Latitudinal Variation in Naticid Gastropod Predation on Western Atlantic Mollusks: Investigating Evolutionary Patterns in the Fossil Record Through Modern Ecosystems

LATITUDINAL VARIATION IN NATICID GASTROPOD PREDATION ON WESTERN ATLANTIC MOLLUSKS: INVESTIGATING EVOLUTIONARY PATTERNS IN THE FOSSIL RECORD THROUGH MODERN ECOSYSTEMS

Christy C. Visaggi

A Dissertation Submitted to the University of North Carolina Wilmington in Partial Fulfillment of the Requirements for the Degree of Doctor of Philosophy

Department of Biology and Marine Biology

University of North Carolina Wilmington

2012

Approved by

Advisory Committee

Gregory P. Dietl Martin H. Posey .

Richard A. Laws Stuart R. Borrett .

Patricia H. Kelley . Chair

Accepted by

. Dean, Graduate School

TABLE OF CONTENTS

ABSTRACT ...... v

ACKNOWLEDGMENTS ...... vii

DEDICATION ...... viii

LIST OF TABLES ...... ix

LIST OF FIGURES ...... x

CHAPTER ONE: Overview ...... 1 References ...... 5

CHAPTER TWO: Equatorward Increase in Naticid Gastropod Drilling Predation on Infaunal Bivalves from Brazil ...... 7 Abstract ...... 7 Introduction ...... 8 Biogeographic Setting ...... 12 Methods...... 15 Field Collection ...... 15 Laboratory Techniques ...... 19 Data Analysis ...... 20 Results ...... 22 Assemblage Analyses ...... 22 Lower Taxon Analyses ...... 22 Size-Standardized Analyses ...... 27 Incomplete and Multiple Drilling ...... 31 Discussion ...... 34 Overall Patterns in Drilling Predation...... 34 Potential Biases and Limitations of the Data ...... 37 Environmental Variation ...... 37 Sampling Methods ...... 39 Anthropogenic Effects ...... 42 Preservational Factors ...... 45 Western Atlantic: North vs. South ...... 46 Temperature and Seasonality ...... 50 Naticid Diversity ...... 53 Alternate Modes of Predation ...... 57 Predator-Prey Size Distributions...... 58 Prey Diversity ...... 59 Paleontological Implications ...... 61

Future Work ...... 65 Conclusions ...... 66 Acknowledgments...... 67 References ...... 68

CHAPTER THREE: Examining the Influence of Seasonality on Naticid Drilling Predation Using an Experimental Approach in Both a Laboratory and Field Setting ...... 75 Abstract ...... 75 Introduction ...... 76 Setting ...... 78 Methods: Laboratory ...... 81 Data Collection: Predators ...... 84 Data Collection: Prey ...... 84 Natural Mortality and Decay ...... 84 Methods: Field ...... 87 Recovery of Specimens...... 88 Data Analysis ...... 88 Results: Lab ...... 89 Natural Mortality and Decay ...... 94 Results: Field ...... 95 Discussion ...... 100 Potential Biases ...... 105 Laboratory Experiments...... 105 Field Experiments ...... 112 Seasonal Variation ...... 115 Fall vs. Spring ...... 115 Field vs. Lab: Summer ...... 117 Latitudinal Patterns ...... 119 Paleontological Implications ...... 123 Future Work ...... 125 Conclusions ...... 126 Acknowledgments...... 127 References ...... 128

CHAPTER FOUR: Influence of Sediment Depth on Drilling Behavior of Neverita duplicata (Gastropoda: Naticidae) With a Review of Alternate Modes of Predation ...... 133 Abstract ...... 133 Introduction ...... 134 Alternate Modes of Predation ...... 135 What is Smothering? ...... 141 Sediment Depth ...... 146 Materials and Methods ...... 148 Sediment Depth ...... 148 Prey Health...... 150

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Results ...... 151 Sediment Depth ...... 151 Prey Health...... 153 Discussion ...... 153 Possible Suffocation Events ...... 153 Influence of Sediment Depth on Suffocation...... 157 Other Potential Explanations for Laboratory Reports of Suffocation ...... 159 Effects of Prey Health ...... 160 Why Suffocation? ...... 162 Susceptible Prey ...... 166 Latitudinal Predictions ...... 168 Interpretation of Incomplete Drilling ...... 170 Paleontological Implications ...... 171 Conclusions ...... 174 Acknowledgments...... 176 References ...... 176

CHAPTER FIVE: Synthesis ...... 185 References ...... 191

ABSTRACT

Escalation characterizes an arms race of adaptation to enemies in which predation is a significant driver of evolution. The fossil record of shell-drilling by predatory naticid gastropods provides substantial evidence for this controversial hypothesis; however, the influence of environmental effects on apparent temporal trends in drilling is poorly understood. Spatial patterns are difficult to assess in the fossil record due to limited outcrops; modern communities offer opportunities to examine latitudinal variation in drilling, with paleontological implications.

Available data on patterns in drilling with latitude are contradictory and mostly limited to the Northern Hemisphere. Furthermore, studies rarely consider processes that may affect spatial patterns in drilling predation. This work examines drilling patterns along an under-sampled coastline in South America and experimentally explores abiotic and biotic factors that may impact latitudinal variation in drilling predation.

Following a brief overview of the dissertation (Chapter One), Chapter Two examines latitudinal variation in naticid drilling on Recent bivalve assemblages from Brazil (6°S–34°S).

Increased drilling equatorward occurred at the assemblage level and for several lower taxa, with no change in results upon size-standardization. Assessment of potential biases such as differences in collection methods or environmental variation corroborated latitudinal interpretations. Chapter Three explores the influence of seasonality on naticid drilling intensity via laboratory and field experiments in North Carolina. Drilling varied seasonally, although not directly with temperature. Fall had more drilling despite lower temperatures compared to spring; drilling was greatest in summer under laboratory conditions but was not documented in field experiments. Drilling and crushing predation were inversely correlated across seasons in the field. Chapter Four investigates whether insufficient sediment in laboratory experiments may

v contribute to literature accounts of suffocation by moon snails; alternate modes of predation are reviewed and their latitudinal context assessed. Shallow sediment did not impact drilling by

Neverita duplicata; poor prey health may have yielded previous reports of suffocation. Thus latitudinal variation in drilling is impacted by seasonal changes including but not limited to temperature, whereas alternate modes of predation are likely unimportant (Chapter Five). These findings demonstrate the utility of an interdisciplinary approach in addressing questions in macroecology and evolutionary paleoecology.

ACKNOWLEDGMENTS

Thanks to my exceptional advisor, P. Kelley, and committee members G. Dietl, R. Laws,

M. Posey, and S. Borrett for their input and efforts in guiding me through the development and completion of this dissertation. I greatly value their insight and enthusiasm regarding my data – yes, even yours Greg! Thank you all for embracing the interdisciplinary nature of my interests.

I am deeply appreciative of research funds granted by many organizations acknowledged in different chapters of my dissertation, including final year support from a Ford Foundation

Fellowship and AWG Chrysalis Scholarship. Thanks to many members of UNCW for their assistance these last six years in the Center for Marine Science, Biology & Marine Biology,

Geography & Geology, Graduate School, Randall Library, and Campus Recreation, especially

T. Chadwick, C. Morris, A. Pabst, S. Kinsey, D. Kubasko, L. Moore, D. Dillaman, B. Roer,

N. Holland, and the ladies of Interlibrary Loan. The Provost’s Office and Evolution Learning

Community supplied financial support early in my PhD; funds obtained through TAs and for conference presentations via BGSA and GSA were instrumental for professional development.

My family fostered my love of science starting with the discovery of my first spiriferid and I am eternally grateful for their support. I love you mom, dad, and Joseph. I am indebted to

S. Kline for his positively British, yet unyielding encouragement during the PhD process and beyond. You are my rock, quite fitting for a geologist. Special hugs to Harriet and mum.

Clam digging, snail hunting, and shell counting abilities of many friends through the years studying paleontology and marine biology are greatly appreciated, but in particular, B. Parnell –

YAMPAJ. Well wishes also to all of the REU students for cheering me on along the way.

Finally, I cherish the steadfast energy offered by M. Smith and the inspiring legacy left behind by S. Kulkofsky. Thank you everyone... I look forward to my next academic journey ahead.

vii

DEDICATION

I would like to dedicate this dissertation to all of the wonderful mentors I’ve had in paleontology over the years, particularly Dr. Patricia Kelley for her endless encouragement, patience, support, and guidance throughout my PhD. She is an inspiration in so many ways, and

I am extremely thankful for the welcoming nature that she and her family extended to me while at UNCW. I am ever grateful to have her as a role model in my life as I continue along my career path devoted to sharing my passion and joy for scientific discovery. P.S. I heart snails.

viii

LIST OF TABLES

CHAPTER TWO: Equatorward Increase in Naticid Gastropod Drilling Predation on Infaunal Bivalves from Brazil ...... 7 Table 1...... 23 Table 2...... 24 Table 3...... 26 Table 4...... 32 Table 5...... 33 Table 6...... 54

CHAPTER THREE: Examining the Influence of Seasonality on Naticid Drilling Predation Using an Experimental Approach in Both a Laboratory and Field Setting ...... 75 Table 1...... 85 Table 2...... 90 Table 3...... 91 Table 4...... 93 Table 5...... 96 Table 6...... 101 Table 7...... 102

CHAPTER FOUR: Influence of Sediment Depth on Drilling Behavior of Neverita duplicata (Gastropoda: Naticidae) With a Review of Alternate Modes of Predation ...... 133 Table 1...... 136 Table 2...... 137 Table 3...... 138 Table 4...... 142

LIST OF FIGURES

CHAPTER TWO: Equatorward Increase in Naticid Gastropod Drilling Predation on Infaunal Bivalves from Brazil ...... 7 Figure 1...... 16 Figure 2...... 18 Figure 3...... 25 Figure 4...... 28 Figure 5...... 30 Figure 6...... 40 Figure 7...... 56

CHAPTER THREE: Examining the Influence of Seasonality on Naticid Drilling Predation Using an Experimental Approach in Both a Laboratory and Field Setting ...... 75 Figure 1...... 79 Figure 2...... 80 Figure 3...... 83 Figure 4...... 92 Figure 5...... 97 Figure 6...... 98 Figure 7...... 99 Figure 8...... 103 Figure 9...... 104 Figure 10...... 106 Figure 11...... 108 Figure 12...... 111

CHAPTER FOUR: Influence of Sediment Depth on Drilling Behavior of Neverita duplicata (Gastropoda: Naticidae) With a Review of Alternate Modes of Predation ...... 133 Figure 1...... 152 Figure 2...... 154 Figure 3...... 155

CHAPTER ONE: OVERVIEW

Understanding patterns of evolution requires an interdisciplinary approach. The fossil record permits detection of patterns and processes operating at longer time scales; modern communities allow for direct observation and experimentation. Nevertheless, utility of neontological research is frequently overlooked in approaching paleontological problems - an unfortunate gap in communication between paleontologists and neontologists (Dietl & Kelley,

2002; Bonuso, 2007). Indeed, such a lack of interdisciplinary research may be impacting our ability to conserve modern fauna and flora effectively (National Research Council, 2005). My dissertation research bridges the gap between evolutionary paleoecology and ecology through use of modern mollusks. Questions are rooted in paleontology; ecological approaches offer insight into an evolutionary pattern observed in the fossil record.

The hypothesis of escalation, originally proposed by Vermeij (1987), characterizes an enemy-driven evolutionary arms race of adaptation as based on paleontological assemblages.

Evidence for this hypothesis includes a rise in the intensity of biological hazards throughout geologic time and a corresponding increase in predatory scars and drillholes preserved in the shells of fossil molluscan faunas. Escalation suggests that ecology drives evolution, particularly as a result of predator-prey interactions. The evolutionary significance of predation is emphasized by the hypothesis of coevolution as well; coevolution is more familiar among biologists as research is based mostly in modern ecosystems, especially in terrestrial environments (Ehrlich & Raven, 1964; Futuyma & Slatkin, 1983). However, coevolution differs from escalation, in that coevolution reflects the adaptation of predator and prey in response to each other; in its most extreme version (Red Queen hypothesis of Van Valen, 1973), such reciprocal adaptation would be continuous. In contrast, in escalation response is to enemies; prey generally do not represent enemies unless they are dangerous to their predators (Vermeij,

1994). Thus, in escalation adaptation need not be reciprocal because of inequalities in selection on predators and prey, with more severe consequences of predator-prey interactions for the prey than for the predator (e.g., life-dinner principle of Dawkins & Krebs, 1979; see also Brodie &

Brodie, 1999; Abrams, 2000; Dietl & Kelley, 2002). The relative importance of coevolution and escalation may depend on scale (Dietl & Kelley, 2002). On an ecological timescale, coevolution may occur, as in Thompson’s (2005) geographic mosaics of selection among populations, but predator-driven escalation may be more important on evolutionary timescales (Vermeij, 1999,

2002; Dietl & Kelley, 2002).

The fossil record of beveled drillholes, attributed mostly to predatory naticid gastropods, provides important evidence for the hypothesis of escalation over the last 100 million years.

Although the fossil record of drilling provides an understanding of the history of predator-prey interactions, recognizing the potential effects of environmental variation is challenging when paleontologists are restricted by the availability of the fossil deposits. Habitat differences such as wave energy, salinity, and depth can be controlled; however, combining samples that derived from different latitudes is typically unavoidable when examining long-term evolutionary trends.

Most studies have focused on characterizing patterns in drilling predation without consideration of potential confounding influences due to geographic variation. Drilling may vary with latitude due to changes in a variety of abiotic and biotic factors such as prey defenses (e.g., ease of

CaCO3 precipitation), predator abundance, diversity, metabolic rate, alternate modes of naticid predation (e.g., suffocation), and the abundance of enemies of drilling predators. Exploring the contributions of processes that may impact drilling intensity spatially is necessary to ensure that

2 fluctuations in drilling documented for different time intervals are not merely due to differences resulting from geographic or climatic variation.

Temporal and spatial patterns of drilling predation are reviewed in the next chapter of this dissertation. Latitudinal patterns in drilling reported in the literature are based on a combination of modern and fossil data at the assemblage and taxon level with mixed results. Trends in drilling are documented poleward, equatorward, and, most recently, with a peak at mid-latitudes along the U.S. East Coast (Kelley & Hansen, 2007). Because latitudinal variation in drilling is not often examined with respect to studies of escalation and no consensus exists in the literature, all research conducted as part of this dissertation focused on improving the understanding of latitudinal patterns in drilling predation, with broader implications for macroecology and evolutionary paleoecology. Spatial patterns and influencing processes are challenging or otherwise not feasible to study in the fossil record and, for that reason, all dissertation research utilized modern faunas for investigating aspects of latitudinal variation in drilling predation with paleontological implications. Study of spatial variation in drilling proceeded by an examination of patterns in drilling along an under-sampled coastline (Chapter Two) and exploration of processes that may have an impact on patterns in drilling with latitude (Chapters Three & Four).

Chapter Two examines frequency of naticid drilling in beach-collected assemblages of

Recent bivalves across 6°S–34°S in Brazil. Temporal and spatial data on drilling in the Southern

Hemisphere are limited and, consequently, latitudinal patterns have been based exclusively on research restricted to North America and/or Europe (Harper, 2006). Knowledge of geographic variation in drilling is vital to interpretations of evolutionary patterns in drilling (Vermeij, 1980;

Vermeij et al., 1989; Harper & Kelley, 2012); enhanced spatial coverage is needed. In particular, an unexpected peak in drilling on modern molluscan faunas along the mid-latitudes of eastern

North America documented by Kelley & Hansen (2007) provided the impetus to investigate variation in drilling predation across eastern South America. Is the mid-latitude peak in drilling noted for Western Atlantic mollusks of the Northern Hemisphere mirrored along the coastline of

Brazil?

Chapter Three explores the influence of seasonality on the intensity of drilling, as the presence, duration, and magnitude of seasons varies with latitude. Temperate ecosystems are subject to increased seasonal variation relative to consistently warm habitats of lower latitudes.

Temperatures fluctuate greatly by season, as do a variety of other abiotic and biotic variables

(e.g., salinity, physical disturbances, density of predators and prey). The Q10 effect states that the rate of metabolism is proportional to temperature and approximately doubles for every rise in

10°C (van’t Hoff, 1884). Temperature is known to affect the feeding behavior of naticids, but how seasonality impacts drilling apart from temperature is unresolved. Using live naticids in a combined laboratory and field experimental approach, I investigated the impact of seasonality on drilling. Temperature and seasonality vary with latitude and, consequently, may influence spatial patterns in the intensity of drilling (e.g., greater drilling documented at lower latitudes may reflect increased metabolic rates due to higher temperatures and/or a lack of seasonality in the tropics).

Chapter Four investigates the prevalence of alternate modes of predation by moon snails via review of the literature, and experimentally assesses whether laboratory effects such as insufficient sediment may be responsible for previous claims of naticid suffocation of prey.

Most naticids prey on other infaunal mollusks while buried in the sediment. Drilling predation is achieved through an alternating sequence of chemical secretions from the accessory boring organ and physical rasping by the radula. Yet, alternate modes of predation such as suffocation

(sometimes referred to as “smothering”) are reported primarily in laboratory settings; further investigation is needed to examine naticid feeding in the absence of completed drillholes.

Because much of the evidence for escalation relies on drillholes attributed to naticids, it is important to understand how pervasive alternate behaviors may be among moon snails for estimates of successful predation. Furthermore, if naticids utilizing alternate modes of predation are concentrated geographically, perhaps behaving uniquely due to environmental factors, recognition of such behaviors is critical for analyzing spatial patterns in naticid predation based on drillholes.

Chapter Five synthesizes and compares the results of the preceding chapters with respect to several hypotheses regarding latitudinal variation in drilling predation, with consideration also of latitudinal gradients in species interactions overall. In addition, areas of future research are suggested based on the findings in this dissertation. Finally, the combined results from the different components of my dissertation have implications for macroecology and evolutionary paleoecology.

REFERENCES

Abrams, P.A., 2000. The evolution of predator-prey interactions: Theory and evidence. Annu. Rev. Ecol. Syst. 31, 79–105.

Bonuso, N., 2007. Shortening the gap between modern community ecology and evolutionary paleoecology. Palaios. 22, 455–456.

Brodie, E.D., III, Brodie, E.D., Jr., 1999. Predator-prey arms races: asymmetrical selection on predators and prey may be reduced when prey are dangerous. Bioscience. 49, 557–568.

Dawkins, R., Krebs, J.R., 1979. Arms races between and within species. Proc. R. Soc. Lon. B. 205, 489–511.

Dietl, G.P., Kelley, P.H., 2002. The fossil record of predator-prey arms races: coevolution and escalation hypotheses, in: Kowalewski, M., Kelley, P.H. (Eds.), The Fossil Record of Predation. Paleontological Society Papers 8, pp. 353–374.

Ehrlich, P.R., Raven, P.H., 1964. Butterflies and plants: a study in coevolution. Evolution. 18, 586–608.

Futuyma, D.J., Slatkin, M., (Eds.), 1983. Coevolution. Sinauer Associates, Inc., Massachusetts.

Harper, E.M., 2006. Dissecting post-Paleozoic arms races. Palaeogeogr. Palaeocl. 232, 322–343.

Harper, E.M., Kelley, P.H., 2012. Predation of bivalves. Treatise on Invertebrate Paleontology, Part N, Revised, Volume 1. Treatise Online 44, 1–21.

Kelley, P.H., Hansen, T.A., 2007. Latitudinal patterns in naticid gastropod predation along the east coast of the United States: a modern baseline for interpreting temporal patterns in the fossil record, in: Bromley, R.G., Buatois, L.A., Mángano, M.G., Genise, J.F., Melchor, R.N. (Eds.), Sediment-Organism Interactions: A Multifaceted Ichnology. SEPM. Spec. P. 88, Tulsa, pp. 287– 299.

National Research Council Committee on the Geologic Record of Biosphere Dynamics. 2005. The Geological Record of Ecological Dynamics: Understanding the Biotic Effects of Future Environmental Change. National Academies Press, Washington, D.C.

Thompson, J.N., 2005. The Geographic Mosaic of Coevolution. University of Chicago Press, Chicago. van’t Hoff, J.H., 1884. Etudes de Dynamique Chimique. Frederik Muller & Co., Amsterdam.

Van Valen, L.M., 1973. A new evolutionary law. Evol. Theor. 1, 1–30.

Vermeij, G.J., 1980. Drilling predation of bivalves in Guam: some paleoecological implications. Malacologia. 19, 329–334.

Vermeij, G.J., 1987. Evolution and Escalation: An ecological history of life. Princeton University Press, New Jersey.

Vermeij, G.J., 1994. The evolutionary interaction among species: selection, escalation, and coevolution. Annu. Rev. Ecol. Syst. 25, 219–236.

Vermeij, G.J., 1999. Inequality and the directionality of history. Amer. Nat. 153, 243–253.

Vermeij, G.J., 2002. Evolution in the consumer age: predators and the history of life, in Kowalewski, M., Kelley, P.H. (Eds.), The Fossil Record of Predation. Paleontological Society Papers 8, pp. 375–393.

Vermeij, G.J., Dudley, E.C., Zipser, E., 1989. Successful and unsuccessful drilling predation in Recent pelecypods. Veliger. 32, 266–273.

CHAPTER TWO: EQUATORWARD INCREASE IN NATICID GASTROPOD DRILLING PREDATION

ON INFAUNAL BIVALVES FROM BRAZIL

ABSTRACT

Understanding the influence of spatial variation on temporal trends is important for interpreting evolutionary patterns of predation in the fossil record. Geographic data on naticid gastropod drilling predation are contradictory and mostly limited to the Northern Hemisphere.

This study examines latitudinal variation in drilling on ~24,000 beach-collected Recent bivalves from 6°S–34°S in Brazil. Twenty-eight localities representing 16 latitudes were sampled in the

Brazilian and Argentinean provinces, further subdivided into four smaller ecoregions

(Northeastern Brazil, Eastern Brazil, Southeastern Brazil, Rio Grande). Analyses were limited to fauna exhibiting infaunal life habits with a few exceptions. Increased drilling equatorward was observed at the assemblage-level across numerous spatial scales (localities, latitudes, ecoregions, provinces). Taxon-level analyses for eight genera drilled across multiple ecoregions indicated greater drilling among lower latitudes in many cases; size-standardization did not affect patterns at the genus level. An equatorward increase in drilling was documented also upon restricting the data to localities characterized primarily by softer substrates and in limiting data to samples obtained by a single collecting strategy, eliminating concerns regarding the influence of local environmental variation and different methodologies on latitudinal patterns in drilling.

Latitudinal patterns in drilling may be related to temperature and seasonality in influencing metabolic rates, as well as diversity and predator-prey size distributions. The results of this study do not correspond to existing patterns previously described for Western Atlantic molluscan

7 assemblages of the Northern Hemisphere. However, they may help explain temporal patterns in the fossil record of naticid predation.

INTRODUCTION

The escalation hypothesis represents an enemy-driven evolutionary arms race as based on the fossil record (Vermeij, 1987). Escalation claims that the intensity of, and adaptations to, biological hazards such as predation and competition have increased throughout geologic time

(Vermeij, 2002). The importance of predator-prey interactions is stressed by this controversial hypothesis as it suggests that predation is a significant force in driving evolution. Much of the history of life can be interpreted as the result of arms races in which prey evolve in response to their predators, but then predators evolve in response to their enemies (Dietl & Kelley, 2002), in contrast to the reciprocal adaptation that typifies coevolution (Ehrlich & Raven, 1964).

Substantial evidence for escalation consists of scars and drillholes preserved in fossil mollusk shells, providing a record of ancient predator-prey interactions. Most of these drillholes are uniquely beveled (representing the trace fossil Oichnus paraboloides Bromley, 1981) and can be attributed to predatory naticid gastropods (moon snails). Because naticids most often prey upon shallow-burrowing marine bivalves and gastropods, evidence of drilling predation is readily preserved in both modern shells and paleontological assemblages.

Based on a limited literature survey, Vermeij (1987) stated that drilling frequencies were low in the Cretaceous and had reached modern levels by the Eocene. Kelley & Hansen (1993,

1996, 2003, 2006) reported instead that escalation appeared to be episodic in nature over the last

~80 million years, using their database on naticid drilling from collections of >150,000 fossil specimens from the U.S. Coastal Plain. Following Vermeij (1987), they originally credited this

8 more complex pattern to mass extinctions that preferentially eliminated highly armored species, leaving a more vulnerable fauna susceptible to drilling predation (Kelley & Hansen, 1996).

However, additional research failed to support that hypothesis (Hansen et al., 1999; Kelley et al.,

2001; Reinhold & Kelley, 2005). More recently, Kelley & Hansen (2007) suggested that the fluctuations in drilling frequency may be linked to variations in climate, in part because samples from different time intervals derived from different latitudes as controlled by the availability of fossil deposits. Temporal patterns are likely influenced by environmental variation in drilling, but no consensus yet exists as to what extent drilling varies at different geographic scales.

Various workers have demonstrated spatial variation in drilling predation, from local

(e.g., Vermeij, 1980) to regional scales. Some fossil studies have found differences in drilling among facies (e.g., Hoffmeister & Kowalewski, 2001, and Sawyer & Zuschin, 2011, for the

Miocene of Central Europe). Hansen & Kelley (1995) documented greater drilling in the Yazoo

Formation, deposited on the outer shelf, compared to the shallower-water Moodys Branch

Formation (both Eocene of the Gulf Coastal Plain). However, within the Moodys Branch, no trend with bathymetry or grain size occurred. Sawyer & Zuschin (2010) found differences in drilling between intertidal and sublittoral habitats of Recent mollusks of the Northern Adriatic, although Sander and Lalli (1982) found no consistent trend in drilling of Recent mollusks along a depth transect off Barbados. Vermeij et al. (1989) commented that geographical patterns in drilling must be “very strong if they are to be detected above the “noise” of local and short-term temporal variation” (p. 268).

Although the history of naticid drilling predation can be explored using the fossil record, evaluating the effect of spatial variation on apparent evolutionary patterns poses a greater challenge due to limited fossil exposures. Trends in predation across latitude are rarely

9 examined in the fossil record, despite the necessity of recognizing environmental effects on evolution. Available data are contradictory (Schemske et al., 2009) and geographically restricted. A poleward increase in drilling is suggested by Allmon et al. (1990) for Paleocene

Turritellidae of the U.S. Coastal Plain, Hansen & Kelley (1995) for Eocene molluscan assemblages and common species therein for the U.S. Coastal Plain, and Hoffmeister &

Kowalewski (2001) for Miocene molluscan faunas from Europe. In contrast, Harries & Schopf

(2007) reported lower drilling frequencies in the Cretaceous of the Western Interior Seaway compared to those found by Kelley & Hansen for coeval lower-latitude assemblages of the Gulf

Coastal Plain.

Modern marine communities provide an excellent platform in which to examine latitudinal variation in drilling. Contemporary spatial patterns have implications for patterns of evolution in the fossil record, and modern habitats are more generally available for testing hypotheses about broad-scale geographic patterns. In addition, modern beach assemblages represent a mixed accumulation of shells from multiple generations similar to the time-averaged deposits utilized for paleoecological studies in the fossil record (Powell & Davies, 1990; Flessa,

1993; Flessa & Kowalewski, 1994). Nevertheless, results based on Recent faunas are also contradictory. Vermeij et al. (1989) reported a poleward increase in drilling for Recent bivalves from tropical America, New England, and several western Pacific localities. Greater drilling equatorward is supported instead based on modern habitats as per Dudley & Vermeij (1978) for

Turritella from various localities distributed globally, as well as Alexander & Dietl (2001) for

Anadara and Divalinga of the U.S. East Coast (but see Kelley & Hansen, 2007, for a reinterpretation of their results).

Because drilling is a slow and risky process for the predator, Vermeij (1993) hypothesized that successful drilling should increase toward the poles, where enemies of drilling gastropods are less abundant. By the same reasoning, the frequency of unsuccessful drilling attempts, indicated by incomplete drillholes (those that do not completely penetrate the prey shell), should increase toward the tropics, where enemies of drilling predators are more abundant. To test this hypothesis, bulk samples of modern mollusk shells were collected by

Kelley & Hansen (2007) from beaches along the U.S. East Coast from Maine (43°N) to the

Florida Keys (25°N). Because their previous work (Kelley & Hansen 1993, 1996, 2003, 2006) used the fossil record of naticid predation to test the hypothesis of escalation, Kelley & Hansen

(2007) focused on naticid-like drillholes in infaunal taxa. Frequency of naticid drilling varied across four major faunal provinces (Nova Scotian, Virginia, Carolinian, Gulf), but not as predicted. The peak in successful drilling occurred along the mid-latitudes and declined both north and south, a pattern characteristic of the assemblage overall and for select lower taxa.

Incomplete drillholes, representing failed attacks, increased toward both the poles and tropics from a low along the Carolinas. Results were consistent between assemblage and lower taxon levels.

This unusual pattern provided the impetus for this investigation of geographic patterns in naticid drilling for the Western Atlantic of the Southern Hemisphere. Too often latitudinal patterns in predation are based on research confined to North America and/or Europe (Harper,

2006), yet understanding geographic variation in drilling is essential for evolutionary interpretations (Vermeij, 1980; Vermeij et al., 1989; Harper & Kelley, 2012). In general, studies of naticid predation in modern and fossil assemblages are limited in eastern South America.

Works include Couto (1996), Pastorino & Ivanov (1996), Lorenzo & Verde (2004), Farinati et al.

(2006), Signorelli et al. (2006), and Simões et al. (2007). Temporal and spatial patterns in predatory drilling are largely unknown (but see Martinelli et al., 2011). This study examines latitudinal variation in naticid drilling at multiple spatial scales along eastern South America both at the assemblage and lower taxon level as advocated by Kowalewski (2002). Tropical through polar environments were sampled in Brazil and Argentina, covering a broader range of latitudes than examined for the Western Atlantic of the Northern Hemisphere. Results are being analyzed in separate phases; only research based on the assemblages collected in Brazil is presented here.

The primary goal of the current investigation is to test the robustness of the pattern reported by Kelley & Hansen (2007) for the east coast of the United States. In particular, the study considers whether Southern Hemisphere patterns also support a peak in drilling frequency at mid-latitudes, or if drilling displays a different pattern of increase towards the poles or equator

(or no significant latitudinal pattern). This work will help disentangle environmental effects from evolutionary patterns seen in the fossil record.

Biogeographic Setting

The oceanographic conditions and Western Atlantic molluscan faunas of eastern South

America offer a context similar to that of the work by Kelley & Hansen (2007) in the Northern

Hemisphere, representing a normal marine shelf along a passive margin. Biogeographic boundaries have been described by several authors for Brazil in regional or global classifications

(e.g., Ekman, 1953; Balech, 1954; Valentine, 1973; Briggs, 1974; Palacio, 1982; Hayden et al.,

1984), but disagreements remain among workers as to the names and latitudinal markers used to delineate marine shelf faunas. Taxonomic richness, faunal similarity, endemism, water masses, productivity, seasonality, coastline features, and more have been considered in characterizing

12 provinces. The most controversial region is the South Brazil Bight (23°S–28°40ʹS) due to the confluence of multiple currents, which bring a combination of warmer and cooler water masses onto the shelf (Castro & de Miranda, 1998; Kowalewski et al., 2002). Transitional faunas occupy this region in Brazil and southward nearing or extending beyond the border with

Uruguay and into Argentina (Floeter & Soares-Gomes, 1999; Schiariti et al., 2004; Benkendorfer

& Soares-Gomes, 2009). Tropical and polar-influenced species are documented in this portion of Brazil, contributing to the uncertainty regarding the appropriate boundary marking the southernmost extent of warmer water assemblages. Demarcations of province limits have varied along this stretch of coastline ranging from 21°S (e.g., Floeter & Soares-Gomes, 1999) to 29°S

(e.g., Aguirre, 1993). However, many recent publications focused on marine benthos (including mollusks) often utilize a break nearer to 23°S (Briggs, 1995; Boschi, 2000; Crame, 2000;

Martínez & del Río, 2002; Schiariti et al., 2004; Harnik et al., 2010).

Large Marine Ecosystems (LMEs) characterize a set of boundaries designed mostly for assessment and management purposes (Sherman, 1991). Trophic relationships, productivity, bathymetry, and hydrography are the criteria utilized for defining boundaries. LME #16 (East

Brazil Shelf: Heileman, 2009) and LME #15 (South Brazil Shelf: Heileman & Gasalla, 2009) are representative of the area sampled during my fieldwork in Brazil. However, this classification is not commonly used by malacologists.

Palacio (1982) outlined provinces based on endemism that are used in several malacological studies (e.g., Floeter & Soares-Gomes, 1999; Benkendorfer & Soares-Gomes,

2009; Souza et al., 2010). In the classification scheme by Palacio (1982), all latitudes between

35°15ʹN in North Carolina and southern Espirito Santo around 22°15ʹS are lumped as the single

Tropical Province (Souza et al., 2010). Other provinces delineated by Palacio for Brazil

13 extending southward are the Paulista and the start of the Patagonic, with the Malvina Province confined to southern Argentina. Harnik et al. (2010) employed a similar system in which all latitudes from Florida to the beginning of the South Brazil Bight are combined into the

Caribbean Province (followed by the Patagonian and Magellanic provinces), after Valentine

(1973). The provinces described in Palacio (1982) and Harnik et al. (2010) were considered unsuitable for the present investigation due to their broad coverage crossing into much of the

Northern Hemisphere and the need for finer spatial resolution.

Examining patterns in drilling across different spatial scales is ideal for facilitating multiple comparisons. Therefore, I followed the boundaries set forth in the nested system of provinces and ecoregions by Spalding et al. (2007), which are structured similarly to the hierarchical approach of Sullivan Sealey & Bustamante (1999). Larger provinces sampled include both the Tropical Southwestern Atlantic and Warm Temperate Southwestern Atlantic, with the latter mostly coinciding with the Eastern South America Province of Hayden et al.

(1984). However, retention of the province names Brazilian and Argentinean (or Argentine) is preferred in this study to maintain consistency with other works on the biogeography of modern and fossil molluscan assemblages of the Western Atlantic in South America (e.g., Scarabino,

1977; Gordillo, 1998a; Aguirre & Farinati, 1999; Martínez & del Río, 2002; Aguirre et al.,

2011). The vicinity of Cabo Frio (~22°50ʹS), a center of upwelling (Franchito et al., 2008), marks the boundary between these provinces (Spalding et al., 2007). This upwelling is unique as it occurs on the western side of an ocean; most upwelling zones in the world are found along eastern edges instead (Franchito et al., 2008). Because of variations in the placement of a provincial boundary in this area (e.g., Benkendorfer & Soares-Gomes, 2009; Harnik et al., 2010),

14 heavy recreational use along the cape, and faunal transitions due to the unique oceanographic conditions surrounding Cabo Frio (Absalão, 1989), I avoided sampling in this region.

The Brazilian Province in my study area is represented by the smaller ecoregions of

Northeastern Brazil and Eastern Brazil. The Argentinean Province consists of the Southeastern

Brazil and Rio Grande ecoregions in Brazil. These ecoregions, based largely on faunal similarities as noted in Spalding et al. (2007), were assessed for specific applicability to molluscan faunas using a database approach, and deemed appropriate by Fortes & Absalão

(2011). The provinces utilized by Kelley & Hansen, 2007 (Nova Scotian, Virginian, Carolinian, and Gulf) are similar in spatial extent to the level of ecoregions outlined for eastern North

America by Spalding et al. (2007).

METHODS

Field Collection

Bulk samples of modern shells were collected along 4000 km of coastline from 6°S–34°S in April 2009 (Figure 1). Shells were recovered from 28 sandy beaches (in proximity to the usual habitat of infaunal naticids) for every 1°–3° latitude. Time, access, and availability of beaches containing a representative sandy fauna limited sampling at every degree change in latitude, as did the need to target localities in less populated areas of coastline to minimize anthropogenic influences. At least 16 additional beaches were investigated during the course of fieldwork; however, sparse shells prohibited adequate sample collection. The 28 localities sampled included eight in the Northeastern Brazil ecoregion (6°S to 12°S) and seven in the

Eastern Brazil ecoregion (15°S to 21°S), combined representing the Brazilian Province. The

Figure 1. Map of localities across Brazil from 6°S–34°S as plotted in Google Earth. The colors correspond to the four different ecoregions sampled, with the Brazilian Province categorized by Northeastern Brazil (red) and Eastern Brazil (orange) and the Argentinean Province represented by Southeastern Brazil (yellow) and Rio Grande (green).

Argentinean Province included eight localities from the Southeastern Brazil ecoregion (23°S to

28°S) and five localities from the Rio Grande ecoregion (30°S to 34°S).

Work by Kelley & Hansen (2007) demonstrated that specimens collected from sections of beach <1 sq. meter provided sufficient material for statistical analyses of predation but, depending on available concentrations of shells (Figure 2), sampling strategies in the present study varied in order to obtain similar volumes of material at different localities. Lower densities required sampling by the sweep method; specimens were collected as encountered by walking on the beach parallel to shore (or less commonly along rocky outcrops where shells accumulated).

Moderate to high concentrations of shells allowed for sampling by quadrats; all specimens on the surface were collected within a defined area, usually several square meters. Extremely high densities in which the substrate consisted almost entirely of shells led to “smash and grab” sampling; handfuls of shells mixed with substrate were collected until a sample bag (~5 liters) was full. For all sampling methods, specimens were mostly obtained on exposed sections of sand, but infrequently were recovered from the surf (by hand collecting and/or use of a sieve) or rock pools where beach concentrations were limited. Shell-rich localities afforded a chance to sample by multiple methods in order to verify that specimens collected using different strategies yielded consistent measures of drilling. Replicate samples were collected either from the same beach or same latitude in all but one case. Samples were sieved as needed on location to remove any accompanying matrix collected upon scooping up shells; processing of samples continued after assemblages were shipped back to the United States.

In consideration of potential environmental controls on patterns in drilling, habitat differences were documented for all localities as based on field observations. Characteristics recorded included beach slope, wave action, rocky outcrop, vegetation cover, human impact,

Figure 2. Typical shell concentrations requiring varied sampling strategies at different beaches: a) sweep (Praia do Mar Grosso, 32°S), b) quadrat (Nova Viçosa, 18°S), and c) “smash and grab” (Praia Calhetas, 8°S).

18 non-marine input, and other relevant features as observed. Sediment samples were additionally collected. Following fieldwork, sea surface temperatures were researched for pertinent latitudes based on Castro & de Miranda (1998).

Laboratory Techniques

Data collection began by picking identifiable shells from the bulk material; only bivalves

>5 mm with visible umbos were processed further. Taxa were sorted and identified at least to genus level using Abbott (1974) and Rios (1994, 2009); abundance data were compiled separately for “whole” (>85% of the valve intact) and “fragmented” remains (<85%). Complete, incomplete, and multiple drillholes (within the same specimen) were documented; stereotypy of the drillhole on the shell was noted as either side or edge. Only beveled drillholes resembling the work of naticids were recorded, in order to maintain consistency with the study by Kelley &

Hansen (2007).

Life modes of all genera were determined based on Abbott (1974) and Rios (1994, 2009) and the Neogene Marine Biota of Tropical America database (Todd, 2001). Evidence of drilling was assessed exclusively for genera exhibiting semi-infaunal and infaunal life habits, as epifaunal bivalves (e.g., oysters, mussels, scallops) are not typically subject to predation by infaunal naticids (Kelley & Hansen, 2007). Rock borers and nestlers were excluded from analyses as well because they typically are not accessible for drilling by naticids. However, arcid bivalves, which may be byssally attached to harder substrates or live semi-infaunally, were included in analyses as most genera exhibited naticid drillholes. The majority of arcid bivalves were represented by species of Anadara, most of which inhabit softer substrates. In many cases, epifaunal organisms constituted only a small proportion of the samples; however, at a few

19 localities, favorable conditions nearby (e.g., hard substrates) led to increased representation of such bivalves.

Analysis of predation at the assemblage level has been criticized because assemblages may differ in their proportion of species with different “adaptive syndromes,” which may influence susceptibility to drilling (Leighton, 2002; Vermeij, 2002). Thus, abundant genera of infaunal bivalves that were commonly drilled in multiple ecoregions were selected for taxon- level analysis. In addition, because drilling frequency may vary significantly among size classes of a single prey species, size-standardized comparison of drilling is desirable (Ottens et al.,

2012). To examine the distribution of size classes, all specimens for select genera were binned in 5 mm intervals based on anterior-posterior lengths. Two consecutive size bins containing the majority of valves were identified for each genus as implemented by Ottens et al. (2012) for size standardized analyses.

Data Analysis

Specimens were analyzed in the laboratory at the level of individual samples, but data on replicates from the same locality were aggregated for evaluation of patterns in drilling.

Calculation of drilling frequency was restricted to the use of “whole” specimens, because it is impossible to determine if a missing piece of a fragmented shell might have borne a drillhole.

Drilling frequencies (=DFs) were calculated as the number of successful attacks divided by the total number of prey individuals, where the number of individuals is equal to half the number of valves. Drilling frequencies were determined at the assemblage level and taxon level for all genera, but only considered valid if based on a minimum of 20 valves (=10 individuals) as advocated by Vermeij (1987).

Assemblage level patterns in DF were analyzed at four different spatial scales: localities

(28 beaches), latitudes (16 sampled), ecoregions (Northeastern Brazil, Eastern Brazil,

Southeastern Brazil, Rio Grande), and provinces (Brazilian, Argentinean). Taxon-level DFs were additionally calculated and evaluated at these same spatial scales for select genera. All taxon-level analyses were repeated using size-standardized data based on the most populated 10 mm size bins for each genus. Finally, to size standardize the assemblage-level data, DFs were calculated for the most common 10 mm size class for the selected genera combined.

I additionally analyzed geographic patterns in failed drilling (Kelley et al., 2001). Prey effectiveness (=PE) was calculated as the number of incomplete drillholes divided by the combined number of complete (successful) and incomplete (failed) drillholes as per Vermeij

(1987). Multiple drillholes (=MULT) in the same specimen represent another measure of failed drilling (Kelley & Hansen, 1993, 1996), where the number of drillholes in multiply bored specimens is divided by the total number of all drilling attempts. Both PE and MULT were considered valid if based on at least 10 drillholes (and not individuals) as they examine how well prey defend themselves if attacked. Multiple complete boreholes in a single valve were not included in calculations of PE, but were restricted to use in MULT.

Differences in frequency of drilled vs. undrilled bivalves between provinces and ecoregions were assessed statistically using a 2x2 chi-square test (or Fisher exact test for cases

<5). These tests were used also to determine the statistical significance of geographic differences in PE and MULT. Relationships between DFs and latitudes as well as localities were examined using Spearman’s rank-order correlation coefficient. Alpha levels for all statistical analyses were set a priori at p<0.05.

RESULTS

Assemblage Analyses

Nearly 24,000 specimens (an average of 852 per locality) were analyzed for naticid drillholes. Data were compiled at the scale of localities, latitudes, ecoregions, and provinces

(Tables 1 & 2). Comparison of assemblage level DFs revealed increased drilling (12%) at the lower latitudes of the tropical Brazilian Province vs. decreased drilling (5%) in the temperate

Argentinean Province (p<0.0001). Greater drilling was further noted equatorward across ecoregions from Rio Grande to Northeastern Brazil (<1%, 10%, 11%, 15%), but differences between Southeastern Brazil and Eastern Brazil were not significant (p=0.420). Spearman rank correlation of DFs for all 16 latitudes (p=0.013) and 28 localities (p=0.002) sampled yielded similar patterns of increased drilling equatorward (Figure 3).

Lower Taxon Analyses

Naticid drillholes were documented in 27 genera (Table 3). Taxa commonly drilled in multiple ecoregions included Anadara, Anomalocardia, Chione, Codakia, Divalinga, Mulinia,

Strigilla, and Tivela. Trends in drilling were assessed among these select eight genera, which made up 62% of all infaunal bivalves and 92% of the drilled specimens.

Comparison of DFs by province (Figure 4a) revealed greater drilling in the Brazilian vs.

Argentinean provinces for Anadara (10% vs. 3%), Anomalocardia (15% vs. 1%), Chione (11% vs. 5%), Codakia (31% vs. 21%), and Tivela (5% vs. 1%); however, differences were not significant for Chione (p=0.194) or Codakia (p=0.064). Slightly less drilling was observed among lower latitudes for Mulinia (9% vs. 11%) and Strigilla (35% vs. 40%), but differences

Table 1. List of localities sampled, corresponding latitudes, number of specimens (near complete infaunal bivalves), and drilling frequency (DF) calculated for each location. Standard abbreviations for states in Brazil are employed.

Locality Latitude # Specimens DF Praia da Pipa, RN -6.2277 209 0.0574 Praia do Amor, RN -6.2336 747 0.1178 Ilha de Itamaracá, PE -7.7781 852 0.2817 Praia Calhetas, PE -8.3439 658 0.0243 Praia do Francês, AL -9.7810 347 0.1960 Barra do São Miguel, AL -9.8270 425 0.2024 Sítio do Conde, BA -11.8449 221 0.3439 Barra do Itarirí, BA -11.9659 1427 0.1163 Praia Cururupe, BA -14.8819 2446 0.1047 Olivença, BA -14.9477 1711 0.0631 Praia Mutari, BA -16.3226 1729 0.3609 Nova Viçosa, BA -17.9160 1542 0.0078 Mucuri, BA -18.0754 1388 0.0101 Penedo, BA -20.9860 1157 0.0847 Marataízes, BA -21.0445 162 0.0494 Laranjeiras, SP -23.3400 378 0.1111 Mongaguá, SP -24.0961 551 0.0000 Praia do Sonho, SP -24.1910 275 0.0145 Praia Grande, SC -26.2782 1507 0.2163 Barra Velha, SC -26.6425 124 0.0161 Sambaqui, SC -27.4900 970 0.0433 Praia Ouvidor, SC -28.1079 37 0.1622 Imbituba, SC -28.2413 219 0.0000 Albatroz, RS -29.9057 1547 0.0013 Praia do Mar Grosso, RS -32.0553 2270 0.0000 Molhes da Barra, RS -32.1611 305 0.0000 Cassino, RS -32.1875 246 0.0081 Hermenegildo, RS -33.6713 403 0.0149

Table 2. Number of specimens collected and drilling frequency (DF) data combined at the scale of latitudes, ecoregions, and provinces.

Brazilian # Specimens DF Argentinean # Specimens DF 6°S 956 0.0523 23°S 378 0.0556 8°S 1510 0.0848 24°S 826 0.0024 10°S 772 0.0997 26°S 1631 0.1006 12°S 1648 0.0734 27°S 970 0.0216 Northeastern Brazil 4886 0.1539 28°S 256 0.0117 15°S 4157 0.0438 Southeastern Brazil 4061 0.1039 16°S 1729 0.1805 30°S 1547 0.0006 18°S 2930 0.0044 32°S 2821 0.0004 21°S 1319 0.0402 34°S 403 0.0074 Eastern Brazil 10135 0.1105 Rio Grande 4771 0.0021 PROVINCE TOTAL 15021 0.1246 PROVINCE TOTAL 8832 0.0489

Figure 3. Drilling frequencies (y-axis) exhibited at the scale of a) provinces, b) ecoregions, c) latitudes, and d) localities. The x-axis for all graphs represents the latitudinal gradient in Brazil starting at the equator for the Southern Hemisphere. Marker colors for assigned ecoregions as in Figure 1. Abbreviations: NE (Northeastern), E (Eastern), SE (Southeastern).

a. 0.3

0.2

0.1

0.0 Brazilian Argentinean b. 0.3

0.2

0.1

0.0 NE Brazil E Brazil SE Brazil Rio Grande c. 0.4

0.3

0.2

0.1

0 00° 1010°S 2020° S 3030° S 4040°S

d. 0.4

0.3

0.2

0.1

0 00° 1010° S 2020° S 3030° S 4040°S

Table 3. Distribution of drilling in four ecoregions across Brazil for 27 genera with documented drillholes. Taxa were either drilled (x), present in samples but undrilled (o), or absent from assemblages in that ecoregion (shaded gray). Ecoregion abbreviations: NE (Northeastern Brazil), E (Eastern Brazil), SE (Southeastern Brazil), RG (Rio Grande).

Drilled Taxa NE E SE RG Abra o o x Amiantis x o Anadara x x x x Anomalocardia x x x o Arca x o x Arcopsis x o o Chione x x x Codakia x x x Corbula x x x o Divalinga x x x o Diplodonta o o x Donax x o x o Glycymeris x x x x Gouldia x x Laevicardium x o o o Lirophora o x Mactra x o x x Mulinia x x x Noetia x x o o Nucula o x Parvilucina x o Semele x x o Strigilla x x x Tellina o x o Tivela x x x o Trachycardium x o o o Transennella x x

26 between provinces were not statistically supported. Equivalent DFs of 54% were determined in the Brazilian and Argentinean provinces for Divalinga.

Drilling was greatest in Northeastern Brazil for Anadara, Chione, Codakia, Mulinia, and

Strigilla vs. Eastern Brazil for Anomalocardia, Divalinga, and Tivela (Figure 5a). Differences between these ecoregions were statistically supported for all genera except Anomalocardia and

Strigilla. Northeastern Brazil and Southeastern Brazil demonstrated significant differences in drilling for most genera, but not Divalinga, Strigilla, and Tivela. Differences between Eastern

Brazil and Southeastern Brazil were significant only for Anadara, Anomalocardia, and Tivela, and marginally lacked support for Mulinia (p=0.056). Small sample sizes or absence from the

Rio Grande prevented comparisons to this ecoregion for all genera except Anadara; differences between the Rio Grande and both Southeastern Brazil and Eastern Brazil were not statistically supported.

All genera showed a negative correlation between latitude and drilling when compared across the 16 latitudes sampled except for Divalinga; however, none were statistically supported.

Comparison of DFs and the 28 localities revealed similar patterns except that correlations were significant for Anadara (p=0.005) and Mulinia (p=0.043). Comparisons of drilling frequency with relative abundances of these eight genera revealed a lack of significant correlations; increased DFs did not correspond to greater relative abundances within prey taxa.

Size-Standardized Analyses

To examine the influence of size on patterns in drilling, all valves for the aforementioned eight genera were binned in 5 mm intervals (~15,000 specimens). Shell size ranged between 5 mm and 70 mm; however, 96% of specimens were <25 mm. No valves larger than 30 mm were

Figure 4. Taxon-level variation in drilling frequency across provinces a) including all data and b) restricted to size-standardized data. a. 0.6 Brazilian

0.5 Argentinean

0.4

0.3

0.2 Drilling Frequency Drilling

0.1

Taxa

b. 0.6 Brazilian

0.5 Argentinean

0.4

0.3

0.2 (Two Size Bins) Size (Two

Drilling Frequency Drilling 0.1

Taxa

28 drilled. Adjacent size classes containing the most specimens for each genus were identified.

The majority of valves ranged 5–15 mm; Mulinia and Tivela were slightly larger at 10–20 mm, with greater representation of Anomalocardia from 15–25 mm. Patterns in drilling at all spatial scales were reanalyzed using only these 10 mm size bins identified for each genus (comprising

44% of all valves and 72% of drilled specimens).

Taxon DFs were similar for all genera at the province level using size-restricted data

(Figure 4b). Greater drilling in the Brazilian Province was reported again for Anadara,

Anomalocardia, Codakia, Chione, and Tivela, but differences between provinces were not significant for Codakia or Chione and were marginally non-significant for Tivela (p=0.059).

Variation in drilling between provinces was not statistically supported for Divalinga, Mulinia, or

Strigilla, similar to the results that incorporated specimens from all size classes.

Comparison of DFs using size-restricted data yielded similar patterns across ecoregions

(Figure 5b). The same genera demonstrated peaks in drilling in Northeastern Brazil (Anadara,

Chione, Codakia, Mulinia, Strigilla) vs. Eastern Brazil (Anomalocardia, Tivela), aside from decreased drilling of Divalinga in the latter ecoregion. Differences between Northeastern Brazil and Eastern Brazil were significant for most genera, excluding Anomalocardia, Strigilla, and

Tivela. Variation in drilling between Northeastern Brazil and Southeastern Brazil was not statistically supported for Chione, Strigilla, or Tivela; differences were only significant in comparisons of Eastern Brazil and Southeastern Brazil for Anadara, Anomalocardia, and Tivela.

Most genera exhibited negative Spearman rank correlations in DF vs. latitude when standardized for size, but not Divalinga or Tivela. Comparison of DFs across localities yielded similar results. None of these correlations was supported statistically, however, apart from

Anadara at both the scale of latitudes (p=0.018) and localities (p=0.015).

Figure 5. Taxon-level variation in drilling frequency across ecoregions a) including all data and b) restricted to size-standardized data. a. 0.7 Northeastern Brazil Eastern Brazil 0.6 Southeastern Brazil

Rio Grande

0.5

0.4

0.3

Drilling Frequency Drilling 0.2

0.1

Taxa

b. 0.7 Northeastern Brazil Eastern Brazil 0.6 Southeastern Brazil

0.5

0.4

0.3

0.2 (Two Size Bins) Bins) Size (Two Drilling Frequency Drilling 0.1

Taxa

Because specimens were most common between 5–15 mm for these genera overall, variation in drilling was additionally assessed based on size-restricted data for these eight taxa combined (38% of all valves, 79% of all drillholes). No difference existed in DFs between provinces using the reduced dataset (20% for the Brazilian vs. 22% in the Argentinean); however, all pairwise comparisons at the ecoregion level were significant. Drilling remained the greatest in Northeastern Brazil (30%), followed by Southeastern Brazil (22%) and Eastern Brazil

(17%). Limited number of specimens prevented comparisons for the Rio Grande. Negative correlations were documented for drilling across latitudes (p=0.285) and localities (p=0.069), but patterns were not statistically supported.

Incomplete and Multiple Drilling

Incomplete drillholes were documented in Northeastern Brazil (PE=2.3%), Eastern Brazil

(PE=0.7%), and Southeastern Brazil (PE=3.7%), but not in the Rio Grande (Table 4).

Significant differences in the number of complete vs. incomplete drillholes were detected in comparisons between Eastern Brazil and other ecoregions, but not for Northeastern Brazil vs.

Southeastern Brazil (p=0.348). The difference in PE between the Brazilian (1.4%) and

Argentinean (3.6%) provinces was statistically supported (p=0.025).

Taxon-level comparisons were conducted for Anadara and Tivela as before, as both contained incomplete drillholes across several ecoregions. For Anadara, PE was greatest in

Southeastern Brazil (10%), followed by Northeastern Brazil (2.6%) and Eastern Brazil (1.9%).

Tivela demonstrated increased PE in Northeastern Brazil (8.3%) relative to Eastern Brazil

(1.8%); limited drilling in Southeastern Brazil prohibited valid comparisons to that ecoregion.

Taxon-level variation in PE for ecoregion comparisons was not statistically supported for either

Table 4. Twenty-one occurrences of incomplete drilling found in 11 genera, listed by locality and latitude. Number of incomplete drillholes (#INC), complete drillholes (#CD), and calculated prey effectiveness (PE) are provided.

Locality Taxa #INC #CD PE 8°S Ilha de Itamaracá, PE Anomalocardia 2 25 0.0741 Chione 1 14 0.0667 Iphigenia 1 0 1.0000 8°S Praia Calhetas, PE Arca 1 1 0.5000 12°S Barra do Itarirí, BA Anadara 1 26 0.0370 Anomalocardia 1 10 0.0909 Tivela 2 12 0.1429 15°S Praia Cururupe, BA Tivela 1 90 0.0110 15°S Olivença, BA Tivela 1 16 0.0588 16°S Praia Mutari, BA Divalinga 1 81 0.0122 21°S Penedo, BA Anadara 1 6 0.1429 24°S Mongaguá, SP Tivela 1 0 1.0000 26°S Praia Grande, SC Anadara 1 9 0.1000 Diplodonta 1 3 0.2500 Mulinia 2 8 0.2000 Tivela 1 1 0.5000 27°S Sambaqui, SC Gouldia 1 4 0.2000 Lirophora 1 1 0.5000

Table 5. Five specimens contained evidence of multiple drilling attempts. One specimen contained both a complete and incomplete drillhole in Eastern Brazil. Abbreviations as in Table 4; number of specimens with multiple drillholes (#MULT); MULT = frequency of drillholes occurring in multiply drilled valves.

Ecoregion #MULT #INC #CD Total Holes MULT Northeastern Brazil 3 9 376 388 0.0155 Eastern Brazil (1) 4 560 564 0.0035 Southeastern Brazil 1 8 211 220 0.0091 Rio Grande 0 0 5 5 0.0000 TOTAL 4 21 1152 1177 NA

33 genus. The difference in PE between provinces was not significant for Anadara (Brazilian,

2.2%; Argentinean, 9.1%); sparse drilling in the Argentinean prevented appropriate comparisons of PE between provinces for Tivela.

Only four specimens contained evidence of multiple complete boreholes, an Anadara,

Chione, and Mulinia each from Praia Amor (6°S) and a single Mulinia from Praia Grande

(26°S). One Tivela specimen from Praia Cururupe (15°S) exhibited both an incomplete drillhole and a complete drillhole. Because of the rarity of multiple drillholes (Table 5), only MULT for ecoregions and provinces could be compared. Percentages for MULT were small at 1.5%

(Northeastern Brazil), 0.4% (Eastern Brazil) and 0.9% (Southeastern Brazil). Only differences between Northeastern Brazil and Eastern Brazil were statistically significant. Multiply bored specimens were not found in the Rio Grande; lack of drilling prevented comparisons to this ecoregion. Nearly equivalent MULT values were calculated at the scale of provinces for the

Brazilian (0.8%) vs. Argentinean (0.9%).

DISCUSSION

Overall Patterns in Drilling Predation

Naticid drillholes were documented at all 16 latitudes sampled. Intensity of drilling at the assemblage level varied across provinces and ecoregions, with increased drilling equatorward.

Analyses conducted using assemblage data for localities and latitudes indicated significant negative rank correlations of DF and latitude. Pairwise comparisons of DF between ecoregions also revealed significantly greater drilling at lower latitudes, but no differences in assemblage- level drilling could be detected between the middle ecoregions of Eastern Brazil and

Southeastern Brazil.

Escalation was originally proposed for drilling predation using assemblage data from the literature; however, recent publications have stressed the utility of examining patterns for lower taxa as well as size-standardizing data (Leighton, 2002; Vermeij, 2002; Ottens et al., 2012). In general, adoption of these protocols did not change the assemblage-level pattern of increased drilling at lower latitudes.

Eight of 27 drilled genera were selected for further analysis of latitudinal patterns at the level of individual taxa. These genera made up 92% of all drilled specimens and 62% of infaunal bivalves overall. Taxon DFs varied more than did drilling at the assemblage level; however, five of the eight genera indicated greater DFs in the Brazilian compared to Argentinean

Province (although not all differences were significant). Differences between provinces could not be detected for the remaining genera. Size-restricted analyses showed similar patterns for genera at the provincial level (Figure 4).

Taxon drilling at the scale of ecoregions fluctuated considerably more, but in many cases,

DFs were greatest for Northeastern Brazil followed by Eastern Brazil. Similar to the results for drilling at the assemblage level, differences between Eastern Brazil and Southeastern Brazil were not supported for most genera. Lack of specimens limited ecoregion comparisons (or support for differences) to the Rio Grande. Similar patterns were revealed using only size-standardized data

(Figure 5). Trends in drilling at the level of latitudes and localities were not usually supported statistically, but yielded negative rank correlations for most genera both with and without size standardization of data.

In summary, Anadara nearly always demonstrated significantly increased drilling equatorward regardless of how the data were treated. Anomalocardia and Tivela were more commonly drilled at lower latitudes, but showed reduced drilling in Northeastern Brazil. Chione

35 and Codakia indicated greatest drilling near the equator, but DFs for Eastern Brazil and

Southeastern Brazil were comparable. Latitudinal variation was not detected at the province level for Divalinga, Mulinia, or Strigilla; however, ecoregion comparisons exhibited decreased drilling of Divalinga and increased drilling of Mulinia in the northernmost ecoregion. Genera revealed negative rank correlations in drilling with both latitudes and localities except for

Divalinga (and Tivela when size-restricted). Most of these correlations were not statistically significant, however.

Size standardization rarely affected patterns in drilling for these eight genera, although significance of statistical analyses varied in several cases. Assessment of drilling using only size-restricted data for these eight genera combined did impact latitudinal patterns. No differences existed between provinces; however, ecoregion results were found to be significantly different, with the greatest drilling in Northeastern Brazil. Intensity of drilling was greater in

Southeastern Brazil vs. Eastern Brazil; insufficient number of specimens prohibited comparisons to the Rio Grande. Negative rank correlations were observed for drilling across both latitudes and localities, but lacked statistical support. This size-restricted dataset based on the eight genera combined accounted for 79% of all drillholes, but only 38% of all valves. Drilling on these genera was limited to specimens <30 mm (99% of all valves measured). Valves larger than

70 mm were not found among these eight genera and, overall, most specimens in my assemblages collected from Brazil were similarly sized.

Failed drilling was infrequent, but less common among lower latitudes based on PE. This pattern was significant upon comparing provinces; more variation existed between ecoregions.

Taxon-level analyses showed that failed attempts were greatest in Southeastern Brazil for

Anadara based on PE; however, this pattern was not statistically supported due to the small

36 number of drillholes in that ecoregion. The paucity of drilling attempts for Tivela limited assessment of failed attacks; a high value for PE in Southeastern Brazil was based on only five drillholes. Eastern Brazil demonstrated the lowest values of PE for both genera, apart from the lack of data for the Rio Grande. Neither incomplete drillholes nor multiply bored specimens were found in that ecoregion. Multiple boreholes were extremely rare, but concentrated at a single locality in Northeastern Brazil. Calculations of MULT revealed similarity between the

Brazilian and Argentinean provinces.

Potential Biases and Limitations of the Data

Environmental Variation

Latitudinal analyses require sampling over wide geographic areas, often encompassing numerous physiogeographic settings. This study attempted to control for environmental variation by focusing on infaunal bivalves indicative of shallow, sandy marine habitats.

However, beaches across Brazil are influenced by a variety of local conditions; mangroves, nearshore reefs, lagoons, river outlets, and rocky outcrops are not uncommon along the coastline

(Couto et al., 2003; Ferreira et al., 2009).

Direct sampling in mangroves, reefs, and lagoons, was explicitly avoided, although these habitats may be proximal to shallow marine ecosystems such as at the outlet of Lagoa dos Patos into the Atlantic (32°S). Output from this lagoon mostly extends southward along the coastline.

Sampling north and south of this outlet assuaged concerns regarding the local impact of this large lagoon as faunal composition and DFs were similar for both locations.

Influence from other waterways such as nearby rivers may have affected assemblages at localities Ilha de Itamaracá (8°S), Barra do São Miguel (10°S), Barra do Itarirí (12°S), Praia

Cururupe (15°S), Nova Viçosa (18°S), Penedo (21°S), and Praia do Sonho (26°S). Two beaches were sampled at each of these latitudes, allowing for a comparison of DFs between localities at the same latitude. Drilling frequency varied only up to 5% in most cases. The exception to this observation is Ilha de Itamaracá, which demonstrated much greater drilling (28%) than Praia

Calhetas (2%) at the same latitude. The latter locality was dominated by epifaunal organisms reflecting the prevalence of hard substrates at this location, likely accounting for the difference in the intensity of drilling. An additional beach that may be influenced by reduced salinities and finer sediments is Sambaqui (27°S), where sampling commenced on the bay side of the island of

Florianopolis. Exclusion of epifaunal organisms was particularly important at this locality, due to nearby oyster aquaculture. No other localities were sampled at this latitude, but DFs of 3% and 6% for the replicates collected here fall well within the range observed for the Southeastern

Brazil ecoregion. These values are also consistent with the average DF of 5.6% reported by

Simões et al. (2007) for bivalves collected from the South Brazil Bight in this ecoregion.

Many beaches in Brazil are characterized by a combination of sandy and rocky substrates

(except for the long stretches of sand that typify the Rio Grande). Sampling in rocky areas was sometimes necessary. Although I avoided direct sampling of rocky communities, reduced availability of softer substrates in a particular area may have influenced shell assemblages collected on the sand. Several localities had a higher representation of epifaunal organisms indicative of hard substrates, such as Praia Calhetas (8°S) and Barra Velha (26°S). Most of these localities yielded DFs <10% regardless of the latitudinal context and despite the fact that epifaunal taxa were removed prior to analyses (with the exception of a few Arcidae). One major exception is Praia Ouvidor (28°S), with a DF of 16%; however, this locality yielded the smallest sample size for a single location in the entire dataset (based on only 37 infaunal bivalves). In

38 addition, most valves were very small, in part due to sampling method (see below) and thereby perhaps more susceptible to naticid predation, as prey have not yet reached a size refuge limiting predatory attacks.

Exclusion of localities influenced by rocky outcrops did not change latitudinal patterns

(Figure 6), as hard substrates were scattered across all ecoregions except for the Rio Grande.

This southernmost ecoregion is composed almost entirely of sandy substrates and yet drilling was extremely rare. Ecoregion DFs for beaches dominated by softer substrates exhibited the same pattern from north to south (18%, 12%, 12%, 1%) as when all localities were included.

The effect of substrate was also limited by employing taxon-level analyses. All eight genera are indicative of shallow habitats with softer substrates (Abbott, 1974; Rios, 2009; Dias et al., 2011).

Focusing on infaunal bivalves inhabiting softer substrates for assemblage-level patterns minimized concerns regarding habitat variation as well.

Sampling Methods

Multiple sampling approaches were used in this study due to varying concentrations of shells available for collection (Figure 2). To assess potential biases resulting from different sampling methods, specimens were collected by both sweep and quadrat strategies at a single locality if feasible given a variety of factors. Most samples in this study were collected using the sweep method, but 10 quadrats were utilized (only one each in Northeastern Brazil and the Rio

Grande). Data from samples collected from the same beach were combined in all previous analyses, but are discussed separately here for the purpose of examining bias due to sampling method.

Figure 6. Increased drilling equatorward in Brazil for a) all localities, b) only beaches represented predominantly by soft substrates, and c) samples collected exclusively by the sweep method. Ecoregion assignment of localities indicated by marker color (see Figures 1, 3, 5).

a. 0.4

0.35

0.3 0.25 0.2 0.15 0.1 Drilling Frequency Drilling 0.05 0 0 10 20 30 40 Latitude

b. 0.4

0.35

0.3 0.25 0.2 0.15

0.1 Drilling Frequency Drilling 0.05 0 0 10 20 30 40 Latitude

c. 0.4

0.35 0.3 0.25 0.2 0.15

0.1 Drilling Frequency Drilling 0.05 0 0 10 20 30 40 Latitude

Both approaches were employed at Olivença (15°S), Laranjeiras (23°S), and Albatroz

(30°S). Quadrat DFs were less than values determined based on sweep samples, but only by

<3% for Olivença and Albatroz. Quadrat and sweep samples from Laranjeiras differed by 10%, perhaps in part due to sample size; only 67 infaunal bivalves were collected by quadrat as opposed to 311 specimens retrieved via sweep. Quadrat sampling did not consistently result in collection of fewer specimens, as nearly double the number of valves was obtained upon employing this approach at Olivença. Maximum DFs derived from quadrat sampling were 12%;

DFs for sweeps ranged up to 36%. This difference may in part be due to the more frequent utilization of the sweep approach overall, especially in that only one quadrat was used in

Northeastern Brazil where drilling was greatest.

Different sampling methods could have affected the size distribution of shells collected and therefore drilling frequencies, as drillholes were more common in smaller specimens <30 mm. For instance, quadrats, “smash and grab” sampling, and the use of a sieve in the surf might yield smaller specimens that could be missed by walking on the beach. In the Rio Grande, low concentrations of shells required employment of mostly sweep methods for sample collection, and small specimens in these samples were rare. Most bivalves were >30 mm, except for abundant Donax. Use of a sieve in the surf to supplement specimens collected on the beach at

Hermenegildo (34°S) may have partially alleviated this concern. More drilled specimens were found in the sample collected in part using this strategy (DF = 5.6%) compared to sweeps on the beach in which no drillholes were found; pooling samples at this locality reduced the DF to

1.5%. Yet, both DFs are relatively low, consistent with levels of drilling reported at other localities in the Rio Grande. Use of a sieve in the surf also supplemented specimens collected on the beach at Ilha de Itamaracá (8°S); intensity of drilling at this locality, however, reflected DFs

41 obtained for nearby sandy beaches in the ecoregion where shells were collected exclusively by sweeps. The only localities in which “smash and grab” sampling was utilized were Praia

Calhetas (8°S) and Praia Ouvidor (28°S), addressed earlier for concerns regarding the influence of rocky substrates and/or small sample sizes. In general, sampling by “smash and grab” methods or use of a sieve in the surf was infrequently employed, and should not have a significant effect on latitudinal patterns in drilling. When analysis is restricted to samples collected exclusively by sweeps, increased drilling equatorward is still observed across localities in Brazil (Figure 6). The robustness of this pattern may in part be due to limiting the dataset to bivalves greater than 5 mm in length. In addition, size standardization of data minimized concerns about different size distributions related to collecting method; greater drilling in the northernmost ecoregion was still noted upon size standardizing data for the eight genera combined.

Anthropogenic Effects

Less populated beaches were sampled when available; however, restricted accessibility to the coastline in parts of Brazil often led to sampling in areas locally impacted by humans.

Factors that might influence DFs can be broadly recognized as either biases in the sampling of shell assemblages on beaches or ecological effects related to harvesting of live animals that directly alter the dynamics of molluscan communities.

Shell collecting is common among beach-goers of all ages globally, and preferential culling of shells both with and without drillholes is conceivable. In addition, the world market for shells used in crafts and as souvenirs is significant. Dias et al (2011) conducted an inventory of mollusk species sold as curio objects and souvenirs in Northeastern Brazil. Gastropods

42 dominated the list of species marketed, comprising 62% of the 116 species recorded (not all endemic to Brazil). For this reason, and because gastropods are less abundant, my studies of drilling predation were restricted to bivalves.

Dias et al. (2011) considered most shells sold as curios to be the result of harvesting live specimens. Declines in some predatory gastropod populations (cassids and volutids) were noted as a result of over-exploitation. However, only two of the dozen species of naticids found in

Northeastern Brazil were documented as sold in souvenir shops by Dias et al. (2011). The infaunal life mode and simple morphology of naticids should make them less attractive targets for souvenirs than large, highly ornamented and more easily accessible gastropods. Natica marochiensis was reported as edible by Dias et al. (2011), and Souza et al. (2010) recorded

Natica canrena and Polinices hepaticus from archaeological shell middens near Rio de Janeiro.

Thus some reduction in the naticid population may occur from human exploitation for food, but probably did not reduce drilling frequencies significantly.

Species inhabiting shallow soft bottom habitats comprised 42% of those documented by

Dias et al. (2011) and are likely collected live frequently due to ease of access. Bivalves are often used for decorative purposes and well-preserved shells on the beach could be collected for such use. Of the 27 genera drilled in my assemblages, over half are recorded on the list by Dias et al. (2011), including seven of the genera analyzed for patterns in drilling (all but Strigilla).

This occurrence is not surprising, as the eight genera I studied composed 62% of the assemblages collected. Bivalves of the Family Veneridae are most commonly exploited for souvenirs; several species are reported as consumable seafood as well. Anomalocardia is noted as an important edible bivalve throughout its range and can be a major source of income for entire fishing villages (Dias et al., 2011). Anadara, Divalinga, and Tivela are additionally documented as

43 edible bivalves, although Couto (1996) stated that Divalinga is not of commercial interest.

Because my samples were dominated by small specimens, and because size-standardized data generally support the same latitudinal trends as non-standardized data, bias due to beach collecting or harvesting for food is unlikely. Furthermore, although beaches were more populated in Northeastern Brazil, Eastern Brazil, and Southeastern Brazil, abundance of shells likely limited potential biases. The more desolate Rio Grande ecoregion may have been more prone to collecting bias by beach-goers, especially for shells that are well-preserved, because of the paucity of shells overall. However, in the Rio Grande, bias was against smaller shells and thus was not likely the result of curio and souvenir collection. Larger specimens and species are collected preferentially for both food and souvenirs (Dias et al., 2011). However, live collection of the small genus Donax by locals was observed at Albatroz (30°S). Lack of drilling on this genus and the dominance of the assemblage by Donax despite clamming activities ameliorates concerns about the impact of live Donax harvesting at Albatroz. No clamming activities were noted at any other collecting sites.

Other anthropogenic impacts were recorded during field work, including vehicles being driven on the beach, which led to broken shells at a few localities. Large shells would be most susceptible to this breakage; size standardization of data alleviated such bias. At Marataízes, boats in dry dock were observed, along with large accumulations of mussels and barnacles likely scraped from them. This problem was mitigated by excluding all epifauna from analysis.

Evidence of water pollution was observed at Mongaguá. In all cases where substantial anthropogenic impact was suspected, DFs were compared between impacted and neighboring localities in the same ecoregions. Good correspondence of DFs (within a few percent) indicated that bias was not significant.

Preservational Factors

Several factors may influence the size, quality, and type of infaunal bivalves preserved in dead assemblages on the beach. Preservational bias against smaller specimens may be present, particularly in the Rio Grande ecoregion, as oceanographic conditions are harsher than in areas to the north due to wind-driven changes that seasonally impact beach profiles (Machado et al.,

2010). It could be that smaller shells do not survive post-mortem processes in such harsh conditions or are deposited farther offshore as a result of these storms (Absalão, 1991), reducing the potential for drillholes to be found in beach-collected specimens. Also perhaps as a consequence of rough oceanographic conditions, larger shells (>30 mm), more commonly found in this ecoregion, are usually not well preserved, with the exception of likely recently deposited intertidal bivalves (e.g., Mesodesma). Many large shells in the Rio Grande lack coloration and are broken, abraded, and worn. It is not uncommon for large irregular rounded sections to be missing from the umbonal region of specimens. Thus, drillholes in larger shells may no longer be visible due to poor preservation, although this particular concern is alleviated by the use of nearly whole specimens for drilling analyses.

In general, all DFs in the Rio Grande are still considerably less compared to the average

DFs of the other ecoregions, suggesting that despite preservational biases, drilling is still lowest in the Rio Grande. This decrease in drilling with latitude is confirmed by taxon-level analyses of drilling in Anadara, with data included for the Rio Grande. Unfortunately, limited number of specimens prevented interpretation of drilling patterns in this ecoregion using size-standardized data.

Western Atlantic: North vs. South

The equatorward increase in drilling for the Western Atlantic of the Southern Hemisphere suggested by assemblage data in this study is contrary to the results of Kelley & Hansen (2007) for the Northern Hemisphere. They reported greatest drilling among mid-latitudes (~28°30ʹN–

35°N), with a decline both poleward and equatorward based on DFs for molluscan faunas overall

(Nova Scotian, 8%; Virginian, 13%; Carolinian, 28%; Gulf, 18%). Their analyses restricted to infaunal bivalves yielded a similar peak in the Carolinian (29%) and reduced drilling for the

Nova Scotian (17%), Virginian (16%), and Gulf (22%) provinces. Less drilling is reported here across Brazil at both the level of ecoregions (Northeastern Brazil, 15%; Eastern Brazil, 11%;

Southeastern Brazil, 10%; Rio Grande, <1%) and provinces (Brazilian, 12%; Argentinean, 5%).

Results for lower taxa also differ between this study and that of Kelley & Hansen (2007).

The mid-latitude peak in assemblage-level drilling described by Kelley & Hansen (2007) was further supported by their data on the Family Arcidae (dominated by Anadara) and for the mactrid bivalve Spisula. The pattern did not hold for the venerid bivalve Mercenaria, but Kelley

& Hansen (2007) dismissed this result based on concerns regarding additional sampling and size bias. The present study examined similar lower taxa to those employed by Kelley & Hansen

(2007). Anadara in Brazil reflected latitudinal patterns observed at the assemblage level.

Venerid bivalves Anomalocardia, Chione, and Tivela revealed greater drilling equatorward at the scale of provinces, but results for ecoregion DFs were more varied. Mactrid bivalves in each hemisphere displayed patterns similar to those at the assemblage level; Mulinia was drilled the most in Northeastern Brazil, although increased drilling equatorward was not detected at the scale of provinces for that genus. Lucinid bivalves in Brazil demonstrated mixed patterns, with greater drilling at lower latitudes for Codakia, but no differences in drilling across ecoregions or

46 provinces for Divalinga (or Strigilla in the Family Tellinidae). Tellinids and lucinids were not explicitly examined by Kelley & Hansen (2007).

Evaluation of failed drilling by Kelley & Hansen (2007) at the assemblage level demonstrated an inverse pattern to DF, with the lowest values for PE and MULT in the

Carolinian Province. Similarly, an inverse relationship was found for PE using assemblage data in Brazil at the scale of provinces. This pattern was partially reflected across ecoregions, with the greatest PE in Southeastern Brazil. Likewise, PE was highest for Anadara in Southeastern

Brazil. Incompletely bored Tivela indicated a similar pattern, but insufficient number of drillholes prohibited statistically valid comparisons. Both PE and MULT for arcid bivalves revealed increased failed attempts at lower latitudes in the study by Kelley & Hansen (2007), similarly supporting the inverse relationship to DF noted at the assemblage level.

Naticid drilling across eastern North America also was studied by Alexander & Dietl

(2001) using beach-collected samples for Anadara and Divalinga only. They reported an increase in drilling equatorward based on samples from New Jersey to Florida. Incomplete drillholes were rare in Anadara, but PE increased toward lower latitudes for Divalinga. Their study focused on differences in drilling data due to changing populations of naticid species along the coastline. Kelley & Hansen (2007) reinterpreted the results presented by Alexander & Dietl

(2001), and suggested that the data coincided instead with intense drilling in the Carolinian

Province and decreased drilling elsewhere.

A study similar to that of Kelley & Hansen (2007) was conducted by Funderburk (2010) from southern Virginia to Texas using beach-collected shells. The peak in mid-latitude drilling found by Kelley & Hansen (2007) was corroborated, with assemblage-level DFs of 32.4% for the

Carolinian Province. Reduced drilling was documented for the Virginian (14%) and Gulf-

Louisianan (16.1%); analyses restricted to bivalves yielded similar patterns. Funderburk (2010) noticed extremely high DFs (~60%–120%) for a few localities in the Carolinian, however

(compared to maximum DFs for the Carolinian of ~45% reported by Kelley & Hansen, 2007).

Funderburk (2010) inferred that his outliers may have been a result of hydrodynamic sorting, and consequently removed them, yielding a revised DF of 17.7% for that province. Because his samples contained mixed fauna indicative of a variety of habitats, multivariate analyses were used to delineate assemblages that derived under different conditions. After removing an outlier in the Carolinian, Funderburk (2010) reported that DFs analyzed for community groups revealed no correlations with latitude. Taxon-level analyses for Anadara, Chione, Donax, and Mulinia, which flourish in different environmental settings, were interpreted to support the lack of latitudinal patterns in drilling regardless of habitat conditions (after removing several outliers that otherwise suggested greater drilling in the Carolinian). Funderburk (2010) also reported inconsistencies in intensity of drilling for some of the localities that were studied also by Kelley

& Hansen (2007). In summary, he concluded that DFs varied widely at a range of spatial scales due to a multitude of complex and random variables, as often occurs with biological data.

Funderburk (2010) hypothesized that higher DFs may be due to ecological variables such as increased diversity and productivity near province boundaries or post-mortem biases in shell accumulation. He proposed that an estimated DF for modern assemblages over the entire area studied is best represented by a mean of 16.6% ± 9.8% or the median value of 14.8%.

The studies by Funderburk (2010) and Kelley & Hansen (2007) differ in several important respects. Latitudinal coverage in the Funderburk study was more limited than that by

Kelley & Hansen (11 degrees versus 18 degrees of latitude). Funderburk (2010) restricted spatial coverage for the Virginian Province to southern Virginia and North Carolina, whereas

Kelley & Hansen (2007) sampled the entire province extending northward to Massachusetts.

Lower latitudes studied by Funderburk (2010) are heavily dominated by localities in the Gulf of

Mexico. Kelley & Hansen (2007) discussed concerns regarding the identity of predators within the abundant seagrass habitats of this region. Predatory muricid gastropods typically drill cylindrical drillholes of the ichnogenus Oichnus simplex, in contrast to the beveled drillholes (O. paraboloides) usually attributed to naticids (Bromley, 1981). However, the muricids

Phyllonotus pomum and Chicoreus dilectus, which are common in seagrass habitats in the Gulf

Province, produce beveled drillholes resembling the work of naticids (Herbert & Dietl, 2002).

Thus to ensure that their data were restricted to naticid drilling, Kelley & Hansen (2007) reanalyzed their data with known seagrass localities in the Gulf Province omitted (although they found no difference in their results). They also focused on infaunal bivalve prey, which are more susceptible to naticid drilling than to predation by epifaunal muricids. Funderburk (2010) did not attempt to distinguish drilling by naticids vs. muricids, in part due to difficulties in predator identification based on drillhole morphology (although drillhole site can be used to aid in characterizing naticid and muricid drillholes). Funderburk (2010) also included both infaunal and epifaunal mollusks (such as oysters, scallops, and mussels) in his analyses. These differences in the approaches of Kelley & Hansen (2007) and Funderburk (2010) may contribute to apparent differences in their results.

Because the goal of the present study was to test the robustness of the latitudinal pattern reported by Kelley & Hansen (2007), I employed similar protocols of limiting assessment of latitudinal patterns to data on naticid predation of infauna. This procedure excluded beveled drillholes that were occasionally noticed in oysters, mussels, and nestling bivalves that were more likely preyed upon by muricids (see Gordillo, 1998b; Gordillo and Amuchástegui, 1998).

Concerns regarding muricid drilling were reduced further by excluding localities influenced by rocky substrates, which are more commonly inhabited by muricids. Any bias due to possible inclusion of muricid drilling is likely to be minimal. For example, beveled drillholes in several byssally attached Arcidae (e.g., Arca, Arcopsis, Barbatia) could have been the result of predation by muricids. However, drilling was infrequent in these genera, and if excluded, existing latitudinal patterns are unaffected or enhanced. Exclusion of these genera at Praia Calhetas

(8°S), of which 85% of the sample is composed, does not change the anomalously low DF of

2%. Elimination of these genera at Praia da Pipa (6°S) yields an increase in DF from 6% to

11%, enhancing the latitudinal pattern of increased drilling at lower latitudes. These genera are not well represented at most other localities, limiting concerns regarding their influence on latitudinal patterns when all data are included.

Multiple treatments of the data in this study suggest that the pattern of equatorward drilling is robust. The following sections examine what factors may be influencing this pattern in Brazil and how differences in latitudinal patterns between hemispheres may be explained.

Temperature and Seasonality

Alexander & Dietl (2001) reported greater drilling toward the equator and suggested that increased rates of metabolic processes due to warmer temperatures in lower latitudes may be part of the explanation for their patterns. Indeed, greater frequency of feeding is supported by laboratory results conducted as part of the next chapter of this dissertation, as well as the work of others studying naticids, as reviewed in Chapter Three. Temperatures are consistently greatest in

Northeastern Brazil near the equator and may contribute to the increased DFs observed in that

50 ecoregion. Similarly, minimal DFs in the Rio Grande could in part be explained by cooler conditions leading to reduced drilling.

Tropical environments offer opportunities for increased protection of prey, due to the ease of CaCO3 precipitation in warmer waters (Graus, 1974). Thicker or more highly ornamented shells should limit susceptibility to drilling predation, implying that near the equator failed attempts should be greater and successful drilling less common. Predation pressure is also regarded as stronger in lower latitudes, in part due to the high diversity of abundant predators

(Vermeij, 1978; Vermeij et al., 1989). Enhanced likelihood of interruption of drilling due to abundant and diverse predators in the tropics should similarly yield lower drilling frequency and greater prey effectiveness at lower latitudes, as partially supported by the results of Kelley &

Hansen (2007). Increased DFs equatorward in Brazil do not support such a pattern; data on unsuccessful drilling are limited but suggest less failed drilling at lower latitudes (except for the absence of incomplete drillholes in the Rio Grande). Higher metabolic rates of naticid gastropods inhabiting lower latitudes may be more important, as suggested by greater drilling equatorward in Brazil.

The mismatch in the peak in drilling for the mid-latitudes of the Northern Hemisphere and the lack of drilling along the same latitudes in Brazil may be partly related to differences in regional climates. The Brazil study area is characterized by Tropical (Northeastern Brazil,

Eastern Brazil) and Warm Temperate (Southeastern Brazil, Rio Grande) provinces; localities studied by Kelley & Hansen (2007) are represented by Cold Temperate (Nova Scotian,

Virginian), Warm Temperate (Carolinian, Gulf - northern Gulf of Mexico only), and Tropical

(Gulf - southern half of Florida only) provinces as outlined by Spalding et al. (2007). Although

Tropical as well as Warm Temperate provinces were sampled in both hemispheres, such

51 equivalent names do not necessarily reflect similarity in sea surface temperatures (SSTs) for these regions.

Temperatures are highest and most consistent in Northeastern Brazil between 26–29°C

(Castro & de Miranda, 1998). Eastern Brazil (22–27°C) and Southeastern Brazil (20–27°C) are still relatively warm, but vary more due to seasonality (and localized upwelling can lead to even cooler conditions in both ecoregions). The Rio Grande is also greatly influenced by seasonality; surface waters in the summer can reach up to 26°C, but may be cooler than 15°C in the winter.

Despite seasonal changes, mean values in this southernmost ecoregion vary within 16.8°C and

20°C (Castro & de Miranda, 1998). Mean SSTs for the provinces studied by Kelley & Hansen are 10°C (Nova Scotian), 15°C (Virginian), 22°C (Carolinian), and 24°C (Gulf), all of which can be impacted greatly by seasonality (based on data compiled for individual localities using the

National Oceanographic Data Center available online through NOAA: http://www.nodc.noaa.gov/dsdt/wtg12.html).

The Tropical and Warm Temperate areas sampled by Kelley & Hansen (2007) are representative of mean SSTs that are 25°C and 22°C, respectively. Mean SSTs are 26°C for

Tropical and 21°C for Warm Temperate regions in Brazil. This broad-scale view demonstrates similarity between hemispheres, but upon examining SSTs over smaller scales, more disparity is revealed. For example, latitudes in the Carolinian (35°N–28°30′N) for the Northern Hemisphere are similar to those of the Rio Grande (28°40′S–34°S) in the Southern Hemisphere. The mean temperature for this ecoregion is 18.4°C whereas in the Carolinian, mean SST is higher at 22°C.

Temperatures of the Rio Grande are more similar, but not fully equivalent, to the cooler conditions of the Virginian (mean SST of 15°C). Temperature differences for specific latitudes may account for some of the variability between hemispheres, but not all. Drilling in the Rio

Grande remains uncharacteristically low. Peak drilling of infaunal bivalves in the Northern

Hemisphere occurred in the Carolinian (29%), with a mean SST of 22°C for these mid-latitudes.

In contrast, lower latitudes of Northeastern Brazil are typified by extremely warm conditions

(27.5°C), yet ecoregion drilling only peaks at 15%. Seasonality may play a role in these differences as it is much more prevalent in the Carolinian compared to the steady warm waters of

Northeastern Brazil, but reduced seasonality in Northeastern Brazil would likely have produced higher DFs than in the Carolinian, contrary to the results. The influence of seasonality apart from temperature such as fluctuations in salinity, storms, and other abiotic and biotic variables is another factor for consideration in interpreting latitudinal patterns of drilling, which is the focus of the next chapter of this dissertation.

Naticid Diversity

Although temperature and seasonality may contribute to latitudinal differences in drilling predation in Brazil, these factors cannot fully explain the paucity of drilling in the southernmost portion of Brazil. Despite similarity to the Carolinian Province in latitude and to the Virginian

Province in temperature, Rio Grande DFs are much lower than those reported by Kelley &

Hansen (2007) for the Northern Hemisphere. Evaluation of naticid distribution across Brazil may shed light on this mystery.

Most naticid species are concentrated to the north of the Rio Grande (Table 6). Only one species, Notocochlis isabelleana, is confirmed across the geographic extent of this ecoregion based on multiple sources; it is not entirely clear if Polinices lacteus is present consistently throughout the Rio Grande. Rios (2009) reported the range of P. lacteus as encompassing all of

Brazil, but the southern limit is listed as Santa Catarina and 30°S in the online database for

Table 6. Shallow water naticids documented in the Brazil study area as based on Rios (2009) and the Malacolog database (Rosenberg, 2009), from which data was obtained also for the study area of Kelley & Hansen (2007). Taxon names and maximum reported sizes are from Malacolog (and do not reflect the latest classification by Torigoe & Inaba, 2011). Questionable occurrences and dubious names discussed in these references are not included here. Abbreviations: NS (Nova Scotian), VA (Virginian), CA (Carolinian), GU (Gulf), NE (Northeastern Brazil), E (Eastern Brazil), SE (Southeastern Brazil), RG (Rio Grande).

Taxon Max Size NS VA CA GU NE E SE RG Amauropsis islandica 40 mm X X Euspira heros 115 mm X X X Euspira immaculata 10 mm X X Euspira pallida 42 mm X X X Euspira triseriata 33 mm X X Haliotinella patinaria 14 mm X Natica livida 21 mm X X X X X Natica marochiensis 40 mm X X X Natica menkeana 18 mm X X X Natica tedbayeri 22 mm X X Naticarius canrena 65 mm X X X X X Neverita delessertiana 67.5 mm X X Neverita duplicata 82 mm X X X X Notocochlis isabelleana 30 mm X X X Polinices hepaticus 51 mm X X X X Polinices lacteus 40 mm X X X X X X Sigatica carolinensis 11 mm X X X Sigatica semisulcata 15 mm X X Sinum maculatum 34 mm X X X X X X Sinum perspectivum 51 mm X X X X X X Stigmaulax cancellatus 24 mm X X Stigmaulax cayennensis 35 mm X Stigmaulax sulcatus 38 mm X Tectonatica micra 4.4 mm X Tectonatica pusilla 8 mm X X X X X X X

Western Atlantic Mollusca (Malacolog: Rosenberg, 2009). Wiggers & Veitenheimer-Mendes

(2003) reported this species, as well as Tectonatica pusilla, from collections retrieved at 100 m depth near 32°55′S. Tectonatica pusilla is extremely small; drillholes resulting from this moon snail are likely to be scarce in any of the samples collected from Brazil as only specimens >5 mm were analyzed. Thus the Rio Grande is characterized by a total of three naticid species, only one of which is common throughout the ecoregion and likely contributed significantly to the drilling observed in this study. The other ecoregions are represented each by 10–12 naticid species.

Low naticid diversity in the Rio Grande may partly account for low frequency of drilling documented in this southernmost ecoregion of Brazil. Similarly, higher diversity of naticids in all other ecoregions analyzed may contribute to the pattern of increased drilling among lower latitudes.

However, naticid diversity cannot fully explain differences in drilling patterns reported for the Western Atlantic of the Northern vs. Southern Hemisphere. Although diversity of moon snails is higher for the entire area studied by Kelley & Hansen (2007), with 20 species compared to only 14 reported in Brazil (Table 6), number of species in the Virginian (10), Carolinian (12), and Gulf (15) is fairly comparable to values reported for Northeastern Brazil (12), Eastern Brazil

(11), and Southeastern Brazil (10). Yet, DFs for these latitudes are very different and range from

16%–29% along the U.S. East Coast, but only vary between 10%–15% in Brazil (Figure 7). The lower drilling frequencies documented here are supported by the work of Simões et al. (2007), who similarly reported lower levels of drilling (0%–13%) for infaunal bivalves of the South

Brazil Bight.

Figure 7. Drilling frequencies across latitudes for ecoregions of Brazil from this study and provinces used by Kelley & Hansen (2007) for eastern North America.

0.35

0.3

0.25

0.2

0.15 EQUATOR

Drilling Frequency Drilling 0.1

0.05

0 45 35 25 15 5 -5 -15 -25 -35 -45 (Northern Hemisphere) Latitude (Southern Hemisphere)

Alternate Modes of Predation

Intra- and inter-hemisphere differences in drilling could occur if naticid species in different regions employed different modes of predation. Drilling is the dominant predatory strategy employed by naticids; however, other forms of predation are reported in the literature, as reviewed in Chapter Four of this dissertation. Kelley & Hansen (2007) commented that alternate modes of predation may help explain the decreased drilling they observed in cooler climates of the Virginian and Nova Scotian provinces. Similarly, Simões et al. (2007) hypothesized that alternative attack strategies may be contributing to low drilling frequencies documented in the

South Brazil Bight. However, my review of the subject as part of this dissertation indicates that reports of behaviors such as suffocation may be due largely to fortuitous events in laboratory settings resulting from unhealthy prey; alternate modes of predation may not be common in natural settings. Furthermore, suffocation is presumably a slow process and should not be favored evolutionarily because results are unpredictable; a predator is not in control, but success depends on prey respiration rates. However, if suffocation is faster as aided by toxins, decreased drilling is more likely to be found in the tropics as a result of this alternate behavior. This hypothesis supports the findings of Kelley & Hansen (2007), but does not align with the peak in drilling observed near the equator as part of this investigation. Review of the literature in

Chapter Four of this dissertation demonstrates that alternate modes of predation are not reported for naticids from Brazil. However, data on feeding behavior are lacking for many naticid species and study of toxins, perhaps used by naticids in alternate modes of predation, are limited to the

Indo-Pacific. Previous reports of suffocation for moon snails found in the Western Atlantic of the Northern Hemisphere need to be re-evaluated in light of concerns regarding poor prey health and questionable extrapolation of laboratory results to field settings. Thus the occurrence of

57 alternative modes of predation by naticids does not appear to be responsible for differences in drilling intensity within Brazil and in comparison to the Northern Hemisphere.

Predator-Prey Size Distributions

Differences in drilling metrics for Anadara and Divalinga along the U.S. East Coast were attributed to varying species of naticids that exhibited differences in pedal mass and consequently the ability to drill their prey successfully (Alexander & Dietl, 2001). Size- standardization of the data and general similarity in predator sizes across ecoregions (Table 6) should limit differences in drilling due to varied handling abilities of different naticid species.

However, size distribution of naticids along the coastline of Brazil and of available prey (or of prey shells present in the death assemblages) may relate to low DFs in the Rio Grande.

Maximum sizes recorded for naticid species in southernmost Brazil are 30–40 mm (Malacolog:

Rosenberg, 2009), suggesting that predation is likely to be limited to smaller prey. However, most bivalves in my assemblages from the Rio Grande were at least 30 mm in size, with the exception of abundant Donax. Because drilling is typically more common in smaller bivalves

(e.g., Couto, 1996), decreased drilling in the Rio Grande may result in part from fewer small specimens (either of available prey or as preserved in beach assemblages). Greater range of predator sizes in the other ecoregions due to enhanced naticid diversity may have allowed for increased opportunities for drilling a larger range of prey sizes elsewhere.

Kelley & Hansen (2007) attributed differences in drilling patterns between Mercenaria and multi-taxon assemblages to inter-province differences in size distribution of Mercenaria.

Specimen size data were not collected for taxa other than Mercenaria, so the effect of predator- prey size distribution on the Northern Hemisphere drilling patterns of Kelley & Hansen (2007) is

58 unclear. Furthermore, size-standardized analyses were not provided by Funderburk (2010).

Predator-prey size distribution differences remain an unknown but potentially important factor in explaining differences in drilling patterns between Brazil and the Northern Hemisphere.

Prey Diversity

Differences in predator-prey size distributions may result from both taphonomic factors

(see above) and available prey taxa inhabiting an area. Availability of prey commonly consumed by naticids is markedly different in the Rio Grande assemblages relative to other ecoregions.

The distinctiveness of the Rio Grande assemblages in terms of taxonomic composition is not an artifact of taphonomic or other biases, as molluscan assemblages recorded for the Rio Grande in this study are consistent with the work of others in the region (Absalão, 1991; Scarabino, 2003;

Scarabino et al., 2006). Assemblages are less diverse overall and are usually dominated by the intertidal genus Donax, followed by larger specimens of poorly preserved arcids, venerids, and especially mactrids. Drilling may be reduced in this southernmost ecoregion because suitable small-bodied prey are sparse in my assemblages (either due to rarity in the living community or due to preservational bias as discussed above). Prey drilled in other ecoregions, including

Anadara, Anomalocardia, Divalinga, and Tivela, are documented, but are less commonly represented compared to assemblages north of the Rio Grande. Prey reported in the literature as drilled by naticids are also uncommon. For example, Rios (2009) noted that the primary moon snail of the Rio Grande, Notocochlis isabelleana, attacks Tellina, and that Polinices lacteus preys upon Tellina and Anomalocardia, but these prey genera are rare in my samples from this ecoregion. Drilling by N. isabelleana is also documented for Mactra, Corbula, and Glycymeris nearby in Quaternary fossil deposits of Uruguay (Lorenzo & Verde, 2004). These genera are

59 present in my Rio Grande assemblages, but only Mactra is common (and mostly at large sizes), although drilled specimens of both Mactra and Glycymeris were collected.

Assemblages in the Rio Grande are also enriched in intertidal taxa compared to assemblages at lower latitudes. Greater relative abundance of intertidal faunas along the Rio

Grande may be diminishing assemblage-level DFs by reducing the comparative abundance of prey more commonly consumed by naticids in Brazil. However, naticids inhabiting the ecoregion should overlap in distribution with the abundant, small-bodied Donax. Notocochlis isabelleana and Polinices lacteus can inhabit deeper environments (~100 m), but ranges for both species are listed as extending into intertidal areas (Malacolog: Rosenberg, 2009). Specimens of smaller, well-preserved Donax are plentiful yet, oddly enough, drilling on Donax was not found in this ecoregion, but only at 12°S and 28°S. Availability of abundant smaller specimens of this genus for drilling suggests that the low DFs characteristic of the Rio Grande ecoregion are not solely attributable to the absence of suitable small-bodied prey.

Interestingly, latitudinal gradients in bivalve diversity exhibit asymmetry between hemispheres, similar to the differences observed in drilling between this study and that of Kelley

& Hansen (2007). Crame (2000) reported that more variability in bivalve diversity existed in global data from the Southern Hemisphere and that the Northern Hemisphere exhibited a marked inflection around 30°N, beyond which diversity declined steeply poleward. He proposed that large-scale north-south asymmetry in biodiversity patterns may be a result of prevailing oceanographic conditions as opposed to the sole influence of latitude. Tropical diversity of bivalves in the Western Atlantic is also reported as greater in the Northern Hemisphere, but

Crame (2000) recognized that a sampling bias may be involved; faunas are likely understudied along eastern South America. Similarly, intensity of drilling along the U.S. East Coast is higher

60 compared to Brazil (Figure 7), but this difference should not be an artifact of sampling. The average number of specimens per locality is greater in this study than in that of Kelley &

Hansen, 2007 (852 vs. 377 specimens); nonetheless, sample sizes in both studies should be sufficient for analyses of drilling predation, unlike earlier reports that may have used pooled data on fewer specimens from unrelated populations, as discussed by Funderburk (2010). However, in using this sort of pooled data, Vermeij et al. (1989) observed a mid-latitude peak in drilling for the Northern Hemisphere but, presumably due to limited data from higher latitudes, interpreted the latitudinal pattern as decreasing into the tropics instead.

Paleontological Implications

Drilling data are spatially variable (e.g., Vermeij, 1980), yet latitudinal patterns have been demonstrated, even if inconsistent among studies. Variable methodological approaches and environmental variation may account for some of the differences reported in the literature. If the patterns documented in this study for eastern South America are biologically meaningful, can they be used to explain any temporal patterns in drilling predation based on paleontological assemblages? What are the implications of this study for conclusions about escalation drawn from the fossil record of drilling?

Most studies of long-term patterns of drilling in the fossil record are based on database or literature surveys (e.g., Vermeij, 1987; Kowalewski et al., 1998; Harper, 2003; Huntley &

Kowalewski, 2007). Such work has revealed general patterns in escalation of drilling predation through the Phanerozoic, including significant intervals of increasing predation intensity in the mid-Paleozoic (or perhaps earlier; Huntley & Kowalewski, 2007) and again in the late Mesozoic-

Cenozoic. These compilations have employed coarse time bins (e.g., at the level of geological

61 period for studies by Kowalewski et al., 1998, and Huntley & Kowalewski, 2007). They have also combined data globally (though Harper, 2003, noted that such “global” datasets are dominated by studies from North America and Western Europe). These works therefore lack the fine stratigraphic and spatial resolution to allow assessment of the influence of geographical variation in drilling predation. Detailed collections by Kelley & Hansen (1993, 1996, 2003,

2006) offer the best opportunity to assess potential influence of spatial variation in drilling on long-term temporal trends (see Walker & Brett, 2002).

Kelley & Hansen (1993, 1996, 2003) examined patterns of escalation in drilling from the

Cretaceous to the Pleistocene for bulk assemblages from 28 shallow marine formations in the

Atlantic and Gulf Coastal Plains. They revealed a more complex pattern than initially described by Vermeij (1987). Drilling was low to moderate in the Cretaceous, declined at the K-P boundary, and abruptly increased in the Paleocene, remaining at high levels for much of the

Eocene. Prior to the E-O boundary, drilling declined, but then increased into the Oligocene. The

Miocene was characterized by more intense drilling, and followed by a decrease into the

Pliocene, steadying through the Pleistocene. Further work at the lower taxon level corroborated these assemblage-based patterns in drilling (Kelley & Hansen, 2006).

This episodic pattern was initially linked to mass extinctions, but upon examining prey morphologies, no relationship was found between increases in drilling and preferential extinction of highly escalated prey (Hansen et al., 1999; Reinhold & Kelley, 2005). Kelley & Hansen

(2007) posited a link between escalation patterns and climate instead, because samples from different latitudes were used in their study of escalation (as controlled by the availability of fossil outcrops). For instance, Cretaceous data were derived from Gulf Coast assemblages, but the initial post-Cretaceous surge in drilling occurred in the Paleocene Brightseat Formation of

Maryland. A latitudinal shift in sampling also occurred between the Paleogene, represented primarily by Gulf Coastal Plain samples, and the Neogene of the middle Atlantic Coastal Plain.

Within the middle Atlantic Coastal Plain, sampling shifted from the Miocene of Maryland to the

Pliocene of Virginia and Pleistocene of North Carolina. Furthermore, climate varied greatly during the Cenozoic (Zachos et al., 2001) and may be contributing to the temporal patterns.

Hansen & Kelley (1995) explicitly examined latitudinal differences in drilling frequency between the Eocene Cook Mountain interval of the Gulf Coast and the coeval Piney Point

Formation of Virginia and found greater drilling at higher latitudes, suggesting that concern about geographic and climatic variation is warranted.

The present study revealed increased drilling equatorward in Brazil, suggesting that warmer conditions might be characterized by more intense drilling in the fossil record. To some extent, this hypothesis is supported by the patterns documented by Kelley & Hansen (1993,

1996, 2003, 2006). The Paleocene-Eocene represents the warmest climates of the Cenozoic

(Zachos et al., 2001); high levels of drilling (~30–40%) on bivalves are noted for this interval.

Cooling of climate in the late Eocene was accompanied by low drilling (<10%); however, moderately high DFs (~20%) were found early in the Oligocene following further cooling crossing the Eocene-Oligocene boundary, contrary to this hypothesis. Increased DFs (~30–40%) in the mid-Miocene are representative of warmer conditions; drilling on bivalves declined from the late Miocene Eastover Formation (35%) through the Pliocene Yorktown Formation (25%) into the Pleistocene (13–14%) as climate cooled. This Miocene to Pleistocene decline is consistent with the decrease in drilling observed in higher latitudes of Brazil, although the pattern reported by Kelley & Hansen (2003, 2006) is complicated by a concomitant shift in sampling to lower latitudes (from Maryland to North Carolina). Thus much of the variation in

63 drilling frequency reported by Kelley & Hansen (1993, 1996, 2003, 2006) is consistent with the results of this study, although an equatorward increase in drilling does not explain the higher drilling frequencies in the Eocene Piney Point Formation of Virginia relative to the Cook

Mountain of the Gulf Coastal Plain (Hansen & Kelley, 1995).

Intensity of naticid drilling predation for ecoregions in Brazil is lower (<1%–15%) compared to the range of percentages reported by Kelley & Hansen (2007) for modern provinces along eastern North America (16%–29%). Maximum drilling at a single locality in Brazil was

36% vs. 45% for the Northern Hemisphere; five of the 28 localities studied here had DFs >20% compared to 12 of 24 localities analyzed by Kelley & Hansen (2007). When data are combined for all localities in each dataset, drilling in Brazil is likewise significantly less than in the

Northern Hemisphere (DF = 9.7% for ~24,000 specimens from Brazil vs. 22% for ~9,000 specimens in the Kelley & Hansen database). Naticid drilling in Brazil is also reduced compared to stratigraphic units of the Cenozoic studied by Kelley & Hansen (1993, 2003, 2006); DFs ranged from 0%–41% at the assemblage level and were even greater for individual lower taxa.

For instance, a drilling frequency of 66% was reported for Choptank Formation lucinids (>1000 specimens), and ~2,800 Yorktown Formation lucinid specimens yielded a DF of 47%.

Interestingly, lucinids demonstrated among the greatest lower-taxon DFs reported for Brazil

(e.g., two localities with >400 specimens of Divalinga had DFs of 51% and 60%). Most other taxa had much lower DFs when present in high abundance (e.g., <10% in Tivela at all latitudes).

Simões et al. (2007) similarly noticed reduced drilling in Recent bivalves from the South Brazil

Bight compared to Cenozoic values (citing Kelley & Hansen, 1993). Whether the comparatively low drilling frequencies reported by Simões et al. (2007) and in the present study are decreased

64 compared to the Cenozoic of Brazil is unknown due to the lack of studies of drilling predation on fossils from Brazil.

Future Work

The data presented in this study represent only a portion of the coastline sampled in eastern South America covering tropical and temperate environments. Specimen collection in

2010 included 18 additional localities in Argentina, offering an extension of data for the

Argentinean Province through the Uruguay-Buenos Aires ecoregion (36°S–40°S) and incorporation of polar-influenced ecoregions in the Magellanic Province via the Northern

Patagonian Gulfs (42°S–46°S) and the Patagonian Shelf (48°S–52°S). Such continuous broad coverage has not yet been examined in studies of geographic variation in drilling predation. The present work investigated drilling over a 28 degree change in latitude, and upon inclusion of data from Argentina, a total of 46 degrees in latitude will be analyzed.

Because the coastlines of Brazil and Argentina are characterized by a variety of physiogeographic settings from 6°S–52°S, examining the influence of environmental variation on patterns in drilling will be even more important. Multivariate analyses (e.g., ordination) could be used to explore similarity of samples by faunal composition; distribution of samples in ordination space often reflects environmental variables. Locality differences could be assessed using the sediment samples that were collected as well, offering a more detailed understanding of the types of habitats represented by these assemblages as based on grain size. It is essential that spatial patterns in drilling address environmental variation, so that latitudinal patterns are not confounded by differences in DF resulting from dissimilar habitats that should not be compared.

More studies of drilling predation in different types of environments (e.g., reefs, seagrasses)

65 should be conducted to aid in disentangling their effects when trying to investigate large-scale latitudinal patterns.

This study is the first to focus on drilling predation by Recent naticid gastropods across a broad range of latitudes in the Southern Hemisphere. Understanding of patterns in drilling on fossil assemblages in South America is also needed. In addition, investigating the evolutionary histories of these faunas would inform comparisons of drilling predation in the Northern and

Southern Hemispheres.

Lastly, molluscan faunas of eastern South America analyzed as part of this study have utility also in addressing research questions related to controversial biogeographic boundaries or aspects of biodiversity conservation such as anthropogenic impacts and invasive species.

Because sampling of live marine benthos can be problematic due to the patchy distribution of such communities, shell accumulations that are time-averaged may offer a unique perspective in aiding these efforts, as is the case for archeological deposits of mollusks in Brazil (e.g., Souza et al. 2010).

CONCLUSIONS

Frequency of naticid drilling is greatest among lower latitudes in Brazil, contrary to the peak at mid-latitudes reported by Kelley & Hansen (2007) for Western Atlantic molluscan assemblages of North America. Increased equatorward drilling is documented at the assemblage-level across all spatial scales analyzed and for multiple lower taxa, including size- standardized data. Analyses of a culled dataset from which potential biases resulting from environmental variation and different sampling strategies were eliminated further validate this pattern. Temperature, seasonality, diversity and size distribution of predators and prey may be

66 linked to these differences in drilling across latitudes. This research provides new information from an under-sampled region in which broad-scale spatial patterns in drilling predation were previously unknown. Due to the discrepancy in latitudinal patterns between the Northern and

Southern Hemispheres, further studies that examine geographic patterns in additional areas are warranted. Analysis of replicate bulk samples across multiple spatial scales and at various taxonomic levels is recommended. Employing neontological approaches by using modern faunas for examining the influence of geographic variation on predator-prey interactions in the fossil record offers insight into how latitude and climate may impact evolutionary interpretations of escalation.

ACKNOWLEDGMENTS

Fieldwork was funded by the National Geographic Society (Grant No. 8616-09),

Conchologists of America, Sigma Xi, UNCW Office of International Programs, a UNCW Brauer

Fellowship, and a UNCW Cahill Award. Supplemental funds for the completion of this project were granted by the UNCW Graduate School. Writing of the dissertation was supported by a

Ford Foundation Fellowship and the Chrysalis Scholarship from the Association for Women

Geoscientists. C. Priester, S. Kline, and D. Priester aided in fieldwork; logistical support generously provided by the entire Priester family and friends in Brazil is greatly appreciated.

Thanks also to J. Visaggi, B. Parnell, and B. Ratchford for assistance in processing samples, and

S. Midway for his skills in using R. Finally, I am extremely grateful to P. Kelley for collaborating throughout the duration of this project.

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CHAPTER THREE: EXAMINING THE INFLUENCE OF SEASONALITY ON NATICID DRILLING

PREDATION USING AN EXPERIMENTAL APPROACH IN BOTH A LABORATORY AND FIELD SETTING

ABSTRACT

Intensity of drilling by naticid gastropods may be affected by a multitude of abiotic and biotic factors. Temperature is among the most important controls on rates in drilling, yet the impact of seasonality on naticid feeding behavior is unclear. This study examined seasonal variation in feeding by Neverita duplicata on Mercenaria mercenaria and its relationship to temperature using both a laboratory and field experimental approach. The laboratory setting offered a constrained environment in which seasonal variables other than temperature were diminished.

Twelve replicate tanks, each with a single predator and six prey (replenished every three days as consumed), were monitored under flow-through conditions for 45 days during four seasonal periods in 2010–2011. Feeding varied seasonally, with proportion of consumed prey greatest in the summer (~41%), followed by fall (~30%), spring (~25%), and winter (~11%). Temperatures fluctuated mostly in the ranges of 27–30°C (summer), 21–25°C (spring), 16–20°C (fall), and 8–

12°C (winter); seasonal differences in feeding could not be attributed entirely to direct temperature effects on metabolic rates. Field experiments provided an opportunity to explore natural variation in feeding rates as affected by seasonal variables not present in a laboratory setting. Twenty experimental plots, each containing 20 clams, were placed in areas occupied by moon snails in the field in each season and recovered after four weeks. Dead clams were categorized as drilled, fragmented, or lacking evidence of predation. Five additional plots with

20 clams each were caged, offering insight regarding prey recovery and background mortality.

Seasonal recovery of clams ranged 96–98% in control plots and 80%–98% in experimental plots.

Proportion of drilled clams (out of all recovered) varied seasonally: fall (~25%), winter (~6%), spring (~10%), summer (0%). Temperature could not account for all of the variation observed in drilling with seasons in the field setting; summer data may have been influenced by heat stress of predators and/or prey, but increased incidence of shell-crushing predation was additionally noted. These results suggest that drilling frequencies determined from shell accumulations may vary latitudinally as a result of seasonality, as the presence, duration, and magnitude of seasons change with latitude. Exploring next whether seasonal signals in drilling intensity are preserved in time-averaged shell deposits will be important for applying these results to the fossil record.

Understanding geographic variation in drilling frequency is essential for interpreting evolutionary patterns in predation such as escalation as based on paleontological assemblages.

INTRODUCTION

The fossil record of naticid drilling predation provides much of the evidence for the hypothesis of escalation, in which predation is posited as a driver of evolution. Support for escalation includes survey of the literature, as originally conducted by Vermeij (1987), as well as work by

Kelley & Hansen (1993, 1996, 2003, 2006), on fossil molluscan assemblages collected from the

U.S. Coastal Plain (reviewed in the preceding chapter of this dissertation). Although study of patterns in naticid drilling is usually restricted to deposits from similar paleoenvironmental settings (e.g., shallow shelf marine habitats comparable in salinity, depth, and wave energy), samples often derive from different latitudes as controlled by the availability of fossil outcrops.

The impact of spatial variation on temporal trends in drilling predation is poorly understood.

Latitudinal patterns in naticid drilling may be influenced by a variety of abiotic and biotic factors, several of which may be linked also to differences in seasonality with latitude. The

76 presence, duration, and magnitude of seasons vary geographically, with decreased effects in lower latitudes due to the decline in seasonality upon approaching the equator. Temporal variation in seasonality exists as well. For example, mid-latitudes from a warmer climate interval may exhibit different seasonal signals compared to mid-latitudes from cooler episodes, as demonstrated by the shift in climate from “greenhouse” to “icehouse” conditions across the

Eocene-Oligocene boundary (Ivany et al., 2000). Except for such work conducted using isotopic methods, most studies of marine ecosystems in the fossil record do not consider the potential impacts of seasonality in the interpretation of paleoecological patterns through time or in space.

Temperate marine communities are influenced by seasonal changes in numerous ecological and environmental variables. Seasonal abiotic factors that may affect frequency of naticid drilling include temperature, salinity, tidal currents, and physical disturbances. A multitude of biological factors may also impact these habitats seasonally. Density of predators and prey can vary each season as a result of reproduction, recruitment, migration, and predation

(e.g., Peterson & Peterson, 1979; Bertness, 2007). Seasonal changes can occur in prey availability, predator-prey abundance, predation risk, competitive interactions, and shell growth or repair (e.g., Paine, 1963; Edwards, 1974). Temperature fluctuates with latitude, and although a number of studies have demonstrated increased feeding with rising temperatures (e.g., Sawyer,

1950; Hanks, 1952; Ansell, 1982a,c), other variables related to seasonal or latitudinal differences in the intensity of predation by moon snails are less commonly explored. To assess impact of seasonality on drilling by naticids, I used a neontological approach that incorporated both field and laboratory experiments. Laboratory work provided a controlled setting in which seasonal factors apart from temperature were excluded. Field investigation offered a view of variability in the frequency of naticid predation, as possibly influenced by a combination of biological and

77 physical variables in nature that fluctuate seasonally. The impact of seasonality on drilling is challenging to assess using fossil assemblages; understanding the extent to which seasonality may affect patterns of drilling predation in modern environments has implications for paleontological interpretations.

SETTING

Seasonal effects on feeding by naticid gastropods were examined in southeastern North Carolina.

The UNCW Research Lease, an intertidal mudflat near Masonboro Inlet, NC, provided the setting for field experiments (34°10′46″N, 77°50′30″W), and the location for predators collected for laboratory work (Figure 1a, Figure 2a). Laboratory experiments were conducted at the

Center for Marine Science at the University of North Carolina Wilmington, only ~5 km from the field locality along the Intracoastal Waterway. Use of flow-through seawater in the laboratory and proximity of the field location allowed for both experiments to be subject to similar seasonal conditions. Temperatures in shallow soft-bottom habitats of this area can range well above 30°C in the summer and may extend below 5°C in the winter (NC Oyster Spat Monitoring Program: www.ncoystermonitoring.org).

The same predator and prey species were utilized in field and laboratory experiments.

Neverita duplicata is an abundant moon snail ranging in distribution from Massachusetts to the

Gulf of Mexico. Nearly all field studies of this naticid are restricted to the northern end of its range (e.g., Edwards & Huebner, 1977; Wheeler, 1979; Wiltse, 1980; Fregeau, 1991); however, it is a common infaunal predator of shallow soft-bottom habitats in southeastern North Carolina.

Temperature affects the rate of feeding by N. duplicata; field and laboratory investigations that

Figure 1. a) The UNCW Research Lease exposed during a negative low tide. Note the pitted sediment surface due to disturbance from rays and the location of a (caged) field plot, as marked by red flags in such depressions, in the lower left corner of the image. b) A caged field plot. c) An experimental plot after excavation.

b. c.

Figure 2. a) Location of the field setting (red) at the UNCW Research Lease behind the Intracoastal Waterway near Masonboro Inlet, NC. b) Distribution of experimental (yellow) and control (green) plots at the field location. Only fall plots are displayed; similar spatial coverage was maintained in subsequent seasons.

80 varied in choice, size, and density of prey and predator all reached this conclusion (Sawyer,

1950; Hanks, 1952; Huebner, 1973; Edwards & Huebner, 1977; Huebner & Edwards, 1981).

Lower limits on feeding are documented by Hanks (1952) at 5°C; upper limits to feeding have not been tested.

The hard clam, Mercenaria mercenaria, is commonly drilled by Neverita duplicata in both field (e.g., Edwards, 1974) and laboratory settings (e.g., Kitchell et al., 1981). Early studies of predation by N. duplicata on M. mercenaria focused on the destructive potential of predatory damage to populations of this commercially important bivalve species (Sawyer, 1950).

Subsequent research has utilized this predator-prey relationship for exploring aspects of ecology and evolution (Kitchell et al., 1981; Kardon, 1988).

METHODS: Laboratory

Laboratory experiments were conducted using 12 aquaria provided with 7 cm of fine sand obtained from nearby Wrightsville Beach, NC. Each tank contained a single Neverita duplicata collected at the UNCW Research Lease. The same naticid individuals were used across all four seasons in laboratory work (except for a few deaths requiring the replacement of predator individuals in a single tank). All moon snails were initially sized at 29–30 mm in length

(perpendicular to the axis of coiling). Naticids were fed only a single clam every three days during the six weeks between seasonal experimental periods to minimize growth over the course of experiments.

Mercenaria mercenaria prey were obtained from hard clam suppliers in Virginia, North

Carolina, and Florida. Seasonal variation in availability limited the use of prey from a single location. All prey were examined for quality control before being used in experiments following

81 protocols described in the next chapter of this dissertation, and each clam was marked with date of placement in an experimental tank. Six Mercenaria (~18–22 mm in anteroposterior length) were offered as prey in each set-up at the start of experimental periods. Predator-prey size ratios

(Figure 3) are appropriate based on the work of Kitchell et al. (1981). The six prey maximum was chosen as it provided more prey than could be drilled during a three day period, even at the highest feeding rates. Of the six Mercenaria prey available in each set-up, any consumed clams were replaced with new individuals every three days for a total of 45 days. Thus, prey numbers remained relatively constant, limiting concerns about the influence of density dependence

(although no such bias was noted in field experiments using other moon snail species in Peitso et al., 1994 or Beal, 2006b). Laboratory experiments began in the summer (July–August 2010), and continued through to the fall (October–November 2010), winter (January–February 2011), and spring (April–May 2011). Variation in feeding with seasons was statistically assessed using a chi-square test.

Upon each experimental check, temperature, salinity, and pH were recorded. Before probing the sediment during experimental checks, surface observations were noted, in part to minimize concerns regarding the health of the prey. Alternate modes of predation such as suffocation have been reported in previous laboratory experiments using this combination of predator-prey species; however, review of the subject in the next chapter of this dissertation demonstrates that such accounts are likely the result of using unhealthy prey. Thus, surface observations such as gaping clams or individuals unable to burrow into the sediment were used as an indicator of poor prey health; affected clams were replaced during experimental checks.

Surface examination further offered an opportunity to locate moon snails beneath the sediment due to visible active siphon function, aiding in limiting disturbance to naticids during checks.

Figure 3. Comparison of predator-prey sizes between Neverita duplicata (29–30 mm) and Mercenaria mercenaria (~18–22 mm) utilized in laboratory experiments.

Data Collection: Predators

Observations on naticid behavior were documented during each experimental check (Table 1). If predators were in the process of handling or drilling prey (as confirmed by feel or sight), individuals were not disturbed if possible. However, unavoidable interruptions usually led to abandonment of drilling. Moon snails that abandoned prey or that were without prey during experimental checks were retrieved from tanks and measured to monitor health and growth.

Both length and height (parallel to the axis of coiling) were recorded.

Data Collection: Prey

During each experimental check, all six prey were removed from each aquarium and examined

(with the exception of individuals in the process of being handled or drilled by moon snails).

Because all clams were marked with their date of entry into experiments, health of individual live clams could be monitored during their residency in aquaria before being consumed. Using a fingernail for prying, strength of valve closure was tested in live clams before returning them to experiments; clams exhibiting signs of weakness were replaced by new individuals. Any incomplete drilling attempts were noted. Complete drillholes in empty shells were counted and degree of staining on the shell assessed as described in Chapter Four of this dissertation. New live clams were added to each set-up based on the number consumed.

Natural Mortality and Decay

Because of concerns regarding the health of prey and potential suffocation by naticids (see next chapter), control aquaria with the same sediment depth and flow-through conditions were used to examine background mortality of prey in the absence of predators. Four trials were conducted

Table 1. List of naticid behaviors documented during experimental checks. Movement on the sediment surface, in the corner, or on the walls of aquaria was additionally noted. Interruptions in drilling due to disturbance from experimental checks were recorded as well.

Observed Behaviors Traveling/Stationary, No Prey Traveling/Stationary, Handling Prey Only Stationary & Drilling Consumption Near/Complete Upside Down, Foot Extended, No Prey Snail Closed, But Alive Snail Died

85 during each season, involving six Mercenaria in each of three replicate tanks. Because residency of clams in experiments prior to consumption varied by season, control periods of different durations were utilized to assess mortality concerns as follows: nine days (summer), 12 days

(spring/fall), and 15 days (winter). Tanks were checked every three days, surface observations noted, and health of prey tested as described above for strength of valve closure. Deaths were recorded if present. Temperature, salinity, and pH were documented during each experimental check.

In addition to assessing background levels of bivalve mortality, separate aquaria were used to examine the degree of decay that might occur in prey individuals experiencing natural mortality during the 72 hours in between experimental checks. Each tank contained only a single bivalve, which was wedged open, in most cases by use of a blunt scalpel. Bivalves were either left on top of the sediment surface or buried in the sand to study differences in decomposition that might occur depending on the particular context in which they could be found in the seasonal feeding experiments. All tanks were subject to the same flow-through conditions as previously described.

During each season, eight trials of three replicates each were conducted both for “decay above the surface” (DAS) and “decay below the surface” (DBS). Observations included degree of staining on the shell as described in the next chapter of this dissertation, odor if any, as well as color, consistency, and amount of soft parts remaining. Any detritivorous fauna found in association with deteriorating Mercenaria were noted upon retrieving bivalves from aquaria

(e.g., amphipods). Photographs additionally were used to record differences in decomposition between individuals in DAS vs. DBS set-ups. Temperature, salinity, and pH were documented both at the start and end of each three day trial.

METHODS: Field

Field experiments were conducted at the UNCW Research Lease near the Intracoastal Waterway

(Figure 2a), only ~5 km from the location of laboratory experiments. Twenty clams were planted in each of 25 plots (0.5 m2), distributed among three different areas of the mudflat separated by channels (Figure 2b). Selected locations were in proximity to areas inhabited by moon snails and were consistent among seasons. All field plots were placed within existing pits made by rays (Figure 1a), as moon snails are found in higher concentrations within these depressions on the mudflat (Dietl, unpublished). Five of these plots served as controls and thus were caged to examine recovery and background mortality of prey as this may differ by season.

Cages were constructed of wire mesh (~1.25 cm) and extended down into the sediment ~15 cm on all sides (Figure 1b). All plots were marked by four red survey flags placed in quadrat corners, with GPS coordinates additionally recorded.

Mercenaria mercenaria (~16–18 mm in anteroposterior length) were marked (using a permanent marker), planted (1–3 cm beneath the sediment surface and evenly distributed across the quadrat), and recovered after 4 weeks. Bivalves utilized as prey in the field were obtained through the same North Carolina and Florida hard clam suppliers as in laboratory experiments; however, smaller individuals were used to enhance the likelihood of drilling predation, as most naticids at this locality are smaller than the predators collected for laboratory work. Tidal cycles limited periods in which experiments could be executed, as negative low tides were required for fieldwork. Thus, seasonal experiments began in 2010 from November 5th – December 5th (fall), and were followed by January 20th – February 19th (winter), April 17th – May 18th (spring), and

July 30th – August 29th (summer) in 2011. Temperatures for the field setting were determined

87 using data collected for Site #13 of the NC Oyster Spat Monitoring Program (along the ICW outside of the UNCW Center for Marine Science at ~5 km from the UNCW Research Lease).

Recovery of Specimens

Several methods were used in the recovery process at each of the plots. Most specimens were retrieved first in digging by hand several centimeters into the sediment. Trowels, shovels, and sieves were utilized to find any remaining specimens at greater depths. Plots were excavated down to at least 25 cm (beyond the maximum foraging depth of 16 cm for Neverita duplicata;

Fregeau, 1991), and the perimeter of plots widened by a minimum of 15 cm on all sides to aid in finding any specimens that may have migrated outside of the marked quadrats (Figure 1c).

Information recorded during recovery included presence and size of moon snails and other predators (e.g., crabs) in and around plot areas, and any pertinent observations such as on the surface of plots (e.g., gaping marked clams, abundant Ilyanassa) or within the excavated sediment (e.g., heavy bioturbation, substantial shell hash). In most cases, recovery of all plots required two consecutive days of fieldwork as limited by the tides.

Data Analysis

Specimens recovered from the field were processed in the laboratory to determine the proportion of live and dead Mercenaria. Shells of dead clams were categorized by apparent mode of death based on shell damage as drilled, fragmented (presumably by durophagous predation), or undamaged (lacking any evidence of predation), similar to Beal et al. (2001) and Beal (2006a,b).

Variation in drilling across seasons was based on the total number of specimens recovered (not planted) and statistically assessed using a chi-square test. Total number drilled divided by

88 number recovered (all seasons combined) was used to obtain an expected proportion for intensity of drilling (if uniform across seasons). In addition, proportion of drilled valves was recalculated using whole shells only, as is customary for determining frequencies of drilling from modern and fossil shell assemblages.

RESULTS: Lab

Neverita duplicata individuals consumed a total of 1155 Mercenaria mercenaria during experimental periods (Table 2). The number of prey consumed was greatest in the summer

(446), followed by fall (320), spring (266), and winter (123). The proportion of clams offered that were drilled (Table 3) was not uniform across seasons based on a chi-square analysis

(p<0.0001): summer (~41%), fall (~30%), winter (~11%), and spring (~25%). The mean number of clams consumed per snail over the 45 days ranged from ~10 in the winter to ~37 in the summer (Table 2; Figure 4).

The same individuals were used for all four seasons, with the exception of one set-up

(Tank II). Naticid deaths in this set-up required replacement of predators during the summer and fall trials. All moon snails fed during each experimental period except for one individual that did not feed during the spring in Tank XI (although feeding resumed in the subsequent summer months). Snail growth (in length) over the course of experiments ranged between 2.39 mm and

8.98 mm for the 11 naticids used during all four seasons (Table 4), with a mean of 5.81 mm.

Growth rates were greatest in the summer or spring in most cases, and lowest during the winter without exception. Naticids were most commonly engaged in drilling or handling clams during experimental checks; very rarely were they inactive with the operculum closed. Only fragments

Table 2. Total clams consumed in each laboratory set-up (Tanks I–XII) across seasons. Averages (=Avg) are provided for seasons and number of clams consumed per day seasonally.

Season/Tank I II III IV V VI VII VIII IX X XI XII Total Avg Avg/Day Summer 46 16 36 43 39 43 40 42 37 37 27 40 446 37.17 0.83 Fall 32 16 31 27 29 34 26 26 24 19 25 31 320 26.67 0.59 Winter 16 8 12 7 12 13 6 12 7 8 9 13 123 10.25 0.23 Spring 33 4 30 9 30 36 26 26 20 20 0 32 266 22.17 0.49 Total Drilled 127 44 109 86 110 126 98 106 88 84 61 116 1155 NA NA

Table 3. The proportion of clams consumed out of all offered seasonally for Tanks I–XII. Seasonal averages are additionally listed (=Avg).

Season/Tank I II III IV V VI VII VIII IX X XI XII Avg Summer 0.51 0.18 0.40 0.48 0.43 0.48 0.44 0.47 0.41 0.41 0.30 0.44 0.41 Fall 0.36 0.18 0.34 0.30 0.32 0.38 0.29 0.29 0.27 0.21 0.28 0.34 0.30 Winter 0.18 0.09 0.13 0.08 0.13 0.14 0.07 0.13 0.08 0.09 0.10 0.14 0.11 Spring 0.37 0.04 0.33 0.10 0.33 0.40 0.29 0.29 0.22 0.22 0.00 0.36 0.25

Figure 4. Mean number of clams consumed per set-up by season in laboratory experiments. Error bars reflect standard deviation.

40 30 20

Consumed Per Tank Consumed Per

Mean Number Mean of Clams 0 Summer Fall Winter Spring

Table 4. Size of moon snails (mm) in each laboratory set-up at the start (July 2010) and end (May 2011) of experiments, with growth recorded by season. Data in Tank II reflect a replacement individual utilized from late October onward; starting length was larger, more similar to the range of sizes exhibited by the other 11 naticids by that time after fall season experiments had commenced.

Season/Tank I II III IV V VI VII VIII IX X XI XII START 29.91 (33.82) 29.46 29.04 29.47 29.82 29.17 29.16 29.22 29.21 29.51 29.44 Summer 3.06 --- 2.67 1.37 3.16 2.41 0.95 2.59 0.88 2.1 0.79 1.93 Fall 1.38 0.47 0.66 1.33 0.93 0.47 0.59 0.51 0.5 0.27 0.47 1.19 Winter 0.35 0.06 0.17 0.42 0.22 0 0.51 0.25 0.48 0.08 0.14 0.69 Spring 2.91 0 1.83 1.2 2 2.58 1.83 2.53 1.37 1.65 0.12 1.86 END 38.89 34.45 35.62 33.83 37.31 36.74 34.23 35.59 33.09 33.75 31.9 36.34 NET Growth 8.98 0.53 6.16 4.79 7.84 6.92 5.06 6.43 3.87 4.54 2.39 6.9 Total Drilled 127 28 109 86 110 126 98 106 88 84 61 116

93 of one egg collar were observed during the course of laboratory experiments in the winter in

Tank VI.

Temperatures in the flow-through system fluctuated primarily between 27–30°C

(summer), 16–20°C (fall), 8–12°C (winter), and 21–25°C (spring). Salinity ranged mostly between 26 and 34 ppt, with no consistent differences among seasons; pH varied between 7.74 and 9.15.

Natural Mortality and Decay

Natural mortality was very low, as indicated by prey health assessed during each experimental period using Mercenaria mercenaria in control aquaria. Of the 288 clams used across all seasons, only a single death occurred, during the fall season.

Decomposition rates varied substantially among seasons, based on decay experiments conducted during each experimental period both above the sand (DAS) and beneath the sediment surface (DBS). Nearly all DAS and DBS clams completely decayed within three days during the summer months; however, small clumps of dark organic matter sometimes lingered on the interior of shells exposed to both sets of conditions. Slight unpleasant odor and light staining of shells occurred in DAS aquaria; a much more pungent smell and darker discoloration reflected clams in DBS set-ups. None of the DAS clams decayed completely during the fall season, but several exposed to DBS conditions did. Differences in odor and discoloration between DAS and

DBS experiments in the fall were similar to observations from the summer. Soft parts remained in all clams during the winter months regardless of location relative to the substrate, but DBS clams exhibited more signs of decay, odor, and discoloration. Staining and odor were very infrequently documented for DAS aquaria. Spring months revealed a mix of either complete

94 decomposition or remaining soft parts in valves for both DAS and DBS set-ups. Darker discoloration of shells and stronger odors were noted for DBS conditions. Presence of worms and amphipods was more commonly observed during the spring season relative to any other experimental periods.

RESULTS: Field

Results of field experiments are summarized in Table 5. Of the 1600 clams planted in experimental plots, shell remains of 1382 were recovered (~80% summer, ~80% fall, ~98% winter, ~89% spring). Total recovery of the 400 clams in control plots did not vary by season, ranging only between 96–98%. Number of live vs. dead specimens recovered varied seasonally; deaths were greatest in the summer and lowest in the winter for both experimental and control plots (Figure 5). Chi-square analysis confirmed that the proportion drilled (out of all recovered from experimental plots) was not uniform across seasons (p<0.0001): summer (0%), fall (~25%), winter (~6%), spring (~10%). Data restricted to whole shells (which are used to calculate drilling frequencies in modern and paleontological molluscan assemblages) revealed similar seasonal patterns in drilling (Figure 6).

Dead clams were documented as drilled, fragmented, or exhibiting no fragmentation or evidence of drilling. The proportion of mortality attributed to different causes varied by season

(Figure 7a). An inverse correlation existed between clams that were found fragmented vs. drilled

(Figure 7b). Observations upon planting and recovery revealed that moon snails inhabited the area of the field plots during all seasons, but were most commonly documented during the fall.

Temperature ranges in the field mostly fluctuated between 28–31°C (summer), 16–19°C (fall),

9–12°C (winter) and 22–26°C (spring).

Table 5. Summary of field results collected seasonally from both experimental and caged plots. Abbreviations: DH (drillhole), Frag (fragmented), no DH/Frag (no predatory damage).

Experimental # Found # Live # Dead # w/ DH # Frag # No DH/Frag Fall 317.5 195 122.5 80.5 8 30 Winter 390.25 349 41.25 24 0.25 17 Spring 356 255 101 34 20.5 46.5 Summer 317.5 3 314.5 0 180.5 132.5

Caged # Found # Live # Dead # w/ DH # Frag # No DH/Frag Fall 96 89 7 4 0 3 Winter 96 94 2 0 0 2 Spring 97.5 88 9.5 0 5.5 4 Summer 98 29 69 0 2 67

Figure 5. Proportion of dead clams found each season out of all recovered in the field for experimental vs. caged plots.

100% Experimental Control 80%

60%

40%

20% % Mortality of Recovered Mortality Clams % 0% Summer Fall Winter Spring

Figure 6. a) Percentage of drilled clams documented out of all recovered for each season in the experimental field plots. b) The same dataset restricted to whole shells only (fragmented specimens excluded).

30%

25%

20%

15%

10%

5% % Drilled of % All Recovered

0% Summer Fall Winter Spring

50%

40%

30%

20%

10% % Drilled of All All of Drilled Recovered % 0% Summer Fall Winter Spring

Figure 7. a) Causes of mortality of recovered dead clams inferred as either drilling, durophagous predation (fragmentation), or natural mortality (not drilled or fragmented = “No DH/Frg”). b) Inverse relationship between percentage of dead clams recovered as fragmented vs. drilled based on field data from all four seasons.

a. 80% Drilled 70% Fragmented No DH/Frg 60%

50% 40%

Recovered 30% 20%

% Type of Mortality of Clams of Mortality Type % 10% 0% Summer Fall Winter Spring

60%

50%

40%

30%

20% % Fragmented % 10%

0% 0% 20% 40% 60% 80% % Drilled

DISCUSSION

Laboratory experiments indicated that drilling by Neverita duplicata was greatest in the summer and lowest in the winter. More clams were consumed during the fall relative to the spring, despite higher water temperatures in the spring. Similar patterns in drilling were documented in field experiments for the fall, winter, and spring; however, drilling was not recorded during the summer (Figure 8). These results demonstrate that, although temperature influences patterns in feeding, seasonal variation in drilling intensity is not solely due to direct temperature effects on metabolic rates (Figure 9).

A number of studies have documented a positive correlation between temperature and rates of feeding by Neverita duplicata (Table 6) and other naticid species (Table 7). Sawyer

(1950) demonstrated that feeding decreased as temperature was lowered from 21°C to 10°C in an artificially controlled laboratory setting for N. duplicata. Hanks (1952) expanded on this work and noted that feeding ceased at 5°C. Temperature effects on feeding for the other dominant moon snail of the U.S. East Coast, Lunatia heros, were reported also based on controlled laboratory conditions over 2°C–21°C (Hanks, 1952) and for 7°C–18°C (Weissberger, 1999).

Ansell (1982a) found similar results in a controlled laboratory setting for Euspira pulchella

(5°C–20°C), a European naticid. In all of these experiments, seawater temperatures were manipulated so that, even for work conducted over multiple seasons (e.g., Ansell, 1982a), effects of natural seasonal variation on feeding other than those related to the influence of temperature on metabolic rates were not examined.

Flow-through experiments conducted in a laboratory setting by Kingsley-Smith et al.

(2003a) on Euspira pulchella across multiple seasons in Wales revealed that the greatest feeding in all size classes occurred in summer and fall, with lower rates in spring and winter. Variation

100

Table 6. Temperature and/or seasonal data on feeding by Neverita duplicata as reported from several examples in the literature. Standard postal abbreviations for states (USA) and provinces (Canada) are used. Sizes reflect shell lengths unless denoted by an (A) for aperture width. Abbreviations as follows for data not provided (NP) or not applicable (NA) based on the experimental setting.

Experiment Temperatures & Naticid Size Prey & Size Time of Year Location Reference Type (Clams Eaten Per Day) Mercenaria Field - Caged 24–57 mm mercenaria NP (0.02) July–August NJ, USA Carriker (1951) ~25–60 mm Mya arenaria All Year & Edwards & Field - Caged ~25–39 mm ~23.3°C (~0.60) MA, USA ~20–50 mm Summer* Huebner (1977) Mya arenaria All Year & Field - Caged 16–48 mm 11.8–23.3°C (~0.53) MA, USA Fregeau (1991) 10–60 mm Summer* Lab - NA: Aronowsky (Various) (Mixed) 19–24°C (~0.25–0.44) CA, USA Controlled June–October (2003) Lab - Mya arenaria Boggs et al. 42.7–54.2 mm 19–22°C (~0.33) NP WI, USA Controlled ~55 mm (1984) Lab - Donax ~15–28 mm (A) 23–27°C (~0.81) NP TX, USA Davies (1977) Controlled variablis 21°C (0.63) 16°C (0.3) 14°C (0.18) Lab - Mya arenaria NA: (Various) 12°C (0.21) MA, USA Hanks (1952) Controlled ~15–30 mm Fall & Winter 10°C (0.2) 7°C (0.11) 5°C (0) Lab - Mya arenaria ~21°C (0.67) 9–12 mm (A) NA: Winter MA, USA Sawyer (1950) Controlled <25 mm 10°C (0.13)

*Only data collected during "summer" experiments are presented for Fregeau (1991) covering mid-May through mid-October and Edwards & Huebner (1977) incorporating mid-June through mid-August.

101

Table 7. Temperature and/or seasonal data on feeding by other species of moon snails as compiled from examples in the literature. Taxonomy of naticids is updated per Torigoe & Inaba (2011). Standard postal abbreviations for states (USA) and provinces (Canada) are used. Sizes reflect shell lengths unless denoted by a (H) for shell height. Abbreviations as follows for data not provided (NP) or not applicable (NA) based on the experimental setting.

Experiment Naticid Species Temperatures & Prey & Size Time of Year Location Reference Type & Size (Clams Eaten Per Day) Venerupis philippinarum Cook & Lunatia lewisii Protothaca staminea BC, Field - Caged NP (0.09) May–September Bendell- 72.4–95 mm Nuttalia obscurata Canada Young (2010) >38 mm

Lunatia lewisii Protothaca staminea 18°C (0.06) BC, Peitso et al. Field - Caged Summer & Winter 89.3–95 mm 10–65 mm 6°C (0.014) Canada (1994)

Kingsley- Lab - Euspira pulchella Cerastoderma edule February– 4–18°C (0.12–0.50) Wales Smith et al. Flow Through 4–15.9 mm 2–16 mm (H) November (2003a)

Lab - Lunatia heros Aronowsky (Mixed) 19–24°C (0.13) NA: June–October CA, USA Controlled (Various) (2003)

21°C (0.63) 16°C (0.29) 12°C (0.26) Lab - Lunatia heros Mya arenaria 10°C (0.24) NA: Fall & Winter MA, USA Hanks (1952) Controlled (Various) 15–30 mm 7°C (0.10) 5°C (0.06) 2°C (0.05)

102

Figure 8. Proportion of drilled clams across seasons based on all offered in laboratory experiments (a) and all recovered in field experiments (b).

a. 50%

40%

30%

20%

% Drilled of % Offered 10%

0% Summer Fall Winter Spring

b. 50%

40%

30%

20%

10% % Drilled of % Recovered

0% Summer Fall Winter Spring

103

Figure 9. Temperature ranges most commonly recorded during each season for both field and laboratory experiments, with the percentage of drilled clams documented for all scenarios. The unshaded purple box represents the absence of drillholes in the field for the summer months.

50% Lab Field Summer 40%

Fall 30% Spring

% Drilled % 20% Winter 10%

0% 1 3 5 7 9 11 13 15 17 19 21 23 25 27 29 31 Temperature °C

104 in consumption was closely correlated with seasonal changes in seawater temperature ranging from 4°C–18°C. Lunatia lewisii, of the Pacific Northwest, drilled more clams during the summer (maximum: 18°C) compared to the winter (minimum: 6°C) in caged field experiments by Peitso et al. (1994). Variation in feeding with seasons was documented by Medcof & Thurber

(1958) also for Lunatia heros based on work in experimental field plots in Canada. Employment of Neverita duplicata in field cages in Massachusetts by Edwards & Huebner (1977) and Fregeau

(1991) similarly revealed that the number of clams consumed across seasons fluctuated, but in direct relationship to temperature (Edwards & Huebner, 1977). This interpretation is at variance with my data in which an unequivocal relationship between feeding rates and seasonal changes in seawater temperatures was not documented in either experimental approach. Before exploring ecological and environmental causes for my results, biases in the data that may be influencing these patterns are examined for both laboratory and field experiments.

Potential Biases

Laboratory Experiments

Utilizing the same naticid individuals (in 11 of the 12 aquaria) across all seasons offers an opportunity to monitor individual variability in feeding behavior throughout the year (Figure 10).

However, because the same moon snails remained in laboratory experiments for all four seasons, concerns may be that the predators became unhealthy or otherwise impacted by being in a laboratory setting for an extended period and/or that growth of individuals over the year biased feeding rates in later seasons (as prey size was held constant). To address these issues, I examined feeding behavior for an additional summer in 2011 after the conclusion of the four seasonal experimental periods.

105

Figure 10. Total number of clams consumed across seasons for each of the 12 replicate tanks. Note that data in Tank II are based on multiple naticids due to deaths and predator replacements in summer and early fall; data for fall, winter, and spring are all from the same individual (which was entered into experiments with 2/3 of the fall season remaining).

Summer

Fall 50 Winter Spring 40

Total Number of Clams Consumed Total 0 I II III IV V VI VII VIII IX X XI XII

106

The same snails were monitored for an additional 18 days from mid-July through early

August 2011 (as in the prior experimental summer), and data on drilling were documented as during the preceding seasons. This shortened interval is appropriate for an understanding of summer season feeding; Edwards & Huebner (1977) noted that rates did not differ in summer experiments of differing duration (14 days vs. 42 days). Mean number of clams consumed per naticid during this shorter observational period was similar between 2010 and 2011 at 14.5 vs. 12 clams, respectively (Figure 11). Total consumption for the 18 days varied from 174 clams in

2010 vs. 144 clams in 2011. Because fewer clams were drilled in summer 2011, concerns regarding increases in consumption due to larger predator sizes are assuaged. Furthermore, feeding rates of many organisms often level off as they approach the maximum size attainable within a population. The maximum size of Neverita duplicata is listed as 82 mm in the online database for Western Atlantic Mollusca (Malacolog: Rosenberg, 2009); more commonly reported maximum sizes are 50–60 mm based on populations in Massachusetts (Fregeau, 1991).

Live moon snails larger than 44 mm were not found at the UNCW Research Lease over the course of seasonal field investigation; most individuals at this locality are less than 25 mm.

These sizes are similar to the ranges (4–40 mm) reported by Wiltse (1980) for Neverita duplicata at Barnstable Harbor, MA. Huebner & Edwards (1981) demonstrated that gross growth efficiencies of N. duplicata varied inversely with size; work on other naticid species similarly revealed that gross growth efficiencies declined with age (Broom, 1982; Ansell, 1982b;

Kingsley-Smith et al., 2003a). Discovery of a ~40 mm moon snail in the field during the middle of the fall season provided an opportunity to examine feeding rates for a larger-sized naticid across seasons in the laboratory, in conjunction with the 12 replicate tanks. This individual only grew ~1 mm over eight months, and fed at rates similar to those of the other naticids utilized in

107

Figure 11. Number of clams consumed in each set-up over 18 days (July 17th–August 4th) in the summers of 2010 and 2011. Data labels list naticid lengths (in millimeters) at the start of each period examined. Only data in Tank II are based on different individuals between summers; all other aquaria contained the same naticids in summers 2010 and 2011.

2010 20 2011

29.9 29.0 18 29.5 29.5 29.8 29.2 36.0 37.6 29.2 16 37.5 34.3 33.4 29.2 29.4 36.6 29.2 14 39.3 35.9 12

10 34.5 8 33.8 29.5 31.9 6 33.9

4 30.3

2 Number of of NumberClams Consumed 0 I II III IV V VI VII VIII IX X XI XII

108 experiments. The mean numbers of clams consumed per day across seasons for the ~40 mm individual vs. data from the 12 replicate tanks (Table 2) are as follows: fall (0.63 vs. 0.59), winter (0.33 vs. 0.23), spring (0.69 vs. 0.49), and summer (0.78 vs. 0.83). These averages are within the range of seasonal variability recorded.

Although concerns regarding increased size of moon snails are alleviated, predator health may be factor for consideration, as demonstrated by the decrease in overall consumption of clams (and despite naticid growth). Three individuals in particular (Tanks II, IV, and XI) exhibited stressed behavior (inactive with a closed operculum) and reduced feeding relative to the other naticids in the spring season. Tank II yielded lower levels of feeding during all seasons

(in part due to replacement of predator individuals); comparison of data between summers is not appropriate as different naticid individuals were used. However, reduced feeding by the moon snail in Tank IV during spring and summer 2011 suggests that this individual was weak and behaving abnormally. The naticid in Tank XI did not feed during the spring, but resumed feeding during the summer (and at low rates similar to those observed for summer 2010). This moon snail fed at lower levels year round and showed minimal growth, but the lack of feeding in spring probably reflects stressed conditions. Three other naticids demonstrated a decline in consumption between summers (Tanks I, VIII, X); however, feeding during the experimental spring period did not deviate from that observed for most other moon snails. These individuals did not appear to be altered by long-term laboratory effects until the second summer, perhaps related to the seasonal return of elevated water temperatures. The remaining six naticids fed at almost exactly the same frequency in summer 2011 vs. 2010, with only a difference of one or two clams consumed (Figure 11). In summary, data obtained from nine of the 11 naticids utilized in laboratory experiments throughout the year should reflect healthy individuals during

109 all four seasons examined. Levels of predation are remarkably consistent each season across the

12 replicates, with a few exceptions. The high number of replicates should ameliorate effects of diminished feeding by a few ailing individuals during the spring. The magnitude of seasonal differences in drilling suggests that patterns should be robust, although greater variation in data derived from the spring season as a result of issues in predator health is noted (Figures 4 and 10).

Differences related to sex additionally might affect seasonal variation in drilling, if moon snails adjust their feeding habits in preparation for or during spawning (e.g., Ansell, 1982a).

Edwards & Huebner (1977) noted that sex did not appear to have an obvious effect on growth rates in their experiments. For individuals monitored in field cages year round, growth of older

Neverita duplicata females perhaps slowed during the spawning season; however, in a separate experiment over the summer season only, females grew slightly faster than males. Spawning normally occurs between June–August for Neverita populations in Massachusetts (Edwards &

Huebner, 1977; Fregeau, 1991), but timing of spawning likely is not consistent throughout the entire range of N. duplicata. The mean temperature of ~23°C in summer experiments by

Edwards & Huebner (1977) is more typical of spring values in North Carolina. The only fragments of a single sand collar found in my laboratory experiments were produced early in the winter period; however, sluggish activity and reduced numbers noted in the field suggest that winter is not the spawning season in North Carolina. Formation of egg collars can occur year round in a laboratory setting; reproduction during warmer temperatures characteristic of late spring through early fall is more common as based on other naticid species (Kinsley-Smith et al.,

2003b), although Ansell (1982a) noted that no egg collars were produced by the European naticid Euspira pulchella at 25°C. Because it is difficult to sex live naticids without injuring them, sex of individuals in my experiment is unknown. Growth rates for the 11 moon snails

110

Figure 12. Tanks I–XII plotted by the number of clams consumed and the final length of naticids for each season. Data in Tank II are based on different individuals for summer vs. all following seasons as explained in Figures 10 and 11.

Summer

50 VIII I Fall IV VI Winter 40 VII XII V IX X III VI Spring VI I I XII 30 III III V XI IV XII V VII VII VIII XI VIII IX 20 X IX X II II I VI XII V 10 XI X VIII III IX IV II IV VII II Number of of NumberClams Consumed 0 XI 29 31 33 35 37 39 Length (mm)

111 monitored for all four seasons were highest in either summer or spring (Table 4), with the exception of two individuals marked as stressed during the spring season (Tanks IV and XI).

The lowest growth rates were consistently recorded in the winter. Individuals grew at different rates, which could be related to sex; growth appears to be linked to overall consumption of clams

(Table 4). However, sex was not reported as a major influence on feeding rates of N. duplicata in experiments by Edwards & Huebner (1977). Lack of egg collar production and consistency in levels of feeding among individuals within each season should ease concerns regarding any potential influence due to differences in sex (Figures 10 and 12). Variation between seasons for a single individual was greater than that among individuals within a single season in most cases.

Field Experiments

Data on drilling in the field rely on the recovery of planted clams. Poor recovery or vastly different levels of recovery across seasons could affect interpretations of seasonal intensity in drilling. This issue was partly examined through the use of control plots, which offered a view of recovery and natural mortality of clams in the field (discussed further below). Control plots yielded high levels of recovery each season (>96%). Recovery in experimental plots varied seasonally (Table 5), but seasonal minimum levels were still quite good at 80%. Experimental field studies of predation by the moon snail Lunatia heros in Maine yielded much lower levels of recovery (47%) in using the prey Mya arenaria (Beal, 2006b). Because Neverita duplicata typically burrows down into the sediment immediately upon prey capture, and does not engage in prey carrying as reported in other moon snails (discussed in the next dissertation chapter), it is unlikely that missing clams were transported out of the plot by naticids prior to being drilled.

Burying with prey and leaving the empty shell behind at greater depths than the clam inhabited

112 in life position further ensures that drilled shells are likely to be found within experimental plots and not carried away with the current. Missing shells in other experimental field studies are usually attributed to durophagous predation (e.g., Beal 2006a,b). Protective barriers used by

Beal (2006b) allowed examination of the fate of missing clams; live clams were rarely found outside plot areas, whereas abundant fragments from dead individuals were documented.

One particular event that could have been very destructive to field experiments and the recovery of clams was landfall of Hurricane Irene in North Carolina over August 26th and 27th in

2011. Field experiments were planted on July 30th, with the intention to excavate all plots four weeks later as in previous seasons. However, due to concerns regarding the hurricane and potential loss of all summer data, exhumation of plots was implemented several days in advance as permitted by low tides on August 25th and 26th. Only half of all plots could be excavated prior to the hurricane making landfall; remaining plots were unearthed shortly after the hurricane had passed (August 28th and 29th). Fortunately, recovery of clams in experimental plots was very similar pre- and post-hurricane (157 vs. 161). Only three live clams were documented before the storm and no live clams were recovered afterward. Due to the paucity of live clams remaining at the end of summer field experiments, early excavation of plots should not have limited data on drilling, and deaths due to environmental changes brought by the hurricane were probably minimal. The storm did not appear to impact field experiments; nearly all flags were intact afterward, and cages for unexcavated control plots were still in situ. Because field experiments were not affected by the most powerful disturbance of the year, field results overall were not likely to have been biased by physical disturbances.

The final concern regarding field data is the health of prey in experimental plots. Empty clams found without drillholes or fragmentation may reflect deaths due to natural mortality.

113

Shells lacking evidence of predation in experimental plots represented only 4–13% of all recovered, except for the summer season (42%). Less than 5% of clams were found dead due to presumed natural mortality in control plots during the fall, winter, and spring; however, summer yielded much higher non-predatory deaths (68%). The high mortality recorded for both experimental and control plots suggests that either clams were stressed before being placed in the field and/or became so after planting during the study period, both of which probably contributed to these summer deaths. All clams were checked for signs of gaping and strength of valve closure using the fingernail method before use in field experiments; numbers of unhealthy (and consequently discarded) prey were greater preceding summer fieldwork compared to the other seasons. Mercenaria used in the summer were all obtained prior to spring experiments; heat stress in flow-through storage conditions likely influenced the health of clams upon the rise in water temperatures during the summer. Even if clams had been stored in cooler waters, increased mortality would have been likely upon exposing clams to the warmer conditions of the summer season in the field. Even though all Mercenaria were inspected before being utilized in experiments, elevated temperatures under field conditions during the summer would have similarly led to high natural mortality, particular in standing pools of water within ray pits that can heat up to extremes of 35°C (Posey, pers. comm.). Edwards & Huebner (1977) documented the most non-predatory deaths of Mya over the late summer in their experiments in

Massachusetts (up to 37% of all recovered), consistent also with earlier observations by Turner

(1950). They further commented that comparable non-predatory losses were noted for adjacent localities. Beal et al. (2001) reported the highest mortality of Mya in Maine during August and

September, additionally coinciding with the greatest proportion of chipped and crushed shells

114 recorded. These results are equivalent to data obtained during the summer season of my field experiments.

Seasonal Variation

Several previous studies have reported that Neverita duplicata feeding varies directly with changes in temperature (Sawyer, 1950; Hanks, 1952; Huebner & Edwards, 1977). My results uphold this perception in the sense that greater drilling generally was observed under warmer conditions and decreased upon exposure to cooler waters. However, other factors appear to be contributing to seasonal variation in drilling, yielding patterns that diverge from what is predicted based solely on the direct influence of temperature on metabolic rates. Deviations from this expected relationship include higher feeding in fall despite lower temperatures when compared with the spring as well as the lack of drilling in summer field experiments in contrast to data derived in the laboratory setting.

Fall vs. Spring

In both field and laboratory experiments, drilling was greater in the fall compared to the spring.

Temperatures were higher during the spring than fall, and yet drilling was decreased contrary to expectations that fluctuations in feeding solely reflect shifts in temperature. Less drilling by a few stressed individuals in the laboratory setting does partly account for reduced feeding in the spring compared to fall. If data from individuals in Tanks IV and XI are excluded (as well as data from Tank II in which multiple moon snails were used), number of drilled clams between fall and spring are nearly equivalent (252 vs. 253). However, temperatures were higher in the spring, so even with removal of data from these problematic tanks, drilling was still lower than

115 what it should be if varying directly with temperature. Depressed drilling could have resulted in part from “laboratory effects” as discussed above, although at least half of all moon snails fed at similar rates in summer 2010 vs. 2011, perhaps mitigating this concern. Although naticids were slightly larger in spring, observations on an additional larger moon snail (~40 mm) revealed similar feeding rates for fall, winter, spring, and summer compared to the 12 replicate tanks (and the individual only grew ~1 mm overall). Because spring represents a return to warmer temperatures after sluggish activity during the winter, reduced feeding in the laboratory setting may be related to a lowered metabolic state from the preceding season.

Temperature and feeding offsets between fall and spring were not limited to laboratory conditions. The magnitude of differences between drilling documented for the fall and spring in field experiments was much greater than that observed in the laboratory setting (Figures 8 and 9).

The isolated laboratory environment limited other seasonal influences that may be present in the field, such as differences in drilling due to density of moon snails. Russell Hunter & Grant

(1966) discussed the difficulties of determining densities for Neverita duplicata in part due to the infaunal life habit of these moon snails. Density estimates have ranged mostly from 0.45–0.7 individuals per square meter based on populations in Massachusetts (Hanks, 1952; Russell

Hunter & Grant, 1966; Edwards & Huebner, 1977; Wiltse, 1980; Huebner & Edwards, 1981).

No data are available on densities in North Carolina, although differences in abundance were noted seasonally during fieldwork. The most moon snails were observed in the fall, with the fewest over the winter, and intermediate and similar concentrations found during spring and summer. Higher levels of drilling in field experiments for the fall may reflect increased numbers of Neverita duplicata. Drilling frequencies that mirrored changes in temperature as reported in field experiments by Edwards & Huebner (1977) were limited to predators in cages buried with

116 prey fed ad libitum. Because their field experimental setting was controlled, other seasonal factors were less likely to influence their results, yielding data more similar to those derived from a laboratory setting.

Field vs. Lab: Summer

Summer represented the only season in which the data on the intensity of drilling did not correspond between laboratory and field experiments. As predicted by the expected influence of temperature on feeding rates, drilling was greatest in laboratory experiments when waters were warmest during the summer. However, no drillholes were documented in field experiments during this season (although a few moon snails were observed while excavating plots). Several factors may be contributing to this lack of drilling recorded from the natural setting of Neverita duplicata for the summer season.

The first concern is related to prey health and heat stress as discussed earlier. High background mortality of Mercenaria may have limited the availability of live individuals for attack by Neverita duplicata, which does not consume carrion (as reviewed in the subsequent dissertation chapter). Although this naticid species is preferentially attracted to injured live prey

(Edwards & Huebner, 1977), it is not clear if weak and gaping prey would attract or repel N. duplicata. Durophagous predators and scavengers such as crabs, however, would likely be drawn to stressed and/or dying prey individuals. Shallow soft-bottom habitats support large predator populations (Bertness, 2007); many of the shell-crushing predators were noted in higher abundances during the summer, consistent with observations by Paine (1963) on the prevalence of blue crabs during warmer months in a similar shallow marine setting in Alligator Harbor, FL.

Increased fragmentation of clams further supports the activity of these predators in my

117 experimental plots. Crabs and other shell-crushers could have accessed prey before moon snails had the chance and/or risk due to the presence of these enemies to naticids may have influenced the behavior of Neverita duplicata (Sih et al., 1998). Crabs are reported as having a greater impact relative to moon snails on smaller Mercenaria (Carriker, 1951; Bricelj, 1993), similar to specimen sizes used in this study. Interestingly, an inverse relationship between the proportion of clams found drilled vs. fragmented was documented across seasons (Figure 7b).

Lack of drilling in experimental plots may be a result also of naticids feeding on other available prey in the field, particularly if clams died or were consumed by other predators first.

Neverita duplicata is known to switch prey depending on seasonal availability in the northern end of its range (Edwards, 1974). It is a generalist predator, and at Barnstable Harbor, MA, preyed on a minimum of 13 different mollusks that were regularly available (although strong preferences for size and species were documented). In addition, Paine (1963) noted that a small naticid incorporated a polychaete, Owenia fusiformis, into its diet at Alligator Harbor in Florida.

Naticids at my field setting may have attacked other mollusks (or non-molluscan prey) during the summer that were more readily available than the presumed heat stressed Mercenaria, perhaps foraging deeper in the sediment also in avoidance of heat stress, or predation from their enemies.

If naticids were heat stressed as well due to higher summer temperatures, drilling levels additionally could be affected if they limited their foraging periods, perhaps by being inactive and buried within the sediment during the day, or migrated into deeper waters of the nearby

Intracoastal Waterway in order to remain submerged during peak exposure to heat at low tides.

Tagged Neverita duplicata in studies by Turner (1949, 1950) revealed that individuals could move up to at least 100 m; experimental plots were situated ~400 m from the Intracoastal

Waterway, but channels that remained inundated at low tide may have been more accessible.

118

Limited data exist regarding heat stress of moon snails; Ansell (1982a) noted that although drilling by Euspira pulchella increased between 10°C–20°C, it was reduced at 25°C. Previous work on Neverita duplicata in Massachusetts did not examine feeding above 21°C due to equipment limitations (Hanks, 1952). My laboratory work demonstrated that naticids are capable of drilling prey up to 30°C in North Carolina; no reduction in feeding was observed at these high temperatures. Laboratory moon snails were continually submerged in flow-through set-ups, however, and not subject to additional heat that might influence benthic infauna such as when the sediment surface is exposed during low tides in the field or from standing pools of water within ray pits that may heat up to 35°C as previously mentioned. Paine (1963) observed that abundances of Neverita and Sinum moon snails in Florida were consistently low during the winter and spring seasons, but that these naticids were particularly uncommon in the summer.

To the contrary, at higher latitudes, moon snails are typically more abundant during the summer compared to winter (e.g., Richardson et al., 2005). These differences demonstrate how seasonal changes may have divergent effects on molluscan communities across latitudes.

Latitudinal Patterns

This study examines seasonal variation in feeding by Neverita duplicata near the center of its distribution along mid-latitudes. Most previous work is based at the northern end of its range in

Massachusetts (Table 6); field studies by Paine (1963) were conducted in Alligator Harbor, FL.

Timing and duration of seasons varies latitudinally, as do seawater temperatures typical of these periods. Temperatures reported by Huebner & Edwards (1981) for Massachusetts averaged

18.5–23°C (May through September), 11.8°C (October to mid-November), 2.6°C (mid-

November to mid-January), and 5°C (mid-January through April). These means are quite

119 different compared to ranges characteristic of these months in North Carolina as documented in this study: 8–12°C (mid-January through February), 16–19°C (mid-October through November),

21–26°C (mid-April through May), and 27–31°C (mid-July through August). Menzel (1961) reported temperatures for Alligator Harbor in Florida comparable to those observed in North

Carolina. Because feeding rates of naticids vary with temperature (e.g., Tables 6 and 7), and magnitude and duration of exposure to seasonal conditions fluctuates with latitude, different seasonal regimes may yield varying intensities of drilling at different latitudes. Seasonal effects are likely not equivalent along all latitudes; for example, summer feeding of N. duplicata in

Massachusetts (~42°N), North Carolina (~34°N), and Florida (~30°N) may be quite different as related to temperature as well as biological variables that respond to abiotic changes seasonally such as the availability of prey.

In addition, seasonal differences in behavior may be exhibited by separate species of moon snails inhabiting the same latitude, and such differences may not be consistent throughout their overlap in distribution among other latitudes. Weissberger & Grassle (2003) found that settlement of Neverita duplicata and Lunatia heros in New Jersey occurred at different times of the year (late June/early July vs. mid-September, respectively). Edwards & Huebner (1977) cited Hanks (1960) in noting an early August settlement period for N. duplicata in Massachusetts instead. Furthermore, different tolerances of naticid species to seasonal changes in abiotic factors may affect seasonal patterns in feeding at the same latitude, and not consistently across latitudes. In Massachusetts, N. duplicata ceases feeding for several months during the winter, unlike L. heros, which is able to feed at colder temperatures (Hanks, 1952; Edwards & Huebner,

1977; Fregeau, 1991). The winter cessation of feeding by N. duplicata near its northern limit is

120 not reflected in North Carolina, as this species consumed clams (albeit at suppressed rates) in both my laboratory and field experiments during the winter season.

Most studies of spatial and temporal patterns in naticid drilling are based on calculation of drilling frequencies (number of drilled individuals divided by the total number of prey individuals). Geographic variation in drilling is a concern for interpreting temporal trends as assemblages from different stratigraphic intervals often originate from different latitudes as controlled by the availability of fossil deposits. Latitudinal variation in drilling may result from a variety of factors (as reviewed in the preceding chapter of this dissertation), one of which may be changes in seasonality across latitudes as is the focus here. This study confirms that drilling fluctuates seasonally, in large part, but not exclusively, due to changes in temperature.

Time-averaged shell assemblages from which drilling frequencies are calculated comprise the accumulation of individuals over multiple seasons and many years (Flessa, 1993).

Smoothing of seasonal effects is normally considered a benefit of time-averaging in studying broad-scale evolutionary patterns (Kidwell & Holland, 2002); however, concerns arise in situations in which seasonality has marked effects on communities (Peterson, 1977). Because feeding by naticids varies seasonally, an intensity of drilling averaged across seasons should be lower among mid-latitudes compared to what it might be nearer to the equator where seasonality is less pronounced and a narrower range of warmer temperatures is present year round. For example, proportion of drilled prey varied seasonally in laboratory experiments (Table 3); averaged drilling based on all seasons combined is 27%. However, if only data from summer are used, suggestive of what drilling might be in the tropics where seawater is consistently warm all year (e.g., Northeast Brazil at 26–29°C, Castro & de Miranda, 1998), mean drilling is much higher at 41%.

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This hypothesis matches the results from modern shell assemblages collected in Brazil where greater drilling was found equatorward (Chapter Two). However, summer field experiments in North Carolina indicated a lack of drilling instead, implying that a decrease in drilling at lower latitudes may be due to interference and/or risk from enemies of moon snails as proposed by Vermeij (1993) and supported by Kelley & Hansen (2007) for data collected on modern shell assemblages of the U.S. East Coast. Whether summer field data are biologically meaningful and support decreased feeding by naticids for a variety of reasons such as the potential influence of other predators, or whether they may be an artifact of poor prey health or movement of moon snails outside of the study area due to heat stress is unclear. Nonetheless, naticids are not feeding in a vacuum in nature; caution should be applied in focusing solely on results derived from laboratory experiments.

Reduced drilling at higher latitudes documented in the study by Kelley & Hansen (2007) supports the hypothesis that drilling frequencies should be less in areas of high seasonality

(although a reduction in drilling was observed also at lower latitudes exhibited by less seasonality). Decreased drilling was noted in the Rio Grande ecoregion of southernmost Brazil, where seasonality has a very strong effect on oceanographic conditions (as reviewed in the preceding chapter). Seasonal upwelling affects portions of the shelf in both Southeastern Brazil and Eastern Brazil (Heileman, 2009), but presumably more so at higher latitudes, and yet the intensity of drilling usually could not be differentiated between these ecoregions. Peak drilling in Northeastern Brazil corresponds well with decreased seasonality in warmer tropical waters.

Temperature and seasonal impacts on patterns in drilling may co-vary latitudinally, however, so that variation in drilling due to temperature shifts with latitude is perhaps reinforced by seasonal influences on drilling. Seasonality may not be imparting a unique effect relative to overall

122 changes in temperature with latitude. The results of my field and laboratory experiments indicate that seasonal differences that do not directly correspond to temperature effects on metabolic rates are present (e.g., fall vs. spring). Furthermore, if summer field data accurately reflect intensity of drilling during that season in nature, seasonal effects are vastly different from expectations based solely on the impacts of temperature on feeding.

Paleontological Implications

The influence of seasonality on marine faunas is challenging to assess using paleontological assemblages; most studies that examine seasonal patterns are restricted to use of stable isotopic analyses. The ratio of 18O and 16O isotopes recorded in a shell reflects the temperature at which

CaCO3 was precipitated; hence, sampling across a shell yields sinusoidal variation in oxygen isotope ratios due to seasonal changes in temperature (Jones, 1980; Jones and Quitmyer, 1996).

Thus, mollusks can be used to examine aspects of seasonality in the fossil record. For example,

Buick & Ivany (2004) utilized oxygen isotopes to show that seasonal changes in light limitation

(and therefore food) contributed to the longevity of the Eocene fossil bivalve Cucullaea raea in

Antarctica, which regularly lived for more than 100 years. Dietl & Kelley (2004) used oxygen isotopes to examine whether different predatory gastropods (shell-chipping whelks and drilling naticids and muricids) seasonally coincided in their attacks on a single prey species in the

Pliocene Yorktown Formation of Virginia. Because each predator leaves a distinct trace on the shell of its victim, season of attack could be determined by examining the location of the predation trace with respect to seasonal shell growth increments. Preliminary data suggested that these predators were active during the same seasons, which has implications for understanding how evolutionary processes may be shaped by emergent effects of multiple predators.

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The importance of seasonality in regards to analyzing patterns of drilling predation in the fossil record relies on whether seasonal signals are preserved in within-habitat time-averaged accumulations of shells. Time-averaged assemblages may represent ecological snapshots

(minutes to years), within-habitat mixing of multiple generations of individuals (years to thousands of years), as well as larger scale environmentally or biostratigraphically condensed deposits, which are less useful for paleoecological analyses due to preservation that incorporates different environmental settings or species with evolutionary ranges that did not overlap

(Kidwell & Flessa, 1996). Within-habitat time-averaged assemblages are most commonly utilized by paleoecologists, and Recent shell accumulations (such as the collections from Brazil analyzed in Chapter Two of this dissertation) similarly reflect mixing of multiple molluscan communities, most likely on the order of decades to hundreds of years.

Work by Yanes et al. (2012) on modern shell accumulations of drilled and undrilled lucinid bivalves from the Bahamas, in combination with isotopic methods, demonstrated seasonal variation in drilling predation in molluscan death assemblages distributed on a beach.

Temperature at the time of death (last episode of growth at the shell margin) was determined using oxygen isotope profiles. Mortality overall was greatest during the warmest months.

Undrilled shells exclusively recorded the highest temperatures (26–27°C); deaths during the coldest periods (19–22°C) were attributed only to drilling. Although seasonal signals in drilling appear to be preserved, concerns regarding post-mortem sorting of drilled vs. undrilled shells are discussed. These preservational biases may be specific to the shoreface setting of their work; such habitats are not usually preserved in the fossil record (Yanes et al., 2012). Tidal flats such as analyzed in this study are not often represented either in paleontological deposits; most data on drilling derives from assemblages indicative of shallow, subtidal shelf conditions. Intertidal

124 environments offer ease of access for examining seasonal differences in marine communities; however, influence of heat stress on infauna is likely diminished in subtidal settings as the sediment surface is never exposed. Nonetheless, molluscan communities inhabiting shallow subtidal environments still experience and respond to seasonal fluctuations in water temperature

(as confirmed by oxygen isotope profiles exhibiting seasonal patterns in rate of shell growth).

The impact of seasonality needs to be considered more frequently in interpretations of spatial and temporal patterns in drilling predation. Seasonal regimes vary with latitude and through time as climate changes. Disentangling various abiotic and biotic influences on seasonal drilling patterns is greatly needed for studying predator-prey interactions in the fossil record. For example, fluctuations in drilling intensity across an extinction boundary could be due to altered seasonal regimes influencing the behavior of naticids and not necessarily a loss of predators or prey. Understanding to what extent seasonal signals are preserved in time-averaged shell accumulations will be essential for identifying seasonal effects on drilling in the fossil record.

Future Work

The results of laboratory and field experiments in this work yielded similar seasonal patterns in drilling predation, with the exception of the summer season. Future study on the location, diet, density, and behavior of Neverita duplicata in the field during summer months in particular could aid in resolving causes for the mismatch between field and laboratory data for the warmest season. In addition, an understanding of drilling frequencies in natural shell accumulations at the field setting would be beneficial. Most drillholes observed in shells at this locality are found in smaller prey; collecting sufficient data on size-appropriate specimens could be a laborious effort, in part because most shells are buried, of variable preservation due to bioerosion, and are mixed

125 with extensive shell hash surrounding oyster reefs. Nonetheless, improved knowledge of naticid activities at this locality is needed. Furthermore, examining the effects of seasonality in a subtidal setting subject to less seasonal extremes and more akin to most paleontological assemblages used in studies of drilling predation would be valuable albeit challenging.

Understanding seasonal effects on drilling predation over broad latitudinal scales requires an examination of seasonal impacts on multiple predatory species from different locations with latitude. This study demonstrates seasonal variation in drilling along mid-latitudes; more work on seasonal impacts in other geographic settings and with different naticid species is desirable.

Most previous studies did not allow for seasonal biological and physical disturbances to affect patterns in drilling, as data are limited primarily to caged field experiments or laboratory efforts.

However, existing literature data, integrated with the results obtained during this study, could be employed in predictive modeling for examining how differences in drilling may vary with latitude as a result of geographic variation in the presence, duration, and magnitude of seasons.

Applicability of such work to drilling patterns based on frequencies determined from modern and fossil shell assemblages requires investigation as to the preservation of seasonal signals in light of time-averaging. Temporal and spatial trends in drilling could be greatly impacted by seasonal fluctuations in the intensity of drilling, if such differences are preserved in shell accumulations.

CONCLUSIONS

Seasonal variation in drilling intensity was documented in both laboratory and field experiments.

Data partly coincided with expectations that changes in feeding should reflect temperature shifts, but seasonal differences in drilling could not be explained entirely by fluctuations in temperature on metabolic rates. Laboratory experiments concluded that drilling was greatest in summer and

126 lowest in winter; more drilling was documented in the fall than in the spring, despite cooler fall temperatures. Field results indicated that drilling was low in winter, increased slightly in spring, and peaked during the fall; no drillholes were found during the summer season, likely due to a combination of heat stress and heightened shell-crushing predation. Utilizing both a field and laboratory experimental approach offered different perspectives as to the influence of seasonality on drilling predation, with and without external factors other than temperature that may vary seasonally. These results imply that seasonality may contribute to variation in the intensity of drilling with latitude, which has implications for studies of predator-prey interactions in the fossil record including escalation, if such signals are preserved in time-averaged shell accumulations.

ACKNOWLEDGMENTS

Funding for this project was provided by the Constance E. Boone Award from the Houston

Conchology Society. Dissertation writing was supported by a Ford Foundation Fellowship as well as the Chrysalis Scholarship from the Association for Women Geoscientists. I am extremely grateful to G. Dietl for his help in developing this project and M. Posey for advice regarding experimental set-up in both the laboratory and field setting. Discussions with P.

Kelley and R. Laws regarding applicability of this work to patterns of drilling predation in the fossil record are greatly appreciated. Thanks to S. Borrett for input regarding data visualization as well as statistical guidance, to which F. Scharf additionally contributed. I am indebted to S.

Kline, B. Parnell, and D. Friend for their repeated assistance with both sets of experiments.

Thanks to the many volunteers that aided in intense fieldwork, often in suboptimal conditions

(L.A. Harden, K. Jabanoski, P. Mason, S. Stanford, C. Stanford, C. Korpanty, J. DePriest, J.

Facendola, J. Eichinger, T.-L. Loh, C. McDougall, L. Muzyczek, C. Kielhorn, Y. Shirazi, J. Lisa,

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L. Unger, D. DiIullo, S. Midway, C. McKinstry, K. Stasser). In addition, experimental work benefitted from logistical support graciously provided by T. Alphin, R. Deans, R. Moore, and

J. Styron, as well as J. Morris for help with clams. Thanks to Y. Yanes for sharing data in press.

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CHAPTER FOUR: INFLUENCE OF SEDIMENT DEPTH ON DRILLING BEHAVIOUR OF NEVERITA

1 DUPLICATA (GASTROPODA: NATICIDAE) WITH A REVIEW OF ALTERNATE MODES OF PREDATION

ABSTRACT

Predatory naticid gastropods typically attack other infaunal molluscs by drilling holes that record their activities in the shells of their prey. Other modes of naticid predation, which need not leave complete boreholes, are noted in the literature and may complicate interpretation of the record of naticid predation in fossil and modern assemblages. “Smothering” is an alternate form of predation that has never been clearly defined with respect to naticid gastropods. Feeding occurs in the absence of a completed drillhole; in most cases suffocation is implied, but reported deaths may be linked to an array of mechanisms (e.g., direct feeding, anaesthetizing mucus). We examine the pervasiveness of alternate modes of predation employed by naticids reported in the literature and offer recommendations regarding the terminology used in referring to such mechanisms. Because it is unclear if predatory behaviours such as suffocation are common in natural settings or are mostly artifacts of laboratory conditions such as insufficient substrate, we examined experimentally the influence of different sediment depths on drilling vs. suffocation of

Mercenaria mercenaria prey by Neverita duplicata. More than 99% of the clams recorded as consumed in our experiments were drilled (n=404), regardless of sediment depth, with <1%

(n=4) noted as cases of potential suffocation. Our results indicate that shallower sediment depths do not affect drilling in this species and that prey health is a more important factor in deaths linked to suffocation. Analysis of previous studies indicates that prey health and other laboratory

1 This chapter is formatted to be submitted to the Journal of Molluscan Studies as: Visaggi, C.C., Dietl, G.P., and Kelley, P.H. Influence of sediment depth on drilling behaviour of Neverita duplicata (Gastropoda: Naticidae) with a review of alternate modes of predation.

133 effects are likely responsible for many instances of suffocation reported in the literature. Thus concerns regarding use of drillholes as an indicator of predation by naticids in modern and fossil deposits should be alleviated. Future work on other alternate modes of predation by naticids should focus on validating reported occurrences of such predation and identifying different mechanisms that may be involved.

INTRODUCTION

The Naticidae are a cosmopolitan family of predatory marine gastropods (Kabat, 1990; Kelley &

Hansen, 2003). Commonly referred to as moon snails, naticids are widely recognized for their shell-drilling (= boring) behaviour that results in characteristically countersunk drillholes in the shells of their prey, comprised mostly of other infaunal molluscs. Naticid drillholes preserved as trace fossils provide a record of ancient predator-prey interactions commonly utilized by palaeontologists in studying evolution (Kitchell, 1986; Vermeij, 1987; Kowalewski & Kelley,

2002; Kelley & Hansen, 2003; Harper & Kelley, 2012). Although drilling is the dominant predatory strategy employed by moon snails, non-drilling mechanisms by naticids are reported in the literature. Over the last decade, increased awareness of alternate modes of predation

(sometimes referred to as “atypical,” “anomalous,” or “aberrant” behaviours) has raised uncertainty about the interpretation of data provided by beveled drillholes attributed to naticids

(Leighton, 2002; Aronowsky, 2003; Harries & Schopf, 2007; Kelley & Hansen, 2007; Kelley et al., 2011); however, no report has yet addressed specifically how pervasive alternate forms of predation are among the Naticidae and how these predatory behaviours are executed. In this study we review literature accounts of alternate forms of naticid predation and employ laboratory experiments to examine how factors in artificial settings, specifically insufficient sediment depth

134 and prey health, may influence alternate modes of predation reported in the literature. In particular, we focus on predation commonly referred to as “suffocation” by biologists and

“smothering” by palaeontologists.

Alternate Modes of Predation

Naticid gastropods are regarded often as models of stereotypy in their predatory behaviour

(Kitchell, 1986; Kabat, 1990). Burrowing through soft substrates, most naticids forage at or below the sediment surface and remain submerged while in pursuit of their prey. Prey manipulation begins as a victim is captured, secured in the large muscular foot of the naticid, and enveloped in a film of mucus. Although foraging often occurs near the sediment surface, an immobilized quarry is usually dragged down into the substrate before drilling is initiated. Shell penetration is achieved by chemical etching and physical abrasion in alternation (Ziegelmeier,

1954; Fretter & Graham, 1962; Carriker, 1981; Kabat, 1990), after which the proboscis is inserted through the hole for consumption of prey. Alternate forms of naticid predation do not require completed drillholes for feeding to commence.

To facilitate discussion, we categorize modes of naticid predation (Table 1) first by the primary attack (drilling or non-drilling) and according to the outcome of each death scenario

(preservation of a complete drillhole, incomplete drillhole, or no drillhole, which would affect interpretation of predation in the fossil record). Non-drilling predation includes operculum wedging, direct feeding via a natural opening, and scavenging. Suffocation is an alternate form of naticid predation that may either accompany or occur without drilling of prey.

Alternate modes of naticid predation are recorded in both field (Table 2) and laboratory

(Table 3) settings. Field reports of alternate predatory behaviours are based mostly on gaping

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Table 1. Types of naticid predation as summarized from the literature and categorized based on initial attack, cause of mortality, entry for feeding, and whether any form of a drillhole (DH) results from the predation event.

Mode of Attack Cause of Mortality Entry for Feeding End Product Drilled Drillhole Complete DH Drilling Suffocation* Aperture/Existing Gape/Opened Valves Incomplete DH Suffocation* Aperture/Existing Gape/Opened Valves No DH Operculum Wedging Aperture No DH Non-Drilling Direct Entry Existing Gape No DH Scavenging Aperture/Existing Gape/Opened Valves No DH

*The precise role of the mucus in this process is unclear; anesthetizing substances are proposed in the literature.

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Table 2. Alternate modes of naticid predation reported in the literature based on field investigations. Taxon names for naticids are updated as per Torigoe & Inaba (2011). Abbreviations include n/a (not applicable), n/p (not provided), Y (yes), N (no), S (slight), Un (undrilled), Inc (incompletely drilled), and Obs (observations). Standard postal abbreviations for states (USA) and provinces (Canada) are employed. Author interpretations are noted as based on observations, shells, or both; items marked by an asterisk indicate that laboratory accounts of alternate predation were additionally discussed (see Table 3 for further details). Only live attacks are incorporated here; scavenging is not reviewed.

Naticid Taxon Localities Prey Taxon Prey Family Gape Un/Inc Obs/Shells Reference Glossaulax reclusiana CA & OR, USA Olivella biplicata Olivellidae n/a Inc Both* Edwards, 1969 Thurber, 1949; NB, Canada Mya arenaria Myidae Y Un, Inc Shells Medcof & Thurber, 1958 NS, Canada Mya arenaria Myidae Y Un Both Wheatley, 1947 Lunatia heros Wheatley, 1947; PE, Canada Spisula solidissima Mactridae S Un Obs Medcof & Thurber, 1958 ME, USA Mya arenaria Myidae Y Un Shells Vencile, 1997 NS, Canada Mya arenaria Myidae Y Un Both Wheatley, 1947 Lunatia triseriata ME, USA Mya arenaria Myidae Y Un Shells Vencile, 1997 BC, Canada Tresus nuttallii Mactridae Y Un Obs Grey, 2001 Saxidomus BC, Canada Veneridae S Un, Inc Both* Bernard, 1967 giganteus WA, USA Tresus nuttallii Mactridae Y Un Obs Reid & Freisen, 1980 Lunatia lewisii Mya arenaria Myidae Y Un Obs Protothaca Veneridae N Un Obs WA, USA staminea Agersborg, 1920 Clinocardium Cardiidae N Un Obs nuttallii MA, USA Ensis directus Pharidae Y Un Shells Edwards, 1974 Neverita duplicata MA, USA Ensis directus Pharidae Y Un Obs Schneider, 1982 n/p Ensis directus Pharidae Y Un Both Turner, 1955 Tectonatica tecta South Africa n/p n/p n/p Un Obs Ansell & Morton, 1985

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Table 3. Alternate modes of naticid predation reported in the literature based on laboratory investigations. Taxon names for naticids are updated as per Torigoe & Inaba (2011). Abbreviations as in Table 2; SL (sand layer provided but precise depth not given). Locations for specimen collection vs. experimentation are noted separately, with the latter enclosed in parentheses. Percentages and numbers listed represent the proportion of prey consumed by alternate means. Both predator and prey size are recorded in millimeters; sizes are based on lengths unless otherwise defined as height (H). Only live attacks are incorporated here; scavenging is not reviewed.

Naticid Collected Prey Un/ Sed Size Prey Taxon Prey Family % #/Total Gape Monitored Reference Taxon (Exp) Size Inc Depth Ansell & Conuber Hong Venerupis ~27.5 20–40 Veneridae 13% 3/23 N Un SL daily Morton, melastoma Kong philippinarum 1985 Venerupis Un, 30–39 Veneridae 50% 8/16 N philippinarum Inc Anomalocardia Veneridae 78% 7/9 N Un squamosa Ansell & Glossaulax Hong Atactodea 47–52 n/p Mesodesmatidae 25% 1/4 N Un SL daily Morton, didyma Kong striata 1987 Coecella Mesodesmatidae 13% 3/23 N Un chinensis Glauconome Glauconomidae 57% 4/7 N Un chinensis Glossaulax CA & OR, Olivella Un, Edwards, ~29.5 18–28 Olivellidae 81% 17/21 n/a SL n/p reclusiana USA biplicata Inc 1969 24.5– NJ (NC), Mercenaria 25–43 Veneridae 27% 13/48 N Inc 3 cm 1–2 days Friend, 2011 47.5 USA mercenaria Venerupis Un, 20–40 Veneridae N Lunatia philippinarum 38% 42/111 Inc heros MA (CA), Mercenaria (Un), (Un), Un, 10–15 Aronowsky, large ~40 Veneridae N daily USA mercenaria 16% 18/111 Inc cm 2003 (Inc)^ (Inc)^ Un, Macoma spp. 8–45 Tellinidae N Inc

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Weissberger (continued) Spisula n/p NJ, USA larger Mactridae n/p n/p S Un n/p n/p & Grassle, solidissima 2003

NB (ON), Protothaca 30–60 20–60 Veneridae N 10 cm n/p Grey, 2001 Canada staminea 9% (Un), Un, 21% (Inc)^ Inc 50– BC (ON), Protothaca 20–60 Veneridae N 10 cm n/p Grey, 2001 100 Canada staminea

BC, Saxidomus 7.6 Bernard, Lunatia n/p n/p Veneridae > 25% n/p S Un daily lewisii Canada giganteus cm 1967 Newel & BC (AB), Venerupis 917/ Un, n/p 37–57 Veneridae 54% N SL n/p Bourne, Canada philippinarum 1687 Inc 2012 1.4– Natica Vermeij, 20.9 Guam Tellina robusta n/p Tellinidae 11% 2/19 N Un 3.5 n/p gualteriana 1980 cm Natica 25–34 Olivella hourly Hughes, Panama 15–20 Olivellidae 100% 3/3 n/a Un 5 cm unifasciata (H) volutella –daily 1985 Neverita Un, 7.6 Siao et al., 33–37 NC, USA 17–23 Naticidae 6% 7/126 n/a 3 days duplicata Inc cm 2010 Mercenaria 7.6 15–26 NC, USA 7–23 Veneridae 10% 81/807 N Un 2–3 days Gould, 2010 mercenaria cm

Un, Neverita Macoma spp. ~25 Tellinidae 4% 11/265 N duplicata (Un), (Un), Inc medium MA (CA), Venerupis 12% 32/265 Un, 10–15 Aronowsky, ~37 Veneridae N daily –small USA philippinarum (Inc)^ (Inc)^ Inc cm 2003 Neverita smaller Naticidae 100% 1/1 n/a Inc duplicata Ansell & Hong Venerupis Polinices ~28 10–40 Veneridae 36% 44/114 N Un SL daily Morton, Kong philippinarum mammilla 1985

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(continued) Venerupis Veneridae 55% 78/142 N Un philippinarum Anomalocardia Veneridae 44% 10/23 N Un squamosa Atactodea Mesodesmatidae 14% 4/28 N Un Ansell & Hong striata larger n/p SL daily Morton, Kong Coecella Mesodesmatidae 20% 10/49 N Un 1987 chinensis

Donax faba Donacidae 16% 3/19 N Un

Glauconome Glauconomidae 15% 5/34 N Un chinensis Gafrarium Veneridae 13% 1/8 N Un pectinatum Timoclea Veneridae 100% 4/4 N Un 1.4– 25.7– marica Vermeij, Guam n/p 3.5 n/p 35.4 1980 Tellina robusta Tellinidae 21% 4/19 N Un cm

Quidnipagus Tellinidae 60% 6/10 N Un palatam

^Available data listed here for prey consumed by alternate means are not divided by prey species for Aronowsky (2003) or by predator species for Grey (2001).

140 prey or rely on indirect observations, such as incompletely drilled or undamaged shells from experimental plots. Documentation of suffocation in bivalves capable of securing their margin is restricted usually to laboratory observations. This situation is not surprising given that the infaunal mode of naticids prevents study of their behaviour in the field without interruption.

The present work focuses on deaths due to suffocation in which entry through the commissure is permitted via forced gaping before or during the drilling process, rather than through an existing permanent gape, which may allow feeding without prior suffocation of prey.

Such suffocation has sometimes been referred to as “smothering.” However, this term is not clearly defined in the literature, and smothering has not been addressed explicitly as a form of naticid predation.

What is Smothering?

Part of the confusion concerning the definition of “smothering” is caused by a division in the language used by different disciplines. “Smothering” is an alternate form of naticid predation usually cited by palaeontologists, whereas “suffocation” is utilized more frequently by biologists

(Table 4), although Aronowsky (2003) incorporated both words in discussing alternate naticid predation. To our knowledge, smothering, as an attack behaviour executed by gastropods, was used first by Morton (1958) to describe predation by members of the Cassididae, Harpidae,

Olividae, Tonnidae, and Volutidae. Suffocation was not explicitly stated as the cause of death but was implied by the phrase “smothering with the foot” (Morton, 1958, p. 95). Non-drilling predation by moon snails has been linked to suffocation for nearly a century (Agersborg, 1920) and Ricketts & Calvin (1939) imparted this information to marine ecologists in their book,

Between Pacific Tides. Interestingly, “smothering” was used alongside “suffocation” in

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Table 4. Use of “suffocation” (SU) vs. “smothering” (SM) in the literature in reference to alternate predation by naticids. These examples do not include unpublished MS or PhD work, abstracts, books, comments or replies to articles, or pers. comm. citations in publications.

Term Reference Text "In the case of Mya, the gasteropod sucks itself over the syphon down into the sand until its victim is dead SU Agersborg, 1920 from suffocation, and then when the clam has opened, Polynices simply sends its proboscis between the valves and devours the content." p. 421 "Although Polinices may occasionally force its prey's operculum, the incomplete bore holes suggest another SU Edwards, 1969 explanation, viz., that O. biplicata suffocates while wrapped in the predator's foot and relaxes." p. 327 "...Arcopagia robusta and Quidnipagus palatam which can be eaten by naticids without drilling. It is likely SU Vermeij, 1980 that these clams suffocate while being enveloped by the predator's foot before drilling has proceeded very far." p. 332 "Since in the present study, N. unifasciata consumed O. volutella within 12 h, a forceful entry through or SU Hughes, 1985 round the edges of the flimsy operculum seems a more likely method than suffocation." p. 334 "The immediate cause of gaping of the prey is interpreted here as suffocation, but it is also possible that SU Ansell & Morton, 1987 the process is facilitated by the presence in the pedal mucus or other secretion of the predator of a narcotizing toxin." p. 117 "We explored the possibility... secretion might have a pharmacological effect [...] There was no such effect, SU Reid & Gustafson, 1989 and we conclude that the condition of prey is due to suffocation […] An identical effect results from sealing clams in seawater in cooled plastic bags for 12 h." p. 327 "… but Ansell & Morton (1987) have shown in laboratory trials with Venerupis japonica eaten by various SU Vermeij et al., 1989 naticids that some incompletely drilled prey had nevertheless been consumed by the predator. In such cases, the prey was apparently suffocated…" p. 270

SU Kabat, 1990 [used repeatedly in citing the work of others]

"Naticid gastropods use several strategies to feed on their prey <…> suffocation in snails with a large SU Calvet i Catà, 1992 mesopodium (Ansell & Morton 1987), and non-boring predation as observed in razor clams (Schneider 1981). p. 58 “Large Glossaulax didiyma begin boring their prey, but consume it after the prey suffocates, before boring SU Peitso et at., 1994 is complete (Ansell and Morton 1987)." p. 323

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"Vermeij (1980) noted that many of the smaller prey species in his study might have been killed by SM Leighton, 2001 smothering before drilling was necessary." p. 57

"Also, some naticids may be capable of smothering, rather than drilling, their prey (Ansell and Morton SM Leighton, 2002 1987)." p. 333

"A naticid may kill a bivalve to large by suffocating it with its foot (Ansell & Morton, 1987; E. Weissberger SU Weissberger & Grassle, 2003 personal observation), leaving no trace of predation on the bivalve's shell." p. 680 "Shell valves cleaned of tissue that lacked evidence of drilling were not recovered from aquaria, such that P. SU Kingsley-Smith et al., 2003 pulchellus did not appear to employ any non-drilling methods of subjugating prey, such as suffocation." p. 182 "Similarly, Ansell & Morton (1987) observed in aquarium experiments that the naticid Glossaulax didyma SU Kowalewski, 2004 abandoned incomplete drill holes and consumed some of its prey, which suffocated during initial phases of drilling, without penetrating the shell." p. 365 "Ansell and Morton (1987) observed that some individuals of the naticid Glossaulax didyma feeding on SU Harper, 2006 Tapes philipinarum started but failed to complete drillholes, but instead suffocated the prey and fed on it successfully." p. 326

SM Kelley & Hansen, 2007 "…alternative modes such as smothering may be more common at higher latitudes." p. 287

"Ansell and Morton (1987) have documented a range of feeding modes, such as smothering […] Because SM Harries & Schopf, 2007 smothering predation leaves no discernable signature in the fossil record…" p. 42–43 "Ansell & Morton (1987) also showed that Polinices tumidus Swainson, 1840, held its prey with the rear of SU Morton, 2008 its foot and, as a consequence, sometimes suffocated it such that there were no drill holes to identify the predation event." p. 317 "…four successive phases of behaviour: (1) capture, (2) smothering, (3) rotation and (4) drilling. […] pedal SM Hasegawa & Sato, 2009 mucus, which enveloped and hardened around the prey, immobilizing it for a few days…" p.149

"It has been shown, however, that some extant boring predators can subdue their prey by suffocating them SU Baumiller et al., 2010 (Kowalewski, 1994)…" p. 639

"…how often smothering or rasping into the tube via the aperture to kill the organism was employed by SM Klompmaker, 2012 naticids cannot be addressed." p. 117

143 describing alternate predation by naticids, but exclusively in the 1962 edition. Use of

“smothering” was edited from later versions. Leighton (2001, 2002) applied “smothering” when citing alternate predation modes described by Vermeij (1980) and Ansell & Morton (1987).

Leighton, as well as subsequent palaeontologists (e.g., Harries & Schopf, 2007; Kelley &

Hansen, 2007), apparently employed this term as a synonym for non-drilling predation by suffocation, although this use was never clearly stated and perhaps led to misinterpretation of the term as a “catch-all” phrase for any instance of naticid feeding in the absence of drilling. More recently, Hasegawa & Sato (2009) used “smothering” to denote merely the encasement of mucus that immobilizes naticid prey for days, even though eventual death is due to drilling and not suffocation, adding further confusion to the meaning of smothering as a predatory behaviour utilized by moon snails.

Even in cases of mortality attributed specifically to suffocation by naticids, relatively little is known about the actual cause of death. Agersborg (1920) described suffocation first as an outcome of siphon plugging (e.g., Mya) or as a result of being held in the naticid foot until adductor muscles relaxed or the victim (e.g., Protothaca and Clinocardium) died. However, many bivalves are noted for their capacity to remain closed for long periods, suggesting that such questionable deaths may not be attributable entirely to suffocation; consequently, copious mucus secretions that aid in prey capture and handling are often considered (Ansell & Morton, 1987).

The role of mucus secretions in naticid predation, particularly by suffocation, is controversial and additional research is warranted. Mucus may: 1) serve in subduing prey by keeping valves or the operculum closed and thus limiting escape (Richter, 1962), 2) produce suffocation by obstructing access to oxygen (Reid & Gustafson, 1989), or 3) have anesthetizing properties that facilitate prey subjugation as hypothesized by many authors (e.g., Wheatley,

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1947; Turner, 1955; Carriker, 1981; Hughes, 1985; Ansell & Morton, 1987). Such a narcotic effect might yield relaxation of the muscles keeping the valves closed, leading to apparent suffocation by permitting an entry for feeding through the margin. Distinguishing among these potential effects of mucus secretions used by naticids is challenging.

Savazzi & Reyment (1989) suggested that mucus from Natica gualteriana affected

Umbonium vestiarium prey even after the predator was removed. Control specimens free of mucus burrowed rapidly (perhaps a flight response), whereas prey with apertures plugged by mucus remained stationary and retracted for several hours. Removal of mucus yielded an active response from U. vestiarium within 30 minutes, however, indicating that any numbing effect was not permanent. Reid & Gustafson (1989) stated that bivalve prey were limp and unresponsive after being drilled, leading them to investigate pharmacological properties of esophageal gland secretions of Lunatia lewisii. They found no paralyzing effect in placing these secretions on the heart of Tresus nuttallii and concluded that prey must be suffocated as suggested by others. The same lifeless condition was observed upon sealing bivalves in cooled plastic bags of seawater for

12 hours.

Non-drilling attacks on bivalves with a permanent gape, or by forced entry through the aperture of gastropods, are not usually considered by palaeontologists to represent deaths by smothering due to the availability of direct access for feeding. This view is supported by Morton

& Morton (1983) in discussions of predation by non-naticid gastropods as “either smothering them with the foot, or plunging the proboscis into the soft parts” (p. 285). Unfortunately, it is often not clear from the literature if feeding occurs directly through the natural opening or if it is only feasible after first suffocating or anesthetizing prey, particularly as Agersborg (1920) initially described suffocation by naticids in part based on the gaping prey Mya. Thus it remains

145 uncertain if a single agent or a combination of factors may be responsible for several so-called smothering fatalities in the literature; resolving such accounts is beyond the scope of our work.

Our review of the literature generates several recommendations concerning terminology applied to alternate modes of naticid predation: 1) avoid using the phrase “non-drilling predation” if death of prey occurs as a by-product of the drilling process (e.g., due to suffocation); 2) restrict use of “suffocation” to situations in which mortality is attributed to respiratory distress; 3) promote the more appropriate phrase “alternate modes of predation” as encompassing all feeding by fossil naticids that is not accomplished using a completed drillhole; and 4) abandon the term “smothering” as it is not employed consistently or clearly in the literature, in part because multiple mechanisms may be executed by naticids in achieving apparent suffocation. This problematic usage extends to descriptions of “smothering” predation by other gastropods as well and all researchers are encouraged to be mindful of how the term is applied in understanding the proximate mode of attack for various taxonomic groups. Our literature review also highlights that different causal mechanisms may allow moon snails to feed in the absence of a completed drillhole; research is needed on alternate naticid predation modes that may be a concern for interpreting evolutionary patterns based on drillholes. The experiments conducted in this study are a first step in such research.

Sediment Depth

Alternate forms of predation such as suffocation may result from unnatural laboratory environments, and in particular a lack of sufficient sediment for burrowing with captured prey.

Most aquaria contain only a few centimeters of sand, in contrast to the potentially greater depths naticids might inhabit in the wild. Maximum depths reported from field observations range

146 upwards of 15 cm – 25 cm (Stinson, 1946; Medcof & Thurber, 1958; Bernard, 1967;

Kenchington et al., 1998; Grey, 2001). Mismatches between field and experimental conditions could lead to altered behaviours in laboratory settings as normal burrowing activities may be restricted (Kabat, 1990). For example, Bayliss (1986) found that Euspira pulchella was unable to drill prey in aquaria containing only a few millimeters of sand; although victims could be captured, moon snails were unable to burrow and merely moved in circles, dragging their prey with them. Drilling captive prey commenced only upon relocation to a set-up containing 9 cm of sand, in which they immediately burrowed. Hasegawa & Sato (2009) capitalized on modified behaviours exhibited by Laguncula pulchella in varying sediment depths to demonstrate how altered life positions of prey led to differences in drilling of right vs. left valves. Although depth of sediment has been considered by several authors in setting up laboratory experiments (Bayliss,

1986; Fregeau, 1991; Aronowsky, 2003; Gould, 2010), whether or not insufficient depths of sand may lead to predation via suffocation has yet to be explored fully. Our goal is to address this concern by investigating changes in predatory mode with sediment depth using a naticid species that is studied intensely in both modern communities and palaeontological assemblages.

Neverita duplicata (Say 1822) is an abundant moon snail inhabiting shallow intertidal to subtidal environments along the eastern coast of the United States. It is a generalist predator that feeds primarily on infaunal bivalves (Edwards, 1974). This species is utilized often in laboratory settings (Kitchell et al., 1981; Fregeau, 1991; Aronowsky, 2003; Dietl & Kelley, 2006; Gould,

2010); field observations are available also, including fisheries reports that use drillholes to infer bivalve mortality due to naticid predation (e.g., Belding, 1930). Fregeau (1991) found that N. duplicata preyed on clams at a mean depth of 12.7 cm in laboratory experiments and that it did not attack prey deeper than 16 cm, even when surface clams were removed. Carriker (1951) also

147 reported feeding by N. duplicata at 12.7 cm depth in a field setting in New Jersey. Local field observations indicate that active drilling by this species occurs at comparable sediment depths in

North Carolina.

The conditions under which apparent suffocation by Neverita duplicata occur have yet to be examined explicitly, despite suggestions of alternate predatory modes based on empty prey presumably consumed in the absence of drilling and/or with incomplete drillholes (e.g.,

Aronowsky, 2003; Gould, 2010). To determine whether insufficient substrate for burying with prey is related to laboratory reports of alternate predation modes, our experiments examined changes in frequency of different forms of predation (drilling vs. suffocation) by N. duplicata when exposed to various substrate levels, ranging from no sand to a maximum depth of 20 cm.

We hypothesize that suffocation should be more common than drilling at shallower sediment depths due to extensive prey carrying during prolonged searching for a preferred location to burrow with prey. By varying only sediment depth, we focus on suffocation rather than other alternate predation behaviours. For instance, any influence from potentially paralyzing mucus secretions should not vary with the amount of substrate provided.

MATERIALS and METHODS

Sediment Depth

The hypothesis that decreasing substrate depths yield increasing deaths by suffocation was tested in a laboratory setting through five treatments: 0 cm (i.e., no sediment), 1 cm, 2 cm, 6 cm, 20 cm.

Sediment consisted of fine sand collected from nearby Wrightsville Beach, NC, similar to the natural habitat of Neverita duplicata. Three replicate trials of 48 days each were conducted at the

University of North Carolina Wilmington in the Center for Marine Science during September–

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October 2010, October–December 2010, and June–July 2011, in part due to limited availability of specimens during the winter and concerns regarding suppressed feeding rates in cooler months. Variation in frequency of clams consumed by drilling in different sediment depths was assessed using a chi-square goodness-of-fit test with an alpha level of 0.05.

Neverita duplicata were collected locally from an intertidal flat near Masonboro Inlet,

NC (UNCW Research Lease: 34°10′46″N, 77°50′30″W); all were initially sized at 25–26 mm.

Height (maximum dimension parallel to the coiling axis) and length (perpendicular to height) were recorded every six days for each naticid to evaluate growth rates during the experimental period. Mercenaria mercenaria (18–21 mm in anteroposterior length) were used as prey.

Predator-prey size ratios for these species are appropriate based on the work of Kitchell et al.

(1981). Bivalves were obtained from Virginia and North Carolina hatcheries and held in aquaria with access to flowing seawater to permit natural filter feeding prior to use in experiments.

The decision to use Mercenaria mercenaria as prey was based on several factors.

Alternate modes of predation on this species are attributed to naticids in multiple laboratory experiments; other members of the Veneridae are additionally noted as suffocated in the literature (Table 3). This species is a common prey item of Neverita duplicata in the field

(Edwards, 1974) and in experimental research in laboratory settings (e.g., Kitchell et al., 1981), in part because it is readily available as a commercial species.

Each experimental set-up contained only a single predator and six prey in a 37.85 liter aquarium with an air pump for oxygen circulation. Bivalves were replaced every six days as consumed. Mercenaria containing incomplete drillholes were returned to the same set-up if exhibiting signs of good health (see next section). Experiments were conducted in a closed system; seawater was partially changed in each set-up halfway between experimental checks. To

149 minimize the impact of external factors on feeding behaviour, only seawater controlled to room temperature was used (19.4–23.4°C). Surface observations were noted at this 72 hour interval, but moon snails within the substrate were not disturbed if possible. Salinity and pH also were monitored every six days. Salinity fluctuated between 19.2 and 37 ppt; pH ranged 6.2–9.2.

Prey Health

To test the hypothesis that suffocation is more common at shallower sediment depths due to prolonged prey carrying, it is essential that prey used in laboratory experiments are healthy.

Otherwise, decay or scavenging following natural mortality of weak prey could leave empty shells that might be misinterpreted as deaths due to suffocation. To minimize concerns regarding prey health in our work, several measures were employed to assess the condition of Mercenaria prey before, during, and after being incorporated in our experiments.

First, strength of valve closure was tested before placing prey in experimental set-ups as well as during experimental checks by trying to insert a fingernail in the ventral margin. The few bivalves exhibiting signs of questionable health, as indicated by successful wedging, were discarded prior to experiments. This process also removed any empty shells that were held together by surface tension (Flimlin, 2004). Ability to wedge a fingernail between valves during the course of experiments was noted as a potential sign of deteriorating health and used as an indicator to replace bivalves as discovered. Secondly, dates of entry into aquaria were recorded on all prey as a way to monitor how long individuals remained in experiments; average duration of occupancy in aquaria was quantified. Thirdly, surface observations were noted every 72 hours to look for signs of decay, or weak clams that had gaped or could not bury themselves in the sand. Finally, following Visaggi (2012), empty shells recovered every six days were analyzed for

150 signs of decay, including odor; degree of staining, categorized as absent, light (faint staining or discoloration covering <20% of shell surface), moderate (20–60% of surface covered by dark discoloration), or heavy (dark discoloration over >60% of shell surface); and whether any soft parts remained.

RESULTS

Sediment Depth

Differences in sediment depth did not impact frequency of prey consumed by drilling vs. suffocation for Neverita duplicata (Fig. 1). All moon snails fed during the course of the experiment except for two of the individuals in aquaria lacking sand. Of 411 dead clams recovered, 404 were consumed by drilling. Frequency of prey consumed by drilling is consistent across aquaria regardless of substrate depth (1 cm, 2 cm, 6 cm, 20 cm) using a chi-square goodness of fit test (χ2 = 2.31, df = 3, P = 0.51).

Three clams were drilled to completion, but were not consumed due to interruption during an experimental check. Two of these individuals (in the 2 cm and 6 cm aquaria) were not subsequently redrilled; observations three days later revealed decay instead. The third clam showed no indication of decay afterward or weakness, yet was discovered in the 20 cm set-up within the substrate and completely empty at the next experimental check. Three additional clams were recovered completely empty, but without a drillhole (one each in the 2 cm, 6 cm, and

20 cm aquaria). One final clam without a drillhole was found gaping atop the sediment surface in the 1 cm set-up, but decaying flesh accompanied by an unpleasant odor indicated death by natural causes.

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Figure 1. Number of bivalves consumed for different sediment depths based on pooled data from all replicates. Mode of death was categorized as either drilled or potentially suffocated.

120 Drilled Suffocated?

100

Total Bivalves Consumed Bivalves Total 20

0 0 cm 1 cm 2 cm 6 cm 20 cm Substrate Depth

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Prey Health

Most prey (75%) were consumed quickly by drilling and did not linger in experiments for more than six days (Fig. 2). Only eight live individuals were removed and consequently replaced during the course of experiments due to health concerns; four of these contained incomplete drillholes. Of the three clams found empty but undrilled, previous signs of poor health followed by evidence suggestive of decay were recorded for the clam in the 6 cm set-up, but not for the individuals in the 2 cm or 20 cm aquaria. Drilled bivalves were void of soft tissue upon recovery from aquaria; only one individual was documented as partially consumed with the remaining residue left to decay. Staining of recovered valves varied from heavy and complete to none (Fig.

3A). In general, staining was greater for shells located within the sediment. For instance, bivalves in 0 cm aquaria were not stained, regardless of whether individuals were consumed or remained unharmed, live, and healthy for the full 48 days. No shells were noted with moderate or heavy staining in only 1 cm of sediment, whereas shells at greater depths showed all levels of staining. In addition, greater staining was noted for shells with some soft parts remaining, and those for which more time had passed since death. Discoloration was not exhibited in live healthy clams except for a few rare instances near the end of the second trial. Incompletely drilled specimens very infrequently displayed stained patches.

DISCUSSION

Possible Suffocation Events

Our experiments indicate a lack of deaths by suffocation in Neverita duplicata consuming

Mercenaria mercenaria. Moon snails were mostly engaged in drilling upon being disturbed during experimental checks; very few were handling prey before drilling started and even fewer

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Figure 2. Residency of clams in experimental aquaria before being consumed by drilling for all substrate depths (all replicates combined).

90 0 cm 80 70 1 cm

60 2 cm

50 6 cm

40 20 cm

30 No. of Clams of No. 20 10 0 6 Days 12 Days 18 Days 24 Days 30 Days 36 Days 42 Days 48 Days

No. of Days in Tanks Before Consumed by Drilling

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Figure 3.

A. Two drilled prey from the experiments conducted in the fall. Note the date of entry and degree of staining from heavy and completely covered (left) to none (right). Nearly all drillholes recovered as part of this investigation were located at the umbo as is visible in these specimens.

B. Neverita duplicata drilling on the surface of the sand in the 1 cm set-up. The bivalve prey is visibly wrapped in the foot of the naticid. The proboscis is engaged as noted by the arrow.

C. Neverita duplicata preying on a Mercenaria mercenaria in the 0 cm aquarium. The position of the prey reflects stereotypical drilling of the umbonal region. Note the date of entry on the bivalve shell used to monitor duration of prey in experiments.

D. The recurrent behavioural display characterized as upside down and foot extended by a naticid in the 0 cm set-up. This behaviour was very rarely observed in moon snails exposed to aquaria containing substrate > 1 cm.

E. Evidence of scavenging by Neverita duplicata in a laboratory setting. This freshly killed Mercenaria mercenaria was offered as prey independent of the sediment depth experiments. Note the proboscis as indicated by the arrow. The naticid wrapped its foot around the prey and attempted to drag and bury with the specimen despite being open and recently dead.

A B C

D E

155 were in the process of consumption after borehole completion. Nearly all bivalves were drilled; only three specimens (<1%) were found empty without drillholes. Two of these non-drilled clams lacked signs of decay and may have been suffocated. One specimen, in the 20 cm aquarium, was discovered empty on the sediment surface after only three days. The other, in the

2 cm tank, was found on the surface at three days but with signs of gaping, perhaps indicating that weakness prevented it from burrowing. Three days later it was discovered empty with no drillhole. In both cases, poor prey health likely made the individuals susceptible to suffocation.

The other non-drilled individual showed clear evidence of decomposition and was probably not suffocated or scavenged. The latter interpretation is further supported by the observation that a naticid repeatedly ignored a decaying Mercenaria on the sediment surface in the 6 cm set-up. All three non-drilled deaths occurred during the first trial in the fall; four of the eight bivalves removed due to signs of deteriorating health were from that same trial.

The only other indication of potential suffocation is represented by a prey item that had lingered in the 20 cm set-up for 24 days before being drilled to completion, but then was not eaten due to interruption by an experimental check. Although the clam appeared healthy and was returned to the tank, a week later it was found empty within the sediment yet with no signs of decay. If the bivalve was in fact injured by the previous drilling attempt and gaped shortly after being enveloped by the naticid at the onset of a second attack, it may have been suffocated, eliminating the need for further drilling. Alternatively, the naticid may have been able to feed using the former drillhole.

The rarity of suffocation in our experiments contrasts with accounts of more frequent suffocation by Neverita duplicata in other laboratory studies (Table 3). For example, Aronowsky

(2003) reported that 16% of prey offered to N. duplicata were suffocated in laboratory

156 experiments (frequency of suffocation was much greater for the naticid Lunatia heros, at 54%).

Gould (2010), in a study of Neverita cannibalism in the presence of bivalve prey, reported that

4–17% of Mercenaria mercenaria in 12 aquaria were consumed without drilling and inferred that suffocation had occurred.

Influence of Sediment Depth on Suffocation

Overall, our experiments indicate that suffocation by Neverita duplicata is not linked to insufficient sediment. Two of the three possible instances of suffocation occurred in aquaria with

20 cm of sand, which exceeds their burrowing depth in the field as well as in this experiment; naticids were always found in the upper half of the sediment (usually in 8 cm of sand or less).

The results demonstrate that shallower sediment depths do not impede the capacity of Neverita duplicata to drill prey as long as at least 1 cm of sand is provided. Predators often attempted to bury themselves at least partially in the sediment, however, indicating that more substrate is preferred. Drilling occurred beneath the sediment, on the sediment (Fig. 3B), and in the absence of it (Fig. 3C). Prey were held underneath the snail in the 6 cm and 20 cm aquaria; less substrate forced naticids to drill while lying sideways or upside down with prey wrapped in the foot.

However, variation in drilling position as a result of different sediment depths did not impact predation mode, frequency of feeding, or stereotypy of drillholes, as nearly all penetrated in the vicinity of the umbo. Drillholes were evenly distributed among right and left valves in each set- up (51.2% R: 48.8% L for all depths combined).

Although shallower sediment depths did not seem to impact outcome of predation by

Neverita significantly, absence of sediment greatly affected predatory behaviour. Two of the naticids in our 0 cm set-up did not feed over the 48 days and mostly remained upside down on

157 the apex of their shell with their foot extended (Fig. 3D). This behaviour is not commonly observed if sand is provided; Bernard (1967) noted that such behaviour by naticids likely reflects undesirable conditions. These moon snails were stressed in the absence of sediment and showed no interest in available prey. Both naticids immediately reverted to infaunal behaviours, however, when placed in aquaria with sand at the conclusion of experiments. They burrowed promptly and drilled prey despite a nearly seven week hiatus from exposure to infaunal surroundings.

Insufficient sediment hindered feeding by naticids in other laboratory experiments

(Bayliss, 1986); nevertheless, some moon snails are capable of foraging in the absence of sand or if given an artificial substrate instead. For example, several authors used clear beads instead of sediment to facilitate viewing of infaunal behaviours (Bernard, 1967; Rodrigues, 1986;

Hasegawa & Sato, 2009); apparently naticids were not deterred by this altered substrate.

Kingsley-Smith et al. (2003) did not provide any substrate in aquaria for Euspira pulchella, but this unnatural state did not impact drilling on cardiid prey (contra Bayliss, 1986). Although sediment likely offers greater stability in handling of prey items, one of our Neverita regularly pursued and drilled clams in the absence of supportive sediment; however, fewer prey were consumed relative to most moon snails in aquaria with sand (22 prey compared to an average of

32 prey per predator in tanks with sediment). Upon conclusion of our sediment depth experiments, four additional Neverita were placed in aquaria lacking sand for additional observations. One individual quickly drilled several Mercenaria prey without difficulty; all others appeared fixated in the upside-down position with their foot extended.

Our results provide insight as to appropriate sediment depths for laboratory work on

Neverita duplicata, alleviating prior concerns that minimal sediment leads to suffocation of prey.

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However, other species may have different depth requirements (e.g., Huelsken et al., 2008) and may not respond in the same way if exposed to varying sediment levels in laboratory settings. In addition, predator size may influence the depth of sediment required for normal feeding behaviour; Kabat (1990) noted that most experiments offer only slightly more sand than the size of the predators or prey under observation. Appropriate substrate depths for prey species should be considered as well, especially for any that exhibit escape behaviours such as leaping or are large and have long siphons for deep burrowing within the sediment as discussed by Bayliss

(1986); extrapolation of laboratory observations to field settings may not be appropriate if artificial conditions do not reflect natural habitats. Rodrigues (1986) specifically commented on this matter, stating that reduced sediment likely altered normal foraging behaviours of

Glossaulax didyma on Venerupis philippinarum. Due to shallow depths of the laboratory set-up, moon snails were limited in their ability to attack prey from below as may occur under natural circumstances.

Other Potential Explanations for Laboratory Reports of Suffocation

The high frequency of suffocation of prey reported by Aronowsky (2003) and Gould

(2010) cannot be attributed to a lack of sediment. Depths of sand provided were more than sufficient for drilling by Neverita duplicata; >10 cm and 7 cm were used by Aronowsky, 2003, and Gould, 2010, respectively. Thus explanations other than absence of sediment are needed for alleged suffocation. Gould (2010) speculated that the presence of multiple predators in a confined area might lead to suffocation if extensive carrying of prey occurred due to a perceived threat from other naticids. Hutchings et al. (2010) also inferred that prey were suffocated in aquaria with multiple Neverita duplicata, and noted an increase in incomplete drilling, which

159 they attributed to interruptions by other naticids. This observation is consistent with the work of

Fregeau (1991), who found that, on several occasions, Neverita stole prey from other moon snails (both Neverita and Lunatia), and/or cannibalized the competing predators. Presence of multiple predators could be a factor influencing suffocation in the studies of Aronowsky (2003) and Gould (2010) and other studies as well (e.g., Ansell & Morton, 1985, 1987; Newel &

Bourne, 2012); hence in our experiments only single predators were utilized in each tank.

However, in both the work by Aronowsky (2003) and Gould (2010), suffocation was reported also in tanks containing only a single predator. In addition, suffocation during prey carrying seems unlikely for Neverita, as Aronowsky (2003) and Fregeau (1991) commented that prey carrying is much less common in Neverita than Lunatia. Prey carrying could have contributed to

Aronowsky’s high frequencies of suffocation by Lunatia, however, especially if prey exhibited poor health.

Effects of Prey Health

Because suffocation is not easily observed, empty shells that lack completed boreholes typically serve as evidence that suffocation has occurred. However, the condition of prey used in experiments is often not mentioned, so it is unclear in many cases if deaths attributed to suffocation are accidental by-products of poor prey health. Quality control and monitoring of prey are crucial to identify cases of natural mortality (as recognized by Ansell & Morton, 1985,

1987) or inadvertent suffocation of stressed prey. Our protocols limited poor prey health from influencing the outcomes of our experiments. However, prey health may have been an issue in the work by both Aronowsky (2003) and Gould (2010).

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High mortality of prey was noted as a problem early in the experiments of Aronowsky

(2003); prey reported as suffocated included species obtained at local fish markets, which were probably stressed before being utilized in experiments. Empty shells without drillholes in

Gould’s (2010) study could have been the result of weak prey that gaped during warmer summer months, allowing for feeding via the margin or, less likely, scavenging. Neverita duplicata avoids carrion (Kitchell et al., 1986; Fregeau, 1991), but consumes freshly injured (Edwards &

Huebner, 1977) or, albeit rarely, recently killed prey (Fig. 3E). However, carrion consumption is reported for several other species, including Lunatia heros (Gould, 1841; Ganong, 1889;

Fregeau, 1991; Kenchington et al., 1998; Grey, 2001). Although never observed by Aronowsky

(2003), scavenging following mortality of weak prey may have contributed to the high frequency of suffocation reported by Aronowsky for Lunatia. Natural mortality and decay cannot be discounted either, as complete decomposition could have occurred between Gould’s experimental checks (every two to three days), especially in conditions exceeding 25°C (Visaggi,

2012). Daily monitoring of tanks by Aronowsky (2003) limited concerns about bivalve decay, although decay rates may have been underestimated based on observations in sediment-free aquaria. Specimens found covered in mucus indicated consumption by naticids (see e.g., Ansell

& Morton, 1987), but preference for weakened prey in both predator species used by Aronowsky

(Wheatley, 1947; Edwards & Huebner, 1977) further promotes poor prey health as a cause of increased suffocation.

Studies that explicitly control for prey health seem to show lower frequencies of suffocation. We were able to minimize prey health as a concern by obtaining prey from hatcheries in the area, assessing the condition of prey before, during, and after experimentation, and monitoring the duration of prey used in aquaria. Because 75% of clams consumed by drilling

161 were preyed upon within six days, most individuals did not survive long enough to merit concerns regarding gradual deterioration of health. In addition, prior to use in experiments,

Mercenaria had access to food in flow-through holding tanks. Seawater changes offered a new source of food every six days, which should have been adequate to maintain prey that likely fed less actively in the presence of predators. Similarly, Edwards & Huebner (1977), Fregeau (1991), and Vencile (1997) used prey collected locally in their laboratory experiments, presumably offering greater control in quality and health, and did not report non-drilling deaths of Mya in studying foraging behaviour of the same predator species studied by Aronowsky (2003). Kardon

(1998) did not observe any alternate modes of predation by Neverita duplicata on Mercenaria mercenaria in long-term experiments that carefully monitored the prey offered.

The issue of prey health has been noted before by Kitchell et al. (1986) in proposing that

Medcof & Thurber (1958) incorrectly ascribed Mya arenaria deaths without drillholes to naticid predation instead of considering background mortality of experimental prey after being placed in the field. Although some authors have attributed undamaged shells to naticid predation in field settings (e.g., Wheatley, 1947; Vencile, 1997), others have regarded natural mortality or disease as the destructive agents (e.g., Turner, 1950; Edwards & Huebner, 1977). Most field experiments are conducted in the summer months; heat stress may be a contributing factor that allows naticids to feed on weakened prey without drilling in nature. These examples highlight the challenges in assessing how undrilled prey perish in the field; concerns regarding prey health are not limited to laboratory experiments in attempting to recognize alternate modes of predation by naticids.

Why Suffocation?

We suggest that suffocation is not a mode employed normally by naticids, but that it is largely

162 due to fortuitous events in laboratory settings. Resolving whether alternate modes of drilling are in fact problematic for interpreting patterns based on drillholes is essential. If suffocation by naticids is uncommon in nature, concerns regarding research that relies on drillholes are mitigated. However, if it is utilized as an alternate predatory mode, what contributing factors might lead to such use?

Drilling is a pervasive, but very slow, form of predation (Vermeij, 1987). Hours to days may be needed to complete a drillhole so that the proboscis can be inserted to feed (Boggs et al.,

1984). Suffocation, whether intentional or not, may be advantageous if it reduces prey handling time before feeding begins, even if drilling has already started.

The fact that different attack behaviours (i.e., drilling, non-drilling, anesthetizing mucus) may be employed in suffocation complicates cost-benefit analyses of this predatory method.

However, some evidence indicates that alternate modes of predation may reduce handling time.

For example, Hughes (1985) noted that Natica unifasciata needed at least 50 hours to drill and consume Nerita funiculata but that non-drilling predation on Olivella volutella (which he attributed to operculum wedging) only required 12 hours. Flesh yield per duration of handling indicated that avoidance of drilling dramatically increased profitability. Ansell & Morton (1987) did not observe consistently higher rates of feeding for prey consumed by Polinices mammilla via presumed suffocation, but predator and prey size were not discussed, which may affect relative profitability. They commented also that suffocation is unlikely to be advantageous in reducing handling times as many bivalves can withstand extended periods of oxygen depletion without gaping, but recognized that this may not hold for all prey.

Even if the act of predation is not shortened significantly by suffocation, it may be less expensive energetically than is drilling (Kabat, 1990) and should limit periods of rest needed for

163 repair of the radula due to wear (Reyment, 1999). Furthermore, suffocation might be advantageous in other ways, e.g., if a quarry were suffocated while being dragged as a naticid searched for further victims. Aronowsky (2003) proposed this explanation upon finding a large

Neverita duplicata carrying prey with incomplete drillholes on three occasions. She suggested that the naticid suspended drilling and “pocketed” the initial item, thereby maximizing foraging efforts by pursuing additional prey while suffocating the “pocketed” prey. However, interruptions caused by escaping prey or other naticids in aquaria may have produced the incomplete drillholes in pocketed prey, especially because two of three pocketed prey were conspecifics. Fregeau (1991) also reported pocketing of prey by Neverita on three occasions, but these items were later drilled and consumed.

The utility of suffocation may vary with specific predator-prey combinations and local environmental conditions. For example, Ansell & Morton (1987) found no clear pattern between the percentage of prey attacked by Polinices mammilla through supposed suffocation and characteristics such as surface ornamentation or shell thickness, yet certain prey (Venerupis philippinarum and Anomalocardia squamosa) were more frequently consumed in the absence of drilling. In part because larger naticids more often employed suffocation in their experiments,

Ansell & Morton (1987) postulated that the abundance of these co-existing species in the intertidal zone may have allowed for learning of this modified predatory strategy, based on discussions by Hughes (1985) regarding non-drilling predation on Olivella. To the contrary,

Boggs et al. (1984) demonstrated that naticids seem to be incapable of learning, although caution should be used in generalizing from single studies. Work on naticids occupying the same habitats

(Vermeij, 1980; Ansell & Morton, 1987; Fregeau, 1991; Aronowsky, 2003) suggests that preferential use of drilling vs. alternative behaviours by certain species might be related to niche

164 partitioning; however, it is unclear if such results can be applied to field settings as most of these observations are based on laboratory conditions.

One final consideration is whether suffocation is in fact aided by paralyzing toxins.

Although many authors have hypothesized that the mucus used to coat and immobilize prey may have anesthetizing properties, no numbing agent has been described yet with respect to moon snail secretions used during predation. Our experiments did not address specifically the role of anesthetizing mucus, though the paucity of unexplained deaths suggests that the mucus of

Neverita duplicata does not contain a narcotizing component. Venomous substances are commonly utilized by predatory gastropods for the capture of active prey (Taylor et al., 1980), but naticids have received little attention in this matter. Reports of suffocation by volutid gastropods are now questionable, as recent research has revealed that prey can be narcotized via salivary glands and consumed alive instead (e.g., Bigatti et al., 2010). More research is needed as to whether suffocation is the actual mechanism responsible for mysterious deaths by naticids; an area of potential research is the role of the neurotoxin TTX (tetrodotoxin) in predation by naticids.

Neurotoxins are reported in several naticids from the Indo-Pacific, as a result of research on shellfish poisonings in humans (Hwang et al., 2007). Tetrodotoxin, produced by marine bacteria, is documented in a variety of organisms and accumulated as ingested through diet at multiple trophic levels in the marine realm. Because TTX-bearing gastropods are strongly attracted to concentrations of TTX, Hwang et al. (2004) suggested that this neurotoxin may serve as a defense or attack strategy for such species. Although TTX is found mostly in the muscle or digestive glands of naticids, Tanea lineata demonstrated an ability to release seawater yielding acute paralytic toxicity in response to external stimulation, i.e., removal from aquaria (Hwang et

165 al., 1990). It is interesting to note that TTX is found in Polinices mammilla and Glossaulax didyma, both reported to suffocate prey; use of TTX in alternate modes of predation by these naticids warrants investigation.

Susceptible Prey

We found suffocation of Mercenaria mercenaria to be extremely infrequent in our experiments.

Mercenaria mercenaria has a moderate metabolic rate and may be able to withstand lower oxygen conditions (Savage, 1976), perhaps in part responsible for the low incidence of suffocation observed here. Nevertheless, recurrent documentation of suffocation in M. mercenaria occurs in laboratory settings (Table 3). Based on our results, we argue that apparent suffocation of Mercenaria and possibly other bivalves under experimental conditions may be due to poor prey health. Reports of suffocation are common for commercially important venerid bivalves, which often are used as experimental prey. Such venerids are easier to obtain in large batches for use in experiments, and bulk purchases are more likely to include empty shells and weakened individuals, perhaps leading to more instances of perceived suffocation. Although we propose that many deaths interpreted as suffocation by naticids are a consequence of unhealthy or weakened prey due to the presence of parasites or stressful holding conditions, we recognize that not all instances of suffocation may be attributed to this problem. Our experiment involved a single prey species with tightly closing valves and moderate metabolism. Other prey may be more susceptible to suffocation.

Naticid prey that may be particularly subject to suffocation include bivalves with a permanent gape and gastropods. Although it is often unclear from the literature whether such prey are suffocated or attacked directly via a natural opening, reports of prey consumed despite

166 incomplete boreholes imply that suffocation may have led to abandonment of a drillhole for easier feeding through the margin or aperture. Christensen (1970) reported that there is an inverse correlation between size of the gape and oxygen tolerance in bivalves, suggesting that widely gaping bivalves are likely more susceptible to suffocation. Incomplete drillholes noted in empty individuals of the slightly gaping Saxidomus giganteus in experiments by Bernard (1967) may suggest vulnerability to suffocation even for narrowly gaping bivalves. Indeed, some of the prey species reported as suffocated in the literature have slight gapes (Table 3). Gastropods that can be attacked through the aperture may also be more easily suffocated. For example, Edwards

(1969) noted that, of 21 Olivella biplicata consumed in laboratory experiments, only 19% were completely drilled; 67% had incomplete drillholes and 14% remained undrilled. Deaths were mostly attributed to suffocation as opposed to operculum wedging, due to the presence of incomplete drillholes.

Bivalves that gape fortuitously in laboratory settings before or during drilling due to an inability to handle restricted access to oxygen are likewise susceptible to suffocation. Ansell &

Morton (1987) proposed that incomplete drillholes in Venerupis philippinarum may be related to oxygen requirements; Day (1980) reported that this species gaped after only a few hours of emersion. Suffocation of this prey species under laboratory conditions was noted also by

Aronowsky (2003) and Newel & Bourne (2012). On the other hand, Hughes (1985) remarked that oxygen depletion limits for Olivella exceeded the duration required for drilling and instead concluded that prey suffered from forced entry through the flimsy operculum. Because the ability to endure lower oxygen concentrations is most often inversely correlated with metabolic rate

(Christensen, 1970), taxa with faster metabolisms may be more prone to suffocation (e.g., highly active prey such as Spisula). Weissberger & Grassle (2003) noted that only larger Spisula

167 individuals, albeit presumably with reduced metabolic requirements (Ricklefs, 1973), were suffocated. Suffocation of large prey has been reported also by Ansell & Morton (1987) for

Venerupis and Friend (2011) for Mercenaria, indicating that prolonged handling of oversized prey merits consideration in susceptibility to suffocation.

If existing gape and anaerobic capacities are factors in susceptibility to suffocation, species able to remain sealed for very long periods should be exclusively drilled. Vermeij (1980) noted this in experiments on bivalves in Guam, in that lucinids were always drilled as opposed to other species apparently expiring from suffocation. Although his comments are based on only 11 observations, high anaerobic capacities of the Lucinidae (e.g., Jackson, 1973) support his speculation. Drilling on lucinids is pervasive in modern and fossil assemblages globally (see compilation by Kabat, 1990); suffocation is not reported in laboratory studies of naticid predation on lucinids (Vermeij, 1980; Ishikawa & Kase, 2007). However, lucinids are not frequently used in predation experiments, likely influenced by the fact that other bivalves of commercial importance are more readily available to use as prey.

Latitudinal Predictions

Although Kabat’s (1990) summary suggested that suffocation was restricted to warm waters of the Indo-Pacific, reports of suffocation extend across multiple latitudes and include species found along both major coastlines of North America (Tables 2 & 3). Information on feeding behaviours in modern naticids is limited, however, and data are lacking for the majority of extant species (Aronowsky, 2003). Yet, if suffocation is indeed a real phenomenon and cannot be attributed solely to poor prey health, can any predictions be made as to where it is likely to be

168 employed, based on the susceptibility of specific prey or the potential advantages of or behaviours utilized in suffocation by predators?

Vermeij & Veil (1978) reported that frequency of bivalves with natural gapes increases poleward, reflecting decreased predation pressure moving away from the equator. If gapers are more prone to suffocation, greater frequencies may be expected at higher latitudes, particularly as drilling is even slower in cooler environments. However, if suffocation enhances efficiency of predatory attacks, it might be more useful in lower latitudes due to high levels of competition as well as the heightened risk for moon snails to become prey to their own predators. Toxins that may aid in suffocation are more likely to be found at lower latitudes; shell entry assisted by anesthetization is more commonly developed among tropical predators (Vermeij et al., 1989). In addition, Vladimirova et al. (2003) noted that energy metabolism of most bivalve families (with the exception of venerids and mactrids) is greater at lower latitudes, which may increase susceptibility to suffocation. Tropical accounts of suffocation also may be related to edge drilling, as suggested by Ansell & Morton (1987) based on very slight chipping sometimes observed on the shell margin.

Palaeontologists have focused recently on analyzing latitudinal trends in drilling by naticids, because evolutionary patterns of predation must be interpreted in light of geographic variation. No consensus yet exists regarding latitudinal variation in drilling frequency; peaks in drilling are reported poleward, equatorward, or at mid-latitudes based on modern and fossil shell deposits (for a review, see Kelley & Hansen, 2007). However, if alternate forms of predation by naticids are common in nature, understanding the latitudinal context of these modes is needed for interpreting spatial patterns based on drillholes. Anecdotal suffocation by Lunatia under laboratory conditions initially guided Kelley & Hansen (2007) to propose that this strategy may

169 account for decreased drilling at higher latitudes; based on the present study, it is unclear whether such reports can be substantiated in light of concerns regarding prey health and extrapolated to natural settings. Furthermore, suffocation of prey noted in laboratory experiments is widespread latitudinally, perhaps indicating that alternate predation modes may contribute to lower drilling at warmer latitudes instead, especially if toxins are involved. Confirmation of alternate modes is needed before a lack of drilling can be attributed to such strategies based on laboratory observations.

Interpretation of Incomplete Drilling

Incomplete drillholes have been considered as evidence of unsuccessful predation attempts in fossil and Recent shell accumulations (e.g., Vermeij, 1987; Kelley & Hansen, 2003), as discussed further below. However, incomplete drillholes in several laboratory studies have been linked instead to abandonment of drilling during suffocation and thus represent successful predation (Table 3). In the present study, incomplete drillholes resulted from interruptions in drilling, which occurred primarily due to experimental checks but may have occurred during water changes as well. Interruptions were most common at the shallowest depths of 1 cm and decreased in frequency as depth of sand increased. Nearly all prey with incomplete drillholes were successfully redrilled regardless of the amount of substrate provided (including the 0 cm set-up). Tracking of incomplete boreholes revealed that subsequent drilling occurred in both valves, with 22 instances in the opposite valve vs. 24 occurrences in the same valve (21 of which coincided completely with earlier incomplete drillings such that incipient attempts were no longer visible). Although Kitchell et al. (1981) reported that reoccupation of an existing perforation rarely occurs, 44.7% of incomplete holes in our specimens were later replaced by

170 complete boreholes and four holes that were complete but not yet sufficiently widened for feeding were subsequently redrilled, as later observations revealed expanded inner diameters.

Moon snails may not be able to identify the location of a previous drillhole, but because of their stereotypic handling of the prey, chance may yield an attack in the same location, especially in laboratory settings where predators readily encounter prey that were attacked previously. The likelihood of a naticid encountering and redrilling previously attacked prey in natural settings should be substantially less.

Palaeontological Implications

The Naticidae originated as part of the Mesozoic Marine Revolution – a dramatic diversification of predators in the marine realm (Vermeij, 1977; Harper, 2003; Kelley & Hansen, 2003). The history of naticid gastropod predation is interpreted largely from calculations of drilling frequency, normally defined as the percent of prey individuals with complete drillholes. The presence of incomplete drillholes has been used to identify failed predation attempts and thus to infer the relative effectiveness of predators and prey. Most palaeontologists have not considered alternate means of predation in studies of evolutionary patterns of naticid predation, such as tests of the hypotheses of escalation and coevolution based primarily on drillholes (e.g., Vermeij,

1987; Kelley & Hansen, 1993, 2003; Dietl & Alexander, 2000). However, if such methods are regularly employed by moon snails, using only drillholes to infer levels of naticid predation could lead to 1) underestimation of mortality due to naticid predation in both modern and fossil deposits (Vermeij, 1980; Ansell & Morton, 1987; Leighton, 2002) as well as 2) incorrect interpretation of incomplete drillholes, as mentioned in the preceding section, and thus estimates

171 of prey effectiveness, i.e., the adaptive gap between predator and prey (Ansell & Morton, 1987;

Kowalewski, 2004; Hutchings et al., 2010).

Mortality due to naticid predation may be underestimated for fossil bivalve prey with permanent gapes (Stump, 1975; Schneider, 1982; Frey et al., 1986), whereas non-gaping prey are more difficult to recognize as susceptible to alternate modes of predation such as suffocation.

Identifying fossil prey vulnerable to suffocation by analyzing morphology or oxygen depletion limits of extant relatives could be useful; focusing on prey apt to reflect predation intensity accurately (e.g., lucinids) might be preferred. However, if most modern accounts of suffocation in tightly closing bivalves can be discounted as a result of weak prey in laboratory settings, as we have argued here based on our experiments, palaeontologists need not be concerned that drilling frequencies underestimate predation mortality.

Incomplete drillholes in Recent and fossil prey are usually perceived as predatory attacks that are unsuccessful (Vermeij et al., 1989; Kelley & Hansen, 2003), resulting from interruptions during drilling, ability of the prey to evade predation, or attempted handling of oversized victims

(Kitchell et al., 1981; Kelley, 1988; Kitchell et al., 1986). Presence of conchiolin layers within the prey shell has also been discussed as a deterrent to drilling, yielding incomplete drillholes in some corbulid and lucinid bivalves (Kardon, 1998; Anderson, 1992; Ishikawa & Kase, 2009).

However, several authors have reported that prey can be consumed despite the presence of incomplete drillholes. Such partially completed boreholes have been used to infer suffocation in gaping prey (as implied by the results of Bernard, 1967), gastropods (Edwards, 1969), and bivalves with tightly closing valves (Ansell & Morton, 1987; Aronowsky, 2003; Grey, 2001;

Friend, 2011; Newel & Bourne, 2012). Reports of suffocation are especially common for larger bivalves (e.g., Ansell & Morton, 1987; Weissberger & Grassle, 2003; Friend, 2011), suggesting

172 that interpretation of incomplete drillholes may be problematic in larger fossil and Recent prey.

Incomplete drillholes could represent failed attempts in drilling, successful suffocation, or merely the fortuitous death of weak prey before drilling ended. Our results demonstrate that carefully controlling prey health limits accounts of suffocation, alleviating concerns regarding the interpretation of incomplete drillholes in the fossil record and in Recent assemblages.

The evolutionary history of suffocation is unclear. The origin of naticids and their shell- drilling behaviours before the Cretaceous has been controversial (Sohl, 1969; Fürsich and

Jablonski, 1984; Kowalewski et al., 1998; Kase & Ishikawa, 2003; Aronowsky & Leighton,

2003), in part due to the temporal offset in purported drillholes attributed to naticid gastropods and appearance of the group in the Mesozoic, as well as the occurrence of non-drilling behaviours by modern moon snails. Ansell & Morton (1987) postulated that non-drilling predation preceded the evolution of drilling in the Naticidae, but mentioned that it might be a secondary development in Recent species. Aronowsky (2003) proposed that both suffocation and drilling evolved multiple times based on phylogenetic work and further suggested that increases in predation intensity through time may represent a shift in the dominant form of naticid predation from suffocation to drilling.

Several factors may have influenced the evolution of suffocation by naticids. Natural selection would be unlikely to favor suffocation if it is slower or more expensive energetically than drilling. If suffocation is faster than drilling, it could be favored by natural selection in highly competitive settings (see Dietl et al., 2004, for an analogous argument concerning edge drilling). However, a predator exerts less control over predation success in suffocation, in which success depends more on prey respiration rates, than in drilling. All else being equal, natural selection should favor active behaviours that are predictable (e.g., drilling time-prey shell

173 thickness relationships are predictable); instead of those in which outcomes are less certain (e.g., suffocation). An exception may be suffocation that is aided by toxicity, as drilling is likely more expensive and slower than use of paralyzing secretions; our results did not indicate use of toxins by Neverita duplicata.

Our work suggests that instances of suffocation simply may be a fortuitous by-product of unhealthy prey or other artificial aspects of laboratory experiments. If so, suffocation by naticids should not be a concern for palaeontologists. Teasing apart multiple mechanisms of alternate naticid predation requires clever experimentation, which will be essential for examining alternate modes of predation employed by naticids within an evolutionary framework.

CONCLUSIONS

Despite exhibiting stereotypic behaviours useful for studying ecological and evolutionary aspects of predator-prey interactions, naticid gastropods are reported as utilizing alternate predatory behaviours. Drilling remains the dominant mode of predation executed by naticids; suffocation may be a result of poor prey health in laboratory settings. Our work indicated a lack of suffocation by Neverita duplicata on Mercenaria mercenaria; 99% of consumed prey were drilled. Different sediment depths did not impact predation by drilling or frequency of feeding except in the absence of any sediment.

Although our data indicate that shallower substrates do not impact predation by drilling, we recognize that only a single predator and prey species are examined here. We offer the following recommendations for future work on alternate modes of naticid predation in laboratory settings.

1) Tank space and substrate depths should be considered with respect to predator and prey sizes,

life habits, and any attack, burrowing, or escape behaviours.

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2) Naticid predators should be isolated and prey abundance controlled and monitored.

3) Prey health must be assessed initially and throughout experimental work. Analyzing

background mortality levels during the course of experiments can be useful; setting up

separate aquaria exposed to the same conditions is recommended. Mortality may be

particularly high in warmer months or if prey are not obtained from local habitats.

4) Dates of entry can be marked on prey for monitoring length of exposure to experimental

conditions. Examining decomposition rates and recording observations of decay can

minimize incorrect attribution of deaths to scavenging or suffocation.

5) Frequent monitoring limits difficulties in interpreting questionable deaths. Time lapse

photography is further recommended to reduce inaccurate reports of putative suffocation.

Although careful control of laboratory conditions may minimize false reports of suffocation by naticids, in some cases alternate modes of predation may be real. To better understand the extent and execution of alternate predatory modes, research in the following areas is needed: oxygen limits of prey, feeding behaviours for naticids not yet studied including scavenging, emergent effects due to multiple predators and especially other Naticidae, and the role of mucus secretions, particularly in regards to neurotoxins such as TTX. Understanding alternate modes of predation by naticids requires enhanced collaboration among malacologists, ecologists, physiologists, biochemists, and palaeontologists.

Lastly, we advise caution in documenting alternate naticid predation and applying terminology to mortality of the prey. Terms such as “smothering” are ambiguous and should be abandoned; “non-drilling predation” is not inclusive of all alternate predatory behaviours.

Examining literature accounts of alternate modes of naticid predation is challenging as potential confounding variables are often not reported (e.g., predator-prey sizes, aquaria set-up, frequency

175 of monitoring, prey health, density of predator and prey individuals). Validation of alternate predatory modes is needed in light of these concerns for several species of moon snails before questioning the quality of data provided by beveled drillholes in modern and fossil shell assemblages used in studies of evolution.

ACKNOWLEDGMENTS

This project resulted from research started as part of the National Science Foundation Research

Experience for Undergraduates program awarded to P. Kelley and G. Dietl (Grant No. EAR-

0755109). Specimen collection, laboratory experiments, and literature review were completed by

C. Visaggi in partial fulfillment of PhD requirements at the University of North Carolina

Wilmington. G. Dietl provided the experimental design; all authors contributed to data interpretation and writing of the manuscript. Funding for writing of the dissertation was provided by a Ford Foundation Fellowship and Association for Women Geoscientists Chrysalis

Scholarship. B. Parnell and D. Friend are valued for support in both the lab and field. E. Gould,

M. Grey, M. Newel, G. Bourne, and E. Weissberger graciously shared data from their work.

Translation guidance provided by C. Janot and J. Nagel-Myers is greatly appreciated.

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CHAPTER FIVE: SYNTHESIS

Understanding patterns and processes that operate over broad spatial and temporal scales has become increasingly important in addressing large-scale environmental problems impacting global habitats and the species therein (Sanford & Bertness, 2009). Local studies have offered insight into the dynamics of marine ecosystems and the importance that factors such as predation have on communities (e.g., Menge, 1976), but how these results scale up in space or time remains unresolved (e.g., Bennington et al., 2009). Examination as to how abiotic and biotic variables influence species interactions over larger latitudinal gradients is desired; a combination of non-experimental and experimental approaches within an interdisciplinary framework is recommended (Sanford & Bertness, 2009). The role of species interactions in evolution has also been debated (Jablonski & Sepkoski, 1996; Jablonski, 2008). Study of escalation (Vermeij,

1987) in the fossil record is impeded by the limited availability of outcrops, requiring the incorporation of greater spatial coverage to achieve a long-term view of patterns in predation.

Recognizing the potential effects of geographic differences on temporal patterns in gastropod drilling predation from paleontological assemblages is challenging and requires improved knowledge of spatial variation in naticid drilling. Modern marine communities offer an opportunity to examine trends in predation and processes influencing these patterns; results can be used to interpret paleontological patterns. My dissertation research explored patterns and processes affecting latitudinal variation in naticid gastropod drilling predation with implications for evolutionary paleoecology as well as macroecology. A brief review of the results from each research project conducted as part of my dissertation is presented here, followed by a discussion of how these data relate to existing hypotheses regarding latitudinal variation in drilling predation and work on latitudinal gradients in species interactions in general.

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The results of Chapter Two indicated that contemporary drilling patterns in Western

Atlantic molluscan faunas of the Southern Hemisphere did not mirror the mid-latitude peak reported in the Northern Hemisphere by Kelley & Hansen (2007). Increased drilling was documented equatorward at the assemblage level and for several lower taxa, with no change in interpretation upon size-standardization, habitat-restricted analysis, or the exclusion of certain sampling methods. Field and laboratory experiments in Chapter Three confirmed the existence of differences in drilling across seasons but demonstrated that fluctuations did not correlate directly to seasonal changes in temperature. Fall had greater drilling compared to spring despite higher temperatures in the spring season in both sets of experiments. Field and laboratory results yielded divergent patterns in drilling for the summer only, most likely attributable to heat stress and greater incidence of crushing predation in the field. Work in Chapter Four revealed that shallow sediment depths did not lead to alternate modes of predation in a laboratory setting for

Neverita duplicata; poor prey health may explain multiple prior accounts of naticid suffocation reported in the literature.

Latitudinal patterns in drilling may be influenced by a host of physical and biological variables. Temperature represents a significant abiotic factor affecting predation, in part through its effects on metabolic rate. Temperature also determines ease of CaCO3 precipitation and thus prey defenses. Other factors that may vary with latitude include abundance and diversity of drilling predators and their enemies, as well as alternate modes of naticid predation (e.g., suffocation). Trends in drilling expected with latitude vary depending on the factor considered; several latitudinal hypotheses are discussed below with respect to the data obtained as part of this dissertation.

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Temperature is the abiotic variable most directly correlated with latitude, and metabolic rates vary significantly with temperature. The hypothesis that higher metabolic rates of predators should lead to increased drilling at lower latitudes was supported by my field collections in

Brazil as well as seasonal experiments conducted in the laboratory setting. Temperature greatly impacted frequency of feeding; summer data revealed the highest levels of drilling in the laboratory. However, absence of drilling in my summer field experiments indicates that other variables affect drilling patterns in the natural setting, at least over small spatial scales.

Temperature effects on feeding are usually examined in laboratory experiments, although some field studies have indicated that temperature plays a role in geographic variation in predation

(Sanford & Bertness, 2009). Temperature restricts the distribution of many organisms; latitudinal gradients in temperature can modify the outcomes and rates of species interactions

(Leonard, 2000; Cossins & Bowler, 1987). However, supposedly predictable factors including temperature may still show complex spatial variation as obscured by other variables such as the timing of the tides (Helmeth et al., 2002). Additionally, even if expected temperature gradients are present, differences in diversity and abundance of predators and prey may produce spatial variation in species interactions (Paine, 1974, 1980; Menge et al., 2004; Sanford et al., 2003).

Community dynamics can be influenced by variation not only in temperature, but also light, desiccation, salinity, nutrients, and other environmental stressors (Travis, 1996). Thus both the biological context and environmental setting can regulate predator-prey interactions. My results demonstrated that seasonal variability in drilling could not be attributed solely to temperature, but that other factors, both abiotic and biotic, contributed to fluctuations in drilling.

Most investigations of the effects of changes in temperature and seasonality on geographic variation in predation have been conducted in intertidal settings, including this

187 dissertation, where environmental stressors may be accentuated. Additional work in other habitats more applicable to studies in the fossil record would be beneficial, as most paleontological deposits reflect shallow subtidal environments. Furthermore, research is needed to examine the contribution of temperature and seasonality to time-averaged fossil assemblages used in studies of drilling predation. Because degree of seasonality varies with latitude, and predatory interactions vary by season (e.g., Paine, 1963), latitudinal patterns in drilling may be impacted by a confluence of abiotic and biotic factors related to seasonal changes. It is additionally essential to resolve whether the effects of seasonality and temperature covary with latitude; use of predictive modeling could improve the understanding of any effects that spatial variation may have on interpreting temporal trends.

Temperature may also affect drilling predation, in that calcium carbonate precipitates more easily in warmer waters, facilitating construction of highly armored shells. Indeed,

Vermeij (1978, 1993, 2004) documented that prey are better defended against predators among lower latitudes. Based on this observation, fewer complete drillholes (and more failed attempts) would be expected at lower latitudes. The equatorward increase in successful drilling observed in my assemblages from Brazil did not support this hypothesis; data on incomplete and multiply bored specimens were limited, preventing meaningful analysis. To the contrary, Kelley &

Hansen (2007) found support for this hypothesis in documenting less drilling and greater failed attacks among lower latitudes of the U.S. East Coast from a peak at mid-latitudes. However, a decline in drilling was observed poleward from the Carolinas as well. Neither Kelley & Hansen

(2007) nor this dissertation examined latitudinal trends in morphological traits, such as shell thickness or ornamentation, that might deter predators (yet latitudinal trends in Brazil were also observed in several lower taxa, for which ornamentation was consistent across latitude).

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Although a negative correlation between latitude and frequency of defenses against shell- crushing predation is documented in the literature (e.g., Vermeij, 1978; Zipser & Vermeij, 1978;

Palmer, 1979), less work has been done on traits resistant to drilling predation, which could be an area of fruitful future research.

Greater intensity of predation on gastropods by shell-crushers has been reported in tropical intertidal environments relative to temperate settings (e.g., Bertness et al., 1981; but see

Ortega, 1986). Although small-scale variation is not uncommon within habitats or regions (Heck

& Wilson, 1987), most studies have found support for increased predation pressures at lower latitudes (e.g., Menge & Lubchenco, 1981; Peterson et al., 2001). If interference is greater in the tropics due to increased predatory interactions, either reducing foraging by naticids or yielding more frequent interruptions, successful drilling should be less common but with greater occurrence of incomplete boreholes or multiple attempts as proposed by Vermeij (1993) and

Kelley & Hansen (2007). Data collected from Brazil did not support this hypothesis as the greatest successful drilling was observed equatorward. This hypothesis can be evaluated also using the results from my seasonality experiments. Laboratory work did not expose moon snails to enemy pressures from other predators or competitors; however, experiments in the field allowed for such interactions. If summer temperatures reflect warmer waters characteristic of the tropics year-round, lack of drilling and greater intensity of crushing predation observed during the summer field season provide support for this hypothesis instead. In addition, crushing and drilling predation were inversely correlated across seasons. Decreased drilling and greater failed attempts noted at lower latitudes along eastern North America by Kelley & Hansen (2007) lend support to this hypothesis as well, although a similar decrease poleward from a mid-latitude peak

189 in drilling along the Carolinas is not likely due to heightened predatory interactions, which are atypical at higher latitudes.

Latitudinal patterns in drilling could be influenced also by alternate modes of predation if occurrences of such behaviors are concentrated geographically. For instance, bivalves with a permanent gape may be more susceptible to suffocation or direct entry in which no drillhole would be left behind. In this case, greater drilling should be observed equatorward, as the frequency of gaping bivalves increases poleward (Vermeij & Veil, 1978). However, gaping bivalves are less common and probably do not exert a major influence on overall latitudinal patterns. Conversely, elevated metabolic rates of prey at warmer temperatures might leave them more prone to suffocation in the tropics. Lower drilling equatorward and increased failed attempts should be expected based on this hypothesis. However, my assessment of alternate modes suggests that suffocation reported in laboratory settings may not reflect natural field behaviors but could be due to poor prey health instead. Although suffocation reported in tropical environments might be accompanied by paralyzing toxins, more work is needed to understand whether these toxins in fact aid in naticid predation. Toxins are not known in naticids from

Brazil and greater drilling at lower latitudes did not support this hypothesis. Suffocation is likely unimportant in interpreting latitudinal trends in naticid predation, as multiple accounts based on tightly closing bivalves may be attributed to laboratory effects.

No consensus yet exists on latitudinal variation in drilling predation and data obtained in different parts of this dissertation offered support for contradictory hypotheses. In examining the importance of biotic interactions with respect to evolutionary hypotheses regarding latitudinal diversity gradients, Schemske et al. (2009) discussed that biotic interactions may be more important in the tropics, whereas abiotic factors may be more influential in temperate habitats.

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Similarly, abiotic and biotic factors may have different impacts on the intensity of drilling along latitude, adding to the challenges of interpreting and understanding latitudinal trends. My experiments imply that both biological and physical variables affect drilling predation locally, but how these processes scale up and characterize broad patterns in drilling is unresolved. In addition, whether abiotic and biotic processes that impact drilling are preserved in time-averaged shell assemblages from which drilling patterns are defined requires further investigation.

Modern ecosystems have utility in exploring these questions with implications for patterns of predation in the fossil record; improved spatial coverage of patterns in drilling is needed.

Sanford & Bertness (2009) state that “latitudinal gradients in species interactions may be more complex than originally imagined” (p. 383). Studies of local processes are often not able to account for all of the variation exhibited among communities over broader scales (Brown, 1995).

Additionally, species interactions may operate at different spatial scales within a hierarchical framework (Ricklefs, 1987; Hutson, 1999). Hence, investigations that explore large-scale patterns in species interactions and their potential abiotic and biotic causes through comparative experimental work, large-scale surveys, and/or modeling are particularly useful. Such interdisciplinary, multifaceted approaches will improve knowledge of geographic variation in species interactions in the past, present, and future.

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