Habitat Ecology of the Native Subtidal Snail, Lacuna Vincta, in the Gulf Of

University of New Hampshire University of New Hampshire Scholars' Repository

Doctoral Dissertations Student Scholarship

Spring 2001 Habitat ecology of the native subtidal snail, Lacuna vincta, in the Gulf of Maine and the impact of two introduced species Suchana Chavanich University of New Hampshire, Durham

Follow this and additional works at: https://scholars.unh.edu/dissertation

Recommended Citation Chavanich, Suchana, "Habitat ecology of the native subtidal snail, Lacuna vincta, in the Gulf of Maine and the impact of two introduced species" (2001). Doctoral Dissertations. 6. https://scholars.unh.edu/dissertation/6

This Dissertation is brought to you for free and open access by the Student Scholarship at University of New Hampshire Scholars' Repository. It has been accepted for inclusion in Doctoral Dissertations by an authorized administrator of University of New Hampshire Scholars' Repository. For more information, please contact [email protected]. INFORMATION TO USERS

This manuscript has been reproduced from the microfilm master. UMI films the text directly from the original or copy submitted. Thus, some thesis and dissertation copies are in typewriter face, while others may be from any type of computer printer.

The quality of this reproduction is dependent upon the quality of the copy subm itted. Broken or indistinct print, colored or poor quality illustrations and photographs, print bleedthrough, substandard margins, and improper alignment can adversely affect reproduction.

In the unlikely event that the author did not send UMI a complete manuscript and there are missing pages, these will be noted. Also, if unauthorized copyright material had to be removed, a note will indicate the deletion.

Oversize materials (e.g., maps, drawings, charts) are reproduced by sectioning the original, beginning at the upper left-hand comer and continuing from left to right in equal sections with small overlaps.

Photographs included in the original manuscript have been reproduced xerographically in this copy. Higher quality 6” x 9” black and white photographic prints are available for any photographs or illustrations appearing in this copy for an additional charge. Contact UMI directly to order.

Bell & Howell Information and Learning 300 North Zeeb Road, Ann Arbor, Ml 48106-1346 USA 800-521-0600

Reproduced with permission of the copyright owner. Further reproduction prohibited without permission. Reproduced with permission of the copyright owner. Further reproduction prohibited without permission. HABITAT ECOLOGY OF THE NATIVE SUBTIDAL SNAIL, LACUNA VINCTA, IN THE GULF OF MAINE AND THE IMPACT OF TWO INTRODUCED SPECIES

Suchana Chavanich B.S. Chulalongkom University, Bangkok, Thailand, 1994 M.A. Central Connecticut State University, 1997

DISSERTATION

Submitted to the University of New Hampshire in Partial Fulfillment of the Requirements for the Degree of

Doctor of Philosophy

Zoology

May, 2001

Reproduced with permission of the copyright owner. Further reproduction prohibited without permission. UMI Number: 3006127

___ ® UMI

UMI Microform 3006127 Copyright 2001 by Bell & Howell Information and Learning Company. All rights reserved. This microform edition is protected against unauthorized copying under Title 17, United States Code.

Bell & Howell Information and Learning Company 300 North Zeeb Road P.O. Box 1346 Ann Arbor, Ml 48106-1346

Reproduced with permission of the copyright owner. Further reproduction prohibited without permission. This dissertation has been examined and approved.

.A . J) hstd ______Dissertation5)irector, Dr. Larry G. Harris Professor of Zoology

Dr. Arthur C. Mathieson, Professor of Plant Biology (Phycology)

Dr. James FT Haney, Professor of Zoolo^

,> r - ^ /'C------Dr. James T. Taylor, Prbfessor of Zo^ogy

Dr. Clayton A. Penniman, Associate Professor of Biology Central Connecticut State University

h r>-^ 'z.opv Date

Reproduced with permission of the copyright owner. Further reproduction prohibited without permission. Acknowledgements

I would like to thank my advisor, Dr. Larry G. Harris for his support,

encouragement, endless patience, understanding, and friendship through this project. He

provided valuable consultation, shared his knowledge of subtidal communities in the Gulf

of Maine, and contributed in many ways to the successful completion of this thesis. He is

not only my advisor but my dive buddy that put up with me throughout my years of

diving in the Gulf of Maine. I deeply appreciate everything he has done for me.

I would also like to thank my committee, Drs. Arthur C. Mathieson, James F.

Haney, James T. Taylor, and Clayton A. Penniman for their useful comments,

encouragement, and friendship through this thesis. The knowledge of algal communities

in the Gulf of Maine was kindly provided by Dr. Arthur Mathieson. I also thank Dr.

Chris D. Neefiis for his advice on statistical analyses.

I am grateful to all the divers who assisted me during my field studies: Christa

Williams, Chad Sisson, Becca Toppin, John Thompson, Nathan Lake, and Megan

Tyrrell. Devin Topp and Heather Sanford are acknowledged for their laboratory

assistance. Jay Gingrich provided his boat for our trips to Isles of Shoals and made me

feel very comfortable while I was diving on his boat.

I also thank Jose Escamilla-Casas for his support, understanding, and

encouragement through my studies. He taught what life was other than studying, stood

beside me, helped me when I was frustrated and confused, and kept me company in a

place that is far from my home. I hope that I can do the same things for him.

iii

Reproduced with permission of the copyright owner. Further reproduction prohibited without permission. I also thank former and current graduate and undergraduate students of UNH: Dr.

Jeff Markert, Dr. Sally Turtle, Dr. Eric Lovely, Petra Bertilsson-Friedman, Monica

Stevens, Chee Yum, Patricia Madigan, Lauralyn Dryer, and Kinsey Frick for their

support and friendship. Barbara Millman, Manya Hult, and Diane Lavalliere helped with

paper works and laboratory instruments, made my life at school easier. I also thank Suroj

and Yuda Chong for their support and friendship.

The present study was supported by grants from a Lemer-Gray Fund for Marine

Research, the Center for Marine Biology of UNH, and the Graduate Research

Enhancement Award of UNH. I also acknowledge the receipt of 1998 and 2000

Graduate School Summer Research Fellowships that provided supports during the

summers as well as Dissertation Fellowship during my final year at UNH.

Finally, I would like to special thank to my loving parents, Surina and Lerseung,

plus my sisters, Sudchanok and Supicha, for their continuous support, advise, and

encouragement through my graduate career. Thank for your endless hours on the phone

making me feel closer to home. Mom and Dad, I would not have been able to

accomplish this goal without your love, support, and belief in me. Thank you...

Reproduced with permission of the copyright owner. Further reproduction prohibited without permission. TABLE OF CONTENTS

ACKNOWLEDGEMENTS ...... iii

LIST OF TABLES ...... vii

LIST OF FIGURES ...... ix

ABSTRACT ...... xii

CHAPTER PAGE

GENERAL INTRODUCTION ...... 1

I. SEASONAL ABUNDANCE OF Lacuna vincta ON DIFFERENT

ALGAL SPECIES ...... 6

Introduction ...... 6

Methods ...... 8

Results ...... 11

Discussion ...... 14

n. FEEDING PREFERENCE OF Lacuna vincta ON DIFFERENT

ALGAL SPECIES ...... 42

Introduction ...... 42

Methods ...... 44

Results ...... 48

Discussion ...... 50

m. GROWTH OF Lacuna vincta FED ON DIFFERENT ALGAL

Reproduced with permission of the copyright owner. Further reproduction prohibited without permission. SPECIES ...... 56

Introduction ...... 56

Methods ...... 58

Results ...... 60

Discussion ...... 62

IV. IMPACT OF Membranipora membranacea ON Laciina vincta

POPULATIONS ...... 71

Introduction ...... 71

Methods ...... 73

Results ...... 78

Discussion ...... 81

V. POTENTIAL IMPACT OF Coclium fragile ssp. tomentosoides ON

Lacuna vincta POPULATIONS ...... 95

Introduction ...... 95

Methods ...... 97

Results ...... 99

Discussion ...... 101

GENERAL CONCLUSION ...... 113

LIST OF REFERENCES ...... 117

Reproduced with permission of the copyright owner. Further reproduction prohibited without permission. LIST OF TABLES

TABLE PAGE

CHAPTER 1 Table 1.1. Abundance of different size classes of Lacuna vincta populations per gram of algal dry weight on nine algal species during April 1998 to March 2000 at -6 m of Cape Neddick, Maine (Size 1 = < 1.1mm, Size 2 = l.l-2.0mm, Size 3 = 2.1-3.0mm, Size 4 = 3.1-4.0mm, Size 5 =4.1-5.0mm, Size 6 = >5.0mm) ...... 35

Table 1.2. Abundance of different size classes of Lacuna vincta populations per gram of algal dry weight on nine algal species during June to July 1999 at -6 m of Star Island, Isles of Shoals, New Hampshire (Size 1 = < 1.1mm, Size 2 = l.l-2.0mm, Size 3 = 2.l-3.0mm, Size 4 = 3.1-4.0mm, Size 5 =4.l-5.0mm, Size 6 = >5.0mm) ...... 41

CHAPTER 2 Table 2.1. Results of one-way ANOVA for differences in the amount algal consumption of snails on eight algal species in choice-ffesh-algal feeding assay, no-choice-fresh-algal feeding assay, choice-dried- algal feeding assay, and no-choice dried-algal feeding assay...... 55

Table 2.2. Results of two-way ANOVA for differences in the amount algal consumption of the snails between two choice assays: fresh and dried algae and eight algal species ...... 55

Table 2.3. Results of two-way ANOVA for differences in the amount algal consumption of the snails between two no-choice assays: fresh and dried algae and eight algal species ...... 55

CHAPTER 3 Table 3.1. Results of one-way ANOVA for differences in the growth rates of snails in each size class: small, medium, and large fed on eight algal species ...... 70

CHAPTER 4 Table 4.1. Results of P-values of Pearson correlation on the relation between the depths of water, % Membranipora membranacea, density, size, and number of egg masses of Lacuna vincta ...... 92

Table 4.2. Results of one-way ANOVA for differences in density and size of the snails in three portions of kelp blades: distal, middle, and proximal ...... 92

vii

Reproduced with permission of the copyright owner. Further reproduction prohibited without permission. Table 4.3. The results of monitoring kelp blades at Cape Neddick from June November 1999 ...... 93

Table 4.4. Results of two-way ANOVA test for differences between times and the growth rate of Lacuna vincta in different treatments ...... 94

Table 4.5. Results of one-way ANOVA for difference in the growth rates of snails in four types of densities of snails...... 94

CHAPTER 5 Table 5.1. Results of two-way ANOVA for differences in the density of snails between two algal species: Codium fragile ssp. tomentosoides and Laminaria saccharina and the two treatments: transplanted and control ...... 112

Table 5.2. Results of two-way ANOVA for differences in the size of snails between two algal species: Codium fragile ssp. tomentosoides and Laminaria saccharina and the two treatments: transplanted and control ...... 112

Table 5.3. Results of one-way ANOVA for differences in the growth of snail in each size class fed on three treatments: Laminaria saccharina , Codium fragile ssp. tomentosoides, and no algae ...... 112

viii

Reproduced with permission of the copyright owner. Further reproduction prohibited without permission. LIST OF FIGURES

FIGURE PAGE

CHAPTER I Figure 1.1. Map of the two study sited: Cape Neddick, Maine and Star Island, Isles of Shoals, New Hampshire ...... 18

Figure 1.2. Average total number oLacuna f vincta plus 1 SE from 115 samples of 23 months of each alga per gram of algal dry weight on nine algal species at Cape Neddick, Maine. Letters above each histogram designate number of snails that differ significantly among algal species (P < 0.05) ...... 19

Figure 1.3. Average total number ofLacuna vincta plus 1 SE from 10 samples of 2 months of each alga per gram of algal dry weight on nine algal species at Star Island, Isles of shoals, New Hampshire. Asterisk represents no algal collection. Letters above each histogram designate number of snails that differ significantly among algal species(P < 0.05) ...... 20

Figure 1.4. Average size ofLacuna vincta plus 1 SE from 115 samples of 23 months of each alga on nine algal species at Cape Neddick, Maine. Letters above each histogram designate size of snails that differ significantly among algal species ...... 21

Figure 1.5. Average size ofLacuna vincta plus I SE from 10 samples of 2 months of each alga on nine algal species at Star Island, Isles of Shoals, New Hampshire. Asterisk represents no algal collection ...... 22

Figure 1.6. Seasonal abundance of the snails per gram of algal dry weight plus 1 SE at Cape Neddick, Maine on four algal species a) Laminaria saccharina b) Ulva lactuca c) Chordaria flagelliformis d) Antithamnionella floccosa. (Note: There is a difference on the scale of y axe of each graph) ...... 23

Figure 1.7. Mean size of the snails per gram of algal dry weight plus 1 SE on four algal species at Cape Neddick, Maine a) Laminaria saccharina b) Ulva lactuca c) Chordaria flagelliformis d) Antithamnionella floccosa. (Note: There is a difference on the scale of y axe of each graph) ...... 26

Figure 1.8. Estimated percent coverage of red, green, and brown algae

Reproduced with permission of the copyright owner. Further reproduction prohibited without permission. on horizontal rocky surfaces of -3 of Cape Neddick, Maine ...... 29

Figure 1.9. Estimated percent coverage of red, green, and brown algae on horizontal rocky surfaces of -7 of Cape Neddick, Maine ...... 30

Figure 1.10. Estimated percent coverage of red, green, and brown algae on horizontal rocky surfaces of -10 of Cape Neddick, Maine ...... 31

Figure 1.11. Estimated percent coverage of algal species on horizontal rocky surfaces plus 1 SE at -3 m of Cape Neddick, Maine...... 32

Figure 1.12. Estimated percent coverage of algal species on horizontal rocky surfaces plus 1 SE at -7 m of Cape Neddick, Maine...... 33

Figure 1.13. Estimated percent coverage of algal species on horizontal rocky surfaces plus 1 SE at -10 m of Cape Neddick, Maine...... 34

CHAPTER 2 Figure 2.1. Estimated grazing byLacuna vincta on eight algal species when fresh algae were offered together (choice assay) and separately (no-choice assay) plus 1 SE. Letters above each histogram designate significant differences in amount of algae eaten by snails (P < 0.05) ...... 53

Figure 2.2. Estimated grazing byLacuna vincta on eight algal species when dried algae were offered together (choice assay) and separately (no-choice assay) plus 1 SE...... 54

CHAPTER 3 Figure 3.1. Growth plus 1 SE ofLacuna vincta (small size class) fed eight algal species for eight weeks ...... 64

Figure 3.2. Growth plus 1 SE ofLacuna vincta (medium size class) fed eight algal species for eight weeks ...... 65

Figure 3.3. Growth plus 1 SE ofLacuna vincta (large size class) fed on eight algal species for eight weeks ...... 66

Figure 3.4. Average weekly growth rate plus 1 SE forLacuna vincta (small size class) fed on eight algal species ...... 67

Figure 3.5. Average weekly growth rate plus 1 SE forLacuna vincta (medium size class) fed on eight algal species ...... 68

Figure 3.6. Average weekly growth rate plus 1 SE forLacuna vincta (large size class) fed on eight algal species ...... 69

Reproduced with permission of the copyright owner. Further reproduction prohibited without permission. CHAPTER 4 Figure 4.1. The percent cover ofMembranipora membranacea (a), average density per available gram of algal dry weight (b), average size (c), and average number of egg masses (d) ofLacuna vincta on Laminaria spp. plus 1 SE at different depths of water ...... 85

Figure 4.2. Density plus 1 SE ofLacuna vincta on different portions of kelp blades ...... 87

Figure 4.3. Size plus 1 SE ofLacuna vincta on different portions of kelp blades ...... 88

Figure 4.4. The growth plus I SE of Lacuna vincta fed on Laminaria saccharina with and without Membranipora membranacea ...... 89

Figure 4.5. The results of the experiment on breakage areas of kelp fronds ...... 90

Figure 4.6. The results showed growth plus 1 SE of Lacuna vincta in different densities fed on limited areas of kelp blades ...... 91

CHAPTER 5 Figure 5.1. Density ofLacuna vincta per gram o f algal dry weight (a) and mean length of Lacuna vincta (b) plus 1 SE on control and transplanted Laminaria saccharina and control and transplanted Codium fragile ssp. tomentosoides at Cape Neddick and Star Island ...... 106

Figure 5.2. Size distribution of Lacuna vincta on each of control and transplanted of each Laminaria saccharina and Codium fragile ssp. tomentosoides at Cape Neddick and Star Island ...... 108

Figure 5.3. Average shell height plus 1 SE of Lacuna vincta in three size classes: a) -1.0 mm b) -2.5 mm c) - 3.5 mm fed on Laminaria saccharina and Codium fragile ssp. tomentosoides for 8 weeks ...... 109

Figure 5.4. Average growth rate per week plus 1 SE of Lacuna vincta in three size classes fed on Laminaria saccharina and Codium fragile ssp. tomentosoides ...... I l l

Reproduced with permission of the copyright owner. Further reproduction prohibited without permission. ABSTRACT

HABITAT ECOLOGY OF THE NATIVE SUBTIDAL SNAIL, LACUNA VINCTA, IN THE GULF OF MAINE AND THE IMPACT OF TWO INTRODUCED SPECIES

Suchana Chavanich University of New Hampshire, May, 2001

Lacuna vincta (Montagu) is a small native herbivorous gastropod that feeds and

lives on algae within the rocky subtidal zone of New England. In this study, a

combination of field samplings and laboratory experiments were conducted in order to

examine the seasonal abundance, feeding preference, and growth of snails on nine

different algal species. The results showed that there were differences in the seasonal

abundance patterns of L. vincta populations on different algal species. However, the

snail populations in all size classes were found year round onLaminaria saccharina (L.)

Lamour. Feeding preference experiments showed that L. vincta preferred

Antithamnionella floccosa (O. F. Mull.) Whittick, Ulva lactuca L., and Laminaria

saccharina. However, the growth experiments demonstrated that growth rates of snails

fed on L. saccharina tended to be higher than those fed on other algae.

Because of the introduction of non-indigenous species, several introduced taxa

have become established within subtidal ecosystems of the Gulf of Maine. The impact of

the introduced bryozoan,Membranipora membranacea (L.), and the green alga, Codium

fragile (Sur.) Hariot subsp. tomentosoides (van Goor) Silva, on Lacuna vincta was

investigated. Results from field samplings, reciprocal transplantations, and laboratory

xii

Reproduced with permission of the copyright owner. Further reproduction prohibited without permission. experiments suggest that these two introduced species have an apparent negative impact

on L. vincta. The preferred habitat and food of snails in the kelp canopy was reduced by

bryozoan coverage and/or replacement of kelp byC. fragile ssp. tomentosoides. The

overgrowth of M. membranacea on kelp blades decreases the available grazing spaces

and affects the growth of L. vincta. The coexistence of these two species in the same

habitat has created intraspecific and interspecific competition for this resource. In

addition, changing algal composition from a kelp-dominated canopy {Laminaria

saccharina) to one dominated by C. fragile ssp. tomentosoides also had a negative impact

on this snail. Field sampling showed that the density of L. vincta at sites dominated by C.

fragile ssp. tomentosoides was less than half that of sites dominated by L. saccharina.

The parallel success C. fragile ssp. tomentosoides and M. membranacea, may lead to an

even higher negative impact on L. vincta populations.

xiii

Reproduced with permission of the copyright owner. Further reproduction prohibited without permission. GENERAL INTRODUCTION

Algae are recognized for their contributions to marine communities, as they serve

as sources of food, shelter, and refuges from predation for herbivores (Southgate, 1982;

McBane and Croker, 1983; D’Antonio, 1985; Hicks, 1986; Buschmann, 1990; Duffy and

Hay, 1991). Macroalgae also play an important role in the survival of many marine

juvenile organisms (Leber, 1985; Maney and Ebersole, 1990; Wilsonet ai, 1990).

Habitat selection by herbivores is influenced by several factors, including food

preference, habitat structure, chemical defenses, predation, and competition (Heck and

Wetstone, 1977; Hacker and Steneck, 1990; Hayet al., 1990; Jensen and Kristensen,

1990; Duffy and Hay, 1991). For example, Duffy and Hay (1991) showed that the

abundance of the marine amphipod Amphithoe longimana (Smith) on different species of

algae was related to the preference of omnivorous fishes for these algae rather than to the

feeding rates on the amphipods.

On rocky shores, molluscan grazers are considered to be one of the most abundant

herbivores (Little and BCitching, 1996). Because they feed and live on the algae, the

relationship between grazers and algae tend to be closely linked. Several papers have

also reported that herbivores play an important role in regulating the distribution of algae

in the community (Lubchenco, 1978; Sousa, 1979; Lubchenco, 1983). Lubchenco (1978)

showed that when Littorina littorea (L.) was added to tidal pools covered by

Enteromorpha intestinalis (L.) Link, it removed this algal species leading to an increase

Reproduced with permission of the copyright owner. Further reproduction prohibited without permission. of Chondms crispus Stackh. However, when L. littorea was removed from the pool,

Enteromorpha was dominant.

Lacuna vincta (Montagu) is a small herbivorous gastropod that feeds and lives on

algae in the rocky subtidal zone. Lacuna vincta is an important food source for numerous

animals, and their annual production can be high enough to support significant

populations o f fish, crabs, and other predators (Menge, 1972; Nelson, 1981). It can be

found on a variety of algal species (Shacklock and Croft, 1981; Southgate, 1982; Thomas

and Page, 1983); however, most studies emphasize the abundance of L. vincta associated

with kelp habitat (Thomas and Page, 1983; Johnson and Mann, 1986; Maney and

Ebersole, 1990; Martel and Chai, 1991). Lacuna vincta has the ability to drift in the

water column by secreting a mucous thread, which allows it to relocate and increase

habitat selection (Martel and Chai, 1991). Even though, L. vincta can be found on a

variety of algae, all species may not be edible or attract grazers. At present, little is

known about the L. vincta - algal associations in the subtidal zone of New England. To

gain a better understanding of the role of this herbivorous snail, I assessed seasonal

abundance, food preferences, and growth rates of snails. I also made detailed

descriptions of the algal communities where L. vincta was found.

At present, the introduction of non-indigenous species into the coastal waters in

the United States poses a serious environmental and economic threat (Carlton, 1996;

Kuris and Culver, 1999; Grosholzet al., 2000). Only recently have ecologists realized

the pervasiveness of introduced species within marine habitats (Berman et al., 1992;

Lambert et al., 1992; Carlton, 1996; Kuris and Culver, 1999; Parkeret al., 1999;

Grosholz et al., 2000; Wortham et al., 2000). Many disastrous invasions by non-

Reproduced with permission of the copyright owner. Further reproduction prohibited without permission. indigenous species have resulted in the loss of native species, changes in community

structure and function, and alterations of the physical structure of the system (Lambertet

al., 1992; Parker et al., 1999; Stohlgren et al., 1999; Ceccherelli et al., 2000; Grosholz et

al.. 2000). Most invasive marine species in North America have originated from distant

waters, with the introduction having occurred either intentionally for aquaculture

purposes or non-intentionally by ballast tanks or the hulls of the ships (Carlton, 1996).

Several introduced species have become established in the subtidal ecosystems in

the Gulf of Maine, for example the bryozoan Membranipora membranacea (L.), the

tunicates Stye la plicata (Lesueur), Diplosoma listerianum (Milne Edwards), and

Botrylloides violaceus (Oka), the green alga Codium fragile (Sur.) Hariot subsp.

tomentosoides (van Goor) Silva, and the red alga Bonnemaisonia hamifera Hariot

(Fralick and Mathieson, 1973; Carlton and Scanlon, 1985; Prince, 1988; Berman et al.,

1992; Lambert et al., 1992; Harris and Mathieson, 2000; Harris and Tyrrell, 2001). The

impact of the introduced bryozoan Membranipora membranacea and the green alga

Codium fragile ssp. tomentosoides, upon a native kelp herbivore, Lacuna vincta, was the

primary focus of my study.

Membranipora membranacea was first observed in the Gulf of Maine during

1987 (Lambert, 1990; Berman et al., 1992; Lambert et al., 1992), being thought to be

introduced from either Europe or the Pacific coast (Ryland, 1970; Yoshioka, 1982;

Berman et al., 1992). The introduced bryozoan has a planktonic larva and benthic adult

in the life stages (Ryland, 1970; Yoshioka, 1982). Adult populations ofM. membranacea

are primarily found on laminarian and fucoid algae (Eblinget al., 1948; Sloane et al.,

1957; Ryland, 1970). In the Gulf of Maine,M. membranacea is mostly found on

Reproduced with permission of the copyright owner. Further reproduction prohibited without permission. Laminaria spp. during the fall and winter (Berman et al., 1992). However, it can also

occur on other algae, such as Agarum clathratum Dumort and Desmarestia acnleata (L.)

Lamour. (Harris and Mathieson, 2000). The overgrowth of kelp blades by the bryozoan

is reported to have a negative impact as it inhibits photosynthesis (Lambert et al., 1992).

Overgrown kelps appear to be susceptible to a decrease in structural integrity of the blade

(Lambert et al., 1992; Harris and Tyrrell, 2001), which may also affect other marine

organisms such as Lacuna vincta that utilize kelp as a food source and habitat (Lambert

etal., 1992).

Codium fragile ssp. tomentosoides, which is originally from Asia, was introduced

from western Europe to Long Island Sound in 1957 (Carlton and Scanlon, 1985).

Codium fragile ssp. tomentosoides was first observed at the Isles of Shoals in 1982

(Harris and Mathieson 2000). The alga now forms dense beds in areas previously

overgrazed by sea urchins (Prince, 1988; Prince and LeB lance, 1992; Harris and

Mathieson, 2000; Harris and Tyrrell, 2001). The sea slugsPlacida dendritica (Alder and

Hancock) and Elysia rnaoria (Powell) are specialist herbivores on C. fragile ssp.

tomentosoides in New Zealand (Trowbridge, 1995). Other herbivores, such as sea

urchins and snails, can also graze upon C. fragile ssp. tomentosoides, but it is not a

preferred food and does not attract these herbivores (Prince and LeBlance, 1992). During

the 1970’s to 1980’s Laminaria spp. were abundant within the shallow subtidal of the

Isles of Shoals (Fig. 1.1); however, C. fragile ssp. tomentosoides is now the dominant

canopy species (Harris and Tyrrell, 2001). Changing of algal composition may affect

organisms, such as Lacuna vincta that utilize kelp beds as a habitat and food source.

Codium fragile ssp. tomentosoides is now found in coastal zone areas such as Cape

Reproduced with permission of the copyright owner. Further reproduction prohibited without permission. Neddick, Maine; however, it is not the dominant species in this nearshore open coastal

site yet (Harris and Mathieson, 2000; Harris and Tyrrell, 2001). IfC. fragile ssp.

tomentosoides continues to spread in other nearshore subtidal communities as at the Isles

of Shoals, they may be changed significantly. The impact of C. fragile ssp.

tomentosoides on L. vincta population was investigated in the present study.

The purpose of my study was to evaluate the habitat ecologyLacuna of vincta in

relation to different algal species. In addition, I have evaluated the potential impact of

two introduced species, the bryozoan, Membranipora membranacea, and the green alga

Codium fragile ssp. tomentosoides on L. vincta populations. Presently little is known

regarding the relationship between L. vincta and several introduced species in the Gulf of

Maine.

Reproduced with permission of the copyright owner. Further reproduction prohibited without permission. CHAPTER 1

SEASONAL ABUNDANCE OF LACUNA VINCTA

ON DIFFERENT ALGAL SPECIES

Introduction

Lacuna vincta is a small herbivorous snail that feeds/lives on algae within the

rocky subtidal zone. Lacuna vincta is normally found on kelp (Martel and Chai, 1991),

but several papers have reported that L. vincta can be found on other algae such as Fuats

distichus L. subsp. edentatus (Pyl.) Powell,Chondrus crispus Stackh., Fucus serratus L.,

Mastocarpus stellatus (Stackh.) Guiry, andLaurencia pinnatifida (Huds.) Lamour. in the

northeast and northwest Atlantic (Shacklock and Croft, 1981; Southgate, 1982; Thomas

and Page, 1983). Most studies have emphasized that L. vincta is associated with kelp

(Thomas and Page, 1983; Johnson and Mann, 1986; Maney and Ebersole, 1990).

The life history and spawning period of Lacuna vincta have been intensively

studied, but the timing of spawning is described differently in several papers: January-

March (Southgate; 1982), January-June (Smith, 1973), January-October (Rasmussen,

1973), March-June (Russel-Hunter and McMahon, 1975), June-August (Thomas and

Page, 1983), and year-round (Maney and Ebersole, 1990). In the Gulf of Maine,L.

vincta reproduces year-round, and veligers occur almost every month (Maney and

Ebersole, 1990). In addition, egg masses of L. vincta can be found on a variety of algae,

Reproduced with permission of the copyright owner. Further reproduction prohibited without permission. which are also used as their nursery habitats (Southgate, 1982). Lacuna vincta selects

habitats for spawning by secreting a mucous thread and drifting in the water column

(Martel and Chai, 1991).

Even though Lacuna vincta is normally found on a variety of algae, most studies

have evaluated its seasonal abundance within kelp habitats (Thomas and Page, 1983;

Johnson and Mann, 1986; Maney and Ebersole, 1990; Martel and Chai, 1991). The

primary objective of my study was to increase our understanding of the seasonal

abundance of L. vincta on nine common seaweeds in the Gulf of Maine. Even though L.

vincta are found on a variety of algae, the relative abundance of snail populations may

vary between different algal species, depending on the snail’s preference.

In addition, the algal community associated withLacuna vincta populations was

investigated. BecauseL. vincta feeds and lives on algae, the relationship between the

grazers and algae tend to be very closely linked. Therefore, the habitat and food selection

of the snails may be related to the differential abundance of algae in the community.

Field sampling was conducted in order to evaluate the algal abundance at Cape Neddick,

Maine.

Reproduced with permission of the copyright owner. Further reproduction prohibited without permission. Methods

Field Sampling

Study Sites and Sampling Locations

Samples of Lacuna vincta were collected from two study sites (Fig. 1.1): Cape

Neddick, York, Maine (43° 10' N, 70° 36' W) and Star Island, Isles of Shoals, New

Hampshire (42° 58' N, 70° 37' W) using SCUBA techniques. The two sites are

moderately exposed, with Cape Neddick being primarily exposed to swells and storms

out of the northeast. Laminaria saccharina is the dominant canopy species at Cape

Neddick while Codium fragile ssp. tomentosoides is the dominant canopy species at Star

Island.

Sampling Methods and Schedules

1. Seasonal Abundance of Lacuna vincta on Different Seaweeds

The seasonal abundance of Lacuna vincta populations on different seaweeds was

investigated at two study sites in the Gulf of Maine: Cape Neddick, Maine, and Star

Island, Isles of Shoals, New Hampshire (Fig. 1.1).

At Cape Neddick, Maine, monthly field samplings of Lacuna vincta were

conducted between April 1998 to March 2000 in order to examine the seasonal

abundance and population dynamics ofL. vincta on nine algal species: Laminaria

saccharina (L.) Lamour., Ulva lactuca L., Desmarestia acideata (L.) Lamour., D. viridis

(O. F. Mull.) Lamour., Chordaria flagelliformis (O. F. Mull.) C. Ag., Chondrus crispus

Stackh., Antithamnionella floccosa (O. F. Mull.) Whittick, Bonnemaisonia hamifera

Hariot, and Codium fragile (Sur.) Hariot subsp. tomentosoides (van Goor) Silva. ForB.

Reproduced with permission of the copyright owner. Further reproduction prohibited without permission. hcimifera, the samples were collected from April 1999-March 2000. Cape Neddick has

diverse algal assemblages, with Laminaria saccharina being the dominant species. Most

of the nine species occur year round; except for C.flagelliformis, D. viridis and A.

floccosa (Mathieson and Hehre, 1986; Villalard-Bohnsack, 1995; personal observations).

The density of the introduced green alga, C.fragile ssp. tomentosoides at Cape Neddick

is very low; approximately 0.1 plant/m2 (Harris pers. obser.), so it was not collected every

month in order to preserve the population. Codium plants were observed to document

whether L. vincta was present on them or not. If snails were present, the Codium plants

were collected. Samples of the snails were collected monthly in the rocky subtidal zone

at Cape Neddick, except during January 1999 due to extreme storms.

At Star Island, Isles of Shoals, samples of snails on eight algal species were

collected during June and July 1999:Ulva lactuca, Desmarestia aculeata, D. viridis,

Chordaria flagelliformis, Chondrus crispus, Antithamnionella floccosa, Bonnemaisonia

hamifera, and Codium fragile ssp. tomentosoides. Codium fragile ssp. tomentosoides is

the dominant canopy species at this site. Due to its very low density at this study site,

Laminaria saccharina was not collected.

Five replicate samples of each algal species were collected monthly at

approximately -6 m below mean low water at both two study sites using SCUBA

techniques. The plants were initially covered with plastic bags, and then removed from

the substratum. The bags were tied shut and returned to the University of New

Hampshire within 1 hour for later analysis. The snails were sorted, counted, and

measured. After being measured, the snails were placed into six shell-height categories:

< 1.1 mm, 1.1-2.0 mm, 2.1-3.0 mm, 3.1-4.0 mm, 4.1-5.0 mm, and >5.0 mm. The

Reproduced with permission of the copyright owner. Further reproduction prohibited without permission. presence of egg masses was also noted. The algal samples were oven dried at 75°C to a

constant weight (about 12 hours). Algal biomass (dry weight) was then measured. Snail

morphological parameters were then analyzed and compared after being adjusted for one

gram of each algal species. A one-way ANOVA followed by Tukey pairwise mean

comparison was used to examine the differences in total number and size of snails on

different algae. Tests were done using Systat 7.0 (Systat, 1997).

2. Description of the Algal Community Associated withLacuna vincta Populations

An analysis of algal community structure was conducted during November 1999

at Cape Neddick, Maine. Photographic records were used to estimate the densities of

canopy species and percent coverage of understory species in the area. A Nikon V

underwater camera with 15 mm lens and electronic flash was used. Ten replicate

photographs were taken of three depths of water: -3, -7, and —10 m. The pictures were

taken on horizontal rocky surfaces along a measurement tape at approximately 5 m

intervals in each depth. Each photo quadrat was about 0.1 m2 area. Percent coverage of

algae was quantified by projecting the images onto a grid and counting the presence of

algae under 100 dots.

Reproduced with permission of the copyright owner. Further reproduction prohibited without permission. Results

Field sampling

1. Seasonal Abundance of Lacuna vincta on Different Algal Species

The abundance of Lacuna vincta populations was different on each algal species

at the two study sites (Tables 1.1-1.2, Figs. 1.2-1.3). In addition, there were seasonal

changes in abundance and size of the snail populations on each algal species (Table 1.1-

1.2; Figs 1.6-1.7). The data from Figure 1.2 showed that at Cape Neddick, the average

total number of L. vincta was highest on Ulva lactuca, Chordaria flagelliformis,

Antithamnionella floccosa, and Laminaria saccharina. At Star Island, the highest

average number of snails was on C.flagelliformis , followed by Bonnemaisonia hamifera

and U. lactuca (Fig. 1.3). At Cape Neddick, the largest of L. vincta were found on L.

saccharina while the smallest were on A. floccosa (Fig. 1.4). By contrast, at Star Island,

the largest of L. vincta were on U. lactuca and B. hamifera and the smallest of L. vincta

were found onDesmarestia acideata and A. floccosa (Fig. 1.5).

Seasonal changes in the numbers of Lacuna vincta on four algal species at Cape

Neddick are shown in Figure 1.6. The seasonal changes of L. vincta on Chondrus

crispus, Desmarestia aculeata, D. viridis, Codium fragile ssp. tomentosoides, and

Bonnemaisonia hamifera are not included in the graph due to their low variability, but the

numbers are shown in Table 1.1 and Table 1.2.

Seasonal changes in the population density of Lacuna vincta on Laminaria

saccharina and Ulva lactuca were similar (Fig. 1.6a-b). On L. saccharina and U.

lactuca, the highest densities occurred during October-November 1998 and October

Reproduced with permission of the copyright owner. Further reproduction prohibited without permission. 1999-January 2000 (Fig. 1.6a-b). The lowest densities of the snails on L. saccharina and

U. lactuca occurred during April-May of each year (Fig. 1.6a-b). By contrast, the highest

densities of the snails on Chordaria flagelliformis and Antithamnionella floccosa

occurred during January - February each year, and the densities of the snails decreased

dramatically in following month (Fig. 1.6c-d).

The seasonal size of Lacuna vincta populations on four algal species varied from

month to month, depending on the algal species: Laminaria saccharina (0.7 mm to 4.0

mm), Ulva lactuca (0.8 mm to 3.3 mm), Chordaria flagelliformis (0.6 mm to 2.5 mm),

and Antithamnionella floccosa (0.9 mm to 2.3 mm) (Fig 1.7a-d). The largest of snails

were found in April and May onU. lactuca and L. saccharina (Fig. 1.7 a-b). The

smallest of snails on L. saccharina occurred in February, July and August, while the

smallest occurred on U. lactuca in June, November, and December (Fig. 1.7a-b). On C.

flagelliformis and A. floccosa, there was no distinguishable pattern for size of snail

throughout the year (Fig 1.7c-d). However, the smallest average size was found in

January and February (Fig. 1.7c-d).

2. Description of the Algal Community Associated withLacuna vincta Populations

The results showed differences in assemblages at the three depths (-3, -7, and -10

m). At the shallowest depth (-3 m), the algal composition (as percent cover) was 18.3%

red algae, 4.8% green algae, and 1.4% brown algae (Fig. 1.8), and more than 70% of the

remaining area being covered with a matrix of small Mytilus edulis and amphipod tubes

(Fig. 1.8). At the same depth, ephemeral red algae occupied 11.8% cover, while other

algae (Chondrus crispus, Ulva lactuca, Corallina officinalis, Laminaria spp. and crustose

corallines) composed < 5 % each (Fig. l.l 1).

Reproduced with permission of the copyright owner. Further reproduction prohibited without permission. At -7 m (Fig. 1.9), there was also a large coverage of the Mytilus and amphipod

tube matrices (73.9%). Brown algae covered 3.3% of the surface, while red algae

occupied 22.8% (Fig. 1.9). No green algae were found at this depth. Most of the red

algae were crustose corallines (14.7%), followed byChondnis (3.1%), and ephemeral

reds, such as Polysiphonia harveyi Bailey (5.0%) (Fig. 1.12). Laminaria saccharina was

the only brown algal species recorded at this depth (Fig. 1.12).

At -10 m, Mytilus and amphipod tubes covered 79.1% (Fig. 1.10). Brown algae

and red algae occupied 5.8% and 15.1% respectively (Fig. 1.10). No green algae were

found at -10 m. Chondnis (4.2%), Corallina (0.3%), and crustose corallines (10.6%)

comprised the red algae, while Laminaria (4.1%) comprised the brown algae (Figure

1.13).

Reproduced with permission of the copyright owner. Further reproduction prohibited without permission. Discussion

The present study describes seasonal differences ofLacuna vincta populations on

different algal species. Seasonal patterns of abundance of L. vincta were similar on

Laminaria saccharina and Ulva lactuca, as well as on Antithamnionella floccosa and

Chordaria flagelliformis (Fig. 1.6). The recruitment of snails (Size 1 = < 1.1 mm) also

seems to vary between algal species (Table 1.1). The highest density of the snails on L.

saccharina and U. lactuca occurred during October and November (Fig. 1.6a-b), with the

largest number of individuals in most size classes, especially the small size class,

occurring during this period (Table 1.1). However, on C. flagelliformis and A. floccosa,

the highest density and the number of small snails occurred during January and February

(Fig. 1.6c-d; Table 1.1).

Maney and Ebersole (1990) suggest that Lacuna vincta has a year-round

reproduction on Laminaria spp. within the Gulf of Maine, with veligers occurring almost

every month. I also found the smallest size class of snails almost every month on

common algal species; however, the highest snail recruitment occurred during the late of

fall and winter (Table 1.1). Johnson and Mann (1986) showed that cunner,

Tautogolabrus adspersus (Walbaum), prefers to feed on large Lacuna vincta, with half of

its gut contents consisting ofL. vincta. Cunners are normally present at Cape Neddick

from May through October (Harris pers. comm.; pers. obser.). As shown in Table 1.1,

the large size classes of L. vincta were rarely found on algae during the summer. Fish

predation could lead to reduced recruitment and densities of snails during the summer

versus the fall and the winter.

Reproduced with permission of the copyright owner. Further reproduction prohibited without permission. The average size of snails on Laminaria saccharina, Ulva lactuca, Chordaria

flagelliformis, and Antithamnionella floccosa varied seasonally (Fig. 1.7a-d). However,

all size classes of the snails tended to occur on L. saccharina and U. lactuca either year-

round or almost year-round, while most of the snails onC. flagelliformis and A. floccosa

were less than 2.5 mm (Fig. 1.7, Table 1.1).

Habitat selection by herbivores is influenced by several factors including their

food source, the abundance of the algae in the community, physical structure, chemical

defense of seaweeds, predation, and competition (Heck and Wetstone, 1977; Hacker and

Steneck, 1990; Hayet al., 1990; Jensen and Kristensen, 1990; Duffy and Hay, 1991;

Trowbridge, 1995). The food value of plants can also determine plant utilization patterns

of herbivores (Hay et al., 1989). Johnson and Mann (1986) suggested that Laminaria

spp. had a higher nutritional quality than other algal foods. The results from Chapter 3

also show that the growth rates of Lacuna vincta fed on Laminaria saccharina were

higher than those fed on other algal species. Because L. vincta has the ability to drift in

the water column by secreting a mucous thread, it is able to relocate and increase habitat

selection (Martel and Chai, 1991). My results showed that even though the small cohorts

of L. vincta can be found on a variety of algal species, the larger ones tended to

concentrate on certain species such as Laminaria saccharina.

Egg masses of Lacuna vincta were observed in each month. However, their

numbers were high in the summer and were found on a variety of algal species. By

contrast, during the spring and fall, egg masses were found primarily onLaminaria

saccharina (pers. obser.).

Reproduced with permission of the copyright owner. Further reproduction prohibited without permission. The results of my field sampling suggest that there were differences in algal

composition at the evaluated depths. For example, at -3 m, brown, green, and red algae

were present, while at -7 and -10 m, only brown and red algae occurred (Figs. 1.8-1.10).

However, all the depths had a large coverage of Mytilus edulis and amphipod tube

matrices (more than 70% at each depth). Harris (pers. comm.) suggested that small

Mytilus, plus amphipods and amphipods tubes can be found during the fall. Sousa (1979)

and colleagues (1981) suggested that storms and seasonal defoliation of algae create the

space for recruitment of other organisms in the low intertidal zone. The algal survey in

my study was conducted during the beginning of November, but in the two previous

months, several storms impacted the Cape Neddick area. Hence, the storms may also have

created more open spaces for the recruitment of other organisms. My results also showed

that there were more algal species in the shallow than in the deep subtidal (Figs. 1.11-

1.13). Crustose corallines were conspicuous at -7 and -10 m (Figs 1.12-1.13), while they

were covered by other algae at shallower depths.

Dawes (1998) suggests that thick and leathery seaweeds dominate in the upper

subtidal zone, as they are able to tolerate intense water movement. By contrast, a variety

of morphologies such as branched, sheetlike, and filamentous algae occur in the mid-

subtidal zone. He also suggests that there are more algal species in the upper zone, as

well as a differential density reduction with depth. Further, deeper algae tend to be broad

blades and crustose in order to maximize light absorption. Mathieson (1979) also noted

that deep subtidal species in the Gulf of Maine tend to be crustose and perennial forms.

The seasonal studies showed that Lacuna vincta occurred on a variety of algal

species. However, densities in all size classes are found year round onLaminaria

Reproduced with permission of the copyright owner. Further reproduction prohibited without permission. saccharina (Table 1.1). As kelps ( Laminaria spp.) can occurred at all three depths

studied, their abundance may influence the habitat and food selection of L. vincta.

Trowbridge (1995) suggests that the feeding preference by herbivorous grazers is

influenced by the abundance of Codium fragile ssp. tomentosoides within subtidal

communities in New Zealand. In a similar way, one of the important factors influencing

habitat preference for L. vincta may be the abundance of kelp (Laminaria spp.) that was

found at multiple depths studied.

Reproduced with permission of the copyright owner. Further reproduction prohibited without permission. Maine

Cape Neddick, Maine

(Cape Neddick NH Isles of Shoals

500m

Appledore Island MA Isles of Shoals Smuttynose Island

Gosport Harbor Cedar Island 7? Lunging Cedar I Island jjj- Island Ledge Star Island

White Island 500m

Figure 1.1. Map of the two study sites: Cape Neddick, Maine and Star Island, Isles of Shoals, New Hampshire.

Average total number of snails per gram of algal dry weight that differ significantly among algal species species algal among significantly differ that at species algal nine on weight dry algal of gram per alga each of months 23of Cape Neddick, Maine. Letters above each histogram designate number of snails of number designate histogram each above Letters Maine. Cape Neddick, Figure 1.2. Average total number of of number total Average 1.2. Figure 1000 200 - 400 - 600 800 a o- y f < * & _x_ a Lacuna vincta Lacuna Algae 19 ' A & (P < (P 0.05). , J pu I Efo 115samples from SE I plus L J a / / - r^~i Reproduced with permission of the copyright owner. Further reproduction prohibited without permission. without prohibited reproduction Further owner. copyright the of permission with Reproduced

Average total number of snails per gram of algal dry weight 200 - 400 0 - 300 100 i 500 - that differ significantly among algal species algal among significantly differ that snails of number designate histogram each above Letters collection. algal at species algal nine on weight dry algalof gram per alga each of months 2 of Star Island, Isles of Shoals, New Hampshire. Asterisk represents no represents Asterisk Hampshire. Shoals,New of Isles Island, Star Figure 1.3. Average total number of of number total Average 1.3. Figure - I Reproduced with permission of the copyright owner. Further reproduction prohibited without permission. without prohibited reproduction Further owner. copyright the of permission with Reproduced

Average size of snails (mm) 1 among algal species species algal among Maine. Neddick, Cape at species algal nine on alga each of months 23 of Letters above each histogram designate size of snails that differ significantly significantly differ that snails of size designate histogram each above Letters Figure 1.4. Average size of of size Average 1.4. Figure - cT L J a.b & X a (P < 0.05). < L J a,b Lacuna vincta Lacuna & _x_ n— b Algae G*° 21 & b f plus 1 SE from 115 samples 115samples from 1 SE plus o- _x_ b a,b X _X_ a,b 9>- X a,b Figure 1.5. Average size ofLacuna vincta plus 1 SE from 10 samples of 2 months of each alga on nine algal species at Star Island, Isles of Shoals, New Hampshire. Asterisk represents no algal collection.

Reproduced with permission of the copyright owner. Further reproduction prohibited without permission. Figure 1.6. Seasonal abundance of the snails per gram of algal dry weight plus 1 SE at Cape Neddick, Maine on four algal species a)Laminaria saccharina b) Ulva lactuca c) Chordaria flagelliformis d) Antithamnionella floccosa (Note: There is a difference on the scale of y axe of each graph).

Average density of snails per gram of algal dry weight Average density of snails per gram of algal dry weight 200 400 - 600 - 800 - 0 n 200 100 120 4 - 140 - 160 8 - 180 0 - 40 20 - 60 0 - 80 - - - - AMJ AMJ J M A A O N F M M F M D JASO A NDF MAMJ 98 99 2000 1999 1998 JASONDF MAMJ 98 99 2000 1999 1998 M F J D N O S A J a) a) Ulva Laminaria 500 i

c) Chordaria 400 -

2 ■*— w 0£ 5 '« * ^ ■a® "O ^

g - 200 - ft v» « C

100 -

AMJ JASO NDF MAMJ

1998 1999 2000

400

d) Antithamnionella

300 -

C /3 ^ ■s -3 200 -

100 -

AMJ JASO NDF

1998 1999 2000

Reproduced with permission of the copyright owner. Further reproduction prohibited without permission. Figure 1.7. Mean size of the snails per gram of algal dry weight plus 1 SE on four algal species at Cape Neddick, Maine a) Laminaria saccharina b) Ulva lactuca c) Chordaria flagelliformis d) Antithamnionella floccosa (Note: There is a difference on the scale of y axe of each graph).

Reproduced with permission of the copyright owner. Further reproduction prohibited without permission. Reproduced with permission of the copyright owner. Further reproduction prohibited without permission. without prohibited reproduction Further owner. copyright the of permission with Reproduced in N V © ■si c a E E Size of snails (mm) 2 - 4 1 - 3 - - 2 -i 5 - AMJ JASO NDF MAMJ JASO NDJFM — I iIII I I ~ i I I 1 'I I I I I I I I I I 1 AMJ JASO 1 --- 1 1 1 1 1 1 1 981999 1998 981999 1998 !~ NDFMAMJ i i i i i i i i 27 ~ 1 i b) b) JASO N D a) a) Ulva ------Laminaria 1 ------i ------1- - r ------—i i i— 1— J F M 2000 2000 1 ------1 ------1 1 Reproduced with permission of the copyright owner. Further reproduction prohibited without permission. without prohibited reproduction Further owner. copyright the of permission with Reproduced

Stec of snails (mm) Sizc #f sna„s (mm) 0 2 3 4 1 5 2 A MJA J S ON D FM AJA M J S O A MJA J S ON D FM AJA M J S OND J F M 98 99 2000 1999 1998 98 99 2000 1999 1998 d) d) c) c) Antithamnionella Chordaria M F J D N -3 m

Brown Algae 1.4% Green Algae 4.8%

Red Algae 18.3%

Mytilus edulis and Amphipod Tube Matrix 75.5%

Figure 1.8. Estimated percent coverage of red, green, and brown algae on horizontal rocky surfaces of -3 m of Cape Neddick, Maine.

Reproduced with permission of the copyright owner. Further reproduction prohibited without permission. -7 m

Brown Algae 3.3%

Red Algae 22.8%

Mytilus edulis and Amphipod Tube Matrix 73.9%

Figure 1.9. Estimated percent coverage of red, green, and brown algae on horizontal rocky surfaces of -7 m of Cape Neddick, Maine.

Reproduced with permission of the copyright owner. Further reproduction prohibited without permission. -10 m

Brown Algae 5.8%

Mytilus edulis and Amphipod Tube Matrix 79.1%

Figure 1.10. Estimated percent coverage of red. green, and brown algae on horizonatal rocky surfaces of -10 m of Cape Neddick, Maine.

Reproduced with permission of the copyright owner. Further reproduction prohibited without permission. -3 m

1 0 0 -i

80 -

s? 0u 60 - > 9 u

1 40 - L a ii.

20 -

ftc.

■0

Algae

Figure 1.11. Estimated percent coverage of algal species on horizontal rocky surfaces plus 1 SE at -3 m at Cape Neddick, Maine.

Reproduced with permission of the copyright owner. Further reproduction prohibited without permission. -7 m

100 n

80 -

60 - o U

I 40 -

20 -

■O

Algae

Figure 1.12. Estimated percent coverage of algal species on horizontal rocky surfaces plus 1 SE at -7 m at Cape Neddick, Maine.

Percent Cover (%) 0 1 100 20 40 - 80 - - rockysurfaces 1plus SE at -10m at CapeNeddick, Maine. iue .3 Estimated 1.13.Figurepercent coverage of algalspecies horizontalon Algae -10 m -10 34 No Collection No Collection No Collection Bonnemaisonia Codium 0 2.04 124.4 19.68 No Lacuna 47.18 50.86 D. D. viridis 0 2.39 0 0 0 0 1.4 12.35 12.56 57.61 204.3 12.53 10.89 28.64 0 0 0 1.56 0.46 0 1.07 88.2 17.34 185.7 200.3 163.2 64.8469.53 70.23 55.85 5.31 12.34 No Lacuna 13.77 1.41 44.36 24.72 14.56 56.55 295.6 11.68 23.1 Algae Chordaria A. floccosa populations pergram ofalgal dry weight on nine algal species 3.2 2.5 2.4 29.93 3.66 9.34 0.36 9.68 47.2 4.09 13.38 0 4.53 3.83 145.1 4.39 7.69 No Lacuna 13.74 20.23 D. aculeata Lacuna vincta 0 0 0.74 8.91 0 2.15 12.84 117.4 25.41 120.2 5.88 8.84 13.47 46.37 274.6 46.69 52.94 0 4.5 11.28 1.5 1.06 6.82 26.53 2.39 0.88 3.56 12.88 72.64 1.875 2.51 0.28 4.78 23.13 49.54 38.01 Laminaria Ulva 0 32.44 22.54 1.2 0 2.59 3.86 4.66 5.48 0 5.55 1.53 4.2 1.43 2.47 5.17 3.38 4.01 20.85 4.15 17.2 2.16 0 10.32 13.18 0.76 51.56 31.86 69.22 201.9 37.16 15.13 10.23 0.389 52.39 Chondrus 1 5 6 1 2 4 5 0 3 6 4 3.27 23 7.09 5 6 0 7.24 3 11.93 5.48 70.62 11.84 24 32.71 Total Total Total May June April 1 1998 Size 4 = 3.1-4.0 mm, Size =5 4.1-5.0 mm, Size 6 = > 5.0 mm). Table 1.1. Abundance ofdifferent sizeduring classes Aprilof 1998 to March 2000 a t-6 m at CapeNeddick, Maine (Size = < 1 mm,1.1 Size2= 1.1-2.0 mm, Size 3 = 2.1-3.0 mm, Months Sizes

Reproduced with permission of the copyright owner. Further reproduction prohibited without permission. No Collection No Collection No Collection Bonnemaisonia 0.4 6.14 6.96 Codium No Lacuna No Collection No Lacuna 0 1.56 9.38 5.49 3.74 Algal No Lacuna 0 0 0 0 1.5 0 600 5.65 0 137.7 172.7 Absence 336.4 84.84 147.8 38.19 0 0 0 0 0 0 0 0 6.55 0 126 117.7 0.71 198.6 86.36 29.04 211.2 5.29 Algae 00 5.22 0 0 0 2.14 56.57 4.54 1.54 3.38 17.52 14.92 0 2.45 165.4 188.4 240.4 721 14.01 12.38 56.89 1.55 48.76 0 0 0 0 0 0 1477 4.13 0 0 0 0 12.75 3.52 109.2 712.7 0 26.58 0 0 0 0 4.83 56.43 14.52 0 13.14 2.33 14.82 90.48 45.53 142.3 14.33 102.6 45.82 76.05 103.3 404.6 94.41 445 19.19 36.11 98.68 7.89 74.45 152.3 0 1.63 60.61 213.8 41.2 41.62 107.5 24.15 71.58 226.5 4.85 Laminaria Ulva D. aculeata Chordaria A. floccosa D. viridis 0.7 11.11 5.33 52.09 112.6 0.27 7.14 9.67 7.11 0.18 1.3 12.24 1.59 7.68 3.25 57.58 344.9 33.21 16.66 4.32 2.61 37.5 42.87 52.3 13.99 11.14 42.71 92.96 72.05 452 25.48 26.64 Chondrus 1 3 5 4 6 0 0 6 0 0.4 5 0.39 0 0 2 3 2 78.41 178.9 457.4 53.66 272.2 1 4 5 0.42 0 5 4 6 0 0 0 0 0 0 0 3 2 2.66 45.44 227.1 3 0.49 0.37 4 2 6 0 0 Total 47.16 35.71 261.8 107.5 220.8 Total 219.7 Total Total 89.95 187 475.6 80.16 290.3 517 4.85 17.62 July August 1 October September 1 Months Sizes

Reproduced with permission of the copyright owner. Further reproduction prohibited without permission. No Collection No Collection No Collection No Collection Bonnemaisonia 0 1.45 1.03 0.34 Codium No Lacuna 0 viridis 344.4 310.5 76.66 No Lacuna D. D. 0 0 8.33 5 0.03 0 Algal Algal No Lacuna 101.7 168.3 33.83 278.3 356.8 671.8 275.9 251.1 Absence Absence Absence Absence A. floccosa 0 0 157 8.71 0 0 13.33 34.11 0 12.4 354.9 696.9 185.4147.8 0.006 911.7 393.9 814.3 256.7 96.61 0 201.1 Algal Algal Algae 0 0 0.6 0 0 0 0.91 0 0 248 4.98 6.18 54.94 16.76 52.29 35.21 55.46 20.77 17.63 55.03 457.2 0 0 0 0 0 0 20 6.14 0 0 0 728 66.42 1095 7.22 3.44 2409 552.8 739.8 90.52 312.5 140.9 116.3 2.564 4.67 300.8 267.1 12 0 23.84 8.1 0.94 2.71 3.04 0 0 0 18.19 13.35 128.4 104.416.26 93.76 22.98 62.12 23.75 557.5 20.3921.4278.12 0 0 5.21 0 694.1 1.5 3.54 1.37 9.03 1.97 48.8 0.63 3.97 0.33 3.81 107.7 46.27 11.36 11.09 41.98 9.79 13.89 94.91 50.02 184.1 189.8 697.6 Chondrus Laminaria Ulva D. aculeata Chordaria 5 3 5 0.99 1 6 1.29 7.88 2 23 54.28 6 24.23 13.7 77.13 14.04 4 2.88 1.94 12.63 0.76 1 5 6 0 2 17.36 7.89 12.5 15.41 3 4 235 136.8 60.33 163.5 216.3 979.44 635 170.3 5.04 110.8 6 4 Total Total 185 129.4 929 132.1 1319 974.7 Total 84.16 Total 1999 March 1 February 1 Months Sizes December November

Reproduced with permission of the copyright owner. Further reproduction prohibited without permission. 0 0 0 0 0 0 0 6.57 5.21 0.65 9.79 13.15 13.46 10.92 64.58 87.52 28.68 No Lacuna 69.58 No Lacuna 3.06 0 0 1.6 9.7 66.63 0.57 0.93 0 4.37 51.61 0 0.32 0 247 80.67 32.89 4.34 2.876.41 6.34 43.32 2.56 4.82 2.87 15.21 7.45 129.8 48.53 56.34 22.38 13.15 11.66 0 0 0 0 2 3.89 1.35 5.4 107.7 14.1 23.88 235.16 179.4 182.3 10.06 0 4.12 14.19 19.91 7.74 3.04 No Lacuna 40.74 34.47 Algae 1.23 0 0 0.29 1.22 0 0 4.22 1.23 0 0 0 5.46 3.56 0 0.93 2.02 0 15.54 130.3 14.56 49.75 36.54 50.61 30.78 34 5.12 14.93 10.53 77.19 41.12 0 0 0 0 0 12.5 1.24 1.66 2.48 30.39 0 0.93 0 24.1 281.5 142.8 301.6 87.22 26.42 66.2 41.32 1.72 No Lacuna 0 100.4 134.6 56.78 23.31 57.26 31.13 22.85 43.89 11.4 7.38 6.13 14.66 25.46 114.8 0 2.24 17.12 27.79 60.63 12.09 0.85 42.92 95.65 59.89 1.82 1.8 6.57 5.35 27.54 2.63 5.19 1.71 39.9 5.42 25.75 0.34 11.09 8.2 36.1 3.57 60.55 56.86 188.8 Chondrus Laminaria Ulva D. aculeata Chordaria A. floccosa D. viridis Codium Bonnemaisonia 1 6 0 1.33 0 0 0 0 0 5 0 1.32 0 5 2.46 2.94 5.13 4.2 2 17.97 34 7.57 9.02 86.11 3 30.32 28.59 62.51 6 0.22 0 1 56 1.682 1.59 1.12 14.12 0.72 2.28 4 5 23 3.14 2.4 3.99 4 6 3 27.98 5.38 21.24 2 62.73 4 4.81 6.92 6.9 Total 33.55 87.34 Total Total 13.81 14.15 50.18 47.94 Total 137.5 43.65 July May 1 3.18 0.37 1.31 0 June 1 2.31 0 April Months Sizes

Reproduced with permission of the copyright owner. Further reproduction prohibited without permission. 0 0 0 0 0 0 0 0 0 0 0 0 Bonnemaisonia Codium No No Lacuna 0 No Lacuna 000 0 0 0 0 0 0 0 0 0 0 8.96 Algal No Lacuna 0 23.56 No Lacuna 0 D. D. viridis 0 0 0 16.84 0 124.5 256.3 64.76 0 0.75 0 54.0930.75 Algal Algal 0 157.3 174.7 8.96 0 96.51 380.2 349.8 17.58 182.6 38.48 258.4 433.4 68.11 Algae 0 0.75 0 55.28 4.34 0 0 21.42 0 00 0.75 11.33 21.19 2.56 0 0 0 1.87 6.023.28 5.88 Absence Absence 9.09 3.29 73.03 38.98 19.25 170.2 33.85 10.98 58.12 14.92 0 0 0 0 0 0 0 1470 190.2 101.6 6.66 78.21 188.2 16.57 338.9 9.65 97.59 72.28 Absence 194.8 0 0 0 0 0 0 0 0 0 1.66 0 5.92 22.2 5.74 2.12 16.99 189.6 1192 177.1 345.3 60.71 17.58 36.35 33.65 51.57 13.21 113.6 216.4 376.3 0 0 00 9.25 0 0 0 9.54 39.7 103.9 4.214.59 23.42 43.36 181.2 18.8 1.69 9.33 0 2.46 0.24 0.26 14.62 18.76 218.5 180.3 924.6 40.86 109.4 43.45 Chondrus Laminaria Ulva D. aculeata Chordaria A. floccosa 1 56 1.4 3 1 3 21.75 72.692 4 189.1 0.36 5 6 5 4 1 0.4 9.42 68.38 40.9 3.29 6 2 23 12.42 10.11 68.58 89.73 106.8 17.48 6 04 0 2.17 31.22 0 41.94 0 3 1.2 5 2 0.93 52.06 4 1 Total 34.38 Total 282.7 396.2 1511 50.89 Total Total 2.81 76.83 393.8 83.85 August October Months Sizes November September

Reproduced with permission of the copyright owner. Further reproduction prohibited without permission. 0 0 0 0 0 0 0 0 0 0 0 0 0 0 0 0 0 0 0 0 45 45 Codium Bonnemaisonia No Lacuna 0 00 0 0 0 0 00 0 0 0 0 40 46.67 0 0 0 0 0 500 80 Algal Algal No Lacuna 0 A. floccosa D. viridis 00 4 0 59.19 33.33 0 111 0 16.67 175.8 0 40 946.7 33.33 575.7 Algae Chordaria 0 0 0 0 0 0 0 0 0 8.92 3.81 14.77 25 74.81 29.68 375 98.56 60 24.44 1708 28.95 720.8 500 556.4 133.9 136 173.7 538.7 157.6 21.42 29.77 363.3 25.56 1250 658.9 139.5 No Lacuna 294.7 825.4 29.11 910.3 277.6320.5 12.68 10.92 198.9 Absence Absence 0 14.45 0 0 193.4 48.99 292.9 53.57 112.1 101 251.9 27.34 75.39 35.58 1.69 24.96 257.8 34.47 88.54 95.04 177.2 299.7 Laminaria Ulva D. aculeata 0 43.01 0 3.9 12.5 0 0 0 7.81 4.65 0 0 0 0 6.25 0 1.6 1.15 43.52 5.7 173 378.9 2198 7.64 26.21 55.45 1.48 138.2 15.18 9.39 152.9 0 0 0 148.3 63.04 61.03 26.2 118.2 71.42 23.85 68.76 194.3 No Lacuna 107.2 Chondrus 1 1 184.4 62.6 6 0 18.9 2.63 0 0 0 3 5 2 4 6.46 30.05 57.46 1 5 5 3 31.15 11.06 6 0 0 3.22 0 0 6 2 26.6 24.31 162.7 4 1 23 11.4 31.25 172.3 5 3 22.65 4 7.6 50.78 142.7 6 4 9.41 2 50.05 Total Total Total 258.9 108.5 1020 70.01 1650 757.5 246.2 Total 190.8 2000 March January Months Sizes February December

Reproduced with permission of the copyright owner. Further reproduction prohibited without permission. 11.89 18.54 53.47 98.47 32.81 61.34 Bonnemaisonia 0 0.29 1.34 163.76 7.67 0 0.17 0 12.86 15.9 49.9 25.64 19.82 0 0 16.65 0.78 72.53 11.33 0.19 0 1.16 0 3.07 34.5 5.37 4.85 13.25 3.5 14,87 40.06 14.77 51.97 45.68 A. floccosa D. viridis Codium 9 0 0.29 0.19 8.26 0 0 0 50.07 22.64 419.9 201.1 Algae 0 0 9 0 0.5 1.6 0 0 0 populations per gram ofalgal dry weight on nine algal species 15.59 164 59.51 369 0 0 0 0 106 65.2 28.96 45.75 3.84 6.71 4.54 Ulva D. aculeata Chordaria 11.41 12.66 85.01 57.21 29.61 32.96 Lacuna vincta Collection Collection Laminaria 0 No 1.01 16.45 1.01 3.07 3.22 No 8.1 26.55 132.6 23.95 16.23 0 Chondrus 1 1 5 0 56 0 0 0 3 1.5 45.12 0 177.2 6 0 0 0 0 0 0 2 4 3 1.5 4 2 3.07 Total 8.8 Total 5.59 July 1999 June Months Sizes Size 3 = 2.1-3.0 mm, Size 4 = 3.1-4.0 mm, Size 5 = 4.1-5.0 mm, Size 6 = > 5.0 mm). during June to July 1999 at -6 m at Star Island, Isles ofShoals, New Hampshire (Size = < 1 mm, 1.1 Size 2 = 1.1-2.0 mm, Table 1.2. Abundance ofdifferent size classes of

Reproduced with permission of the copyright owner. Further reproduction prohibited without permission. CHAPTER 2

FEEDING PREFERENCE OF LACUNA VINCTA ON

DIFFERENT ALGAL SPECIES

Introduction

Food selection by animals is influenced by food quality and environmental

condition, such as predation, competition, and chemical defense against herbivores

(Duffy and Hay, 1991; Raffaelli and Hawkins, 1996). For small marine herbivores that

live on the plants they consume, food and habitat are closely linked (Hayet al., 1989).

Therefore, the food value of plants can be as important as the refuge value in determining

patterns of plant utilization (Hayet al ., 1989).

Predation also plays an important role on foraging and habitat utilization by

foragers. In order to avoid predators, foragers prefer to choose food of low quality but

high in chemical defenses against predators (Holomuzki and Short, 1988). Duffy and

Hay (1991) showed that the abundance of the marine amphipod Ampithoe longimana

(Smith) on five different species of seaweeds was more related to the algal preference of

a fish predator than the amphipods’ feeding rates.

In addition, chemical defenses of seaweeds against different types of marine

herbivores play an important role in selection of seaweed by herbivores (Paul and Hay,

Reproduced with permission of the copyright owner. Further reproduction prohibited without permission. 1986; Hay et al., 1990). Recently, several studies have shown that small herbivores

(mesograzers) often graze selectively on seaweeds that are not eaten by fishes. In

addition, secondary metabolites of seaweeds, which significantly deter fish feeding, may

stimulate and/or affect feeding by mesograzers (Paul and Hay, 1986; Hayet al., 1988;

Hay and Fenical, 1988; Hayet al., 1990, Lobban and Harrison, 1994; Duffy and Hay,

1994).

My results outlined Chapter 1 showed thatLacuna vincta occurred on a variety of

algal species. Therefore, feeding preference experiments were conducted in order to

determine its food preference on different algal species and to determine whether each

algal species was used as a food source. Feeding trials onL. vincta, utilizing fresh and

dried algal species, involved both choice and non-choice assays. As aromatic, water-

soluble chemicals, and secondary metabolites of seaweed that might function as

deterrents in algae may play an important role in food preference byL. vincta, trails on

pre-dried and rehydrated algae were investigated.

Reproduced with permission of the copyright owner. Further reproduction prohibited without permission. Methods

Site o f Snail Collections

Lacuna vincta samples were collected using SCUBA techniques at Cape Neddick

Maine, during the summer of 1998 (Fig. 1.1). Snails were randomly collected from

algae. To collect the samples, plastic bags were placed to cover the algae, and then the

algae were removed from the substratum. The bags were tied shut and returned to the

University of New Hampshire within one hour. In the laboratory, the snails were sorted

and measured. Snails that were approximately 3.5-4.0 mm in shell length were selected

for the experiments. All of the selected snails were starved by placing them in containers

with no food for five days before starting the experimental trials.

Feeding Preference on Fresh Algae

Experiment 1: Feeding Preference on Fresh Algae by Lacuna vincta (Choice Assay)

Lacuna vincta were offered approximately an equal weight (O.lg) of eight algae,

including Laminaria saccharina, Codium fragile ssp. tomentosoides, Ulva lactuca,

Desmarestia acideata, D. viridis, Chordaria flagelliformis, Chondms crispus, and

Antithamnionella floccosa. One pre-weighed piece of each algal species was placed in a

7-cm diameter container with a single L. vincta. The algal-wet weights were obtained by

spinning the algae in a salad spinner and then blotting them dry before weighing. Two

treatments with ten replicates each were employed. Each container received one of the

following: 1) one L. vincta and eight different algal species; 2) only eight algal species

but no L. vincta. The experiment was run for five days in a constant temperature room at

Reproduced with permission of the copyright owner. Further reproduction prohibited without permission. 10°C. After five days, the remaining algae were weighed. The final weights were also

done by spinning the algae in a salad spinner and then blotting them dry before weighing.

Experiment 2: Feeding Preference on Fresh Algae (No-Choice Assay)

In no-choice assays, each container contained only one algal species and one

Lacuna vincta. Lacuna vincta was offered approximately an equal weight (O.lg) of each

of eight algae: Laminaria sacckarina, Codium fragile ssp. tomentosoides, Ulva lactuca,

Desmarestia acideata, D. viridis, Chordaria flagelliformis, Chondrus crispus, and

Antithamnionella floccosa. There were nine treatments with ten replicates each. With

each algal species, ten replicate containers received one L. vincta, and ten replicate

control containers of each algal species received no L. vincta. One pre-weighed piece of

each algal species was placed in each 7-cm diameter container. The initial-algal weights

were obtained as described above. Environmental conditions were the same as the food

choice assay. Lacuna vincta were allowed to feed for five days, after which the

remaining algae were weighed as outlined previously.

Feeding Preference on Dried Algae

Experiment 3: Feeding Preference on Dried Algae (Choice Assay)

The experiment was similar to the feeding preference on wet algae (Experiment I:

Choice Assay), except that the algae were dried to constant weight before and after the

experiment. Algae were dried and rehydrated in order to remove any aromatic or water-

soluble chemicals that might function as deterrents. Lacuna vincta was offered

approximately an equal dry weight (O.lg) of each of eight algae:Laminaria saccharina,

Codium fragile ssp. tomentosoides, Ulva lactuca, Desmarestia acideata, D. viridis,

Reproduced with permission of the copyright owner. Further reproduction prohibited without permission. Chordaria flagelliformis, Chondrus crispus, and Antithamnionella floccosa. One pre-

dried-weighed piece of each algal species was placed in a 7-cm diameter container with

one L. vincta. The dried algal weights were obtained by drying the algae in an incubator

at 75°C to constant weight before weighing. Two treatments with ten replicates each

were employed. Each container received one of the following: 1) oneL. vincta and eight

different algal species; 2) only eight algal species but no L. vincta. The experiment was

run for five days in a constant temperature room at 10°C. After five days, the remaining

algae were weighed. The final-dried-weights were also done by drying the algae in the

incubator at 75°C to constant weight before weighing.

Experiment 4: Feeding Preference on Dried Algae (No-Choice Assay)

The experiment was similar to the food preference study on wet algae

(Experiment 2: No-Choice Assay), except that the algae were dried to constant weight

before and after the experiment. Lacuna vincta was offered approximately an equal dried

weight (O.lg) of each of eight algae: Laminaria saccharina, Codium fragile ssp.

tomentosoides, Ulva lactuca, Desmarestia acideata, D. viridis, Chordaria flagelliformis,

Chondrus crispus, and Antithamnionella floccosa. There were nine treatments with ten

replicates each. With each dried algal species, ten replicate containers received one L.

vincta and ten replicate control containers of each algal species received no L. vincta.

One pre-dried-weighed piece of each algal species was placed in each 7-cm diameter

container. The pre-dried-algal weights were obtained as described above. Environmental

conditions were the same as the food choice assay. Lacuna vincta was allowed to feed

for five days, after which the remaining algae were weighed as outlined previously.

Reproduced with permission of the copyright owner. Further reproduction prohibited without permission. Statistical Analysis

A one-way ANOVA, followed by Tukey pairwise mean comparison was used to

examine the differences between the amount of each alga eaten by the snails in each of

the four assays. In addition, a two-way ANOVA was used to determine the differences in

the amount of algae eaten by the snails of eight algal species in choice assays on both

dried and fresh algae. A two-way ANOVA was also used to examine the differences in

the amount of algae eaten by the snails in eight algal species in no-choice assays on both

dried and fresh algae. Tests were done using Systat 7.0 (Systat, 1997).

Reproduced with permission of the copyright owner. Further reproduction prohibited without permission. Results

The results show that Lacuna vincta fed on all eight algal species. However, the

amounts of algae eaten were different for fresh and dried algal materials, and for the

choice and no-choice assays (Figs. 2.1, 2.2). Table 2.1 shows that there was a significant

difference in the amount of eight fresh algae eaten by the snails in the choice assay (P =

0.001). When using fresh algae in the choice assay, L. vincta consumed primarily

Antithamnionella floccosa, followed by Ulva lactuca, Laminaria saccharina, and

Chordaria flagelliformis (Fig. 2.1). Table 2.1 also shows that there was a significant

difference in the amount of fresh algae eaten by the snails in the no-choice assay (P <

0.0001), where the order of no-choice assay was A. floccosa, U. lactuca, L. saccharina,

and C. flagelliformis (Fig. 2.1). The amounts of each fresh algal species consumed in the

no-choice assay were higher than with the choice assay (Fig. 2.1). For the dried algal

assays, there was no difference in the amount of dried algae eaten by the snails in both

choice and no-choice assays (choice: P > 0.1, no-choice: P > 0.1).

The experiments also show that there were differences in feeding preference for

snails using dried and fresh algae (Figs. 2.1, 2.2). From Table 2.2, there was a significant

difference in the amount of algae eaten by the snails between eight algae and two choices

(P < 0.05). In the dried-algal-choice assay, Lacuna vincta preferred dried Chondrus

crispus and Laminaria saccharina (Fig. 2.2). Table 2.3 showed that there was a

significant difference in the amount of algae eaten by the snails between eight algae and

two no-choices ( P < 0.01). In the dried-algal-no-choice assay, L. vincta consumed

mostly C. crispus followed by Codium fragile ssp. tomentosoides, and L. saccharina

Reproduced with permission of the copyright owner. Further reproduction prohibited without permission. (Fig. 2.2). The amounts of each dried algal species consumed in the no-choice assay

were higher than those in the choice assay (Fig. 2.2).

Reproduced with permission of the copyright owner. Further reproduction prohibited without permission. Discussion

My study demonstrates thatLacuna vincta uses algae as both a habitat and food

source, and further that there are feeding preferences for different algal species. Algal

structure and secondary metabolites may play an important role in food selection (Figs.

2.1, 2.2). When comparing the amount of fresh and dried algae eaten in choice assays,

there were differences feeding preference by L. vincta (Figs. 2.1, 2.2), with L. vincta

preferring fresh over dried Antithamnionella floccosa (Figs. 2.1, 2.2). By contrast,L.

vincta preferred dried Chondrus crispus and Laminaria saccharina to fresh samples of

the same two species (Figs. 2.1, 2.2). There were also differences in feeding preferences

in two no-choice assays (Fig. 2.2), with L. vincta preferring fresh A. floccosa and Ulva

lactuca over dried A. floccosa and U. lactuca (Figs. 2.1, 2.2). By contrast,L. vincta

preferred dried C. crispus, Codium fragile ssp. tomentosoides, and L. saccharina over

corresponding fresh plants (Figs. 2.1, 2.2).

Several studies have emphasized the importance of algal morphology as a factor

affecting feeding preference of animals inhabiting seaweeds (Steneck and Watling, 1982;

Johnson and Mann, 1986; Clark and DeFreese, 1987; Hacker and Steneck, 1990; Hayet

al., 1990; Norton et al., 1990). Steneck and Watling (1982) suggested that most

herbivorous mollusks eat algae that have either a minute form (such as micro and

filamentous algae) or large and expansive blades (e.g., kelps). The latter algae are more

accessible to these herbivores, while the micro and filamentous algae are softer and easier

for herbivores to graze (Steneck and Watling, 1982). Algae that have a flat blade

structure like laminarian algae orUlva lactuca may also create more space forLacuna

Reproduced with permission of the copyright owner. Further reproduction prohibited without permission. vincta to graze on compared to cylindrical algae. Further, ephemeral soft algae such as

Antithamnionella floccosa may facilitate grazing because of their softness.

Nutritional quality in seaweeds is also a factor influencing the feeding preference

of herbivores (Johnson and Mann, 1986; Duffy and Hay, 1991). Johnson and Mann

(1986) suggested that the toughness and nutritional quality ofLaminaria spp. may

influence Lacuna vincta’’ s food selection, with the plants having a high nutritional value.

Duffy and Hay (1991) also suggest thatDictyota menstmalis (Hoyt) Schnetter, Homing

& Weber-Peukert is a preferred food of Ampithoe longimana (Smith) due to its high

protein and nitrogen content. Furthermore, the local distribution of algae in a benthic

community may affect food selection of animals. For example, Trowbridge (1995)

demonstrates that the introduced green alga Codium fragile ssp. tomentosoides is

primarily preferred by herbivores because of its abundance.

When dried algae were offered to the snails, the range of feeding preference

between fresh and dried algae changed, with dried Chondrus crispus, Laminaria

saccharina, and Codium fragile ssp. tomentosoides being highly preferred (Fig. 2.2).

Various algae may have different mechanisms for avoiding herbivores, including

chemical defenses (Paul and Hay, 1986; Hay and Fenical 1988; Hayet al., 1988; Hayet

al., 1990, Duffy and Hay, 1991). Duffy and Hay (1994) showed Gammarus that

mucronatus (Say) did not feed onDictyota menstrualis (Hoyt) Schnetter, Homing &

Weber-Peukert, which has secondary metabolites that deter grazers. Hay and Fenical

(1988) suggested that seaweeds produce terpenes, aromatic compounds, acetogenins,

amino acid-derived substances, and polyphenolics as secondary metabolites, and they

also suggested that various algae produce different types of secondary compounds.

Reproduced with permission of the copyright owner. Further reproduction prohibited without permission. Browns (Phaeophyta) produce polyp’nenolics, reds (Rhodophyta) terpenoids and

acetogenins, and greens (Chlorophyta) sesquiterpenoid and diterpenoid compounds (Hay

and Fenical, 1988). In addition, cells ofDesmarestia have sulfate ions. When the sulfate

reacts with water, it produces sulfuric acid, which deter grazers (Sze, 1998).

In feeding preferences on dried algae, the snails tended to prefer dried versus

fresh Chondrus crispus and Codium fragile ssp. tomentosoides. The preference may be

due to loss of some secondary compounds within the seaweeds when heated and dried.

However, more studies are needed to determine what secondary water-soluble

compounds are present in each of these eight algae.

Estimated Amount of Fresh Algae Eaten (g) 0.000 0.005 0.010 - 0.015 0.020 0.025 0.030 0.035 - 0.040 .4 - 0.045 -| 0.050 0.000 - 0.005 0.010 - 0.015 0.020 0.025 0.030 0.035 - 0.040 - 0.045 .5 -| 0.050 amount of algae eaten by snails (P < 0.05). < (P bysnails eaten of algae amount assay) (no-choice separately and assay) (choice together offered were algae plus 1 SE. Letters above each histogram designate significant differences insignificanthistogram differences designate each above Letters SE. 1plus Figure 2.1. Estimated grazing by grazing Estimated Figure2.1.

- - - -

✓ X X c a d,e JE_ a / cT aua vincta Lacuna 53 Algae _ x _ X d a 0- o- & & X c a on eight algal species when freshwhen species algal eight on o- O' - oc ssay A hoice o-C N a a oc ssay A hoice C cT f c e T

Reproduced with permission of the copyright owner. Further reproduction prohibited without permission. without prohibited reproduction Further owner. copyright the of permission with Reproduced

Estimated Amount of Dried Algae Eaten (g) 0.000 .0 - 0.005 0.010 - 0.015 0.020 0.025 - 0.030 - 0.035 .4 - 0.040 - 0.045 .5 - 0.050 0.000 0.005 0.010 0.010 0.015 0.020 - 0.025 .3 - 0.030 - 0.035 - 0.040 .4 - 0.045 -i 0.050 dried algae were offered(no-choice andseparately together (choice were assay) driedalgae sa)pu 1 SE. 1plusassay)

iue22 Estimatedgrazingby Figure 2.2. -

X 1 v‘ X X f < aua vincta Lacuna o- Algae O' 54 & o- oneightspecieswhen algal x oc ssay A hoice C X oCoc ssay A No-Choice cT cT X X

Table 2.1. Results of one-way ANOVA for differences in the amount algal consumption of snails on eight algal species in choice-fresh-algal feeding assay, no-choice-fresh-algal feeding assay, choice-dried-algal feeding assay, and no-choice-dried-algal feeding assay.

Feeding Assays df FP Choice-fresh algae 7 4.161 0.001 No-choice-fresh algae 7 6.894 <0.0001 Choice-dried algae 7 1.399 0.219 No-choice-dried algae 7 1.069 0.392

Table 2.2. Results of two-way ANOVA for differences in the amount algal consumption of the snails between two choice assays: fresh and dried algae and eight algal species.

Sources df F P Dried and fresh assays 1 0.000 1.000 Algae 7 1.976 0.062 Assays X Algae 7 2.109 0.046

Table 2.3. Results of two-way ANOVA for differences in the amount algal consumption of the snails between two no-choice assays: fresh and dried algae and eight algal species.

Sources df F P Dried and fresh assays 1 1.975 0.162 Algae 7 2.040 0.054 Assays X Algae 7 3.453 0.002

Reproduced with permission of the copyright owner. Further reproduction prohibited without permission. CHAPTER 3

GROWTH OF LACUNA VINCTA FED ON

DIFFERENT ALGAL SPECIES

Introduction

Herbivores in rocky shores are generally faced with food choices among various

algae. However, food quality is probably one of the important factors influencing

feeding selection, habitat utilization, and growth of herbivores (Nicotri, 1980; Viejo and

Arrontes, 1992). Growth of herbivores typically depends upon the quality and quantity

of food (Nicotri, 1980; Viejo and Arrontes, 1992).

In the rocky subtidal of the Gulf of Maine, several algal food sources are available

to Lacuna vincta. My results outlined in Chapter 1 plus those of several other researchers

indicate that L. vincta can be associated with a variety of algal species (Shacklock and

Croft, 1981; Southgate, 1982; Thomas and Page, 1983). The results in Chapter 2 also

indicate that L. vincta uses algae for both a habitat and a food source, while different

feeding preferences exist for different algal species. Although, L. vincta can consume a

variety of algal species, not all seaweeds have a nutrition of status for enhanced growth.

So far, no study has differentiated between the growth of L. vincta fed on various algal

Reproduced with permission of the copyright owner. Further reproduction prohibited without permission. species. Therefore, growth rate experiments were conducted in order to determine what

algal species support optimal growth of L. vincta.

Reproduced with permission of the copyright owner. Further reproduction prohibited without permission. Methods

Site o f Snail Collection

Lacuna vincta samples were collected using SCUBA techniques at Cape Neddick,

Maine during September 1999 (Fig. 1.1). Snails were randomly collected from algae as

described in previous Chapters. In the laboratory, the snails were sorted, measured, and

divided into three size classes: small (1.0 mm), medium (2.3-2.8 mm), large (3.3-3.8

mm). All of the selected snails were starved by placing them in containers for five days

before starting the experimental trials.

Laboratory Experiments

Experiment 1: Growth of Small Size (~1.0 mm) Snails

Juvenile smallLacuna vincta (~1.0 mm) were offered approximately equal weight

(0.1 g) of eight algal species: Laminaria saccharina, Codium fragile ssp. tomentosoides.

Ulva lactuca, Desmarestia acideata, D. viridis, Chordaria flagelliformis, Chondrus

crispus, and Antithamnionella floccosa. Ten replicates were utilized for each algal

experiment. Each 7-cm diameter container received either one snail and one species of

alga or one snail and no alga. The experiment was run for 8 weeks, with 12 hours light

and 12 hours dark each day. The shell lengths of L. vincta were measured weekly, and a

new piece of each algal species was given at the same time.

Reproduced with permission of the copyright owner. Further reproduction prohibited without permission. Experiment 2: Growth of Medium Size T2.3-2.8 mm) Snails

Medium Lacuna vincta (2.3-2.8 mm) were offered approximately equal weight

(0.1 g) of eight different algal species: Laminaria saccharina, Codium fragile ssp.

tomentosoides, Ulva lactuca, Desmarestia aculeata, D. viridis, Chordaria flagelliformis,

Chondrus crispus, and Antithamnionella floccosa. Ten replicates were utilized for each

algal experiment. Each 7-cm diameter container received either one snail and one species

of alga or one snail and no alga. The experiment was run for 8 weeks. The shell lengths

of L. vincta were measured weekly, and a new piece of each algal species was given at

this time.

Experiment 3: Growth of Large Size (3.3-3.8 mm) Snails

Large Lacuna vincta (3.3-3.8 mm) were offered approximately equal weight (0.1

g) of each of eight algal species: Laminaria saccharina, Codium fragile ssp.

tomentosoides, Ulva lactuca, Desmarestia acideata, D. viridis, Chordaria flagelliformis,

Chondrus crispus, and Antithamnionella floccosa. Ten replicates were utilized in each

algal experiment. Each 7-cm diameter container received either one snail and one species

of alga or one snail and no alga. The experiment was run for 8 weeks. The shell lengths

of L. vincta were measured weekly, and a new piece of each algal species was given at

this time.

Statistical Analysis

A one-way ANOVA test was used to test differences between average weekly

growth rates of snails fed on eight algal species in each size class; small, medium, and

large. Tests were done using Systat 7.0 (Systat, 1997).

Reproduced with permission of the copyright owner. Further reproduction prohibited without permission. Results

The results from the growth experiments showed that there were differences in the

growth of snails fed on the eight algal species (Figs. 3.1-3.3). With small snails, the

growth on Chordaria flagelliformis was higher than on all other seven algal species

during weeks 1 through 7 (Fig. 3.1). Thereafter, the growth of Lacuna vincta feeding on

Laminaria saccharina started to be higher than other algae on week 8 (Fig. 3.1). Lacuna

vincta had the lowest growth when they fed on Codium fragile ssp. tomentosoides (Fig.

3.1). In Table 3.1, there was a significant difference in the growth rate per week of L.

vincta fed on eight algal species (P = 0.001). In Figure 3.4, the snails fed on L.

saccharina had a higher growth rate per week (average 0.04 mm per week) than those fed

on other algae (average range: 0.0025 to 0.03 mm per week).

In the medium size snails, the growth on Laminaria saccharina was the highest

followed by those fed on Ulva lactuca and Chordaria flagelliformis. Table 3.1 showed

that there was a significantly different weekly growth rate for snails fed on different

seaweeds (P = 0.000). These snails fed on L. saccharina had a higher weekly growth rate

(average 0.09 mm per week) than all other algae (average range: 0.02 to 0.07 mm per

week). The mean size of animals used with L. saccharina and C. flagelliformis at the

start of the experiment was slightly smaller than for the other six algal species, but at the

end of the experiment they was larger, accentuating the enhanced growth on these algal

species (Fig. 3.2).

Growth rates of large snails were also highest on Laminaria saccharina, while

those on other seven algae and control did not have significant growth (Fig. 3.3). In

Reproduced with permission of the copyright owner. Further reproduction prohibited without permission. Figure 3.6, snails fed on L. saccharina had a higher growth rate per week (average 0.12

mm per week) than snails fed on the other algae (average range: 0.01 to 0.04 mm per

week).

Reproduced with permission of the copyright owner. Further reproduction prohibited without permission. Discussion

The present study demonstrates that there are differences in growth rates for

Lacuna vincta populations fed on different algal species (Figs. 3.1-3.6). Lacuna vincta

occurs on a variety of algae, but not all species are suitable or have a high nutritional

value for growth. Growth rates for all three size classes with Laminaria saccharina

tended to be higher than those fed other algal species (Figs. 3.4-3.6). Snails fed on Ulva

lactuca and Chordaria flagelliformis also had high growth rates (Figs 3.4-3.6), while

those fed on Codium fragile ssp. tomentosoides tended to be the lowest (Figs. 3.4-3.6).

My results also showed that the relative growth rates of snails declined on most of the

algae versusL. saccharina (Figs. 3.4-3.6). Moreover, the growth of the control snails

hardly increased due to starvation (Figs. 3.1-3.3). Starvation could also influence the

decreasing of the snails’ weight.

Nutritional quality of seaweeds is probably one of the main factors influencing the

growth rates o f herbivores (Johnson and Mann, 1986; Duffy and Hay, 1991). Johnson

and Mann (1986) suggested that Laminaria spp. had a higher nutritional quality than

many other algae. Lacuna vincta is not the only herbivore that prefers Laminaria as a

source of food. Grazers such as urchins and amphipods also choose laminarian algae as

their preferred food (Duffy and Hay, 1991; Prince and LeBlanc, 1992; Williams and

Harris, 1998).

Several studies also suggest that chemical defenses in seaweed may influence the

habitat and food selection o f herbivores (Paul and Hay, 1986; Hayet al, 1990; Duffy and

Hay, 1991). Therefore, chemical defenses in seaweeds may also play an important role

Reproduced with permission of the copyright owner. Further reproduction prohibited without permission. in deterring the growth of herbivores on algae. However, more studies are needed to

determine how chemical defenses in seaweeds may inhibit or slow the growth rate of a

herbivore. In addition, chemical attraction to seaweeds may influence the feeding pattern

of herbivores. Prince and LeBlanc (1992) suggested that Codium fragile ssp.

tomentosoides appears to lack a chemical attraction to herbivores; therefore, sea urchins

were unable to detect C. fragile ssp. tomentosoides, but will eat it when they contact it.

Moreover, algal morphology may influence the pattern of feeding preference of

various herbivores. The algae that have large and expansive forms, such asLaminaria

and Ulva, are probably more accessible for herbivores to graze on (Steneck and Watling,

1982). It is interesting to note that in my feeding study (Chapter 2),Lacuna vincta

consumed high amounts of Antithamnionella floccosa. However, the results from

Chapter 3 showed that the growth rate of snails fed on A. floccosa was not as high as

Laminaria saccharina or Ulva lactuca. Microscopic and filamentous algae are often

softer and easier for herbivores to graze on (Steneck and Watling, 1982).

Antithamnionella floccosa, which is a soft, bushy, and filamentous alga, may be easier for

L. vincta to graze. However, its nutritional value may not be as high as other algal

species.

Shell Length (mm) 0.0 0.1 0.9 A 0 2 3 6 1 5 algal species for eight weeks. for eight species algal Figure 3.1. Growth plus 1SE of 1SEof plus Growth 3.1. Figure 64 Lacuna vincta Lacuna eeks W 4 Antithamnionella Control viridis D. . aculeata D. Laminaria Ulva Chondrus Chordaria Codium (small size class) fed eight eight fed class) size (small

Reproduced with permission of the copyright owner. Further reproduction prohibited without permission. without prohibited reproduction Further owner. copyright the of permission with Reproduced

Shell Length (mm) 0.0 2.4 2.6 2.8 . -i 3.4 algal species for eight weeks. eight for species algal Figure 3.2. Growth plus 1 SE of 1 SEof plus Growth 3.2. Figure -. 0 Lacuna vincta Lacuna eeks W 65 Antithamnionella Control viridis D. D. aculeata D. Laminaria Ulva Chondrus Chordaria Codium 4

(medium size class) fed eight fedeight class) size (medium 82 6 Reproduced with permission of the copyright owner. Further reproduction prohibited without permission. without prohibited reproduction Further owner. copyright the of permission with Reproduced

Shell Length (mm) 0.0 0.1 3.2 3.4 3.6 3.8 4.0 4.4 4.6 4.8 5.0 0 algaispecies for eight weeks. Figure Growth 13.3. plus SE of 2 —O— Chondrus—a — — Chordaria—v — —O— Weeks Lacunavincta • *» r r 66 4 Control viridisD. Antithamnionella D.aculeata Ulva Laminaria Codium

(largesize class) fed eight

6 8 Reproduced with permission of the copyright owner. Further reproduction prohibited without permission. without prohibited reproduction Further owner. copyright the of permission with Reproduced

Average growth rate of snails per week (mm/wk) 0.00 0.01 - 0.03 0.02 - 0.04 .5 - 0.05 n 0.06 (small size class) fed on eight algal species. algal eight fedon class) size (small Figure 3.4. Average weekly growth rate plus 1 SE for 1 SE plus rate growth weekly Average 3.4. Figure / v y / p i .P JP ..P lip Jp • ? < jf

y 0^°

67 Algae J , Lacuna vincta Lacuna i i

Reproduced with permission of the copyright owner. Further reproduction prohibited without permission. without prohibited reproduction Further owner. copyright the of permission with Reproduced

Average growth rate of snails per week (mm/wk) 0.00 0.02 - 0.06 .4 - 0.04 - 0.08 0.10 .2 i 0.12 - - (medium size class) fed on eight algal species. algal eight on fed class) size (medium Figure 3.5. Average weekly growth rate plus I SE for SE I plus rate growth weekly Average 3.5. Figure V / / ' f c ^ / 68 V ( . . Algae I Lacuna vincta Lacuna • ? < T

Reproduced with permission of the copyright owner. Further reproduction prohibited without permission. without prohibited reproduction Further owner. copyright the of permission with Reproduced

Average growth rate of snails per week (mm/wk) 0.00 0.02 - 0.04 - 0.06 0.08 0.10 0.12 -| 0.16 .4 - 0.14 - - - (large size class) fed on eight algal species. algal eight on fed class) size (large Figure 3.6. Average growth rate per week plus 1 SE SE 1 plus week per rate growth Average 3.6. Figure

9 - a \® X & & X 69 Algae X for Lacuna vincta Lacuna for . X

Table 3.1. Results of one-way ANOVA for differences in the growth rates of snails in each size class: small, medium, and large fed on eight algal species.

Size class df F P Small 8 3.631 0.001 Medium 8 4.775 0.000 Large 8 2.525 0.017

Reproduced with permission of the copyright owner. Further reproduction prohibited without permission. CHAPTER4

POTENTIAL IMPACT OF MEMBRANIPORA MEMBRANACEA

ON LACUNA VINCTA POPULATIONS

Introduction

Membranipora membranacea was first found at the Isles of Shoals in the Gulf of

Maine during the summer o f 1987 (Lambert, 1990; Bermanet al., 1992; Lambert et al.,

1992). Membranipora membranacea mostly occurs on flat-bladed algae, such as

laminarian and fucoid algae (Ebling et al., 1948; Sloane et al., 1957; Ryland, 1970).

However at present, M. membranacea has also been found on cylindrical algae such as

Coclium fragile ssp. tomentosoides, Chordaria flagelliformis, Desmarestia aculeata, and

Ascophyllum nodosum (Harris and Mathieson, 2000; Harris and Tyrrell, 2001).

Overgrowth of kelp blades by the bryozoan is reported to have a negative impact as it

inhibits photosynthesis and causes defoliation (Lambert et al., 1992).

Lacuna vincta is a small herbivorous snail that feeds and lives on algae in the

rocky subtidal zone. Lacuna vincta is normally found on kelp (Martel and Chai, 1991),

but several papers have reported that L. vincta can be found on other algae such as Fucus

distichus ssp. edentatus, Chondrus crispus, Fucus serratus, Mastocarpus stellatus, and

Laurencia pinnatifida (Shacklock and Croft, 1981; Southgate, 1982; Thomas and Page,

1983). Based on previous results (Chapters 1, 2 and 3), kelp is one of the most important

Reproduced with permission of the copyright owner. Further reproduction prohibited without permission. habitat and food sources for Lacuna vincta. When the introduced bryozoan

Membranipora membranacea utilizes kelp as its habitat, this may affect L. vincta

populations that live and feed on kelp blades.

The purpose of this study was to enhance our understanding of the potential

impact of the introduced bryozoan Membranipora membranacea on Lacuna vincta

populations in the Gulf of Maine. Both M. membranacea and L. vincta use laminarian

algae as their habitats but little was known about the interaction between these two

potential competitors. The coexistence of both species on the same resource may have a

negative impact on either or both of these species by creating intraspecific and

interspecific competition for space. A combination of field samplings and laboratory

experiments were conducted in order to evaluate the impact ofM. membranacea on L.

vincta populations.

Reproduced with permission of the copyright owner. Further reproduction prohibited without permission. Methods

Field Samplings

Study Site and Sampling Location

Samples of Lacuna vincta were collected from Cape Neddick, York, Maine (43°

10' N, 70° 36' W) using SCUBA techniques (Fig. 1.1). The site is moderately exposed,

particularly to swells and storms out of the northeast.

Sampling Methods and Schedules

1. Comparing the Percent Cover of Membranipora membranacea and Density of

Lacuna vincta on Kelp Blades

Collections were made during October and November 1998 along transects at

three depths (-3, -6, -9 m). Five replicates of kelp sporophytes ( Laminaria spp.) were

collected at each depth, with replicates being taken 5 meter intervals. Samples were

collected by initially being covered with plastic bags, and then the algae were removed

from the substratum. Kelp samples were then returned to the University of New

Hampshire within one hour. In the laboratory, the snails and their egg masses were

counted and measured. A grid was used to determine the percent cover ofMembranipora

membranacea on each kelp blade. Both sides of the blades were measured and the results

were averaged to give a mean percent cover per blade. In addition, kelp blades were

dried and weighed. Weight of M. membranacea was determined by scraping off from

kelp surfaces before drying, and then was subtracted from the total algal weight to give

algal biomass. The percent of Laminaria weight covered byM. membranacea was also

subtracted to give area and biomass of Laminaria available to L. vincta. Then, density,

Reproduced with permission of the copyright owner. Further reproduction prohibited without permission. size, and the number of egg masses of L. vincta were related to the percent of available

grams of algal dry weight. Pearson correlation tests were used to test for correlations

between water depth, percent cover of M. membranacea, density, size, and number of egg

masses of L. vincta. Tests were done using Systat 7.0 (Systat, 1997).

2. Distribution o f Lacuna vincta on Kelp Blades

Ten kelp sporophytes were collected in approximately -6 m of water during

August 1999. Each kelp blade was approximately 30-40 cm long. Each kelp blade was

measured and divided into three parts (distal, middle, and proximal areas) using a pair of

scissors. Each part of the kelp blades was then placed separately in a plastic bag and

brought back to the surface. In the laboratory, the snails were sorted from the samples,

counted, and measured. Each part of kelp was also dried and weighed, with the snail

population parameters analyzed versus kelp blade weight. A one-way ANOVA test was

used to test density differences of snails on three portions of kelp blades. Tests were

done using Systat 7.0 (Systat, 1997).

3. Monitoring Kelp Blades

Field studies were conducted at Cape Neddick, Maine, to determine the types of

organisms using kelp habitats and the relationship between Lacuna vincta,

Membranipora membranacea, and Laminaria saccharina. The data were collected from

June 1999 through November 1999. Kelp sporophytes were tagged at a series o f water

depths: -3, -6, and -9 m along transects. Thirty replicates of kelp blades were tagged at

each depth, with the replicates being 1-2 meter apart. Kelp blades were monitored

monthly using SCUBA techniques. The types of organisms occupying the kelp blades

and the duration of their residence were recorded. The number of snails was counted,

Reproduced with permission of the copyright owner. Further reproduction prohibited without permission. and the percent coverage byMembranipora membranacea on kelp blades was estimated

and placed into one of five categories of percent cover: 0%, 1-25%, 26-50%, 51-75%,

and 76-100%. In addition, the kelp growth was measured using Chapman and Craigie’s

(1977) method. Kelp sporophytes lengthen by an intercalary meristem (transition zone)

that is formed at the base of the blade. In order to measure the kelp growth, four holes, 5

cm apart, were punched along the length of each blade with the first hole 1 cm above the

meristem. The distance moved by each hole from the meristem provided a measurement

of the elongation growth.

Laboratory Experiments

1. Impact of Membranipora membranacea Cover onLacana vincta Growth

To examine the impact of Membranipora membranacea on the growth of Lacuna

vincta, an experiment was conducted to compare the growth of snails fed on kelp

(Laminaria saccharina) with M. membranacea and without M. membranacea. All snails

used in the experiment were 2 mm long. Three treatments and ten replicates were used.

Each 7-cm diameter container received one of the following: 1) one snail and one piece

of kelp (approximately 3 cm X 3 cm) with 100% cover ofM. membranacea on both

sides; 2) one snail and one piece of kelp (approximately 3 cm X 3 cm) without M.

membranacea-, 3) a control with one snail and no kelp. Shell lengths of snails were

measured weekly for six weeks. A two-way ANOVA was used to test differences

between times and growth rates of the snails in different treatments. Tests were done

using Systat 7.0 (Systat, 1997).

Reproduced with permission of the copyright owner. Further reproduction prohibited without permission. 2. Structural Integrity of Kelp Fronds

The results of the field samplings in this Chapter showed that Membranipora

membranacea and Lacuna vincta coexist on kelp blades. Hence an experiment was

conducted .to determine whether M. membranacea or L. vincta had more effect on the

structural integrity of kelp fronds. Thirty kelp sporophytes were randomly collected from

Cape Neddick, Maine, using SCUBA techniques, and all samples were brought back to

the laboratory for analysis. Each sample of wet kelps was hung blade down from its

holdfast, and lead sinkers were attached at the tip of each blade with a C-clamp. Weights

were gradually added until the blade tore apart or a total of 2,940 grams was reached.

The location of any break was recorded, and the presence of L. vincta grazing holes

and/or M. membranacea cover was noted.

Prior to testing, each kelp blade was measured for length and width, and then

number of holes and the percent cover of Membranipora membranacea were recorded.

The maximum weight of lead sinkers used in this experiment was 2,940 grams. If a kelp

blade did not break after the addition of 2,940 grams, the blade was recorded as intact.

3. Effect of Intraspecific Competition for Space on Lacuna vincta

When Membranipora membranacea covers the surface o f a kelp blade, the

available space that Lacuna vincta can utilize for food decreases. Coverage byM.

membranacea increases the density of the snails in the open areas and may create

intraspecific competition within the snail population. The hypothesis is that the

competition between the snails in a limited area will influence their growth.

Laboratory experiments were conducted to examine intraspecific competition

between the snails. All snails were approximately 2 mm, with five treatments and five

Reproduced with permission of the copyright owner. Further reproduction prohibited without permission. replicates being used. Each 7-cm diameter container received one of the following: 1)

one snail and one piece of kelp (3 cm X 3 cm); 2) ten snails and one piece of kelp (3 cm

X 3 cm); 3) twenty snails and one piece of kelp (3 cm X 3 cm); 4) thirty snails and one

piece of kelp (3 cm X 3 cm); 5) one snail and no piece of kelp. Lengths of snails were

measured weekly for eight weeks. A one-way ANOVA test was used to test differences

between growth rates of Lacuna vincta at different densities. Tests were done using

Systat 7.0 (Systat, 1997).

Reproduced with permission of the copyright owner. Further reproduction prohibited without permission. Results

Field Samplings

1. Comparing the Percent Cover of Membranipora membranacea and Density of

Lacuna vincta on Kelp Blades

The patterns of percent cover of Membranipora membranacea, its density, the

size, and the number of egg masses of Lacuna vincta on Laminaria spp. at different

depths are summarized in Figure 4.1. There was a significant positive correlation

between the depth of the water and the percent cover of M. membranacea on kelp blades

(P < 0.01), with percent cover increasing from about 5% at -3 m depth to 35% at -9 m

(Fig. 4.1a; Table 4.1).

There was also a pattern of increasing density of Lacuna vincta per available

gram of kelp with depth (Fig. 4.1b), though the correlation of density and depth was not

statistically significant (Table 4.1). The highest density ofL. vincta was found at -9 m

(mean density of 137 per available gram of algal dry weight), but the variation between

blades was too great for statistical significance (range 17 per gram to 478 per gram).

Table 4.1 showed that there was a positive correlation between percent cover of

Membranipora membranacea and Lacuna vincta density on kelp(P < 0.005). There was

no correlation between water depth and size of L. vincta (P > 0.1). In Figure 4.1c, the

highest mean size of L. vincta was found at -6 m (2.16 mm), and the size of L. vincta

decreased at -9 m (2.06 mm). Egg masses were only found at -6 and -9 m, and the

number of egg masses per blade was similar for both depths (Fig. 4. Id).

Reproduced with permission of the copyright owner. Further reproduction prohibited without permission. 2. Distribution o f Lacuna vincta on Kelp Blades

Table 4.2 showed that there was a significant difference in the snail density on the

three portions of kelp blades (P < 0.0001). The results from Figure 4.2 showed that the

highest density of Lacima vincta was on the distal portions of kelp blades (mean density

of 33.58 snails per gram of algal dry weight), while the density of the snails was low on

the proximal portions of the kelp blades (mean density of 2.35 snails per gram of algal

dry weight). There was no significant difference in the size of the snails on the three

portions of kelp blades (P = 0.557). However, Figure 4.3 showed that the mean largest

snails were on the proximal portions of the kelp blades (2.09 mm), while the mean

smallest snails were on the distal portions of the kelp blades (1.65 mm).

3. Monitoring Kelp Blades

Table 4.3 shows that Membranipora membranacea initially occurred on kelp

blades during August, and by the end of November, it covered 75-100% of the plant

blades. The average number of Lacuna vincta also decreased when percent cover of

Membranipora exceeded 75%. In addition, kelp blades initiated growth in October.

Laboratory Experiments

1. Impact of Membranipora membranacea Cover on Lacuna vincta Growth

Table 4.4 showed that there were significant differences in the growth of Lacuna

vincta fed on Laminaria saccharina with and without Membranipora membranacea (P <

0.001). The growth rate of L. vincta fed on Laminaria without M. membranacea was

higher than when fed on Laminaria with M. membranacea in every week (Table 4.4; Fig.

4.4).

Reproduced with permission of the copyright owner. Further reproduction prohibited without permission. 2. Structural Integrity of Kelp Fronds

There were clear differences in the structural integrity of kelp blades with and

without Lacuna vincta feeding holes and Membranipora membranacea (Fig. 4.5). None

of the kelp blades without holes broke during the tests. By contrast, 82% of kelp blades

with L. vincta feeding holes broke, while 88% of those blades with holes and M.

membranacea cover separated (Fig. 4.5). The breaks were always in areas containing

feeding holes. In the case of the blades with both holes and M. membranacea, 62.5%

were in areas with only holes, while 25.5% were in areas of holes overgrown by M

membranacea (Fig. 4.5).

3. Effect of Intraspecific Competition for Space on Lacuna vincta

Significant differences in the growth rates were shown for snails in four density

treatments in Table 4.5 (P < 0.0001). When the density of snails on the kelp blades

increased, the growth of snails fed on kelp decreased (Fig. 4.6). The growth of one snail

per a piece of kelp was the highest, while the growth of 30 snails per piece of kelp was

the lowest (Fig 4.6).

Reproduced with permission of the copyright owner. Further reproduction prohibited without permission. Discussion

Lacuna vincta is a common herbivorous gastropod in subtidal habitats within the

Gulf of Maine (Maney and Ebersole, 1990), occurring on a variety of algal species

(Chapter 1). Laminaria spp. is its preferred food and the largest individuals ofL. vincta

tend to occur on kelp (Chapter 1), at least in part due to the seaweed’ s high nutritional

content (Martel and Chai, 1991). Grazing by L. vincta has been implicated as having a

negative impact on Laminaria populations (Fralick et al., 1974). Membranipora

membranacea, which first appeared in 1987 (Berman et al., 1992), also occupies

Laminaria blades and has been described as having a negative impact on kelp

populations (Lambert et al., 1992).

In the field study, both the percent cover ofMembranipora membranacea and the

density ofLacuna vincta on kelp blades increased with increasing water depth. At

increasing water depth there is less wave action, which may be beneficial to M.

membranacea (Ryland, 1970) and provide stability forL. vincta on kelp blades. In this

study, the statistical analysis showed there was a positive correlation between the percent

cover ofM. membranacea and the density ofL. vincta on kelp blades (Table 4.1). The

results suggest that these two species coexist on kelp blades (Fig. 4.1). Membranipora

membranacea uses laminarian algae for its substratum, whileL. vincta uses kelp for both

habitat and food (Ryland, 1970; Lambert et al., 1990; Martel and Chai, 1991; Berman et

al., 1992). Coexistence o f organisms on the same habitat may have negative impacts

either directly or indirectly, creating intraspecific and interspecific competition for the

resource (Jensen, 1985; Jensen and Kristensen, 1990). When M. membranacea covers

Reproduced with permission of the copyright owner. Further reproduction prohibited without permission. the surface of a kelp blade, the available space that L. vincta can utilize for food

decreases. Coverage byM. membranacea increases the density of snails in the limited

open area (Fig. 4.1b). The results from the intraspecific competition experiment suggest

that higher densities of snails in a limited area can have a negative impact on snail growth

(Fig. 4.6).

Like intraspecific competition, the effect of interspecific competition and

coexistence of Membranipora membranacea and Lacuna vincta may also have an impact

on the size of L. vincta. The largest L. vincta were found at -6 m where they occurred at

intermediate densities (Fig. 4.1c). By contrast, when the densities of snails were lower,

the growth of snails was higher (Fig. 4.6). The results suggest that crowding can inhibit

larger Lacuna from occupyingLaminaria spp. The decline in L. vincta’s mean size and

increased density at -9 m (Fig. 4.1c) would seem to support this pattern.

The laboratory results showed that the growth of Lacuna vincta fed on kelp with

Membranipora membranacea was lower than of that for those fed on kelp without M.

membranacea (Fig. 4.4). Thus, when M. membranacea overgrows kelp blades, it

obstructs L. vincta’s ability to graze on kelp, reducing the grazing area for L. vincta.

Lacuna vincta cannot penetrate blade surfaces covered by encrusting bryozoans likeM.

membranacea.

Berman et al. (1992) reported that Membranipora membranacea occurred

abundantly on kelp blades during the fall and winter at Cape Neddick, Maine. Lacuna

vincta occurs year round in the Gulf of Maine, and it has year-round reproduction

(Maney and Ebersole, 1990). Even thoughM. membranacea and L. vincta coexist on the

Reproduced with permission of the copyright owner. Further reproduction prohibited without permission. same kelp source, the overlap in spatial distribution is seasonal and Lacuna's ability to

utilize alternative algae may reduce the actual competition between the two species.

It is possible that Lacuna vincta may have a negative impact onMembranipora

membranacea occupyingLaminaria blades. The results from laboratory experiments

showed that the structural integrity of kelp fronds was decreased by holes made byL.

vincta as well as by overgrowth ofM. membranacea (Fig. 4.5). Kelp blades are more

easily broken in areas with holes caused byL. vincta grazing than with M. membranacea

because the former reduce the cross-sectional area of the kelp blade.

Fralick et al. (1974) suggested that grazing byLacuna vincta and the resulting

holes were an important factor leading to the severe breakage of kelp fronds observed at

Cape Neddick during the fall of 1973. Lambert et al. (1992) also reported that the

occurrence ofMembranipora membranacea on kelp fronds played an important role in

the defoliation of kelp blades at Cape Neddick. My study shows that both L. vincta and

M. membranacea can lead kelp breakage (Fig. 4.5). When both L. vincta and M.

membranacea occur, they make the blades more susceptible to breakage by wave action.

My results also showed that when M. membranacea was absent from kelp blades, L.

vincta normally accumulates and grazes on its distal and middle areas (Johnson and

Mann, 1986; Fig. 4.2). Like L. vincta, M. membranacea recruits most heavily near the tip

of kelp blades and grows basally (Ryland, 1970; Table 4.3). When M. membranacea

settles and overgrows portions of the kelp blades, it may impact L. vincta populations by

obstructing the preferred grazing area of L. vincta. Therefore, L. vincta may migrate

towards the base of the kelp fronds and increase in density on a small portion of clear

blade. Heavy grazing in a limited area may increase the likelihood of kelp breakage by

Reproduced with permission of the copyright owner. Further reproduction prohibited without permission. wave inducing breakage closer to the base of the blades or intercalary meristem and

creating more defoliation of kelp blades and/or decreasing the kelp growth.

Membranipora membranacea overgrowth may actually reduce its survival during

the winter, as areas heavily covered are less flexible to water movement. Furthermore,

M. membranacea overgrowth focuses Lacuna vincta grazing to the remaining free area

close to the base of the blade. Thus, when the breakage does occur, distal parts of kelp

blade covered by M. membranacea are most likely lost (see Figure 4.5). Studies by

Harris and Tyrrell (2001) suggest that in order to increase its survival rate,

Membranipora membranacea alters its habitat preference to other algal species. The

shift to alterative algal substratum would avoid indirect effects ofLacuna vincta grazing

on Laminaria blades, which decrease winter survival of M. membranacea colonies

through blade loss.

In summary,Membranipora membranacea appears to have a negative impact on

Lacuna vincta populations occupyingLaminaria spp. The overgrowth of M.

membranacea on kelps reduces grazing spaces for L. vincta, creating both intraspecific

and interspecific competition for space. Competition between these two species may also

have a negative impact on M. membranacea populations occupyingLaminaria spp.,

which may be facilitating the shift of this bryozoan to new algal substratum. Further

studies of the interactions between the introduced bryozoan and this common herbivorous

snail should provide interesting insights into the mechanisms governing their competition

for a common resource.

Reproduced with permission of the copyright owner. Further reproduction prohibited without permission. Figure 4.1. The percent cover ofMembranipora membranacea (a), average density per available gram of algal dry weight (b), average size (c), and average number of egg masses (d) of Lacuna vincta on Laminaria spp. plus 1 SE at different depths of water.

Reproduced with permission of the copyright owner. Further reproduction prohibited without permission. 250

200

& 150

100

2.5

2.4

2.3

2.2

O) 2.0

i\\M l\\N l\\M

Depth (meters)

Average density ofLacuna per gram of algal dry weight 5 - 25 20 -i 40 0 - 30 5 - 35 10 ep blades. kelp Figure 4.2. Density plus 1 SE of of 1 SE plus Density 4.2. Figure - - Distal 87 Lacuna vincta Lacuna Middle on different portions of of portions different on Proximal 2 -

c/5

1 -

o A------1------1------i Distal Middle Proximal

Figure 4.3. Size plus 1 SE ofLacuna vincta on different portions of kelp blades.

Length (mm) 0.00 0.05 2.00 2.05 2.20 1.95 - 2.25 2.30 -i 2.35 0 anacea. a e c a n ra b m e m nara sacchari a in r a h c c a s ria a in m a L gr 4. Th go h pu l E f o SE l plus th grow he T . .4 4 igure F 1 2 w ith and w ith o u t t u o ith w and ith w eeks W 5 3 89 4 una vi ta c in v a n cu a L Fed on on Fed on Fed Control pora r o ip n a r b m e M ami ria a in m La ria a in m La with without e on fed mbrartipora em M 6

mbrartipora em M

Breakage in Plain Area > i Breakage in Membrartipora Area ■ ■ I Breakage in Hole Area i i Breakage in Hole Area Covered By Membrartipora

100

80 -

re reO) 60 re m 40 -

20 ■

No Hole and Hole Only Hole no Membrartipora and Membrartipora

Type of kelp sam p les

Figure 4.5. The results of the experiment on breakage areas of kelp fronds.

Reproduced with permission of the copyright owner. Further reproduction prohibited without permission. 1 snail 10 sn a ils 2 0 sn a ils 3 0 sn a ils Control

3 E E £ O) 2 '3 z « (0

0 0 1 2 34 5 6 7 8 Week

Figure 4.6. The results showing growth plus 1 SE of Lacuna vincta in different densities fed on limited areas of kelp blades.

Reproduced with permission of the copyright owner. Further reproduction prohibited without permission. Table 4.1. Results of P-values of Pearson correlation on the relation between the depths o f water, % Membrartipora membranacea, density, size, and number of egg masses of Lacuna vincta.

Depth % Lacuna Lacuna Lacuna Membranipora Density Size Egg Masses

Depth - - - -- % 0.006 ““ * * Membranipora Lacuna 0.070 0.004 “ - " Density Lacuna 0.1654 0.235 0.418 “ Size Lacuna Egg 0.096 0.178 0.394 0.463 " Masses

Table 4.2. Results of one-way ANOVA for differences in density and size of the snails in three portions of kelp blades: distal, middle, and proximal.

df FP Density of snails 2 30.616 <0.0001 Size of snails 2 0.598 0.557

Months Average Average Average % Others growth of number of number of Membrani kelp blades Lacuna Lacuna egg pora cover (cm) masses (measured by punching holes) June 0 12 0 0 -

July 0 31.4 1.7 0 - August 0 37.9 2.4 1-25 Membrani pora on the distal portion of the blade, small mussels, flat worms September 0 58.4 1.9 25-50 epiphytes, flat worms October 1.4 65.7 0.5 50-75 flat worms November 1.2 37.2 0 75-100 flat worms

Reproduced with permission of the copyright owner. Further reproduction prohibited without permission. Table 4.4. Results of two-way ANOVA test for differences between times and the growth rate of Lacuna vincta in different treatments.

Sources df FP

Treatments 2 13.576 0.000828

Times 6 10.309 0.00

Treatments X Times 12 2.646 0.003

Table 4.5. Results of one-way ANOVA for difference in the growth rates of snails in four types o f densities of snails.

df FP Four types of 4 39.832 <0.0001 densities

Reproduced with permission of the copyright owner. Further reproduction prohibited without permission. CHAPTER 5

POTENTIAL IMPACT OF CODIUM FRAGILE SSP. TOMENTOSOIDES

ON LACUNA VINCTA POPULATIONS

Introduction

Lacuna vincta is a small herbivorous snail that feeds and lives on algae in the

rocky subtidal zone. Lacuna vincta is normally found on kelp (Martel and Chai, 1991),

but several reports indicated that it can be found on other algae such as Fucus distichus

ssp. edentatus, Chondms crispus, Fucus serratus, Mastocarpus stellatus, and Laurencia

pinnatifida (Shacklock and Croft, 1981; Southgate, 1982; Thomas and Page, 1983).

Based on previous results (Chapters 1-3),Laminaria spp. is one of the most important

habitats and food sources for Lacuna vincta.

At the Isles of Shoals in the Gulf of Maine, the introduced Asian green alga

Codium fragile ssp. tomentosoides has replaced Laminaria spp. and become a dominant

canopy species, while on the nearshore open coast at Cape Neddick, Maine, the kelp

species is still the dominant canopy species (Harris and Mathieson, 2000). However, in

the past year at Cape Neddick, the number of individual Codium plants has been

increasing (Harris pers. obser.). Changing algal composition from kelp bed to Codium

bed may affect herbivores that use kelp beds as their habitat and food source. The

purpose of this study was to compareLacuna vincta populations between an area

Reproduced with permission of the copyright owner. Further reproduction prohibited without permission. dominated by C. fragile spp. tomentosoides (Star Island) versus one dominated by

Laminaria saccharina (Cape Neddick).

A combination of a reciprocal transplants, and laboratory feeding experiments

were conducted in order to determine the impact of Codium fragile ssp. tomentosoides on

Lacuna vincta populations, as well as to compare L. vincta selectivity for habitat and

growth rates on the historically dominant versus the new canopy species.

Reproduced with permission of the copyright owner. Further reproduction prohibited without permission. Methods

Field Sampling

Reciprocal Transplant Experiment

A reciprocal transplant experiment was conducted during July 1999. Twenty

plants of Codium fragile ssp. tomentosoides collected from Star Island, Isles of Shoals

were transplanted to Cape Neddick, Maine, while twenty plants of Laminaria saccharina

from Cape Neddick were transplanted to Star Island. Each alga was tied to weighed

plasticized wire frames (approximately 33 X 63 cm), with five plants on each frame. The

frames were placed at -7 m at each study site. After two weeks, the transplanted algae

were collected and brought back to the laboratory. Five attached plants of C. fragile ssp.

tomentosoides from Star Island and five sporophytes of L. saccharina from Cape

Neddick were also collected as controls. In the laboratory, the snails associated with each

plant were counted and measured. In addition, the algae were dried and weighed, while

the density and size ofLacuna vincta were compared per gram of algal dry weight.

Laboratory Experiment

Laboratory Feeding Experiment

In order to examine the impact of Codium fragile ssp. tomentosoides on Lacuna

vincta’ s growth, an experiment was conducted to compare the growth rates of snails fed

Laminaria saccharina or C. fragile ssp. tomentosoides. Ninety snails in three size classes

(small ~ 1.0 mm; medium ~ 2.5 mm; large ~ 3.5 mm) were used, with three treatments in

each size class of the snails. Each 7-cm-diameter container received one of the

Reproduced with permission of the copyright owner. Further reproduction prohibited without permission. following: I) one snail and one piece of Laminaria saccharina (O.lg); 2) one snail and

one piece of C. fragile ssp. tomentosoides (O.lg); 3) a control with one snail and no algae.

Shell heights of the snails were measured weekly for eight weeks.

Statistical Analysis

A two-way ANOVA was used to examine the differences between the density and

size of Lacuna vincta associated with both control and transplanted specimens o f the two

algal species. In addition, a one-way ANOVA was used to determine the differences

between the growth of L. vincta fed on different algal species within each size class of the

snails. Tests were done using Systat 7.0 (Systat, 1997).

Reproduced with permission of the copyright owner. Further reproduction prohibited without permission. Results

Field Sampling

Reciprocal Transplant Experiment

The results of the reciprocal transplant experiment in Figure 5.1a showed that the

density ofLacuna vincta was higher on both control Laminaria saccharina at Cape

Neddick (17.21 snails per gram of algal dry weight) and transplanted L. saccharina at

Star Island (11.37 snails per gram of algal dry weight) than on control Codium fragile

ssp. tomentosoides at Star Island (5.38 snails per gram of algal dry weight) and

transplanted C. fragile ssp. tomentosoides at Cape Neddick (2.7 snails per gram of algal

dry weight). There was a significant difference in the densities of the snails between the

two algal species (P < 0.0001); however, there was no significant difference between

control and transplanted treatments in each algal species (P > 0.5). The average largest

size of snails was found on control C. fragile ssp. tomentosoides at Star Island (2.24 mm),

while the average smallest size of snails was found on control L. saccharina (1.43 mm) at

Cape Neddick (Fig. 5.1b). Table 5.2 showed that there was a significant difference in the

size of snails occurring on control and transplanted plants at both sites (P < 0.05). In

addition, the small and medium size classes of snails were found to be higher on control

L. saccharina than on transplanted C. fragile ssp. tomentosoides at Cape Neddick (Fig.

5.2). At Star Island, the medium and large size classes of snails were higher on

transplanted L. saccharina than on control C. fragile ssp. tomentosoides (Fig. 5.2). The

density of the small size class ofL. vincta was similar for transplanted specimens of both

algal species (Fig. 5.2).

Reproduced with permission of the copyright owner. Further reproduction prohibited without permission. Laboratory Experiment

Laboratory Feeding Experiment

Table 5.3 shows that there were significant differences in the growth of Lacuna

vincta fed on Laminaria saccharina and Codium fragile ssp. tomentosoides in all three

size classes (small: P < 0.05, medium: P < 0.0001, large: P = 0.001). Figure 5.3 shows

that the total growth of snails fed on L. saccharina was higher than those that fed on C.

fragile ssp. tomentosoides in each of three size classes for the eight-week period (Figs.

5.3a-c). The snails fed on L. saccharina had a higher growth rate per week (range: 0.03

to 0.09 mm per week) than snails fed on C. fragile ssp. tomentosoides (range: 0.0025 to

0.02 mm per week).

100

Reproduced with permission of the copyright owner. Further reproduction prohibited without permission. Discussion

The data from Chapter 1 showed that Laciina vincta occurs on a variety of algal

species including Laminaria saccharina. The results from field sampling showed that the

invasive green algaCodium fragile ssp. tomentosoides has a negative impact on snail

populations (Chapters I, 5). The average total density of the snails at Star Island, a site

dominated by C. fragile ssp. tomentosoides, was less than half that of Cape Neddick, a

site dominated by L. saccharina (Chapter 1). The average size of the snails at Cape

Neddick was smaller than at Star Island (Chapter 1, Fig. 5.1b). The results may imply

that there were more snails recruiting at Cape Neddick compared to at Star Island.

In this study, the kelp Laminaria saccharina is the preferred habitat and food

source for Lacuna vincta compared to the introduced Codium fragile ssp. tomentosoides.

In the reciprocal transplant experiment, the density of the snails was higher on L.

saccharina, even on the transplanted sporophytes at Star Island after only two weeks,

than on C. fragile ssp. tomentosoides. The growth of the snails of all three size classes

was higher when fed on L. saccharina, versus C.fragile ssp. tomentosoides. Laminaria

saccharina is considered to have high nutritional content for herbivores (Martel and Chai,

1991). Prince and LeBlance (1992) suggested that I.saccharina produces chemicals that

attract herbivores such as sea urchins, while C. fragile ssp. tomentosoides appears to lack

a chemical attractant, and they also found that sea urchins were unable to detect C.fragile

ssp. tomentosoides but would eat it when they contacted plants. The lack of chemical

attractant in C. fragile ssp. tomentosoides may explain the occurrence of higher densities

of the snails on both control and transplanted L. saccharina (Fig. 5.1a), as well as higher

101

Reproduced with permission of the copyright owner. Further reproduction prohibited without permission. growth rates for snails fed on L. saccharina (Figs. 5.3a-c, 5.4). In addition, the structure

of the habitat may play an important role for the distribution of herbivores (Hacker and

Steneck, 1990). Laminaria saccharina has a single flat blade while C. fragile ssp.

tomentosoides is composed of branched cylinders, which forms a bush so that branches at

the center of the plants may be less accessible to recruiting snails than outer portions.

Laminaria saccharina probably provides more flat space for L. vincta to colonize and

graze on than C. fragile ssp. tomentosoides.

In this study, we found that the mean size of the snails was larger on Codium

fragile ssp. tomentosoides than on Laminaria saccharina at both sites (Fig. 5.1b), while

the densities were higher on L. saccharina (Fig. 5.1a). However, the size distribution of

the snails showed that there were higher densities of the small, medium, and large size

classes of the snails on control and transplanted L. saccharina (Fig. 5.2). Relative

proportions of large and medium sized snails resulted in the mean being skewed to C.

fragile ssp. tomentosoides even though absolute densities were higher in those size

classes on L. saccharina.

There was no difference in the density of the smallest size class of Lacuna vincta

on transplanted plants at either site (Fig. 5.2), suggesting similar recruitment rates for the

two-week period and no selection at that stage. The controls had higher densities of

small snails, which is probably due to an accumulation over a longer time period (Fig.

5.2). Because Laminaria saccharina is the preferred habitat, juveniles of L. vincta tend

to settle on L. saccharina and they will not move frequently if it is a suitable habitat.

When the snails are older, they tend to move around more from one algal habitat to

another if the habitats are not suitable and so accumulate on more preferred algal species.

102

Reproduced with permission of the copyright owner. Further reproduction prohibited without permission. Martel and Diefenbach (1993) suggested that L. vincta showed a foot-raising behavior

and initiated mucous-thread drifting 3 to 5 times more often in no-algal habitat than in

algal habitat, and they also suggested that juvenileL. vincta demonstrated these two

behaviors more frequently than adults. In this study, the density of the small size class of

L. vincta was higher at Cape Neddick on control L. saccharina than on transplanted

Codium fragile ssp. tomentosoides, while at Star Island the density of medium and large

size classes of L. vincta was higher on transplanted L. saccharina than on control C.

fragile ssp. tomentosoides. Because L. vincta has an ability to drift in the water column

by secreting a mucous thread, it allowsL. vincta to relocate and to increase their ability

for habitat selection (Martel and Chai, 1991; Martel and Diefenbach, 1993). My results

suggest that this behavior may be more common in medium and large size classes than in

small size class of snails.

Lacuna vincta can be associated with a variety of algal species (Shacklock and

Croft, 1981; Southgate, 1982; Thomas and Page; 1983; Chapter 1); however, it can be

found in high density on kelps year round (Johnson and Mann, 1986; Maney and

Ebersole, 1990; Martel and Chai 1991; Chapter 1). The data from Chapter 3 showed that

when L. vincta was fed each of eight different algal species ( Codium fragile ssp.

tomentosoides, Laminaria saccharina, Ulva lactuca, Chordaria flagelliformis,

Desmarestia acideata, D. viridis, Chondrus crispus, and Antithamnionella floccosa), the

snails fed on L. saccharina had the highest growth rate, and the snails fed on C. fragile

ssp. tomentosoides had the lowest growth rate. The results implied that L. vincta become

associated with L. saccharina are more likely to remain and accumulate in numbers than

those that settle on C. fragile ssp. tomentosoides. From figure 5.3, it can be estimated

103

Reproduced with permission of the copyright owner. Further reproduction prohibited without permission. that if juvenile snails continue to feed onL. saccharina, they will reach the average adult

size (about 4-5 mm) in 6-7 months, while the juvenile snails that feed on C. fragile ssp.

tomentosoides will take more than 12 months to reach the average adult size.

Codium fragile ssp. tomentosoides is not a preferred food source of Lacuna

vincta. The snails fed on C. fragile ssp. tomentosoides had very low growth rates.

Feeding on C. fragile ssp. tomentosoides can lead to low reproductive output by the

snails. Lacuna vincta is an important food source for numerous animals and their

production can be high enough to support significant populations of organisms in higher

trophic levels such as fish, crabs, and other predators (Nelson, 1981; Johnson and Mann,

1986). Johnson and Mann (1986) showed that cunner ( Tautogolabrus adspersus) prefers

to feed on the larger size classes of L. vincta and half of the gut content of cunners

consisted of L. vincta. As field sampling demonstrated in Chapter 1, L. vincta densities

were lower on understory algae in C.fragile ssp. tomentosoides beds than in Laminaria

saccharina dominated communities. If the spread of C. fragile ssp. tomentosoides

continues in the subtidal communities in the coastal areas such as Cape Neddick, it will

have a negative effect, changing algal composition from a canopy dominated byL.

saccharina to one dominated by C. fragile ssp. tomentosoides. Changing algal

composition may lead to a decline in theL. vincta populations and it also may affect and

decrease the populations in higher trophic levels that consume L. vincta as a major food

source.

In the past year, Codium fragile ssp. tomentosoides has increased in numbers at

the Cape Neddick; however, the population density is still very low compared to Star

Island where it is now the dominant canopy species. Codium fragile ssp. tomentosoides

104

Reproduced with permission of the copyright owner. Further reproduction prohibited without permission. has been successfully established in several places such as in New Zealand and the Gulf

of Maine due to having several dispersal mechanisms (Fralick and Mathieson, 1972;

Carlton and Scanlon, 1985; Trowbridge, 1995; Chapman, 1999). The dispersal

mechanisms include gametes, parthenogenesis of female gametes, and reattachment of

fragments from adults (Fralick and Mathieson, 1972; Chapman, 1999). Another

introduced species that also has a negative effect on Lacuna vincta population is the

bryozoan Membranipora membranacea that overgrows kelp blades (Chavanich and

Harris, 2000; Chapter 4). The overgrowth reduces the grazing space for L. vincta and

creates intraspecific and interspecific competition between the snails and M.

membranacea for space on the kelp blades (Chavanich and Harris, 2000; Chapter 4). The

parallel success of these two introduced species, C. fragile ssp. tomentosoides and M.

membranacea, within subtidal of marine communities can lead to a higher level of

negative impact on L. vincta populations.

As preferred habitat and food in the kelp canopy is reduced by bryozoan coverage

and/or replacement of kelps by Codium fragile ssp. tomentosoides, Lacuna vincta may

switch to alternative algal food sources such as Ulva lactuca and Chordaria

flagelliformis. Some of these algal species are annuals (Mathieson and Hehre, 1986) and

the increased herbivore pressure may have a cascading effect of altering species

composition or relative abundance. Further studies are needed to determine how the

change in community state presently underway in the Gulf of Maine may affectL. vincta

in its roles as herbivore and food source in algal dominated subtidal communities.

105

Reproduced with permission of the copyright owner. Further reproduction prohibited without permission. Figure 5.1. Density oLacuna f vincta per gram of algal dry weight (a) and mean length of Lacuna vincta (b) plus 1 SE on control and transplanted Laminaria saccharina and control and transplanted Codium fragile ssp. tomentosoides at Cape Neddick and Star Island.

106

Reproduced with permission of the copyright owner. Further reproduction prohibited without permission. 2 0 -

3 E 3 Larrinaria saccharina S 3 Codium fragile ssp.tementosoides

Control Transplanted Control Transplanted Lamrtaria Cocfum Codum Larrinaria

Cape Neddick Star Island

107

Reproduced with permission of the copyright owner. Further reproduction prohibited without permission. Small (<1.1mm) Medium (1.1-2.5 mm) ] Large (> 2.5 mm)

Control Transplanted Control Transplanted Laminaria Codium Codium Laminaria

Cape Neddick Star Island

Figure 5.2. Size distribution of Lacuna vincta on each of control and transplanted Laminaria saccharina and Codium fragile ssp. tomentosoides at Cape Neddick and Star Island.

108

Reproduced with permission of the copyright owner. Further reproduction prohibited without permission. Figure 5.3. Average shell height plus 1 SE of Lacuna vincta in three size classes: a) -1.0 mm b) ~2.5 mm c) ~3.5 mm fed on Laminaria saccharina and Codium fragile ssp. tomentosoides for 8 weeks.

109

Average # •» shell § height % a Control L arrin aria saccharina aria arrin L oimfa ile frag Codium ssp. tomentosoides Reproduced with permission of the copyright owner. Further reproduction prohibited without permission. without prohibited reproduction Further owner. copyright the of permission with Reproduced classes fed on on fed classes Figure 5.4. Average growth rate per week plus 1 SE of of 1 SE plus week per rate growth Average 5.4. Figure

Average growth rate of e .8 ■ 0.08 je 0.02 - 0.04 - 0.06 0.10 0.12 i 0.14 - - - Laminaria saccharina Laminaria Codium and and Laminaria Codium fragile Codium Ill Lacuna vincta Lacuna r l tro n o C ssp. ssp. tomentosoides. I ------1 in three size size three in re - 5 mm) .5 (-3 mm) arge L .5 (-2 edium mm) M .0 (-1 all Sm Table 5.1. Results of two-way ANOVA for differences in the density of snails between two algal species: Codium fragile ssp. tomentosoides and Laminaria saccharina and the two treatments: transplanted and control.

Sources df F P

Algae 1 14.748 <0.0001 Treatments 1 2.435 0.127 Algae x Treatments 1 0.450 0.506

Sources df F P

Algae 1 3.781 0.059 Treatments 1 0.743 0.394 Algae x Treatments 1 4.917 0.033

Table 5.3. Results of one-way ANOVA for differences in the growth of snail in each size class fed on three treatments: Laminaria saccharina, Codium fragile ssp. tomentosoides, and no algae.

Size Classes df FP

Small 2 5.295 0.011 Medium 2 16.475 <0.0001 Large 2 9.094 0.001

112

Reproduced with permission of the copyright owner. Further reproduction prohibited without permission. GENERAL CONCLUSIONS

The results of the seasonal studies of the Lactma vincta at Cape Neddick, Maine

showed that it occurs on a variety of algal species (Chapter 1). However, the snail

populations in all size classes are normally found year round Laminariaon saccharina

(Table 1.1). At Star Island, Isles of Shoals, a site dominated by Codium fragile ssp.

tomentosoides, the average total density of snails was less than half of that at Cape

Neddick, a site dominated by L. saccharina (Figs. 1.2-1.3). In addition, Laminaria spp.

can be found at all three depths studied (Figs 1.11-1.13). The abundance o f the kelp may

influence the habitat and food selection of these snails. Trowbridge (1995) suggested that

feeding preference by herbivorous grazers was influenced by the abundance ofCodium

fragile ssp. tomentosoides in the subtidal community in New Zealand. Similar to

herbivores in New Zealand, one of the important factors influencing habitat preference by

L. vincta, may be the abundance of Laminaria spp. that was found at all three depths

studied.

Chapter 2 demonstrated that Lacuna vincta uses algae for both a habitat and a

food source, and there are feeding preferences shown by L. vincta on different algal

species. However, structures and secondary metabolites of algae may play an important

role in food selection o f L. vincta (Figs. 2.1, 2.2). When dried and fresh algae were given

to the snails, there was a difference in the preference range of the algae by the snails.

Lacuna vincta consumed primarily freshAntithamnionella floccosa, followed by Ulva

113

Reproduced with permission of the copyright owner. Further reproduction prohibited without permission. lactnca, Laminaria saccharina, and Chordaria Jlagelliformis (Fig. 2.1). In the dried-

algal assays,L. vincta preferred Chondrus crispus and L. saccharina (Fig. 2.2), which

may be due to loss of some secondary compound in seaweeds when heated and dried.

Lacuna vincta can be found on a variety of algae; however, not all algae are

suitable and high in nutrition for the growth of L. vincta. The growth rate of snails in all

three size classes fed on Laminaria saccharina tended to be higher than the ones fed on

other algal species (Figs. 3.4-3.6), particularly for the largest size class (Fig. 3.6).

Johnson and Mann (1986) suggested that Laminaria spp. had a higher nutritional quality

than other algal food. In Chapter 2, L. vincta consumed high amounts of

Antithamnionella Jloccosa. However, the results from Chapter 3 showed that the growth

of the snails fed on A. Jloccosa was not as high as L. saccharina or Ulva lactuca. Micro

and filamentous algae are softer and easier for herbivores to graze on (Steneck and

Watling, 1982). Antithamnionella Jloccosa is a soft, bushy, and filamentous alga, which

is more facilitative for L. vincta to graze on in a limited time. However, the nutrition in

this alga might not be as high as other algal species.

Laminaria spp. is a preferred food of Lacuna vincta, and the largest individuals

tend to be found associated with this kelp (Chapter 1), at least in part due to its high

nutritional content (Martel and Chai, 1991; Chapter 3). Grazing by L. vincta has been

implicated as having a negative impact on Laminaria populations (Fralick et al., 1974).

Membranipora membranacea, which first appeared in 1987 (Berman et al., 1992), also

occupies Laminaria blades and has a negative impact on kelp population (Lambert et al.,

1992). Coexistence in the same habitat may have a negative impact on organisms either

directly or indirectly and may create intraspecific and interspecific competition for a

114

Reproduced with permission of the copyright owner. Further reproduction prohibited without permission. resource (Jensen, 1985; Jensen and Kristensen, 1990). When M. membranacea covers

the surface of a kelp blade, the available space that L. vincta can utilize for food

decreases. Cover byM. membranacea increases the density of snails in limited open

areas (Fig. 4.1b). The results from the intraspecific competition experiment suggest that

high densities of snails in a limited area can have a negative influence on the growth of

the snails (Fig. 4.6). Overall, M. membranacea appears to have a negative impact on L.

vincta populations occupyingLaminaria spp. The overgrowth of M. membranacea on

kelps reduces the grazing space for L. vincta and creates intraspecific and interspecific

competition for space on kelp blades. The competition between these two species may

also have a negative impact on M. membranacea populations occupyingLaminaria

saccharina, which may be facilitating the shift of this bryozoan to new algal substratum.

The results from field sampling showed that the spread of Codium fragile ssp.

tomentosoides can have a negative impact on snail populations (Chapters 1, 5). The

average total density of the snails at Star Island, a site dominated by C.fragile ssp.

tomentosoides, was less than half that of at Cape Neddick, where dominated by

Laminaria saccharina (Chapter 1). The average size of the snails at Cape Neddick was

smaller than at Star Island (Chapter 1, Fig. 5.1b) that may imply that there were more

snails recmiting at Cape Neddick as compared to Star Island. In addition, the growth of

the snails of all three size classes was higher when fed on L. saccharina versus C.fragile

ssp. tomentosoides (Fig 5.3).

If the spread of Codium fragile ssp. tomentosoides continues in coastal subtidal

communities such as Cape Neddick, it may change algal composition from a canopy

dominated by Laminaria saccharina to one dominated by C.fragile ssp. tomentosoides

115

Reproduced with permission of the copyright owner. Further reproduction prohibited without permission. that may lead to a decline in Lacuna vincta populations, and it may also affect and

decrease the populations in higher trophic levels that consume L. vincta as a major food

source.

Two introduced species, Membranipora membranacea and Codium fragile ssp.

tomentosoides, have an apparent negative impact on Lacuna vincta populations. The

parallel success of these two introduced species in subtidal communities may lead to a

higher level of negative impact on L. vincta populations. As preferred habitat and food in

the kelp canopy is reduced by bryozoan coverage and/or replacement of kelps by C.

fragile ssp. tomentosoides, L. vincta may switch to alternative algal food sources such as

Ulva lactuca and Chordaria flagelliformis. Some of these algal species are annuals

(Mathieson and Hehre, 1986) and the increased herbivore pressure may have a cascading

effect of altering species composition or relative abundance that would further impact

both benthic community composition and the role of L. vincta.

116

Reproduced with permission of the copyright owner. Further reproduction prohibited without permission. List of References

Berman, J., L. Harris, W. Lambert, M. Buttick, and M. Dufresne. 1992. Recent invasions of the Gulf of Maine: Three case histories. Conservation Biology. 6:435-441.

Buschmann, A. H. 1990. Intertidal macroalgae as refuge and food for Amphipoda in central Chile. Aquatic Botany. 36:237-245.

Carlton, J. T. 1996. Pattern, process, and prediction marine invasion ecology. Biological Conservation. 78:97-106.

Carlton, J. T. and J. A. Scanlon. 1985. Progression and dispersal of an introduced alga: Codium fragile spp. tomentosoides (Chlorophyta) on the Atlantic Coast of North America. Botanica Marina. 28:155-165.

Ceccherelli, G., L. Paizzi, and F. Cinelli. 2000. Response of the non-indigenous Caulerpa racemosa (Forsskal) J. Agardh to the native seagrass Posidonia oceanica (L.) Delile: effect of density of shoots and orientation of edges of meadows. Journal of Experimental Marine Biology and Ecology. 243: 227-240.

Chapman, A. R. O. and J. S. Craigie. 1977. Seasonal growth in Laminaria longicruris: Relations with dissolved inorganic nutrients and internal reserves of nitrogen. Marine Biology. 197-205.

Chapman, A. S. 1999. From introduced species to invader: what determines variation in the success ofCodium fragile ssp. tomentosoides (Chlorophyta) in the North Atlantic Ocean? Helgo lander Meeresuntersuchungen. 52: 277-289.

Chavanich, S. and L. G. Harris. 2000. Potential impact of the introduced bryozoan, Membranipora membranacea, on the subtidal snail, Lacuna vincta, in the Gulf of Maine. In Pederson, J., (ed.), Proceeding of Marine Bioinvasions Conference, Massachusetts Institute of Technology, (in press)

Clark, K. B. and D. DeFreese. 1987. Population ecology of Caribbean Ascoglossa (Mollusca: Opisthobranchia): a study of specialized algal herbivores. American Malacological Bulletin. 5:259-280.

D’ Antonio, C. 1985. Epiphytes on the rocky intertidal red algaRhodomela larix (Turner) C. Agardh: Negative effects on the host and food for herbivores? Journal of Experimental Marine Biology and Ecology. 86:197-218.

117

Reproduced with permission of the copyright owner. Further reproduction prohibited without permission. Dawes, C. J. 1998. Marine Botany. John Wiley & Sons, Inc., New York. 480 pp.

Duffy, J. E. and M. E. Hay. 1991. Food and shelter as determinants of food choice by an herbivorous marine amphipod. Ecology. 72:1286-1298.

Duffy, J. E. and M. E. Hay. 1994. Herbivore resistance to seaweed chemical defense: the roles of mobility and predation risk. Ecology. 75: 1304-1319.

Ebling, F. J., J. A. Kitching, R. D. Purchon, and R. Bassindale. 1948. The ecology of the Lough Ine rapids with special reference to water currents. Journal of Animal Ecology. 17:223-244.

Fralick, R. A. and A. C. Mathieson. 1972. Winter fragmentation of Codium fragile (Suringar) Hariot ssp. tomentosoides (van Goor) Silva (Chlorophyceae, Siphonales) in New England. Phycologia. 11: 67-70.

Fralick, R. A. and A. C. Mathieson. 1973. Ecological studies ofCodium fragile in New England, USA. Marine Biology. 19:127-132.

Fralick, R. A., K. W. Turgeon, and A. C. Mathieson. 1974. Destruction of kelp populations byLacuna vincta (Montagu). Nautilus. 88:112-114.

Grosholz, E. D., G. M. Ruiz, C. A. Dean, K. A. Shirley, J. L. Maron, and P. G. Connors. 2000. The impact of a nonindigenous marine predator in a California bay. Ecology. 81:1206-1224.

Hacker, S. D. and R. S. Steneck. 1990. Habitat architecture and the abundance and body-size-dependent habitat selection of a phytal amphipod. Ecology. 71:2269-2285.

Harris, L. G. and A. C. Mathieson. 2000. Patterns of range expansion, niche shift, and predator acquisition in Codium fragile ssp. tomentosoides and Membranipora membranacea in the Gulf of Maine. In Pederson, J., (ed.), Proceeding of Marine Bioinvasions Conference, Massachusetts Institute of Technology, (in press)

Harris, L. G. and M. Tyrrell. 2001. Changing community states in the Gulf of Maine: synergism between invaders, overfishing and climate changes. Biological Invasions, (in press)

Hay, M. E., J. E. Duffy, and W. Fenical. 1990. Host-plant specialization decreases predation on a marine amphipod: an herbivore in plant’s clothing. Ecology. 71:733-743.

Hay, M. E., J. E. Duffy, W. Fenical, and K. Gustafson. 1988. Chemical defense in the seaweed Dictyopteris delicatula: differential effects against reef fishes and amphipods. Marine Ecology Progress Series. 48:185-192.

118

Reproduced with permission of the copyright owner. Further reproduction prohibited without permission. Hay, M. E. and W. Fenical. 1988. Marine plant-herbivore interactions: The ecology of chemical defense. Annual Review of Ecology and Systematics. 19:111-145.

Hay, M. E., J. R. Pawlik, J. E. Duffy, and W. Fenical. 1989. Seaweed-herbivore- predator interactions: Host-plant specialization reduces predation on small herbivores. Oecologia. 81:418-427.

Heck, K. L. and G. S. Wetstone. 1977. Habitat complexity and invertebrate species richness and abundance in tropical seagrass meadows. Journal of Biogeography. 4:135-142.

Hicks, G. R. F. 1986. Meiofauna associated with rocky shore algae. Pages 36-5 6 in P. G. Moore and R. Seeds, eds. The Ecology of Rocky Coasts: Essays Presented to J. R. Lewis, Columbia University Press, New York.

Holomuzki, J. R. and T. M. Short. 1988. Habitat use and fish avoidance behaviors by the stream-dwelling isopod Lirceus fontinalis. Oikos. 52: 79-86.

Jensen, K. T. 1985. The presence of the bivalve Cerastoderma edule affects migration, survival, and reproduction of the amphipodCorophium volutator. Marine Ecology Progress Series. 25: 269-277.

Jensen, K. T. and L. D. Kristensen. 1990. A field experiment on competition between Corophium volutator (Pallas) and Corophium arenarium Crawford (Crustacea:Amphipoda): effects on survival, reproduction, and recruitment. Journal of Experimental Marine Biology and Ecology. 137:1-24.

Johnson, C. R. and K. H. Mann. 1986. The importance of plant defense abilities to the structure of subtidal seaweed communities: the kelpLaminaria longicruris de la Palaie survives grazing by the snailsLacuna vincta (Montagu) at high population densities. Journal of Experimental Marine Biology and Ecology. 97:231-267.

Kuris, A. M. and C. S. Culver. 1999. An introduced sabellid polychaete pest infesting cultured abalones and its potential spread to other California gastropods. Invertebrate Biology. 118:391-403.

Lambert, W. J. 1990. Population ecology and feeding biology of nudibranchs in colonies of the hydroid Obelia genicidata. Ph.D. Dissertation, University of New Hampshire, Durham, New Hampshire.

Lambert, W. J., P. S. Levin, and J. Berman. 1992. Changes in the structure of a New England (USA) kelp bed: the effect of an introduced species? Marine Ecology Progress Series. 88: 303-307.

Leber, K. M. 1985. The influences of predatory decapods, refuge and microhabitat selection on seagrass communities. Ecology. 66:1951-1964.

119

Reproduced with permission of the copyright owner. Further reproduction prohibited without permission. Little, C. and J. A. Kitching. 1996. The Biology o f Rocky Shores. Oxford University Press, Oxford, England. 240 pp.

Lobban, C. S. and P. J. Harrison. 1994. Seaweed Ecology and Physiology. Cambridge University Press, Cambridge. 366 pp.

Lubchenco, J. 1978. Plant species diversity in a marine intertidal community: importance of herbivore food preference and algal competitive abilities. American Naturalist. 112:23-39.

Lubchenco, J. 1983. Littorina and Fuciis: effects of herbivores, substratum heterogeneity, and plant escapes during succession. Ecology. 64:1116-1123.

Maney, E. J. and J. P. Ebersole. 1990. Continuous reproduction and episodic recruitment ofLacuna vincta (Montagu, 1803) in the Gulf of Maine. The Veliger. 33:215-221.

Martel, A. and F. S. Chai. 1991. Oviposition, larval abundance, in situ larval growth, and recruitment of the herbivore gastropod Lacuna vincta in kelp canopies in Barkely Sound, Vancouver Island (Britain Columbia). Marine Biology. 110: 237-247.

Martel, A. and T. Diefenbach. 1993. Effects of body size, water current and microhabitat on mucous-threat drifting in post-metamorphic gastropods Lacuna spp. Marine Ecology Progress Series. 99:215-220.

Mathieson, A. C. 1979. Vertical distribution and longevity of subtidal seaweeds in northern New England USA. Botanica Marina. 30: 511-520.

Mathieson, A. C. and E. J. Hehre. 1986. A synopsis of New Hampshire seaweeds. Rhodora. 88:1-139.

McBane, C. D. and R. A. Croker. 1983. Animal-algal relationships of the amphipod Hyale nilssoni (Rathke) in the rocky intertidal. Journal of Crustacean Biology. 3:592-601.

Menge, B. A. 1972. Foraging strategy o f a seastar in relation to actual prey availability and environmental predictability. Ecological Monographs. 42:25-50.

Nelson, W. G. 1981. Experimental studies of decapod and fish predation on seagrass macrobenthos. Marine Ecology Progress Series. 5:141-149.

Nicotri, M. E. 1980. Factors involved in herbivore food preference. Journal of Experimental Marine Biology and Ecology. 42: 13-26.

120

Reproduced with permission of the copyright owner. Further reproduction prohibited without permission. Norton, T. A., S. J. Hawkins, N. L. Manley, G. A. Williams, and D. C. Watson. 1990. Scraping a living: a review of littorinid grazing. Hydrobiologia. 193: 117-138.

Parker, I. M., D. Simberloff, W. M. Lonsdale, K. Goodell, M. Wonham, P. M. Kareiva, M. H. Williamson, B. Von Holle, P. B. Moyle, J. E. Byers, and L. Goldwasser. 1999. Impact: toward a framework for understanding the ecological of invaders. Biological Invasions. 1:3-19.

Paul, V. J. and M. E. Hay. 1986. Seaweed susceptibility to herbivory: chemical and morphological correlates. Marine Ecology Progress Series. 33: 255-264.

Prince, J. S. 1988. Sexual reproduction inCodium fragile spp. tomentosoides (Chlorophyceae) from the northeast coast of North America. Journal of Phycology. 24: 112-114.

Prince, J. S. and W. G. LeBlanc. 1992. Comparative feeding preference of Strongylocentrotus droebachiensis (Echinoidea) for the invasive seaweed Codium fragile ssp. tomentosoides (Chlorophyceae). and four other seaweeds. Marine Biology. 113:159-163.

Raffaelli, D. and S. Hawkins. 1996. Intertidal Ecology. Chapman & Hall, London. 356 pp.

Rasmussen, E. 1973. Systematics and ecology of the Isefjord marine fauna. Ophelia. 11:1-495.

Russel-Hunter, W. D. and R. F. McMahon. 1975. An anomalous sex-ratio in the sublittoral marine snail Lacuna vincta Turton, from near Woods Hole. Nautilus 89:14-16.

Ryland, J. S. 1970. Brvozoans. Hutchinson University and Co., London, England. 175 pp.

Shacklock, P. F and G. B. Croft. 1981. Effect of grazers on Chondrus crispus in culture. Aquaculture. 22:331-342.

Sloane, J. F., F. J. Ebling, J. A. Kitching, and S. L. Lilly. 1957. The ecology of the Lough Ine rapids with special reference to water currents Part V. The sedentary fauna of the laminarian algae in the Lough Ine area. Journal of Animal Ecology. 26:197-211.

Smith, D. A. S. 1973. The population biology ofLacuna pallidula (De Costa) and Lacuna vincta (Montagu) in Northeast England. Journal of the Marine Biological Association of the United Kingdom. 53:493-520.

Sousa, W. P. 1979. Experimental investigations of disturbance and ecological

121

Reproduced with permission of the copyright owner. Further reproduction prohibited without permission. succession in a rocky intertidal algal community. Ecological Monographs. 49:227-254.

Sousa, W. P., S. C. Schroeter, and S. D. Gaines. 1981. Latitudinal variation in intertidal algal community structure: the influence of grazing and vegetative propagation. Oecologia. 48: 297-307.

Southgate, T. 1982. A comparative study Lacunaof vincta and Lacuna pallidula (Gastropoda: Prosobranchia) in littoral algal turfs. Journal of Mollucan Study. 48: 302-309.

Steneck, R. S. and L. Watling. 1982. Feeding capabilities and limitation of herbivorous molluscs: a functional group approach. Marine Biology. 68:299-319.

Stohlgren, T. J., D. Binkley, G. W. Chong, M. A. Kalkhan, L. D. Schell, K. A. Bull, Y. Otsuki, G. Newman, M. Bashkin, and Y. Son. 1999. Exotic plant species invade hot spots of native plant diversity. Ecological Monographs. 69:25-46.

Systat. 1997. Statistics: Systat 7.0 for Windows. SPSS Inc., Chicago, Illinois. 751pp.

Sze, P. 1998. A Biology of the Algae. WCB/McGraw-Hill Inc., Boston, Massachusetts. 278 pp.

Thomas, M. L. H. and F. H. Page. 1983. Grazing by the gastropod, Lacuna vincta, in the lower intertidal area at Musquash Head, New Brunswick, Canada. Journal of the Marine Biological Association of the United Kingdom. 63: 725-736.

Trowbridge, C. D. 1995. Establishment of the green alga Codium fragile spp. tomentosoides on New Zealand rocky shores: current distribution and invertebrate grazers. Journal of Ecology. 83:949-965.

Viejo, R. M. and J. Arrontes. 1992. Interaction between mesograzers inhabiting Fucus vesiculosus in northern Spain. Journal of Experimental Marine Biology and Ecology. 162:97-111.

Villalard-Bohnsack, M. 1995. Illustrated key to the seaweeds of New England. A Publication of the Rhode Island Natural History Survey, Kingston, RI. 144 pp.

Williams, C. T. and L. G. Harris. 1998. Growth of juvenile green sea urchins on natural and artificial diets. In Mooi, R. and M. Telford., (ed.), Proceeding of the ninth international echinoderm conference, San Francisco, California, USA. 887-892.

Wilson, K. A., K. W. Able, and K. L. Heck. 1990. Predation rates on juvenile blue crabs in estuarine nursery habitats: evidence for the importance of macroalgae (Ulva lactuca). Marine Ecology Progress Series. 58:243-251.

122

Reproduced with permission of the copyright owner. Further reproduction prohibited without permission. Wonham, M. J., J. T. Carlton, and G. M. Ruiz. 2000. Fish and ships: relating dispersal frequency to success in biological invasions. Marine Biology. 136:1111-1121.

Yoshioka, P. M. 1982. The role of planktonic and benthic factors in the population dynamics of the bryozoanMembranipora membranacea. Ecology. 63:457-468.

123

Reproduced with permission of the copyright owner. Further reproduction prohibited without permission.