literature, and expert opinions, the specimens analyzed were identified to the species level. Once the specimen was identified, it was plotted on a distribution map of the Broad Caribbean using the ArcView 9.2 mapping program.

An acceptable biogeographic study includes many specimens of each species under consideration, including all the life-history stages, precise distribution within the 9

study area, and a complete geographic range of each species. This study included 4190

specimens that had known locales and 1000 secondary regional specimens that were

distributed throughout the Broad Caribbean for a total o 5190 specimens examined.

Many of the regional specimens were from the Caribbean Sea and were important to

include. The regional data was used in the analysis of the distributions of cephalopods but not included for the application of RR.

A key component of biodiversity exploration is the discovery of new species.

Some factors that affect proper identification of cephalopods are the:

- Basis for identification: recent comprehensive reviews are more reliable. - Experience level of identifiers: some taxonomic groups are more difficult than others to identify. - Difficulty of characters necessary for confident identification. - Life-history stages examined. - Conditions of specimens: quality can be greatly affected by methods used for collection, fixation and preservation, potentially limiting or eliminating the usefulness of important characteristics. - Possible presence of similar, easily confused species: confidence in identification is limited. (Vecchione and Collette, 2000)

The above six factors were taken into consideration while the study was

conducted. Identification guides (Voss 1956; Nesis 1975, 1987; Roper and Young, 1984;

N. Voss 1998; Vecchione, 2002) were used to identify each organism to species level.

The majority of the specimens examined had been preserved well and were in excellent condition. The specimens date from 1898 to present.

Identification of specimens was conducted in the micronekton museum at the

College of Marine Science at the University of South Florida, the Rosenstiel School for

Marine and Atmospheric Science, University of Miami as well as the National Museum of Natural History at the Smithsonian Institution in Washington, D.C.. A dissecting

microscope was used to identify small specimens and specific features of the animals.

Micrometer calipers were used for length measurements. The bulk of preserved specimens analyzed were from two institutions, the Smithsonian Institution’s National

Museum of Natural History and the University of Miami’s Rosenstiel School of Marine and Atmospheric Science. Smaller collections from the Florida Fish and Wildlife

Research Institute were also analyzed.

The methods used for identifying and cataloguing specimens were to identify the

individual using the cephalopod dichotomous keys, and to record its mantle length, sex,

number of gill lamellae (octopods), and species name into an excel file for statistical

analysis. If the specimen was in a mixed lot, individuals were separated according to

species. All station and cruise information was copied and put into the additional

collection jars as needed. Once all the organisms were identified, known specimens from

all institutions were also added to the excel file for analysis. Distribution was calculated

using the 9.2 ArcView software program.

Chapter II of the dissertation focuses on the biogeography of cephalopods in the

Broad Caribbean region. Species richness of cephalopods was analyzed for alignment to

Rapoport’s Rule which was proposed by Stevens (1989): that species richness tends to be

greater towards lower latitudes. Potential cephalopod “hotspots” are compared within 8 subareas of the Broad Caribbean and lastly, distribution of all species examined are plotted on regional maps of the area. Eighteen range extensions are added to the cephalopod database for the region. The third chapter of this study utilizes cephalopod

literature as the basis for a species checklist of the Gulf of Mexico. Comprehensive

studies of large oceanic regions are not present in current cephalopod research. The

chapter updates Voss (1956) and utilizes over 40 cephalopod studies of the area to

compile the checklist. Chapter IV describes a range extension of the chiroteuthid,

Asperoteuthis acanthoderma, a species newly found in the Broad Caribbean. It describes

two specimens discovered floating dead at the surface off the coast of Key West and

Marathon, Fl in 2007. Both specimens were examined by the author in collaboration

with experts in the field. Unique defining characteristics were used for identification

with emphasis on the Y-shaped funnel locking mechanism, sucker ring form and

dentition, beak morphology, photophore patch configuration on ventral surface of eyeballs, and the numerous small cartilaginous tubercles that cover the mantle, head and

aboral surface of the arms. The concluding chapter is an overall summary of the Broad

Caribbean cephalopod assemblage.

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CHAPTER 2

BIOGEOGRAPHY OF CEPHALOPODS OF THE BROAD CARIBBEAN REGION

2.1 Introduction

Cephalopod studies in the Caribbean region have not provided a well-rounded,

comprehensive view of distribution and abundance in the group. Various island groups

or individual cephalopod species have been addressed, (Diaz, 2000, 2004; Gracia, 2002)

mainly in coastal waters, but to date, no study describes the Broad Caribbean species

complex as a whole. Rosa et al. (2008) and Smith et al. (2002) conducted literature- based studies on latitudinal gradients of species richness but none have utilized large

numbers of specimens from the region to improve our understanding of cephalopod

ecology. This paper fills that need and based on 5190 specimens, reports on the

distribution, abundance, and diversity of cephalopods in the Broad Caribbean region.

The Broad Caribbean

The Broad Caribbean region is defined as the Gulf of Mexico and the coastal and

marine areas of the Caribbean Sea, including the chain of islands forming the Greater and

Lesser Antilles, Turks and Caicos, the Bahamas, and the gulf coasts of the United States,

Central and South America (Stanley, 1995). The Caribbean Sea proper covers

approximately 1,063,000 square miles while the Gulf of Mexico is smaller, covering an

area approximately 1,592,842 square kilometers (615,000 sq. miles).

The region is influenced by waters that flow through the lower Caribbean islands,

originating from the Guiana Current that moves north along Brazil’s coast. The Guiana

Current is joined by the North Equatorial Current, which flows through the lower

Caribbean, veering north around western Cuba and into the Gulf of Mexico. Some

upwelling occurs along the southern region of the Caribbean Sea (Longhurst, 1998).

Loop Current water moves through the Gulf of Mexico, flowing down the west Florida

coast before moving through the Straits of Florida. The water becomes the Gulf Stream, which moves northward through the Bahamas and eastern coast of Florida. The general

movement of the Broad Caribbean is from east to west with gyres often spinning off the

main water flow. (Stanley, 1995) (Fig. 2.1)

Figure 2.1: current flow through Caribbean Sea and Gulf of Mexico (from Carpenter et al. 2002)

The surface temperature of the ocean in the tropical half of the Broad Caribbean

region averages 27˚C with little variation throughout the year. Temperatures in the

southern portion of the Gulf of Mexico also average near 27˚C but the northern Gulf of

Mexico has larger temperature fluctuations due to seasonal changes: from 16˚C in winter 17

to 28˚C in summer (Stanley, 1995). Salinity is relatively high between January and May

(36.39) and lower between June and December in the surface waters of the region (36.09)

(Tomczak & Godfrey, 1994), due mainly to the inflow in fall of lower-salinity waters from the Orinoco and Amazon Rivers. Geologically, the Caribbean Sea consists of two main basins separated by a broad, submarine plateau. The Cayman Trench, a trench between Cuba and Jamaica, contains the Caribbean’s deepest point (7,535 m) and divides two tectonic plates (Stanley, 1995).

The Cephalopods

Fewer than 1000 species of living cephalopods have been described worldwide; over 720 are listed in the present catalogues (Jereb et al., 2005). Cephalopods occur in all marine habitats, though none are found at salinities less than 17.5. Their depth range extends from the intertidal to over 5,000 m. Due to their accessibility, many of the near surface and coastal cephalopod species of the Greater Caribbean have been studied in detail (Voss 1956, 1973; LaRoe, 1967; Lipka, 1975; Passarella, 1990). Deep-sea species are more difficult to study because of net avoidance and other escape tactics by the cephalopods (Passarella, 1990). A diverse cephalopod fauna is associated with the bottom in both shallow and deep-seas.

Biogeography of the Region

Briggs (1995) divided the Broad Caribbean into four distinct regions: the

Brazilian Province, the Caribbean Province, the West Indian Province and the Carolina

Region. The Brazilian Province occupies the area between the Orinoco delta and Cape

Frio which has a distinct biota because of the habitat change. Almost the entire northeastern coast of South America is virtually devoid of coral reefs and there are vast

stretches of mud bottom. Near the mouths of the rivers, salinity is greatly reduced

(Briggs, 1995).

The West Indian Province includes an extensive geographic area and consists

entirely of islands. Bermuda is an isolated northern outpost while the main portion is an archipelago stretching from the Bahamas to Grenada. Recognition of a West Indian

Province means that the Straits of Florida- only 80 km wide, is an important barrier to the dispersal of the marine shore biota. It seems clear that the barrier results not from distance, but from the fast-flowing Florida Current. The Yucatan Channel is only 180km wide and the passage between Grenada and Trinidad is about 100km wide (Briggs,

1995). The Caribbean Province extends southward from Cape Canaveral in eastern

Florida, Cape Romano in western Florida, and Cape Rojo, Mexico. From those points, it follows the shore all the way to the northern edge of the Orinoco River delta in

Venezuela. The west coast of Florida supports a complex biotic assemblage. From north

to south, warm-temperate species reach their range limits and tropical species make their

appearance at various points. There is also considerable faunal change with depth, the

tropical species being more numerous on the outer edges of the shelf. The northern Gulf

of Mexico is included as part of the Carolina Region. Within this region, the warm-

temperature biota occupies an area north of the tropical boundaries at Cape Romano, Fl, and Cape Rojo, Mexico (Briggs, 1995). Examples of Broad Caribbean cephalopod regional locations (Table 2.1) are as follows:

Table 2.1: Examples of regional cephalopod locations (Clarke, 1996)

Region: Species: Inshore coastal region Octopodidae- rocky or coral shores including continental shelf Sepiolids- sand or mud Loliginidae Seasonally- Ommastrephidae Off slopes and island spawning aggregations slopes Surface water offshore Onychoteuthids, Argonautids, Ommastrephids

Midwater Histioteuthids and Enoploteuthids

The western central Atlantic (WCA) includes the world’s greatest concentration of small countries including the full range of the world’s major political systems. All of the Caribbean Sea and nearly all of the Gulf of Mexico are included within one or another of the region’s 42 jurisdictional units, the largest number found in any ocean area of this size. When the EEZ’s are compared to the geographic and ecological features of the same area, it becomes clear that the countries of the region are faced with managing the biological outcomes of oceanic and ecological processes that operate on a scale that is far larger than any of the region’s individual management units (Smith et al., 2002).

Four commercially important squid species occur in the Caribbean: longfin squid (Doryteuthis pealeii), arrow squid (Doryteuthis plei), brief squid (Lolliguncula brevis), and southern shortfin squid (Illex coindeti). The sharptail shortfin squid (Illex oxygonius) is found as well in the Caribbean region but is often unrecognized in the catches. Octopus maya is a commercially important octopod species. It is important to accurately identify and to determine the distribution of commercially harvested species.

Voss studied the seasonal distribution of the commercially harvested species and found

that their distribution showed a relationship between squid occurrence and temperature, bottom topography, and areas of high productivity (Voss & Brakoniecki, 1985).

Abundance of Cephalopods

Today, cephalopods are important in neritic waters although numerically they only constitute a small part of the shelf fauna. In most nearshore regions they are outnumbered by fish of similar size, except during certain seasons and in some localities.

In oceanic waters they are more diverse in size and play an important role in food webs

(Clarke, 1996).

Abundance of cephalopods varies (depending on group, habitat, and season) from isolated territorial individuals (primarily benthic octopods) through small schools with a few dozen individuals, to huge schools with millions of oceanic squids (Vecchione,

2002). Approximately 109 cephalopod species in 31 families occur in the Western

Central Atlantic Ocean and adjacent areas (Caribbean Sea and Gulf of Mexico). Both decapods and octopods are common in those waters (Vecchione, 2002). Records of cephalopod species in the Gulf of Mexico date back to Leseur (1821), but the modern comprehensive systematics of the group begin with Voss, who reported 24 neritic and oceanic species in 1954, and 42 species in 1956. Since that time, many species have been added to the list (Passarella, 1990).

Ecological Focus

The ecological portion of this paper examines Rapoport’s Rule (RR) by focusing on small-scale patterns within a region that had been described as an ecotone. Stevens

(1989) proposed that the greater biodiversity often seen in the tropics is explained by the fact that tropical species have very narrow ranges while at higher latitudes there is a

higher proportion of species with wider ranges (Stevens, 1989). He explained the pattern

on the basis of differing tolerances of tropical and temperate species to climatic

variations. Organisms inhabiting lower latitudes are subject to less variation in climate,

and therefore their geographical distributions tend to be limited to a narrow climatic

range. Higher latitude species would be adapted to more marked climate variation

(Fortes, 2004).

Biodiversity for the purpose of this study is defined as species richness- numbers

of species per area examined. The species richness correlation is found in all higher taxa

whose geographical ranges are well known, both terrestrial and marine. Rapoport (1982)

had noted that the latitudinal ranges of individual species became smaller in lower

latitudes. Thus more species could be accommodated at lower latitudes because each required less space.

Many studies have tested RR and the outcomes have been mixed. Some authors

(Steele, 1988, Macpherson, 2002; Roy et al. 1998) have found evidence in their studies supporting RR while others (Clarke, 1992; Mokievsky & Azovsky, 2002) failed to find such a relationship (Rosa, et al. 2008). Fortes (2004) examined selected bivalves and

gastropods along the Pacific and Atlantic coasts of the Americas and attempted to

evaluate the applicability of Rapoport’s rule in those regions; he concluded that

Rapoport’s Rule does apply in those cases (Fortes, 2004).

Other studies, such as one conducted by Rohde (1992), suggests that Rapoport’s

Rule does not apply to all taxonomic categories. The study focused on marine teleosts

using data collected from the Indo-Pacific and Atlantic oceans. Rohde (1992) found that

RR does not apply in all range areas within a taxon’s range and that it may be premature

to explain greater species numbers by narrower environmental tolerances of tropical species (Rohde, 1992). The biogeographical pattern proposed by Stevens (1989) has acquired increasing importance among researchers as an explanation for the biodiversity gradient related to latitude (Fortes, 2004). Many studies have utilized a large latitudinal range (ie. 80˚N to70˚S) for analysis while this study will examine a narrow range, 22˚ of latitude, for comparison purposes. Understanding the application of Rapoport’s rule may be essential for conservation and management (Fortes, 2004).

The systematics of cephalopods are rapidly changing, as research has increased in the past 25 years. Phylogenetic relationships among families within the major groups remain uncertain (Vecchione, 2002). Species that have been collected in the Caribbean allow the opportunity to further describe the cephalopod assemblage as a whole as well as addressing the ecological importance of the cephalopods within the region.

The goals of this study were:

1. To examine Rapoport’s Rule within the latitudinal range of 8˚ N to 30˚ N in the Broad Caribbean, looking for an increase in cephalopod diversity at lower latitudes following Stevens (1989) original predictions for RR.

2. To compare the cephalopod species richness to that of other studies conducted (Smith et al., 2002). There are species “hot spots” reported for portions of the Broad Caribbean using a wide range of vertebrate and invertebrate species. The present study will address how the cephalopods fit into that picture.

3. To determine the species composition, distribution and abundance of cephalopod species within the Broad Caribbean region. The specimens examined come from a variety of preserved materials from various institutions within the region. The study will expand on Voss’s work (1956, 1973, 1985) to include all cephalopod species and their importance in terms of abundance, distribution, and ecology.

Study Area:

The Broad Caribbean region includes the Bahama Islands, Gulf of Mexico, and the

Caribbean Sea. The range for the present study is between 8 °-30° N and 60°– 95° W

(Figure 2.2).

Figure 2.2: Study Area

2.2 Materials and Methods

The present study used previously collected specimens, both identified and unidentified, to determine the distribution of all cephalopods in the Broad Caribbean region. The most reliable taxonomic information comes from examination of specimens, in conjunction with, but not limited to, data compiled from sources in the literature. The most helpful taxonomic studies include examination of comparative material from a variety of locations, including specimens from the original type locality when possible

(Vecchione and Collette, 2000). Based on current cephalopod dichotomous keys, type specimens, literature, and expert opinions, the specimens analyzed were identified to the

species level. Once a specimen was identified, it was plotted on a distribution map of the

Broad Caribbean region using the ArcView 9.2 mapping program.

The present study included 4190 specimens that were collected from known

locations, and 1000 specimens collected within less-specific regional locations within the

Broad Caribbean. Twenty coastal regions were arbitrarily assigned for inclusion into the dataset (Appendix A). Many of the regional specimens were from the Caribbean Sea and

were important to include. The regional data were used in the analysis of the

distributions of cephalopods but not included for the application of RR or species

richness analysis.

Identification guides (Voss 1956; Roper and Young, 1984; Nesis 1987;

Vecchione, 2002) were used to identify each organism accurately to the species level.

The majority of specimens examined had been preserved well and were in excellent condition. The specimens dated from 1898 to present. The bulk of preserved specimens analyzed were from two institutions, the Smithsonian Institution’s National Museum of

Natural History and the University of Miami Rosenstiel School of Marine and

Atmospheric Science. Smaller collections from the Florida Fish and Wildlife Research

Institute were also analyzed. The Hourglass cruises were conducted from 1965-1967 in the shelf waters off west central Florida where cephalopod species were identified and documented by Dr. Ronald Toll and Dr. Steven Hess. Approximately 500 specimens were included in the present study from those cruises.

Identification of specimens was conducted in the micronekton museum at the

College of Marine Science at the University of South Florida, the Rosenstiel School for

Marine and Atmospheric Science, University of Miami as well as the Smithsonian

Institution’s National Museum of Natural History. A dissecting microscope was used to identify small specimens and specific features of the animals. Micrometer calipers were used for length measurements.

The methods used for identifying and cataloguing specimens were to identify each specimen using the cephalopod dichotomous keys and then to record its mantle length, sex, number of gill lamellae (octopods), and species name into an excel file for statistical analysis. Once all the organisms were identified, known specimens from all institutions were also added to the excel file for analysis. Distribution was calculated using the 9.2 ArcView software program.

Statistical Analysis

Rapoport’s Rule (RR) was evaluated by using species richness, which is defined here as species number per 5˚ latitudinal bin within the study’s scope (5 bands). This was plotted as species richness versus latitude (Fig. 2.3). Figure 2.4 represents the two variables addressed when comparing the 5 degree latitudinal bins- the number of species, as well as total number of individuals used for calculations in each bin.

Rarefaction curves were created for all 5 latitudinal bands using Primer 6.2 for estimates and graphic output (Fig. 2.5, 2.6). Rarefaction is a tool used to correct for unbalanced sampling structure. The rarefaction curve is produced by repeatedly re- sampling the pool of N individuals or N samples, at random, plotting the average number of species represented by 1,2,….N individuals or samples (Gotelli & Colwell, 2001). It is dependent on the shape of the species abundance curve rather than the absolute number of specimens per sample. This method is valid when the same groups of organisms are being compared and contrasted. Another requisite is that all the habitats sampled be

similar, in this case, coastal habitats. Methods of capture should be similar and lastly,

this method does not specify which species taken from the residue will be present, and it

can only be used to interpolate (Sanders, 1968). The rarefaction curve (Fig. 2.5) is

species observed (Sobs) compared to latitude. A second set of curves (Fig. 2.6) is the

Chao 1 estimator curve which gives a most likely total species estimate for each region

based on the actual sample provided. Anne Chao devised a non-parametric estimator

used for species richness comparisons. It is based on the number of rare species in a

sample and creates an estimate of total species for a region (Magurran, 2004). The Sobs

graph accounts for sample-size differences while the Chao 1 estimator gives an absolute

number for species richness in a region.

Hotspots were calculated using an excel spreadsheet for comparison of species numbers in 8 subareas (Figs. 2.7, 2.8). The 8 sites were chosen by location in the Broad

Caribbean which also correlates with a species richness study conducted by Smith et al.

(2002). The 8 subarea coordinates are in Appendix B. Rarefaction curves for the sites were created using Primer 6.2 for comparison of the species observed and the Chao 1 estimator (Fig. 2.9, 2.10).

2.3 Results

Rapoport’s Rule and Species Richness

Species richness in the Broad Caribbean showed an increase with increasing latitude (Fig. 2.3). The 8-10˚ band showed the lowest species richness, 34 species, gradually increasing up through the highest latitudes to the 26-30˚ band with 77 species represented. Figure 2.4 compares the number of individual cephalopods examined to the number of species found in each latitudinal band. There was an increase in species found

per band while the number of individuals varied among bands. Latitudinal band 11-16˚

N had a decrease in individuals examined while species richness was increasing, which indicates that sampling effort was not the sole factor for species richness increasing northward. The species observed (Fig. 2.5) rarefaction curve shows a trend for all latitudinal bands headed towards asymptote but only the higher latitudes close in on approaching it. The Chao 1 estimator curve (Fig. 2.6) represents the expected number of species found in each band.

Cephalopod Biogeography

Eight subareas (Fig. 2.7) were chosen to compare species richness within the

Broad Caribbean. Each of the regions incorporated features of biogeographical significance; e.g. important current patterns or seafloor features, or exhibited potential as human management areas. These subareas correspond to a biogeography study of various marine organisms compared by Smith et al. (2002) analyzing invertebrates and vertebrates for potential diversity hotspots in the region.

Figure 2.8 compares the 8 subareas and the number of species per region. It shows that subarea 4 (Eastern central Florida) has the highest species richness (n=32), followed by subarea 1, northern Gulf of Mexico (n=27), subarea 3 in the Straits of

Florida (n=22), subarea 8 in the southwestern Caribbean Sea (n=20), subarea 2 in the

West central Florida waters (n=13), subarea 5 with 11 different species, subarea 6 with 4 species, and lastly, subarea 7 with only 3 species types collected. Rarefaction curves were used to determine the expected number of species per sample site as a function of organisms sampled. Table 2.2 is the number of samples and species analyzed for the bar graph analysis.

Figures 2.9 and 2.10 show the rarefaction curves derived for each region.

Subregion 6 was not included due to the low number of samples (n=4). The trendline is similar with differences between subareas in close proximity of one another. Subarea 7 and 8 are both in the lower Caribbean Sea yet show a large difference in both species observed and expected species. Another example of difference in species richness is between subareas 2 and 4. Subarea 2, the eastern central Gulf of Mexico has a much lower number of species observed and expected number of species than subarea 4 of approximately the same latitude.

Distribution and abundance of Broad Caribbean Cephalopods

Distribution maps for each cephalopod species found within the Broad Caribbean are in Appendix C. Species maps are in order by family groups in most cases. All 5190 specimens were located within the distributional effort map shown in Figure 2.11. The figure represents all of the known coordinate sampling sites for specimens as well as the

20 regions created to define areas throughout the Broad Caribbean, including the 1000 specimens that were collected with a regional location but lacked precise latitude and longitude coordinates (Appendix A).

Cephalopod Range Extensions

Range extensions for several species of cephalopods in the Broad Caribbean region were observed based on the dataset collected in the present study. Table 2.3 shows 18 extensions to previously known ranges based on the work of Roper and

Sweeney, 1984; Nesis, 1987; and Vecchione, 2002.

Species Richness by Latitude

80 76 77

60 53 54

40 34

Total # of species # of Total 30

0 8-10 11-15 16-20 21-25 26-30 5 degree latitudinal bins

Figure 2.3: Species richness for all cephalopod species per 5˚ latitudinal bin

RR- # individuals 2500

2000

1500

1000 # individuals 500

0 90 8-10 11-15 16-20 21-25 26-30 RR total species 80

40 # species 30

20 10 0 8-10 11-15 16-20 21-25 26-30 Latitude (deg N)

Figure 2.4: Comparison of species richness and number of individuals 30

Species Observed (RR Analysis)

40 Sobs 26-30

Sobs 21-25

30 Sobs 16-20 Number of Species of Number Sobs 11-15

20 Sobs 8-10

0 1 15 29 43 57 71 85 99 113 127 141 155 169 183 197 211 225 239 253 267 281 295 309 323 337 351 Number of Samples

Figure 2.5: RR rarefaction curves for species observed

RR Chao 1 estimates

100

50 Chao1 26-30

40 Chao1 21-25

Number of Species of Number Chao1 16-20 30 Chao1 11-15

20 Chao1 8-10

0 1 15 29 43 57 71 85 99 113 127 141 155 169 183 197 211 225 239 253 267 281 295 309 323 337 351 Number of samples

Figure 2.6: RR samples; Chao 1 estimator curve 31

1 2 4

7 6 8

Figure 2.7: Eight subareas for richness and diversity comparison; Subarea 1= Northern Gulf of Mexico; Subarea 2= West central Florida; Subarea 3= Straits of Florida; Subarea 4= East central Florida; Subarea 5= Mid-Island Caribbean group; Subarea 6= Southeast Caribbean Sea; Subarea 7= South central Caribbean Sea; Subarea 8= Southwest Caribbean Sea- Colombia area

Species Richness Comparison

Species Number 20

0 1 2 3 4 5 6 7 8 Broad Caribbean Regions

Figure 2.8: Species Richness Regional Comparison; Subarea 1= Northern Gulf of Mexico; Subarea 2= West central Florida; Subarea 3= Straits of Florida; Subarea 4= East central Florida; Subarea 5= Mid-Island Caribbean group; Subarea 6= Southeast Caribbean Sea; Subarea 7= South central Caribbean Sea; Subarea 8= Southwest Caribbean Sea- Colombia area 32

Table 2.2: Region, Species # and Sample # for hotspot comparison

Location Region Species # # samples North GOM 1 27 46 West Central Florida 2 13 151 Straits of Florida 3 22 32 Eastern Central Florida 4 32 68 Mid-Island Group 5 11 17 Southeast Caribbean 6 4 4 South Central Caribbean 7 3 10 Southwestern Caribbean 8 20 25

Hotspot Species Observed- Rarefaction Curve

25 Region1 Region2 Region3 20 Region4 Region5 Region7 Region8 15

10 Cumulative # species Cumulative

0 1 2 3 4 5 6 7 8 9 101112131415161718192021222324252627282930 Sample number

Figure 2.9: rarefaction curve species observed comparison among regions 1-8

Chao 1 Estimate Curve

Region 1

25 Region 2 Region 3 Region 4 20 Region 5 Region 7

Region 8 15

10 Cumulative numberof species

0 1 2 3 4 5 6 7 8 9 101112131415161718192021222324252627282930 Sample number

Figure 2.10: Chao 1 estimated number of species for regions 1-8

Figure 2.11: Sample Effort Map of Study; x= sample site

Table 2.3. Cephalopod distribution and range extensions to the Broad Caribbean

Gulf of Caribbean Atlantic Range Mexico Sea Ocean Extension Architeuthidae Architeuthis sp X X X

Bathyteuthidae Bathyteuthis abyssicola X X X X Bathyteuthis sp. X X X

Chiroteuthidae Chiroteuthis sp. Asperoteuthis acanthoderma X X X Grimalditeuthis bonplandi X Planctoteuthis danae X

Cycloteuthidae Discoteuthis discus X

Cranchiidae Bathothauma lyromma X X Cranchia scabra X X X Egea inermis X Helicocranchia pfefferi X X Leachia atlantica X Leachia lemur X X Leachia spp. X X Liocranchia reinhardti X X Megalocranchia abyssicola X Megalocranchia sp. X X Sandalops melancholicus X Taonius pavo X X Teuthowenia megalops X

Enoploteuthidae Abralia redfieldi X X Abralia veranyi X X X Abraliopsis atlantica X Abraliopsis pfefferi X Enoploteuthis leptura X X Enoploeuthis anapsis X X

Histioteuthidae Histioteuthis corona X X X Histioteuthis dofleini X X Histioteuthis reversa X X Histioteuthis sp. X X Stigmatoteuthis arctura X X

Joubiniteuthidae Joubiniteuthis portieri X

Loliginidae Doryteuthis brasilensis X Doryteuthis ocula X Doryteuthis pealeii X X X X Doryteuthis plei X X X X Doryteuthis roperi X X X X Doryteuthis sp. X X X Doryteuthis surinamensis X Lolliguncula brevis X X X X Pickfordiateuthis pulchella X X X Sepioteuthis sepioidea X

Lycoteuthidae Lycoteuthis diadema X X Lycoteuthis sp. X Lycoteuthis springeri X Selenoteuthis scintillens X X X X

Mastigoteuthidae Mastigoteuthis agassizi X X Mastigoteuthis hjorti X X

Octopoteuthidae Octopoteuthis sp. X Taningia danae X

Ommastrephidae Illex coindetii X X X X Illex illecebrosus X X X Illex oxygonius X Hyaloteuthis pelagica X Ommastrephes bartrami X X X Ornithoteuthes antillarum X X X

Onychoteuthidae Ancistroteuthis lichensteinii X Onychoteuthis banksii X X X Onykia sp. X Moroteuthis aequatorialis X

Pholidoteuthidae Pholidoteuthis adami X X X

Pyroteuthidae Pterygioteuthis gemmata X X Pterygioteuthis giardi X Pterygioteuthis sp. X X X Pyroteuthis margaritifera X X X

Sepiolidae Heteroteuthis dispar X X Nectoteuthis pourtalesi X Austrorossia antillensis X 36

Rossia bullisi X X X X Rossia tortugaensis X X Neorossia sp X X Semirossia equalis X X X Semirossia tenera X X X X Stoloteuthis leucoptera X

Spirulidae Spirula spirula X X X

Thysanoteuthidae Thysanoteuthis rhombus X X

Alloposidae Haliphron atlanticus X

Argonautidae Argonauta argo X X Argonauta sp. X

Bolitaenidae Japetella diaphana X X Bolitana pygmaea X

Octopodidae Bathypolypus bairdii X X X Benthoctopus januari X X Benthoctopus oregonae X X Danoctopus schmidti X X Euxaoctopus pillsburyae X Ocellate Octopods X X Octopus briareus X X X X Amphioctopus burryi X X X X Octopus carolinensis X X Macrotritopus defilippi X X X Octopus filosus (hummelincki) X X Octopus joubini X X X Callistoctopus macropus X X Octopus maya X X Octopus occidentalis X X Octopus americanus X X X Octopus zonatus X Pteroctopus tetracirrhus X X X Scaeurgus unicirrhus X X X X Tetracheledone spinicirrus X X

Tremoctopodidae Tremoctopus gelatus X Tremoctopus violaceus X X X

Opisthoteuthidae Grimpoteuthis megaptera X X Grimpoteuthis sp. X X 37

Opisthoteuthis agassizii X X X

Vampyroteuthidae Vampyroteuthis infernalis X X X

New Species to Area

Two Asperoteuthis ancanthoderma specimens were examined demonstrating a

very significant range extension to the species; the only other specimens found previously

were off the coasts of Japan. Two nearly intact individuals were found floating dead on

the surface of the ocean and collected: one specimen was found off the coast of Key

West, FL and the other off the coast of Marathon, FL. Both specimens were dissected

and analyzed for identification. It was determined that they were both Asperoteuthis acanthoderma. A description paper is in press with the Proceedings of the Biological

Society of Washington (Judkins et al. 2009).

2.4 Discussion

Rapoport’s Rule and Species Richness

Rapoport’s Rule attributes the many observations of increasing diversity with

decreasing latitude to a reduction in size of species’ distributional ranges as you approach

the equator (Rosa et al., 2008). Stevens (1989) supported his claim with studies of

diverse taxa including North American trees, North American marine molluscs,

freshwater and coastal fishes, reptiles and amphibians.

Since that time, many scientists have studied the ecological patterns driving

biological diversity. There have been numerous hypotheses to explain diversity patterns

(Peet, 1974; Evans, 2005) and various groups of organisms have been examined to prove

or disprove RR. Many studies of marine groups have supported RR (Steele, 1988;

Stevens, 1996; Roy et. al. 1998, 2000; Rex et al. 2000, 2005; Macpherson 2002) while

others have failed to find such a relationship (Clarke, 1992; Lambshead et al. 2000;

Mokievsky and Azovsky, 2002; Rosa et al., 2008). The latter studies found a negative

correlation to RR as discussed below.

There have been a few molluscan species richness studies in the Atlantic Ocean to

date (Rosa et al., 2008, Fortes and Absalao, 2004, Macpherson, 2003). Fortes and

Absalao (2004) examined gastropods and bivalves using literature-based studies from

both the Pacific and Atlantic sides of the continental North and South American coasts.

After analyzing 4067 species they determined that RR applied to these organisms on both

coasts. They noted that regional features, such as the size of a biogeographical province, seemed to affect the pattern strongly. They also found support for RR when they incorporated depth into the study.

Macpherson (2003) studied the variability in size of species ranges in terms of depth and latitude for various marine taxa, including cephalopods and fishes in the

Atlantic Ocean. The results showed that RR could hold true for those organisms but was not solely responsible for latitudinal patterns in range sizes.

The research conducted by Rosa et al. (2008) examined cephalopod species of the coastal Atlantic Ocean using primary literature, reports, and online databases. Their

results showed that latitudinal gradients of species richness were present along both

Atlantic coasts, but were distinct from one another. When the median latitudinal ranges

of the Western Atlantic neritic cephalopods were determined, it was evident that the size

of the distributional ranges did not decline with decreasing latitude which means that RR

may not explain the distribution patterns. Stevens, (1996) proposed that RR could extend

to elevation and water depth in terms of species richness. When species’ depths were taken into consideration for the organisms in the western Atlantic, RR was exhibited

(Rosa et al. 2008).

The present specimen-based study showed that the cephalopods of the Broad

Caribbean do not exhibit the diversity patterns described originally by Stevens (1989).

Within the small latitudinal range of 8˚ to 30˚ N, cephalopods of the region increase in species richness with increasing latitude. The lack of concordance with RR in the present study agrees with Rosa et al. (2008). It should be noted that the lowest latitude band, (8˚-

10˚) includes only 3˚ latitude while the other 4 include 5˚ in each band. Therefore, there may be more than the 34 species in the region that the present study suggests. However, the species richness trend is still obvious as latitude increases.

One of the reasons for an increase in species number at higher latitudes could be the convergence of the Florida current and the North Equatorial current in the middle to northern end of the study area. The two currents converge to become the Gulf Stream and may be transporting cephalopods northward. The Florida Current becomes the Gulf

Stream and then leaves the coast of the eastern United States at Cape Hatteras to head across the Atlantic Ocean. This current has a profound influence on the distribution of shore animals in the western Atlantic (Briggs, 1995).

Another factor possibly contributing to the northward increase in species richness is the larger number of studies in the northern Broad Caribbean region. Numerous studies have been conducted in Florida waters which may be contributing to the increased richness of cephalopods in the northern portion of the study area. The RR rarefaction curve (Fig. 2.5) showed a similar richness trend for all regions and pointed out the need

for more sampling in the lower latitudes, as the upper 2 bands were close to asymptote

while the lower 3 bands were still rising. The Chao 1 estimator analysis showed differences among species richness between the bands. Note that the 8˚- 10˚ latitude band approached 60 species expected and then decreased rapidly (Fig. 2.6). A possible reason for the decline is that there was a smaller sample size for that latitudinal band in conjunction with numerous singleton species counted, which caused a decrease in the species richness curve for that region.

Cephalopod Biogeography

Based on range map overlays, Smith et al. (2002) examined the distribution of

1172 vertebrate and invertebrate species and concluded that the area of highest species richness was located in the waters surrounding southern Florida, the eastern Bahamas, and northern Cuba. Secondary centers of diversity were located (in descending order of richness) on the continental shelves of northern South America, Central America, and in the northern Gulf of Mexico. Those patterns are apparently robust as they are repeated in composite distributions for fishes and for other invertebrates taken separately (Smith et al., 2002).

Analyzing the present study’s cephalopod species richness information, eastern central Florida has the highest species richness in the Broad Caribbean (n=32), likely because the Gulf Stream acts as a large transporter of larvae from the southern waters feeding into it. Another possible, but less likely, factor for this subarea’s species richness is that it is a well-traveled path for seasonally migrating cephalopods.

The cephalopods of the Broad Caribbean generally follow the pattern found by

Smith et al.(2002) in that the two regions exhibiting the highest richness were the same in

both studies. However, subarea 6, the southeastern Caribbean Sea, had too few samples

to include in the analysis (n=4). Subarea 7, south central Caribbean Sea, had 10 samples

and was included in the analysis. Smith et al. suggested that the southern edge of South

America was the second richest in terms of species whereas the present study does not

show that trend. The two areas of low sampling effort (6 & 7) over 111 years of

collecting indicate the need for further fieldwork in those regions.

The subarea rarefaction curve displays curious trends within the Broad Caribbean.

It was anticipated that there would be variations in species richness between the major

basins of the Caribbean and the Gulf of Mexico. This does not appear to be the case. For example, subareas 7 and 8 were both located in the lower Caribbean and yet showed significantly different trends in species richness (Fig. 2.9). Another example of a variation within regions can be seen between subareas 2 and 4 in the northern sections of the Broad Caribbean. A reason for the variation in this case could be the intense work that was conducted by the Hourglass cruises in the mid 1960’s by the Marine Research

Laboratory of the Florida Board of Conservation, creating an artifact from sampling efforts. Two experts identified and catalogued cephalopod shelf species which were included in the present study. Although over 500 specimens were included in subarea 2, the species richness of the subarea (n=13) was still lower than subareas 3 (n=22) and 4

(n=32). Another explanation for the increase in species richness in subarea 4 could be

the influence of the water depth changes and flow of the Gulf Stream. These two

examples of variation within regions (Gulf of Mexico and Caribbean basin) exceed the

variations between the northern and southern regions of the study’s scope.

Distribution and abundance

There were 110 cephalopod species from 27 families examined in the present

study. This number is larger than that found in earlier studies (Voss, 1956- 42), but quite similar to more recent work (Nesis, 1975-100), (Vecchione, 2002-109). This study examined unidentified and identified specimens that were primarily from two large institutions.

Broad Caribbean cephalopods are widely distributed, many finding niches within coastal and island ecosystems. The abundance of organisms differs between species, with Doryteuthis plei (n=1205) and Doryteuthis pealeii (n=702) being the most numerous

squid. Doryteuthis plei and D. pealeii move in large schools, are commercially harvested, used in medical studies and are distributed throughout the region. Octopus joubini

(n=351) and Octopus americanus (vulgaris) (n=306) were the most abundant octopods

and are also commercially harvested throughout the region. Over 30 species were

represented by 3 or fewer specimens for the entire region. An example of a lesser known

cephalopod is Discoteuthis discus, found in deep water with little known about its

distribution or biology (Vecchione, 2002). Euaxoctopus pillsburyae inhabit small niches

surrounding a particular island group and only 1 specimen was recorded for this study.

Few deep-sea cephalopods have been collected, indicating the need for increased research

efforts in the area to uncover other unique organisms below 500m with regularity.

Few studies of cephalopod distribution have been reported in context for the

Broad Caribbean area. Two studies that focused on the region were completed by

Barrientos and Garcia-Cubas (1997) and Vecchione et al. (2001). Barrientos focused on

three loliginids, Doryteuthis (Loligo) plei, Doryteuthis (Loligo) pealeii, and Lolliguncula

brevis in the western Gulf of Mexico. The authors associated squid abundance and

distribution with currents, warm layers, fronts, water masses, and climate changes

(Barrientos and Garcia-Cubas, 1997). These results are concordant with the current

findings as D. plei were most abundant (n=1205) followed by D. pealeii (n=702) with L. brevis (n=374) rounding out the top three most abundant cephalopods in this study.

Another study (Vecchione et al., 2001) centered on paralarval cephalopod distribution and abundance in the western North Atlantic Ocean. The two most abundant and frequently collected species were the neritic squids Doryteuthis pealeii and Illex illecebrosus collected north of Cape Hatteras, both valuable fishery resources. The highest abundance and diversity of planktonic cephalopods in the oceanic samples were

consistently found in the vicinity of the Gulf Stream. According to Vecchione (2001) the

most likely species other than D. pealeii to be present in the south is D. plei (Vecchione,

1981). Other Doryteuthis species such as D. ocula are restricted to Caribbean islands

whereas Doryteuthis roperi, once considered a Caribbean species, had a range extension

into the Gulf of Mexico and Atlantic Ocean, demonstrated in the present study.

Doryteuthis pealeii was abundant in the Broad Caribbean in the present study as

well as in Vecchiones’ work while Illex illecebrosus was only present in small numbers

(n=6). Another Illex species, I. coindetii was more abundant in the Gulf of Mexico and

the northern Caribbean (n=82) which suggests that it is better suited for tropical

temperatures than Illex illecebrosus. Findings here differ from Vecchiones’(2001) work

in that D. roperi were abundant (n=89) and found not only in the Caribbean but were

distributed through the Straits of Florida and up the Gulf Stream to the northernmost region of the study. D. ocula is confined to the Caribbean as the 3 specimens revealed in

this study. It should be noted that there seem to be fewer species found in the western regions of both the Gulf of Mexico and the Caribbean Sea. This could be attributed to low sampling effort (Fig. 2.11).

Range Extensions

The observed range extensions are extremely valuable. There have been recent studies conducted (Rosa et al., 2008; Judkins et. al 2008) that compare organisms of the region based on literature sources so to find 18 new extensions based on fresh identification is helpful in studying the biology and habits of the organisms. It is also important as the hunt for new fishery resources increases worldwide.

New Species to the Area

It is not surprising to find a new species in the Broad Caribbean as research funding has decreased and cephalopod studies have been limited in past years. The species described, Asperoteuthis acanthoderma, was found prior to this only in the West

Pacific Ocean. More studies targeting deep water species are needed to determine the role these large and important species play in the oceans food webs as well as learning their biology and habits to better understand cephalopod adaptations.

To summarize, the present study found that 110 cephalopod species of the Broad

Caribbean are dispersed throughout its waters, they occupy a myriad of niches along coastlines and deep water, and there is no support for RR. Hotspots are patchy with the most species richness occurring along the eastern edge of Florida in the Gulf Stream.

The range extensions based on data important to note for future conservation and fishery ventures. Asperoteuthis acanthoderma is a fortunate discovery and begs the question

“what else is down there”? Areas of the southeastern Caribbean as well as the western

Gulf of Mexico appear to be understudied.

The present study is the first to examine the specimen-based species richness area with rarefaction curves to support it, attempting to determine species richness of the

Broad Caribbean region. The study size range is unique in that it is not encompassing numerous latitudes but focusing on 22˚ of a tropical/subtropical area important to a variety of species. Studies surrounding all aspects of cephalopod life- diversity, biology, ecology, and capture methods would improve the world database for these important organisms.

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CHAPTER 3

CEPHALOPODS (MOLLUSCA: CEPHALOPODA) OF THE GULF OF MEXICO

Heather L. Judkins, Michael Vecchione, and Clyde F.E. Roper

(HJ) College of Marine Science, University of South Florida, St. Petersburg, Fl, 33701; USA (email: [email protected])

(MV) NMFS National Systematics Laboratory, National Museum of Natural History, Smithsonian Institution, Washington, DC 20013-7012 USA (email: [email protected])

(CR) Invertebrate Zoology, MRC 118, National Museum of Natural History, Smithsonian Institution; Washington DC 20013-7012 USA (email: [email protected])

3.1 Introduction

The cephalopods of the Gulf of Mexico have not been studied comprehensively

since Voss’ (1956) monograph. Several cephalopod studies have included this region in

broader studies (e.g., Vecchione 2002) or have examined distribution based on limited

geographic area (e.g. Nesis 1975, Passarella and Hopkins 1991). Collectively, approximately 109 species of cephalopods in 31 families occur in the Western Central

Atlantic and adjacent areas, including the Caribbean Sea and the Gulf of Mexico. Both squids and octopods are common in these waters (Vecchione 2002). The present paper updates Voss’ works and summarizes the species found in the Gulf of Mexico to date.

Two major groups of cephalopods exist today: the Nautiloidea, with a few species of the pearly nautilus confined to the Indo-West Pacific, and the Neocoleoidea, consisting 52

of squids, cuttlefishes, octopods, and their relatives. Neocoleoidea comprise more than

700 species worldwide:

(http://tolweb.org/tree?group=Cephalopoda&contgroup=Mollusca). The neocoleoids that

exist today evolved from forms that first appeared in the upper Triassic and Lower

Jurassic (between 200 and 150 million years ago). Although there are relatively few

species of living cephalopods, they occupy a great variety of habitats in all of the world’s

oceans. Individual species may be very abundant and are important in marine food webs.

Some species are major targets for commercial fisheries.

The Neocoleoidea contains two extant Superorders: the Octopodiformes

(octopods and vampire squid) and the Decapodiformes (squid and cuttlefishes). These

groups occupy all major habitats in the oceans from intertidal to great depths (deepest

record is 7279 m, Aldred et al. 1983, Voss 1988) and from southern to northern polar seas. No cephalopods are found in salinities less than about 17.5 practical salinity units

(psu).

Many species of oceanic cephalopods undergo diel vertical migrations, wherein they occur at depths of about 400 m to 1000 m during the day, then ascend to the

uppermost 200 m or so during the night (e.g., Enoploteuthidae, Ommastrephidae).

Abundance patterns vary (depending on group, habitat, and season) from isolated

territorial individuals (primarily octopods and sepioids), through small schools with a few

dozen individuals, to massive schools with millions of oceanic squids.

Although many cephalopods reach large sizes, generally they have a very short

life span. The life expectancy appears to be about 1–2 years in most cephalopods, but

large species of squids and octopods and those in cold water habitats may live longer.

Conversely, some small oceanic squids such as pyroteuthids may complete their life cycles in less than six months. This is part of a life history strategy that seems designed for rapid increase in population size. It has been suggested that this “life-strategy” may

guarantee survival against environmentally stressful conditions, including those by heavy

predation or over-fishing. However, as cephalopod fisheries experienced further

extensive development, parallel concern developed regarding potential overexploitation

(Jereb and Roper, 2005).

Cephalopods are important in terms of food web relationships, commercial

fisheries, and biomedical research. Cephalopods are born into the third trophic level and

progress one or two stages through their life. Research has not shown them as achieving

top-predator status because there always seems to be some vertebrate that preys upon

them (Summers 1983). Cephalopods are active predators that feed upon shrimps, crabs,

fishes, and other cephalopods, and, in the case of octopods, on other molluscs. In turn,

cephalopods are major food items in the diets of toothed whales, seals, pelagic birds and both benthic and pelagic fishes as well as other cephalopods.

Cephalopod fisheries provide an important food source for humans across the globe. Over three million metric tons are caught each year worldwide (Jereb and Roper,

2005). Squid fisheries also have existed in North America, historically principally to provide bait for other fisheries, but recent decades have seen the development of substantial fisheries for food production, as well. The total commercial catch of cephalopods in the Western Central Atlantic varied during 1993 to 1998 between 19,000 tons and 31,000 tons, mostly landed in Mexico (Vecchione 2002). However, Voss reported in 1973 that of the numerous species known on the coasts of Florida, the Gulf of

Mexico and the Caribbean Sea, “only about 12 species seem to have actual or potential

(fisheries) importance” (Voss et al. 1973; p.1). Of those, species that are commercially

important to the Gulf of Mexico include: Octopus maya, Illex coindetii, Doryteuthis

(Loligo) pealei, and Doryteuthis (Loligo) plei (Voss et al. 1985).

Squids also are important to biomedical research; for instance, much of what is known about human neurophysiology results from experiments with the giant axon of squids. Scientists culture squid in laboratories in order to study the giant axon. Lee et. al. (1994) cultured the Indo-West Pacific species Sepioteuthis lessoniana (Ferussac,

1830) for this purpose because of its large hatchlings, and the quality of its large-diameter axons for study (Lee 1994). LaRoe (1971) previously had worked with a Caribbean species, S. sepioidea, for this purpose. Because of the highly developed brain and sensory organs, cephalopods are valuable in behavioral and comparative neuroanatomical studies as well.

The fauna of the Gulf of Mexico lacks the nautiloids and true cuttlefishes but does include sepiolids, myopsid and oegopsid squids, octopods, and the vampyromorph,

Vampyroteuthis infernalis. Published records of cephalopod species in the Gulf of

Mexico date back to LeSueur (1821), but the modern, comprehensive systematic studies

begin with G.L. Voss, who reported 42 neritic and oceanic species in 1956(G. Voss

1956). Since then, many oceanic species have been added to the list (N. Voss and G.

Voss 1962, Roper 1964, Voss 1964, Roper et al. 1969, Lipka 1975, Passarella 1990).

Although the composition of the cephalopod fauna off southern Florida is known almost exhaustively, the fauna of the rest of the Gulf of Mexico is less well studied. The cephalopods of the Mexican waters of the Gulf were reviewed by Salcedo-Vargas (1991)

using specimens and past literature, he reported some questionable identifications. The

most recent compilation of the cephalopods in the Gulf of Mexico is that of Vecchione

(2002).

3.2 Major systematic revisions since 1954

The status of the systematics of cephalopods is rapidly changing, as research has increased substantially world-wide, during the past 30 years. The families of living cephalopods are, for the most part, well resolved and relatively well-accepted. Species- level taxa can usually be placed in well-defined families (Jereb and Roper, 2005).

However, phylogenetic relationships among families within the major groups remain uncertain (Vecchione 2002). Sweeney and Roper (1998, p.561) addressed the confusion, stating, “We realize that numerous systematic problems exist at all taxonomic levels of the Cephalopoda. For example, several higher taxa have been proposed (i.e., superorder

Pseudoctobrachia Guerra, 1992, and order Cirroctopodida Young, 1989).” The resolution of these problems requires considerable research and review, as new cephalopod research initiatives are being pursued globally.

3.3 Comparative assessment of group in GOM

One of the elements absent in current cephalopod research is comprehensive studies of large oceanic or faunal regions. Numerous isolated island studies, studies from a fisheries perspective, or those for biomedical advances do exist, but the need for comprehensive systematics, abundance, distribution, and ecology requires significant attention. The Broad Caribbean Realm, which includes the Caribbean Sea proper, the

Gulf of Mexico, and waters that extend through the Bahamas, is an area that is in need of such comprehensive study. The first author of this study currently is researching this

area. Species that have been collected in the area allow the opportunity to further define phylogenetic relationships within the cephalopods as a whole as well as to address the trophic importance of cephalopods within the region, for example.

Because of the great diversity in the form, habitat, and behavior of cephalopods, no single method is adequate to capture and/or sample the complex cephalopod fauna

(Rathjen 1991). The excellent vision and high mobility of most cephalopods traditionally means that they have been undersampled with standard trawling and collecting protocols.

Despite their limitations, midwater trawls offer a starting point for population assessment of pelagic species and provide minimum estimates of oceanic cephalopod abundance

(Passarella 1990). Numerous facilities around the Broad Caribbean house unidentified cephalopods which when identified, will add further insight to the diversity of the cephalopod families and ecology, and provide a better fisheries perspective about potentially viable future catches in the region.

3.4 Explanation of Checklist

The classification and nomenclature used here follow that of Vecchione (2002), as it is the most recent compilation for the Western Atlantic region. Orders and families are arranged phylogenetically, and genera and species are arranged alphabetically.

Cephalopods are not exclusively benthic as are most other mollusca, and many are highly mobile, pelagic/oceanic species. This habitat niche requires the use of the term “central” in the Gulf of Mexico range column. Depth data and overall range for organisms are in italics where they could not be determined exclusively for the Gulf of Mexico. Depth ranges include paralarval through adult stages, so they represent the total known vertical range for the species. However, most pelagic species exhibit several more specific

ranges during different phases of their life cycles: for example, paralarvae are epipelagic,

restricted to the upper 100–200 m; many then undergo ontogenetic descent, moving into

deeper waters with growth. Adults of many species then exhibit diel vertical migration

from around 400 m to 1000 m during the day into the upper 200–400 m at night to feed.

Very little information is available on biology and lifestyle for many of the deep sea

cephalopods in the Gulf of Mexico; this explains the “unknown” notation in some

columns.

The abbreviations used in the “Habitat-Biology” category are as follows: bat =

bathypelagic (> 1000 m); ben = benthic; cep = coastal surface and epipelagic; crr = coral

reef; cts = continental shelf; dps = deep sea; end = endemic; epi = epipelagic (0–200 m);

ins = insular; mes = mesopelagic (200–1000 m); ner = neritic; oce = oceanic; sft = mud,

sands, clays; sgr = seagrass; shw = shallow water; slp = continental slope. The

abbreviations used in the “Overall geographic range” category are as follows: AT =

Atlantic Ocean; BE = Bermuda; BH = Bahamas; BR = Brazil; CH = Cape Hatteras,

North Carolina; CT = Connecticut; CR = Caribbean; FL = Florida; IO = Indian Ocean;

ME = Mediterranean; N = North; NE = New England; PO = Pacific Ocean; S = South;

SA = South America; ST = Subtropical; T = Tropical; TWA = Tropical Western Atlantic;

UR = Uruguay; W = West; WA = Western Atlantic.

The abbreviations used in the “Gulf of Mexico Range” category vary because of the high mobility of the species. In some cases, a specific region cannot be defined at

this point. Therefore, the term, “central” (cen) is indicative of the mid-Gulf of Mexico

species. The term, “entire” (ent) is used where the species is found throughout all regions

of the Gulf of Mexico. For those species that are found in more than one region, an

overall region is use. For example, instead of “se” and “ne” being used, the term “e”

(east) is used where appropriate.

3.5 Acknowledgements

(HJ) would like to acknowledge Dr. Joseph Torres and the College of Marine

Science at the University of South Florida for providing invaluable guidance, resources, and facilities for furthering her doctoral research.

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Table 3.1: Checklist of cephalopods (Mollusca: Cephalopoda) from the Gulf of Mexico

Taxon Habitat-Biology Depth (m) Overall geographic range GOM range References/Endnotes

Class: Cephalopoda

Order: Spirulida

Family: Spirulidae

Spirula spirula (Linneaus, 1758) oce 550–1000 worldwide T & ST ent 14, 29

Order: Sepioidea

66 Family: Sepiolidae

Austrorossia antillensis (Voss, 1955) oce 305–775 CR, N SA, GOM se 6, 12, 23, 34

Heteroteuthis dispar Ruppell, 1845 mes, oce 200–1000 T, ST worldwide e 14, 16

Rossia bullisi Voss, 1956 end, oce ? T AT ent 12, 34

Semirossia equalis (Voss, 1956) sft 130–260 GOM, N SA ne 6, 12, 23, 34

Semirossia tenera (Verrill, 1880) sft 85–135 NE to GOM & CR ent 6, 12, 31

Order: Myopsida

Family: Loliginidae

Doryteuthis pealeii (LeSueur, 1821) cep, cts 1–366 WA; NS to VE; GOM and CR ent 12, 14, 29

Doryteuthis plei (Blainville, 1823) cep, cts, slp 1–366 WA, GOM, CR ent 12, 14, 29, 34

Doryteuthis roperi (Cohen 1976) cep, cts 1–50 WA, GOM, CR ent 4, 34

Lolliguncula brevis (Blainville, 1823) cts, shw 1–18 WA, GOM, CR ent 12, 29

Pickfordiateuthis pulchella Voss, 1956 sgr 1–30 FK–BR se 14, 34

Sepioteuthis sepioidea (Blainville, 1823) crr, shw 1–20 BE, FL, BH, & CR se 12, 29, 34

Order: Oegopsida

Family: Architeuthidae

Architeuthis dux Steenstrup, 1860 oce, cts 400–1000 AO ent 23 i

Family: Brachioteuthidae

Brachioteuthis sp. epi–mes 1–300 NA, PO, ME e 14, 16, 29

Family: Cranchiidae 67

Bathothauma lyromma Chun, 1906 mes 1–1400 T, ST e 16, 40

Cranchia scabra Leach, 1817 oce 2–1000 T, ST worldwide ent 12, 14, 16

Egea inermis Joubin, 1895 oce 1–800 TA, WP, IO e 14, 16, 40

Helicocranchia pfefferi Massy, 1907 oce 1–500 T, ST worldwide e 14, 16

Leachia atlantica (Degner, 1925) oce 1–2000 T, ST ent 16, 40, 44

Leachia cyclura LeSueur, 1821 oce 1-2000 T, ST worldwide ent 40

Leachia lemur (Berry, 1920) oce 1-2000 T, ST worldwide ent 40

Liocranchia reinhardti (Steenstrup, 1856) oce 1–1200 circumglobal e 12, 14, 16

Megalocranchia spp. oce 1–2000 T, ST worldwide e 16, 22

Family: Cycloteuthidae

Cycloteuthis sirventi Joubin, 1919 oce 200-1000 T, ST AT ? 15, 29

Discoteuthis discus Young and Roper, 1969 oce 1–700 AT, S PO e 14, 16, 25

Discoteuthis laciniosa Young and Roper, epi–mes 400-1000 T, ST, AO, IO, PO ? 45, 48 1969 Family: Enoploteuthidae

Abralia redfieldi Voss, 1955 epi, ins 1–200 T, ST WA e 12, 14, 34

Abralia veranyi (Ruppell, 1844) oce, slp 20-800 T, ST AT, E AT ent 12, 14, 34

Abraliopsis atlantica Nesis, 1982 mes 1–1000 T, ST AT e 16, 48

Abraliopsis pfefferi Joubin, 1896 mes–bat 1–200 T, ST AT, IO, W PO e 2, 12, 14, 16

Enoploteuthis leptura (Leach, 1817) oce 200–800 T, ST AT, IO, W PO e 12, 16

Family: Magnapinnidae 68

Magnapinna sp. bat, oce 1000–4000 GOM, NA cen 32 ii

Family: Pyroteuthidae

Pterygioteuthis gemmata Chun, 1908 oce 1–-600 T worldwide e 16, 23

Pterygioteuthis giardi Fischer, 1896 oce 1–600 T, ST worldwide e 12, 16, 23

Pyroteuthis margaritifera (Ruppell, 1884) oce 75–500 T, ST AIWPO e 12, 16, 25

Family: Ancistrocheiridae

Ancistrocheirus lesueuri Orbigny, 1839 mes 1–700 T, ST worldwide e 12, 14, 16, 25, 46

Family: Histioteuthidae

Histioteuthis bonnellii (Ferussac, 1834) oce 1–2000 T, ST worldwide cen 14, 41

Histioteuthis corona (Voss & Voss, 1962) oce 200–1000 T, ST worldwide e 12, 16

Histioteuthis reversa (Verrill, 1880) oce 1–1000 ? cen 12, 29, 34, 42

Family: Bathyteuthidae

Bathyteuthis abyssicola Hoyle, 1885 oce 200–4000 T, ST worldwide e 12, 16, 34

Family: Chtenopterygidae

Chtenopteryx sicula (Verany, 1851) mes, oce 200–1000 AT, PO, ME e 14, 16

Family: Lepidoteuthidae

Lepidoteuthis grimaldii Joubin, 1895 oce ? T worldwide ent 12, 14, 16

Family: Lycoteuthidae

Lampadioteuthis megleia Berry, 1916 mes, oce 200–1000 AT, SPO e 14, 16, 29

Lycoteuthis lorigera (Steenstrup, 1875 ) mes, oce 200–1000 WA, GOM cen 14, 21, 29, 34 69

Lycoteuthis springeri (Voss, 1956) end, oce 200–1000 T WA cen 12, 34

Selenoteuthis scintillans Chun, 1900 oce 200–800 WA, GOM e 14, 16

Family: Ommastrephidae

Hyaloteuthis pelagica (Bosc, 1802) oce 1–200;1700 T, ST worldwide ent 12, 13, 23, 34

Illex coindetii (Verany, 1839) cts, ner, oce 1–1000 AT ent 14, 22, 25, 29

Illex oxygonius Roper, Lu, and Mangold, ner, oce 50–500 WA se 12, 14, 29, 31 1969 Ommastrephes bartramii (LeSueur, 1821) oce 1–1500 worldwide ent 12, 29, 31

Ornithoteuthis antillarum Adam, 1957 ner, oce 1–1000 PO, AT ent 14, 16, 29, 31

Sthenoteuthis pteropus (Steenstrup, 1855) oce 1–1500 T, ST Pan-Atlantic ent 16, 29, 34

Family: Chiroteuthidae

Chiroteuthis joubini Voss 1967 mes, oce 200–1000 ST AO, IO e 16, 48

Chiroteuthis veranyi (Fersussac, 1834) mes, oce 200–1000 T, ST W AT, E PO ent 12, 34

Chirotuethis mega (Joubin 1932) mes, oce 200–1000 ? e 16, 48

Grimalditeuthis bonplandi (Verany, 1839) oce 200–1500 AT, GOM cen 12, 29, 34

Planctoteuthis danae (Joubin, 1931) mes, oce 200–1000 worldwide T, ST cen 29

Family: Pholidoteuthidae

Pholidoteuthis adami Voss, 1956 oce 20–230 PO, GOM, AT cen 14, 34

Pholidoteuthis boschmai Adam, 1950 mes, oce 200–1000 ST worldwide cen 29, 48

Family: Octopoteuthidae

Octopoteuthis megaptera (Verrill, 1885) mes, oce 200–1000 T, ST A se 12, 34 70

Octopoteuthis sicula Ruppell, 1844 mes, oce 200–1000 T, ST A, IWP ? 15, 48

Tanangia danae Joubin, 1931 oce 25–300 T, ST worldwide e 12, 16, 24

Family: Onychoteuthidae

Moroteuthis aequatorialis Theile, 1920 oce 100–1000 T, ST AT, IO, W PO e 12, 48

Onychoteuthis banskii (Leach, 1817) oce 100–1000 Worldwide se 7, 12, 14, 34, 38

Onykia carriboea LeSueur, 1821 epi, oce 1–200 T, ST worldwide e 12, 34

Family: Thysanoteuthidae

Thysanoteuthis rhombus Troschel, 1857 oce 25–85 day nets AT, PO, IO, ME e 12, 14, 16, 25

Family: Mastigoteuthidae

Mastigoteuthis agassizi Verrill, 1881 oce 200–1000 T, ST A e 16, 29

Mastigoteuthis hjorti Chun, 1913 oce 200–1000 T A cen 29

Mastigoteuthis magna Joubin, 1913 oce 200–1000 N AT, GOM cen 29

Family: Joubiniteuthidae

Joubiniteuthis portieri (Joubin, 1912) oce 1–1500 AO, PO ent 2, 3, 12, 14, 16

Order: Octopoda

Family: Opisthoteuthidae

Opisthoteuthis agassizi Verrill 1883 ben, cts 100–1000 AT, PO ent 12, 29, 33, 34, 36

Family: Octopodidae

Benthoctopus januarii (Hoyle, 1885) dps 400–750 GOM, CR, TAT cen 12, 29

Octopus briareus Robson, 1929 shw ? W N AT, SE USA, BH, CR s 12, 29 71

Octopus burryi Voss, 1950 cts 10-200 GOM, CH to BR e 12, 29

Octopus defilippi group shw 6– > 60 WA, FL to BR e 12, 16, 29

Octopus hummelincki Adam, 1936 shw 1–200 TWA, FL to BR se 29

Octopus joubini Robson,1929 cts, shw 1–80 TWA ent 12, 29

Octopus macropus group shw ? TWA se 12, 29

Octopus maya Voss & Solis Ramirez, 1966 sgr, shw 1–50 S GOM s 12, 29

Octopus mercatoris Adam, 1937 ? ? GOM ? 29

Octopus cf. vulgaris group cts 1–200 WA, CT to BR ent 12, 29

Pteroctopus schmidti (Joubin, 1933) dps 300–1200 Scattered se 29

Pteroctopus tetracirrhus (Chiaie, 1830) cts, sft 100–750 WA, CH to UR ent 12, 29

Scaeurgus unicirrhus (Chiaie, 1839-1841) sft 100–400 WA, N CH to S BR e 15, 29

Tetracheledone spinicirrus Voss, 1955 sft 200–400 GOM s 12, 29

Family: Alloposidae

Haliphron atlanticus Steenstrup, 1861 oce 1–700 AT, PO, IO T, ST ent 12, 14, 16, 34

Family: Ocythoidae

Ocythoe tuberculata Rafinesque, 1814 mes, oce 1–200 T, ST worldwide cen 48

Family: Bolitaenidae

Bolitaena pygmaea (Verrill, 1884) oce >1000 T, ST WA ?

Japetella diaphana Hoyle, 1885 dps 600–4000 T, ST worldwide e 5, 12, 16, 45

Family: Tremoctopodidae 72

Tremoctopus violaceus Chiaie, 1830 oce 1–250 T, ST worldwide se 12, 14, 25, 34

Family: Argonautidae

Argonauta argo Linnaeus, 1758 oce 1–155 T, AT, PO, ME e 12, 16, 34

Argonauta hians Lightfoot, 1786 29

Order: Vampyromorpha

Family: Vampyroteuthidae

Vampyroteuthis infernalis Chun, 1903 bat 100–3000 T, ST worldwide ent 12, 14, 16, 30, 34

Table 3.2: Taxonomic summary for Cephalopods of the Gulf of Mexico.

Component Subgroups Total Species Number Endemic Number Non- indigenous species Only 2 known at this Spirulida 1 Not enough study time Sepiodea 5 yet to give good 1 Myopsida 6 account Oegopsida 58 1 Octopoda 22 Vampyromorpha 1

CHAPTER 4

FIRST RECORDS OF Asperoteuthis acanthoderma (Lu, 1977) (CEPHALOPODA:

OEGOPSIDAE: CHIROTEUTHIDAE), FROM THE NORTH ATLANTIC OCEAN,

STRAITS OF FLORIDA

Heather Judkins, Debra A. Ingrao and Clyde F. E. Roper

(HJ) College of Marine Science, University of South Florida, 140 7th Ave South, St.Petersburg, FL 33701; [email protected]

(DI) Mote Marine Laboratory, 1600 Ken Thompson Parkway, Sarasota, FL 34236; [email protected]

(CR) Musuem of Natural History, Smithsonian Institution, Washington D.C. 20013- 7012 USA; [email protected]

4.1 Abstract The first observation in the North Atlantic Ocean of the deep sea squid

Asperoteuthis acanthoderma (family Chiroteuthidae) is reported here from off the coast of Key West, Fl in the Straits of Florida. We describe the morphology of the two nearly complete, but damaged, specimens. A third record is based on photographs of a specimen from off Grand Cayman Island; this specimen was not available for examination. The multiple occurrences of this species, heretofore unknown in the North Atlantic Ocean, within a 10-month period are so unusual that we attempt to hypothesize an explanation

for these events. All previously known records are recorded from a few specimens

scattered from Hawaii to the Philippines. The present specimens were identified by the

following characteristics unique to the species: Y-shaped funnel locking apparatus,

sucker ring form and dentition, beak morphology, photophore patch configuration on

ventral surface of eyeballs, and numerous, small cartilaginous tubercles that cover the

mantle, head and the aboral surface of the arms.

4.2 Introduction

A mature female Asperoteuthis acanthoderma was discovered approximately 90

miles southwest of Key West, Florida on February 20, 2007. It was found floating at the

surface above a bottom depth of approximately 259 meters. The specimen was retrieved

by a charter boat captain, Clint Moore, who recognized the uniqueness of the squid and

donated it to Mote Marine Laboratory in Sarasota, Florida. This specimen is now located

in the cephalopod collection of the Smithsonian Institution’s National Museum of Natural

History in Washington D.C. A second specimen was found by Captain Jack Carlson in

the Straits of Florida, 16 miles east of Marathon, Florida in June 2007, floating at the

surface above a water depth of approximately 355m (24˚43’N 81˚06W). This specimen

is deposited in the Marine Invertebrate Museum at the Rosenstiel School of Marine and

Atmospheric Sciences, University of Miami, in Miami, Florida (UMML 31.3212).

The posterior portion of the primary fin is missing in the Key West specimen, so

the mantle length (ML) is measured from the anterior tip of the mantle, along the dorsal mid-line, to the posterior end of the existing portion of the fins. Also missing are both tentacular clubs and stalks, with the exception of a very short section of the left tentacle.

Internal structures are in relatively good condition, including the female reproductive

organs, so that the principal specific characters are present except for those found on the

tentacular clubs.

The Marathon specimen compliments the Key West specimen by having more

complete tentacles that show the photophore patches along their lengths, and it retains the

majority of the pair of flaps known as the “secondary fin” or “tail flap” along the sides of the tail. The tentacular clubs and eyes are missing. Although the internal organs are damaged, sufficient evidence remains to indicate that the specimen is a spent female.

4.3 Systematics

Asperoteuthis acanthoderma (Lu, 1977)

Diagnosis.---A chiroteuthid with mantle, head and arms covered with numerous, minute cartilaginous tubercles; photophore patch present on ventral surface of eyes; 3-4 broad, rounded teeth on arm-sucker rings; funnel locking apparatus an inverted Y-shape. (Lu,

1977)

Material examined.---Specimen 1. (Fig. 1) Female, 620+ ML, 90 miles southwest of

Key West, FL. Found floating dead at surface. The posterior tip of the mantle, primary,

and secondary fins are missing. When approximate measures are used, the TL is

estimated to have been 1250 mm. Specimen 2.(Fig.2) Female, 1630 mm ML, and 3420

TL; measured to tip of tail posterior to “tail flap”.. Found floating dead at surface, 16

miles off Marathon, FL.

4.4 Description

External anatomy.---The description is based primarily on the Key West

specimen with additional details included from the Marathon specimen as appropriate.

The mantle is long, narrow, semigelatinous, with dark purple pigmentation. Numerous,

minute cartilaginous tubercles cover the mantle, head and arms. The mantle is tapered posteriorly towards the fins. The fins together form an elongate oval shape and are estimated to have been 220 mm long (including estimated length of missing portion). The fin length is therefore approximately 50% of ML. The width of the fins is 340 mm at their widest part. The tail with its posterior extension of the gladius and lateral structures is missing altogether. The Marathon specimen had a nearly complete fin assemblage with only the very tip of the tail missing. The fin length measures 460 mm, the tail is 610 mm long. The fin width measures 330 mm and the secondary fin width is 235 mm. The fins and tail flaps are each elongate oval-shaped. The fins become proportionately narrower posteriorly. The tail flaps are very thin, while the fins are noticeably thicker.

The funnel is large in comparison to the head. It measures 173 mm from the anterior funnel opening to the posterior border along the ventral midline. The diameter of the anterior funnel aperture measured (flattened) is 86 mm. The funnel locking apparatus is ovoid and is in an inverted Y-shape; the mantle component matches the funnel counterpart. The dorsal component of the funnel organ is roughly diamond shaped with

one triangular flap on each side. The ventral pads are present and oval shaped. The flaps

form a skirt-like sheath that is attached to the dorsal surface of the funnel organ

suggesting that this organ hangs ventrally open while the animal is alive. The funnel

valve is very large.

The head is elongate, narrow; it is deep dorsoventrally, narrow laterally.

Olfactory papillae are present on each side of the postero-lateral surface of the head in the

form of a slender stalk with a bulbous terminal head. The eyes are large with a ventral

photophore patch that extends toward the posterior surface of each eye. Diameter of right

eye, 28mm; horizontal opening of the eyes: left, 44 mm and right, 37 mm. The nuchal

cartilage is long and narrow; the central groove is distinct.

The arms are very long and attenuate. Little difference is apparent among the

lengths of arms, but only two are completely intact. The intact AL of right arm I is 880

mm and of intact left arm IV, 870 mm. All arms have approximately the same semi-

gelatinous consistency and appear to be closely equal in diameter at their bases. Right

arm III has a distinct keel distally, but no other keels are omm. able. All arms have

trabeculae along the oral bases from which the sucker stalks arise. The arm suckers are

biserial and evenly spaced. The diameters of the suckers range from 4 mm to 12 mm on each arm, varying slightly between arms but consistently patterned small- enlarged- small as they progress distally. On the arms that are intact, the tips have minute suckers on small stalks, clustered together much more closely than along the rest of arms. The arm sucker rings have 3 to 4 broad, rounded teeth around the rim.

The remnants of the tentacles of the Key West specimen have only short, extremely thin stalks that extend from the arm crown. The longest remaining portion is on the right side and it measures 100 mm with no visible photophore patches. The

Marathon specimen has larger tentacle remanants measuring 1560 mm on the left side and 780 mm on the right side. No tentacular clubs are present. The tentacles have photophore patches scattered along their length in no discernable pattern. Forty such patches occur on the most intact (left) tentacle of the Marathon specimen.

The gladius was not extracted from the Key West specimen because it is broken in many places. The gladius of the Marathon specimen is in much better condition. The gladius is approximately 1630 mm long and 74 mm wide at its widest point. The most

anterior portion of the gladius is flattened and becomes rounded as it extends to the

posterior end. The gladius could not be completely reconstructed because pieces are missing.

The buccal membrane has 7 connectives that attach on the dorsal sides of the bases of arms I and II and on the ventral sides of arms III and IV. The lappets are too indistinct to be counted.

The beaks were extracted from the Key West specimen for examination and preservation. The anterior tip of the upper mandible is narrow, sharply pointed. It has a deep, dark brown pigmentation. The hood is normal in size and has a brownish coloration that lightens toward the edges, which are translucent in appearance. The curve of the dorsal half of the hood margin of the beak is irregularly shaped, not smooth. The anterior tip of the lower beak also is pointed with its inner edges curved. It is somewhat broader than the upper mandible, with dark brown pigmentation and the edges of the wings are a lighter brown in tone.

The radula has 7 teeth per transverse row. The width at the dorsal side of the radula measures 4 mm, while the ventral portion of the set measures 3.5 mm. The length of the radula is 14 mm. The rhachidian tooth has a long central cusp with shorter, lateral cusps. The first lateral tooth is bicusped, with a long, pointed cusp and a shorter, blunt lateral cusp. The second lateral tooth is pointed with a broad base but no lateral cusp.

The third lateral tooth is longer than the other lateral teeth and is pointed and curved.

Most of the surface of the squid is covered with cartilaginous tubercles. They are very numerous and thickly-concentrated on the head, mantle and aboral surfaces of arms.

There appear to be fewer on the oral surfaces of arms. Each tubercle has a wide base that

ends with a pointed cartilaginous tip. Numerous dark purple chromatophores cover the squid, as well. Histological sections of the tubercles of the mantle wall indicate that they are similar to a published description (Roper and Lu, 1990), as well as in the original description of the mantle by Lu (1977) which states that there is an outer vacuolated dermal layer followed by a longitudinal muscle layer, an exceptionally thick vacuolated medullary layer, an inner circular muscle layer and the lining of the mantle cavity.

Internal anatomy.---The internal organs of the Key West specimen are in relatively good condition, while the organs from the Marathon squid are significantly deteriorated. Key West specimen (Fig. 3): The gladius extends the length of the mantle on the internal dorsal side. The gills extend approximately half the length of the mantle cavity on both sides, lateral to the digestive gland. The ink sac is small and appears to be empty; it was difficult to locate during dissection. The nidamental glands lay medial to the gills. They are paired, oval, enlarged and milky white in appearance; the right gland is damaged by a tear. The branchial hearts are small, white, and round; they are located posterior to the kidney at the base of each gill with the systemic heart lying along the central midline, dorsal to the nidamental glands. The digestive organs are intact; the stomach, thin walled, and collapsed, leads to the caecum, which is creamy white in color, and thick with an ovoid spongy, reticulated mass. The ovary is posterior to the digestive organs, translucent and appears empty of oocytes and eggs. All organs appear proportional in size compared with mantle length, with the exception of the substantially enlarged nidamental glands.

4.5 Discussion

The first species of Asperoteuthis was originally desribed as Chiroteuthis acanthoderma by Lu (1977) from the tropical western Pacific. Nesis (1980) moved this species to the new genus Asperoteuthis. He considered C. acanthoderma Lu, 1977 to be a junior synonym of Aspreoteuthis famelica (Berry 1909), described from a damaged specimen caught near Hawaii. Subsquent studies found that A. famelica was actually

Mastigotuthis famelica (Young, 1978), so the valid name for Lu’s specimens is

Asperoteuthis acanthoderma (see Young et al. 2007, Arkhipkin et. al, 2008). We identify the present specimens as Asperoteuthis acanthoderma because of the unique characteristics that exist based on Lu’s description of the species.

The genus Asperoteuthis is distinguished from the other genera of the family

Chiroteuthidae by the presence of a terminal photophore on the tentacular clubs and an elongate oval photophoric patch on the ventral surface of each eyeball; the absence of intestinal photophores and of a tragus/antitragus in the funnel component of the locking apparatus.

Other features that distinguish Asperoteuthis from other chiroteuthids include 1) the structure of arm IV is similar to that of arms I-III, not significantly enlarged in advanced subadults; 2) absence of characteristic pairs of adjacent club suckers drawn together with an intermediate widening on the stalk and absence of an enlarged, central tooth on the club suckers as occurs in other chiroteuthids; and 3) the forked (Y-shaped) funnel cartilage

Asperoteuthis acanthoderma (Lu, 1977) is characterized by the possession of numerous, minute, sharply pointed, conical cartilaginous tubercles distributed over the

entire surface of the mantle, head, and arms. The tubercles measure 1 mm in diameter

and 0.4 mm in height from a specimen of 144 mm ML. The tubercles are discrete structures, and their bases are embedded in the dermis of the mantle (Roper & Lu 1990, as C. acanthoderma). The small number of rounded teeth on the arm suckers (3-4) and the prominence if the funnel valve (Tsuchiya & Okutani 1993) are additional specific characteristics.

The morphological characteristics of our specimens, that are about 4 times larger than the holotype and paratype, conform closely with the original description, which was based on females of 188 mm and 144.5 mm ML. Exceptions are minor, such as the inconspicuousness of the dermal tubercles on the smaller specimens, and the number of knobs on the tentacular stalks. We concur with Tsuchiya and Okuntani, (1993) that these and other minor differences are attributable to variation due to the size and stages of maturity of specimens.

Distribution.---Asperoteuthis acanthoderma has been recorded in the central and western Pacific and Indo-Pacific waters as follows: in the southern part of Philippine Sea and in the Celebes Sea to the west, southeast, and east of the Philippine Islands by Lu

(1977) and Nesis (1980), (as Chiroteuthis acanthoderma and Mastigoteuthis famelica, respectively). A specimen of A. acanthoderma was recorded near the bottom by a

SERPENT-Project ROV off western Australia (18˚30’S, 115˚30’E) at 580 m depth in

April, 2005 (Vecchione pers. omm..).

A recent survey of literature of the cephalopods of the Gulf of Mexico revealed

that only three genera of Chiroteuthids previously have been recorded there: Chiroteuthis

joubini, Chiroteuthis veranyi, and Chiroteuthis capensis, as well as Grimalditeuthis

bonplandi (Verany, 1839) and Plancoteuthis danae (Joubin, 1931) (Judkins et. al, in press). The present report of A. acanthoderma is therefore a dramatic range extension into the North Atlantic.

Information on the vertical distribution of Asperoteuthis acanthoderma is limited,

but the following capture data indicate that this is a deep-sea species (as also

demonstrated by its morphology and rarity of capture):

Holotype.---914-0 m (Lu 1977).

Paralarvae.---Daytime 600-1100 m and night 700-925 m (Roper & Young 1975).

Night on horizon of 200-300 m, (Lu 1977, Nesis 1980). Based on the limited information, we believe that the vertical movements of A. acanthoderma may not be ontogenetic descent but diel vertical migrations as Nesis (1980) suggested. This is similar to other chiroteuthids (Roper & Young 1975).

The state of knowledge about the chiroteuthids is expanding as teuthologists discover and report new findings of genera and species. For example, Young et. al.

(2007) published information of a new Asperoteuthis species found off the coast of

Hawaii. Asperoteuthis mangoldae (Young, Vecchione, & Roper, 2007) shares some A.

acanthoderma characters but differs in the absence of tubercles in the skin; a more

gelatinous consistency of tissues; the absence of an anti-tragus in the funnel locking

apparatus; 8-10 slender, truncated teeth on the arm sucker rings; club and club

photophore structure and fin length characteristics. Arkhipkin and Laptikhovsky (2008)

introduced a fourth species to the Asperoteuthis genus, Aspreoteuthis nesisi which shares

many characteristics of A. acanthoderma, such as the funnel locking apparatus, the

numerous tubercles on head and mantle, and the photophore patches on eyes.

Asperoteuthis acanthoderma may be a circumglobal species whose broad

distribution has just recently been recognized because of fortuitous findings of specimens

and intensified research in previously under-sampled study areas. The global

understanding of the oceanic environment and its inhabitants is enhanced as those who participate in maritime activities, deep sea fishermen, for example, become more cognizant of their surroundings and the organisms that inhabit their specific regions. Our knowledge is advanced when they report their observations and findings to marine scientists.

The two specimens we examined from off Florida and the one record via photos of A. acanthoderma in Grand Cayman suggest that certain physical parameters of the region may be different from earlier years. All three specimens were found within a 10- month period from mid-2006 to May 2007, rare discoveries that seem to be more than coincidental. Even though they appear to be spent females that could have drifted to the surface, a typical event for many deep sea squids and octopods, the total absence of specimens in the North Atlantic Ocean until now could suggest additional causative effects.

Based on our detailed examination of the two large, nearly intact specimens, and our comparisons with descriptions in the literature, we conclude that our specimens are indeed A. acanthoderma. Consequently, this species is now shown to occur not only in the tropical western Pacific Ocean, but also in the Caribbean/Gulf of Mexico/Straits of

Florida region.

4.6 Acknowledgments

Photos were taken by Chuck Stevenson at Mote Marine Laboratory, for which we are grateful. We acknowledge the enormous help of the faithful Mote Marine lab volunteers as the dissections were conducted. We also thank the two captains from the fishing vessels that made the original finds and contacted us. Captain Clint Moore found the Key

West specimen on February 20, 2007, while Captain Jack Carlson discovered the specimen off Marathon, FL on May 17, 2007; He coordinated with Gabe Delgado of the

Florida Wildlife Research Institute to ensure retrieval of the specimen. We appreciate the help of Mike Vecchione, NMFS Systematics Laboratory, Natural Museum of Natural

History, Washington D.C., and Nancy Voss, Rosenstiel School of Marine and

Atmospheric Science, and their expertise during the examination of material and the preparation of this manuscript. Heather Judkins acknowledges the College of Marine

Science at the University of South Florida for the opportunity to pursue her scientific goals. Clyde Roper acknowledges with appreciation the association with and support of

Mote Marine Laboratory as an adjunct scientist.

REFERENCES

1. Judkins, H, M. Vecchione, & C. F. E Roper.In press. Cephalopods (Mollusca: Cephalopoda) of the Gulf of Mexico. Gulf of Mexico Origin, Waters and Biota Biodiversity, Volume 1 (Darryl L. Felder and David A. Camp, editors, Texas A&M University Press, College Station, Texas).

2. Lu, C. C. 1977. A new species of squid, Chiroteuthis acanthoderma, from the Southwest Pacific (Cephalopoda: Chiroteuthidae). Steenstrupia, Zoological Museum of University of Copenhagen; 4:179-188.

3. Nesis, K. N. 1980. Taxonomic Position of Chiroteuthis famelica Berry (Cephalopods, Oegopsida). Byulleten Moskovskogo Obsestva Ispytatelei Prirody (Otdel Biologicheskii); 85 (4): 59-66. ------. 1982. Cephalopods of the World, Squids, Cuttlefishes, Octopuses, and Allies. T.F.H. Publications, Inc. 385 pp.

4. Roper, C. F. E. and R. E. Young, 1975. Vertical Distribution of Pelagic Cephalopods. Smithsonian Contributions to Zoology, no. 209: 51pp. ------& C. C. Lu, 1990. Comparative Morphology and Function of Dermal Structures in Oceanic Squids (Cephalopoda). Smithsonian Contribution to Zoology, no. 493: 41 pp.

5. Tsuchiya, K. and T. Okutani. 1993. Rare and interesting squids in Japan, recent occurrences of big squids from Okinawa. Venus, 52 (4): 299-311.

6. Young, R. E., 1991. Chiroteuthid and related paralarvae from Hawaiian waters. Bulletin of Marine Science, 49(1-2): 162-185. ------& C. F. E. Roper. 1999. Asperoteuthis acanthoderma (Lu, 1977). Version 01 January 1999. (under construction). http://tolweb.org/Asperoteuthis acanthoderma/19466/1999.01.01 in the Tree of Life Web Project, http://tolweb.org/ ------, M. Vecchione, & C. F. E. Roper. 2007. A new genus and three new species of decapodiform cephalopods (Mollusca: Cephalopoda). Review of Fish Biology and Fisheries, 17:353-365.

4.8 FIGURE LEGENDS

Fig. 1. Key West Asperoteuthis acanthoderma specimen.

Fig. 2. Marathon Asperoteuthis acanthoderma specimen.

Fig 3. Internal organs of Key West specimen: A. digestive gland B. gill; C. nidamental glands; D. branchial heart; E. stomach; F caecum; G. ovary.

Manuscript Note.---After the manuscript was completed, we received information that an additional specimen of Asperoteuthis had been found floating at the surface by a fisherman five miles south off Little Cayman Island in the northern Caribbean Sea on 18 May 2008. It was donated to the Little Cayman Research Center for identification by station manager, Jon Clamp, who in turn, contacted us for positive identification via photographs. The damaged specimen had a mantle length of approximately 152.4 cm when collected. The specimen will be deposited at the Smithsonian Institution along with the Key West specimen once additional studies have been conducted. We thank Jon Clamp, Judie Clee, and the fisherman who discovered the specimen for their efforts to insure that the specimen was made available for study and permanent deposition.

Table 4.1. Measurements of specimens (mm).

Key West Marathon Sex Female Female

Mantle Length: 620 1630

Total Length

(existing portions): 1817 3420

Mantle width: 190 210

Head length : 230

Head width: 35 50

(eye to eye)

Funnel valve length: 55 n/a

(base-tip)

Funnel valve-base width: 60 n/a

Fin length (primary): estimated 220 460

Total fin length: n/a 610

Fin width primary: 340 330

Secondary fin width: n/a

Tentacle length: R: 100 + L: n/a R: 1560+ L: 780

Club length: n/a n/a

Arm length I: R L R L

880(ti) 655 845 810

Arm length II: 895 680 1030 970

Arm length III: 1000 897 760+ 1100

Arm length IV: 560 870(ti) 520 825

Sucker diameter I: 1st 30cm tip 1st 30cm tip

(right) 4 6 2 5 6 0.7

Sucker diameter IV: 4 4 1 4.5 4.5 4.5 (left) Eye diameter: 28 n/a

Ti= to tip, complete; + = feature incomplete/broken

Figure 4.1. Key West Asperoteuthis acanthoderma specimen.

Figure 4.2. Marathon Asperoteuthis acanthoderma specimen.

Figure 4.3. Internal organs of Key West specimen: A. digestive gland B. gill; C. nidamental glands; D. branchial heart; E. stomach; F caecum; G. ovary.

CHAPTER 5

CONCLUSIONS

Summary

The cephalopods of the Broad Caribbean are widely distributed with

concentrations along the continental shelves. There are gaps in the collections from the western Gulf of Mexico and the Caribbean Sea, both nearshore and offshore, which are important to investigate further. Distribution maps (Appendix C) display a wide variety of localities that the cephalopods occupy with island nations hosting many octopod species.

According to the present study, Rapoport’s Rule does not apply to the cephalopods of the Broad Caribbean. This finding is supported by a literature survey conducted by Rosa in 2008 (Rosa et al., 2008) describing species richness of cephalopods along the Atlantic coast. Cephalopod species richness increased with increasing latitude

contrary to Stevens’ (Stevens, 1989) belief that species richness increases towards the

equator. The search for diversity “hotspots” of the Broad Caribbean was not conclusive

in most instances as the sample sizes were too small to allow the rarefaction curves to

reach asymptote. According to the analysis, region 4, the eastern coast of Florida

exhibited the highest species richness (n=32). Species richness may be higher here

because of increased nutrient mixing in the Gulf Stream, patterns of current transport in

the region and presence of both shallow and deep water habitats existing along the

eastern Florida coast. Collection intensity could have been an attributing factor to

increased richness although the majority of the rarefaction curves were headed towards an asymptote. The low sample size in the southeastern Caribbean Sea (n=4) displays the need for increased study to enrich the cephalopod knowledge base in that region.

The Gulf of Mexico species checklist exposes the advantages and pitfalls of creating species checklist studies today based on literature alone. The literature provided an excellent collection of species that are found within the region, dating back to the

1800’s. However, when it is compared to the actual data collected in chapter 2 of this study, discrepancies were discovered.

Table 5.1: Gulf of Mexico Checklist Species not included in Ch II:

1. Brachioteuthis sp. 10. Chiroteuthis veranyi 2. Leachia cyclura 11. Chiroteuthis mega 3. Cycloteuthis sirventyi 12. Pholidoteuthis boschmai 4. Discoteuthis laciniosa 13. Octopoteuthis sicula 5. Histioteuthis bonnelleii 14. Mastigoteuthis magna 6. Chtenopteryx sicula 15. Octopus mercatoris 7. Lepidoteuthis grimaldii 16. Pteroctopus schmidti 8. Lampadioteuthis megaleia 17. Ocychoe tuberculata 9. Chiroteuthis joubini

Seventeen species (Table 5.1) were found in the Gulf of Mexico checklist were

not found in the biogeography study described in chapter 2. If the biogeographical

results are combined with the checklist, the result is a total of 127 cephalopod species that

are found in the Broad Caribbean region. When the species from Vecchione’s work

(2002) is merged in, a total of 131 species exist in the Broad Caribbean. Although the study presented a few discrepancies in the Gulf of Mexico species totals, the overall

picture is one of large species diversity throughout the region. A factor to consider is that

some of the checklist species are based on one or two specimens which were badly

damaged animals. The paucity of species samples demonstrates the need to investigate the Broad Caribbean thoroughly for additional samples to ascertain the validity, abundance, and range limits of species distribution. The 18 range extensions reported here are of value for understanding how cephalopods fit into the ecosystems of this area.

Many facets are needed to create the “complete” picture in terms of marine ecosystems and the role that the cephalopods play in them. Neither data nor literature alone will complete the picture for any diverse marine group.

The deep-dwelling squid, Asperoteuthis acanthoderma was an exciting new find for the Broad Caribbean and illustrates how little is known about the distribution of deep- water cephalopods. The species was only found off the coast of Japan prior to this discovery. Further research may reveal that A. acanthoderma’s distribution is circumglobal. To find and describe a new species of large squid after extensive studies have been conducted in the region (G. Voss 1956, Lipka 1975, Nesis 1975, Roper et al.

1984, N. Voss et al. 1988, Passarella, 1991, Vecchione 2002) reveals the likelihood of finding new cephalopods in the Broad Caribbean.

A recent paper (Norman & Hochberg, 2005) examined the status of octopods worldwide. There have been new discoveries in many regions of the world including

New Zealand, New Caledonia, South Africa, and Hawaii. There is an obvious absence of octopod findings in the Broad Caribbean region. G. Voss (1977) calculated the projected amount of octopod species that would be found on an annual basis, and suggested that an average of 6.7 species being described annually worldwide. He also stated that “it seems clear that we are still in the descriptive stage of systematics”. These statements seem to hold true over 25 years later (Norman & Hochberg, 2005). The study went on to describe

the progress and impediments to taxonomic studies today. Progress is visible in

advanced electronic communication, better technology, and better international links.

Areas that are in need of improvement: poor retention of materials, few replicates, poor

curation, little support for taxonomic research, very few understudies to continue

progress, and museum curators are not being replaced as they retire, collections being

maintained but not active or growing, and lastly fewer primary field studies are being

undertaken (Norman & Hochberg, 2005).

Proper identification and collection will also provide better understanding of the

potential for cephalopod fisheries. Over 50% of the global cephalopod catch recorded by

the Food and Agricultural Organization (FAO) is not segregated into single species

categories, and this significantly reduces any value the data may have for population

assessment (Boyle & Boletzky, 1996) Collaboration between scientists throughout the

Caribbean would further quantify and identify important and scarcely known species.

Improved collection methods and new species specific research cruises are sorely

needed to discover what else lies in the deeper waters of the Caribbean Sea and Gulf of

Mexico. There is a demand for the information as finfish harvests collapse, the fisheries will turn to cephalopods for commercial exploitation. An immediate priority for the ocotopods is production of detailed and accurate descriptions of all species as the octopod

taxonomy needs major revision and stabilization (Norman & Hochberg 2005)

Bottom depth and vertical migration can be important elements in the cephalopod

lifestyle as many (e.g. Selenoteuthis scintillans, Spirula spirula) ascend nightly for

feeding (Roper and Young, 1975). Deep-sea cephalopod collection has been traditionally

difficult (Wormuth & Roper, 1983). Also, connections in food webs are sometimes

difficult to determine as the cephalopods need to break down their prey into small parts

prior to digestion and stomach contents are therefore difficult to identify. Vertical

migration of cephalopods and the role they play in the transfer of energy between the

layers are not well known. Less than half of the specimens with known locales of the

5190 examined had depth of collection recorded. The depth information available was

not adequate to describe specific depth ranges for the cephalopods in the region.

Another challenge in this study was the lack of detail on capture locations for

many specimens. Many had only regional information associated with the sample and

over 200 specimens were not used due to a complete absence of information (e.g.

“collected in the Caribbean Sea”). A universal standard for recording sample information

throughout the Broad Caribbean could improve sample details and would glean

consistent accuracy for research studies. The sample information should include the

following: latitude/longitude, date, time, depth, water temperature, identification (if

possible) and collection method used for capture.

A technique that has been successful in solidifying relationships between cephalopod species is DNA analysis. An example of an organism to examine in the

Broad Caribbean for genetic relatedness could be Doryteuthis plei and determine the genetic linkages between the northern and southern populations. Also, DNA comparisons with cephalopod species from the eastern tropical Pacific could lead to insights concerning the origins of the fauna. Past geological occurrences provide an excellent backdrop to examine the origins for cephalopods in the region.

There have not been any previous comprehensive cephalopod studies of the Broad

Caribbean since the early work of Voss (1956) and there is little literature from other

similar-sized regions for comparison. There are many smaller scaled studies, and it may be because cephalopod taxonomy is in flux that large biogeography studies have been neglected. Cephalopods have been the focus of many studies in the Broad Caribbean region and the results from the present research paper build and highlight additional advances in the comprehensive overview of the group. Much work is still needed to attain a better understanding of this complex cephalopod assemblage.

REFERENCES

1. Boyle, P.R. & Boletzky, S.V. 1996. Cephalopod populations, definition, and dynamics. Philosophical Transactions of the Royal Society, London. Series B. Biological Sciences; B351:985-1002.

2. Lipka, Douglas. 1975. The systematics and zoogeography of cephalopods from the Gulf of Mexico. Dissertation, Texas A&M. August 1975; 1-347.

3. Nesis K.N. 1975. Cephalopods of the American Mediterranean Sea; English Translations of Selected Publications on Cephalopods; Editor M. Sweeney; Smithsonian Institutions Libraries; 1; 318- 358.

4. O’Dor, R.K., J.A. Hoar, D.M. Webber, F.G. Carey, S. Tanaka, H.R. Martins and F.M. Porteiro. 1994. Squid (Loligo forbesi) performance and metabolic rates in nature. Physiology of Cephalopod Molluscs- Lifestyle and Performance Adaptations. Gordon and Breach Publishers. 163-177.

5. Passarella, K.C., 1990. Oceanic Cephalopod Assemblage in the Eastern Gulf of Mexico, Department of Marine Science. University of South Florida: St. Petersburg, Fl. 50pp.

6. Roper, Clyde F. E. and Richard E. Young. 1975. Vertical distribution of pelagic cephalopods. Smithsonian Contribution to Zoology; 209; 1-51.

7. Roper C.F.E, M.J. Sweeney & C.E. Nauen, 1984. FAO species catalogue. v.3 Cephalopods of the world. An annotated and illustrated catalogue of species of interest to fisheries. FAO Fish. Synop. (125) v3: 277p.

8. Rosa, Rui, Heidi M. Dierssen, Liliana Gonzalez, and Brad Seibel. 2008. Ecological biogeography of cephalopod molluscs in the Atlantic Ocean: historical and contemporary causes of coastal diversity patterns; Global Ecology and Biogeography; 17: 600-610.

9. Semmens, Jayson M., Gretta T. Peel, Bronwyn M. Gillanders, Claire M. Walunda, Elizabeth K. Shea, Didier, Jouffre, Taro Ichii, Kartsen Zumhotz, Oleg N. Katugin, Stephen C. Leporati and Paul W. Shaw. 2007. Approaches to resolving cephalopod movement and migration patterns. Review of Fish and Biological Fisheries; 17: 401-423.

10. Stevens, G.C., 1989. The Latitudinal Gradient in Geographical Range: How So Many Species Coexist in the Tropics. The American Naturalist; 133(2): 240-256.

11. Vecchione, 2002. Cephalopods. Carpenter, K.E.(ed.) The living marine resources of the Western Central Atlantic. Volume 1: Introduction, molluscs, crustaceans, hagfishes, sharks, batoid fishes, and chimaeras. Cephalopods of Western Central Atlantic; FAO Species Identification Guide for Fisheries Purposes and American Society of Ichthyologists and Herpetologists Special Publication No. 5. Rome, FAO. 2002. 1-600.

12. Voss, G.L. 1956. A review of the cephalopods of the Gulf of Mexico. Bulletin of Marine Science: Gulf and Caribbean; 6:85-178.

13. Wormuth, John H. and Clyde F.E. Roper. 1983. Quantitative sampling of oceanic cephalopods by nets: problems and recommendations. Biological Oceanography; 2 (2-4) 357- 377.

100

APPENDICES

101

Appendix A: Regional Distribution Point Reference

Regional Distribution Points

Regional Number Region Lat (N) Long (W) 1 NE Florida 29.26 -80.76 2 SE Florida 26.41 -79.65 3 Florida Keys 24.81 -80.58 4 SW Florida 26.29 -82.31 5 Bahamas 24.5 -76.19 6 West Cuba 22.77 -82.06 7 SE Cuba 20.42 -76.06 8 Dominican Republic 19 -70.94 9 Jamaica 18.09 -78.19 10 Puerto Rico--> Antigua 18.35 -64.92 Guadeloupe-- 11 >Martinique 15.38 -61.24 12 St. Lucia--> Grenada 13.32 -61.24 Trinidad-->East 13 Venezuela 11.31 -61.83 14 Columbia 9.47 -76.22 15 Panama-->Costa Rica 9.28 -81.39 16 Mexico- Yucatan area 21.47 -86.46 17 Belize 17.25 -88.43 18 Texas/ North Mexico 26.35 -96.51 19 Louisiana 29.57 -88.02 20 NW Florida 27 -83.63

102

Appendix B: Species Richness Comparison Quadrats

Species Richness Comparison Quadrats Area Region Latitude Longitude 28.38- 86.44- Area 1 Mississippi River Delta 30.28N 90.8W

25.56- 82.12- Area 2 West Central Florida 28.38N 84.12W

79.9- Area 3 Straits of Florida 23.14-25.2N 82.17W

25.56- 78.48- Area 4 Eastern Central Florida 28.33N 80.32W

14.42- 61.12- Area 5 Mid Caribbean Islands 18.04N 64.35W

10.41- 61.12- Area 6 Southeast Caribbean Sea 12.26N 64.35W

11.12- 68.5- Area 7 South Central Caribbean Sea 13.01N 71.44W

75.19- Area 8 Southern Caribbean-Colombia region 8.30-11.28N 78.27W

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ABOUT THE AUTHOR

Heather Judkins received her Bachelor’s Degree in Marine Affairs from the University of

Rhode Island in 1993. She moved to Florida and received her Master’s Degree in

Secondary Science Education while teaching high school marine science classes. In

2003, she entered the Marine Science graduate program through the University of South

Florida pursuing a biological track focusing on cephalopods. While enrolled, she received two fellowships through the GK12 Oceans Program which was sponsored by the

National Science Foundation. She also coordinated the Regional National Ocean

Sciences Bowl, the Spoonbill Bowl, as a result of her fellowship project from 2004- present. She has continued teaching full time while tackling her degree. She has coauthored two publications regarding cephalopods of the Broad Caribbean to date.

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