Growth Inhibition of Red Abalone (Haliotis Rufescens) Infested with an Endolithic Sponge (Cliona Sp.)

Home , Cliona, Cliona celata, Haliotis, Haliotis rufescens

GROWTH INHIBITION OF RED ABALONE (HALIOTIS RUFESCENS) INFESTED WITH AN ENDOLITHIC SPONGE (CLIONA SP.)

Kirby Gonzalo Morejohn

A Thesis

Presented to

The Faculty of Humboldt State University

In Partial Fulfillment

Of the Requirements for the Degree

Master of Science

In Natural Resources: Biology

May, 2012

GROWTH INHIBITION OF RED ABALONE (HALIOTIS RUFESCENS)

INFESTED WITH AN ENDOLITHIC SPONGE (CLIONA SP.)

HUMBOLDT STATE UNIVERSITY

Kirby Gonzalo Morejohn

We certify that we have read this study and that it conforms to acceptable standards of scholarly presentation and is fully acceptable, in scope and quality, as a thesis for the degree of Master of Science.

______Dr. Sean Craig, Major Professor Date

______Dr. Tim Mulligan, Committee Member Date

______Dr. Frank Shaughnessy, Committee Member Date

______Dr. Laura Rogers-Bennett, Committee Member Date

______Dr. Michael Mesler, Graduate Coordinator Date

______Dr. Jená Burges, Vice Provost Date

ABSTRACT

Understanding the effects of biotic and abiotic pressures on commercially important marine species is crucial to their successful management. The red abalone (Haliotis rufescensis) is a commercially important mollusc, whose shell surface is frequently populated with bright yellow colonies of Cliona sp., an endolithic sponge known to excavate substrates on which it grows. To determine whether a relationship exists between the growth of red abalone and infestation by Cliona sp., divers with the

California Department of Fish and Game surveyed abalone in multiple areas within

Mendocino and Sonoma counties. Individual abalone (n = 786) were scored for shell length and relative shell coverage by Cliona sp. Animals were tagged, released and resurveyed one year later (12±2 mo). Statistical analyses of this previously unpublished data demonstrated a significant, inverse correlation between the growth of red abalone and extent of shell coverage by Cliona sp. Red abalone acquiring even minimal infestation by Cliona sp. showed significantly inhibited shell growth, with the growth of smaller abalone affected to a greater degree than larger animals. Further surveys by this author in 2010 and 2011 were conducted to determine whether differences exist between the frequency and extent of Cliona sp. infestation of red abalone located in Humboldt

County (n =89) versus Mendocino County (n = 106). The frequency of infestation in these counties was not significantly different, but the extent of Cliona sp. infestation was found to be significantly greater in Mendocino County than in Humboldt County. The results strongly suggest that red abalone growth is inhibited by Cliona sp. infestation and

iii

that regions of the northern California abalone fishery are differentially impacted by this infestation.

ACKNOWLEDGEMENTS

I would like to extend special thanks to Dr. Sean Craig for providing me this great opportunity, to Dr. Laura Rogers-Bennett for crucial advice, direction, and enthusiasm, as well as supplying much of the data used, and to thank Dr. Robert Van Kirk for his patience, mastery, and unrelenting guidance through the statistical analyses. I also thank

Dr. Steven Shultz, Dr. John DeMartini and all of the other California Department of Fish and Game divers who for years collected subsurface data. I greatly appreciate discussions with Dr. John DeMartini, who provided insights on specifics of north coast abalone populations. Thanks also to, Andrew Weltz and Sam Parker for their expertise in and under water, as well as in traversing the steep Humboldt cliffs, and Humboldt State

University DSO Rich Alvarez for his training and willingness to make sure this project was done safely. I also thank John Banks for supplying Banks Board surface floats used in data collection. Most of all, I would like to thank my parents, Dr. Brooke S. Kirby and

Dr. Louis C. Morejohn. Their guidance and criticism was invaluable in the creation of this thesis, and because they have surely read it more times than they would have liked, I am dedicating it to them.

TABLE OF CONTENTS

Page

ABSTRACT ...... iii ACKNOWLEDGEMENTS ...... v LIST OF FIGURES ...... vii INTRODUCTION ...... 1 MATERIALS AND METHODS ...... 11 RESULTS ...... 18 DISCUSSION ...... 23 LITERATURE CITED ...... 27 PERSONAL COMMUNICATION ...... 34

LIST OF FIGURES

Figure Page 1 Map Locations of Humboldt County, Mendocino County, and Hardy Creek.. 3

2 Normal Red Abalone Shell with No Apparent Infestation by Cliona sp. . . . . 6

3 Infested Red Abalone Shell Exhibiting Yellow Colonies of Cliona sp...... 7

4 Map of Survey Sites in Humboldt County ...... 14

5 Map of Sampling Sites in Mendocino County ...... 15

6 Growth of Red Abalone Exhibiting an Absence or Gain of Cliona sp. Infestation ...... 20

7 Relationship Between Red Abalone Growth Rate and Infestation by Cliona sp ...... 21

vii

INTRODUCTION

Commercial and recreational fisheries of abalone (Haliotis spp.) once thrived in

southern California, with annual landings surpassing 2,000 metric tons throughout the

1950s and 1960s (Karpov et al. 2000). These fisheries collapsed due to improper

management, disease and sea otter predation, and in 1996 they were subsequently closed

in all areas south of San Francisco Bay (Karpov et al. 2000, Haaker et al. 2001, Micheli

et al. 2008, CDFG Code 5521). Since the implementation of this closure, two of

California’s five targeted abalone species, the white abalone (Haliotis sorensini) and

black abalone (Haliotis cracherodii), have been placed on the endangered species list

(Lundy 1997, Federal Register 66: 103, June 2001, Federal Register 74: 9, January,

2009). In contrast to southern California, the northern California fishery continues to

maintain recreational harvests of the most heavily targeted species, the red abalone

(Haliotis rufescens; Tegner et al. 1992, Karpov et al. 2000).

The continued survival of the northern California fishery is commonly thought to result from longstanding prohibitions against commercial fishing and recreational take by means of SCUBA (Karpov et al. 1998). Recreational fishing has been and remains limited to freediving (breath hold), which limits abalone take to relatively shallow depths and results in deep water abalone refugia. Readily accessible inshore abalone populations are thought to be replenished in part by the spawning and migration of deep water animals into shallower water habitats (Ault and DeMartini 1987, Karpov et al.

1998). This fishery is heavily monitored by annual fishery-independent SCUBA surveys, 2

shore-based creel surveys, mandatory abalone report cards, and telephone surveys

(CDFG: Abalone Recovery and Management Plan). The SCUBA surveys are conducted by the California Department of Fish and Game (CDFG) in multiple areas within Sonoma and Mendocino counties, and while these two counties account for the bulk of

California’s total abalone landings, thousands more are taken from outside of county borders (CDFG: Abalone Report Card Data and Information 2009). In nearly every year during the period 2002-2009, more than 5,000 abalone were taken from Humboldt

County (CDFG: Abalone Report Card Data and Information 2009).

Among the five coastal counties in northern California, Humboldt County has the largest expanse of coastline, with infrequent rocky reefs scattered within large expanses of sandy beaches. Recreational diving in Humboldt County is known for its remoteness and the difficulty of coastal access, with lower abalone densities and poor freediving conditions along with low visibility and strong surf (Friedman and Finley 2003, pers. obs.) A marked change in oceanic conditions occurs approximately 37 km south of the

Mendocino-Humboldt County border, near Hardy Creek (John DeMartini pers. comm.)

(Fig. 1). South of this area the conditions are generally better for diving, with clearer and calmer waters (John DeMartini pers. comm.). Abalone residing south of Hardy

Creek are found at depths of up to 25 m, whereas animals to the north are rarely found deeper than 6 m (Tegner et al. 1992, John DeMartini pers. comm.). The shallow depth- wise distribution in the latter area allows freediver access to virtually all abalone, and deep-water refugia appear to be absent (John DeMartini pers. comm.). The lack of deep- water refugia for the Humboldt County population may make these populations

Figure 1. Map Locations of Humboldt County, Mendocino County, and Hardy Creek.

especially vulnerable, requiring close monitoring to ensure maintenance of healthy populations.

Many marine invertebrates exhibit non-linear growth rates over their life span.

Different size classes of a given species may exhibit very different growth rates, which require the use of non-linear growth modeling (Day and Fleming 1992, Rogers-Bennett et al. 2007). Rogers- Bennett et al. (2007) derived red abalone growth rates from tag- recapture data, estimating years to reach minimum legal size (MLS) to be 12.4±1 y

(Rogers-Bennett et al. 2007).

Protecting larger size classes has been shown in some species to have the greatest positive effects on population growth (Gotelli 1991, Heppell et al. 2006). In a study performed by Rogers-Bennett and Leaf (2006) examining red abalone, the pattern of larger, mature size classes having greater impacts on population growth was apparent.

Abalone from 150-178 mm contribute most to population growth, despite having lower numbers of mature eggs than larger size classes (Rogers-Bennett et al. 2004, Rogers-

Bennett and Leaf 2006). These findings supported the 178 mm MSL measure, and showed that protecting the 150-178 mm size class is most important to maintaining sustainable population levels.

Although red abalone populations are impacted by human take, they are also affected by other organisms. Some marine fauna use abalone as a food source, whereas others live on or within its shell (Wendel 1994, Alvarez-Tinajero et al. 2001). Among the latter organisms are sponges in the family Clionidae, which are known for their

characteristic hole boring through calcareous substrates, such as rocks, coralline algae and shells of molluscs and cirripeds (Hartman 1957, Hansen 1970, Hoeksema 1983).

Clionid excavation of shell and rock is accomplished by specialized archeocytes called etching cells that enzymatically dislodge small chips of substrate that are expelled

through the sponge’s oscula (Hatch 1980, Rupert et al. 2004). The normal shell surface

of red abalone is usually smooth and brick red in color (Fig 2). In clionid-infested

abalone, yellow papillae protrude from small surface holes (Fig. 3), with the bulk of the

sponge biomass residing in a network of subsurface galleries (Rupert et al. 2004). Small

surface holes observed without yellow papillae may be indicative of prior infestation, but

are not considered as an indication of active infestation.

Figure 2. Normal Red Abalone Shell with No Apparent Infestation by Cliona sp. (mm ruler).

Figure 3. Infested Red Abalone Shell Exhibiting Yellow Colonies of Cliona sp. (mm ruler).

Blank page intentional…

Within the family Clionidae, sponges in the genus Cliona cause deleterious effects to some but not all host species (Dunphy and Wells 2001, Stefaniak et al. 2005,

Le Cam and Viard 2011). For example, in slipper shells (Crepidula fornicata) infested with a clionid sponge, neither somatic growth nor female fertility was significantly impacted (Le Cam and Viard 2011). However, such results appear to be an exception to the rule: most host species are negatively impacted by clionid sponge infestation.

In a shell strength experiment by Stefaniak et al. (2005), shells of the common periwinkle (Littorina littorea) without Cliona sp. infestation resisted 40% greater mechanical force than shells with obvious infestation. Similarly, shells of the New

Zealand abalone (Haliotis iris), which were completely penetrated by both clionid sponges and polydorid worms, had significantly decreased resistance to crushing when compared to lesser bored shells (Dunphy and Wells 2001). Crush testing of red abalone shells also revealed a significant inverse correlation between levels of Cliona sp. infestation and strength (Lamarra 2009, unpublished data). Observed reductions in host shell strength have been assumed to increase mortality by facilitating predation and by breakage during human harvest or movement of rocky substrates during periods of high wave activity (Shepherd 1972, Haaker et al. 1986, Stefaniak et al. 2005).

Indirect, negative impacts of boring damage on abalone have also been noted

(Shepherd 1972, Kojima and Imajima 1982, Haaker et al. 1986, Clavier 1992, Stefaniak et al. 2005, Pedrén-Caballero et al. 2010). In an attempt to repair boring damage, an allocation of biosynthetic resources to additional nacre production has been thought to

decrease gastropod growth rate (Haaker et al. 1986, Clavier 1992, Stefaniak et al. 2005).

L. littorea infested with Cliona sp. shows increased nacre production and deposits within

the shell which reduces inner shell volume (Stefaniak et al. 2005). This decrease in shell

volume was correlated with reduced animal tissue mass and was hypothesized to decrease

fecundity.

The sponge Cliona celata is widely distributed throughout the world. On the

California coastline this brilliantly yellow colored sponge has been documented to

colonize red abalone shells (Cox 1962, Hansen 1970). Recent molecular analyses

however, indicate that the species Cliona celata may in fact be composed of multiple

cryptic species (Xavier et al. 2010). For this reason, all clionid sponges in this study will

be referred to as Cliona species.

Unpublished data collected by Shultz and DeMartini showed Cliona sp. to infest

over 35% of the red abalone (n = 1414) at Pedotti Reef in Sonoma County, California.

However, data from the same study showed <1% of the red abalone (n = 703) at Van

Damme Beach, in Mendocino County, California to have active Cliona sp. infestations.

These results indicate variability of Cliona sp. frequencies along California’s north coast.

In a study examining red abalone size and C. celata infestation, Hansen (1970) derived a

shell size index (sum of maximum diameter, minimum diameter and height) and found

that individuals having an index <15 cm were free of C. celata. However, as shell size

index increased above 15 cm, the coverage of shell surface by C. celata increased

exponentially, which is consistent with other studies (e.g. Shepherd 1972, Clavier 1992,

Stefaniak et al. 2005). Previously published estimates of red abalone growth rates,

mortality, and time to MLS have been derived from surveys of animals irrespective of the extent of Cliona sp. infestation (Rogers-Bennett 2007). It has not yet been determined whether red abalone growth is affected by Cliona sp. infestation. Furthermore, no baseline information exists on the extent of Cliona sp. infestation in red abalone populations outside of the heavily studied California counties of Sonoma and Mendocino.

If red abalone growth is negatively influenced by Cliona sp. infestation, current estimates of time to MLS may not be appropriate for managing distinct populations exhibiting higher levels and frequencies of Cliona sp. infestations.

The purpose of this study was i) to examine whether a relationship exists between red abalone shell growth rate and the gain of Cliona sp. infestation ii) to examine whether a relationship exists between red abalone shell growth rate and the extent of Cliona sp. infestation and iii) to compare the frequencies and levels of Cliona sp. infestation on red abalone in Humboldt County and Mendocino County via freediving. Results from these analyses could be used for fisheries management in determination of time to MLS in areas with high frequencies of Cliona sp. infestation. Furthermore, data regarding differences in Cliona sp. frequency and extent of infestation between Humboldt County and Mendocino County could be used to more appropriately manage populations within each of these two counties.

MATERIALS AND METHODS

Measurement of Abalone Growth and Shell Coverage by Cliona sp.

Statistical analyses were performed to examine the potential relationship between

red abalone growth and shell infestation by Cliona sp. Data from a large tag-recapture study of red abalone performed by Shultz & DeMartini (CDFG) were provided by Laura

Rogers-Bennett (CDFG). Data were collected from 1971-1979 by teams of CDFG

SCUBA divers at five sites in Mendocino and Sonoma counties: (1) Cabrillo Reserve

North Cove, (2) Cabrillo Reserve South Cove, (3) Van Damme State Park, (4) Point

Arena, and (5) Fort Ross State Park. Divers collected abalone on random swims and

transported them to a boat for shell measurement and marking by attachment of a

numbered steel tag to respiratory holes with steel wire. During the initial tagging and for

each subsequent recapture, shell length measurements were made. The extent of shell

coverage by Cliona sp. was scored semi-quantitatively by visual means, wherein for each

individual abalone captured, two or more divers independently estimated the extent of

shell coverage, compared their estimates and subsequently agreed to one of four

categories of fractional shell coverage: i) none (0%), ii) low (1-33%), iii) medium (34-

66%) or iv) high (67-100%). Tagged abalone were then returned to a suitable substrate in the general locations in which they were found.

Approximately 6,000 abalone were initially marked, released and relocated for future scoring. However, seasonal variations in growth are known to occur due to

changes in water temperature and food availability (Leighton et al. 1981, Tegner et al.

1992). Thus, to obviate potential impacts of seasonal growth variation, analyses were performed only on data obtained from 786 animals recaptured within 12±2 mo. from their prior collection date. The growth rate value for each individual abalone was normalized to 1 y by dividing each change of length datum by the number of days between its initial scoring and subsequent scoring, and then multiplying by 365. Data for the third, fourth and fifth recaptures were omitted from this analysis due to low sample sizes and lack of statistical independence.

An analysis was performed to determine whether acquisition of Cliona sp. infestation by red abalone is correlated with changes in red abalone growth. This was done by comparing the change in shell length for control animals that did not gain Cliona sp. infestation over the 12 month study period (“Absent,” n = 683) with the change in shell length of infested animals that gained Cliona sp. (“Present,” n = 103) at some point over the same 1 year period. In a subsequent analysis, abalone that gained an infestation of Cliona sp. were divided into three classes that substantially differed in the extent of infestation as follows: low (1-33% coverage, n = 65), medium (34-66% coverage, n = 23) and high (67-100% coverage, n = 15). The three infestation classes (and non-infested control) were compared to determine if acquisition of different levels of Cliona sp. infestation during the 1 year period were correlated with abalone growth. Linear regression models were used in both of these analyses which were performed in Minitab

V16.1.1. Levels of statistical significance were established at p = 0.05. Red abalone growth rate has been shown to decrease with an increase in size (Tegner et al. 1989,

Haaker et al. 1998, Rogers-Bennett et al. 2007). To account for the influence of size on growth rate, initial length was included as a covariate. These data were found to be normally distributed and analyzed without transformation (Snedecor & Cochran 1967).

To derive abalone growth rates and time to reach MLS, the Gaussian model is ideal in accounting for slow growing juveniles (Rogers-Bennett et al. 2007). In this study, juvenile abalone were excluded and only abalone having shell lengths of 58-227 mm were used; the growth rate of abalone in this size range most closely follow the von

Bertalanffy function (Rogers-Bennett et al. 2007). However, the von Bertalanffy function cannot be used to represent negative growth that was exhibited by some larger abalone scored in the present study. This necessitated use of the similar linear regression.

Use of a linear function is appropriate in this case because we do not seek time to reach

MLS, but wish to examine the potential relationship between growth rate of mature abalone and Cliona sp. infestation.

Comparison of Cliona sp. Infestation Frequency and Levels in Humboldt and Mendocino Counties

To study the extent of Cliona sp. infestation of red abalone in Humboldt and

Mendocino counties, abalone were examined during the periods May-August 2010 and

May-August 2011. Three study sites within each of the two counties were chosen for their similarities in: (1) rocky reef substrata, (2) abalone fishing pressure (pers. obs.), and

(3) westward facing beaches. Humboldt County sites included Elk Head (H1), Scotty

Point (H2), and Patrick’s Point (H3) (Fig. 4); Mendocino County sites included Van

Damme (M1), Mendocino Headlands (M2), and Jug Handle (M3) (Figs. 5). GPS

Figure 4. Map of Survey Sites in Humboldt County: Elk Head (H1), Scotty Point (H2), and Patrick’s Point State Park (H3).

Figure 5. Map of Sampling Sites in Mendocino County: Van Damme State Park (M1), Mendocino Headlands (M2), and Jug Handle State Reserve (M3).

coordinates of study sites may be requested from the author, but are not provided herein for protection of these abalone populations.

Initially, two transects (2 m x 30 m) were placed within each of the three study sites in each county. Low densities of abalones were found within Humboldt County, so an additional transect was added to each of the three Humboldt sites. Within each site, transects were parallel to the beach and placed in the center of the area with the highest abalone density. This non-random transect site selection was necessary, specifically within the Humboldt sites, because of the narrow depth range distribution of the abalone bed and relatively low number of animals.

Due to the remoteness of most study sites that often had steep cliff entrances, it was impractical to use SCUBA equipment, so all data were collected via freediving. A surface float attached with a rope to a 2 lb dive weight was used as a visual marker to maintain position along each transect. The dive weight was advanced along the transect as two or more divers took measurements. During surface intervals, this weight was left on the bottom in order to relocate the previous position on the following dive. For each abalone falling within the transect area, Vernier calipers were used to measure shell length. Unlike the CDFG tag-recapture survey described above, data collection for this study was performed without removing abalone from their substrata. Semi-quantitative estimates of Cliona sp. coverage of each abalone shell were made visually by two divers independently and rounded to the nearest 5%. These estimates were then compared and a final estimate of fractional coverage was agreed upon. Active Cliona sp. infestation was

characterized by round ~1-2 mm pits, each filled with a bright yellow papilla (Fig. 3).

Areas of normal shell surface between papillae were included in the Cliona sp. coverage

estimates to account for sponge living in subsurface galleries (Rupert et al. 2004). Areas

of bored shell lacking bright yellow papillae were assumed to be damaged from a

previous Cliona sp. infestation, and were therefore not included.

To compare frequency of Cliona sp. infestation among sites, the statistical

package R was used to perform binary logistic regression. For comparison of Cliona sp.

infestation frequency between counties, Minitab V16.1.1 was used to perform binary

logistic regression. For both of these tests, each abalone was scored “1” or “0”

representing Cliona sp. presence or absence, respectively. For comparisons of the extent

of Cliona sp. infestation between sites and between counties, linear regression was used.

Abalone lacking Cliona sp. infestation (n = 137) were omitted from comparisons of the extent of infestation; only those animals with active Cliona sp. growth (n = 19) were included. Levels of statistical significance were established at p = 0.05.

RESULTS

Positive Correlation of Red Abalone Growth Inhibition and Cliona sp. Infestation

After accounting for influence of length on growth, results from the analysis comparing the growth of abalone that gained Cliona sp. infestation to that of non-infested abalone showed a significant inverse correlation (F1,783 = 13.06, p < 0.001). Abalone that gained infestations were found to have significantly lower growth rates than abalone never observed to have Cliona sp. within the 1 year study period (Fig 6). The differences in growth rates of infested and non-infested animals was significantly affected by initial size, as indicated by a significant interaction term (F1,783 = 7.58, p = 0.006). This is

reflected by the difference in slope of the regression lines (Fig. 6). Growth rates of

smaller abalone were affected by infestation to a greater degree than those of larger

animals. When abalone approach a length of 194 mm, regression lines representing

Cliona sp. presence and absence converge on a growth rate of zero. At this point, shell

length growth apparently stops, and beyond this point shell length actually decreases in

very large animals.

To determine whether abalone shell growth and the extent of Cliona sp.

infestation are related, the growth of abalone that gained no infestation (control) was

compared to that of 3 subgroups of abalone that gained either a low, medium or high

level of infestation in the same 1 y period. The plot given in Fig. 7 shows that abalone

shell growth is inhibited significantly at each level of infestation (F3,779 = 4.36, p =

0.005). The relationship between shell length and differences in growth rates across the

50 C. celata Infestation Absent

40 Present

30 R² = 0.49

10 R² = 0.27

0 50 70 90 110 130 150 170 190 210 230

-10 Shell Growth Rate (mm / year) (mm Rate Growth Shell

-20

-30

-40

-50 Initial Shell Length (mm)

Figure 6. Growth of Red Abalone Exhibiting an Absence or Gain of Cliona sp. Infestation. Non-infested (control) abalone growth (absent, black dots and line); abalone that gained Cliona sp. infestation over the 1-year growth period (present, brown dots and line).

50 C. celata Infestation None Low 40 Medium High

30 R² = 0.49

10 R² = 0.31

R² = 0.03

0 R² = 2E-06 50 70 90 110 130 150 170 190 210 230

-10 Shell Growth Rate (mm / year) (mm Rate Growth Shell

-20

-30

-40

-50 Initial Shell Length (mm)

Figure 7. Relationship Between Red Abalone Growth Rate and Infestation by Cliona sp. Control, non-infested abalone (None, black dots and line); abalone with a low-level infestation (Low, blue dots and line), abalone with a medium-level infestation (Medium, brown dots and line) and abalone with a high-level infestation, (High, red dots and line).

varying levels of Cliona sp. infestation was represented by an interaction term that was

also significant (F3,779 = 4.37, p = 0.005). This term accounted for the differences in

slopes between the four regression lines, as seen in Figure 7. For all categories of Cliona

sp. infestation, growth rates of smaller abalone were affected to a greater degree than

growth rates of larger abalone. Few abalone greater than 200 mm in length were found,

preventing accurate growth rate comparisons of the largest animals.

Survey of Cliona sp. Infestation Frequencies and Levels in Humboldt and Mendocino Counties

Abalone in Humboldt County occurred on substrates that made them much more

cryptic than those in Mendocino County. All Humboldt County abalone were isolated in

cracks and beneath boulders, which complicated animal scoring procedures. Among 103

abalone located within Humboldt County, only 89 were exposed sufficiently for reliable

scoring. In Mendocino County, all were sufficiently exposed for scoring. The highest

densities of abalone in Humboldt County were found in waters of 3-5 m depth. Highest

abalone densities in Mendocino County sites were found in slightly deeper water, ranging

from 5-8 m depth.

The average length of abalone shells from Humboldt County (n = 89) was 2.6 cm

2 larger (χ 1 = 5.80, p < 0.001) than that from Mendocino County (n = 106). Among

Humboldt County abalone, 10 animals had visible shell infestations. Among abalone in

Mendocino County, only 9 individuals showed signs of infestation. Results from binary logistic regression tests show no significant difference between the frequency of Cliona

2 2 sp. infestation between sites (χ 5 = 6.897, p = 0.228) or among counties (χ 1 = 0.413, p =

0.521).

For comparisons of the extent of Cliona sp. infestation between sites and counties,

abalone showing active Cliona sp. infestation were compared. Results from the linear

models showed no significant difference in the extent of Cliona sp. infestation between

sites (F5,14 = 2.60, p = 0.090). A difference in the extent of Cliona sp. infestation

between counties was found however, with significantly higher infestations in

Mendocino County (F1,17 = 11.47, p = 0.004). It should be noted that this significant p- value was obtained by using a sample of only 19 animals, because all abalone lacking

active Cliona sp. infestations were excluded from the analysis.

DISCUSSION

In California, the MLS for red abalone is established at 178 mm, and allows

abalone to reproduce before reaching legally harvestable size (Tegner et al. 1989, Rogers-

Bennett et al. 2004). The current study shows that red abalone growth rate decreases

with increasing levels of Cliona sp. infestation. The majority of the red abalone <194

mm were animals below the MLS, and these showed the largest decreases in growth rate

with Cliona sp. infestation (Figs 6 and 7). In abalone >194 mm, differences in growth

rates were negligible. These findings indicate additional time is necessary for infested

sublegal animals to reach MLS, and suggest that infestation may completely inhibit some abalone from reaching MLS, thereby substantially impacting the fishery.

In a study by Rogers-Bennett and Leaf (2006), the red abalone size class found to contribute most to population growth was the largest sublegal size class (150-178 mm).

My findings show that abalone of this size range gained low, medium and high infestations Cliona sp. If the decreased growth rates seen in Cliona sp. infested abalone are also indicative of decreased reproductive output, abalone smaller than MLS may not be contributing substantially to reproduction in the fishery as assumed, and areas with abalone populations exhibiting high frequencies and levels of Cliona sp. infestation may

be less resilient to high levels of take.

As suggested by Hansen (1970), larger abalone may have a higher extent of C.

celata due to senescence. In other words, as abalone growth rates decline with size, C.

celata is able to ‘catch up,’ and subsequently cover the entire shell. Although we did not

test for potential relationships between the extent of Cliona sp. infestation and abalone

length, both the levels of infestation and rates of colonization increase with abalone size.

For example, only the largest abalone (147-212 mm) gained high infestations, and they did so in one year. The majority of the abalone included in this study were smaller (<147

mm), yet none in that size class gained a high level of Cliona sp. infestation. As shell

size is a function of age, and age is representative of time exposed to potential Cliona sp. infestation, it follows that Cliona sp. frequencies would be higher in larger abalone. This however, does not explain the increased rates of colonization seen in larger abalone and warrants further research.

The convergence of the regression lines representing abalone growth rates under different levels of infestation is puzzling (Fig. 7). It is possible that abalone with both low and no Cliona sp. infestation, and that also show low or negative growth rates, are also hosts for other species of shell-boring parasites. Piddocks, (Penitella conradi) and date mussels, (Lithophaga subula) are two species of endolithic bivalves frequently observed living within red abalone shells (Cox 1962, Hansen 1970). It is conceivable that abalone shell infestations by these bivalves may be metabolically costly to their host and may contribute to decreased growth rates such as those seen with Cliona sp. infestations in this study.

There were differences in Cliona sp. frequency between site and county, and differences in extent of infestation between sites, but the observed differences were not statistically significant. This lack of significance may be attributed to the small sample size, however. Nevertheless, the extent of infestations was found to be higher in

Mendocino County, with the percentage of the shell covered by Cliona sp. being 47%

higher. Unfortunately, this result was obtained with a sample size of only 19 abalone.

While having a larger sample would have been ideal, the low frequencies of Cliona sp.

infestations in field locations make increasing the sample size further a prohibitive and

expensive undertaking. For a study omitting infestation frequencies and only examining

infestation levels, timed swims targeting infested abalone would be a more effective

option to gain larger sample sizes.

With the exception of Van Damme, all sites sampled demonstrated Cliona sp. presence. Van Damme is protected from waves by offshore rocks and islands, has easy ocean access, and therefore has extremely high levels of red abalone take (CDFG:

Abalone Report Card Data and Information 2009). My analyses show the likelihood of

Cliona infestation increases with shell length, consistent with past studies of clionid

infestation in a variety of gastropods (Hansen 1970, Dunphy and Wells 2001, Stefaniak et

al. 2005). Because large abalone are deliberately targeted by recreational abalone divers,

we would expect in areas with high levels of take that average abalone sizes within the

remaining population would be smaller, therefore leading to fewer observations of Cliona

sp. Surprisingly, between Humboldt and Mendocino counties, this pattern did not hold

true.

On average, abalone in Humboldt County were 14% (2.6 cm) larger than those in

Mendocino, but Cliona sp. frequencies were similar. While I believe that this difference

in size between counties is a result of different levels of abalone take, the similar

frequencies of Cliona sp. presence between the larger Humboldt County abalone and the

smaller abalone in Mendocino County remains unexplained.

The endolithic nature of Cliona sp. may have limited the effectiveness of the

visual assay used in this study. Cliona sp. predators have been shown to graze on papillae

which extend beyond the substrata. After grazing, sponge tissue remaining below the

substrata has the ability to regrow papillae within 12 days (Guida 1976). Red abalone

shells with apparently empty Cliona sp. borings may have had active Cliona sp.

infestations lying within subsurface chambers. Visual examination therefore, may have

underestimated the frequency and extent of Cliona sp. infestation. For future studies,

development of an assay more sensitive to Cliona sp. detection would prove helpful.

Determination of the factors that lead to higher frequencies of Cliona sp. infestation and shell colonization rate are important for fisheries managers. While

Humboldt and Mendocino counties were found to have similar frequencies of Cliona sp., the lack of deep-water refugia in Humboldt County is potentially problematic, in that these populations may be less resilient to the same level of fishing found in Mendocino and Sonoma counties. Continued monitoring of the far northern populations in Humboldt

County is imperative to ensure sustainable populations and healthy fisheries for years to come.

LITERATURE CITED

Alvarez-Tinajero, D. C., J. Cacares-Martinez, and J.G. Gonzalez-Aviles. 2001. Shell

boring clams in the blue abalone Haliotis fulgens and the yellow abalone Haliotis

corrugata from Baja California, Mexico. Journal of Shellfish Research 20(2):889-

893.

Ault, J.S. and J.D. DeMartini. 1987. Movement and dispersion of red abalone, Haliotis

rufescens, in northern California. California Fish and Game. 73(4):196-213.

Clavier, J. 1992. Infestation of Haliotis tuberculata shells by Cliona celata and Polydora

species. Pages 16-20 in S. A. Shepherd, M. J. Tegner, and S. A. Guzmán del Próo,

editors. Abalone of the world: biology, fisheries and culture. Blackwell Scientific

Publications, Oxford, UK.

Cox, K. W. 1962. California abalones, family Haliotidae. California Department of Fish

and Game Fish Bulletin 118:1-133.

Day, R. W. and A. E. Flemming. 1992. The determinants and measurement of abalone

growth. Pages 141-168 in S. A. Shepherd, M. J. Tegner, and S. A. Guzmán del

Próo, editors. Abalone of the world: biology, fisheries and culture. Blackwell

Scientific Publications, Oxford, UK.

Dunphy, B. J. and M. G Wells. 2001. Endobiont infestation, shell strength and index in

wild populations of New Zealand abalone, Haliotis iris. Marine Freshwater

Research 52:781-786.

Friedman, C. C. and C. A. Finley. 2003. Anthropogenic introduction of the etiological

agent of withering syndrome into northern California abalone populations via

conservation efforts. Canadian Journal of Fisheries and Aquatic Sciences

60:1424-1431.

Gotelli, N. J. 1991. Demographic models for Leptogorgia virgulata, a shallow-water

gorgonian. Oecologia 104:79-84.

Guida, G. V. 1976. Sponge predation in the oyster reef community as demonstrated with

Cliona celata Grant. Journal of Experimental Marine Biology and Ecology

25(2)109-122.

Haaker, P. L., D. O. Parker, and K. C. Henderson. 1986. Red abalone size data from

Johnsons Lee, Santa Rosa Island, collected from 1978 to 1984. California

Department of Fish and Game, Marine Resources Technical Report 53.

Haaker, P. L., D. O. Parker, K. C. Barsky, and C. Chun. 1998. Growth of red abalone

Haliotis rufescens (Swainson), at Johnsons Lee, Santa Rosa Island, California.

Journal of Shellfish Research 17:747-753.

Haaker, P. L., K. Karpov, L. Rogers-Bennett, I. Taniguchi, C. C. Friedman. and M. J.

Tegner. 2001. Abalone. Pages 89-96 in W. S. Leet, C. M. Dewees, R. Klingbeil

and E. J. Larson, editors. California’s living marine resources: a status report.

California Department of Fish and Game, California.

Hansen, J. C. 1970. Commensal activity as a function of age in two species of California

abalones (Mollusca : Gastropoda). The Veliger 13:90-91.

Hartman, W. D. 1957. Ecological niche differentiation in the boring sponges (Clionidae).

Evolution 1:294-297.

Hartman, W. D. 1958. Natural history of the marine sponges of southern New England.

Peabody Museum of Natural History, Yale University, Bulletin 12:1-155.

Hatch, W. I. 1980. The implication of carbonic anhydrase in the physiological

mechanism of penetration of carbonate substrata by the marine sponge Cliona

celata (Demospongiae). The Biological Bulletin 159:135-147.

Heppell, S. S., C. J. Limpus, D. T. Crouse, N. B. Frazer, and L. B. Crowder. 1996.

Population model analysis for the loggerhead lea turtle, Caretta caretta, in

Queensland. Wildlife Research 23:143–159.

Hoeksema, B. W. 1983. Excavation patterns and spiculae dimensions of the boring

sponge Cliona celata from the SW Netherlands. Senckenbergiana Maritima

15:55-85.

Karpov, K. A., P. L. Haaker, D. Albin, I. K. Tanaguchi., and D. Kushner. 1998. The red

abalone, Haliotis rufescens, in California: importance of depth refuge to abalone

management. Journal of Shellfish Research 17(3)863-870.

Karpov, K. A., P. L. Haaker, I. K. Tanaguchi. and L. Rogers-Bennett. 2000. Serial

depletion and the collapse of the California abalone fishery. Pages 11-24 in A.

Campbell, editor. Workshop on Rebuilding Abalone Stocks in British Columbia.

Canadian Special Publication of Fisheries and Aquatic Sciences 130.

Kojima, H. and M. Imajima. 1982. Burrowing polychaetes in the shells of the abalone

Haliotis diversicolor aquatilus chiefly on the species of Polydora. Bulletin of the

Japanese Society of Scientific Fisheries 48(1):31-35

Lamarra, D. 2009. Commensals influence on the shell strength of the abalone, Haliotis

rufescens. Unpublished student report. On file at the Cadet Hand Library, U.C.

Davis Bodega Marine Laboratory.

Le Cam, S. and F. Viard. 2011. Infestation of the invasive mollusk Crepidula fornicata

by the native shell-borer Cliona celata: high parasite load without detrimental

effects. Biological Invasions 13:1087-1098.

Leighton, D. L., M. J. Byhower, J. C. Kelly, G. N. Hooker, and D. E. Morse. 1981.

Acceleration of development and growth in juvenile green abalone (H. fulgens)

using warmed effluent seawater. Journal of the World Aquaculture Society

12(1):170-80.

Lundy, A. L. 1997. The California Abalone Industry, A Pictorial History. Best

Publishing, Flagstaff, Arizona.

Micheli, F., A. O. Shelton, S. M. Bushinsky, A. L. Chiu, A. J. Haupt, K. W. Heiman, C.

V. Kappel, M. C. Lynch, R. G. Martone, R. B. Dunbar, and J. Watanabe. 2008.

Persistence of depleted abalones in marine reserves of central California.

Biological Conservation 141:1078-1090.

Pedrén-Caballero, R., F. Caballero-Alegría, J. Castro-González, D. Romero-Arce, and E.

Carpizo-Ituarte. 2010. Effects of endolithic boring on the muscle scar and growth

of pink Haliotis corrugata (Gray 1828). Journal of Shellfish Research 29(2):449-

454.

Rogers-Bennett, L., R. F. Dondanville, and J. V. Kashiwada. 2004. Size specific

fecundity of red abalone (Haliotis rufescens): evidence for reproductive

senescence? Journal of Shellfish Research 23(2):553-560.

Rogers-Bennett, L., R. T. Leaf. 2006. Elasticity analyses of size-based red and white

abalone matrix models: management and conservation. Ecological Applications

16(1):213-224.

Rogers-Bennett, L., D. W. Rogers, and S. A. Schultz. 2007. Modeling growth and

mortality of red abalone (Haliotis rufescens) in northern California. Journal of

Shellfish Research 26(3):719-727.

Rupert, E. E., S. F. Fox, and R. D. Barnes. 2004. Invertebrates of the world: A functional

approach, 7th edition. Cengage Learning, Stamford, Connecticut.

Shepherd, S. A. 1972. Studies on southern Australian abalone (Genus Haliotis) I.

Ecology of five sympatric species. Australian Journal of Marine and Freshwater

Research 24:217-257.

Snedecor, G. W. and W. G. Cochran. 1967. Statistical Methods. Sixth edition. The Iowa

State University Press, Ames Iowa.

Stefaniak, L. M., J. McAtee, and M. J. Shulman. 2005. The costs of being bored: effects

of a clionid sponge on the gastropod Littorina littorea (L). Journal of

Experimental Marine Biology and Ecology 327:103-114.

Tegner, M. J., P. A. Breen, and C. E. Lennert. 1989. Population biology of red abalones,

Haliotis rufescens, in southern California and management of the red and pink,

Haliotis corrugata, abalone fisheries. Fishery Bulletin 87(2)313-339.

Tegner, M. J., J. D. DeMartini, and K. A. Karpov. 1992. The California red abalone

fishery: A case study in complexity. Pages 370-383 in S. A. Shepherd, M. J.

Tegner, and S. A. Guzmán del Próo, editors. Abalone of the world: biology,

fisheries and culture. Blackwell Scientific Publications, Oxford, UK.

Wendell, F. 1994. Relationship between sea otter range expansion and red abalone

abundance and size distribution in central California. California Fish and Game

Bulletin 80(2)45-56.

Xavier, J. R., P. G. Rachello-Dolmen, F. Parra-Velandia, C. H. L. Schönberg, J. A. J.

Breeuwer, and R. W. M. van Soest. 2010. Molecular evidence of cryptic

speciation in the “cosmopolitan” excavating sponge Cliona celata (Porifera,

Clionaidae). Molecular Phylogenetics and Evolution 56:13-20

PERSONAL COMMUNICATION

DeMartini, J. D. 2011. Personal Communication. Humboldt State University, 1 Harpst

Street, Arcata, CA 95521