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
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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.
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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.
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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