FEEDING ECOLOGY AND BIOTURBATION:DETERMINING THE ECOLOGICAL ROLE OF EUSPIRA

LEWISII

by

Nicola Ashley CookB.Sc., University of British Columbia, 2001

THESIS SUBMITTED IN PARTIAL FULFILLMENT OFTHE REQUIREMENTS FOR THE DEGREE OF

MASTER OF SCIENCE

In theDepartment

ofBiological Sciences

© Nicola Ashley Cook 2008

SIMON FRASER UNIVERSITY

Spring 2008

All rights reserved. This work may not bereproduced in whole or in part, by photocopy

or other means, without permission of the author.

Name:

Degree:

Title of Thesis:

APPROVAL

Nicola Ashley Cook

Master of Science

Feeding ecology and bioturbation: Determining the ecological role ofEuspira lewisii

Examining Committee:

Chair: Dr. F. Law, Professor

Dr. L. Bendell-Young, Professor, Senior SupervisorDepartment of Biological Sciences, S.F.V.

Dr. M. Hart, Associate ProfessorDepartment of Biological Sciences, S.F.V.

Dr. I. Cote, ProfessorDepartment of Biological Sciences, S.F.V.Public Examiner

27 February 2008Date Approved

11

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Revised: Fall 2007

ABSTRACT

The burrowing, predatory snail Euspira lewisii is being removed from

intertidal habitats due to its reputation as an economically damaging species to

shellfish aquaculture. Here, the objectives were to examine feeding ecology and

determine the functional role of a poorly understood species. Feeding

experiments and shell assemblages showed distinct prey preferences, avoidance

of the commercially valuable Manila clam, a low, species-dependent feeding rate

and a limited yearly consumption of the clam population. Exclusion experiments

demonstrated increased sediment compaction, silt content and nutrient

accumulations and decreased water content when E. lewisii is absent.

Homogenized biological communities in cages resembled less diverse areas.

These results demonstrate that E. lewisii is a low impact predator and acts as an

ecosystem engineer to the benefit of other organisms. These results can be used

to advise shellfish growers that control measures are not necessary and they will

benefit from the maintenance of a healthy ecosystem.

Keywords:

Euspira lewisii; intertidal; community structure and function; feeding ecology;bioturbation; shellfish aquaculture

iii

DEDICATION

To Chris, for your tireless love and support. You inspire me to take my

dreams lito the moon and back".

iv

ACKNOWLEDGEMENTS

I am forever grateful to Leah Bendell-Young for inspiring this work and for her

role in supervising and funding this project, and to Mike Hart for his enthusiasm and

constructive advice along the way. I would like to acknowledge Isabelle Cote for making

me challenge myself during my defence and for the helpful comments she provided. A

huge thank you goes to Tracey L'Esperance for her assistance in the field. I am so

grateful to our Hornby Island family, Frances and Garth Millan, for their role in finding

and providing places to live.

Thank you to Carolyn Allen for her interest in and contributions to parts of this

project. Jonathan Whiteley, Chris Kowalchuk, Bruno L'Esperance, Carlos Palomera,

Jenna Thomson, Mike White, Charlotte Voss and John Driftmier volunteered their time to

help in the field. Wayne Kowalchuk provided invaluable help building equipment and

preparing materials for the field. Many thanks to Jonathan Whiteley, Tracey

L'Esperance, Carolyn Duckham, Carlos Palomera, Jeff Christie, Joline Widmeyer, Wade

Brunham and all the lab-mates who made my time at SFU fabulous and for supporting

me through all of my graduate school adventures.

This work would not have been possible without the unwavering love, support,

and encouragement of my family, the Cooks and the Kowalchuks, who have taught me

to live well, laugh often, and love much. Finally, the biggest thanks goes out to Chris for

encouraging me to challenge myself in everything I do, for the love, support, guidance,

and patience along the way, and for being there to share in all the adventures.

v

TABLE OF CONTENTS

Approval ii

Abstract iii

Dedication iv

Acknowledgements v

Table of Contents vi

List of Figures viii

List of Tables x

Chapter 1 Introduction 11.1 Study Rationale 2

1.1.1 Community Structure and Function 31.1 .1 Predation 61.1.2 Bioturbation 91.1.3 Biology of Euspira lewisii 13

1.2 Research Objectives 151.3 Literature Cited 15

Chapter 2 Using Prey Preferences and Feeding Rates to Examinethe Influence of Euspira lewisii on Bivalve Communities 20

2.1 Abstract 212.2 Introduction 222.3 Methods 24

2.3.1 Study Areas 242.3.2 Feeding Experiments 242.3.3 Density and Drill Collection 272.3.4 Community Impacts 29

2.4 Results 292.4.1 Prey Preference 292.4.2 Feeding Rates 302.4.3 Bivalve and E. lewisii Density and Abundance 312.4.4 Shell Assemblage Prey Preference 352.4.5 Impacts of E. lewisii Predation on Intertidal Clam

Communities 372.5 Discussion 40Acknowledgments 472.6 Literature Cited 47

vi

Chapter 3 Effects of Bioturbation by Lewis's Moon Snail (Euspiralewisii) on Sediment Properties and Biological Communities inBritish Columbia 51

3.1 Abstract 523.2 Introduction 523.3 Methods 56

3.3.1 Study Areas 563.3.2 Cage Design 573.3.3 Sediment Characteristics 593.3.4 Sediment Chemistry 603.3.5 Biological Community 613.3.6 Analyses 61

3.4 Results 623.4.1 Physical Characteristics of the Sediment 623.4.2 Grain Size Analyses 633.4.3 Chemical Properties of the Sediment. 653.4.4 Biological Community 673.4.5 Control Cage Impacts 70

3.5 Discussion 70Acknowledgments 743.6 Literature Cited 75

Chapter 4 Conclusions and Recommendations 784.1 Conclusions 794.2 Future Work 804.3 Recommendations 81

Appendices 83Appendix A: Exclusion Experiment By-Tide-Height Results 83Appendix B: Exclusion Experiment Supplementary Data 93

vii

Figure 2.1.

Figure 2.2.

Figure 2.3.

Figure 2.4.

Figure 2.5.

Figure 2.6.

Figure 2.7.

Figure 3.1.

Figure 3.2.

Figure 3.3.

LIST OF FIGURES

E. lewisii (e) prey preference (± 95% C.I.). The dashed linerepresents zero preference (0.33). Values above the dashedline indicate prey preference, values below indicateavoidance. Where the C.1. does not overlap the line,preference is significant. 30Medians and interquartile ranges of the feeding rates of E.lewisii on P. staminea, V. philippinarum and N. obscurata inclams/day/snail for each species 31Density of clam species in number of individuals per m2 forFillongley (A) and Shingle Spit (B) 33The proportion of drilled shells collected from Fillongley (A)and Shingle Spit (B) compared to the proportion of clamsavailable at each site (H-high, M-mid, L-Iow, T-total) 37Electivity coefficients for E. lewisii feeding on the clampopulations in the high (A), mid (B), low (C) and all threezones (D) at Fillongley. Negative values indicate avoidance,while positive values indicate preference 38Electivity coefficients for E. lewisii feeding on the clampopulations in the high (A), mid (B), low (C) and all threezones (D) at Shingle Spit. Negative values indicate avoidance,while positive values indicate preference 39The number of clams consumed by E. lewisii at the rate of0.09 clams/day at a density of 0.22 snails/m2 in 1 month, 6months and over 12 months compared to the total number ofclams available at Fillongley and Shingle Spit. 40Map showing the location of the study sites on Denman andHornby Islands (Based onhttp://atlas.nrcan.gc.ca/site/english/maps/reference/outlinecanada/canada01,http://atlas.nrcan.gc.ca/site/english/maps/reference/outlineprov_terr/bc_outline) 58Compressive strength of the sediments at each study siteunder each treatment (Medians, error bars representinterquartile range) 62

Water content of the sediments at each study site under eachtreatment (Medians, error bars represent interquartile range) 63

viii

Figure 3.4. Percentages of gravel, coarse sand, fine sand, and silt ateach site under each treatment (Medians, error bars representinterquartile range) 64

Figure 3.5. Nutrient concentrations of ammonium, carbon andphosphorous for each treatment at each study site (Medians,error bars represent interquartile range) 66

Figure 3.6. Total invertebrate species richness for each tide height at bothsites. * indicates a significant result (Medians, error barsrepresent interquartile range) 67

Figure 3.7. Tree diagram illustrating the Bray-Curtis similarities for theFillongley community at all tide heights under each treatment.H =high, M =mid, L =low. E =Exclusion, CA =Control area,CC =Control cage 68

Figure 3.8. Tree diagram illustrating the Bray-Curtis similarities for theShingle Spit community at all tide heights under eachtreatment. H =high, M =mid, L =low. E =Exclusion, CA =Control area, CC =Control cage 69

ix

LIST OF TABLES

Table 2.1. Density of E. lewisii at Fillongley and Shingle Spit indensity/m2 ± 95% C.1. and in total abundance in the surveyarea ± 950/0 C.I 33

Table 2.2. Total clam abundance by species at Fillongley and ShingleSpit for each stratum ± 95% C.1. 34

Table 2.3. Raw numbers of drilled shells collected in each stratum ateach site with totals 35

Table 3.1. Length of the three tide strata at each site 57

Table 3.2. Summary of the non-parametric Kruskal-Wallis analyses onthe physical properties of the sediments between treatmentsat both sites. * indicates a significant result and ** indicates amarginally significant result. 63

Table 3.3. Summary of the non-parametric Kruskal-Wallis analyses onthe grain size analyses between treatments at both studysites. * indicates a significant result and ** indicates amarginally significant result. 65

Table 3.4. Summary of the non-parametric Kruskal-Wallis analyses onthe sediment nutrient characteristics between treatments atboth sites. * indicates a significant result and ** indicates amarginally significant result. 66

x

CHAPTER 1 INTRODUCTION

1.1 Study Rationale

The loss of biodiversity has come to the forefront of science recently for

both scientists and the public. As the human population grows, more demands

are put on our coastal and marine ecosystems that result in alterations in marine

communities, habitat loss and bioinvasions. The most important part of this issue

is to try to link and understand the interplay between the function and the

structure of an ecosystem as we lose the structure in the form of biodiversity.

Over 70% of the sea floor is soft-sediment habitats and hence can be

considered one of the more important habitat types (Lohrer et al. 2004). These

habitats provide nurseries, are sites for nutrient exchange with the water column,

and provide food for marine organisms from all levels of the food chain. It is

imperative to fill knowledge gaps and gain understanding on the role of individual

species in these functions.

, studied how Euspira lewisii (Lewis's moon snail), an intertidal, soft­

sediment predator of bivalves, influences the populations of its prey species and

other species that share its habitat in British Columbia (B.C.), Canada. The goal

of the work is to determine the role of this species in structuring communities as

both a predator and a bioturbator.

This work also allows the opportunity to study a species (E. lewisiI) that is

thought to have negative impacts on shellfish aquaculture (Bernard 1967). The

B.C. Shellfish Growers Association (BCSGA) (2002) suggests that E. lewisii is a

predator to the commercially valuable Manila clam, Venerupis philippinarum. The

BCSGA Code of Practice (2002) states:

2

"A few select species (including starfish, Japanese drills, moon

snails, crustaceans, and some birds) can have significant economic

impact depending on their frequency and the type of farm operation.

Farmers are entitled to take reasonable steps to prevent the destruction of

their crops by pests and predators."

This has led to shellfish farmers actively removing E. lewisii from the intertidal

zone. This is of some concern because very little is known about the role or

function of E. lewisii in the intertidal community. Thus, information generated by

this study will fill the knowledge gap and can be used to advise shellfish

aquaculture activities and ensure a sustainable industry.

1.1.1 Community Structure and Function

A community is made up of a group of populations that live and interact in

a given area (Krebs 2001). Communities have a set of five characteristics unique

to this level of organization that help to study and understand them. Krebs (2001)

defines these characteristics as growth form and structure, diversity, dominance,

relative abundance and trophic structure. Community structure can be defined as

how the populations in a given area are organized (Krebs 2001). The structure of

a community can be physical or biological. Species composition and abundance,

temporal changes, and relationships between species are all involved in the

biological structure of a community. Species composition and abundance can be

put under the umbrella of biodiversity. Predation, competition, herbivory, and

biological disturbance are the relationships that influence the structure of a

community and may influence biodiversity at a local scale.

3

Organisms living in sediments create much of the structure in soft­

sediment habitats (Thrush & Dayton 2002). Burrows, tubes, mounds and other

alterations to the sediment comprise this physical structure. Organisms that

provide this habitat structure often have important roles in sequestering and

recycling processes essential to ecosystem function (Thrush & Dayton 2002).

Small-scale disturbances by benthic feeding organisms can increase 3-D

structure of habitat (Thrush & Dayton 2002). The physical and biological

structures are closely related and strongly influence each other.

Physical and biological attributes also influence the function of a

community, i.e., how energy and nutrients are processed within a community.

Nutrient cycling and primary and secondary production are all ecosystem

functions (Krebs 2001). How an ecosystem functions is in part an outcome of the

metrics that define that structure such as species richness and evenness

(Raghukumar & Anil 2003). Soft-sediment marine organisms have functional

roles crucial to many ecosystem processes: protein supply to ecosystems,

sediment stability, water column turbidity, nutrient and carbon processing (Thrush

and Dayton 2002).

It is important to recognize that many recent studies have focused on the

importance of maintaining biodiversity and function in marine systems. Previous

work has shown that decreased ecosystem function occurs when there is a

decrease in biodiversity (Lohrer et al. 2004). Heterogeneity is important in

ecosystem function and makes for stable communities (Thrush & Dayton 2002).

Losing one species could have large impacts on marine systems including

4

function (Lohrer et al. 2004). Duarte (2000) showed that similar seagrass species

may have different functions, so the species involved in each ecosystem function

are important, not just the number of species. Removing ecosystem engineers

was found to influence both biological diversity and ecosystem function (Coleman

& Williams 2002).

When trying to understand the interplay between ecosystem structure and

function, the contribution of individual species to a specific function is difficult to

assess (Lohrer et al. 2004). For example, Chalcroft & Resetarits (2003) found

that six different predators on anuran larvae each had different impacts on their

measured response variables of prey biomass, total prey number, prey species

richness and prey evenness. They concluded that grouping species by function

might lead to poor understanding of communities and that losing one predator

species might result in loss of ecosystem function but it is difficult to differentiate

each predator's role in this system. Within the intertidal region, E. lewisii can

reach large populations, but unique aspects of this species are its relative size,

mobility and deeper burial depth relative to other invertebrates within the same

region. Hence, it may be possible due to these attributes to discern the role this

species has on ecosystem function, specifically in the intertidal. This becomes of

acute importance, in light of the culling of the moon snail from beaches.

Predators and predation activities are likely to influence the structure and

function of their community (Thrush & Dayton 2002). The manual removal of E.

lewisii has been recommended without knowing the functional role of the moon

snail in the intertidal. For any system, biodiversity is important as is

5

understanding the role of each species in ecosystem processes (RClghkumar &

Anil 2003). Increasing concern about alterations to diversity of various life forms

makes it necessary now for management to understand the relation between

biodiversity and ecosystem functioning in our coastal and offshore waters

(Raghkumar & Anil 2003).

1.1.1 Predation

Moon snails are predators on clams in the intertidal. The impacts of E.

lewisii as a predator on clam populations are thought to be quite large

demonstrated by their inclusion on the SCSGA (2002) list of species of economic

threat. Several studies have shown that predation influences the abundance,

composition, distribution, and productivity of infaunal prey species (Seal 2006;

Seal et al. 2001; Como et al. 2004; Gee et al. 1985; Palomo et al. 2003; Peitso et

al. 1994; Quijon & Snelgrove 2005; Wiltse 1980). In soft-sediment communities,

in the absence of a predator Menge et al. (1994), Peterson (1979), and Wiltse

(1980) found that prey biomass and abundance increased. In Maine, predation

was shown to be the most important factor affecting the survival of juvenile clams

(Seal 2006). Under severe predation pressures, the densities of all the prey

populations would decrease, leading to a decrease in diversity in that community

(Virnstein 1977).

However, limited studies have been conducted on the basic feeding

ecology of E. lewisii and its impacts on intertidal clam populations are unclear.

The response of a natural community to predation is influenced by the

relationship between prey preferences and the abundance, competitive abilities

6

and rates of increase of the prey species (Wiltse 1980). To best understand the

functioning of intertidal communities and the role of a predator in those

communities, a knowledge of the patterns of foraging activity and rates of feeding

of the major predators is crucial (Moran 1985; Thiel et al. 2001). Higher feeding

rates lead to higher community impacts (DeGraaf & Tyrrell 2004). Most predators

increase feeding rate as the density of prey increases, but feed at a decelerating

rate, reaching a plateau when prey are very dense (Moran 1985; Thiel et al.

2001). Other predators reduce their prey intake when offered low numbers of

preferred prey (Thiel et al. 2001). Species and size of prey also affect feeding

rates (DeGraaf & Tyrrell 2004; Moran 1985; Thiel et al. 2001). Abiotic conditions

such as temperature, tide height, intensity of wave action and duration of

submersion affect feeding rates, as do other predator activities such as breeding

or sheltering (Moran 1985; Thiel et al. 2001). Predation is often most intense in

warmer temperatures (Weissberger 1999). The physical conditions of the habitat

also impact predation: in a physically stressful environment, prey populations

prioritize adapting to the physical regime over adapting to biological interactions

(Byers 2005; Virnstein 1977).

The effects of predation decrease when the prey species is able to avoid

or escape predation (Byers 2002; Smith et al. 1999; Tallqvist 2001). The three­

dimensional nature of soft-sediment habitats allows some burrowing species to

escape predators by burrowing deep into the sediment while other species, such

as the razor clam, display elaborate escape responses (Byers 2002; Schneider

1982; Smith et al. 1999). With all these factors influencing the intensity of

7

predation, it is difficult to make generalizations about the effects of predation on

infaunal communities. Predation needs to be understood to reliably evaluate

ecological impact of predatory species (Savini & Occhipinti-Ambrogi 2006).

Not all effects of predation are negative. Predator effects on prey

populations depend on the intensity of predation in that community (Palomo et a!.

2003; Virnstein 1977; Wiltse 1980). When predation pressure is low, predators

can reduce the number of the dominant species that leads to the competitive

release of other species (Ambrose 1984; Gee et a!. 1985; Quijon & Snelgrove

2005). Species densities may even be brought to a level below which competitive

exclusion occurs (Virnstein 1977). Predators feeding on discrete areas of the

intertidal would result in patches in the community that are at various stages of

succession increasing community diversity (VanBlaricom 1982).

It is important to note that most soft-sediment predation studies have

mainly focused on epibenthic predators such as birds, crabs and fish. It must be

considered that many benthic infauna are themselves predators, and can

influence abundances of other infaunal species in their own ways. Predatory

infauna may influence abundances of other infaunal organisms by preying on

adults, juveniles, or larvae, or by disturbing the sediment surface and reducing

larval settlement and juvenile survivorship (Ambrose 1984). Infaunal predators

may cause more damage to prey populations by injuring prey rather than

consuming them (Gee et a!. 1985). These predators are usually small,

inconspicuous and commercially important (Ambrose 1991). Their smaller size

8

tends to lead to lower feeding rates, which suggest that the role of infaunal

predators is less than that of epibenthic predators (Ambrose 1991).

1.1.2 Bioturbation

Bioturbation is the mixing of sediment from the action of infauna, epifauna,

fish and mammals (Biles et al. 2002). Benthic infauna are major bioturbators of

the sediment in marine and estuarine habitats. The burrowing and feeding

activities of E. lewisii make it a bioturbator. It is well established that particular

species of bioturbators have important roles in providing nutrient regeneration

and structure to an otherwise homogeneous substratum (Dayton 1984). Infaunal

species differ in their feeding behaviour and mode of movement consequently

creating different levels of disturbance to the sediment structure. Bioturbators

impact both the physical and chemical properties of the sediment and could

therefore impact the distribution of organisms living within the sediments. The

removal of E. lewisii from the intertidal by shellfish growers could have large

implications to the properties of the intertidal as broad-scale losses of benthic

bioturbators have been shown to impair marine ecosystem functioning (Lohrer et

al. 2004).

Bioturbation leads to particle redistribution and resuspention (Escapa et al.

2004; Katrak & Bird 2003; Widdows & Brinsley 2002). Larger animals, for

example E. lewisii, playa particularly important role in influencing sediment

reworking rates. Typically animals increase particle exchange between water and

sediment by a factor of 2-10 (Thrush & Dayton 2002). Burrowing crabs trap fine

grained and cohesive sediments that stabilize the sediment decreasing the

9

bedload transport. These fine sediments may act to protect the sediments

against evaporation during low tide, increasing water content and humidity in the

sediment (Escapa et al. 2004). The fine sediment also increases sediment

softness (Palomo et al. 2003). Bioturbation affects stability and composition of

marine sediments and influences their role as geochemical sources and sinks

(Thrush & Dayton 2002).

Porosity generally decreases with depth due to sediment compaction;

however, burrowing organisms mix the sediment and increase porosity by

altering the size of interstitial spaces within the sediments and breaking up the

cohesive sediment structure (Katrak & Bird 2003). This leads to increased water

content and permeability while sediment hardness decreases, which enhances

the movement of water between sediment grains (Escapa et al. 2004; Lohrer et

al. 2004; Palomo et al. 2003; Snelgrove 1999; Widdows & Brinsley 2002).

Infaunal organisms that construct burrows increase porosity of the sediments by

pumping water through their burrows and manipulating sediments (Katrak & Bird

2003).

Studies have shown that large, deposit-feeding, bioturbating organisms

dominate sediment reworking processes and related effects on sediment

biogeochemistry (Katrak & Bird 2003). Benthic habitats supply up to half the

nutrients for primary production in coastal seas, with ammonium being

particularly important to nitrogen-limited marine waters (Lohrer et al. 2004).

Sediment disturbance and particle erosion through burrowing, feeding and

movement enhance both (1) the direct release of nutrients sequestered in

10

porewater and (2) nutrient cycling back to the water column (Biles et al. 2002;

Katrak & Bird 2003; Thrush & Dayton 2002). Bioturbation also helps to decrease

sulphide and ammonium concentrations in the sediments (Katrak & Bird 2003).

The activities of the burrowing urchin, Echinocardium led to the release of NH4-N

from the sediments, which is linked to increases in primary production (Lohrer et

al. 2004). Active burrowers such as E. lewisii would lead to the highest release of

nutrients (Biles et al. 2002).

Burrowing and burrow construction increase the oxygen levels in the

sediment (Biles et al. 2002; Coleman & Williams 2002; Katrak & Bird 2003;

Snelgrove 1999; Thrush & Dayton 2002). Increased oxygen levels as well as

enhanced microbial activity caused by increased sediment surface area from

burrowing help with the breakdown and recycling of organic matter (Biles et al.

2002; Coleman & Williams 2002; Katrak & Bird 2003). Bioturbation improves the

conditions for production by microphytobenthos and increases the concentrations

of chlorophyll a in the sediment which leads to increased photosynthesis (Katrak

& Bird 2003; Lohrer et al. 2004).

The disturbance caused by bioturbation or burrow construction leads to an

accumulation of organic matter (Escapa et al. 2004; VanBlaricom 1982). This

means that there is more food available for the organisms in the bioturbated

habitat (Escapa et al. 2004; Palomo et al. 2003). This also makes the food

availability more homogeneous across a bioturbated area (Escapa et al. 2004).

Bioturbation also increases the available habitat of the intertidal by

extending the depth of hospitable living conditions. For example, the irrigation of

11

burrows extends the oxic water-sediment interface into the sediments (Katrak &

Bird 2003). The deeper bioturbator organisms live, feed or burrow in the

sediments, the more impact they will have on the physical and chemical

characteristics of the sediment (Katrak & Bird 2003).

Physical and chemical characteristics of the sediment control the

movement and zonation patterns of infauna, and habitat use by shorebirds and

their consumption rate (Escapa et a!. 2004). Ambrose (1991) and Widdows &

Brinsley (2002) found that nutrient enrichment from faecal material and creation

of biogenic structures can be expected to enhance densities of some infaunal

species. The biogeochemical changes driven by spatangoid urchins shifted

microphyte community composition towards species with high productivity per

amount of pigment. Biological disturbances such as bioturbation may increase

diversity (Thrush & Dayton 2002). For example, burrowing crabs can moderate

the physical harshness of the upper intertidal allowing some organisms to extend

their distribution to higher intertidal levels. Bioturbator activities have a positive

effect on infaunal polychaetes and nematodes, increasing their prey density and

availability (Escapa et al. 2004).

Bioturbatory effects on infaunal populations can influence higher level

predators at the surface. The activities of bioturbators can increase the amount of

area available for predation. Many species of shorebird benefit from the presence

of bioturbators, providing another link between infaunal and surface communities

(Escapa et a!. 2004; Palomo et a!. 2003).

12

Not all bioturbation activities are positive. Ambrose (1991) found that

sediment modification by surface active predators or predators that plough

through the surface can have a negative effect on infaunal densities in some

communities. Beal et al. (2001) found that bioturbatory disturbance by predators

affects the growth rates of some clam species. Disturbance can cause non­

selective mortality of other infaunal species (Gee et al. 1985). The effects of

disturbance include the burial of newly settled larvae, juveniles, and adults

(Ambrose 1984).

1.1.3 Biology of Euspira lewisii

E. lewisii is a large, infaunal snail that inhabits the west coast of North

America from southeastern Alaska to southern California (Harbo 2001; Harbo

2002). It usually inhabits protected mud, sand, gravel or cobbles beaches in the

intertidal to 50 m deep in the subtidal (Harbo 2001; Sept 1999; Snively 1978). It

is the largest species of moon snail in the world and can have a shell that

measures up to 14 cm high. This species displays sexual dimorphism, males

being smaller than the females in larger size classes (Bernard 1967). It is thought

that males grow at a slower rate than females. Males also have thicker shells.

Approximately six whorls make up E. lewisils shell, one very large whorl and the

remainders being small. Its muscular foot is very large and almost completely

surrounds its shell. It can pull its foot completely inside its shell for protection.

Water is squeezed out of small pores along the edge of its foot and a horny

operculum seals the opening (Sept 1999; Snively 1978).

13

It is a long-lived species, living 11 to 14 years (Bernard 1967). E. lew;s;;

begins breeding when snails are larger than 55 mm. This species lays its eggs in

a distinctive sand collar (Harbo 2001; Harbo 2002; Sept 1999; Snively 1978). The

collar is formed by the curvature in the shell as it is released from the body

(Bernard 1967). The eggs are found in a central jelly layer sandwiched between

two thick mucous-bonded sand coats. When in the collar, the eggs measure

approximately 250 IJm in length. Much of the development occurs in the collar. It

is thought that the jelly layer may provide food for the developing snails. Up to

10% of the eggs disintegrate in the collar and might also provide a food source to

the larvae. The collars are laid on the intertidal and deeper waters in the spring

and summer with a peak in density occurring in May and June (Harbo 2001;

Harbo 2002; Sept 1999; Snively 1978). Each collar contains close to a million

eggs and close to half a million hatch out of the collar. The collar disintegrates

approximately 6 weeks after being constructed, and the larvae are released as a

veliger larva during high tide (Bernard 1967). There is some discrepancy at this

point as to what happens to the larvae. Some say that the larvae are often

associated with VIva spp. which serves as a food source for the developing

larvae. After this, they enter their carnivorous stage.

E. lew;s;; is a predator of bivalves that ploughs through the sediment in

search of its prey (Bernard 1967; Harbo 2001; Harbo 2002; Sept 1999; Snively

1978). They attack by drilling through the shell of their prey using a toothed

radula assisted by secretions from an accessory boring organ. This leaves a

distinct counter-sunk hole unique to this species. Protothaca stam;nea (the

14

Pacific littleneck clam), Saxidomus gigantea (the butter clam), Mya arenaria (the

softshell clam), and Macoma nasuta (the bent-nose macoma) are species that

are commonly found with drill marks (Bernard 1967).

1.2 Research Objectives

The goal of this research was to broaden the knowledge base on the

ecology of E. lewisii. This was achieved by addressing three objectives. The first

objective was to determine the feeding ecology of E. lewisii through an

examination of prey preference and feeding rates. Secondly, I examined the role

of E. lewisii as a bioturbator. This was done through an exclusion experiment to

look at how this species influences the physical and chemical properties of the

sediment. The final objective was to use the information collected in each section

to determine the impacts that E. lewisii predation and bioturbation have on

infaunal community structure. This information is especially pertinent now given

that shellfish growers are removing E. lewisii. The information collected will fill

knowledge gaps on this species and demonstrate the importance of

understanding the role of each species in an ecosystem to better comprehend

ecosystem function. Such information can then be used to advise the shellfish

industry.

1.3 Literature Cited

Ambrose WG,: ,Jr. 1984. Role of predatory infauna in structuring marine soft­bottom communities. Marine Ecology Progress Series 17(2):109-15.

Ambrose WG,: ,Jr. 1991. Are infaunal predators important in structuring marinesoft-bottom communities? American Zoologist 31 (6):849-60.

15

BCSGA. British Columbia Shellfish Farming Industry - Environment management

system code of practice. <http://bcsga.netfirms.com/wp­

content/uploads/2007/08/enviro-mgmt-code-of-practice 02feb7.pdf>.

Accessed 2007 10/29.

Beal BF. 2006. Biotic and abiotic factors influencing growth and survival of wild

and cultured individuals of the softshell clam (Mya arenaria L.) in eastern

Maine. Journal of Shellfish Research 25(2):461-74.

Beal BF, Parker MR, Veneile KW. 2001. Seasonal effects of intraspecific density

and predator exclusion along a shore-level gradient on survival and growth

of juveniles of the soft-shell clam, Mya arenaria L., in Maine, USA. Journal of

Experimental Marine Biology and Ecology 264(2):133-69.

Bernard FR. 1967. Studies on the biology of the naticid clam drill Polinices lewisii(Gould) (Gastropoda Prosobranchia). Fisheries Research Board of Canada

Technical Report 42:1-41.

Biles Cl, Paterson OM, Ford RB, Solan M, Raffaelli OG. 2002. Bioturbation,

ecosystem functioning and community structure. Hydrology and Earth

System Sciences 6(6):999-1005.

Byers JE. 2002. Physical habitat attribute mediates biotic resistance to non­

indigenous species invasion. Oecologia 130(1):146-56.

Byers JE. 2005. Marine reserves enhance abundance but not competitive

impacts of a harvested nonindigenous species. Ecology 86(2):487-500.

Chalcraft OR and Resetarits WJ,Jr. 2003. Predator identity and ecological

impacts: Functional redundancy or functional diversity? Ecology 84(9):2407­

18.

Coleman FC and Williams SL. 2002. Overexploiting marine ecosystem

engineers: Potential consequences for biodiversity. Trends in Ecology &

Evolution 17(1 ):40-4.

Como S, Rossi F, lardicci C. 2004. Response of deposit-feeders to exclusion of

epibentllic predators in a mediterranean intertidal flat. Journal of

Experimental Marine Biology and Ecology 303(2): 157-71.

16

Dayton P. K. 1984. Processes structuring some marine communities: Are theygeneral? Ecological communities: Conceptual issues and the evidence.Princeton University Press. 181-197 p.

DeGraaf JD and Tyrrell MC. 2004. Comparison of the feeding rates of twointroduced crab species, Carcinus maenas and Hemigrapsus sanguineus, onthe blue mussel, Mytilus edulis. Northeastern Naturalist 11 (2): 163-6.

Duarte CM. 2000. Marine biodiversity and ecosystem services: An elusive link.Journal of Experimental Marine Biology and Ecology 250(1-2):117-31 .

Escapa M, Iribarne 0, Navarro D. 2004. Effects of the intertidal burrowing crabChasmagnathus granulatus on infaunal zonation patterns, tidal behavior, andrisk of mortality. Estuaries 27(1 ):120-31.

Gee JM, Warwick RM, Davey JT, George CL. 1985. Field experiments on therole of epibenthic predators in determining prey densities in an estuarinemudflat. Estuarine, Coastal and Shelf Science 21 (3):429-48.

Harbo RM. 2001. Shells and shellfish of the Pacific Northwest. Madeira Park:Harbour Publishing.

Harbo RM. 2002. Whelks to whales - Coastal marine life of the Pacific Northwest.Madeira Park: Harbour Publishing.

Katrak G and Bird FL. 2003. Comparative effects of the large bioturbators,Trypaea australiensis and Heloecius cordiformis, on intertidal sediments ofWestern Port, Victoria, Australia. Marine and Freshwater Research54(6):701-8.

Krebs CJ. 2001. Ecology: The experimental analysis of distribution andabundance. 5th ed. San Francisco: Benjamin Cummings.

Lohrer AM, Thrush SF, Gibbs MM. 2004. Bioturbators enhance ecosystemfunction through complex biogeochemical interactions. Nature (London)431 (7012):1 092-5.

Menge BA, Berlow EL, Blanchette CA, Navarrete SA, Yamada SB. 1994. Thekeystone species concept - variation in interaction strength in a rockyintertidal habitat. Ecological Monographs 64(3):249-86.

17

Moran MJ. 1985. Effects of prey density, prey size and predator size on rates of

feeding by an intertidal predatory gastropod Morula marginalba Blainville(Muricidae), on several species of prey. Journal of Experimental MarineBiology and Ecology 90(2):97-105.

Palomo G, Botto F, Navarro D, Escapa M, Iribarne O. 2003. Does the presenceof the SW Atlantic burrowing crab Chasmagnathus granulatus Dana affectpredator-prey interactions between shorebirds and polychaetes? Journal ofExperimental Marine Biology and Ecology 290(2):211-28.

Peitso E, Hui E, Hartwick B, Bourne N. 1994. Predation by the naticid gastropodPolinices lewisii (Gould) on littleneck clams Protothaca staminea (Conrad) in

British Columbia. Canadian Journal of Zoology 72(2):319-25.

Peterson C. H. 1979. Predation, competitve exclusion, and diversity in the soft­sediment benthic communities of estuaries and lagoons. Ecological

processes in coastal and marine systems Florida: Plenum Press. 233-264 p.

Quijon PA and Snelgrove PVR. 2005. Predation regulation of sedimentary faunalstructure: Potential effects of a fishery-induced switch in predators in anewfoundland sub-arctic fjord. Oecologia (Berlin) 144(1):125-36.

Raghukumar Sand Anil AC. 2003. Marine biodiversity and ecosystemfunctioning: A perspective. Current Science 84(7):884-92.

Savini D and Occhipinti-Arnbrogi A. 2006. Consumption rates and preypreference of the invasive gastropod Rapana venosa in the northern AdriaticSea. Helgoland Marine Research 60(2):153-9.

Schneider D. 1982. Escape response of an infaunal clam Ensis directus Conrad1843, to a predatory snail, Polinices duplicatus Say 1822. Veliger 24(4):371­

2.

Sept JD. 1999. The beachcomber's guide to seashore life in the PacificNorthwest. Madeira Park: Harbour Publishing.

Smith TE, Ydenberg RC, Elner RW. 1999. Foraging behaviour of an excavatingpredator, the red rock crab (Cancer productus Randall) on soft-shell clam(Mya arenaria L.). Journal of Experimental Marine Biology and Ecology

238(2): 185-97.

18

Snelgrove PVR. 1999. Getting to the bottom of marine biodiversity: Sedimentary

habitats - Ocean bottoms are the most widespread habitat on earth andsupport high biodiversity and key ecosystem services. Bioscience 49(2): 129­

38.

Snively G. 1978. Exploring the seashore in British Columbia, Washington andOregon. Vancouver: Gordon Soules Book Publishers.

Tallqvist M. 2001. Burrowing behaviour of the Baltic clam Macoma balthica:Effects of sediment type, hypoxia and predator presence. Marine EcologyProgress Series 212:183-91.

Thiel M, Ullric~1 N, Vasquez N. 2001. Predation rates of nemertean predators:The case of a rocky shore hoplonemertean feeding on amphipods.Hydrobiologia 456:45-57.

Thrush SF and Dayton PK. 2002. Disturbance to marine benthic habitats bytrawling and dredging: Implications for marine biodiversity. Annual Review ofEcology and Systematics 33:449-73.

VanBlaricom GR. 1982. Experimental analyses of structural regulation in amarine sand community exposed to oceanic swell. Ecological Monographs52(3):283-305.

Virnstein RW. 1977. Importance of predation by crabs and fishes on benthicinfauna in Chesapeake Bay. Ecology 58(6):1199-217.

Weissberger EJ. 1999. Additive interactions between the moon snail Euspiraheros and the sea star Asterias forbesi, two predators of the surfclam

Spisula solidissima. Oecologia 119(3):461-6.

Widdows J and Brinsley M. 2002. Impact of biotic and abiotic processes onsediment dynamics and the consequences to the structure and functioning of

the intertidal zone. Journal of Sea Research 48(2002): 143-56.

Wiltse WI. 1980. Effects of Polinices duplicatus (Gastropoda: Naticidae) oninfaunal community structure at Barnstable Harbor, Massachusetts, USA.Marine Biology (Berlin) 56(4):301-10.

19

CHAPTER 2 USING PREY PREFERENCES ANDFEEDING RATES TO EXAMINE THE INFLUENCE OFEUSPIRA LEWISII ON BIVALVE COMMUNITIES1

1 The following chapter has been submitted to the Journal of Experimental Marine Biology andEcology under the co-authorship of Leah Bendell-Young.

20

2.1 Abstract

The predatory naticid snail Euspira lewisii, native to the west coast of

North America, is stated to be an economic threat to the shellfish aquaculture

industry in British Columbia (B.C.). This species is being manually removed from

the intertidal ecosystem, yet little is known about the ecology of this species.

Enclosures and beach shell assemblages were used to determine the prey

preference, feeding rates and community impacts of E. lewisii. Protothaca

staminea, the native little neck clam, was found to be the preferred prey, while

the commercially valuable Manila clam, Venerupis philippinarum, was avoided.

Drilled shells collected from the intertidal revealed similar feeding preferences.

The feeding rate on a variety of species was found to be 0.09 clams/day or 1

clam every 14 days. The feeding rate was dependent on prey species and was

highest for the preferred species and significantly lower on avoided species. The

overall impact of E. lewisii to the bivalve community was found to be extremely

low. Based on these results, E. lewisii consumed only approximately 3% of the

clam population over one year, assuming maximal feeding rates and typical

population densities found on the west coast of B.C. E. lewisii has minimal

impacts to the Manila clam industry in B.C. and control measures are not

necessary for this species. Baseline ecological field studies are important for

gaining understand of poorly understood species, especially those considered

threats to industry.

21

2.2 Introduction

Predation is one of the most important factors effecting community

structure in intertidal communities. It can affect the distribution pattern, size and

age composition and abundance of prey species (Beal 2006; Peitso et al. 1994).

Recent studies have stressed the importance of a full understanding of predation

such that we can evaluate the ecological impact a predator has on a community

(Savini & Occhipinti-Ambrogi 2006). The key to understanding the role a predator

plays in a community includes knowing its prey preferences and feeding rates

(Moran 1985; Thiel et al. 2001). From an applied aspect, without a full

understanding of predation it is difficult to manage intertidal communities or know

if antipredator practices, such as predator removal, are effective (Miron et al.

2005).

Many intertidal predators demonstrate prey preferences and select prey

that is the quickest to handle and consume to maximize their net energy intake

(Savini & Occhipinti-Ambrogi 2006). The effects of selective predation on

community structure vary with relative abundance of prey species (Moran 1985)

and the escape abilities of the prey species. Selective feeding on non-dominant

species can have adverse effects on the community such as decreasing species

diversity by removing rare species (Wiltse 1980b).

Feeding rates of predators depend on a number of biotic and abiotic

factors. Biotic factors include prey biomass, density, species, quality, and

predator and prey size (DeGraaf & Tyrrell 2004; Moran 1985; Thiel et al. 2001).

Time spent on other activities such as mating or predator avoidance also

22

influences feeding rates (DeGraaf & Tyrrell 2004; Thiel et al. 2001). Abiotic

factors such as temperature, season, wave action, and duration of submersion

(Moran 1985; Weissberger 1999) also affect feeding rates. Greater feeding rates

can lead to greater impacts on the prey community such as reduced abundance

of the prey species (DeGraaf & Tyrrell 2004; Savini & Occhipinti-Ambrogi 2006).

Moon snails are infaunal, predatory snails that feed on bivalves. Several

species of moon snails have shown both size and species preferences while

feeding (Bernard 1967; Commito 1982; Dietl & Alexander 1997; Peitso et al.

1994; Rodrigues et al. 1987; Wiltse1980b). Through drilling activities, very clear

artefacts of the predation of these species are left in intertidal habitats. For this

reason, they are considered pest species, especially to shellfish aquaculture

(BCSGA 2002; Beal 2006; Bernard 1967; Peitso et al. 1994). However, little is

known about the predation pressure of the moon snail on bivalve populations. A

review of the literature suggests that bivalve mortality attributed to moon snails

may in fact be overestimated (Beal et al. 2001; Miron et al. 2005; Peitso et al.

1994; Wiltse 1980a).

On the west coast of B.C., the native moon snail, E. lewisii is being

actively eliminated from shellfish farms, based on the assumption that they are

effective predators. Hence, the objectives of this study are to assess the impacts

of predation by E. lewisii on bivalve communities with special emphasis on the

commercially valuable Manila clam, Venerupis philippinarum. We use both field

experiments and the collection of drilled bivalve shells to determine moon snail

prey preference, feeding rates, and impacts on the prey community.

23

2.3 Methods

2.3.1 Study Areas

Field research was conducted in southern B.C. at Fillongley Provincial

Park, on Denman Island (49°31'59"N, 124°49'0"W) and Shingle Spit, on Hornby

Island (49°31 'O"N, 124°37'59"W). Both sites are home to known populations of E.

lewisii. Venerupis philippinarum, the commercially valuable Manila clam and

Protothaca staminea, the native Pacific littleneck clam dominate the bivalve

community at these sites. Nuttallia obscurata, the varnish clam, a recent

introduction to southern B.C., as well as several other clam species are also

found at these sites.

2.3.2 Feeding Experiments

Cage Design

We used enclosure experiments, i.e. cages, to determine the prey

preferences of E. lewisii. The cages were made of PVC pipe frame measuring

1x1xO.3m, and enclosed an area of 1m2. All sides of the frame were covered with

plastic mesh with an aperture of 1cm2. The cages were dug into the sediment to

a depth of 0.2m, leaving 0.1 m exposed at the surface. Sediment was sieved back

into the cage and all bivalves and drilled shells were removed. A 4 by 3 grid was

created, using 12 cages, oriented parallel to the water line. The cages in the grid

were spaced approximately 2m apart. Studies were conducted from May to

September in 2005 and 2006.

24

Prey Preference

Three clam species collected from Fillongley were used in the

experiments to analyze the prey preferences of E. lewisii: P. staminea, V.

philippinarum and Nuttallia obscurata. Twenty clams of each species were buried

in each cage, five individuals of each species in each corner. This led to 60

clams in each cage and 720 in all 12 cages. This was in the range of clam

densities found at this site. Two cages, selected at random, served as controls

that contained only clams and no snail that tested for clam transplant

survivorship. In the ten remaining cages, a single moon snail, collected from the

site, was measured and buried into the centre of the cage. All cages were sealed

and left.

The cages were checked every other tide cycle, approximately once every

three weeks, throughout the course of 4 months and all drilled and dead clams

were removed and replaced with live individuals of the appropriate species. Only

completely drilled shells were used in the prey preference analyses.

Manly's a was used as an index of preference for constant prey

populations (see Krebs 1999).

where: aj = Manly's a (preference index) for prey type i

Tj, '1 = proportion of prey type i or j in the diet (i and j = 1,2,3, .. .m)

nj, nj = proportion of prey type i or j in the environment

m =number of prey types possible

25

Similar preference experiments have used this index (Dudas et al. 2005) and it is

well established in the feeding preference literature (Krebs 1999; Manly 1974;

Manly et al. 1972). The interpretation of the 0 values for this index are:

OJ = 1/m = no preference for species i

OJ> 1/m = preference for species i

OJ < 1/m =avoidance of species i

where m =number of prey species.

For these experiments, three species were used therefore an 0 value of

0.33 indicates no preference, >0.33 is an indication of preference and <0.33 is an

indication of avoidance. These 0 values are considered significant if the 95%

confidence intervals does not overlap the 0.33 prey types.

Feeding Rates

Feeding rates were determined in tandem with the prey preference data.

Feeding rates were calculated as the # clams consumed/# days the moon snail

was contained within the cage.

By-species feeding rates were also determined. Due to time constraints in

August of 2006, a single trial was carried out where the 12 cages were randomly

selected to contain one of each of the three species. Fifteen individuals of each

species were buried in each of the four corners of the cage Le., 4 cages/species,

240 clams/species for a total of 720 clams. Snails were added as described

above and cages were sealed for approximately 3 weeks. After the 3 weeks, all

the cages were checked and any drilled shells were removed and tallied.

26

A Kruskal-Wallis test was applied to determine significant differences

among species feeding rates on these three clam species.

2.3.3 Density and Drill Collection

Density surveys were conducted at both the Fillongley Provincial Park site

and at Shingle Spit. To account for tidal influences a 60m wide strip

representative of the intertidal communities was stratified into tide heights by

dividing into a high (2.3-1.7m above chart datum), mid (1.7-1.3m above chart

datum) and low (1.3-0.7m above chart datum) zone.

Survey Design

Within each stratum 4 and 3-60m long transects were randomly selected

at Fillongley and Shingle Spit respectively. Along each transect 6 quadrat

locations were selected at random. Random numbers were selected using a

random number table. At each coordinate, a 0.5 by 0.5m quadrat was dug

(0.25m2) down to a depth of 0.2m. All sediment dug from the quadrat was sifted

through a 6mm mesh and all infaunal bivalves were identified and counted to

determine community composition and densities.

During the sifting process any shells containing the distinct counter-sunk

E. lewisii drill marks were removed and the clam species was identified (Peitso et

al. 1994). All live organisms and drilled shells were replaced post sampling.

Euspira lewisii densities were determined using a mark-recapture

technique. Fifty individual snails were marked by scratching a number into their

shell then the snails were buried back into the sediment. After three weeks, we

27

returned and dug up 30 snails and determined the number of marked snails. The

total E. lewisii population was calculated based on Bernard (1967) as follows:

T =M/(R/C)

Where: T = total population in the area

M = # marked animals in 1st sample

R =# marked animals in 2nd sample

C = total caught in 2nd sample.

Prey Preferences from Beach Shell Assemblages

The density measurements and drills collected were used to determine if

E. lewisii prey preferences were also evident under natural conditions.

Proportions of the clams were calculated based on a stratified multi-stage design

(Krebs 1998; Schwarz 2005). The proportions of shells and species in the

community were also used to calculate electivity coefficients (E) based on Ivlev

(1961):

E = (r- p)l(r + p)

Where: r =proportion of a food item in the dietp =proportion of the food item in the environment

Preference is indicated by a positive value of E, avoidance is indicated by

a negative value and no preference is indicated by a value of O.

Ivlev's electivity coefficient was selected because of the variable nature of

the bivalve communities in the intertidal. Manly's a is appropriate for constant

prey populations or in experimental situations where the prey is being replaced

maintaining a constant supply of food (Krebs 1999). It is also not recommended

28

that 0 values calculated based on populations with different numbers of prey

types (Krebs 1999).

2.3.4 Community Impacts

Density measurements and average feeding rates were used to represent

the effects of E. lewisii predation on these intertidal communities. The average

feeding rate was used to calculate the number of clams consumed in a month, in

6 months and in a year based on:

# consumed =(feeding rate) x (days) x (# snails)

2.4 Results

2.4.1 Prey Preference

When offered equal numbers of P. staminea, V. philippinarum and N.

obsGurata, E. lewisii showed significant preference for P. staminea (0 = 0.57, P <

0.05, Figure 2.1). N. obsGurata was preferred although it was not statistically

significant (Figure 2.1). A significant avoidance was observed for V.

philippinarum (0 =0.07, P < 0.05, Figure 2.1).

29

0.7

0.6

...-.. 0.5ij---><Q)

""0 0.4c

~c0.3~

~~a.. 0.2

0.1

0.0

--------------------

Protothacastaminea

Venerupisphilippinarum

Nuttalliaobscurata

Species

Figure 2.1.E. lewisii (e) prey preference (± 95% Col.). The dashed line represents zeropreference (0.33). Values above the dashed line indicate prey preference, valuesbelow indicate avoidance. Where the Col. does not overlap the line, preference issignificant.

2.4.2 Feeding Rates

The average summer feeding rate of E. lewisii consuming a variety of prey

species was found to be O.09±O.02 clams/day (± 95% C.I.), 1 clam consumed

every 14 days.

When the feeding rates were analyzed for each of the three species

individually, the consumption rate on P. staminea was greater than that on N.

obscurata, which was greater than the rate on V. philippinarum (Figure 2.2).

30

0.14

.- 0.12>,ro

"'C-(f) 0.10E 0ro

I(,)--Q) 0.08--fl.0>c: 0.06

"'C

IQ)Q)

u...0.04

0.02P.staminea V. phi. N. obscurata

Species

Figure 2.2.Medians and interquartile ranges of the feeding rates of E. lewisii on P.staminea, V. philippinarum and N. obscurata in clams/day/snail for eachspecies.

The Kruskal-Wallis test showed that the feeding rates in clams per day

were significantly different (H = 6.17, P < 0.05, Figure 2.2). The feeding rate on V.

philippinarum was significantly different from that of P. staminea. N. obscurata

was not significantly different from either species (Wilcoxon p <0.05).

2.4.3 Bivalve and E. lewisii Density and Abundance

At both sites, the total density/m2 decreased as the tide level decreased

(Figure 2.3A & B). The density of V. philippinarum was greatest in the high tide

zone and decreased through the other strata to the water line. However, at both

sites the density followed the same pattern of being highest in the mid-intertidal,

31

followed by the high zone and was the least dense in the low zone. Nuttallia

obscurata was found in very low densities in the study areas, and was only found

in the high, and to a lesser extent in the mid-tide zone (Figure 2.3A & B).

Macoma spp. was found in much higher densities at Shingle Spit and at both

sites, it was at its highest densities in the mid and low strata (Figure 2.3A & B).

The other species we found at both sites were Mya arenaria, Saxidomus

gigantea, Parvaleucina tenuisculpta, and Rhamphidonta retifera. Tellina

carpenteri, Clinocardium nuttalli and Lyonsia californica were exclusively found at

Fillongley while Tresus nuttallii and Cryptomya californica were only found at

Shingle Spit. Macoma spp. was predominantly Macoma nasuta but at smaller

sizes, it was difficult to distinguish it from Macoma obliqua so both of these

species were represented in these communities.

Venerupis philippinarum was the most abundant species at both sites

(Table 2.2). Protothaca staminea was the second most abundant species at

Fillongley while Macoma spp. was the second most abundant species at Shingle

Spit (Table 2.2). From the quadrat surveys, E. lewisii was found only in the

lowest stratum at Fillongley at an abundance of 2000 individuals in a 60m strip of

the intertidal although data variability for these measurements was very high

(Table 2.2). E. lewisii was collected in both the mid and the low strata at Shingle

Spit and rough estimates suggested abundances of 200 and 300 snails in the

mid and low stratums respectively (Table 2.2). Euspira lewisii densities were

more accurately estimated using the mark-recapture techniques. At both sites,

the density of E. lewisii was 0.2 snails/m2 (Table 2.1). Due to the shorter, steeper

32

intertidal area at Shingle Spit, the total population was less than that of Fillongley

at 700 individuals compared to that at Fillongley at 2000 individuals.

500 ..,-----------.,- 500 ,------------------,

A B

o

400

o

400

N 300 300E _ Protothaca

'! staminea

~ rz.zz;j Venerupis·00 philippinarumcQ)

200 200 [[[[[[l] Nuttallia0 obscurata

c=::J Macoma spp.IlII:'l::Im Other

100 100

High Mid Low

Tide Level

High Mid Low

Tide Level

Figure 2.3.Density of clam species in number of individuals per m2 for Fillongley (A) andShingle Spit (8).

Table 2.1. Density of E. lewisii at Fillongley and Shingle Spit in density/m2 ± 95% C.1. andin total abundance in the survey area ± 95% C.I.

Site

Fillongley Shingle Spit

Density (#/m2) O.2±O.2 O.2±O.1

Total population 2000±1000 700±500

33

Ta

ble

2.2.

To

talc

lam

ab

un

da

nce

by

spe

cie

sa

tF

illo

ng

ley

an

dS

hin

gle

Sp

itfo

re

ach

stra

tum

±95

%C

.1.

Site

Fill

ongl

eyS

hing

leS

pit

Tid

eZ

on

eH

igh

Mid

Low

Hig

hM

idLo

w

Pro

toth

aca

1900

00±4

0000

6000

00±2

0000

036

0000

±600

0070

000±

2000

039

000±

9000

3000

0±10

000

stam

inea

Ven

erup

is54

0000

±800

0060

0000

±500

000

029

0000

±800

0020

960±

2000

020

00±3

000

phili

ppin

arum

Nut

talli

a30

0±60

010

00±3

000

020

000±

2000

00

0ob

scur

ata

Mac

oma

8000

±800

040

000±

2000

060

000±

3000

010

000±

1000

090

000±

3000

018

0000

±300

00sp

p.

Oth

er

2100

±200

020

000±

1000

070

000±

2000

020

000±

1000

080

00±4

000

6000

±300

0

Tot

al75

0000

±800

0012

0000

0±60

0000

5000

00±7

0000

4100

00±6

0000

1600

00±2

0000

2200

00±4

0000

Eus

pira

00

2000

±300

00

200±

300

300±

500

lew

isii

34

2.4.4 Shell Assemblage Prey Preference

P. staminea was the most abundant of the drills collected at Fillongley,

followed by Macoma clams (Table 2.3). These were also the most common of

the drilled shells collected at Shingle Spit but the abundances were reversed,

Macoma spp. being the most abundant P. staminea being second. The highest

number of drilled shells were collected from the lowest tide stratum at both sites.

Table 2.3. Raw numbers of drilled shells collected in each stratum at each site with totals.

Fillol1gley Shingle Spit

High Mid Low Total High Mid Low Total

Protothaca 16 278 623 917 12 106 157 275stamineaVenerupis 1 6 2 9 1 4 2 7philippinarumNuttallia 0 0 0 0 1 0 0 1obscurataMacoma spp. 0 67 176 243 0 51 334 385

Other 1 38 103 142 3 22 26 51

Total 18 389 904 1311 17 183 519 719

At Fillongley 9 species were found with E. lewisii drill marks. The "other"

group included: M. arenaria, S. gigantea, P. tenuisculpta, C. nuttallii and Nucella

lamellosa. The diversity in the diet of E. lewisii was slightly lower at Shingle Spit,

where 6 species were consumed. The "other" group was comprised of M.

arenaria and S. gigantea.

35

When the proportions of the collected drilled shells were compared to the

proportions of the species available in the community E. lewisii does not take

clams in direct proportion to their availability (Figure 2.5). Even though V.

philippinarum represented the species available in the highest proportion, the

proportion of drilled shells collected for this species were very low.

When looking at each species individually, Ivlev's electivity coefficients

showed that there was a preference for P. staminea, N. obscurata, Macoma spp.,

M. arenaria, S. gigantea, P. tenuisculpta and C. nuttallii at Fillongley (Figure

2.50). V. philippinarum, R. retifera, L. californica, and T. carpenteri were avoided.

At Shingle Spit only P. staminea, Macoma spp., and S. gigantea were preferred

while all other species were avoided (Figure 2.60). Differences in this feeding

pattern were noted when each stratum was analyzed individually. P. staminea

was a preferred prey item at both sites in every stratum with the exception of the

low zone at Fillongley where it was close to the no preference line (Figure 2.5A,

B & C). S. gigantea was present only in the mid and low zones at both sites.

Whenever it was present it was a preferred prey species for E. lewisii. According

to the Ivlev electivity coefficients Macoma clams were avoided at all tide heights

at Shingle Spit, even though they were the most commonly collected drilled shell

at that site (Figure 2.6A, B, & C). However, E. lewisii did show a preference for

them when the study area was looked at as a whole. They were preferred prey in

the mid and low zones at Fillongley.

36

80

.-..~~ 60(1)Cl!9c~ 40(1)0-

20

100

80

~ 60(1)Cl!9c~ 40(1)0-

20

o

Drills-H Clams-H Drills-M Clams-M Drills-L Clams-L Drills-T Clams-T

Drills-H Clams-H Drills-M Clams-M Drills-L Clams-L Drills-T Clams-T

_ Protothacastaminea

r:zzzJ Venerupisphilippinarum

£ITIIII] Nuttalliaobscurata

c==J Macomaspp.

m±lm Other

Figure 2.4.The proportion of drilled shells collected from Fillongley (A) and Shingle Spit(B) compared to the proportion of clams available at each site (H-high, M-mid,L-Iow, T-total).

2.4.5 Impacts of E. lewisii Predation on Intertidal Clam Communities

There were close to three million clams available in a 60 m -wide strip of

beach at Fillongley within the range of E. lewisii. There was on average

228clams/m2. At an overall density of 0.22 snails/m2 in this area, E. lewisii,

feeding at a rate of 0.09 clams/day, in one month approximately 6500 clams37

would be consumed (Figure 2.7). This is 0.26% of the clam population in the

study area. If these values are then converted to 6 months and 1 year of feeding

in the area, E. lewisii consumes 1.61 % and 3.22% of the clam population

respectively. The year values should also be considered high estimates as E.

lewisii decreases its feeding rate over the winter months (Huebner & Edwards

1981; Peitso 1993).

10

c(J) 05'0iE(J)o 00

U>.'5 -05

~(J)

W -10

-15

1.0

c(J) 0.5'0iE(J)o 0.0

U>..~ -0.5

'-B(J)w -1.0

-1.5

A

n'----

-

c

nn nU

- ~ ~

1.0

c(J)

'(3 0.5iE(J)oU 00

C'>t5 -05(J)

UJ

-1.0

1.0

-c.~ 0.5uiE(J)o 00U>..~ -0.5

~(J)

W -1.0

-1.5

8 -r- r--

n n,

'---~ ~

0~r-

n ~ n n

'-'-'-

Species

Figure 2.5.Electivity coefficients for E. lewisii feeding on the clam populations in the high(A), mid (B), low (C) and all three zones (0) at Fillongley. Negative valuesindicate avoidance, while positive values indicate preference.

38

0r-

n n IU

l-'-- I

- -'--

1.0 B--Cill 0.5'0iEQ)

0 0.00.c'> -0.5:;=;()

illiIi -1.0

-1.5~. ~. R ,<Z> ,,' ~Oj

q.'O ~« 0'< ~'P',-<Z>

Q.. v· Q. e"~'O

Ar-

-

-- ~ - ~

1.0

C.Q2 0.5()

i:Q)0 0.00»..-:> -05:sQ)

iIi -1.0

-1.5

l' :1:-" 'S:J'" 5l" ,<Z> ,,' ". ~.

~ ~«"",O "~ '0 Q. ,-<Z> «-,<Z> C)'Q.' ~'Ov

1.0 C 1.0»

C()c

Q) 0.5 Q) 0.5'u Tii: if:Q) Q)0 0.0 0 0.00 02: »':> -0.5 () -0.5:s c

Q)Q) '0W -1.0 !E -1.0

W

-1.5 -1.5

'O~. <to e,,"" ,-<Z>" ,<G. ~o, ,$'-~ ~. Q. «- e". G"

Q.' ~'Ov

Species

Figure 2.6.Electivity coefficients for E. lewisii feeding on the clam populations in the high(A), mid (B), low (C) and all three zones (0) at Shingle Spit. Negative valuesindicate avoidance, while positive values indicate preference.

The impacts were similar at Shingle Spit (Figure 2.7). There were fewer

clams total at Shingle Spit, close to 800,000 and 228 c1ams/m2. At the rate

previously mentioned and a density of E. lewisii of 0.22 snails/m2, 2010 clams

are consumed in 1 month, which is 0.25% of the total clam population.

Continuing at these feeding rates, E. lewisii consumes 1.54 and 3.08% of the

clam population in 6 and 12 months.

39

4e+6 .,----------------------------,

_ Fillongley

c::=::J Shingle Spit

3e+6

(/)

E~ 2e+6

:j::j:

1e+6

oTotal Clams 1 month 6 months 12 months

Figure 2.7. The number of clams consumed by E. lewisii at the rate of 0.09 clams/day at adensity of 0.22 snails/m2 in 1 month, 6 months and over 12 months compared tothe total number of clams available at Fillongley and Shingle Spit.

2.5 Discussion

The work described here found that V. philippinarum is avoided by E.

lewisii, suggested by the results of both prey preference experiments and

observed shell assemblages. The only other study conducted on E. lewisii prey

preferences found that only 0.4% of the drilled shells collected were V.

philippinarum, indicating that this species is not favoured (Bernard 1967).

Protothaca staminea was the preferred prey of E. lewisii based on our

experiments. Bernard (1967), Harbo (2001), Peitso (1980), and Reid &

Gustafson (1989) also found this preference. Beach shell assemblages also

confirmed a preference for P. staminea. Despite the observed prey preference,

40

the beach shell assemblages showed a diverse diet. At specific tide heights other

prey were chosen including Macoma spp., P. tenuisculpta, M. arenaria, S.

gigantea, N. obscurata, and C. nuttallia. The beach shell assemblages gave

important indications of the prey preferences of E. lewisii. The accuracy of this

data is limited in that the drilled valves of thinner shelled prey species are not

likely to persist as long in the habitat.

Prey preference is common in naticid snails. Wiltse (1980b) found that

Polinices duplicatus, an east coast naticid snail, ate 13 different species but

showed preferences for M. arenaria and Gemma gemma. Euspira heros was

shown to favour Macoma balthica and M. arenaria (Cornmito 1982). Spisula

solidissima was preferentially consumed by E. heros (Weissberger 1999). Vignali

and Galleni (1986) found that Donax trunculus was the species that was most

attacked by the naticids from the Piombino, Italy.

Preferences from the cage experiments may be attributed to the

stratification of the three tested species within the sediment, since burial depth is

a phenomenon that can affect prey preferences (Committo 1982). Venerupis

philippinarum lives very close to the sediment surface due to its short siphons

(Meyer & Byers 2005). Euspira lewisii may burrow below V. philippinarum and

therefore does not encounter it as readily as it does P. staminea and N.

obscurata, species found deeper within the sediment.

The distribution of clams throughout the intertidal could also result in the

preferences. Venerupis philippinarum lives at the higher end of the range of E.

lewisii, and therefore there is limited overlap in their distributions on the intertidal.

41

However, this does not explain the observed preferences because N. obscurata

lives even higher on the intertidal than V. philippinarum and was consumed to a

greater extent by E. lewisii.

Prey species is known to affect feeding rates (Moran 1985; Rodrigues et

al. 1987; Thiel et al. 2001; Vignali & Galleni 1986). Our by-species feeding rates

show that P. staminea was preyed upon at the highest rate by E. lewisii. Nuttallia

obscurata, a newly introduced species in the area, was consumed at the second

fastest feeding rate. Venerupis philippinarum was the avoided prey type with the

lowest feeding rate. Bernard (1967) found that E. lewisii consumed P. staminea

faster than it consumed S. gigantea and T. nuttalli, which supports the

conclusions of this work. Euspira heros had higher feeding rates on soft-shell

clams, its preferred prey type (Miron et al. 2005).

The feeding rate of 0.09 clams per snail per day was determined for E.

lewisii consuming a variety of available species. This is within the range found in

previous studies (Peitso et al. 1994). Earlier studies by Bernard (1967) found the

feeding rate to be 0.25 clams per snail per day. However, in the Bernard (1967)

study, snails were starved for 5 days prior to experimentation, placed in tanks

with a limited amount of sediment, and all attempts and partially consumed clams

were used in feeding rate calculations. Studies have shown that moon snails will

not return to same drill site to continue feeding on the prey item once interrupted

(Dietl & Alexander 1997; Kingsley-Smith et al. 2003). Thus, including drill

attempts could have inflated the feeding rate. Peitso et al. (1994) found that the

summer feeding rate was approximately 0.07 clams per snail per day, which is

42

close to our 0.09 estimates. Our rate translates to one clam consumed every 14

days, a very slow feeding rate. Previous work on moon snail feeding rates has

shown a wide range of feeding rates between snail species. Euspira heros had a

maximum feeding rate of 1 clam per day (Weissberger 1999). Polinices

pulchellus was found to consume 14.S7 clams per snail per month at its

maximum rate (Kingsley-Smith et al. 2003). Thus, feeding rates are not

comparable between species.

Predator size, prey size and temperature can all influence feeding rates.

These factors must be considered when looking at feeding ecology as they can

lead to an elevated feeding rate. Smaller snails have higher consumption rates

(Seal 2006; Edwards & Huebner 1977; Huebner & Edwards 1981; Kingsley­

Smith et al. 2003; Peitso et al. 1994; Wiltse 1980a). Prey size can be optimized

for best grip by the moon snail that facilitates drilling and increases feeding rates

(Commito 1982; Vignali & Galleni 1986; Wiltse 1980a). Peitso (1980) found

significant differences between the summer and winter feeding rate of E. lewisii,

the rate being highest in the summer. The rate determined in our study is a

summer feeding rate. The spring, fall and winter rates are lower due to the lower

temperatures. Kingsley-Smith et al. (2003) and Weissberger (1999) found that

moon snail feeding rates were dependent on temperature. Many naticid snails

will actually stop feeding for 4 months in the winter, as was seen in P. duplicatus

(Huebner & Edwards 1981). This species stopped feeding completely at a

temperature below SoC (Edwards & Huebner 1977). Therefore, the feeding rate

43

determined in the current work is an upper limit, which must be considered when

estimating the snails impact on the community.

Prey preferences and the resulting feeding rates can be explained using

the optimal foraging theory where predators consume prey that lead to the

highest energy gain for the least amount of time and energy input (Boggs et a!.

1984). Naticid gastropod prey preference follows this hypothesis (Dietl &

Alexander 1997). Savini & Occhipinti-Ambrogi (2006) found that moon snails

maximize their energy intake by selecting a specific prey species that they can

consume efficiently, rather than the immediately available species. Euspira lewisii

followed this pattern, except where its preferred prey was not readily available.

Venerupis philippinarum is the numerically dominant species at both study sites,

yet it was avoided in our experiments and the beach shell assemblages, where

other species are available in lower numbers.

Feeding in E. lewisii is a large investment of energy, as they must spend

quite a lot of time and energy drilling through the shell of its prey before feeding

actually begins. It therefore needs to find prey that will facilitate these activities.

Rodrigues et a!. (1987) found that prey was selected based on a shell

morphology that eases handling and reduces energy input. Protothaca

staminea's round and inflated shell morphology facilitates drilling at the umbo

(Reid & Gustafson 1989; Vignali & Galleni 1986). Variations in shell thickness

lead to variations in feeding rates and handling time. Minor changes in shell

thickness can lead to dramatic changes in feeding rate. In a slow feeding

organism, such as E. lewisii, fractions of millimetres can increase drilling time by

44

at least 25 hours (Dietl & Alexander 1997). It may take longer to drill P. staminea

due to its relatively thick shell but it contains more calories than the other two

species (Kirk 2007). Although N. obscurata has the lowest energy content, it may

be selected over V. philippinarum because it has a thinner shell and takes less

time to drill. In P. duplicatus, drilling alone took approximately 36 hours on its

preferred prey species Mya arenaria (Boggs et al. 1984). Finding exact feeding

rates in burrowing snails such as E. lewisii is complicated due to not being able

to directly measure drilling times.

In eastern Canada and USA, moon snail predation on commercially

valuable shellfish has been considered to be high enough to warrant the use of

public funds to control their populations. Beal et a!. (2001) proposed that moon

snails are responsible for 96.5% of the mortality of M. arenaria. Predation is

stated to be the most important factor determining juvenile clam survival in

Maine, USA, where 77% of clam mortality is attributed to the moon snail E. heros

(Beal 2006). In B.C., the code of practice (2002) put out by the B.C. Shellfish

Growers Association listed E. lewisii as one of several species that can have

significant economic impact to the V. philippinarum industry. To protect their

crop, the shellfish growers are removing E. lewisii from the intertidal.

Recent work has shown that feeding rates and impacts may be

exaggerated. Clam deaths by crabs and other predators have been attributed to

moon snails in some studies, implying that moon snail predation was over

emphasized (Beal et a!. 2001). Green (1968) estimated annual mortality rates of

28.2% from skate predation and other shell destroying causes, 14.3% from

45

crowding related causes and only 4% from naticid predation and this was by two

different species. Predation by P. duplicatus was found to be only a minor source

of mortality for G. gemma, one of its preferred prey species (Wiltse 1980a). Miron

et a!. (1985) found that the naticid E. heros, was the predator that had the lowest

feeding rate on all clam species tested compared to two sea star predators in

eastern North America. Feeding rates in P. duplicatus were found to be less than

previously believed (Huebner & Edwards 1981). Our work and the work

performed by Peitso (1980) and Peitso et a!. (1994), demonstrated that the

feeding rates of E. lewisii are much lower than Bernard (1967) originally found.

Our findings as with Peitso (1994) suggest that over a year about 3% of clam

population mortality is due to E. lewisii predation. This study stresses the

importance of understanding the feeding ecology of a predator before suggesting

anti-predation measures.

E. lewisii's avoidance of V. philippinarum, low feeding rate and low

impacts to the bivalve community can be applied to sustainable shellfish

aquaculture practices. The results demonstrate that there is no longer a need to

remove E. lewisii from intertidal lease areas, saving the time and energy of

shellfish growers. The impact to the intertidal ecosystem by aquaculture activities

is thereby reduced and E. lewisii can be left in place to fulfil its ecological

function.

Our study and the results of recent studies can lead to the general

conclusion that moon snails have very low impacts on natural clam populations

through predation activities. Biases on the amounts the moon snail prey on could

46

stem from the incriminating artefacts that are left behind, the bored shell, which

numbers will accumulate over time given a false impression of the numbers of

clams actually preyed upon in a given time period. Studies prior to 1990 have

also been conducted under artificial conditions over short time periods, which

lead to predation overestimates.

Acknowledgments

Many thanks go out to Tracey L'Esperance for all her assistance in the

field. Thanks also to Carolyn Allen, Chris Kowalchuk, Bruno L'Esperance,

Jonathan Whiteley, and Wayne Kowalchuk for their support and assistance on

various aspects of this research. Appreciation also goes out to Jenna Thomson,

Mike White and Charlotte Voss for taking such a keen interest in the project and

helping out with data collection. Mike Hart provided constructive and helpful

comments throughout this research. Funding for this work was provided by an

NSERC strategic grant to L. Bendell-Young.

2.6 Literature Cited

BCSGA. 2002. British Columbia Shellfish Farming Industry - Environment

Management System Code of Practice. <http://bcsga.netfirms.com/wp­

content/uploads/2007/08/enviro-mgmt-code-of-practice 02feb7.pdf>.

Accessed 2007/10/29.

Beal BF. 2006. Biotic and abiotic factors influencing growth and survival of wild

and cultured individuals of the softshell clam (Mya arenaria L.) in eastern

Maine. Journal of Shellfish Research 25(2):461-74.

Beal BF, Parker MR, Veneile KW. 2001. Seasonal effects of intraspecific density

and predator exclusion along a shore-level gradient on survival and growth

47

of juveniles of the soft-shell clam, Mya arenaria L., in Maine, USA. Journal of

Experimental Marine Biology and Ecology 264(2):133-69.

Bernard FR. 1967. Studies on the biology of the naticid clam drill Polinices lewisii(Gould) (Gastropoda Prosobranchia). Fisheries Research Board of Canada

Technical Report 42:1-41.

Boggs CH, Rice JA, Kitchell JA, Kitchell JF. 1984. Predation at a snail's pace:

What's time to a gastropod? Oecologia (Berlin) 62(1 ):13-7.

Commito JA. 1982. Effects of Lunatia heros predation on the population

dynamics of Mya arenaria and Macoma balthica in Maine, USA. Marine

Biology 69(2):187-93.

DeGraaf JD and Tyrrell MC. 2004. Comparison of the feeding rates of two

introduced crab species, Carcinus maenas and Hemigrapsus sanguineus, on

the blue mussel, Mytilus edulis. Northeastern Naturalist 11 (2):163-6.

Dietl GP and Alexander RR. 1997. Predator-prey interactions between the

naticids Euspira heros Say and Neverita duplicata Say and the Atlantic

surfclam Spisula solidissima Dillwyn from Long Island to Delaware. Journalof Shellfish Research 16(2):413-22.

Dudas SE, McGaw IJ, Dower JF. 2005. Selective crab predation on native and

introduced bivalves in British Columbia. Journal of Experimental MarineBiology and Ecology 325(1 ):8-17.

Edwards DC and Huebner JD. 1977. Feeding and growth rates of Polinicesduplicatus preying on Mya arenaria at Barnstable Harbor, Massachusetts.

Ecology 58(6):1218-36.

Green RH. 1968. Mortality and stability in a low diversity subtropical intertidal

community. Ecology 49(5):848-54.

Harbo RM. 2001. Shells and shellfish of the Pacific Northwest. Madeira Park:

Harbour Publishing.

Huebner JD and Edwards DC. 1981. Energy budget of the predatory marine

gastropod Polinices duplicatus. Marine Biology (Berlin) 61 (2-3):221-6.

48

Ivlev VS. 1961. Experimental ecology of the feeding fishes. Scott 0, translator;New Haven: Yale University Press. 302 p.

Kingsley-Smith PR, Richardson CA, Seed R. 2003. Stereotypic and size­selective predation in Polinices pulchellus (Gastropoda: Naticidae) Risso

1826. Journal of Experimental Marine Biology and Ecology 295(2):173-90.

Kirk M. 2007. Movement and foraging behaviours of surf scoters wintering inhabitats modified by shellfish aquaculture. MSs Thesis, Simon FraserUniversity, Burnaby, B.C.

Krebs CJ. 1999. Manly's a. In: Ecological methodology. 2nd ed. Menlo Park,California: Addison-Wesley Educational Publishers, Inc. 483-486 p.

Manly BFJ. 1974. Model for certain types of selection experiments. Biometrics30(2):281-94.

Manly BFJ, Miller P, Cook LM. 1972. Analysis of a selective predationexperiment. American Naturalist 106(952):719-36.

Meyer JJ and Byers JE. 2005. As good as dead? Sublethal predation facilitateslethal predation on an intertidal clam. Ecology Letters 8(2):160-166.

Miron G, Audet 0, Landry T, Moriyasu M. 2005. Predation potential of theinvasive green crab (Garcinus maenas) and other common predators oncommercial bivalve species found on Prince Edward Island. Journal ofShellfish Research 24(2):579-86.

Moran MJ. 1985. Effects of prey density, prey size and predator size on rates offeeding by an intertidal predatory gastropod Morula marginalba Blainville

(Muricidae), on several species of prey. Journal of Experimental MarineBiology and Ecology 90(2):97-105.

Peitso E. 1980. Predation by the moon snail, Polinices lewisii (Gould), on thelittleneck clam, Protothaca staminea (Conrad). MSs Thesis, Simon Fraser

University, Burnaby, B.C.

Peitso E, Hui E, Hartwick B, Bourne N. 1994. Predation by the naticid gastropodPolinices lewisii (Gould) on littleneck clams Protothaca staminea (Conrad) inBritish Columbia. Canadian Journal of Zoology 72(2):319-25.

49

Reid RGB and Gustafson BD. 1989. Update on feeding and digestion in themoon snail Polinices lewisii (Gould, 1847). Veliger 32(3):327.

Rodrigues Cl, Nojima S, Kikuchi T. 1987. Mechanics of prey size preference inthe gastropod Neverita didyma preying on the bivalve Ruditapesphilippinarum. Marine Ecology Progress Series 40( 1-2):87-93.

Savini D and Occhipinti-Ambrogi A. 2006. Consumption rates and preypreference of the invasive gastropod Rapana venosa in the northern Adriatic

Sea. Helgoland Marine Research 60(2): 153-9.

Schwarz, C.J. 2005. Stat 403/Stat 650 - Intermediate sampling and experimentaldesign and analysis - Course notes. Simon Fraser University, Burnaby, B.C.

Thiel M, Ullrich N, Vasquez N. 2001. Predation rates of nemertean predators:The case of a rocky shore hoplonemertean feeding on arnphipods.Hydrobiologia 456:45-57.

Vignali Rand Galleni L. 1986. Naticid predation on soft bottom bivalves: A studyon a beach shell assemblage. Oebalia 13:157-77.

Weissberger EJ. 1999. Additive interactions between the moon snail Euspiraheros and the sea star Asterias forbesi, two predators of the surfclamSpisula solidissima. Oecologia 119(3):461-6.

Wiltse WI. 1980a. Predation by juvenile Polinices duplicatus (Say) on Gemmagemma (Totten). Journal of Experimental Marine Biology and Ecology42(2):187-99.

Wiltse WI. 1980b. Effects of Polinices duplicatus (Gastropoda: Naticidae) oninfaunal community structure at Barnstable Harbor, Massachusetts, USA.Marine Biology (Berlin) 56(4):301-10.

50

CHAPTER 3 EFFECTS OF BIOTURBATION BY LEWIS'SMOON SNAIL (EUSPIRA LEWISII) ON SEDIMENTPROPERTIES AND BIOLOGICAL COMMUNITIES INBRITISH COLUMBIA2

2 The following chapter has been submitted to Journal of Experimental Marine Biology andEcology under the co-authorship of Leah Bendell-Young.

51

3.1 Abstract

Lewis's moon snail, Euspira lewisii, is being manually removed from

intertidal ecosystems in western British Columbia (B.C.) due to its reputation as

an economically detrimental species to the shellfish aquaculture industry. Little is

known about the ecological role of E. lewisii and it is hypothesized that due to its

burrowing activities, E. lewisii has large impacts on the physical, chemical and

biological properties of the sediments. To determine the ecological role of E.

lewisii an exclusion experiment was carried out. The sediment became

significantly less permeable in exclusion cages. There were no significant

differences in terms of sediment grain size profiles. Nutrients accumulated in

exclusion areas but these trends were not statistically significant. The biological

communities in exclusion cages at different tide heights became more

homogenous and tide zones with more diverse communities became very similar

to tide zones with lower diversity. This study stresses the importance of

understanding the function of all the organisms in a community before control

measures are carried out. We recommend that further studies be conducted to

accurately determine E. lewisifs role in nutrient exchanges.

3.2 Introduction

Bioturbation is recognized as an important contributor to ecosystem

processes including sediment modification and nutrient cycling (Lohrer et al.

2004; Thrush & Dayton 2002). Bioturbation is the dominant mode of transport in

the upper centimetres of oceanic sediments. It also affects the composition of

52

marine sediments and influences their role as geochemical sources and sinks

(Thrush & Dayton 2002).

Bioturbation influences a wide range of physical, chemical and biological

variables within the sediment. Grain-size distributions, shear strength, stability,

sediment resuspension, sediment softness, and permeability are all physical

parameters influenced by burrowing activities (Biles et al. 2002; Katrak & Bird

2003; Palomo et al. 2003). Increased permeability allows organic matter, water,

and oxygen to penetrate deeper into the sediment (Biles et al. 2002; Coleman &

Williams 2002; Palomo et al. 2003; Snelgrove 1999; Thrush & Dayton 2002).

Larger animals, such as predators, playa particularly important role in sediment

reworking rates resulting in increased permeability (Thrush & Dayton 2002).

Organisms that burrow and create mounds or tubes generate structure in the

habitat and increase the surface area of the sediment that is in contact with the

water column which helps in nutrient recycling and increases water and oxygen

availability in the sediments (Coleman & Williams 2002; Katrak & Bird 2003;

Lohrer et al. 2004; Snelgrove 1999; Thrush & Dayton 2002). Increased nutrient

fluxes can contribute to increased ecosystem functions such as primary

production and can influence the biological community (Lohrer et al. 2004).

Bioturbation affects infaunal communities through direct disturbance and

through its influences on the physical and chemical nature of the sediments.

Ploughing and moving through the sediment can smother or bury larvae or adult

infauna within the sediment (Ambrose 1991; Gee et al. 1985). Bioturbators can

have negative effects on infaunal densities and clam growth rates (Beal et al.

53

2001). Snelgrove (1999), however, found that disturbance through bioturbation

increased infaunal diversity. The increased surface area created by burrowing

activity and burrow construction provides favourable conditions for microbial

activity and microphytobenthos productivity (Biles et al. 2002; Lohrer et al. 2004).

The modification of the physical and chemical properties through bioturbation can

increase the three-dimensional nature of the sediment allowing more organisms

to live in these areas (Katrak & Bird 2003; Palomo et al. 2003; Thrush & Dayton

2002). Small-scale disturbances that occur through burrowing and predatory

activities create patches in the habitat, which increases the heterogeneity and

diversity and play an important role in structuring communities (Biles et al. 2002;

Escapa et al. 2004; Raghkumar & Anil 2003).

The structure of soft-sediment habitats, including biodiversity, is tightly

linked to the functioning of those ecosystems (Raghkumar & Anil 2003). Several

studies have shown that decreases in biodiversity lead to loss of ecosystem

function (Chalcroft & Resetarits 2003; Duarte 2000; Lohrer et al. 2004). Losing

one species, especially if the species is a large, bioturbating predator can have

severe impacts on ecosystem function and can influence benthic diversity

(Coleman & Williams 2002; Lohrer et al. 2004). Losing the species that influence

the cycling of nutrients can have significant consequences on many ecosystem

processes. To effectively manage our coastal and offshore waters, it is essential

to understand the relationship between biodiversity and ecosystem functioning

(Raghkumar & Anil 2003). Understanding the role of all species in a community

54

has become more important than a simple biodiversity inventory (Raghkumar &

AniI2003).

Euspira lewisii is a large, infaunal predator of the family Naticidae found in

intertidal to subtidal habitats on the west coast of North America from Mexico to

southern Alaska. This species burrows through the sand at depths of 10-20cm

searching for and consuming clams. Feeding rates for this species were

originally thought to be high at 0.25 clams/snail/day, however, recent studies

have shown that this rate may be much lower at 0.07-0.09 clams/snail/day

(Bernard 1967; Cook 2008; Peitso 1994). Shellfish managers consider E. lewisii

a pest species to the shellfish aquaculture industry and for this reason it is being

removed from intertidal lease areas (Bernard 1967).

Little is known as to the effects of moon snails as bioturbators. Work on

this species has focused on feeding ecology or development. No work has been

conducted on the effects of moon snails on the physical or chemical properties of

the sediment. Wiltse (1980) showed that Polinices duplicatus, a moon snail

species from the east coast of North America, decreased diversity. Species

richness, evenness and heterogeneity all decreased with increasing moon snail

density. Wiltse's (1980) study, as with several others, focuses only on the effects

of moon snails as predators.

Here, our objective is to determine the role of E. lewisii as bioturbators of

intertidal sediments. The influences on the physical and chemical properties of

the sediment and on the biological community are examined. The focus is on the

penetrability, water content, grain size distributions, and the ammonium, carbon

55

and phosphate concentrations of the sediment. To determine these properties an

exclusion experiment was conducted to mimic the impact of the removal of E.

lewisii from intertidal shellfish leases. It is expected that the exclusion cages will

show decreased penetrability of the sediment, decreased water content due to

the decrease in permeability, an accumulation of fine and silt sediment particles,

an accumulation of ammonium, organic matter and phosphate within the

sediment, and shifts in the biological community driven by the altered physical

and chemical state of the sediment.

3.3 Methods

3.3.1 Study Areas

Field research was conducted in southern B.C. (Figure 3.1) at Fillongley

Provincial Park, on Denman Island (49°31'59"N, 124°49'0"W) and Shingle Spit,

on Hornby Island (49°31'0"N, 124°37'59"W). Both sites are home to a known

population of E. lewisii at a density of approximately 0.2snails/m2 (Cook 2008).

Venerupis philippinarum, the commercially valuable Manila clam and Protothaca

staminea, the native Pacific littleneck clam dominate the bivalve community at

these sites. Nuttallia obscurata, the varnish clam, a recent introduction to

southern B.C., as well as several other clam species, are also found at these

sites.

At each site, a 60 m wide strip of the intertidal was selected based on

preliminary surveys that showed the area was representative of the intertidal

area at each site. A tide height of 2.3 m above chart datum was the top of the

56

strip as this was towards the high end of the moon snail intertidal range. The strip

was stratified into a high, mid and low zone in order to reduce the variability

across the intertidal. Table 3.1 shows the tide heights and length of each stratum

at each site.

Table 3.1. Length of the three tide strata at each site.

Zone Length (meters)

Tide Zone Tide Height Fillongley Shingle Spit

(m above chart datum)

High 2.3-1.7 30 25

Mid 1.7-1.3 67 12

Low 1.3 - 0.7 80 20

Within each stratum, coordinates were selected at random for the

locations of the exclusion cages, control cages, and control areas. Four exclusion

cages, four control areas and two control cages were placed in 3 strata at 2 sites

for a total of 24 exclusion cages, 24 control areas and 12 control cages.

3.3.2 Cage Design

Exclusion cages, 1x1 xO.3 m, enclosing an area of 1m2 with mesh having a

3cm aperture, were constructed to determine the role of E. lewisii as a

bioturbator. The cages were designed so that infaunal organisms were free to

enter and exit the cages while excluding E. lewisii. Cages were dug into the

sediment to a depth of 0.2m, leaving 0.1 m exposed at the surface. This design

mimics the impact of anti-predator netting used in aquaculture practices as large

predators are excluded. Due to its infaunal nature, its large size, and its

57

BritishColumbia

Vancouver 'Island

Scale

IwoooI IwoooI

Figure 3.1.Map showing the location of the study sites on Denman and Hornby Islands(Based onhttp://atlas.nrcan.gc.ca/site/english/maps/reference/outlinecanada/canada01,http://atlas.nrcan.gc.ca/site/english/maps/reference/outlineprov terr/bc outline)

distribution to depths of 20cm, E. lewisii is the species that would have the

strongest effects to the infaunal communities and properties at the study sites at

interest. It can therefore be assumed that any significant findings within the

sediment can be attributed to the exclusion of moon snails.

Sediment was sieved back into the cage through 6 mm mesh and all

macroinfauna was removed. Whiteley (2005) found that only 10% of species and

58

25% of species count data were lost using 6mm versus 1mm sieve mesh. The

larger aperture mesh also allowed for increased sampling as field researchers

were not limited by the lengthy sieving time through 1mm mesh. Control cages

used the same frame as the exclusion cages but only 3 sides were covered with

mesh to test for alterations to water and sediment flow and shading due to the

cage structure. Control areas were marked with rope that was held in place in the

four corners using rebar sunk into the sediment. Control cages, control areas and

exclusion cages were prepared in the same way differing only in the cage type or

lack of cage used. The cages were dug in May and June 2005 and sealed until

the summer of 2006. In 2006, the cages were opened and dug up and data were

collected on the physical, chemical and biological properties.

3.3.3 Sediment Characteristics

A Durham S-170 pocket penetrometer was used to collect sediment

penetrability measurements for each cage or control area. Three measurements

were taken for each replicate to account for variability within the cage itself.

Three 3.8cm diameter bulk sediment cores were taken to a depth of 10cm.

The samples were immediately put on ice and frozen for determination of water

content, grain size and chemical concentrations in the lab in September 2006.

One hundred grams of each sample was weighed out, dried in a drying

oven for at least 48 hours and weighed to determine percent water content. The

dried sediment was separated into 4 grain size fractions through wet sieving

using 3 sieves: gravel (>2mm), coarse sand (>0.5mm), fine sand (>0.0625mm).

59

Each size fraction was dried for 24 hours and weighed. The silt fraction was

calculated from the total dry weight less the weight of the three larger fractions.

Using the total dry weight the percent of each fraction was calculated.

3.3.4 Sediment Chemistry

The concentration of organic matter was determined through loss on

ignition. 0.5g of sample were weighed and dried for 24 hours in a drying oven.

The dry sample was weighed and ashed in a muffler furnace at 400°C for 1 hour.

The samples were cooled and weighed.

Ammonium concentrations within the sediments were determined using

the indophenol blue method of Page (1982), a method deemed acceptable for

intertidal sediments which are between soils and marine sediments. Ten grams

of sample were mixed with 2M potassium chloride. After the sediments had

settled EDTA, phenol-nitroprusside solution and a buffering solution were

combined and heated with 5mL of the sample. After heating for 30 minutes at

40°C, the sample absorbance was read in a spectrophotometer at 636nm.

Weights were then calculated based on the slope of the calibration curve

determined before sample analysis.

The sulfuric acid - nitric acid digestion technique and

Vanadomolybdophosphoric Acid colorimetric method were used to extract

phosphate from the intertidal sediments based on Greenberg (1992). Five grams

of sediment was placed in a Teflon tube and 0.1 002N sulfuric acid and

concentrated nitric acid were added. The samples were placed in a CEM MDS-

60

2000 Microwave for 18 minutes at 200°C. Each sample was filtered and diluted

to 100ml using distilled water. 17.5mL of the sample was mixed with Vanadate­

Molybdate reagent and distilled water. The sample absorbances were read at

470nm on a spectrophotometer. The phosphate concentrations were determined

using a calibration curve.

3.3.5 Biological Community

When the cages were extracted from the intertidal, all the sediment in the

cage was sifted through a 6mm mesh. All of the macroinfauna in the cage was

identified and counted. All bivalves were measured using vernier calipers to the

nearest 0.1 mm. Measurements of species richness, evenness and the Shannon­

Weiner diversity index were calculated.

3.3.6 Analyses

In order to present general trends for this experiment, the data for each

treatment was pooled across all tide heights and the results presented represent

the total intertidal area used in the study.

As the data were not normally distributed and could not be transformed, all

statistical analyses were carried out using non-parametric Kruskal-Wallis tests.

Bonferroni corrections were applied to all the analyses which reduced the

significant p-value to 0.017.

Similarities within the biological communities at the study sites were

compared using a Bray-Curtis similarity index. Values close to one indicate a

61

high degree of similarity between communities while values close to zero indicate

dissimilarity. The results are displayed in a tree-diagram.

3.4 Results

3.4.1 Physical Characteristics of the Sediment

The unconfined compressive strength of the sediments at both study sites

was found to be significantly higher in exclusion cages (Figure 3.2, Table 3.2).

No significant differences were found in terms of sediment water content (Figure

3.3).

1.8 .----------------------------,

0.6

_ Exclusion

[:==J Control AreaControl Cage

1.6

1.2

1.4

1.0

0.4

0.2

0.0 ...L.- _

.r.+-'OJC

~+-'(f)Q) 0.8>'i/.iCf)

~0-Eoo

Fillongley Shingle Spit

Study Site

Figure 3.2.Compressive strength of the sediments at each study site under each treatment(Medians, error bars represent interquartile range).

62

18 .,------------------------------,

_ Exclusion

c::=:J Control AreaControl Cage

6

8

4

2

o --'--------

12

10

.......cQ)

.......cooI-Q)

.......

~Q)0)ro.......cQ)

eQ)

0....

Fillongley Shingle Spit

Study Site

Figure 3.3.Water content of the sediments at each study site under each treatment(Medians, error bars represent interquartile range).

Table 3.2. Summary of the non-parametric Kruskal-Wallis analyses on the physicalproperties of the sediments between treatments at both sites. * indicates asignificant result and ** indicates a marginally significant result.

StudyChi-

Physical Property squared p-value Significant?Site

Value

Compressive Strength 11.01 0.0041 *Fillongley

Water Content 2.12 0.347

Compressive Strength 18.25 0.0001 *ShingleSpit Water Content 0.22 0.8948

3.4.2 Grain Size Analyses

Although we expected to see an accumulation of fine sand and silt in the

exclusion cases this was not the case. We did not detect any significant trends in

63

terms of the grain size profiles of the sediment at either site (Figure 3.4, Table

3.3).

100

~0 80----Qj>C\l 60.....(9(j)OJ

40C\l--c(j)U..... 20(j)

0..

0

-,

I,

........ 60~0

----"D 50cC\lif)

40(j)(/J.....C\l 300(.)

I(j)20OJco--c

(j) 10u.....(j)

0.. 0Fillongley Shingle Spit

Study Site

Fillongley Shingle Spit

Study Site

1.5

10

2.0

2.5

0.5

3.5 -,-------------------,

3.0~o----=:U)(j)OJco--c~(j)

0..

,

II

50~0----"0 40cC\lif)

(j) 30c

u:::(j) 20O'lC\l--c(j) 10u.....(j)

0..0

Fillongley Shingle Spit

Study Site

Fillongley Shingle Spit

Study Site_ Exclusion

c:::=J Control AreaControl Cage

Figure 3.4.Percentages of gravel, coarse sand, fine sand, and silt at each site under eachtreatment (Medians, error bars represent interquartile range).

64

Table 3.3. Summary of the non-parametric Kruskal-Wallis analyses on the grain sizeanalyses between treatments at both study sites. * indicates a significant resultand ** indicates a marginally significant result.

Study Physical Property Chi- p-value Significant?Site squared

Value

Percentage of Gravel 5.14 0.0765

Percentage of Coarse Sand 5.16 0.0756Fillongley

Percentage of Fine Sand 2.99 0.2236

Percentage of Silt 0.22 0.8942

Percentage of Gravel 1.77 0.4132

Shingle Percentage of Coarse Sand 4.9 0.0865

Spit Percentage of Fine Sand 0.09 0.9536

Percentage of Silt 0.02 0.9919

3.4.3 Chemical Properties of the Sediment

There were no statistically significant trends in terms of nutrient

concentrations at the Fillongley field site (Figure 3.5, Table 3.4). There are

indications of slight accumulations of ammonium and carbon in exclusion cages.

At Shingle Spit no significant accumulations of nutrients were detected

but, as was seen at Fillongley, there is a possibility of carbon and ammonium

accumulations in exclusion cages (Figure 3.5, Table 3.4).

65

---.OJ 0.012--OJE--....-

0.010c0

:;:::;C\l 0.008...........cQ)0 0.006c0U 0.004E::J'c 0.0020EE 0.000«

---.OJ 0.16--OJE 0.14c0 0.12:;:::;C\l.... 0.10.-cQ)

0.080c0 0.06UQ)

0.04.-C\l.cQ. 0.02en0.c 0.00

0...

T

Fillongley Shingle Spit

Study Site

T T

;:r:;

OJ 0.18 .--------------------,

--E 0.16

-- 0.14c2 0.12~C 0.10

~ 0.08c8 006

§ 0.04

~ 0.02U 0.00 -'---.....,r'-L'-------"a...y..J.L-----.J

Fillongley Shingle Spit

Study Site

_ Exclusion

c::::=:::::J Control AreaControl Cage

Fillongley Shingle Spit

Study SiteFigure 3.5.Nutrient concentrations of ammonium, carbon and phosphorous for each

treatment at each study site (Medians, error bars represent interquartile range).

Table 3.4. Summary of the non-parametric Kruskal-Wallis analyses on the sedimentnutrient characteristics between treatments at both sites. * indicates asignificant result and ** indicates a marginally significant result.

Study Site Nutrient Chi- p- Significant?squared valueValue

Ammonium 2.58 0.2754

Fillongley Carbon 2.4 0.3017

Phosphorous 6.23 0.0444

Ammonium 3.26 0.1955

ShingleCarbon 3.97 0.1372

Spit

Phosphorous 5.94 0.0512

66

3.4.4 Biological Community

At Fillongley, the high and mid exclusion areas were closely similar

(Figure 3.7). Included in this grouping yet less similar were the control area and

control cage for the high zone. Excluding E. lewisii makes the community more

similar to that found in the high zone, a community of lower diversity (Figure 3.6).

Based on baseline density measurements these communities show marginal

significant differences (Wilcoxon, i =5.05, P =0.02). The removal of moon

snails from the low zone had the lowest impact. The communities in the

exclusion areas in the low zone were similar to communities of the control cages

and control areas of the low and mid zones.

o -L..- _

12

*_ High

10 c:::==J MidLow

(/)(/) 8Q)c.c()

ex: 6C/)Q)

'uQ)

4Q.(f)

2

Fillongley Shingle Spit

Study Site

Figure 3.G.Total invertebrate species richness for each tide height at both sites. * indicatesa significant result (Medians, error bars represent interquartile range).

67

0.0

0.2

...cQ) 0.4"0!EQ)

8~·Cco"E 0.6Ci5

0.8

1.0

IIII

HE ME HCC HCA LE LCC LCA MCA MCC

Treatment

Figure 3.7.Tree diagram illustrating the Bray-Curtis similarities for the Fillongleycommunity at all tide heights under each treatment. H =high, M =mid, L =low.E =Exclusion, CA =Control area, CC =Control cage.

At Shingle Spit, there were three groupings amongst the communities

(Figure 3.8). The exclusion communities in the low and the mid zones were

similar to the control cages and control areas of the low zone. The similarities

amongst the exclusion areas indicates the homogenization of these communities.

The low zone at Shingle Spit had lower species richness than the mid zone

68

(Figure 3.6). There was a grouping of the mid and high control cages with the

mid control areas. The high exclusion community was similar to that of the high

control areas.

0.0

0.2

.....c

.~ 0.4IEQ)

8.?:''Cro'E 0.6U5

0.8

1.0

III

I

LCC LE ME LCA MCA MCC HCC

Treatment

HE HCA

Figure 3.8.Tree diagram illustrating the Bray-Curtis similarities for the Shingle Spitcommunity at all tide heights under each treatment. H = high, M = mid, L = low.E = Exclusion, CA = Control area, CC = Control cage.

69

3.4.5 Control Cage Impacts

Due to the low number of replicates used to test the effects of the cage

structure on the parameters tested in this experiment, it was hard to determine

whether the cages had a significant effect. Cage structures had impacts to grain

size profiles which could be due to the way the cages were prepared for

exclusion (Table 3.3). There also was a marginal impact of the cage structure on

phosphate concentrations (Table 3.4). In most cases it appears that the control

cages showed similar results to the control area implying that the cage structure

did not have a large impact on the chemical, physical and biological

measurements taken throughout the course of this research.

3.5 Discussion

The goal of the work presented was to determine the ecological role of E.

lewisii in terms of how it influences the functioning of the intertidal ecosystem.

This role is especially important to determine in light of the fact that E. lewisii is

being treated as a pest species and manually removed from intertidal shellfish

lease areas, a management strategy that does not take into account any function

this species may have in the ecosystem. More studies like this one are needed to

understand the ecological function of the species that we are busy eradicating.

The exclusion of E. lewisii had a significant impact on the penetrability of

the sediment. The activities of bioturbators break up the surface of and displace

sediment, creating interstitial spaces which are available for water and make

sediment less compact (Katrak & Bird 2003; Lohrer et al 2004; Volkenborn et a!.

2007). Larger organisms, such as E. lewisii, are particularly important for their

70

role in the redistribution of sediments (Snelgrove 1999). The burrowing crab,

Chasmagnathus granulatus (Escapa et al. 2004; Palomo et al. 2003), the

lugworm, Arenicola marina (Volkenborn et al. 2007), the ghost shrimp Trypaea

australiensis, and the semaphore crab Heloecious cordiformis (Katrak & Bird

2003) have all been shown to decrease sediment softness and increase the

water content of the sediment through their bioturbatory activities.

Sediment penetrability and water content have significant consequences

to infaunal organisms. Larger infaunal bioturbators and those that build deeper

burrows within the sediment, extend the available habitat for other infaunal

organisms by creating interstitial spaces thereby increasing the depth to which

water, nutrients and oxygen penetrate the sediments (Escapa et al. 2004; Katrak

& Bird 2003; Snelgrove 1999). This would reduce competition for space, oxygen

and nutrients in areas of high infaunal density (Widdicombe & Austen 1998). Low

densities of T. australiensis created oxidizing conditions within the sediments

(Katrak & Bird 2003). Oxygen within the sediment decreases sulphide

concentrations and can benefit infaunal organisms with low sulphide tolerances

(Morrisey et al. 1999; Volkenborn & Reise 2007). Maintaining permeable

sediments is essential in locations, such as Fillongley, where the sediment is on

average finer grained and interstitial spaces are smaller in fine-grained sediment

and more susceptible to clogging (Volkenborn et al. 2007).

Permeability is directly related to grain size (Katrak & Bird 2003;

Volkenborn et al. 2007). Sediments become less permeable in areas where there

are many fine-grained and silt particles as these clog the interstitial spaces

71

(Volkenborn et al. 2007). We did not see the predicted significant trends in the

grain size data due to the heterogeneous nature of the sediments at the study

sites. This prediction was based on previous work that showed that the burrowing

activities of the amphipod Corophium vo/utator (Biles et al. 2002), T. australiensis

(Katrak & Bird 2003), and A. marina (Volkenborn et al. 2007) caused the

resuspension of fine grained sediments, which altered sediment grain profiles.

For future work, smaller and more homogeneous areas of the intertidal should be

selected and a larger sampling size should be used to better determine the

impacts of E. lewisii on grain size. The preparation of the study areas could also

have led to the lack of significance through the action of sieving the sediments

facilitating the removal of finer grained sediment through tidal action.

Increased permeability increases pore-water nutrient exchanges (Lohrer

et a!. 2004; Volkenborn et al. 2007). Bioturbation is important in intertidal regions

as it increases the depth to which chemicals and nutrients penetrate the

substratum (Volkenborn et al. 2007). When lugworms are excluded, organic

matter accumulated at the surface of the sediment (Volkenborn et al. 2007).

Bartoli et al.'s (2001) study in Italy demonstrates that accumulated organic

carbon under shellfish aquaculture netting led to anoxic conditions and bivalve

mortality. Volkenborn et al. (2007) found the decrease in pore-water spaces

resulting from the exclusion of the bioturbator A. marina led to accumulations of

several nutrients in the sediment. The burrowing urchin Echinocardium and

Austrovenus stutchburyi, a bivalve that actively ploughs across the surface of the

sediment, both had significant effects on the release of NH4-N from the

72

sediments (Lohrer et al. 2004; Thrush et al. 2006). The experimental design used

in this study may have prevented the detection of significant effects of E. lewisii

on nutrient cycling therefore further work in this area is recommended.

The exclusion of large organisms including E. lewisii led to the

homogenization of intertidal biological communities. The mid and low zone

communities were similar at Shingle Spit. The communities in the high exclusions

at both sites and the Fillongley mid exclusion were also found to be very similar.

This is problematic because the high communities are those with the lowest

species richness and diversity. Through its influences on the physical properties

of the sediment E. lewisii may have a positive impact of other infaunal species.

Burrowing to a depth of approximately 20 cm, E. lewisii would supply organisms

living at this depth with water containing nutrients and oxygen (Bernard 1967).

Bioturbators create favourable conditions for other organisms through increased

oxygenation, increasing the available habitat, which supports higher infaunal

densities and allows them to live deeper in the sediment which leads to

competitive release and protection from predators (Escapa et a1.2004; Palomo et

al. 2003; Widdicombe & Austen 1998). Through these and other processes,

bioturbation enhances diversity (Snelgrove 1999).

This study stresses the importance of understanding the role of an

organism before management strategies are carried out. Infaunal organisms are

very important as they are responsible for their habitat's structure and have

crucial roles in many population, community and ecosystem processes (Thrush &

Dayton 2002). The preliminary findings here on sediment compaction and the

73

biological communities imply that this species may be an ecosystem engineer

because it modifies the physical properties of the sediment and facilitates the

survival of other organisms (Coleman & Williams 2002). Removing ecosystem

engineers can be especially detrimental as they are responsible for ecosystem

function and biological diversity (Coleman & Williams 2002; Volkenborn et al.

2007). In some marine systems, key species have been linked to a single role in

terms of ecosystem function so losing it can have devastating effects (Lohrer et

al. 2004). Increasing numbers of studies are showing the importance of each

species in a community and the link between species richness and ecosystem

function (Duarte 2000). It is important that it not be assumed that functionally

similar organisms such as predators all have identical functions in the community

as each species can have an individual function (Chalcraft & Resetarits 2003).

With further work on E. lewisii it is very possible that this species will be linked to

nutrient cycling and ecosystem functioning. Not enough is known to determine

which species are critical so we should consider all species important (Snelgrove

1999). Species loss and even simply density changes, through activities such as

E. lewisii removal, can lead to losses in biodiversity, resilience or provision of

ecosystem services (Thrush & Dayton 2002).

Acknowledgments

We are extremely grateful to 1. L'Esperance for all her assistance in the

field and support in the lab. Much appreciation goes to J. Whiteley and M. Hart

for their constructive criticisms and guidance on various aspects of this research.

Thanks also to C. Allen, C. Kowalchuk, B. L'Esperance, and W. Kowalchuk for

74

their support and assistance. Funding for this work was provided by an NSERC

strategic grant to L. Bendell-Young.

3.6 Literature Cited

Ambrose WG, Jr. 1991. Are infaunal predators important in structuring marine

soft-bottom communities? American Zoologist 31 (6):849-60.

Bartoli M, Nizzoli D, Viaroli P, Turolla E, Castaldelli G, Fano EA, Rossi R. 2001.

Impact of Tapes philippinarum farming on nutrient dynamics and benthic

respiration in the Sacca di Goro. Hydrobiologia 455:203-212.

Beal BF, Parker MR, Veneile KW. 2001. Seasonal effects of intraspecific density

and predator exclusion along a shore-level gradient on survival and growth

of juveniles of the soft-shell clam, Mya arenaria L., in Maine, USA. Journal ofExperimental Marine Biology and Ecology 264(2): 133-69.

Bernard FR. 1967. Studies on the biology of the naticid clam drill Polinices lewisii(Gould) (Gastropoda Prosobranchia). Fisheries Research Board of Canada

Technical Report 42:1-41.

Biles Cl, Paterson DM, Ford RB, Solan M, Raffaelli DG. 2002. Bioturbation,ecosystem functioning and community structure. Hydrology and Earth

System Sciences 6(6):999-1005.

Chalcraft DR and Resetarits WJ,Jr. 2003. Predator identity and ecological

impacts: Functional redundancy or functional diversity? Ecology 84(9):2407­

18.

Coleman FC and Williams SL. 2002. Overexploiting marine ecosystem

engineers: Potential consequences for biodiversity. Trends in Ecology &Evolution 17(1 ):40-4.

Cook N. 2008. Feeding ecology and bioturbation: determining the ecological role

of Euspira lewisii. MSc Thesis, Simon Fraser University, Burnaby, B.C.

Duarte CM. 2000. Marine biodiversity and ecosystem services: An elusive link.

Journal of Experimental Marine Biology and Ecology 250(1-2): 117-31.

75

Escapa M, Iribarne 0, Navarro D. 2004. Effects of the intertidal burrowing crabChasmagnathus granulatus on infaunal zonation patterns, tidal behavior, andrisk of mortality. Estuaries 27(1 ):120-31.

Gee JM, Warwick RM, Davey ..IT, George CL. 1985. Field experiments on therole of epibent~licpredators in determining prey densities in an estuarinemudflat. Estuarine, Coastal and Shelf Science 21 (3):429-48.

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Lohrer AM, Thrush SF, Gibbs MM. 2004. Bioturbators enhance ecosystemfunction through complex biogeochemical interactions. Nature (London)431 (7012): 1092-5.

Morrisey OJ, DeWitt TH, Roper OS, Williamson RB. 1999. Variation in the depthand morphology of burrows of the mud crab Helice crassa among differenttypes of intertidal sediment in New Zealand. Marine Ecology Progress Series182:231-242.

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Raghukumar Sand Anil AC. 2003. Marine biodiversity and ecosystemfunctioning: A perspective. Current Science 84(7):884-92.

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77

CHAPTER 4 CONCLUSIONS ANDRECOMMENDATIONS

78

4.1 Conclusions

Euspira lewisii is a species of naticid snail native to the west coast of

North America. Due to its predatory nature and the way in which it attacks its

prey, this species has been presented as a hindrance to clam aquaculture in

British Columbia. In response to its reputation, E. lewisii is manually removed

from the intertidal by shellfish growers. The goals of this study were to fill the

gaps in knowledge about this species and gain understanding as to its feeding

ecology and functional role in intertidal ecosystems by mimicking the manual

removal through an exclusion experiment.

This work demonstrates that E. lewisii has distinct prey preferences on the

native littleneck clam, Protothaca staminea and avoids the commercially valuable

Manila clam, Venerupis philippinarum. This feeding pattern was observed in both

experiments and collected drilled shells and could be attributed to the

stratification of different bivalve species within the sediment. The feeding rate on

a variety of prey species was found to be only O.09c1ams/day or 1 c1am/14 days.

The feeding rate was species dependent and was slower for non-preferred prey

types. This would be a maximal rate for E. lewisii as it was determined in the

summer when feeding rates are highest. At the determined feeding rate, E.

lewisii would have very low impacts on the bivalve communities at the study

sites. Due to the high densities of clams in these areas and the slow feeding rate,

only 3% of the bivalve community is consumed in one year and that is feeding at

a constant, maximal feeding rate for 12 months. Realistically the impact would be

even lower.

79

The exclusion experiment revealed that E. lewisii does playa role in the

intertidal ecosystem. Sediment permeability decreased in the absence of this

bioturbator as was expected. The effects on grain size and sediment chemistry

were not statistically significant yet showed trends towards accumulations of

several nutrients in exclusion areas. These alterations to the physical and

chemical properties of the intertidal community impact the biological properties.

Several of the exclusion communities at various tide heights became very similar

indicating a homogenization of the intertidal towards less diverse communities.

The results of the exclusion experiment demonstrate the importance of E. lewisii

in this community and stress the importance of a full understanding of the role of

each species in an ecosystem prior to carrying out control measures.

The results of the work presented here provide evidence of the limited

impact of E. lewisii on bivalve communities as well as the importance of the

ecological function of this species in the intertidal. These results are conclusive

enough to advise the shellfish aquaculture industry that control measures of E.

lewisii are not necessary. Even though the evidence is strong more work is

needed to get a full understanding of the role of this species in the ecosystem.

4.2 Future Work

I recommend that more work be done on the bioturbation activities of E.

lewisii. A better design for this experiment would be to compare enclosures to

exclusion cages. If this design were to be used, larger cages or a fencing

technique would be recommended allowing more mobility for the enclosed moon

80

snails. This would allow for better generalizations about the impacts this species

has on the physical, chemical and biological properties of the intertidal.

To understand the extent to which this species influences sediment grain

size profiles, I recommend that smaller, more homogeneous sections of the

intertidal be used to reduce the variability that comes from the patchy nature of

the sediments at the study sites. I would also recommend that a larger sample

size be used.

The trends towards nutrient accumulations under E. lewisii exclusion

conditions imply that with further work significant trends may be detected. It is

therefore recommended that bulk cores be taken at regular intervals to track the

changes of the nutrient concentrations over time. The time scale for the current

study may have too long and the nutrient concentrations would be more

influenced by daily tidal fluctuations than the presence or absence of E. lewisii.

Porewater peepers should also be used to determine the depth to which E.

lewisii influences nutrient fluxes from the sediment. An alternative to field studies

would be to carry out measurements in lab mesocosms, enabling control over as

many variables as possible and to use more accurate measurement techniques.

4.3 Recommendations

The results from this study can be used to advise the clam aquaculture

industry. The feeding experiments demonstrate that E. lewisii is not detrimental

to the industry in that they avoid Venerupis philippinarum, they feed at a low rate,

and natural and aquaculture tenure densities the numbers of clams consumed

81

are extremely low. For these reasons it is no longer necessary to recommend or

continue practicing the manual removal of moon snails from intertidal areas. It

can also be stated that E. lewisii alters sediment properties and further work

might show that this species is a benefit to infaunal organisms including those

inhabiting shellfish leases.

82

APPENDICES

Appendix A: Exclusion Experiment By-Tide-Height Results

1.6 1.6

A B1.4 1.4

N N

E Eu 1.2 u 1.2OJ --OJC ~

~

..c 1.0 ..c 1.0 _ ExclusionOJ ......

OJC C c::::::::::J Control AreaQ) Q).... 0.8 .... 0.8 Control Cageti5 ti5Q) Q)> 0.6 >·w ·w 0.6(/) (/)Q) Q).... ....0- 0.4 0- 0.4E E0 0U

02U

0.2

0.0 0.0High Mid Low High Mid Low

Tide Height Tide HeightCompressive strength of the sediment at Fillongley (A) and Shingle Spit (8) in each of the

treatments at each tide height (Medians, error bars represent interquartilerange).

83

20 20

A B~

~

~0 ~'-'

C 15 C 15Q) Q)

c ......c

0 00 0 - Exclusion.... ....Q) Q)

c=::J Control Area...... 10 ...... 10~

cuS Control Cage

Q) Q)OJ OJcu cu...... ......c cQ) 5 Q) 5u u.... ....Q) Q)

n... n...

0 0High Mid Low High Mid Low

Tide Height Tide Height

Percentage of water in the sediment at Fillongley (A) and Shingle Spit (8) in each of thetreatment conditions at each tide height (Medians, error bars representinterquartile range).

84

Summary of the non-parametric Kruskal-Wallis analyses on the physical properties of thesediments between treatments at each site and at each tide height. * indicates asignificant result and ** indicates a marginally significant result.

Study Site Physical Tide Chi- p- Significant?Property Height squared value

Value

High 8.22 0.0164 *

CompressiveMid 1.5 0.4724

Strength

Low 4.05 0.1321Fillongley

High 4.32 0.115

WaterMid 1.95 0.3779

Content

Low 9.44 0.0089 *

High 12.46 0.002 *

CompressiveMid 10.74 0.0047 *

Strength

Shingle Low 2.54 0.2804

Spit High 0.91 0.6342

WaterMid 2.6 0.273

Content

Low 1.77 0.4125

85

100 100A B

80 80~ ~0 ~~

ill ill> 60 > 60co co.... ....

l') l')(J) (J)OJ OJco 40 co 40C -c(J) (J)u u.... ....(J) (J)

n... n...20 20

0 0High Mid Low High Mid Low

Tide Height Tide Height

_ Exclusion

c::=::J Control AreaControl Cage

Percentage of gravel in the sediment at Fillongley (A) and Shingle Spit (B) in each of thetreatment conditions at each tide height (Medians, error bars representinterquartile range).

60 60

A B~

50 ~ 50-:!2.0~'-'

u uc cco 40 co 40(f) (fJ

(J) (J) _ Exclusionen en

c:::::=J Control Area.... ....CO 30

CO 300 0 Control Cage0 0(J) (J)OJ OJco 20 co 20...... ......c c(J) (J)u u.... ....(J)

10(J)

10D... D...

0 0High Mid Low High Mid Low

Tide Height Tide Height

Percentage of coarse sand in the sediment at Fillongley (A) and Shingle Spit (B) in each ofthe treatment conditions at each tide height (Medians, error bars representinterquartile range).

86

50 50

A B

~ 40---.

40~0 0......... ........."0 "0C Cro ro

(J) 30 (J) 30Q) Q) _ Exclusionc c

u:: u:: c==:J Control AreaQ) Q) Control Cage0) 20 0) 20ro roC -cQ) Q)u u'- '-Q)

10Q)

100- 0-

a a I~High Mid Low High Mid Low

Tide Height Tide Height

Percentage of fine sand in the sediment at Fillongley (A) and Shingle Spit (B) in each of thetreatment conditions at each tide height (Medians, error bars representinterquartile range).

3.0 3.0

A B2.5 2.5

~---.~

~ 2.0 0 2.0.........~ ~

U5 U5Q) Q)0) 1.5 0) 1.5ro ro- -c cQ) Q)u u'- 1.0 '- 1.0Q) Q)0- 0-

0.5 0.5

0.0 0.0High Mid Low High Mid Low

Tide Height Tide Height

_ Exclusion

c=:::J Control AreaControl Cage

Percentage of silt in the sediment at Fillongley (A) and Shingle Spit (B) in each of thetreatment conditions at each tide height (Medians, error bars representinterquartile range).

87

Summary of the non-parametric Kruskal-Wallis analyses on the grain size analysesbetween treatments at each site and at each tide height. * indicates a significantresult and ** indicates a marginally significant result.

Study Site Physical Tide Chi- p- Significant?Property Height squared value

Value

High 3.64 0.1619Percentage

Mid 0.84 0.6564of Gravel

Low 5.83 0.0541

High 7.5 0.0235Percentageof Coarse Mid 0.37 0.8294Sand

Low 4.34 0.1142Fillongley

High 1.31 0.5195Percentage

Mid 1.19 0.5515of Fine Sand

Low 8.26 0.0161 *

High 15.74 0.0004 *

PercentageMid 2.47 0.2904of Silt

Low 7.25 0.0267

High 4.66 0.0972

PercentageMid 2.37 0.3061

of Gravel

Low 1.25 0.534

High 6.48 0.0392Percentageof Coarse Mid 1.36 0.5071Sand

Shingle Low 1.19 0.5527

Spit High 2.64 0.2667

PercentageMid 5.98 0.0502

of Fine Sand

Low 1.26 0.5317

High 1.46 0.4806

PercentageMid 1.44 0.4855

of Silt

Low 4.3 0.1163

88

0.012 0.012A B

~

OJ OJ-- 0.010 -- 0.010OJ OJE -Sc ca 0.008 a 0008~

.~

..... .....c C<IJ <IJu 0.006 u 0.006c ca a0 0E 0.004 E 0.004::J ::J'c 'ca aE 0.002

E 0.002E E« «

0.000 0.000 L-

High Mid Low High Mid Low

Tide Height Tide Height

_ Exclusion

c:==J Control AreaControl Cage

Ammonium concentrations at Fillongley (A) and Single Spit (8) in each treatment at eachtide height (Medians, error bars represent interquartile range).

0.18 018A B

0.16 016OJ OJ

0> 014 -- 0.14OJ

-S E-c 0.12 c 0.12a a~

.~_ Exclusion

..... 0.10 ..... 0.10 c:==J Control AreaC C<IJ <IJ Control Cageu 008 u 0.08c ca a0 0.06 0 0.06c ca a.D 0.04

.D 004..... .....ro ro0 0

002 0.02

0.00 0.00High Mid Low High Mid Low

Tide Height Tide Height

Carbon concentrations at Fillongley (A) and Shingle Spit (8) in each treatment at each tideheight (Medians, error bars represent interquartile range).

89

016 0.16

A B~

0.14~

0.14OJ OJOJ OJE

0.12E

012- -c c0 0

'iU 0.10 ~ 0.10L.. L.. _ ExclusionC CQ)

0.08Q)

0.08 c=:J Control Areau uc c Control Cage0 00 0.06

0 0.06Q) Q)

ro roJ:: 0.04

J::0.040- 0-

(/J (/J

0 0J::

0.02J::

0... 0... 0.02

0.00 0.00

High Mid Low High Mid Low

Tide Height Tide Height

Phosphorous concentrations at Fillongley (A) and Shingle Spit (8) in each treatment ateach tide height (Medians, error bars represent interquartile range).

90

Summary of the non-parametric Kruskal-Wallis analyses on the sediment nutrientcharacteristics between treatments at each site and at each tide height. *indicates a significant result and ** indicates a marginally significant result.

Study Site Nutrient Tide Chi- p- Significant?Height squared value

Value

High 7.49 0.0236 **

Ammonium Mid 3.45 0.1778

Low 0.26 0.8768

High 6.58 0.0371

Fillongley Carbon Mid 2.26 0.3223

Low 0.73 0.6932

High 6.73 0.0346

Phosphorous Mid 3.97 0.1369

Low 0.71 0.702

High 6.39 0.0409

Ammonium Mid 4.44 0.1084

Low 1.36 0.5056

High 2.2 0.3321

Shingle Spit Carbon Mid 0.64 0.724

Low 3.05 0.2176

High 7.18 0.0275 **

Phosphorous Mid 2.63 0.2683

Low 1.98 0.3705

91

0.0

0.2

+oJCQ) 0.4·u

li=Q)

8.z-·eco·E 0.6U5

0.8

1.0

I

t- 1 1~~

SLC SLE SME SLA SMA SMC SHC SHA FHA FHC SHE FHE FME FLE FLC FLA FMA FMC

Treatment

Tree diagram illustrating the Bray-Curtis similarities for the communities under alltreatment at all tide heights at both sites. F =Fillongley, S =Shingle Spit. H =high, M =mid, L =low. E =Exclusion, A =Control area, C =Control cage.

92

Appendix B: Exclusion Experiment Supplementary Data

Total invertebrate abundance means/m2±95% confidence interval for each treatment overthe entire study area and each tide height at both sites.

Study Site

Tide Heights Treatment FillongleyShingleSpit

Exclusion 756±354 185±116

Overall Control Area 342±110 172±57

Control Cage 478±302 99±47

Exclusion 651±518 372±358

High Control Area 281±128 259±84

Control Cage 368±1340 114±616

Exclusion 692±755 103±54

Mid Control Area 450±136 175±117

Control Cage 414±2255 106±540

Exclusion 924±1378 81±33

Low Control Area 296±429 82±25

Control Cage 823±O 77±25

93

Bivalve abundance means/m2±95% confidence interval for each treatment over the entirestudy area and each tide height at both sites.

Study Site

Tide Heights Treatment Fillongley ShingleSpit

Exclusion 453±260 180±117

Overall Control Area 153±114 169±57

Control Cage 203±218 95±49

Exclusion 610±519 370±358

High Control Area 278±126 258±84

Control Cage 354±1455 112±642

Exclusion 664±770 94±44

Mid Control Area 153±421 171±118

Control Cage 140±1010 104±546

Exclusion 85±79 76±35

Low Control Area 28±17 80±25

Control Cage 27±O 70±6

94

Non-prey abundance means/m2±95% confidence interval for each treatment over the entirestudy area and each tide height at both sites.

Study Site

Tide Heights Treatment Fillongley ShingleSpit

Exclusion 302±376 5±3

Overall Control Area 190±140 3±1

Control Cage 275±456 4±4

Exclusion 40±56 2±1

High Control Area 3±4 2±2

Control Cage 14±114 2±25

Exclusion 28±32 9±12

Mid Control Area 298±300 4±4

Control Cage 275±3265 2±6

Exclusion 838±1341 6±4

Low Control Area 268±426 3±2

Control Cage 796±O 8±19

95

Total invertebrate species richness means/m2±95% confidence interval for each treatmentover the entire study area and each tide height at both sites.

Study Site

Tide Heights Treatment FillongleyShingleSpit

Exclusion 8.3±1.8 6.1±1.3

Overall Control Area 7.0±1.4 5.8±1.2

Control Cage 7.6±3.0 5.5±1.4

Exclusion 5.8±2.0 4.8±2.0

High Control Area 5.0±1.8 5.0±2.2

Control Cage 7.0±25.4 4.5±6.4

Exclusion 8.2±4.6 7.2±3.5

Mid Control Area 7.0±1.3 7.0±4.1

Control Cage 7.5±31.8 5.0±O.O

Exclusion 11.0±1.8 6.2±3.3

Low Control Area 9.0±3.4 5.2±2.0

Control Cage 9.0±O.O 7.0±12.7

96

Bivalve species richness means/m2±95% confidence interval for each treatment over theentire study area and each tide height at both sites.

Study Site

Tide Heights Treatment FillongleyShingleSpit

Exclusion 4.7±1.1 3.4±O.7

Overall Control Area 3.9±O.9 4.1±O.8

Control Cage 3.6±1.4 3.5±O.9

Exclusion 3.0±1.3 3.5±1.6

High Control Area 3.5±1.6 4.0±1.3

Control Cage 3.5±6.4 3.0±12.7

Exclusion 4.8±2.7 3.8±1.5

Mid Control Area 3.5±1.6 5.0±2.2

Control Cage 3.5±19.0 3.5±6.4

Exclusion 6.2±O.8 3.0±2.2

Low Control Area 4.8±3.0 3.2±2.0

Control Cage 4.0±O.O 4.0±O.O

97

Non-prey species richness means/m2±95% confidence interval for each treatment over theentire study area and each tide height at both sites.

Study Site

Tide Heights Treatment FillongleyShingleSpit

Exclusion 3.7±O.8 2.7±1.2

Overall Control Area 3.1±O.9 1.7±O.6

Control Cage 4.0±1.8 2.0±1.5

Exclusion 2.8±O.8 1.2±O.8

High Control Area 1.5±1.6 1.0±1.3

Control Cage 3.5±19.0 1.5±19.0

Exclusion 3.5±2.0 3.5±4.6

Mid Control Area 3.5±O.9 2.0±2.2

Control Cage 4.0±12.7 1.5±6.4

Exclusion 4.8±1.5 3.2±2.0

Low Control Area 4.2±O.8 2.0±O.O

Control Cage 5.0±O.O 3.0±12.7

98

Total invertebrate species evenness means/m2±95% confidence interval for each treatmentover the entire study area and each tide height at both sites.

Study Site

Tide Heights Treatment Fillongley ShingleSpit

Exclusion OA5±O.13 O.39±O.10

Overall Control Area O.34±O.10 OA8±O.13

Control Cage O.33±O.22 O.58±O.16

Exclusion O.58±O.25 O.25±O.11

High Control Area OA4±O.19 O.51±O.31

Control Cage OA8±1A5 O.62±O.O4

Exclusion OA3±O.25 O.51±O.23

Mid Control Area O.24±O.23 O.57±O.26

Control Cage O.28±O.17 O.71±O.O4

Exclusion O.33±OAO OA2±O.26

Low Control Area O.35±O.28 O.34±O.22

Control Cage O.12±O.OO OAO±O.64

99

Bivalve species evenness means/m2±95% confidence interval for each treatment over theentire study area and each tide height at both sites.

Study SiteI

Tide Heights Treatment FillongleyShingleSpit

Exclusion 0.47±0.15 0.43±0.10

Overall Control Area 0.36±0.13 0.52±0.23

Control Cage 0.38±0.28 0.64±0.27

Exclusion 0.69±0.17 0.28±0.14

High Control Area 0.53±0.24 0.57±0.32

Control Cage 0.60±0.96 0.74±1.29

Exclusion 0.45±0.22 0.54±0.28

Mid Control Area 0.26±0.002 0.62±0.11

Control Cage 0.28±0.003 0.85±0.44

Exclusion 0.26±0.32 0.46±0.22

Low Control Area 0.28±0.00 0.37±0.07

Control Cage 0.11±0.00 0.32±0.28

100

Non-prey species evenness means/m2±95% confidence interval for each treatment overthe entire study area and each tide height at both sites.

Study Site

Tide Heights Treatment FillongleyShingleSpit

Exclusion O.20±O.O9 O.19±O.O7

Overall Control Area O.15±O.O6 O.12±O.18

Control Cage O.13±O.11 O.26±O.22

Exclusion O.24±O.26 O.12±O.10

High Control Area O.10±O.O3 O.OO±O.91

Control Cage O.14±1.29 O.29±3.65

Exclusion O.16±O.18 O.23±O.17

Mid Control Area O.11±O.O6 O.16±O.13

Control Cage O.16±O.24 O.20±O.52

Exclusion O.21±O.26 O.22±O.25

Low Control Area O.23±O.OO O.19±O.O1

Control Cage O.O3±O.OO O.30±O.O5

101

Total invertebrate Shannon-Wiener index means/m2±95% confidence interval for eachtreatment over the entire study area and each tide height at both sites.

Study Site

Tide Heights Treatment FillongleyS~lingle

Spit

Exclusion O.90±O.25 O.72±O.22

Overall Control Area O.64±O.19 O.84±O.22

Control Cage O.65±O.40 O.95±O.19

Exclusion 1.01±O.43 O.38±O.17

High Control Area O.71±O.30 O.83±O.50

Control Cage O.93±2.82 O.93±O.O6

Exclusion O.91±O.52 1.00±O.45

Mid Control Area O.46±O.45 1.11±O.50

Control Cage O.57±O.35 1.14±O.O7

Exclusion O.79±O.95 O.76±O.48

Low Control Area O.76±O.63 O.57±O.37

Control Cage O.26±O.OO O.77±1.25

102

Bivalve Shannon-Wiener index means/m2±95% confidence interval for each treatment overthe entire study area and each tide height at both sites.

Study Site

Tide Heights Treatment FillongleyShingleSpit

Exclusion O.65±O.17 O.52±O.14

Overall Control Area OA8±O.16 O.74±O.22

Control Cage OA7±O.34 O.78±O.30

Exclusion O.76±O.19 O.36±O.17

High Control Area O.67±O.30 O.8O±OA9

Control Cage O.75±1.21 O.82±1A2

Exclusion O.71±O.34 O.71±O.36

Mid Control Area O.33±OA4 1.00±OAO

Control Cage O.36±O.O1 1.06±O.55

Exclusion OA7±O.59 O.50±O.24

Low Control Area OA3±O.36 OA3±O.34

Control Cage O.15±O.OO OA5±O.39

103

Non-prey Shannon-Wiener index means/m2±95% confidence interval for each treatmentover the entire study area and each tide height at both sites.

Study Site

Tide Heights Treatment FillongleyShingleSpit

Exclusion O.26±O.12 O.19±O.11

Overall Control Area O.17±O.10 O.O9±O.O4

Control Cage O.18±O.13 O.18±O.16

Exclusion O.25±O.26 O.O3±O.O2

High Control Area O.O4±O.O1 O.O3±O.O4

Control Cage O.18±1.62 O.12±1A8

Exclusion O.20±O.22 O.29±O.22

Mid Control Area O.13±O.O6 O.11±O.11

Control Cage O.22±O.34 O.O8±O.62

Exclusion O.32±OAO O.26±O.27

Low Control Area O.33±O.28 O.13±O.O7

Control Cage O.12±O.OO O.32±O.86

104