ECOLOGICAL ASPECTS OF TUBULARIA CROCEA (AGASSIZ, 1862) AND ITS PREDATORS IN ELKHORN SLOUGH, CALIFORNIA

A Thesis Presented to the Graduate Faculty of California State University, Hayward

In Partial Fulfillment Of the Requirements for the Degree Master of Arts in Biological Sciences

By John W. Cooper August 1979 Copyright © 1979 by John W. Cooper ABSTRACT

The occurrence of Tubularia crocea (Agassiz, 1862), a complex of tunicate , and nudibranch molluscs upon fouling plates at two subtidal sites in Elkhorn Slough, Monterey County, California was documented from March 1977 to February 1978. Autumn and winter settlements ofT. crocea were accompanied by infestations of nudibranchs. In most instances the regenerative capacity of hydroid colonies could compensate for polyp losses to predation. Several species of tunicates were most abundant upon fouling plates in the summer and displayed an annual settle­ ment periodicity. The exclusion of Tubularia crocea by tunicate invasion and overgrowth was not verified by hydranth predation experiments. Of the fourteen species of nudibranchs collected upon fouling plates, eight species fed upon Tubularia crocea. Aspects of feeding, spawning, and foraging behavior were investigated in predatory Coryphella trilineata 0 1 Donoghue,

1921 and Cumanotus beaumonti (Eliot, 1906). The seasonal occurrence of Tubularia crocea in Elkhorn Slough suggested the presence of predatory nudibranchs was primarily due to the allochthonous transport of veligers. The repeated seasonal occurrence of predatory nudibranch species may be facilitated by planktonic larval survival of long duration. The decline in abundance of Tubularia crocea was coincident with, but not solely the result of feeding by predatory nudibranchs. Polyp losses and the sloughing of hydroid colonies were primarily attributed to environmental fluctuations in Elkhorn Slough. ACKNOWLEDGEMENTS

Appreciation is extended to the many individuals who have contributed to this study. I thank my major professor, Dr. Jim Nybakken, for his introduction to the literature on nudibranch feeding ecology, support of my work, and advice, during the completion of my thesis. I am grateful to Dr. Greg Cailliet for his lucid commentary and thorough reading of my thesis. To Dr. Ned Lyke I owe appreciation for thought-provoking discussions and his continued interest in my work. Monica Farris contributed unending assistance, encour­ agement and love, even while cursing into her regulator on nearly seventy dives with me to the darkest reaches of Elkhorn Slough. The outstanding talents, unflagging spirit, and top­ side wit of Chris Jong contributed immeasureably to the completion of the field work. Her reluctance to let the flame go out even in the face of adversity should remain' an inspiration to all that probe Elkhorn Slough. I wish to acknowledge- Messrs. Bob Christensen, Terry Eckhardt, and Mark Silberstein as the true pioneers of slough diving. The noteworthy aid and camaraderie of Moss Landing Marine Laboratories divers Cynthia Annett, Cheryl Hannan, Rober Helm, Gary Ichikawa, Lynne Krasnow, Rodger Ogren, Steve Pace, Carl Schrader, Howard Teas, Doug Vaughan,

vi and Mary Yoklavich was significantly beneficial on innumerable occasions. The following institutions and persons have provided facilities, literature, comments and correspondence that has contributed a great deal to the scope of this study: the William G. Kerckhoff Marine Laboratory, Gary McDonald, Baron, Susan Harris, Don Cadien, David Franz, Larry Harris, Alan Kuzirian, Sandra Millen-Crane, George Mackie, Richard Miller, Pierre Tardent, and Jack Word. I thank Dr. Nybakken for bringing to my attention recent synonymies and generic revisions by Gary McDonald of: alpha (Baba and Hamatani, 1963) to columbiana (O'Donoghue, 1922); Hermissenda crassicornis (Eschscholtz, 1831) to Phidiana crassicornis (Eschscholtz, 1831); albocrusta (MacFarland, 1966) to Cuthona albocrusta (MacFarland, 1966); and Trinchesia fulgens (MacFarland, 1966) to Cuthona fulgens (MacFarland,l966).

Lastly, I wish to thank Peggy Rupp for the typing of this final manuscript.

vii TABLE OF CONTENTS

INTRODUCTION 1

Study site 6

MATERIALS AND METHODS 10

RESULTS 24

Occurrence of fouling species at the Dairies 24

Occurrence of fouling species at Kirby Park 34

Occurrence of nudibranchs and spawn upon fouling plates 42

Prey chemosensory experiments 58

Nudibranch feeding and spawning experiments 63

Hydranth predation experiments 70

Regeneration in Tubularia crocea 74

DISCUSSION 76

SUMMARY 98

LITERATURE CITED 100

viii LIST OF FIGURES

Figure Page 1 Map of Elkhorn Slough, Monterey County, California with station sites at the Dairies and Kirby Park 8 2 Diagram of (a) the sampling apparatus and (b) rack with the arrangement of fouling plates 11

3 Cumulative average of (a) the number of Tubularia crocea colonies and (b) the percent basal cover of colonies per panel for January and February 1978 as a func­ tion of the number of fouling panels de­ ployed at the Dairies station 14

4 Diagram of the Y tube apparatus utilized in chemosensory experiments 17

5 Smoothed monthly mean surface water temperatures at (a) the Dairies and (b) Kirby Park 22

6 Average (a) number of Tubularia crocea colonies, (b) percent basal cover of Tubularia crocea, and (c) fortnightly number of actinulae per panel at the Dairies station from March 1977 to February 1978 25

7 Average (a) number of tunicate species colonies and (b) percent basal cover of tunicate species colonies per panel at the Dairies station from March 1977 to February 1978 30

8 Bar graph of the average (a) number of Tubularia crocea and tunicate species colonies and (b) percent basal cover of Tubularia crocea and tunicate species per panel at the Dairies station from March 1977 to February 1978 32

ix LIST OF FIGURES Figure Page

9 Average (a) number of Tubularia crocea colonies' (b) percent basal cover of Tubularia crocea, and (c) fortnightly number of ·actinulae per panel at the Kirby Park station from March 1977 to February 1978 35 10 Average (a) number of tunicate species colonies and (b) percent basal cover of tunicate species colonies per panel at the Kirby Park station from March 1977 to February 1978 38 11 Bar graph of the average (a) number of Tuhularia crocea and tunicate species colonies and (b) percent basal cover of Tubularia crocea and tunicate species per panel at the Kirby Park station from March 1977 to February 1978 40

12 The (a) feeding and (b) spawning rate of Coryphella trilineat~ at different predator-prey densities as a function of the number of predatory _Coryphella trilineata per combination 65

X LIST OF TABLES

Table Page

1 The age in days of Tubularia crocea colonies with mature, actinul~earing gonophores collected upon fouling plates 28 2 Occurrence of nudibranchs and spawn at the Dairies station and the monthly total for each species collected upon two and four week fouling plates from March 1977 to February 1978 43

3 Occurrence of nudibranchs and spawn at the Kirby Park station and the monthly total for each species collected upon two and four week fouling plates from March 1977 to February 1978 44 4 Number of nudibranch species and indivi­ duals collected upon predation and control fouling panels for three experiments at the Dairies and a single experiment at Kirby Park 45 5 The prey of nudibranch species occurring upon fouling plates in Elkhorn Slough 46

6 Summary of the known embryonic periods of nudibranch species found upon fouling plates in Elkhorn Slough 47 7 The chemosensory behavior of Coryphella trilineata to seawater supplied by Y and T tube apparatuses 60 8 The chemosensory behavior of Coryphella trilineata to seawater and seawater with Tubularia crocea effluent supplied by Y and T tube apparatuses 61 9 The chemosensory behavior of Cumanotus beaumonti to seawater supplied by Y and T tube apparatuses 62

xi LIST OF TABLES

Table Page 10 The chemosensory behavior of Cumanotus beaumonti to seawater and seawater with Tubularia crocea effluent supplied by Y and T tube- apparatuses 62 11 The feeding and spawning rate of Cory­ phella trilineata at various densities upon Tubularia crocea during 36 hour experiments 64 12 The feeding and spawning rate of Cumanotus beaumonti at various densities upon Tubularia crocea during 36 hour experiments 67

13 Average number of colonies and percent basal cover of Tubularia crocea per panel upon control and experimentally clipped fouling plates in Elkhorn Slough 72

14 Average number of colonies and percent basal cover of tunicate species per panel upon control and experimentally clipped fouling plates in Elkhorn Slough 73

15 The known duration of metamorphosis and of the free-swimming planktotrophic veliger stage of selected species of nudibranchs 89

xii INTRODUCTION

The large gymn.oblastic hydroid Tubularia crocea (Agassiz, 1862) is a predominant fouling species at certain times of the year in Elkhorn Slough, California. No quan­ titative, long term fouling study has been conducted in Elkhorn Slough, except for fouling and community succession projects by students in the Marine Ecology classes at Moss Landing Marine Laboratories in 1968, 1970 and 1971. MacGinitie (1927, 1935) conducted no investigations of foul­ ing organisms in his study of Elkhorn Slough, but did note the occurrence of nine hydroid species, including T. crocea. Thus, the composition and seasonal nature of this epiphytic marine community has yet to be comprehensively studied. Many life history attributes of Tubularia species have been investigated in the field as well as in the laboratory. Tubularia species are characteristically found inembayments and harbors with swift moving waters (McDougall, 1943; Woods Hole Oceanographic Institution, 1952; Knight-Jones and Nelson-Smith, 1977; Knight-Jones, et. al., 1957; Miller,

1976). Hydrocauli which ~nfrequently branch, bear single feeding hydranths and arise from a basal stolon mat. There are no free-swimming medusae in this . Colonies are dioecious and females liberate benthic actinula larvae. Settlement and reproduction in Tubularia crocea is interrupted by high (above 18 - 240C) and cold (below 10 -

1 2

18°C) water temperatures (Pearse, 1906; Morse, 1909; Sumner, et. al., 1913; Hyman, 1920; Moore, 1939; McDougall, 1943; Graham and Gay, 1945; Woods Hole Oceanographic Institution, 1952; Clark, 1975). Polyp autotomy is a controversial feature of the life history of Tubularia crocea and the subject has been re­ viewed by McDougall (1943) and Rungger (1969) . The general concensus is that it occurs in response to changing environ­ mental conditions (Moore, 1939; Berrill, 1948; Pyefinch and Downing, 1948; Mackie, 1966; Rungger, 1969). Rungger (1969), however, concluded that endogenous factors govern sponta­ neous autotomy in T. crocea at Naples, Italy, and that this event was an integral feature of the life cycle. He did not observe an epidemic loss of hydranths from colonies in any particular season, but that a certain number of hydrocauli were always lacking hydranths. The shedding of polypswith the gonophores compensates for the missing medusae stage of this hydroid by aiding the dispersal of larvae for the prop­ agation of new colonies (Tardent, 1963; Mackie, 1966; Rungger, 1969). The polyps of Tubular_ia crocea are readily regenerated in most circumstances. Only Tardent (1956) has investigated the potential duration of the regeneration process. He followed colonies in the laboratory through fifteen cycles of autotomy with subsequent hydranth regeneration during a 74 day period. 3

There has been no investigation as to the influence of nudibranch predation upon the process of polyp loss. In studies to date of Tubularia species, authors have con­ cluded that the influence of all predators is negligible (McDougall, 1943; Pyefinch and Downing, 1948; Rungger, 1969). Several investigators, however, have noted the ability of hydroid-eating nudibranchs to "overgraze" their prey (Swennen, 1961; Thompson, 1964; Clark, 1975). These authors imply or state this grazing is responsible for the extinction of the food source, resulting in the subsequent disappearance of the nudibranchs. This conclusion is based primarily upon observations in the field, without investi­ gations of feeding rates, quantitative determination of prey availability, or a complete knowledge of prey life histories. Other workers, such as Chambers (1934), Miller (1962), Waters (1966), and Rivest (1978) conclude that aeolid nudibranchs crop their food and do not entirely kill prey populations. Hence, the disappearance of hydroids may be due to a combination of predation by nudibranchs and other factors. There is a paucity of information on many aspects of the feeding ecology of the nudibranch molluscs of the Pacific coast of North America. Geographical surveys ofthe opisthobranch fauna of California usually denote only collecting localities and substrates of occupancy (Sphon and Lance, 1968; Roller and Long, 1969; Gosliner and 4

Williams, 1970; Bertsch, et. al., 1972; Holleman, 1972; Goddard, 1973; Behrens and Tuel, 1977). Observations of feeding are scarce. Robilliard (1971) briefly discussed feeding of six nudibranch species from Washington and British Columbia. A comprehensive review and summary of the known food of 60 species of California nudibranchs has been compiled by McDonald and Nybakken (1978). Several methods have been used to establish the food of nudibranchs. Swennen (1961) combined field and labora­ tory observations of feeding with the ability of nudibranchs to live a considerable period of time on the suspected food item to confirm prey species. Choice experiments by means of a Y-tube or similar apparatus have also been utilized to determine a preferred food species (Stenhouwer, 1952; Braahms and Geelen, 1953; Harris, 1970; Bloom, 1976; Willows, 1978). The induction of metamorphosis in the presence of prey species appears to be an additional im­ portant criterion in establishing the food of nudibranchs. It is likely that veligers will metamorphose only in the proximity of the prey of the adult (Hadfield, 1963; Thompson, 1964). Miller (1961) separated nudibranchs into two ecological groups, those that are annual species with one generation and those that produce several generations a year. Annual species were those that fed upon prey present year round, while subannual species fed upon prey exhibiting seasonal 5 fluctuations in their presence and abundance. A majority of authors (Thompson, 1964; Waters, 1966; Clark, 1975; Franz, 1975; Nybakken, 1978) have continued to employ this classification. Franz (1975) further classified the annual species as K-strategists and the subannual species as r-strategists. Most ecological investigations to date have been con­ ducted upon annual species of nudibranchs (Thompson, 19 58:.,. 1961, 1966; Potts, 1970). Comprehensive accounts of the life histories and ecology of subannual species of nudi­ branchs are few. By and large, hydro ids comprise the diets of many subannual species of nudibranchs (Miller, 1962; Thompson, 1964). Elkhorn Slough affords the opportunity to investigErte the relationship between predatory nudibranchs and hydroid prey. The aeolid nudibranchs Coryphella trilineata and Cumanotus beaumonti are present in sufficient numbers upon Tubularia crocea to conduct experimental studies of their feeding ecology. Coryphella trilineata is also found year round in rocky intertidal habitats of central California (Nybakken, 1974). The author has seen this species eat a variety of hydroid prey, including Campanularia everta Clark, 1876, Eudendrium californicum Torrey, 1902, Syncoryne spp., and Tubularia marina (Torrey, 1902). The enigmatic and cryptic C. beaumonti is of interest in that this species was described from Europe, though it has not been collected 6 there for a period of about fifty years (Thompson and Brown, 1976). The species of Cumanotus used in this study matched the description of Eliot (1906) for C. beaumonti and has only been found upon T. crocea. My study was conducted to answer two ecological questions: 1) does the seasonal abundance of predatory aeolid nudibranchs coincide with that of their preferred prey; and 2) is nudibranch predation responsible for the decline and disappearance of Tubularia crocea in Elkhorn Slough? Field and laboratory investigations were under­ taken to elucidate the interaction between nudibranchs and T. crocea, and to evaluate changes in fouling community development as a result of predation.

Study Site

The study side was Elkhorn Slough, Monterey County, California (Figure 1). Elkhorn Slough is a coastal embay­ ment with a single opening to Monterey Bay near the apex of the Monterey Submarine Canyon. A tidal prism extends four to five km. up the channel of this shallow, marine embay­ ment (Smith, 1973). Waters inshore of the tidal prism may have a residence time in excess of 300 days and are generally more saline and warmer in summer and cooler in winter than open ocean water ($mith, 1973). Tidal currents may approach 1~ knots (SO - 72 em/sec) in the main channel at the Highway 1 bridge on ebbing spring tides (Clark, 1972). 7

An additional hydrographic feature is the Pacific Gas and Electric Company discharge of 1.6 x 106 m3 I day of heated seawater into the lower reaches of Elkhorn Slough (Smith, 19 7 3) . Sampling was conducted at two stations, in the upper reaches of Elkhorn Slough at Kirby Park and more seaward at the Dairies (Figure 1). These stations correspond to the hydrographic station numbers 3 and 2, respectively of Broenkow and Smith (1972). 8

Figure 1. Map of Elkhorn Slough~ Monterey County, California with station sites at the Dairies and Kirby Park. 9

Kilometers 2

0 1/2 Nautical Miles

·. ~ ::. (\,_.. ;· .. ~-· ·.-. ::. @. · ELKHORN ,.:'~/:···· SLOUGH ·.:: / f ~ ..

DAIRIES f.lATERIALS AND METHODS

Subtidal fouling plate racks capable of 360 degree rotation in currents were deployed at the Dairies and Kirby Park in a manner similar to that of Bourget and Lacroix (1971). The Dairies rack was at 6.7m (22 ft.) and the Kirby Park rack at 4.75m (15ft.) depth below mean higher high water. The racks were constructed of 1 inch diameter white polyvinylchloride pipe and were positioned about a meter above the bottom of the slough in mid-channel (Figure 2). The plates were lOcm x lOcm black plexiglass of 2.5mm thickness with the surfaces roughened by sandblasting. Sampling commenced on 7 March 1977 and was concluded on 22 February 1978. A series of five replicate fouling plates was exposed for approximately two week (12 - 19 days) and four week (26 - 36 days) intervals. Fouling plates were successfully deployed and recovered during the entire study period, except for the month of December 1977. This was due to the breakage of a support post for the rack. The two week interval sampling of fouling plates at both stations was precluded due to inclement weather and winter rains only in January and February 1978. Fouling plates were set and retrieved by SCUBA diving at slack high tide. The larval jar stand and fouling plate

rack were wirebrushed to clean off settled oraanisms1::> and algae at each two week interval. Fouling plates were

10 11

Figure Za. Diagram of sampling apparatus and mooring with larval jar stand and fouling plate rack in place.

Figure Zb. The arrangement of fouling plates in the rack. A total of twenty plates were deployed, se~arated at ten centimeter intervals from each other and the rack frame. 12

I I I l I I I{

1 ll I l I I I~ ------I. . ·1 I I I I 13

transported in 1~ quart freezer containers and examined alive within 48 hours of collection. In the laboratory each side of a fouling plate consti­ tuted a panel, which was examined, photographed and the number of Tubularia crocea colonies and settled actinulae enumerated. The reproductive condition of colonies was noted, and those possessing five or fewer hydrocauli were arbitrarily designated actinulae. A photographic enlarge­ ment of each panel was projected and traced upon paper. The basal cover of T. crocea was determined by utilizing a K & E compensating polar planimeter. Area was measured to the nearest square millimeter. The minimum number of fouling plates necessary to adequately sample Tubularia crocea was determined according to the methods of Pielou (1966) and Nybakken (1978). In months of either low (January 1978) or high (February 1978) mean number ofT. crocea colonies or mean percent basal cover per panel, as few as five panels represented the minimum number of sampling units necessary (Figure 3). Thus, the deployment of 10 panels for each sampling interval was adequate.

Due to the considerable abundance of compound tunicates upon fouling plates, the mean number of colonies and their basal cover was determined by planimetry. Tunicate larvae and colonies of less than 1 mm2 area were not measured. Nudibranchs upon Tubularia crocea colonies and fouling 14

Figure 3a. The cumulative monthly average of the number of Tubularia crocea colonies for January and February 1978 as a function of the number of fouling panels deployed at the Dairies station.

Figure 3b. The cumulative monthly average percent basal cover of Tubularia crocea for January and February 1978 as a function of the number of fouling panels deployed at the Dairies station. 15

20 a

Ul Feb. lJ IS 2 - 0 _j 0 v

0 1!21 z lX

2: :::J s v

-Jan.

s 1121 IS 2S NO. OF PRNELS

IS: b 0:::w > 0 v Feb . ...J a: I !a Ula: tf1 1-z LJ v l1:w s a.. lX ~ :J v -Jan.

s: 1!21 IS: NO. OF"' PANELS 16 plates were enumerated and their crawling length measured to the nearest millimeter. This measurement corresponds to the standard length (anterior margin of head to poster- ior tip of tail) of Risso-Dominguez (1963). Nudibranchs were observed for feeding and spawning activity. The food of nudibranchs upon fouling plates was determined using the criteria of Swennen (1961). Fouling plates were re- tained for an additional two weeks in running aerated sea- water and re-examined for overlooked or metamorphosed nudi- branchs. All plates were subsequently scraped clean, soaked in freshwater, and dried before reuse. The chemosensory abilities of Coryphella trilineata and Cumanotus beaumonti were tested utilizing Y and T tube apparatuses (Figure 4) ~ Individuals collected from fouling plates and floating rafts in Elkhorn Slough were randomly placed in a 20cm diameter bowl. An inclined tube of 9mm

diameter introduced seawater from Y or T tubes supplied by an overflow from 800ml beakers. A prey species of hydroid was randomly placed in one of the beakers and the number of nudibranchs entering the arms of the tube was counted after

24 hours. The apparatus ~as disassembled, scrubbed, and soaked in freshwater between experimental trials. On repeated occasions, trials in these apparatuses were conducted to assure that nudibranchs were exhibiting a chemosensory response to prey hydroids and not a rheotactic response to the water current. 17

Figure 4. Diagram of the Y tube apparatus utilized in chemosensory experiments. A constant flow of seawater through the tube was assured by an overflow of water from the beakers. A screened siphon tube maintained a constant volume of water in the large fingerbowl and prevented the loss of nudibranchs. 18 19

Feeding and spawning rates were determined for

Coryphella trilineata and Cumanotus beaumonti. Stems with mature Tubularia crocea polyps of approximately equal size were utilized as prey. Juvenile £. trilineata (10 - 15 mm length), adult C. trilineata (15 - 25 mm length), and adult C. beaumonti (5 - 8 mm length) were tested. Nudi- branchs and T. crocea polyps were confined in fingerbowls, with 4 to 20 replicates per combination. The predator: prey combinations tested were: 1:5, 1:10, 2:20, 2:50, 5:25, and 5:50. Experiments were of 36 hour duration, and it was assumed that nudibranchs ate and spawned at the same aver­ age rate during experiments. The fingerbowls were placed in an incubator or on the wet lab table at Moss Landing

Marine Laboratories. Seawater in the bowls was changed at

6 hour intervals and consumed polyps were replenishedafter

24 hours. Upon termination of experiments the number of polyps eaten and the spawn laid were counted. The average rnmber of prey consumed per nudibranch per 36 hours was

calculated, as was the average number of egg masses laid.

The veliger larvae from the spawn of available species

of nudibranchs collected from fouling plates were cultured.

Egg masses were isolated in individual autoclaved Pyrex

culture dishes containing 0.8~ Millipore filtered seawater. Cultures were incubated in the dark at 15°C. Cetyl alcohol

akes were added to cultures to prevent veligers from be­

coming trapped at the surface (Hurst, 1967). Larvae were 20 fed algal cultures procured from International Shellfish Enterprises, Moss Landing, California. The induction of metamorphosis of veligers was attempted by introducing potential species of hydroid prey to the cultures. A series of experiments was conducted to assess the response of Tubularia crocea to predation. Five of ten replicate fouling plates with four to six weeks growth were "preyed" upon with scissors to remove the hydranths from colonies. These plates were subsequently retrieved after two weeks and examined as described above. Colonies of Tubularia crocea scraped from fouling plates were tied in clumps and hung from the buoy lines at both stations. These colonies had lost all their hydranths after being held in laboratory aquaria. The regenerative capacity of these colonies was qualitatively evaluated. The surface water temperature was measured fortnightly at each station with a bucket thermometer to the nearest 0.1°C. Monthly average temperatures were plotted after undergoing a weighted "smoothing" process. These "smoothed" monthly values were computed using the formula:

smoothed value Tz = 1 1 + 2 lTz) + T3 4 where Tl = month 1 average temperature value.

Tz = month 2 average temperature value, etc. At the Dairies station, the surface temperature ranged from 16°C in .January 1977 to 18.7°C in September 1977, with 21 a steady decline to a low temperature of 14.6°C in February 1978 (Figure Sa). The range of surface tempera­ ture was greater at the Kirby Park station. It ranged from 16.3°C in January 1977 to a peak of 22.3°C in August 1977, with a precipitous drop to a low temperature of 15.4°C in December 1977 and January 1978 (Figure Sb). 22

Figure Sa. The smoothed monthly mean surface water temperature at the Dairies station from January 1977 to February 1978.

Figure Sb. The smoothed monthly mean surface water temperature at the Kirby Park station from January 1977 to February 1978. 23

a

...... v 0 :2JZI v w 0:: :::! !- a: 0:: w 11. IS: :E: w !-

.J F M A M .J .J A S 0 N 0 .J F MONTHS

b

...... v 2lZI v w ct ::I 1-cc w0:: Q.. IS: !:w 1--

ll2!

.J FMAM.J .J AS 0 NO .J F MONTHS RESULTS

Occurrence of Fouling Species at the Dairies

Tubularia crocea colonies were present upon four week plates during all months at the Dairies station except in

May 1977 (Figure 6a). The fewest colonies (x = 0.3, S.D.= 0.6) were present from April to June, and a peak in the mean number of colonies of 13 per panel occurred in October. There was a decline in the number of colonies until January 1978, when an average of only one colony was present per panel. A dramatic increase followed in February, when a mean of 16 colonies per panel was present. The mean percent basal cover of Tubularia crocea colonies exhibited similar trends ·(Figure 6b). Coverage was minimal Cx = 0.8, S.D. = 1.6) during the months of April to July 1977 at the Dairies station. A peak occurred in October, when the mean percent basal cover of T. crocea colonies was 14% of panel surfaces. A decline subsequently occurred in November and by January 1978 an average of only 1% of panel surfaces was occupied. Concomitant with the February settlement of colonies, the mean basal cover reached a second peak of 12%. The mean number of settled actinulae of Tubularia crocea was determined from two week interval plates (Figure

6c) · There was a peak in the number of actinulae lx = 8 .1, S.D. = 7.4) per panel that occurred during late March at

24 25

Figure 6a. The average number of Tubularia crocea colonies per panel at the Dairies station from March 1977 to February 1978. The bars represent the 95% confidence limits.

Figure 6b. The average percent basal cover of Tubularia crocea per panel at the Dairies station from March 1977 to February 1978. The bars represent the 95% confidence limits.

Figure 6c. The f0rtnightly average number of settled Tubularia crocea actinulae per p~nel at the Dairies from March 1977 through November 1977. The bars represent the 95% confidence limits. 26

' I

0 1121 z iX ( r\!

MA,\11~ ..J ASQi'\JCJ..J MONTHS

2S: b w0::: > 0 21

_j 0: li1 0: IS ClJ .... 'z w v 1121 j 0:::w 0.. IX s:

M A M ..J ..J A S 0 N 0 ..J F MONTHS

112112l c 312l

31

'-112l 0z 31;3 IX

212l

1121

121 M A M -.J -.J A s D N D -.J F MONTHS 27 the Dairies station. Recruitment ofT. crocea actinulae was minimal (x = 0.8, S.D. = 1.2) from April until August. Peak actinulae settlement occurred in late August, Septem­ ber, and October, with an average of 46, 70, and 36 actinulae present per panel, respectively. During the latter part of November, an average of 20 actinulae were present per panel. It was observed that Tubularia crocea colonies on two week plates and the rack attained sexual maturity and liberated actinulae from July to October at the Dairies station (Table 1). Colonies with gonophores bearing de­ veloping gametes were present on March and November foul­ ing plates immersed for 17 days. Tubularia crocea took about a month to reach maturity in January and February, and actinulae liberating colonies were present inFebruary upon plates immersed for 29 days. The seasonal occurrence and distribution of two other hydroid species on fouling plates at the Dairies was qualitatively noted. The calyptoblast Obelia cf. longissima (Pallas, 1766) generally displayed maximal growth from May through July, with a second less abundant bloom in November. Settlement and growth of Bougainvillia glorietta Torrey, 1904 was maximal in May with a second bloom in August and September. This species occurred more abundantly at Kirby Park.

Several species of compound tunicates were abundantly 28

Table 1. The age in days of Tubularia crocea colonies with mature, actinulae-bearing gonophores collected upon fouling plates.

MONTH DAIRIES KIRBY PARK

MARQI 17

APRIL

MAY

JUNE

JULY 15* 12

AUGUST 16* 16,27*

SEPTEMBER 13* 27*

OCTOBER 13* 13, 27*

NOVEMBER 17 19*

DECEr,ffiER No data 38*

JANUARY 32 32

FEBRUARY 29*

* = liberating actinulae 29 present upon fouling panels at both stations. The most frequent was an unknown species of Botrvllus, which had a brilliant orange test. Botryllus tuberatus (?) Ritter and

Forsyth, 1917 was also abundant, and possessed a purple test with silver, gold, or white zoids. The white tunicate Diplosoma macdonaldi Herdman, 1886 was present only in July at the Dairies. An unusual, unidentified turicate with a translucent, filmy tunic and golden zooids was the only species observed to overgrow the aforemen­ tioned species of tunicates. Tunicates were considered together because of the difficulty in species identifica­ tion, their similar morphology, habitat, and presumed influence upon community structure and development.

Data are not available for tunicate settlement in

May or December 1977 at the Dairies station. An average of seven tunicate colonies per panel were present in March and reached a peak of 48 colonies in September at the

Dairies station (Figure 7a). This high abundance continued through October and November with 47 colonies present per panel. Tunicate colonies were absent from fouling plates in January and February +978, and the presence of larvae was not noted during these months.

Tunicate colonies occupied an average of 1% of panel surfaces in March at the Dairies and reached a peak in coverage of 14% in August (Figure 7b). There was a sub­

sequent decline to 3% coverage per panel by November. 30

Figure 7a. Average number of Tubularia crocea colonies per panel at the Dairies station from March 1977 to February 1978.

Figure 7b. Average percent basal cover of Tubularia crocea per panel at the Dairies s~ation from March 1977 to February 1978. 31

5!21 a

Sl21

U1 l.J Yl2!· z 0 ...J 0 v 3!21

0 z 2!21 IX I 112! rt

M A M ..J A S 0 N 0 ..J F MONTHS

3!21 b 0:: w > 0 v ..J a: 2!21 Ul a: tlJ 1- :z w v ~ 10 0.. I><

M A M · ..J A S 0 N 0 ..J F MONTHS 32

Figure Sa. Bar graph of the average number of Tubularia crocea colonies (white) and tunicate species colonies TDiack) per panel at the Dairies station from March 1977 to February 1978.

Figure Bb. Bar graph of the average percent basal cover of Tubularia crocea (white) and tunicate species (black) per panel at the Dairies station from March 1977 to February 1978. 33

S!Z! a l f l ;:• • Y!2l '· 1- ' l wlJ1 ::312! - z 0 _j 0 v 2!Z! 1- ,.... 0z I ~· IX 10 1- , I r-

I L.c I ._..._ 11 M A M ~ ~ A S a N a ~ F MONTHS

:25:: b a:: w > 0 :2l2l 1- 1,) a:....J Ul a: IS: F- t:O r- f- r- ,.... :zw - v 10 F- r- a:: w 0.. I 1>< s 1=- I

,_. L r a..- n M A M ~ ~ A S a N a ~ F MONTHS 34

Although tunicate colonies were most numerous in October and November, they were of small size. In all months that Tubularia crocea and colonies of tunicates were present on fouling plates at the Dairies, the tunicates were numerically abundant (Figure Sa). The average percent basal cover ofT. crocea on panels, how­ ever, was greater than that occupied by tunicates in the months of March, October and November {Figure 8b).

Occurrence of Fouling Species at Kirby Park At the Kirby Park station, no Tubularia crocea colonies were present upon fouling plates from March to June 1977 (Figure 9a). Colonies became established dur­ ing July 1977 and were present every month until January

1978. A peak in the number of hydroids occurred in November with an average of five colonies present per panel. Only a single T. crocea colony settled upon December fouling plates. In January, an average of two colonies per panel were present at Kirby Park. Tubularia crocea was absent from this station in February. The mean percent basal cover of Tubularia crocea colonies was maximai in October at Kirby Park, when 12% of panel surfaces was occupied (Figure 9b). In November colonies occupied 9% of panel surfaces, and by December the lone colony present occupied 1% of a panel surface.

Settled actinulae of Tubula~ia crocea were present in 35

Figure 9a. The average number of Tubularia crocea colonies per panel at the Kirby Park station from March 1977 to February 1978. The bars represent the 95% confidence limits.

Figure 9b. The average percent basal cover of Tubularia crocea per panel at the Kirby Park station from March 1977 to February 1978. The bars represent the 95% confidence limits.

Figure 9c. The fortnightly average number of settled Tubularia crocea actinulae per panel at the Kirby Park station from March 1977 to February 1978. The bars represent the 95% confidence limits. 36

2S: a

2!3 LJl w z c iS av

I Ia 0z IX s:

M A M -..J ..JASONQ..j MCJNTHS

2S: b 0:: w > 0 213 v

_j a: Lna: IS: Ill r- z w v 1!3 0::w a.. IX s:

M A M ...J J A S 0 N 0 ...J ,= MONTHS

11

I Ia 1-

0 I I I I I I M A M .J .J A sJ~ a N 0 .J F MONTHS 37

April, July, and from September through November at Kirby Park (Figure 9c) . Peaks in the occurrence of actinulae took place in late October and November, with an average of 18 and 21 larvae present per panel respectively. At Kirby Park the first settled colony of Tubularia crocea to possess mature gonophores was present in July, upon a plate immersed for 12 days (Table 1) . In the sub­ sequent months of August to December, mature colonies of T. crocea on fouling plates and the rack were noted to be liberating actinulae. Obelia cf. longissima was noted to be present from June until August, being most abundant during the latter month. A second less abundant bloom occurred in October and November. Bougainvillia glorietta was present upon panels in April and May, with a second bloom from September through November. Tunicate settlement data were not recorded for March, May, July, and August. Thus, the interpretation oftrends in the occurrence of tunicates at Kirby Park station is difficult. An average of four colonies of tunicates was present per panel in Apr~l at this station (_Figure lOa) . A peak in abundance occurred in October, when an average of 33 colonies was present per panel. In December and February no tunicates were present. An·average of four tunicate colonies per panel was present in January 1978. The average cover of tunicate species was 1% per panel 38

Figure lOa. The average number of tunicate species colonies per panel at the Xirby Park station from March 1977 to February 1978. The bars represent the 95% confidence limits.

Figure lOb. The average percent basal cover of tunicate species per panel at the Dairies station from March 1977 to February 1978. The bars represent the 95% confidence limits. 39

6121 a

sra

li1 w Yl2f 2 0 ..J 0 !...,) 312!

0 2 20 /X i 1!2] t I

M A M ...J A S 0 N 0 ...J F MONTHS

3!2! b ct w > 0v

_j 0: 20 Ul 0: tlJ f- w2 v 0:: w ll2l 0... I)( t

M A M ...J ...J A S 0 N 0 ...J F MONTHS 40

Figure lla. Bar graph of the average number of Tubularia crocea colonies (white) and tunicate species colonies (black) per panel at the Kirby Park station from March 1977 to February 1978.

Figure llb. Bar graph of the average percent basal cover of Tubularia crocea (whit~ and tunicate species (black) per panel at the Kirby Park station from March 1977 to February 1978. 41

a

Y0

Ul w 30 z 0 _j 0 v 20 0z /X 1.0

M A M ~ ~ A S a N 0 ~ F MONTHS

10

M AM~~ AS aN 0 ~ F MONTHS 42 in April at Kirby Park, and 5% in June. September panels had an average of 14% tunicate doverage, which declined to 2% by November (Figure lOb). In January 1978 an average of 1% of panel surfaces was occupied. In all months that Tubularia crocea and colonies of tunicates were present together on fouling plates at Kirb~ Park, the tunicates were numerically abundant (Figure lla). The average basal cover ofT. crocea on panels exceeded that of the tunicate species in October, November; and January (Figure llb).

Occurrence of Nudihranchs and Spawn Upon Fouling Panels A combined total of 14 species of nudibranchs were collected upon fouling plates deployed in Elkhorn Slough. All 14 species occurred at the Dairies, with frondosus (Ascanius, 1774), Coryphella trilineata~ and adspersa (Nordmann, 1845) being the predominant species (Table 2). For the most part, the nudibranch species that occurred at this station displayed pro­ nounced abundances in March and April and from September through November. Only seven nudibranch species were collected at Kirby Park (Table 3). was by far the most abundant species, particularly during June. Doto .§:_myra (Marcus, 1961) and Eubranchus rustyus (Marcus, 1961) Were maximally abundant from October through December. Table 2. Occurrence of nudibranchs and spawn at the Dairies station and the cumulative monthly total for each species collected upon two and four week fouling plates from March 1977 to February 1978.

SPECIES MAR APR MAY JUN JUL AUG SEP OCT NOV DEC JAN FEB ------Coryphella cooperi 1

Coryphella trilineata 13* 3 * 8* 10* 22* 1

Coryphella sp. 1 3 1

Cumanotus beaumonti 1 3* * *

Cuthona a1bocrusta 1 1 1 7

Cuthona columbiana 1

Cuthona fu1gens 1

Dendronotus frondosus 10 20* 6* 13* 5* 5

Dendronotus iris 1 1 1

Doto amyra 5* 2 1 2 * 6 34 1

Eubranchus rustyus 3* 1 2 1 7

Phi diana crassicornis 4 * 1 2 3 10 1*

Spurilla chromo soma 1 ·----- ~ Tenellia adspersa 2* 5* 19* 23* 12* 5* 2* 1* lN

* ::: Spawn Present Table 3. Occurrence of nudibranchs and spawn at the Kirby Park station and the cumulative monthly total for each species collected upon two and four week fouling plates from March 1977 to February 1978.

SPECIES MAR APR MAY LJUN JUL AUG SEP OCT NOV DEC JAN FEB

Cory-ehella COOJ2eri Coryphella trilineata 3 Co:IJ:T.!1ella sp. Cumanotus beaumonti ----Cuthona a1bocrusta 2 ---Cuthona columbiana _Cuthona fu1gens Dendronotus frondosus 3 Dendronotus iris Doto amyra 1* 3 2 2 Eubranchus rustyus l 4 1 5

Phi diana crassicornis.. 1 6 SJ2uri11a chromo soma ----Tenellia ad sEers a 2* 38+* 492+* 71+* 93+* 141+* 67+* 31+* :64+* 53+* *

* = Spawn Present Table 4. The cwnulative nWJlbo.rs of species and individuals collected upon predation: control panels for three experiments at the Dairies and a single experiment at Kirby Park. * = Spawn present.

DAIRIES KIRBY PARK SPECIES I II III I

Coryphella cooperi 1:2 0:1 Coryphella trilineata 28: 52* 23:40 0:1* Coryphella sp. 2:0 Cumanotus beawnonti - 3*:3* 2:2* Cuthona albocrusta 1:0 Cuthona columbiana 2:0 Dendronotus frondosus 1:1 --Do to amyra 12:3 Phi diana crassicornis 1:1 6:5 Tenellia adspersa 7:10* * 0:1 *

Total number of species 1 5 7 3

Total ntm1ber of individuals 7:10 35:58 47:51 0:3

DAIRIES I conducted 07/16/77 to 08/18/77 II conducted 08/18/77 to 10/14/77 III conducted 10/14/77 to 12/02/77 KIRBY PARK I conducted 09/03/77 to 11/15/77 46

Table 5. The prey of nudibranch species occurring upon fouling plates in Elkhorn Slough.

Bougainvillia Obelia cf. Tubularia SPECIES Diadumene glorietta longissima crocea sp. ?

Coryphepa cooperi X

CoryPhella sp. X

Coryphella trilineata X X

Cumanotus beaumonti X

Cuthona albocrusta X

Cuthona --columbiana X

Phi diana crassico:rmis X

Tenellia adspersa X X

Do to amyra X X

Dendronotus frondosus X

Dendronotus iris X Eubranchus rustyus X S_eurilla chromo soma X Table 6. Summary of the known embryonic periods (spawn to hatch) of nudibranch species occurring upon fouling plates in Elkhorn Slough. Legend to Locality Abbreviations

AZ/SSR :::: Azov Sea, Russia FH/WA :::: Friday Harbor, Washington CP/CA ::: Carmel Point, California IM/ENG :::: Isle of Man, England CP/DM :::: Copenhagen, Denmark IS/DM :::: Isefjord, Denmark DB/CA ::: Dillon Beach, California MB/CA :::: Monterey Bay, California ES/CA = Elkhorn Slough, California

ADULT EMI3RYONIC SPECIES LENGTH (MM.) LOCALITY TE!vlP. °C PERIOD (DAYS) REFERENCE

Coryphella trilineata 5 - 20 DB/CA 15 - 16 4.5 - 6 Bridges and Blake 1972 15 - 25 ES/CA 15 5 - 6 Cooper February 1976 about 15 CP/CA 15 9 - 10 Cooper February 1976 15 - 26 ES/CA 15 6 Cooper July 1976

Cumanotus beaumonti FH/WA 8 - 11 10 Hurst 1967

Cuthona a1bocrusta 5 - 6 FI-1/WA 8 - 11 20 - 21 Hurst 1967

Cuthona columbiana to 8 CP/CA 15 7 Cooper November 1976

Dendronotus frondosus IM/ENG 10 32 Thompson 1967 ~ --J ADULT EMBRYONIC SPECIES LENGTH (MM. ) LOCALITY TEMP. °C PERIOD (DAYS) REFERENCE

(Continued) Dendronotus frondosus PH/WA 8 - 11 7 - 15 Hurst 1967 10 30 FH/WA - 13 16 Robilliard 1970 DB/CA 14 6 Williams 1971 10 - 40 ES/CA 15 6 Cooper 1976

Dendronotus iris 65 120 FA/WA 13 17 Robilliard 1970

Do to amyra 3 - 8 ES/CA 15 4 Cooper September 1977 3 - 8 ES/CA 15 4 - 7 Cooper June 1978

Phi diana crassicornis 25 MB/CA 13 - 15 5 - 6 Harrigan and A1kon 1978

Tenellia adspersa 2 - 8 ES/CA 10 - 11 11 Cooper August - October 1977 2 - 8 ES/CA 15 4 - 5 Cooper August - October 1977 4 - 5 AZ/SSR 12 - 17 9 Turpaeva 1963 4 - 5 AZ/SSR 20 - 22 4 Turpaeva 1963 2 - 8 CP/DM 17.3 9 Rasmussen 1944 2 - 8 IS/OM 20 - 25.5 4 - 5 Rasmussen 1944

.j::>. 00 49

Ten of the 14 species were also collected upon pre­ dation plates deployed at the Dairies and Kirby Park (Table 4). These species were maximally abundant at the Dairies during predation experiment III, which was con­ ducted from mid-October to December. In contrast, nudi­ branchs were virtually absent upon predation plates at Kirby Park. A brief description follows of the occurrence, size and observed feeding and spawning behavior for each species of nudibranch. Three species of Coryphella were present upon fouling plates and all were found to co-exist in October upon Tubularia crocea at the Dairies station (Table 2). A single Coryphella cooperi Cockerell, 1901 of 40mm length was collected in October at the Dairies (Table 2), as was another specimen from predation panels retrieved in this month (Table 4). At Kirby Park this species was not found upon fortnightly or four week panels, although a 49mm specimen was present on November predation panels (Table 4). Coryphella cooperi were observed to feed only upon the hydranths and gonophores of Tubularia crocea (Table 5). Coryphella trilirieata was collected at the Dairies in March and April, September through November, and in February (Table 2). This species was very abundant 6n pre­ dation panels retrieved at the Dairies in October and 50

December (Table 4). Specimens of this species ranged

from 2 to 45mm in length. At Kirby Park, ~- trilineata was collected only upon November panels (Table 3 and 4).

Coryphella trilineata was consistently found upon

colonies of T~bularia crocea and actively fed upon the hydranths and gonophores. This species was neither ob­

served nor collected upon Bougainvillia glorietta, though

this hydroid was eaten when offered to nudibranchs in the

labor a tory_ (Table 5) .

The spawn of Goryphella trilineata was found only

once at Kirby Park, upon predation plates retrieved in

November (Table 4). Egg masses of C. trilineata from

Elkhorn Slough hatched after five to six days in the lab­

oratory at 1soc, in contrast to nin-e to ten days for

spawn cultured from Carmel Point, Monterey County,

California (Table 6). The induction of metamorphosis in

the presence of Tubularia crocea was unsuccessful, though

the free-swimming veligers of C. trilineata were main­

tained and fed Dunaliella sp. for two days.

As undescribed species of CoryPhella, matching the

description of McDonald ~1977), was collected at the

Dairies station in March, October, and February (Table 2

and 4). Specimens ranged from 2 to 22mm in length. This

species of CoryPhella was not collected at Kirby Park.

Individuals were found upon Tubularia crocea and readily 51 fed upon the hydranths and gonophores of the hydroid

(Table 5).

At the Dairies station, Cumanotus beaumonti was collected only in September and October (Table 2). Four additional individuals were present upon predation panels retrieved in early December (Table 4). Specimens ranged from 2 to 8mm in length. This species was always associ­ ated with Tubularia crocea and fed voraciously upon the polyps of the hydroid. When starved in the laboratory, however, C. beaumonti would consume I· marina (Table 5). The corkscrew shaped egg masses of Cumanotus beaumonti were noted at the Dairies in October, November, December and in February (Table 2 and 4). Egg masses cultured in

the laboratory hatched after three to £our days and were fed Dunaliella sp. for two days (Table 6). Repeated

attempts to induce metamorphosis in the presence of

Tubularia crocea were unsuccessful.

Three species of Cuthona were collected upon fouling

plates, and two of these species were noted to feed and

spawn upon Tubularia crocea.

Collections of Cuth9na albocrusta were made in March,

April, October and November at the Dairies (Table 2). A

single specimen was found upon predation panels retrieved

in December at the Dairies (Table 4). At Kirby Park, a

single specimen was collected upon predation panels in

November (Table 4). It was inferred that this species fed 52 upon Tubularia crocea by rasping through the perisarc of hydroid stolons (Table 5). The individuals collected ln November had pinkish red cerata identical to the color of T. crocea. Two specimens were collected in December at Kirby Park (Table 3). Individuals of C. albocrusta measured from 1 to 8mm, and were typically found among the basal stolon tangles ofT. crocea colonies. A single Cuthona columbiana (O'Donoghue, 1922) of Zmm length was collected in March at the Dairies (Table 2). Two additional specimens of 3 and 8mm length were found on predation panels retrieved in December at this station (Table 4). Cuthona columbiana was not collected at Kirby Park. Cuthona columbiana was consistently observed to rasp upon Tubularia crocea stolons (Table 5). Individuals collected upon December predation panels were identical in color to the pink coenosarc ofT. crocea. This nudi­ branch species was neither collected nor observed to feed on other species of hydroids in Elkhorn Slough. The period from spawning to hatching for Cuthona columbiana egg masses was seven days at 1soc (Table 6). Attempts to induce metamorphosis in f_. columbiana veligers in the presence of Tubularia crotea were unsuccessful. A single 12mm specimen of Cuthona fulgens (MacFarland, 1966) was found in April at the Dairies station (Table 2). 53

This nudibranch was not observed to feed or spawn ln the laboratory.

Three species of Dendronotacean nudibranchs, Dendra­ notus frondosus, D. iris Cooper, 1863, and Doto amyra were collected upon fouling plates and were observed to feed upon species of hydroids other than Tubularia crocea:

(Table 5).

Dendronotus frondosus was found at the Dairies station from March through July, and again in November

(Table 2 and 4). Specimens at this station ranged from 1 to 40mm in length. Only large, adult Q. frondosus of 20 to 40mm length were collected at Kirby Park in

December (Table 3).

Dendronotus frondosus was observed to feed upon Obelia cf. longissima in two ways. Nudibranchs upon hydroid stems either rasped the hydranths from their thecae or gnawed through the perisarc proximal to the thecae. The coanosarc and hydranth were then sucked from the hydro­ caulus and consumed. At no time were D. frondosus observed to eat Tubularia crocea.

Spawn of Dendronotus frondosus was noted only at the

Dairies, from April through July (Table 2). Egg masses hatched after six days in culture at 1soc in the labora­ tory (Table 6). The induction of metamorphosis was not successful, though veligers fed upon Dunaliella sp. and lived four days after hatching. 54

Single individuals of Dendronotus iris were collected upon four week plates at the Dairies during March, April, and June (Table 2) . All the specimens collected were juveniles no greater than 7mm in length. The color phase of these nudibranchs was grayish white, with orange and brown banded cerata. Dendronotus iris was not collected ' at the Kirby Park station. Dondronotus iris was observed to feed upon Obelia cf. longissima in the manner previously described for D. frondosus.

Doto amyra was collected at the Dairies from March through May, in August, and from October to January (Table

2 and 4). Nudibranchs ranged from 1 to 7mm in length. At

Kirby Park, D. amyra was collected in September and from

November through January (Table 3).

Doto amyra was characteristically adhered tightly among the basal stolons of hydroid colonies, including

Tubularia crocea. At no time, however, were D. amvra ob­ served to have rasped through the perisarc of I· crocea. Vvhen feeding upon the stolons of Bougainvillia glorietta,

the cerata of this species were most often a vivid red

color. Nudibranchs were-observed to feed upon the basal

stolons of Obelia cf. longissima, and spawn was often

present upon colonies.

Egg masses of Doto amyra were noted upon fouling

Plates at the Dairies in March, while spawn was noted at 55 both stations in September. In culture egg masses hatched between four and seven days (Table 6) . Attempts to induce metamorphosis in this species were unsuccessful, although the free-swimming veligers were maintained for two days after hatching. The aeolid Eubranchus rustyus was collected at the Dairies station in March, April, and from September through November (Table 2) . Spawn was noted at the Dairies only in March. At Kirby Park, E. rustyus was collected from September through December (Table 3). Specimens ranged from 1 to 6mm in length. Eubranchus rustyus was consistently found upon Obelia cf. longissima and fed upon the hydranths of this hydroid (Table 5). The irregularily inflated cerata would often discharge their milky white contents when this nudibranch was handled with forceps.

Phidiana crassicornis (Eschscholtz, 1831) was collected in March, July and August, October to December, and in February at the Dairies (Table 2 and 4). Spawn was noted in April and October. At Kirby Park P. crassicornis was collected in November and December (Table

3). Individuals of this species ranged in length from 2 to 62mm.

Phidiana crassicornis was observed to eat Tubularia crocea polyps in the laboratory, though these nudibranchs 56

£aired poorly in captivity when provided solely with this hydroid as food (Table 5). A single specimen of Spurilla chromosoma Cockerell and Eliot, 1905 was collected upon a four week fouling plate at the Dairies in November (Table 2). This species did not feed upon hydroids, but was observed to eat the brown sea Diadumene sp. (Table 5). By far the most abundant nudibranch collected during the course of this study was Tenellia adspersa. At the Dairies, T. adspersa and its spawn were collected in April, June through November, and again in January (Table 2). Additional specimens were present upon predation panels retrieved in mid-August (Table 4). At Kirby Park, where this species was most abundant, nudibranchs were collected from April through January (Table 3). Spawn was present all these months, as well as in February. Tenellia

~spersa were also present upon predation panels retrieved November (Table 4). This species ranged in length less than a millimeter to 9mm. Tenellia adspersa fed most frequently upon the

, stems, and hydranths of E6tig~invillia glo~ietta 5). Small nudibranchs of 1 to 3mm length could eating the primordia of stems growing from of this hydroid. On one occasion, T. a was observed to feed upon the coenosarc of 57

Tubularia crocea, at the tip of a stem in the process of regenerating a hydranth. Adult I· adspersa were not ob­ served to eat the polyps ofT. crocea, though individuals were often observed rasping epizooitic growth upon stems and stolons. Spawn of I· adspersa was deposited upon

colonies of B. glorietta and Obelia cf. longissima, thoug~ nudibranchs were infrequently found and were not observed to feed upon the latter hydroid species. Tenellia adspersa was successfully reared through its entire life cycle in the laboratory. The embryonic period from spawning to hatching was four to five days at 15°C and 11 days at 10 - 11°C (Table 6). Cultures ofT. adspersa veligers reared in the absence of hydroids, how­ ever, died after hatching. i',fetamorphosis was accomplished by hatchlings in three ways when in culture with hydroids. Veligers were infrequently seeh to swim freely from egg masses. More often they would leave their capsules and metamorphose upon the stems of hydroids. It was inferred that veligers leaving the egg mass with their shells accomplished metamorphosis within 12 to 48 hours, though the process was not entirely observed. Metamorphosis also commonly occurred within the egg mass, and crawling juveniles left their veliger shells within the egg capsule. Juvenile I· adspersa grew and matured most rapidly upon !ougainvillia glorietta, as opposed to Obelia cf.

~ongissima or Tubularia crocea. At lSOC, nudibranchs 58 reared from egg masses laid in the laboratory upon sprigs of ~· glorietta took about 31 days to reach maturity. Thu~ the total life cycle was completed in about 35 to 36 days.

Prey Chemosensory Experiments A total of 132 adult Coryphella trilineata were tested in Y and T tube apparatus experiments to evaluate the behavior of this species to water currents (Table 7).

These trials served as controls for ex~eriments testing the ability of C. trilineata to locate Tubularia crocea at a distance. In theY tube apparatus, 75% of the nudi­ branchs tested in five trials displayed no response to the seawater current emanating from the entry tube (Table 7). Of the 24 C. trilineata that entered the apparatus, three nudibranchs resided within the entry tubes (desig­ nated 'no choice'), while the remainder were within the arms of the Y tube. There was no significant difference between the numbers of nudibranchs that made no choice and those found in each arm of the Y tube (Kruskal-Wallis

AN OVA, P > • 0 5) . In two T tube trials, 86% of the Coryphella trilineata tested did not respond (Table 7). Only five of the 37 nudibranchs tested entered the arms of the apparatuses. A total of 237 adult Coryphella trilineata were tested in Y and T tube apparatus experiments to determine the ability of this species to locate colonies of Tubularia 59 crocea prey at a distance (Table 8). In nine Y tube trials, 50% of the nudibranchs tested did not respond to a seawater current laden with T. crocea effluent. Of the 96 responsive nudibranchs, 87 of these entered the arms of the apparatuses, while nine individuals made no choice.

A total of 77% of the responsive C. trilineata entered th~ apparatus arm supplying seawater with T. crocea effluent.

A significantly greater number of responsive nudibranchs chose to enter this arm than the arm supplying only sea- water (Mann-Whitney U-test, P< .OS). In five T tube trials, 71% of the Coryphella trilineata tested did not respond (Table 8). Of the 24 nudibranchs that entered apparatuses, 17 individuals chose the arm supplying seawater with Tubularia crocea effluent. There was a significant difference between the mean number of C. trilineata in the T. crocea arm and in the arm of the tube with only seawater. Ct _ = 2.34, d.f. = • 0 !J 3,P<.OS).

A total of 109 adult Cumanotus beaumonti were tested 1n Y and T tube apparatus experiments to evaluate their behavior to water currents (Table 9). These trials served as controls for experiments testing the ability of this species to locate colonies of Tubularia crocea prey at a distance. In five Y tube trials, only a single f. beau­

~ of the 89 nudibranchs tested entered the apparatus 60

Table 7. The chemosensory behavior of Coryphel1a trilineata to sea­ water supplied by Y and T tubes. Of four possible responses, the categories labelled seawater are indicative of nudibranchs that resided in either of the two arms of the apparatus. No choice repre­ sents individuals that entered the inclined approach tube to the Y or T junction, while nudibranchs remaining in the bowl made no response.

NO NO APPARATUS TRIAL # IND. SEAWATER SEAWATER CHOICE RESPONSE

y 1 20 2 0 1 17

2 22 6 4 0 12

3 23 5 2 2 14

4 10 0 0 0 10

5 20 1 1 0 18

95 14 7 3 71

T 1 20 1 0 0 19

2 17 3 1 0 13

37 4 1 0 32 61

Table 8. The chemosensory behavior of Coryphella trilineata to sea­ water and seawater with Tubularia crocea effluent supplied by Y and T tubes. Of four possible responses, nudibranchs had a choice of seawater with or without hydroid prey effluent. Individuals that entered the approach tube to the Y or T junction only were designated no choice. Nudibranchs remaining in the bowl made no response.

SEAWATER+ NO NO APPARATUS TRIAL # IND. T. l:ROCEA SEAWATER CHOICE RESPONSE EFFLUENT

y 1 10 8 0 0 2 2 30 15 1 0 14 3 20 6 2 0 12 4 12 5 0 1 6 5 31 14 2 6 9 6 30 8 2 0 20 7 28 8 3 0 17 8 10 6 0 1 3 9 20 4 3 1 12

191 74 13 9 95

T 1 10 5 0 0 5 2 12 3 5 0 4 3 20 0 0 0 20 4 12 4 0 0 8 5 28 5 2 0 21

82 17 7 0 58 62 Table 9. The chemosensory behavior of Cumanotus beaumonti to seawater supplied by Y and T tube apparatuses.

NO NO APPARATUS TRIAL # IND. SEAWATER SEAWATER CHOICE RESPONSE

y 1 20 0 0 0 20 2 14 0 0 0 14 3 25 1 0 0 24 4 20 0 0 0 20 5 10 0 0 0 10

89 1 0 0 88

T 1 20 0 0 0 20

Table 10. The chemosensory behavior of Cumanotus beaumonti to seawater and seawater with Tubularia crocea effluent supplied by Y and T tube apparatuses.

SEAWATER+ NO NO APPARATUS TRIAL # IND. T. CROCEA SEAWATER CHOICE RESPONSE EFFLUENT

y 1 96 27 ,)" 0 51 2 20 1 0 0 19 3 25 2 0 0 21 4 25 0 0 3 22 5 20 2 0 0 18 6 10 1 0 0 9 .,. 198 33 ,) 3 140

T 1* 50 3 0 0 34 2 20 1 0 2 17

70 4 0 2 51

* Thirteen nudibranchs were lost. 63

(Table 9). Of the 2G C. heaumonti tested in a single T tube trial, none entered the apparatus.

A total of 268 Cumanotus beaumonti were tested in

Y and T tubes with Tubularia crocea offered as a prey item

(Table 10). In six trials, 71% of the nudibranchs tested in Y tubes did not respond. Of 39 responsive f. beaumonti, 33 individuals entered the arm supplying seawater with T. crocea effluent, while three others resided in the arm with only seawater. Three nudibranchs made no choice. Although a clear majority of the responsive nudibranchs pursued the

T. crocea effluent source, there was no significant differ­ ence between the numbers of C. beaumonti present in the arm supplying only seawater and the arm providing sea­ water with hydroid effluent (Mann-Whitney U-test, P > .OS).

In two T tube trials, a total of 70 Cumanotus beau­ manti were tested, and only six of these nudibranchs were responsive (Table 10). Four individuals entered the apparatus arm supplying seawater with Tubularia crocea effluent, while two C. beaumonti made no choice.

Nudibranch Feeding and Spawning Experiments

As the total number of Tubularia crocea prey avail­ able to predatory Coryphella trilineata in laboratory ex­ periments increased, the average number of polyps eaten increased (Table 11). The maximum predation rate of 13

T. crocea polyps consumed per nudibranch in 36 hour Table 11. The feeding and spawning rate of Coryphella trilineata at various densities upon Tubularia crocea during 30 hour experiments,

It It x It It x It SPAWN PREDATORS PREY PREY EATEN EATEN/PREDATOR ± S.E. SPAWN LAID LAID/PREDATOR ± S.E.

1 (juveniles) s 0, 0, 0, 0, 0, o.s, o.s, o.s, 0.3 + 0.1 none none 0.1

1 (adults) s 1' 1, l. s' 2.S, 0, 0, o.s, o.s 3, 4, 4, 4, 4, s 3.0 + 0.4 1, 1, 1, 1, 1' 1 0.7 + 0.1 1 10 3 , 3.S, 6, 6.5, 10 S.8 + 1.2 1, 1, 1, 1. s, 2 1.3 + 0.2 2 20 10, 11, 11. s, 14, 14 6.1 + 0.4 0, 1, 2, 2, 2 0.7 + 0.2 2 so 23, 2S, 27, 32 13.3 + 1.0 0, 1, 1, 3 0.3 + 0.1 s 2S 21, 23, 23, 2S 4.6 + 0.2 1, 2, 2, 3 0.4 + 0.1 s so 20, 2S, 2S, 2S, s, 27, 28, 32, 0, 0, 0, 0, 0, 3S S.3 + 0.3 l, 1. s, 2, O.S 0.1 + 0.0 65

Flgure 12a. The feeding rate of Coryphe11a trilineata at different predator-prey densities as a function of the number of predatory C. trilineata per combination. The bars representone standard error measurement. • = 1 predator: 5 prey o = 1 predator: 10 prey A= 1 predator: 25 prey

Figure 12b. The spawning rate of Coryphella trinineata at different predator-prey densitles as a function of the number of predatory C. trilineata per combination. The bars represent one standard error measurement. a= 1 predator: 5 prey o = 1 predator: 10 prey A= 1 predator: 25 prey 66

2 5 ~ NUMBER OF PREDATORY CORYPHELLA CD :::E :::;) z

(/) 0: ::c tO j'() 8 "3 1.5 Lj

~J.: ~ 1.0 ~ Cl <:t ..J z: 0.5 a.~ (/) IJ.. 0 a: I 2 5 !.U CD NUMBER OF PREDATORY CORYPHELLA :E :::;) z: Table 12. The feeding and spawning rate of Cumanotus beaumonti at various densities upon Tubu1aria crocea during 36 hour experiments.

# # :X # # X: # SPAW!\1 PREDATORS PREY PREY EATEN EATEN/PREDATOR + S.E. SPAWN LAID LAID/PREDATOR + S.F..

1 5 1. 5' 1. 5, 1. 5, 1' 1, 1, 1, 2 1. 5, -,? 2, 2.5, 2, 2, 2, 2.5, 2.5, 2.5, 2.5, 2.5, 2.5, 2.5, 2.5, 2.5, 3.5, 3, 3.5, 4, 4.5, 3.5, 3.5, 3.5, 3, 3, 3, 3 4, 4.5, 4.5, 5.5, 2.9 + 0.3 2.5 + 0.2

2 10 1, 1' 1. 5' 1' 1, 1' 1' 1' 1. 5' 1. 5, 2, 2, 2, 2.5, 3, 3, 2, 2.5, 2.5 0.9 + 0.1 4.5 1.0 + 0.2 68

experiments occurred with two C. trilineata upon 50 prey (Figure 12a). The minimum predation rate for adult (15 - 25mm) f_. trilineata was three polyps per predator with single nudibranchs upon five T. crocea (Table 11). In contrast to the feeding rate of adults, juvenile (10 - lSmm) Coryphella trilineata only consumed an aver­ age of 1/3 polyp in 36 hour experiments (Table 11). Single adult nudibranchs ate a significantly greater number of prey than did juvenile nudibranchs upon five Tubularia crocea polyps (Mann-Whitney U-test, P< .05). There were significantly fewer prey consumed per pre­ dator (Mann-Whitney U-test, P< .OS) with a halving of total available prey from ten to five polyps (Figure 12). Single Coryphella trilineata provided ten Tubularia crocea prey ate almost six polyps in 36 hour ex.periments (Table 11). Similarly, with paired nudibranchs, a decrease from 50 to 20 total available prey resulted in a significantly fewer number of polyps (Mann-Whitney U-test, P~ .OS) being consumed (Table 11). In high predator density experiments of 5 adult nudi­ branchs with 25 Tubulari.a crocea, Coryphella trilineata ate an average of nearly five polyps in 36 hours (Table 11). This was significantly greater (Mann-Whitney U-test,

P< .05) than the number consumed by single nudibranchs with five prey (Figure 12a). There was no significant difference (Mann-Whitney U-test, P >.OS) however, in the 69 number of prey consumed at this high predator density when 50 T. crocea polyps were available (Table 11). In low predator-to-prey ratio experiments there was no change in the feeding rate of Coryphella trilineata. At three different combinations with one C. trilineata to ten Tubularia crocea, the feeding rate remained nearly' constant (Figure 12a). There was no significant differ­ ence (Kruskal-Wallis ANOVA, P > .05) between the mean number of hydroid prey consumed by single nudibranchs on ten polyps, by paired nudibranchs on 20 polyps, or by five C. trilineata upon 50 polyps (Table 11). An increase in the total available prey and in the number of Coryphella trilineata resulted in a decrease in the number of egg masses laid per predator (Figure 12b). The maximum spawn rate of 1.3 egg masses per predator occurred with single C. triTineata upon ten Tubularia crocea prey (Table 11). The minimum spawn rate of 0.1 egg mass per predator occurred with five nudibranchs upon SO T. crocea prey. There was a significant difference (Kruskal-Wallis

ANOVA, P < • OS) in the rate of spawn production by Cory­ phella trilineata upon 10, 20 and 50 polyps at a ratio of one nudibranch to ten Tubularia crocea prey (Figure 12b). With a ratio of one Coryphella trilineata predator to five Tubularia cr~cea prey there were significantly 70 fewer (Mann-Whitney U-test, P< .OS) egg masses laid by five nudibranchs with 25 polyps than by single nudibranchs with five polyps (Table 11). Similarly, there were significantly fewer (Mann-Whitney U-test, P=.OS) egg masses laid by five nudibranchs with 50 polyps than with 25 polyps (Table 11). In experiments with Cumanotus beaumonti upon Tubularia crocea, there was a decline in the feeding rate as the number of predators increased. At a ratio of one nudibranch to five polyps, an average of three T. crocea prey were consumed in 36 hours (Table 12). The feeding rate was significantly lower when paired f. beaumonti were provided with ten T. crocea polyps (Mann-Whitney U-test, P< .OS}. In these experiments an average of one polyp was consumed (Table 12). A decrease in the rate of spawn produced by Cumanotus beaumonti occurred as the number of nudibranchs was doubled (Table 12). Single C. beaumonti upon five Tubu­ laria crocea laid an average of 2.5 egg masses in 36 hour experiments. When paired nudibranchs were provided ten polyps, the spawning rate-was significantly lower (Mann­ Whitney U-test, P <.OS). In these experiments, only one egg mass was laid per nudibranch (Table 12) .

!i_vdranth Predation Experiments Scissor predation experiments were performed in the 71 field to ascertain if a cropping of hydroid cover would precipitate a change in either hydroid or tunicate cover upon fouling panels. Three experiments were conducted at the Dairies station; during the months of July to August (I), August to October (II), and October to December (III). There were no significant differences (Mann-Whitney

U-test, P > .05) in the mean number of colonies upon control and experimentally clipped panels for either Tubularia crocea or tunicates in any of the three experiments (Table 13 and 14). There was no significant difference (Mann-Whitney

U-test, P > .05) in the mean percent basal cover on control and experimentally clipped panels of either Tubularia crocea or tunicates for Dairies experiment I and II (Table 13 and 14). In Dairies experiment III there was no significant difference (Mann-Whitney U-test, P > • 05) in the mean per­ cent basal cover of Tubularia crocea colonies on control and experimentally clipped panels (Table 13). In contrast, there was a significant difference (Mann-Whitney U-test, P< .05) in the basal cover of tunicate species upon control and experimentally clipped p.anels (Table 14). This difference was attributable to the settlement of large colonies of an unidentified tunicate species with gold zooids upon control panels. Table 13. Average number of colonies and percent basal cover of Tubularia crocea per panel upon control and experimentally clipped fouling plates in Elkhorn Slough.

DAIRIES KIRBY PARK I II III I

X# T. CROCEA COLONIES + S.E.

CONTROL 2.6 + 5.4 9.9 + 7.7 9.5 + 6.3 4.4 + 5.2

CLIPPED 3.3 + 5.3 8.6 + 10.3 9.3 + 6.1 5.1 + 5.6

X% BASAL COVER OF T. CROCEA + S. E.

CONTROL 4.9 + 15.9 22.5 + 11.7 7.8 + 12.2 40.9 + 40.7

CLIPPED 7.2 + 13.0 26.1 + 38.4 7.4 + 7.9 38.0 + 49.9

DAIRIES I conducted fl·om 07/16/77 to 08/18/77 II conducted from 08/18/77 to 10/14/77 III conducted from 10/14/77 to 12/02/77

KIRBY PARK I conducted from 09/03/77 to 11/15/77 Table 14. Average number of colonies and percent basal cover of tunicate species per panel upon control and experimentally clipped fouling plates in Elkhorn Slough.

DAIRIES KIRBY PARK I II III I

X # TUNICATE COLONIES + S.E.

CONTROL 19.5 + 25.2 9.2 + 12.2 32.3 + 49.1 6.3 + 18.9

CLIPPED 18.8 + 28.7 13.7 + 10.4 26.2 + 47.1 7.9 + 14.5

X % BASAL COVER OF TUNICATES + S. E.

CONTROL 31.3 + 66.8 17.7 + 36.2 12.3 + 33.8 26.3 + 57.4 ** CLIPPED 29.9 + 69.3 21.5 + 47.5 2.6 + 6.2 27.5 + 51.5

DAIRIES I conducted from 07/16/77 to 08/13/77 II conducted from 08/18/77 to 10/14/77 III conducted from 10/14/77 to 12/02/77

KIRBY PARK I conducted from 09/03/77 to 11/15/77

'-1 Vl ** (a significant difference, Mann-Whitney U-test, P <: • 05) 74

In a single scissor predation experiment conducted at Kirby Park in September through November, there was no significant difference (Mann-Whitney U-test, P> .OS) in the mean number of colonies upon control and exper­ mental panels of either Tubularia crocea or tunicates

(Table 13). Similarly, there was no significant differ- ence (Mann-Whitney U-test, P > .OS) in the mean percent basal cover on control and experimental panels of either

T. crocea or tunicates species (Table 14).

Regeneration in Tubularia crocea

In August and November, experimentally clipped Tubu­ laria crocea colonies at both stations were noted to have regenerated polyps. Regenerating hydranths possessing actinulae-bearing gonophores were present upon colonies after 17 to 18 days.

Bunches of Tubularia crocea without hydranths collect­ ed in November and tied to buoy lines at the Dairies sta­ tion in early December had regenerated hydranths within

21 days. Colonies collected in November and December at the Dairies and deployed in January had undergone hydranth regeneration when observed in late February 1978. In contrast, no regeneration was noted in November and

December colonies deployed at Kirby Park.

Hydranth regeneration was apparent in colonies deploy­ ed in January and February at both stations when observed 75 in May 1978. At no time were reproductive gonophores noted upon regenerated hydranths of colonies deployed from buoy lines. DISCUSSION

Tubularia crocea occurred seasonally in Elkhorn

Slough, with autumnal (mid-August through November) and winter (mid-January through March) peaks in abundance upon fouling plates. Supplemental, qualitative observa­ tions at Skippers Dock and the International Shellfish

Enterprises' rafts confirm similar settlement periods elsewhere in Elkhorn Slough. MacGinitie (1927, 1937) noted that T. crocea was exceedingly abundant in Elkhorn

Slough, particularly in August.

Hydroid colonies were not present upon Elkhorn

Slough fouling plates from April through June. Scant actinulae settlement suggests very few reproductive colonies of T. crocea persisted in Elkhorn Slough during these months. Alternatively, low temperature waters or some other factor may have caused viable colonies to re­ main sexually dormant or suspend the development of

gonophores.

The seasonality of Tubularia crocea was not as pro­ nounced at Kirby Park as-at the Dairies. The peak in

abundance of T. crocea occurred in November, a month later

than at the Dairies. Despite warmer water temperatures at

Kirby Park, colonies took longer to reach maturity and

liberate actinulae. A winter settlement of hydroid

colonies was virtually absent at Kirby Park.

76 77

The lag in establishment of Tubulari.a crocea as a major fouling species at Kirby Park may be attributable to the limited exchange and mixing of oceanic waters with resident waters in the upper reaches of the slough. Smith (1973) proposed that differing hydrographic regimes in­ fluenced the Dairies and Kirby Park. Supportive evidence' was presented by Pace (1978), who found differences in the seasonal occurrences and abundances of Acartia spp. on either side of the tidal prism. Alternatively, some factor(s) may inhibit the growth and development ofT. crocea colonies at Kirby Park. Actinula larvae were pre­ sent in April, though colonies did not become established and grow upon fouling plates until July. The results of replacement experiments with TubuTaria crocea at Kirby Park suggest that regeneration does not occur subsequent to the autumnal settlement of colonies. This may account in part for the apparent differences in the seasonal occurrence of colonies at the two study sites. The seasonal occurrence of Tubularia crocea may be in­ fluenced by the settlement of other fouling organisms that eventually displace this-hydroid species. Only T. crocea and a complex of colonial tunicate species qualify as rrfoundation species", which are "the group of species which define much of the structure of a community" (Dayton, 1972). Sutherland and Karlson (1977) operationally 78 define these as the species that attach and occupy at least

10% of fouling plate surfaces.

The invading ability of Tubularia crocea and its re- sistence to invasion by other fouling species has been elaborated upon by Sutherland and Karlson (1977). Though a good initial invader, Tubularia crocea was found to be easily displaced by tunicates at Beaufort, North Carolina, where Styela plicata (Lesueur, 1823) dominated fouling plates within three months after initial occupation by T. crocea. In Elkhorn Slough the actinulae ofT. crocea did not settle or grow upon tunicate colonies. Tunicate colonies were able to overgrow hydroid stems and it would appear they have a long-term competitive advantage overT. crocea.

The occurrence of tunicates upon fouling plates is suggestive of peak settlement during the summer. Follow- ing the peak in numerical abundance of tunicates in

September and October there was a sharp decline in the cover occupied by these colonial species. During this period the occurrence of numerous, small tunicate colonies was indicative of larval release and settlement.

This trend is apparent at both stations, though infrequent sampling at Kirby Park makes interpretation of tunicate settlement data difficult.

The settlement of tunicates is likely suspended during the winter. Though data are lacking at the Dairies 79 for December, no tunicate colonies were present during this month or in February at Kirby Park. At the Dairies, tuni­ cates were absent in January and February. Fouling plates were remarkably clean of all organisms, except for a bac­ terial film and protozoans. The existing tunicate colonies presumably grow by budding asexually and resume sexual reproductive activity in the spring. Sutherland and Karlson (1977) noted the unpredictable recruitment of Botryllus schlosseri (Pallas, 1766), and Orton (1914) observed this species to mature in less than three months. Colonies of B. schlosseri displayed a re­ sidence time on fouling plates from one to more than four months (Sutherland and Karlson, 1977). Millar (1952) found that older tunicate colonies degenerated as a pre­ lude to death. These events were not observed in Elkhorn Slough tunicate colonies, but this may be because fouling plates were immersed for too short a period of time.

Botryllus schl~sseri was noted to occur when hydroid growth was at a maximum during August and September in Cawsand Bay, England. There was a coincident occurrence of Tubularia crocea and the complex of tunicate species in Elkhorn Slough, though the peak in coverage by tunicates preceeded that of hydroid colonies. In studies at Androssan, Scotland, Botryllus schlos­

~ displayed an annual reproductive cycle (Miller, 1952; 1958). Millar also noted asexual budding in colonies was 80 infrequent during periods of summer larval release. Asexual budding was also subdued during larval release in the species of Botrvllus and Botrylloides studied by Berrill (1935). That the onset of sexual reproduction may curtail or reduce asexual colony growth may explain the indetectable differences between tunicate cover upon control and predation panels deployed in July, August, and October. The complete loss of hydranths by Tubularia crocea colonies did not result in significantly different changes in basal cover of hydroids or tunicates, as demonstrated by predation experiments. Thus, it is unlikely that the autotomy of polyps or their consumption by nudibranchs is a prelude to the disappearance of !· crocea by being over­ grown or displaced by tunicates. Alternatively, the small number of panels and their brief interval of deploy- ment may be insufficient for detectable changes 1n community development to occur. It is not surprising that eight of the 14 species of nudibranchs that reside on Tubularia crocea in Elkhorn Slough also prey upon this hydroid. In New England, Clark

(1975) documented that Catriona aur~ntia, a species of Coryphella, Cratena pilata (Gould, 1870), Dendronotus fron­ dosus, Facelina bostoniensis Cuthouy, 1838, and Tenellia fuscata (Gould, 1870) fed upon !· crocea and !· larynx. 81

Qualitative investigations of nudibranchs associated with

T. crocea in Alamitos Bay, Los Angeles County (J. Word, pers. comm.) and Newport Bay, Orange County, California (1. Harris, pers. comm.; observations by the author) indi­ cate that the occurrence of this assemblage of predatory species in Elkhorn Slough is not a local phenomenon. The most apparent damage to Tubularia crocea in Elkhorn Slough was primarily inflicted by Coryphella spp., followed by Cumanotus beaumonti and Phidiana crassicornis. In New England, Catriona aurantia has been observed to be the major predator of Tubularia (Clark, 1975; D. Franz, pers. comm.; A. Kuzirian, pers. comm.). In terms of numerical abundance and the ability to consume polyps, Coryphella trilineata was the major preda­ tor of T~bularia crocea. The effect of predation by juvenile or small (10 - lSmm) C. trilineata, however was minimal in feeding experiments. Maximal damage was in­ flicted by adults feeding at low predator densities upon colonies ofT. crocea with large numbers of polyps. In no case was the damage observed to be so severe as to result in the death of hydroid colonies. At constant predator densities there was a reduction in the feeding rate of Coryphella trilineata with a re­ duction in total number of available prey. In the constant predator : prey density combinations tested, as the number of C. triTineata individuals increased the average 82

feeding rate per nudibranch remained the same. MacLeod

and Valiela (1975) attributed a plateau in the feeding

rate of C. rufibranchialis (Johnston, 1832) unon T. - '- - larynx to 11 mutual interference!! among nudibranchs at high

predator densities. Though nudibranchs may hinder the

feeding of others upon a colony, the reproductive activi­

ties of C. rlifibranchialis were not influenced (MacLeod

and Valiela, 1975),

The spawning behavior of Coryphella trilineata

appeared to be influenced by changes in available prey

and in predator densities. In general, more egg masses were laid on colonies of small size by single nudibranchs

than by many nudibranchs on larger hydroid colonies. A

reduction in total ayailable prey at low predator densi-

ties resulted in a lowered rate of spawn. Conversely, at high predator densities, a reduction prey number resulted

in an increased spawn rate by adult ~· trilineata. It is

difficult to imagine that oviposition in nudibranchs could be markedly altered during 36 hour experiments. Clearly

the interrelationship of feeding and spawning needs to be more carefully and thor?ughly investigated. The decline

or leveling off of feeding rate in C. trilineata attribut-

able to mutual interference may be a manifestation of in-

creased spawning or copulation at high predator densities.

If indeed mutual interference does occur at high

densities of Coryphella trilineata, it may serve as a 83 feedback mechanism whereby predation of TubuTaria corcea colonies is slowed or limited. At certain, as yet un­ determined predator - prey densities, interference may cause nudibranchs such as C. trilineata to search out new colonies of prey by chemosensory means. Thus, the crowd­ ing of nudibranchs upon a few hydroid colonies may be averted. Responsive Goryphella trilineata displayed an ability to locate Ttibularia crocea at a distance in laboratory ex­ periments. A few responsive individuals would often immediately traverse a 30cm distance in the arms of the tube apparatuses. Of all the nudibranch species tested by Turner (1978), C. trilineata demonstrated the maximum recorded speed of locomotion (65 - 157 mm/sec) and dis­ played maximal tenacity in withstanding water currents equal to that endured by dorid species. Coryphella trili­ neata is well adapted for the habitat in which Tubularia crocea occurs in Elkhorn Slough. This nudibranch can readily crawl to new prey patches upon the depletion of existing hydroid colonies. It is not known how long this species can live without ·food, but observations suggest it could survive a week or longer. The success of Goryphella trilineata as a predator of Tubularia crocea is attributable to the rapid comple­ tion of its life cycle, a short embryonic period, and the 84 ability to opportunistically forage for fresh prey. Though able to eat a variety of hydroid prey, C. trilineata occurs most abundantly upon T. crocea and is most strongly allied with this hydroid species in Elkhorn Slough. The feeding and foraging strategy of Coryphella cooperi and CorypheTla sp. may be similar to that of C. trilineata, although the former two species were infre­ quently encountered. They also did not display the vita­ lity characteristic of C. trilineata when confined in the laboratory. Despite an abundance ofT. crocea prey, C. cooperi and C. sp. were rarely maintained in a healthy state for longer than a week. The feeding strategy of Cumanotus heaumonti is some­ what different than that of CorYPhella trilineata. Adult nudibranchs fed at a very low rate, and predator-prey combinations other than those tested were difficult to evaluate because feeding by C. beaumonti was difficult to detect. At identical combinations of predators and prey, the maximum feeding rate of C. beaumonti was comparable to the minimum feeding rate of adult C. trilineata. In contrast to C. tri1ineata, an increase in the number of C. heaumonti and total available prey at the same density resulted in a decreased feeding rate. As with Coryphella trilineata, the number of spawn laid by Cumanotus heaumonti varied with changes in preda­ tor densities and the amount of available prey. 85

The most egg masses were laid by single Gumanotus beaumonti on Tubularia crocea colonies of small size. There was a reduction in the number of spawn laid with an increase 1n the number of predators and prey. Thus, both species tested had a similar reproductive response. More spawn was laid as prey became limited. Though~· beaumonti feed at a slower rate than do ~- trilineata, they lay more egg masses at comparable combinations of predators and prey.

Cumanotus beaumonti would often cryptically perch and feed upon Tubularia crocea polyps. Consequently, the shedding of partially eaten or damaged polyps may result in the disappearance of this species fromhydroid colonies.

Cumanotus beaumonti characteristically lay spawn near the distal end ofT. crocea stems, resulting in the ready dis­ persal of veligers at hatching. Thus) the initiation of spawning by this species assures the rapid production and transport of veligers to areas where T. crocea actinulae may eventually become established.

The chemosensory ability of Cumanotus beaumonti is not as pronounced as that of Coryphella trilineata. Ob­ servations suggest this ~pecies can survive about a week without food. Dislodged nudibranchs have a difficult time righting and reattaching to substrates or hydroid stems.

This species also displays a low tenacity relative to other aeolid nudibranchs (Turner, 1978). 86

Of all the predatory nudibranchs investigated in this study, the life span of Cumanotus beaumonti appears to be most intimately dependent upon Tubularia crocea. Death is the likely result of spawning in this nudibranch species.

Cuthona columbiana and C. albocrusta were usually found amidst the basal stolon tangles of Tubularia crocea~ even upon colonies lacking polyps. Both species could sur­ vive for long periods of time in the laboratory, as they fed upon the coenosarc rasped from hydroid stems and stolons. C. columbiana and C. albocrusta have low loco­ motory rates, relative to other aeolid nudibranchs tested by Turner (1978). It is unlikely they move about after becoming established upon a colony ofT. crocea.

During this study, Phidia.na crassicornis fed upon -­

Tubularia crocea and ate Coryphella trilineata and Gmnan­ otus beaumonti as well. This nudibranch may be respons­ ible in part for the disappearance of nudibranchs upon colonies, as it preys upon nudibranchs in addition to T. crocea.

Phidiana crassicornis. is known to eat a wide variety of invertebrate prey (Yarnell, 1972; Harris, 1973;

Birkeland, 1974; McDonald and Nybakken, 1978). This species has been successfully reared in the laboratory upon a diet of tunicates, squid, mussels, and hydroids

(Harrigan and Alkon, 1978). In Elkhorn Slough, this nudi­ branch is encountered year round, and is known to eat the 87

lophophore of Phoronopsis viridis Hilton, 1930 (J. Oliver, pers. comm.; Ronan, 1978).

Although Tenellia ad-?persa was occasionally found upon Tubularia crocea, it is doubtful the persistence of

this species is dependent upon this hydroid. Despite large numbers of I· adspersa collected, spawn of this species was never found attached toT. crocea colonies. The small size of I· adspersa relative to that of T. crocea polyps precludes feeding damage to this hydroid.

The only individuals found to feed upon colonies were ob­ served to eat the tips of regenerating hydranthprimordia.

Of the eight predatory nudibranch species found upon

Tubularia crocea, only Goryphella !rilineata, Phidiana crassicornis, and Tenellia adspersa were observed to feed upon alternate prey species. Field and laboratory obser­ vations confirm that C. trilineata is allied with T. crocea and T. adspersa with Bougainvillia glorietta. It

is unclear if the seasonal occurrence of·P. crassicornis

is dependent upon hydroids at all, due to the broad diet

of this species. In the habitat dominated by tidal currents where

Tubularia crocea occurs, it is hard to imagine that veli­ gers can exercise discriminant settlement upon suitable

substrates. It seems more reasonable that they are

effectively filtered from the water column by the stolon 88 tangles of hydroid colonies. The seasonal occurrence of predatory nudibranch species demonstrated a marked fidelity to that of I· crocea. Although conclusive in­ vestigations have not been conducted, it would seem that successful metamorphosis and survival of predatory species is greater upon T. crocea than other co-occurring hydroid species. Juvenile nudibranchs probably derive protection and food amid T. crocea colonies that enable successful survival to adulthood. Those species of nudibranchs for which embryological data are available show some similarities (Table 6). The time from spawning to hatching is short in species that p~ey upon Ttibularia crocea in Elkhorn Slough, ranging from three to seven days at 15°C. In selected plankto­ trophic species for which data are available, metamorpho­ sis is completed within 72 hours, regardless of tempera­ ture, prey of the adult, or taxonomic affinity (Table 15). Clark (1975) attributed the recruitment of a majority of New England aeolid species to allochthonously trans­ ported larvae. With the possible exception of Coryphella trilineata and Phidiana crassicornis, examination of other hydroid prey species in Moss Landing Harbor and Elkhorn Slough suggests the presence of aeolids upon Tubularia crocea is the result of allochthonous transport. In the case of species such as Cumanotus beaumonti, this could only be facilitated by larval survival of long Table 15. The known duration of metamorphosis and of the free-swimming planktotrophic veliger of selected species of nudibranchs.

FREE-SWIMMING PERIOD SPECIES REFERENCE TEMP.°C METAMORPHOSIS (HRS.) (DAYS) MIN. MAX.

Eubranchus olivaceus Waters 1966 12 24 - 72 2 14+

Cumanotus beaurnonti Hurst 1967 8 - 11 30+

Aeolidiella glauca Hadfield 1963 10 - 12 36+

Phi diana Harrigan and crassicornis Alkon 1978 13 - 15 12 - 24 34+ 58 - 76

Rostanga Chi a and Koss pulchra 1978 10 - 15 24 3 - 4 55 - 60+

Archidoris Allen and pseudoargus Nelson 1911 15 - 17 ? 78+

Doridella Perron and obscura Turner 1977 25 0.8 - 2 9 23

00 1.0 melanobranchia Harris 1975 25 - 27 24 - 48 8 - 10 90 duration in the plankton.

It is known how long nudibranch larvae may persist.

1n the plankton. Sheltema (1971) collected prosobranch larvae of over 200 days calculated age from the tropical

Atlantic Ocean. Mileikovsky (1960) reported opistho­ branch larvae 800km distant from its source. Successful. laboratory experiments to determine the ability of nudi­ branch veligersto postpone metamorphosis are few, and have only been recently conducted (Table 15).

Subannual species of nudibranchs generally possess short and rapidly completed life cycles to take advantage of transitory or short-lived prey (Miller, 1961; 1962;

Thompson, 1964; Clark, 1975). It would seem advantageous for these species to survive the periods of time when their seasonally abundant prey is absent. One possible way would be for their larvae to persist in the plankton for long periods to enable their transport to new areas of abundant prey.

It is reasonable to assert that veligers of hydroid­ eating nudibranchs are capable of planktonic survival as long, if not longer tha~ those species for which the maximum duration of planktonic existence is known. In the case of Cumanotus beaumonti, veligers remain free­ swim~ing for a month or possibly longer (Table 15). The maximum duration of planktonic survival for a subannual 91 species of nudibranch that feeds exclusively on hydroids has yet to be determined. Planktotrophic veligers of

Phidiana crassicornis may remain free-swimming for one to two months, which is comparable to that of the larvae of the dorids Rostang~ pulchra MacFarland, 1905 and Archi­ doris pseudoargus (Rapp. 1837) (Table 15). It is questio;n­ able that hydroid-eating nudibranchs have only short or inflexible life cycles. The preceding examples and the observed plasticity of developmental modes in Tenellia

adspersa point out that much remains to be learned about aeolid nudibranch life histories.

The autumnal decline in hydroid abundance at the

Dairies is coincident with the presence of large numbers of pTedatory nudibranchs. The decline in the abundance of Tubularia crocea, however, cannot solely be attributed to the feeding activities of these predators. The in- fluence of predatory nudibranchs upon the seasonal occurrence of Tubularia crocea at the Dairies is difficult to interpret. In March, 20 individuals representing five predatory species were collected upon fouling panels

(Table 2). Five of 13 Coryphella trilineata ranged from

~.16 - 24mm in length, while the remainder measured less than 15mm. Predation by C. trilineata is most severe at this time of year, due to the considerable number of nudi- branchs and the low abundance ofT. crocea. Additionally, 92

the recruitment of actinula larvae was virtually nil in

subsequent months.

Adult nudibranchs and their spawn were numerous dur­

ing the October peak in hydroid abundance at the Dairies.

Twenty-six nudibranchs of seven predatory species were

documented (Table 2). Half of the Coryphella trilineata '

present were adults of 25 - 45mm length. The deployment

of predation panels from mid-August to mid-October re­

sulted in the occurrence of substantially more individuals

of predatory species (Table 4). Of 93 C. trilineata pre­

sent, over half were adult nudibranchs greater than lSmm

in length. While these individuals could crop large

numbers of T~bularia crocea polyps, hydroid colonies were

numerous and of large size. There was also the continued

noteworthy recruitment of actinula larvae upon panels from

September through November.

The recruitment of 41 individuals of four predatory

. nudibranch species upon November panels resulted in

minimal cropping of Tubularia crocea polyps (Table 2).

The majority of these individuals were juveniles or nudi­

branchs of small size. All 22 of the Coryphella trili­

neata present measured less than 6mm in length. Similar!~

the 63 C. trilineata upon predation panels deployed in

mid-October and retrieved in December measured less than

lOmm crawling length (Table 4). These juveniles probably 93 represent recruitment from spawn laid during the initial infestation of T. crocea in August and September. It is unlikely that the decline in the abundance ofT. crocea at the Dairies is the result of feeding by these numerous, small juvenile nudibranchs.

A small proportion of the hydroid stems on Tubularia crocea colonies were always noted to lack hydranths, even in the months when predatory nudibranchs were absent.

The autotomy of these hydranths was likely governed in part by an endogenous but as yet unidentified mechanism.

The nearly complete absence of hydranths from colonies at the Dairies was observed in October. There is the like­ lihood that predatory nudibranchs could crop the entire canopy of Tubularia crocea. Alternatively, predation by nudibranchs may precipitate increased or epidemic polyp autotomy. The loss of hydranths bearing mature gonophores may serve as a propagational escape response by Tubularia crocea colonies.

An epidemic autotomy response was not induced within a 24 hour period by physically disturbing (i.e., squeezing, pinching) or scissor cl1pping a portion of Tubularia crocea hydranths at the Dairies in mid-November. A detailed in­ vestigation is clearly warranted to determine if epidemic polyp autotomy may be induced by natural physical distur­ bances or by predatory nudibranchs. 94

The loss of hydranths upon Dairies colonies did not result in the disappearance of Tubularia crocea in October or November. Hydroid colonies displayed some measure of regeneration from November to February, no matter the means by which polyps were lost. The decline in hydroid abundance during December at Kirby Park is certainly not the result of feeding by nudi­ branchs upon ].:ubularia crocea. Of three predatory species recruited upon November panels, all 35 individuals were juveniles of 6mm or less (Table 3). With the exception of Phidiana crassicornis of 7 to 17mm length, the 72 nudi­ branchs of three predatory species on December panels were less than 6rnrn length (Table 3). Upon September 'to mid-November predation panels, only three nudibranchs representing three predatory

species were collected at Kirby Park (Table 4), Further­ more, the presence of three predatory Chelidonura inermis (Cooper, 1862) of 12 - 25mm may have further reduced the number of nudibranchs present during these months at Kirby Park. Clearly the feeding activities of predatory nudibranchs upon Tubularia crocea are minimal at Kirby Park. The physical disturbance by artificial predation in excess of that observed to normally occur in the field did not result in the death or subsequent disappearance 95 of Tubularia crocea. The ability of this hydroid to re­ place lost or damaged hydranths is indicative that even severe nudibranch predation results in the cropping of prey, not the extinction of the species.

The regenerative potential of Tuhularia crocea is well documented. At water tem~eratures comnarable to those recorded in October (15 - 18°C) at the Dairies, T. crocea can regenerate mature polyps within eight to 14 days

(Rungger, 1969). During September, colonies at Skipper's

Dock regenerated polyps and liberated actinulae after nine days in 170C waters. The regeneration of polyps by T. crocea is a formidable defense mechanism of colonies. It would seem that the continuous growth of new and regenerat­ ing polyps can compensate for losses to predatory nudi­ branchs. Additionally, the settlement of actinulae of

Tubula~ia crocea upon or near existing colonies may result in aggregated masses that possibly persist for long periods of time.

Nudibranch predation is contributory, but not respons­ ible for the loss and destruction of Tubularia crocea in

Elkhorn Slough. The disappearance of this species can be primarily attributed to the sloughing of colonies in the autumn and winter. Waters of Elkhorn Slough become turbid and tidal exchanges bear increased loads of suspended sedi­ ments and Ehteromorpha sp. that clog the stolon tangles of 96 colonies. Colonies grazed by nudibranchs or that have autotomized their polyps may become more susceptible to being torn loose by tidal currents.

Environmental fluctuations combined with nudibranch predation effectively disrupt the occurrence of Tubularia crocea in Elkhorn Slough in late autumn and again in the spring. McDougall (1943) estimated the age ofT. crocea at Beaufort, North Carolina to be from five weeks to several months. At the same location, Sutherland and

Karlson (1977) concluded that colonies live for five to eight months. Based upon my investigations, the length of life ofT. crocea colonies in Elkhorn Slough probably does not exceed six months.

It is impossible to estimate how long stolons of

T~bularia crocea may remain dormant but alive. Schmid,

Schmid, and.Tardent (1974) have considered the possibility that some hydroids may be somatically immortal. Stolons of Elkhorn Slough colonies were alive upon fouling panels after five months in laboratory aquaria. It is unlikely, however, that an increase in the abundance of this species

is the result of colony r~generation from a stolonal mat.

In many instances the survival of hydroid species has been attributed to the persistence of subtidal populations

(Swennen, 1961; Miller, 1962; Thompson, 1964: Clark, 1971:

Harris, 1973). Colonies of Tubularia crocea may indeed 97 survive in certain subtidal areas that are less influenced by environmental fluctuations or the activities of pre­ dators. In this study the repetitive sampling at sites in Elkhorn Slough for a year confirmed the seasonal occurrence of Tubularia crocea in shallow subtidal coastal waters. SU:MMARY

1. The occurrence of Tubularia crocea, a complex of

tunicate species, and fourteen species of nudibranch

molluscs was documented from March 1977 to February

1978 upon subtidal fouling plates at the Dairies and

Kirby Park in Elkhorn Slough, Monterey County,

California.

2. Tubularia crocea occurred seasonally, with autumnal

and winter peaks in abundance on fouling plates.

Botryllus sp., Botryllus tuberatus (?), Diplosoma

macdonaldi, and an unidentified species of tunicate

displayed annual settlement periodicity.

3. The occurrence of predatory Coryphella cooperi, C.

trilineata, Coryphella sp., Cumanotus beaumonti,

Cuthona albocrusta, C. columbiana and Phidiana crassi-

corni~, Tenallii adspersa was coincident with Tubu-

laria crocea. Coryphella trilineata and Tenellia ad-

spersa also ate Bougainvillia glorietta, although C.

trilineata was allied to T. crocea. T~nellia adspe~sa

was allied to B. Blorietta.

4. Although Tenellia adspersa was the most numerically

abundant species of nudibranch encountered, Coryphella

trilineata was determined to be the major predator

of Tubularia crocea. At low predator densities, adult

98 99

f. trilineata could consume 13 polyps within a 36 hour period. Juveniles ate 1/3 polyp within a 36 hour period.

5. Goryphella triTineata was better able to locate Tubu­

laria crocea colonie.s at a distance than was Cumanotus

beaumonti.

6. Cumanotus beaumonti fed upon Tubularia crocea at a

much slower rate. Three T. crocea were eaten in 36

hours, which was comparable to the minimum feeding rate

of adult Coryphella trilineata.

7. Increased amounts of spawn was laid by Coryphella

trilineata and Cumanotus beaumonti with a reduction in

Tubularia crocea prey.

8. The possible exclusion of Tubularia crocea by tunicate

invasion and overgrowth was not verified by hydranth

predation experiments in the field. Tubularia crocea

colonies subjected to artificial predation displayed

some degree of hydranth regeneration throughout the

year.

9. The autumnal decline of Tubularia crocea in 1977 was

coincident with, but not solely the result of feeding

by predatory nudibranchs. Polyp loss and colony

sloughing was primarily attributed to the combined

effects of temperature and environmental fluctuations

at Kirby Park. At the Dairies, nudibranch predation

further contributed to the decline in abundance of

this hydroid, particularily during March of 1977. LITERATURE CITED

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