1-(-?:1-( Fjh__ Date Copyright 1996 by Albert Carranza

PSAMMOLITTORAL MARINE TARDIGRADA FROM COLEMAN BEACH, CALIFORNIA by Albert Carranza

A thesis submitted to Sonoma State University in partial fulfillment of the requirements for the degree of MASTER OF ARTS in Biology

ii AUTHORIZATION FOR REPRODUCTION OF MASTER'S THESIS

I grant permission for the reproduction of the thesis in its entirety, without further authorization from me, on the condition that the person or agency requesting reproduction absorb the cost and provide proper acknowledgement of authorship.

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iii PSAMMOLITTORAL MARINE TARDIGRADA FROM COLEMAN BEACH, CALIFORNIA

Thesis by Albert Carranza

ABSTRACT

Purpose of the Study:

Most of what is known about marine tardigrades is based on research conducted in Europe and along the east coast of the United States. Prior to this study only two cursory surveys of marine sand-dwelling taxa had been conducted along the coast of California. In each case a new species was described, but the number of species recovered from any single beach did not exceed three, giving the impression that species diversity along the California coast is unusually low.

This study is a survey of the taxonomic composition, intertidal distribution, and temporal variation of marine interstitial tardigrades from Coleman Beach, Sonoma County, California.

Procedure:

Sand cores were collected on March 23, July 23, and November 3, 1994 at Coleman Beach, Sonoma County, California. These were treated as representative samples for spring, summer, and fall respectively. The cores were taken along an 1 8 meter transect within the upper intertidal area (mean lower low water to mean higher high water) in 3.5cm diameter by 10cm depth (1 OOcm3) sections to a maximum depth of 60cm.

Findings:

Eight species representing three arthrotardigrade families were encountered. Two of these are new records for the west coast of North America and two others are new to science. In the family, Batillipedidae Batillipes tridentatus were the most abundant in the spring and B. sonomacus n. sp. were most abundant in fall.

iv Halechinischus remanei was the single most common member of the family Halechiniscidae and the most abundant species in summer samples. H. californiensis n. Spa occurred along with its congener in very low abundance. The Halechiniscidae was also reprsented byTanarctus arborspinosus in summer and T. ramazzotti in fall. Stygarctus spinifer and S. bradypus comprised the family Stygarctidae. The halechiniscids and stygarctids typicaly occurred in the deepest (40-60cm) cores at mid to high tide level.

Conclusions:

The presence of seven different species of tardigrades in the summer samples alone establishes that species diversity along the California coast is as rich as that found elsewhere. The distribution patterns observed during this study conform to the findings in both Europe and the eastern United States. Seasonal variation patterns suggest an alternation in abundance between congeneric species at Coleman Beach and may be the out come of interspecific competition.

Chair:

MA Program: Biology Sonoma State University Date: ~j1., dft

v ACKNOWLEDGEMENTS

I would like to thank Dr. Leland W. Pollock of Drew University for providing literature, advice and species confirmations. I also thank Dr. Diane R. Nelson of East Tennessee State University for her advice and for providing some essential literature. I am most grateful to Dr. Colin O. Hermans for his support and guidance throughout this project. For their assistance in the preparation of this manuscript, wish to thank Dr. Colin O. Hermans, Dr. Chris K. Kjeldsen and Marilyn Cannon. I also wish to thank the following people for their support, assistance and inspiration; Dr. Jean Renaud-Mornant, Dr. Mathew James, Dr. Joe H. Brumbaugh, Dr. John Hopkirk, Sam Horton, Ron Dudash, Rosemary Saunders, Jeff Hughey, William F. Samaras, Ann Hill, Walter Brelje, Ben Race, Wilford E. Dickinson and Linda M. Dickinson. This work is dedicated to Megan and our daughter, Hannah.

vi LIST OF TABLES TABLE 1 . Salinity, temperature and beach slope readings at

Coleman Beach...... a ...... , ••••••••••••••••••••••••••••" ...... JI ••• 1 5 2. Cumulative frequency series assesment of sediment...... 16 3. Morphometry of BatilJipes tridentatus and B. sonomacus n.sp ...... "...... 24 4. Morphometry of Halechiniscidae from Coleman Beach ...... 35 5. Morphomometry of Stygarctus spinifer and S. bradypus from Coleman Beach ...... 41 6. Arthrotardigrada recovered during Spring 1 994 ...... 43 7. Arthrotardigrada recovered during Summer 1994 ...... 46 8. Arthrotardigrada recovered during Fall 1994...... 49

vii LIST OF FIGURES Figure 1 . Feeding structures of the tardigrada ...... 2 2. Schematic representation of the cephalic appendages of an arthrotardigrade ...... 4 3. Foot Morphology of the Heterotardigrada ...... 5 4. Diagramatic representation of eutardigrade claws ...... 6 5. Cumulative frequency curve for sediment assessment data ...... 1 6 6. Intertidal distribution and abundance, Spring 1994...... 43 7. Vertical distribution within substratum at 10m from MLLW , Spring 1994 ...... 44 8. Horizontal (intertidal) distribution of Tardigrada Summer 1994 ...... ,. ... 4 7 9. Distribution and abundance of Tardigrada in samples collected Summer 1994...... 47 10. Horizontal distribution of Tardigrada observed during

Fall 1994...... "...... t ...... 50 11 . Distribution and abundance of specimens in samples collected Fall 1994..... ".. ,...... ".....,...... 11." ••"...... 50 12. Distribution of Batillipes tridentatus and B. sonomacus Fall 1994...... "."."... ""' ...... "...... ,, ...... 51 13. Relative Temporal Abundance of all Tardigrade Taxa...... 52

viii LIST OF PLATES

List of abbreviations ...... 65

Plate 1 Batillipes sonomacus. n. sp...... 66 2 Batillipes tridentatus Pollock, 1989 ...... 67 3 Halechiniscus remanei remanei Schulz, 1955 ...... 68 4 Halechinscus californiensis n. sp...... 69 5 Tanarctus arborspinosus Lindgren, 1971 ...... 70 6 Tanarctus ramazzotti Renaud-Mornant, 1975 ...... 71 7 Stygarctus spinifer Hiruta, 1985...... 72 8 Stygarctus bradypus Schulz, 1951 ...... 73

ix TABLE OF CONTENTS List of Tables...... •...... ,...... ,...... wvii List of Figures...... viii

List of Plates ...... •...... ~ ...... ,...... 1x Chapter I INTRODUCTION ...... 1 General Description of the Phylum ...... 1 Systematics of the Phylum ...... 3 Ecology of the Phylum ...... 6 Phylogenetic Affinities ...... 8 Marine Tardigrada in Western North America ...... 9

I I MATERIALS AND METHODS...... ,...... iII •••• ~ 12 III RESULTS..... "...... "...... "' ...... ,,...... " ...... ,...... ,..... 15 Physica I Parameters ....."...... ,..."."...... "' ...... "...... ,'" 15 Systematic Account ..•...."" ...... ,...... ,...,...,', .. "' ...... ,...... ,",.....•.....,...... , 1 7 Batillipes sonomacus n. sp...... 19 Batillipes tridentatus Pollock, 1989...... 22 Halechiniscus remanei remane; Schulz, 1955...... 27 Ha/echinscus californiensis n. sp...... 28 Tanarctus arb orspin osus Lindgren, 1971 ...... 32 Tanarctus ramazzotti Renaud-Mornant, 1975 ...... 33 Stygarctus spinifer Hiruta, 1985 ...... 37 Stygarctus bradypus Schulz, 1951 ...... 38 Distribution and Temporal Abundance ...... 42 Spring Samples (March 23,1994}...... 42 Summer (July 23) 1994...... 44

Fall (November 3) 1994...... ".!Ii."...... " ...... , ...... ItlI ..~ ...... 48 Relative Temporal Abundance ...... 48

I V DISCUSS10N ...... ••4 ...... " ...... ·••••••• " ••••••••" ••••••••••••••• 53

Bibliography...... •...... "...... "'11 •• "...... 5.9

Plates...... ,1 ...... " .. 65 x 1

CHAPTER I INTRODUCTION

General Description of the Phylum The first observation of a tardigrade was by J. A. E. Goeze in 1773 who is credited with giving them their present common name

of "water bears. II In 1776 the Italian abbot, Lazzaro Spallazani, noted their slow movement and called his specimen if Tardigrado (slow walker) introducing their current taxonomic name (Ramazzotti and Maucci, 1982). Tardigrada are microscopic, bilaterally symmetrical metazoans. Adults range in length from 100-500Jim ( Kinchin, 1994), although there are accounts of specimens reaching 1.7mm in length ( Brusca and Brusca, 1990). Their bodies are somewhat vermiform, dorsally convex, ventrally flattened in shape. They consist of a head region, three indistinct trunk segments, and a posterior, caudal region. The head region in some tardigrades possesses up to five pairs of sensory appendages (sensillae) and a set of eye spots. The trunk segments each bear a pair of telescopically retractable legs that are directed ventrally and the caudal region bears a fourth pair directed posteriorly. In some tardigrades the legs terminate in claws, and in others they terminate in toes, which may bear either claws or adhesive discs. They feed primarily on the fluids of plant cells by piercing the cell wall with a pair of rigid stylets that extend along the side of a buccal tube. A muscular pharynx posterior to the buccal tube is used to suck the fluid from the plant cells into the buccal tube. -- 2

mo-----

--- st ss -->r---- pi

A B FIGURE 1. Feeding structures of the tardigrada. (A) Pharyngeal apparatus typical of the class Eutardigrada; (B) Apparatus found in the order Arthrotardigrada; rna, mouth; bt, buccal tube; st, stylet; SS, stylet support; pi, placoid; ph, pharynx.

Cuticular thickenings called placoids line the inside of the pharynx. These structures vary among different groups of tardigrades and are presumably used to grind ingested solid material (Figure 1). Tardigrades possess a thin, transparent, layered cuticle that forms thickened plates or ornamental extensions in some taxa. The cuticle is water permeable and lines the foregut and hindgut (Nelson, 1991 ). Growth in tardigrades occurs by molting. During ecdysis the cuticle is shed along with the claws and the entire feeding apparatus. The musculature is composed of both smooth and striated fibers. These are attached to the cuticle and control locomotion by acting against the antagonistic hydrostatic pressure of fluid in the body cavity (Kinchin, 1994). 3

The nervous system consists of a dorsal, lobed, cerebral ganglion (brain) connected to a ventral, sub-esophageal ganglion by a circum-oral ring. A metamerized, ventral, nerve ladder extends posteriorly consisting of two main trunks connecting ganglia associated with each pair of legs. Cephalic appendages (sensillae) are innervated by the brain and eyes spots, when present, lie within the brain (Renaud-Mornant and Pollock, 1971).

Systematics of the Phylum The Phylum Tardigrada is divided into three classes: Heterotardigrada, Mesotardigrada, and Eutardigrada. The class Heterotardigrada is characterized by the presence of paired cephalic appendages and cuticular plates that are lacking in the other two classes. The outermost cuticular layer in this group is composed of epicuticular pillars supporting a striated "honeycomb" layer (Kristensen, 1976). Placoids in this class are usually thin rod shaped structures (Figure 1). The Heterotardigrada are further divided into two orders: Arthrotardigrada and Echiniscoidea. With the exception of Styraconyx hal/as; Kristensen, 1977 found in freshwater Springs in Greenland (Renaud-Mornant, 1988), all known Arthrotardigrada are marine. Cephalic appendages are well developed in this group and taxonomically important. These sensory appendages consist of a median cirrus; a pair of internal cirri; one pair of external cirri; paired lateral cirri; one pair of variably shaped clava; and sometimes, a pair of secondary clava (cephalic papillae) may be present (Figure 2). 4

mc / /iC I ___ ec l l 1'1-) I ;-IC ~>:>==rr-y_~ d '\ = -+-(----mo

FIGURE 2. Schematic representation of the cephalic appendages of an arthrotardigrade. Abbreviations used: me, median cirrus; ic, internal cirrus; ec, external cirrus' Ie, lateral cirrus; el, clava; mo, mouth. '

In most arthrotardigrades the legs terminate in digits (toes) bearing either claws or adhesive discs (Figure 3). In one extraordinary case, however, Kristensen and Higgins (1989) report the occurrence of both claws and adhesive structures in the species Paradoxipus orzeliscoides Kristensen and Higgins, 1989. The Echiniscoidea are represented in marine, freshwater, and terrestrial habitats. The dorsal cuticle forms thickened plates, the morphology of which delineates the systematics of this group. Marine members of this order lack cuticular plates. Cephalic appendages are not as well developed as in the Arthrotardigrada, although a lateral cirrus is typically present. The legs terminate in four or more claws. Digits (toes) are absent. 5

A B c

FIGURE 3. Foot Morphology of the Heterotardigrada. A, toes and adhesive discs of the family Batillipedidae (order Arthrotardigrada); B, toes and claws of the family Halechiniscidae (order Arthrotardigrada); C, claws typical of the order Echiniscoidea.

The class Mesotardigrada is a monotypic taxon based entirely on a single species seen only once and reported 'from a hot Spring near Nagasaki, Japan (Ramazzotti and Maucci, 1982; Renaud-Mornant, 1988; Kinchin 1994). Members of the class Eutardigrada are mostly terrestrial, but some are marine (Hallas, 1971). They lack cuticular plates of any kind. As in the Echiniscoidea, eutardigrade legs terminate in claws. In this order, however, there are two branched claws per foot. The two branches of these claws vary in shape and size and are therefore taxonomically important ( Figure 4). Eutardigrade placoids are composed of pairs of elements arranged in rows ( Figure 1). The placoids are also taxonomically important features. 6

3 1---4

FIGURE 4. Diagrammatic representation of eutardigrade claws. (1) Primary branch; (2) secondary branch; (3) internal claw; (4) external claw.

Cephalic sensory structures are absent in most eutardigrades. When present they consist of reduced papillae that are not considered to be homologous with those of heterotardigrades (Nelson, 1991). The reduction of sensillae and the ability to achieve latent states (discussed below) are considered to be derived characteristics of the Eutardigrada and are cited as evidence that this is the most phylogenetically recent group (Renaud-Mornant, 1982; Kinchin, 1994).

Ecology of the Phylum Tardigrada inhabit marine, fresh water, and terrestrial environments. Terrestrial forms occur in habitats such as mosses, lichens and in leaf litter and require the cover of a film of water in 7 order to remain active. Should substrate dehydration occur, these organisms have the capability of achieving a state of anhydrobiosis. In this latent condition metabolism is suspended and a state of dehydration is achieved in which all of the body's water is lost. This includes both free water in body fluid and molecular bound water (Kinchin, 1994). In order to retain structural support the bound molecular water is replaced by the compound trehalose (Crowe et aI., 1992). The first marine tardigrade was described in 1851 by Dujardin (Hay, 1 91 7). Marine representatives are now known from intertidal to abyssal habitats beyond 4000m in depth (Renaud-Mornant, 1975a). Renaud-Mornant (1982) recognizes three major ecological groups: a) a small group of species restricted to the slime on algae or other substrates, including facultative and obligatory invertebrate ectoparasites; b) a much larger contingent of psammophilic (interstitial) species; c) a group of relatively highly diversified abyssal mud and deep sea ooze dwellers. Interstitial species are those which inhabit the interstices of marine sediments. They are part of a larger ecological group collectively known as "psammon tl or "interstitial meiofauna." Psammophilic forms do not undergo anhydrobiosis because they are not subjected to the extreme perturbations of the terrestrial environment. Non-armored marine Echiniscoidea which inhabit the algal mats and barnacle plates within the higher littoral zone, however, are known to survive periods of aerial exposure in an 8 immobile state (Kinchin, 1994). The generally accepted theory concerning the evolution of tardigrades is that they originally evolved in the marine environment and gradually made a transition to land (Renaud-Morna nt, 1982; Kinchin, 1994).

Phylogenetic Affinities The phylogenetic position of the Tardigrada within the animal kingdom remains one of the most intriguing aspects of the phylum. They share many characteristics with several lines of invertebrate evolution. Their overall appearance is reminiscent of the phylum Arthropoda. In fact, early researchers had classified tardigrades as a group within the Acari (phylum Arthropoda) because of the presence of four pairs of legs (Ramazzotti and Maucci, 1982). Tardigrades were considered as a group within the Arthropoda until the erection of the Phylum Tardigrada by Ramazzotti (1962). In addition to morphological appearance, tardigrades share other features with the Arthropoda, among these are a chitinous component of the endocuticle (Nelson, 1991), as well as the nature of cephalic sensory appendages, golgi beads, muscle attachments and muscle cells (Kinchin, 1994). The presence of vasa Malpighii in Eutardigrada (Greven, 1979) is another characteristic shared with the Arthropoda, It is likely, however, that this feature may have evolved independently in this mostly terrestrial group as an adaptation to living on land. Tardigrades also share a number of features with the aschelrninth line of evolution including the nature of the cuticle, 9

absence of circular muscles, pharynx, buccal stylets, digestive system and the presence of a pseudocoelous body cavity in the adults (Renaud-Mornant & Pollock, 1971). They share these features with nematodes along with the ability to withstand dehydration. The latter of these features is again unique to terrestrial members and is likely a case of convergent evolution as noted by Kinchin (1994 citing Pilato, 1979). A third group to which tardigrades have been phylogenetically linked are the Annelida. The features shared in this case include the ladder-shaped nervous system, the cephalic sensillae (Renaud Mornant and Pollock, 1971), and the nature of the claws (Kinchin, 1994). Recent molecular analyses by Garey et al. (1996) using 185 rRNA have provided evidence linking Priapulida, Tardigrada and Arthropoda. They suggest that these results may explain why both aschelminth-like and arthropod-like characters are observed in Tardigrada.

Marine Tardigrada in Western North America The vast majority of tardigrade studies have been conducted in Europe. In the United States studies on marine representatives have been largely limited to the Atlantic Coast. The earliest report of a marine tardigrade in the United States is the description of Batillipes caudatus from North Carolina (Hay, 1917). McGinty & Higgins (1968) studied ontogenic variation of taxonomic characters in two species of Batillipes. Pollock (1970a) contributed a substantial study on the distribution and dynamics of the 10 interstitial Tardigrada at Crane's Beach near Woods Hole, Massachusetts. Lindgren (1971) studied psammolittoral tardigrades at Bogue Bank, North Carolina. Studies along the West Coast, however, remain scarce. Three surveys conducted in western North America focused on terrestrial tardigrades. Mathews' (1938) study contains the first accounts of West Coast species from algae. Shuster & Grigarick's (1965) general survey of western North American tardigrades included only one marine species, Echiniscoides sigismundi Shultze, 1865, from algae and barnacles. Finally, Kathman (1990) studied the terrestrial tardigrada of Vancouver Island, British Columbia. Only two publications on marine interstitial tardigrades from the Pacific coast of the United States existed prior to my study. McGinty (1969) sampled beaches near Hopkins Marine Station at Monterey Bay. She described the species 8atil/ipes gilmartini and also reported finding Halechiniscus remanei Schulz, 1955. Pollock (1989) surveyed interstitial Tardigrada at various beaches from Washington to southern California. His publication included the description of 8atil/ipes tridentatus as well as a range extension for two members of the genus Stygarctus. In both cases the total number of species encountered at any given beach did not exceed three. Indeed, the composition in all but one beach consisted of only two species. Three species were recovered by Pollock at Big Sur, California in 1989. Clearly the existence of two cursory studies is not sufficient to understand the population dynamics of psammophilic West Coast fauna. Although species composition along the West Coast appears 1 1 to be limited based on the previous studies, surveys conducted over a longer period of time could demonstrate this species shortage to be a seasonal phenomenon. Furthermore, low species diversity could also be characteristic of the beaches previously sampled, perhaps attributable to edaphic factors. In any case, a more thorough study was needed in order to expand the current baseline data. To this end, a survey of the species composition, temporal variation and intertidal distribution of psammolittoral tardigrada was conducted at Coleman Beach, Sonoma County, California. 12

CHAPTER II. MATERIALS AND METHODS

Coleman Beach (230 19.41 N, 1230 S.8 1 W) is an exposed rocky beach approximately 101 kilometers (63 miles) north of San Francisco, California. Sampling was conducted within a small sandy cove at the northern extreme of the beach where large boulders did not dominate the substrate,

Core samples were collected along a 1 8~meter transect within the intertidal zone from mean lower low water (MLLW) to mean higher high water (MHHW) in Spring (March 23), Summer (July 23), and Fall (November 3) 1994. Samples were taken at two meter intervals along the transect. Additional samples were taken at other intervals and other times of the year. The cores were collected as 1Oem vertical sections to ground water depth using a plastic corer (PVC pipe) with a diameter of 3.5cm which provided an opening with an area of 1Ocm2 and thus a total volume of 1OOcm3• Coleman Beach is accessible only by a steep trail that winds along the face of a cliff. Due to weight constraints, collection was limited to one set of samples per transect. Also, the depth to which samples could be collected was limited to sand above the ground water level as the most saturated sand could not be retained within the core sampler. Each 100cm 3 sample was placed in a plastic bag, and either preserved with 5% buffered formalin, stained with rose bengal, and 13 further processed in the lab or taken to the lab in fresh condition for live observations. The cores were processed as follows: 1) Specimens were extracted by placing the cores in a 1000ml graduated cylinder, filling it with de-ionized water (tap water was used with preserved samples) and agitating for 30-40 seconds. This process osmotically shocked the tardigrades causing them to release the sand grains and become suspended in the water (Renaud-Mornant, 1988). 2) The water containing suspended specimens was then decanted from the graduated cylinder through a 63J.1m sieve which retained the specimens. These were rinsed with seawater (5% Borax-buffered formalin for preserved samples) into glass culture dishes for observation. The extraction procedure was repeated five or six times for each sample. Initial observations were made at SOx using a dissecting microscope. Tardigrades were transferred to microscope slides and examined with a light microscope at 250x and 900x magnification. Permanent mounts were prepared from preserved specimens by transferring them onto slides in a drop of formalin. Oversleeps with modeling clay supports at each corner were then placed over the formalin drop. The mounts were infused with a solution of 1 0% glycerin in 95% ethanol, allowed to evaporate to glycerin for a few days and finally sealed with Permount. Beach slope was measured using a Brunton's Pocket Transit. Temperature and salinity of seawater and ground water were measured with a YSI-33 salinometer. Ground water samples were 14

taken by digging a hole deep enough to allow about 1OOml of ground water to seep into a small plastic container. Granulometric analyses of sediment (compiled from 15 different samples taken at various heights and depths from within the transect) were performed using the methods described by Giere et al. (1988). The procedure is as follows:

1) 1~Og samples were dried in an oven at 80c(; for 24 hours. 2) After drying, sand fractions were separated by passing them through a geometric series of test sieves with 1.0 phi intervals. Phi= -1092 of mesh size in mm. Thus mesh sizes consisted of 2000pm, 1000pm, 500pm, 250pm, 125pm, and 63pm with corresponding phi values of -1, 0, 1, 2, 3, and 4, respectively. 3) Sediment weight fractions were calculated as a percent of the total sample, transformed into a cumulative frequency series (Table 2), then plotted as a cumulative frequency curve (Figure 5), 4) Median grain diameter (Md) was obtained from the phi value corresponding to the 50% point of the resulting curve (Figure 5), while particle size distribution is represented by the 25% (Q,) and 75%(03) quartiles. A measure of how well the sediment is sorted (uniformity coefficient) was determined by calculating the quartile deviation (QD) using the following equation:

QD=03...:J21 2 15

CHAPTER III RESULTS

TABLE 1. Salinity, temperature and beach slope at Coleman Beach. (S.W.) sea water; (G.W.) ground water. Spring Summer Fall (March 23 1994) (July 23 1994) (Nov. 11 1994)

S.W G.W. S.W. G.W S \AI I G.W. Salinity (0/00) 31 31 30 30 30 30

Temperature (~) 1 1 1 1 13 13 12 12 Slope (% grade) 13.6 14.0 12.0

Physical Parameters There was no significant seasonal variation in temperature or salinity, and ground water and seawater readings remained the same. Beach slope readings varied slightly throughout the year (Table 1). Granulometric analysis showed a median grain diameter (Md) of

1000pm (phi value = 0.0) categorized as very coarse sand according to Wentworth Scale classification (Fetter, 1988). The sand at Coleman Beach is very well sorted with a uniformity coefficient (QD) of 0.175. It consists of silt, fine and medium sand as well as pebbles and cobbles (Table 2, Figure 5). 16

TABLE2CumuaIt'Ive freQuency series assessment of sediment.

sieve size (pm) phi value dry wt. (%) cum.

<63 >4 <0.01 0

63 4 <0.01 0

125 3 0.337 0.337

250 2 0.160 0.497

500 1 17.8 22.7

1000 0 27.0 49.8

2000 - 1 50.2 100

"'"""'#. 100 '-" ..,; 80 ~ 60 ~ "0 40 E 20 :::I (.) 0 -2 - 1 0 1 2 3 4 phi value

FIGURE 5. Cumulative frequency curve of data in Table 2. 17

Systematic Account A total of ten species of tardigrades were encountered. Two of them, however, are problematical. A single specimen in the genus Hypsibius (class Eutardigrada) was recovered from a sample collected in January 1995. Because only one specimen was found and its identification to species is uncertain, it is merely mentioned in this report. Another problematical species is Echiniscoides sigismundi Shultze, 1865 in the order Echiniscoidea which is not considered to be an interstitial tardigrade (Shuster & Grigarick, 1965; Pollock, 1970a; 1975; Hallas & Kristensen 1982). Two specimens were found in the Summer 1994 samples at 8m along the transect from MLLW in cores from 0-10cm and 30-40cm depths. The eight remaining species are all interstitial Arthrotardigrada. Two of these are new records for the west coast of North America and two others are new to science.

Family Batillipedidae Ramazzotti, 1962

Diagnosis: Arthrotardigrada with six toes terminating in variably shaped adhesive discs, no claws present.

TYQe genus: Batillipes Richters, 1909 18

Discussion: Formerly known as the Discopodidae, the name of this family was changed to Batillipedidae by Ramazzotti (1962). It was once comprised of the two genera BatilJipes and Orzeliscus Bois Reymond Marcus, 1952 until the latter was reclassified as belonging to the family Halechiniscidae by Pollock (1982).

Genus Batillipes Richters, 1909

Diagnosis: Batillipedidae with six toes in the adult stage, four in the juveniles and a variable pattern of five and six toed appendages in immatures; cephalic appendages simple and well developed. Bell shaped secondary clava (cephalic papillae) are present in some species as well as eye spots (Kristensen, 1978).

Discussion: Despite the numerous species currently known, the Batillipedidae remains a monotypic family. Evidently there are no differences between species worthy of the establishment of a new genus. In fact, the characteristics which delineate individual species can often be so subtle as to cause confusion. McKirdy (1975) has reviewed some of these characteristics and cautions that some may not be of taxonomic importance, but merely represent geographical variations among populations of the same species. 19

Batillipes sonomacus n. sp. (Plate 1, Table 3)

Diagnosis: Batillipes relatively small in size with a very short rounded caudal extension; with long lateral cirri; legs IV spines long, extending to as much as half the total body length; with a prominent tapering lateral body projection between legs III and IV, a small rounded ventro-posterior projection constitutes the caudal extension; with toes terminating in circular adhesive structures; secondary clavae (cephalic papillae) present, located ventro anteriorly between internal and external cirri.

Etymology: The specific epithet is based on the type locality of this species in the County of Sonoma, California.

Type specimens:

Deposited in the National Museum of Natural History ~ Division of Crustacea, Washington D.C. Collected by Albert Carranza 23 July 1994.

Type locality: Coleman Beach, Sonoma County, California (230 19.4' N, 1230S.8'W). In well sorted sand at mid tidal height, 30-40cm in depth. 20

Description: Batillipes with ventro-Iateral body projections between the head and leg I (first leg pair) and between each leg pair thereafter. A similar ventra-caudal projection comprises the short caudal extension. Projection between legs III and IV wide at base tapering to blunt point directed posteriorly. Body length relatively small, 120J.lm in average length from anterior head margin to base of caudal extension; cuticle punctate. Body width increasing gradually in posterior direction, Head width between bases of lateral cirri extending beyond anterior lateral body margins. Median cirrus long, placed close to the anterior head margin. Internal cirri equal in length to median cirrus. Small cephalic papillae placed antero-ventrally between internal and external cirri. External cirri shorter than lateral cirri in length and set laterally, close to clavae and lateral cirri. Clavae rod~shaped, distally rounded with a very slight flare. Lateral cirri long, equal to about one quarter of body length, set dorsad and posterior to clavae. Buccal tube straight 13J.1m in average length. Stylets 11pm in average length and symmetrical. Stylet supports with slight posterior arch at distal end, 6pm in length. Support knobs oval and thicker than shaft. Pharyngeal bulb circular with a slight posterior cleft, 12J.1m in average diameter. Finer features of the buccal apparatus such as the stylet furcae and the placoids were not readily visible. Adhesive discs circular. Legs I-III with spines directed dorsa posteriorly. Leg IV with large spine equal to as much as half the body length. 21

Discussion: Batillipes sonomacus resembles B. roscoffensis Kristensen, 1978. Characteristics common to both species include relatively long lateral cirri, the presence of cephalic papillae and the nature of the lateral body projection between legs III and LV. There are some very important differences, however, which serve to distinguish the two. The most noticeable feature of B. sonomacus is the length of the leg IV spine (Table 3). The average length obtained for leg IV spine was 54~m, the longest ever reported for this genus. The impressiveness of this feature is compounded by the relatively small size of the species. The average body length obtained was

120~m. Fully mature adults never exceeded 136~m in body length. B. roscoffensis specimens studied by Kristensen (1978) measured

230-250~m in length while leg IV spine measured 18~m. When considered alone these differences could be interpreted as intraspecific variations. Leg IV spine length is considered an unreliable taxonomic characteristic (Pollock, 1971; McKirdy, 1975). Toe disc shape, however, is considered a more reliable feature (McKirdy 1975). The adhesive discs of B. sonomacus are round. Kristensen (1978), on the other hand, described elliptical shaped structures for B. roscoffensis "with a characteristically cut end." Innervation to the cephalic papillae from the brain occurs via connections which branch from the external cirrus connection and then curve slightly anteriad and toward the center of the head. 22

Batillipes sonomacus also shares characteristics with B. marcelli (Morone de Lucia et al. 1988). Among these are the nature of the lateral processes between legs III and IV, presence of secondary papillae and small body size. More importantly, however, the caudal appendage of B. marcelli consists of a spine which extends from a base very similar to the caudal extension found in B. sonomacus. Four toed juvenile specimens found were very similar in appearance to adult individuals. The lengths of leg IV spines in juveniles was proportionately smaller than that of the adults. In relation to total body length for example, juvenile leg IV spines were approximately one third the body length as opposed to one half in adults. Sculpturing of the cuticle in B. sonomacus was completely lacking except for the evenly dispersed punctae, which were visible only in living animals. Likewise, reproductive structures were not visible in preserved specimens. In living females, however, rosette gonopore openings typical of Batillipeds (Pollock, 1 970b) were observed.

Batillipes tridentatu5 Pollock, 1989 (Plate 2, Table 3)

Diagnosis: Batil/ipes with a two-pointed caudal apparatus, two pairs of lateral projections between legs TIl and IV; with a prominent spike on the shank of leg IV.

Distribution: Clallam Bay, Washington and Big Sur, California (Pollock, 1989); Coleman Beach, California in upper , /2 tidal height with a maximum

of 7S individuals (1 OOcm3)-', 0-1 Oem in depth, Spring 1994.

Description: Morphometric data agree well with those obtained by Pollock (1989). No deviations from the original species description were observed at Coleman Beach.

Discussion: The occurrence of B. tridentatus at Coleman Beach serves to support its existing range since Coleman Beach lies between the two localitieS from which it was recovered by Pollock. Its absence from Bodega Head (Pollock, 1989) only 2 miles south of Coleman Beach may be attributable to the patchy distribution typical of psammolittoral tardigrada (Pollock, personal communication). It is also likely, however, that B. tridentatus are present at Bodega Head and simply eluded Pollock1s sampling. 24

TABLE 3 Morolh ometrv 0 f Bat}'/I' 'foes tn'd entatus andB.sonomacus n.

B. tridentatus B. sonomacus

Bodvlenath 151+16.7 (9) 12Q±.13.6 (13)

Median cirrus 37.S±- 2.8 (9) 23.Q±.3.S (12)

Internal cirri 25.9±..3.4 (9) 22.D±2.3 (12)

External cirri 20.9+2.3 (9) 12.9±'1.4 (17)

Lateral cirri 37.5+ 5.5 (11 ) 32.6±'3.9 (15)

Clava 14.1±2.2 (11 ) 14.6±'1.6 (11)

Lateral soike a 17.4±2.1 (5) none present

Lateral spike b 20.9±2.2 (5) 14.1±1.6 (3)

Leo IV soike 13.o±2.7 (5) none present

Leorv spine 46.8±.S.6 (5) 58.D±6.0 (14)

Caudal Soike 22.S± 0 (5) none oresent a Lengths±' standard deviation (n); all lengths in 11m 25

Family Halechiniscidae Thulin, 1928

Diagnosis: Arthrotardigrada with four toes terminating in claws of variable structure; dorsal plates absent; with a set of nine cephalic appendages.

Type genus: HaJechin;scus Richters, 1908

Discussion: This widely distributed family is perhaps the most diverse and morphologically variable in the entire phylum. Seven subfamilies were recognized before Pollock (1995) erected the Dipodarctinae bringing the total to eight.

Subfamily Halechiniscinae Thulin, 1928

Diagnosis: Halechiniscidae with rectilinear tibia and enlarged tarsus on which toes are inserted; claws are simple or posses an accessory spine; primary clava well developed; secondary clava rare.

Discyssion: This subfamily includes the genera HaJechiniscus Thulin, 1928, Chrysoarctus Renaud-Mornant, 1984 and Paradoxipus Kristensen and Higgins, 1989. Genus Ha/echiniscus Richters, '908

Diagnosis: Halechiniscidae with simple claws or with accessory spine; clava well developed; lacking external calcar embedded within the toe.

Discussion: Pollock (1976) contributed a definitive list of the marine tardigrada of the world at the time. He lists five species of

Halechiniscus: H. guiteli Richters, , 908; H. intermedius Renaud~ Mornant, 1967; H. remanei Schulz, 1955; and H. subterraneus Renaud Mornant, 1956. Since then the descriptions of H. greveni Renaud Mornant & Deroux, 1976 and H. flabellatus Grimaldi de Zio, Morone de Lucia, D'Addabbo Gallo & Grimaldi, 1982 have increased the number of species described thus far.

Halechiniscus remane; Schulz, 1955

Diagnosis: Halechiniscus with a prominent caudal spike; with lateral body projections between each leg pair as well as between lateral cirri and leg I; clava shorter than lateral cirri.

Discussion: The subspecies H. remanei antillensis Renaud-Mornant, (1984b) has been described from Guadeloupe, Martinique and from Florida, 27

U.S.A. It is distinguished by the presence of a small anterior secondary process extending from the base of the lateral body projection between legs II and IV •

Halechiniscus remanei remanei Schulz, 1955 (Plate 3, Table 4)

Diagnosis: H. remanei with simple lateral body projections between legs ill and IV.

Distribution: Naples, Italy (Schulz, 1955); near Hopkins Marine Station in Monterey, California (McGinty, 1969); subtidally off the coast of

Brest, France at 130m in depth (Renaud~Mornant, 1971); from the Ionian and Mediterranean coasts of southern Italy (D'Addabbo Gallo et aI., 1978; Grimaldi de lio et aI., 1979); east coast of Australia (Renaud-Morna nt, 1981 a); Bodega Head, Big Sur, Little Corona Beach and La Jolla, California (Pollock, 1989); Coleman Beach California in the upper intertidal zone almost exclusively below 20cm in depth.

Description:

The average body length of H. remanei was 86~m. Although these measurements are within the range of 86-120pm reported in the original description (Schulz, 1955), they are relatively low. These are consistent, however, with measurements reported by Pollock (1989) for specimens collected at Newport Beach, California. 28

Discussion: A distal constriction of the lateral process on leg IV was not observed among the population in this study. It has been observed by McGinty (1969) from California specimens and by Renaud-Mornant (1984b) in specimens of H. remanei antillensis. Pollock (1989) reported that this feature was not routinely obvious in specimens he collected along the west coast of the United States.

HaJechiniscus californiensis n. sp. (Plate 4 Table 4) Diagnosis: Halechiniscus with a broad caudal expansion composed of four tapering processes; with dorsal cuticular expansions extending anterior to base of leg Ill, a small knob of similar origin extending anterior to lateral process base; with an obovate lateral process between legs ill and IV; with a prominent lateral spike extending from the base of leg IV. Distinct articulations lie at bases of all leg pairs. Similar articulation located at base of lateral process between legs TIl and IV.

Type Specimens: Deposited in the National Museum of Natural History, Division of Crustacea, Washington D.C. Collected by Albert Carranza 23 July 1994. 29

Type Locality: Coleman Beach, Sonoma County, California (230 19.4' N, 1230 S.8 'W), at 10 meters above MLLW in sediments 40-S0cm in depth.

Description: Body length from anterior head margin to base of caudal process 101 J.lm in average length. Median cirrus set close to anterior head margin. Internal cirri almost twice the length of median cirrus. external cirri set close to internal cirri and equal in length to median cirrus. Clava rod-shaped equal to or greater in length than internal cirri and about 1.6J.1m wide. Lateral cirri dorsal to clava, twice the length of median cirrus. All cephalic cirri consist of a scapus and terminal flagellum. Small lateral processes extending just below head expansion. All legs have what appear to be articulating sheaths at their bases. Dorsal cuticular extensions lie anterior to leg ill base. An obovate lateral process extends between legs ill and IV. It is distally concave and bears a proximal base with articulation sheath similar to that at leg bases. A small rounded dorsal cuticular expansion lies anterior to the lateral process base. Leg IV spike without distal constriction. Caudal appendage composed of two pairs of symmetrical, narrow, pointed processes. The anterior processes extend laterally from a short base. The posterior processes are narrower and are directed somewhat postero-Iaterally extending from the central axis of the caudal apparatus. 30

Discussion: There are some significant morphological similarities between H. californiensis and H. f/abeJ/atus Grimaldi de Zio et al. (' 982). Both species have an extension of the dorsal cuticle anterior to the leg I I base. Both species also posses a caudal appendage composed of four expansions. The differences in the nature of the lateral projections and the caudal apparatus, however, are significant enough to justify the designation of the California population as a new species. The lateral process in H. flabellatus tapers distally resembling that of H. remanei. The lateral process in H. californiensis, on the other hand has a concave terminus that is unique. The four lobes which make up the caudal apparatus in H. fJabellatus are also not as demarcated as in California specimens. One of the specimens encountered possessed fine bristles which covered most of the anterior portion of the head. Because a total of only three specimens were found it is unknown whether this is a common feature in this species.

Subfamily Tanarctinae Renaud-Mornant, 1980

Diagnosis: Halechiniscidae with toes inserted on the broad end of a conical tarsus, attached to the tibia by a spindle-shaped strip of cuticle; claws simple with an external calcar; accessory spine, when present, found only on median claws; leg IV spines modified into long caudal projections, simple or branched; epicuticle supported by a

prominent layer of pillars which are wider at the bases and narrow in the center giving them a crescent-shaped appearance, visible around the periphery of the body.

Type genus: Tanarctus Renaud-Debyser, 1959

Discyssion: The Tanarctinae was erected by Renaud-Mornant (1980) to include the genera Actinarctu5 Schulz, 1935 (Renaud-Mornant, 1971) and Tanarctus Renaud-Mornant, 1959.

Genus Tanarctus Renaud-Debyser, 1959 (emend. Lindgren, 1971; Renaud-Mornant, 1975)

Diagnosis: Tanarctinae with median cirrus; internal cirri longer than external cirri; lateral cirri greatly reduced; clavae extremely long, smooth or with small spiny projections and/or secondary and tertiary branches; leg IV spine long exceeding body length, simple or with secondary and tertiary branches. DiScussion: In the description of the type species, Tanarctus tauricus, Renaud-Debyser (1959) did not observe a median cirrus. Consequently, the absence of this sense organ was included as one of the characteristics of the genus. Lindgren (1971) emended the genus description to include the presence of a median cirrus when he 32

described T. arborspinosus from Bogue Bank, North Carolina. The description of T. ramazzotti Renaud-Mornant, (1975b) confirmed the presence of a median cirrus as a characteristic of this taxon.

Tanarctus arborspinosus Lindgren, 1971 (Plate 5, Table 4)

Diagnosis: Tanarctus with extremely long clava bearing short fine spines throughout its length; clavae length exceeding that of body; length of postero-Iateral spines also exceeding that of body, bearing secondary and smaller tertiary branches.

Distribution: Bogue Bank near Morehead City, North Carolina (Lindgren, 1971); Coleman Beach, California in samples collected Summer 1994, 10m along the transect from MLLW, 30-40cm and 40-50cm in depth.

Description: The specimens encountered at Coleman Beach are morphologically identical to those described by Lindgren (1971). Morphometric results are very similar but the Coleman Beach specimens are slightly smaller. 33

Discussion: Many specimens observed were in the process of molting. It is therefore possible that the smaller size of specimens at Coleman Beach is attributable to life stage rather than a population characteristic. The long clavae and postero-Iateral appendage (leg IV spine) in most specimens were either badly damaged or missing all together making morphometric analysis difficult. The damage was likely caused by the mechanical action involved in the extraction procedure. The occurrence of T. arborspinosus extends its range of distribution to the Pacific coast of North America, and is also the first report of this species since its discovery in 1971.

Tanarctus ramazzotti Renaud-Mornant, 1975b (Plate 6, Table 4) Diagnosis: Tanarctus with important ventral cephalic papillae; long postero-Iateral spines simple without secondary branches or projections.

Distribution: Collected subtidally from the Bay of Biscay, France at a depth of 3039m and off the coast of Brittany, France at a depth of 20m (Renaud-Mornant, 1975b); Coleman Beach, California in cores collected Fall 1994 at 2m, 4m, 8m, and 12m along the transect above MLLW, usually below 20cm in depth. 34

Qescription: Compared with the morphometry of the original description the California specimens are slightly smaller otherwise they are identical, except for the length of the clavae which are longer in the Californian specimens.

DiscussiQn: As in the case of T. arborspinosus, the occurrence of T. ramazzotti at Coleman Beach extends its known range to the Pacific Ocean and marks the first report of this species since it was described. Furthermore, this is the first account of T. ramazzotti from an intertidal environment. A total of only eight specimens were recovered, two of which were juveniles. Also as with the T. arborspinosus, smaller lengths may be due to life stage rather than population differences. 35

Table 4. Morphometry of Halechiniscidae from Coleman Beach

H. remanei H. californiensis T. arborspinosus T. ramazzotti

Body Length 86.3+8.0 (9) 101+1.4 (2) 75.8+8.9 (1l) 69.8+5.7 (5)

Median cirrus 10.6+0.9 (9) 10.4+0.6 (2) 7.8+1.4 (6) 11.9+1.6 (5)

Internal cirrus 15.3+1.9 (9) 18.5+0.7 (2) 25.5+2.3 (11) 22.5+3.2 (4)

i ..... t'" 10.4+0.8 (9) 9.9+1.2 (2) 18.6+3.3 (11) 1 5.3+3.2 (4)

I". 12.4+2.1 (9) 16.5+1.7 (2) 160+20 (7) 64.0+18 (4)

Secondary clava none present none present none present 11.4+2.2 (4)

Lateral Cirrus 18.9+2.3 (8) 22.5+0.0 (2) 10.6+1.0 (10) 10.5+2.7 (3)

Lateral spike 13.2+2.4 (7) 18.0+0.0 (1) present none present

Trunk spine 22.5+2.5 (9) 19.8+0.0 (2) .9 (7) 32+0.0 (1)

LegIv spike 9.9+1.3 (2) nodata none present none present

Leg IV spine nodata nodata 189+42 (4) 120+18 (5) Caudal -'. a~l~ 15.4+3.4 (7) 13.0+0.0 (2) none present none present Lengths±' standard deviation (n); all lengths in pm 36

Family Stygarctidae Schulz. 1951

(emend. McKirdy, Schmidt & McGinty~Bayly, 1976)

Diagnosis: Arthrotardigrada with median cirrus and five pairs of cephalic appendages; anterior clavae elongate or modified into spherical structures. Cuticle thickened into unpaired dorsal plates. Toes absent; in adults, four claws per foot with medial pair bearing a long filament or accessory spine, three claws per foot each with an accessory spine, or four claws on legs I-llI and two large claws on leg IV each with an accessory spine. Claws often attached to the foot by a basal membrane.

Discussion. This diverse family includes the genus Parastygarctus which is believed to be most ancestral group in existence among the Tardigrada (Renaud-Mornant, 1982). It was found to dominate the interstitial habitat in the Galapagos Islands where three new and unique genera were discovered by McKirdy et al. (1976). 37

Genus Stygarctus Schulz, 1951 (emend. Pollock, 1989)

Diagnosis: Stygarctidae with dorsal cuticle thickened to form three unpaired plates between a one piece cephalic plate and a caudal plate; legs with four claws, center pair with long accessory filaments; anterior clavae elongate.

Discu~sion: This genus description was emended by Pollock (1989) in order to accommodate the absence of caudal spikes in Stygarctus spinifer Hiruta, 1985.

Stygarctus spinifer Hiruta, 1985 (Plate 7, Table 5)

Diagnosis: Stygarctus with anterior clavae equal in length to posterior clavae; without caudal spikes; with small spines along lateral portion of dorsal plates; with paired non-bifurcated dorsal spines extending posteriorly from body plate n.

DistrjbytiQo: Kushiro, on the Pacific Coast of Hokkaido, Japan (Hiruta, 1985); Shilshole Bay, Washington; Bodega Head, California; Big Sur, California; (Pollock, 1 989); Coleman Beach, California in Spring and Summer samples in low numbers with maximal densities occurring 38 during Fall 1994 1 6m along the transect from MLLW at 50-60cm depth.

Description: Pollock (1989) observed in his study that S. spinifer specimens from western North America were slightly smaller than those studied by Hiruta (1985) from Japan. The same holds true for specimens studied at Coleman Beach; otherwise the morphological features agree well with those in the original description.

Discussion: S. spinifer is easily distinguished from its congeners, not only by its lack of caudal spikes, but also by the nature of its dorsal plates. In all other members of the genus, with the exception of S. granulatus Pollock (1970c) the dorsal plates are flared along the margins. In S. spinifer the margins extend postero-Iaterally forming a spike. The row of spinules along the lateral margin of each plate is also unique to this species.

Stygarctus bradypus Schulz, 1951 (Plate 8, Table 5)

Diagnosis: Stygarctus with large, recurved anterior clava, longer than posterior clava; with a pair of distally bifurcate processes passing postero-Iaterally from midposterior margin of body plate n; dorsal • 39

plates I-III with flared lateral margins; caudal plate with two long posterior spines. Legs I-Ill without spines.

Distribution: Baltic and the North Sea (Schulz, 1951); the Bahamas (Renaud Debyser 1959); Roscoff, France (d'Hondt, 1970); Bogue Beach, North Carolina (Lindgren, 1971); Shilshole Bay and Clallam Bay, Washington; Cape Meares, Oregon; Crescent City, Newport Beach and La Jolla, California (Pollock, 1989); Coleman Beach, California during Summer 1994 at 10m and 14m along the transect from MLLW in cores from 40-50cm and 20-30cm depth respectively.

Description: As is the case with all the other species encountered at Coleman Beach, the population of S. bradypus is slightly smaller than that reported elsewhere and in agreement with measurements reported by Pollock (1989) from other California beaches. Measurements obtained from animals at Coleman Beach, however, Fall well within the adult ( developmental stage N) range of 95-11 OlJm determined for this species by Renaud-Mornant & Anselme-Moizan (1969) from specimens collected in France. Of note among the Coleman Beach population was the variation in shape of the caudal plate lateral projections. These projections were pointed in some individuals while in others they were round and short. This phenomenon appears to be unique to the Coleman Beach population. 40

Discussion: This cosmopolitan species bears a remarkable resemblance to Stygarctus abornatus (McKirdy et aI., 1976). Among the only features separating the two are the absence of the dorsal processes at body plate II in S. abornatus. Another similar species is Stygarctus gourbaulitae (Renaud-Mornant, 1 981 b) which is distinguished by the presence of small spines on the anterior margins of dorsal plates I and n as well as by small posterior extensions on these same plates. It is evident from the similarities that these species are closely related. 41

TABLES Morpi h ometry 0fStv.oarctus sJ)inifer and S. bradypus from Coleman Beach.

S. spinifer S. bradypus

Body length 1OB.B ±B.3 (9) 107.1+13.6 (B)

Median cirrus 9.5 ±.a.S (4) 9.5+0.6 (4)

Internal cirrus 9.0+0.9 (7) 10.4±0.4 (6)

External cirrus 11.4+2.0 (6) 7.a±1.9 (3)

Anterior clava 6.3±.a.B (9) 14.6±.3.0 (6)

Latera I cirrus 12.6+2.3(9) 12.1+1.4 (5)

Posterior clava 7.4±0.4 (9) 6.5+1.2 (5)

Dorsal spike 20.2±5.0 (7) 21.3±1.6 (6)

Trunk spine 23.1 + 5.6 (9) 22.7+3.3 (6)

Lateral spike 8.6±1.2 (9) 6.6±1.0 (5)

Leglv hair 20.8+ 5.3 (9) 11.1±0.B (4) Caudal spike . none present 2S.3±4.0 (7) Length+ standard deViation Cn); all lengths In Jim 42

Distribution and Temporal Abundance

Spring Samples (March 23,1994; Table 6, Figures 6,7) Three species of tardigrades were encountered in these samples; Batillipes tridentatus, Halechiniscus remanei and Stygarctus spinifer. All were found in cores collected at 5 and 10 meters above MLLW, with the most abundant species being Batillipes tridentatus. Eleven individuals were recovered 'from the core sample representing a depth 30-40cm at Sm along the transect. They were found in every core sample collected at 10m along the transect with 75 individuals occurring in the surface (0-10cm) core. The number of B. tridentatus specimens present in the core samples decreased as the depth of the cores increased. Only two specimens were encountered in the deepest sample at ground water level (50-60cm). H. remanei specimens occurred in the deeper cores at 10m beginning with the 30-40cm core and continued to the ground water depth at 50-60cm. Two specimens of H. remanei were found in each of the cores, except for the SO-60cm core which contained only one individual. Stygarctus spinifer was represented in the 40-S0cm and the sO-60cm cores of 1Om by one individual in each. The specimens found at sm consisted of eleven Batillipes tridentatus and one Halechiniscus remanei, all found in the ground water sample at 30cm depth. 43

TABLE 6 Arthrotard'IQrada recovere d d'unnQ S'ipnng 1994

Sample B. tridentatus H. remanei S. spinifer MS 30-40 11 1 - Ml0,0-10 75 - - Ml0 10-20 15 - - Ml020-30 12 - - M10 30-40 6 2 - M1040-S0 4 2 - M10S0-60 4 1 1 M10, G.W. 2 2 1 Totals 129 8 2

120~------~ --m- B. tridentatus 100 • H. remanei -II-- S. spinifer

20 o~~~~~~~~~~--~ o 10 20 meters along transect from MLLW FIGURE 6. Intertidal distribution and abundance, Spring 1994 44

B. tridentatus

0 M10,0-10 111 Ml0, 10-20 ~ x Ml 0, 20~30 ~ H. remanei 0 +-' ~ M10, 30-40 III Ml0, 40-50 Ml0, 50-60 • Ml0, G.W. S. spinnifer

° 20 40 60 80 number of individuals

FIGURE 7. Vertical distribution within substratum at 10m from MllW (sta. 2), Spring 1994. Cores designated as depth in centimeters, G.W. denotes the sample at ground water level. 45

Summer (July 23 1994; Table 7, Figures 8, 9) Seven different species were recovered from these samples with the majority occurring in cores collected between 8m and 14m along the transect from MLLW. The most abundant species was H. remanei. A total of 96 specimens were recovered. 8. tridentatus was again present and was the second most abundant species. The greatest diversity and abundance of tardigrades occurred at 1Om along the transect from MLLW in sediments from 40-S0cm deep. These included twenty-four H. remanei, eleven Tanarctus arborspinosus, eleven Stygarctus bradypus, and all three H. californiensis. 46

TABLE 7 Arthrotardigrada recovered during Summer 1994

B. tridentatus B. sonomacus S. spinifer 5 bradypus

M420-30 - 2 - -

M5 10-20 - - - - M8 20-30 25 2 - - M1 0,0-1 0 - 1 - - M1020-30 - - - - M1030-40 - - 2 - M1040-50 - - - 1 1 M14 10-20 1 1 - - M1420-30 - - 2 2 Totals 26 6 4 1 3

T. arborspinosus H. californiensis H. remanei M4,20-30 - - - M5,10-20 - - 1 M8,ZO-30 - - 5 M100-10 - - - Ml020-30 - - 13 Ml0,30-40 8 - 22 M10,40-50 11 3 24

M14,10-20 - - 12 M14,20-30 - - 19 Totals 19 3 96 47

-a--- B. tridentatus • B. sonomacus III ----Ii- H. remanei (il 60 ::I --0- H. californien. "C 'S; T. arborspino. '5.s ----t1- S. bradypus I+ S. spinlfer 0 40 ' Q.) ..a E ::I c:: 20

2 3 4 5 8 10 14

meters along transect from MLLW

FIGURE 8. Horizontal (intertidal) distribution of Tardigrada Summer 1994

M14,20-30 M14,10-20 :.__ _ M14,0-10 0 M10,30-40M10,40-5 1555:==~~§iiii5'l11l11- • B. tridentatus Ml0,20-30 .. S. sonomacus Ml 0,10-20 H. remanei Ml 0,0-1 0 ~ H. californiensis MB,20-30 • ______o T arborspinosus MB,10-20 II S. bradypus M8,0-10 o S. spin/fer MS,20-30 , f MS,10-20 MS,0-10 M4, 20-3 0 ~---'---'------f--r--r----r--....----r-....-----l o 10 20 30 40 so number of individuals FIGURE 9. Distribution and abundance of Tardigrada in samples collected Summer 1994 48

Fall (November 3 1994; Table 8, Figures 10, 11, 12) The samples collected during Fall 1994 were dominated by Batillipes sonomacus with a total of 95 specimens recovered. The second most abundant species was S. spinifer with thirty-three specimens. All but one of these were found at 16m along the transect from MLLW in sand 40-S0cm deep. The distribution of tardigrades was not limited to the upper intertidal area. As before, however, maximal densities were recovered from samples collected at a distance greater than 8m landward of MLLW. B. tridentatus and H. remane; were again present. A total of twenty-four and twenty two specimens were recovered respectively. T. ramazzotti occurred in low abundance with all eight specimens well distributed throughout the transect. During Fall 1994 a pattern emerged in the distribution of B. tridentatus and B. sonomacus. The greatest abundance of these species occurred at a depth of 30-40 cm (Figure 12),

Relative Temporal Abundance (Figure 13) Different species were encountered throughout the study year at Coleman Beach and dominant species changed along with the seasons. B. tridentatus was common throughout the year but was most abundant in the Spring. H. remane; was most abundant in the Summer and the B. sonomacus population maximum was observed in the Fall. 49

TABLE 8. Arth rotar d' igra da recovered during Fall 1994.

8. tridentatus 8. sonomacus H. remanel hramazzotti S. spinifer M2, 20-30 1 2 - 1 - M2. 30-40 1 7 - 3 - M2 40-50 - 2 - - - M4 10-20 - 9 - 1 - M6. 10-20 1 1 - - - M6 20-30 - 10 - - - M6 30-40 - 12 - - - M8 10-20 - 2 - - - M8 20-30 1 - - - , M8 30-40 9 3 1 1 - M8 40-50 - 4 - - - M9 20-30 2 4 - - - M9 30-40 4 29 1 1 - M9 40-50 1 6 1 - - M10 10-40 1 - - - - M10.40-50 - 2 1 - - M12.10-20 - - - 1 - M12 20-30 - 1 -- - M1230-40 1 1 - - - M1250-60 2 - 5 - - M16, 0-10 - - 1 - 1 M16 20-30 - - 1 - - M16 30-40 - - 3 -- M16,40-50 - - 8 - 32 TOTALS 24 9S 22 8 33 50

40.------,

III "iii 30 ::l ~ B. tridentatus "0 :~ • B. sonomacus "0 .,---11/-- H. remanei £ ----<> T. ramazzotti 4 20 0 S. spinifer ' ..aQ.l E ::l c: 10

10 20 meters along transect from MLLW FIGURE 10. Horizontal distribution of Tardigrada observed during Fall 1994

M16,30-40M16,40-50 J::======:r---I M16,20-30 M16,0-10 M12,SO-60 __• M12,30-40 M12,20-30 M12,10-20 Ml0,40-50 M9,40-50 M1M9,30-400,30-40 i55:=~------M9,20-30 M8,40-50 )I___aa M8,30-40 M8 ,ZO-30 • B.trldentatus • B. sonomacus M8,1M6,30-400-20 ~====-. M6,20-30 II H. remanei M6,10-20 T. ramazzotti M4, 10-20 )11___1':8 liiI S. splnlfer M2,40-50 "'__1IZiZI o M2,30-40 JII M2,20-3 0 i==="-'---""--~--r--...... ,..---r---"",--1 o 10 20 30 40 number of Individuals

FIGURE 11. Distribution and abundance of specimens in samples collected Fall 1994. 51

M16,40-50 M16,30-40 M16,20-30 • B.tridentatus M16,O-10 II B. sonomacus M12,50-60 M12,30-40 M12,20-30 Ml 2,10-20 Ml0,40-50 M10,30-40 1/ M9,40-50 ~==:.______i M9,30-40)l '" M9,20-30 IA MS,40-50 ..____ MS,30-40 ~ MS,20-30 MS,10-20M6,30-40 J====: M6,20-30 M6,10-20 M4,1 0-20 :'___111 M2 ,40-5 0 ....__l1li M2,30-40 }II M2,20-3 0 -F=--,----r--....----r--...... ,---,.----,..---; o 10 20 30 40 number of Individuals

FIGURE 12. Distribution of Batillipes tridentatus and B. sonomacus Fall 1994

S. brady pus • Fall Summer S.spinifer II • Spring

T.ramazzotti

T. arborspinosus

1\1 >C ....1\1 H. remanei

H. californiensis

B. sonomacus

B. tridentatus

0 20 40 60 80 100 120

number of individuals

FIGURE 13. Relative Temporal Abundance of aU Tardigrade Taxa 53

CHAPTER IV. DISCUSSION

The abundance of large sand grain sizes at Coleman Beach provides large interstitial spaces which enables the circulation of water containing oxygen and nutrients. A rich diversity of fauna was encountered including interstitial representatives from the phyla Arthropoda, Nematoda, Annelida, Cnidaria, Gastrotricha, Kinorhyncha and Mollusca among others in addition to a diversity of Tardigrada. Batillipes sonomacus is the third species described from the west coast of North America in as many studies. The diversity of Batillipes species here still appears low, however, when compared to that along the East Coast: only four species here compared to six along the East Coast (Pollock, 1970a; Undgren, 1971; McKJrdy, 1975). Pollock (1970a) identified a common pattern of species composition based on his studies at Woodis Hole, Massachusetts as well as on findings from European studies. This pattern consisted of one common species of Stygarctus, a rare Ha/echfn.iscus, and two to four species of Batillipes; with one or two BatillJpes sp. as the most abundant constituents. Although this pattern was subsequently reported at Bogue Bank, North Carolina (Lindgren. 1971), it has not been observed for Tardigrada studied in the Pacific Ocean. McKirdy et al. (1976) reported a complete absence of Batillipes at beaches in the Galapagos Islands. One species of BatilJipes was encountered by Noda (1985) at Tanabe Bay, Japan and Pollock (1989) noted the 54 presence of only one species, if not the complete absence, of Batillipes at beaches sampled along the west coast of the United States. My study presents the first account of two species of Batillipes in a single Pacific ocean beach. As in the pattern observed by Pollock (1970a), two BatiJlipes species comprise the more abundant constituents at Coleman Beach. In this case, however, the abundance varies throughout the year with B. tridentatus the dominant species during Spring and B. sonomacus the most abundant in the Fall. The abundance of Batillipedidae that I observed during Spring and Fall at Coleman Beach agrees with observations made along the Atlantic coast of North America and in Europe. McGinty & Higgins (1968) reported population increases of both B. mirus and B. bullacaudatus in Virginia during Spring and Fall. Grimaldi deZlo at D'Addabbo Gallo (1975) also found population maxjma in Spring and Fall while studying B. pennaki at a beach near Bad, Italy and Pollock (1970a) reported population increases of B. bulJacaudatus in Spring and Fall at Woods Hole, Massachusetts. An alternation in species abundance has not been previously reported, yet this appears to be the case at Coleman Beach. Although the mechanisms influendng this phenomenon cannot be presently identified, it is likely associated with intra-generic competition. The fact that Batillipes tridentatus and R sonoms(;us were encountered at all tidal heights and depths is consistent with results obtained elsewhere as no definitive distribution pattern has emerged for this genus, although intra-generic distribution patterns were observed at a single beach by Pollock (1970a). PoHock ( 1989) 55 noted a general absence of Batillipes spp. from the top 15 cm of sand sampled at sites along the Pacific coast of the United States. The greatest concentration of B. tridentatus encountered during the present study (75 individuals 1OOcm- 3) was extracted from the top 10cm at 10m above MLLW during Spring. Nonetheless, it is still likely that the occurrence of Tardigrada within the top 1Scm is not as common on the Pacific coast as it is elsewhere. From the distribution observed at Coleman Beach it appears that the most common depth for both species is about 30-40cm. Greater densities were consistently found at tidal heights above 8m from MLLW Indeed, the most common tidal height for all tardigrades at Coleman Beach was at mid to high tide level. Pollock (1989) reported Halechiniscus remane; to be the most abundant species in southern California beaches during Summer 1987. It is possible that his observations are related to Summer densities seen at Coleman Beach as H. ramana! was present throughout the year and was the most abundant species in Summer samples. The dominance of Halechiniscids in terms of diversity during Summer at Coleman Beach is unprecedented in North America and contradicts Pollock's pattern of spedes diversity. Besrdes Ii remanei, Tanarctus arborspinosus was also present along with H. californiensis. Tanarctus ramazzotti replaced T. arborsplnosus in Fall samples. Once again this congeneric alternation suggests intra .. generic competition. Although H. remanei was previously known to occur in California ( McGinty, 1969; Pollock, 1989), the present study extends the known range for the remaining three 56

Halechiniscids and represents the first sighting of each since their original descriptions as new taxa. Halechiniscus remanei is known to have an intertidal distribution pattern similar to that of Stygarctus spp. (Pollock, 1989). With few exceptions all H. remanei specimens encountered at Coleman Beach occurred at mid to high tide levels (8m above MLLW or greater) and at depths greater than 20cm. This pattern was also observed for Tanarctus arborspinosus and H. californiensis. Tanarctus ramazzotti occurred at similar depths but the six specimens found were evenly distributed in terms of tidal height throughout the transect. There are two possible explanations for the even distribution of T. ramazzotti. The most obvious is that perhaps tidal height is not a factor which influences its distribution. A second possibility is that this even distribution was caused by wave transport. T* ramazzotti was originally described from subtidal sediments (Renaud-Mornant, 1975b). The specimens I found could have been subtidal and deposited intertidally during high tide. This phenomenon is likely the mechanism behind the occurrence of Echiniscoides siglsmundi in interstitial habitats since thfsspecies is more commonly known to occur on barnacles ( Shuster & Grigarick, 1965; Pollock, 1970a, 1975; Hallas & Kristensen 198.2). In either case, there is a degree of uncertainty because of the limited extent of my study compounded by the existence of only one previous report of this species. The apparent low abundances of T. arborspinosus, T. ramazzotti and H. californiensis could possibly be inaccurate representations 57 resulting from the limited sampling regimen. T. arborspinosus was reported to occur primarily at the ground water level by Lindgren (1971) and T. ramazzotti was originally described from subtidal sediments (Renaud-Mornant, 1975b) which suggests that these species may be more common in the saturated sediments deeper than 60cm at Coleman Beach where I did not collect. The known range for Stygarctus spinifer and S. bradypus was extended to the west coast of North America by Pollock (1989), Although this is the first temporal abundance observation for S. spinifer, the population peak in Summer observed for S. bradypus is similar to abundances observed March through July in France (Renaud-Mornant & Anselme-Moizan, 1969) and in Summer at Bogue Bank, North Carolina (Lindgren, 1971). Pollock (1989) found S. bradypus in 6 of the 8 beaches sampled along the west coast of North America which suggests it is most abundant in Summer throughout the West Coast. Population maxima during Summer and Fall were reported for S. granulatus by Pollock (19708) at Woods Hole, Massachusetts where no congeneric species were present. At Coleman Beach peak densities of S. spinifer occurred during Fall. Based on these observations, it appears that Stygarctus spp. population maxima are common in Summer and Fall in North America and that reciprocal relationships occur where congeneric species are present. Alternations in abundance were noted for S. granulatus and S. bradypus by Lindgren (1971) at Bogue Bank, North Carolina. When present at Coleman Beach Stygarctus species never occurred in depths less than 20cm. Based on the literature this is a typical depth for the genus. S. spinifer was found below 20cm depth 58 with maximum densities at a depth of 50-60cm. In its type locality S. spinifer was extracted from depths of 40-150cm (Hiruta, 1985). It is, therefore, likely that greater densities could exist in deeper sediments at Coleman Beach. Likewise, S. bradypus has been reported from deep sand (Schultz, 1951; d'Hondt, 1970; Lindgren, 1971; Pollock, 1989). In the present study S. bradypus was extracted exclusively from sediments 20-30cm and 40"SOcm in depth. Stygarctids are typically also found to occur in the upper intertidal heights ( Pollock, 1970a; Lindgren, 1971; Pollock, 1989). Specimens recovered from Coleman Beach were all found at 10m along the transect from MLLW and higher with the greatest densities of S. bradypus at 14m above MLLW and of S. spinifer at 16m above MLLW. Although tentative, the species composition and patterns of distribution and temporal variation observed at Coleman Beach are consistent with those found elsewhere. The surprising result of this study has been that species diversity along the coast of California is much more rich than previously known. A total of 10 species were found at Coleman Beach over the course of the year. In addltlon to the eight discussed above, Echiniscoides slgismundi and a Hypsibius sp. were also encountered. Clearly this composition establishes that diversity along the Pacific coast of North America is as great as that found elsewhere. The occurrenCe of seven different psammophilic species at one time (Summer 1994) parallels the diversity observed in Europe and the eastern United States. 59

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PLATES

List of abbreviations; acl...... anterior clava ca...... caudal appendage cl...... clava dp...... dorsal plate ec...... external cirrus ic...... internal cirrus Ic...... Iateral cirrus I IS ...... leg I spine

I IIs ...... leg II spine INs...... Ieg IV spine Itp ..••...... dorsal plate lateral process Ispk ...... Iateral spike mc...... median cirrus pcl...... posterior clava pts ...... posterior trunk spine scl...... secondary clava (cephalic papillae) 66

-----Ic

SOllm ~'\-----..·Ispk ~Pts

------IIVs

PLATE 1. Batillipes sonomacus, ventral view. 67

ic \ Ie '--t~/

-Ins 50#Jm

pts

PLATE 2. Batillipes tridentatus, ventral view 68

_-----·11S

SOllm

~Pts ea

PLATE 3. Halechiniscus remanei remanei, ventral vjew 69

me i e

------115

SO#lm

----pts

PLATE 4. Halechiniscus californiensis, ventral view 70

50IJm ------pts

-----IIVs

PLATE 5. Tanarctus arborspinosu5, ventral view 71

pts

50pm

----IIVs

PLATE 6. Tanarctu5 ramazzotti, ventral view. 72

Ie ~ -----pcl

-----dp

-----ltp 50pm

.~-....------pts

------aes

PLATE 7. Stygarctus spinifer, dorsal view, legs i-IIJ not shown. 73

me ic acl / ec

\"J4£ _____ Ie ------pel

_-----dp

- Itp

SOpm

----acs

PLATE 8. Stygarctus bradypus, dorsal view, legs I-Ill not shown"