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
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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
Eastern Brazil 10135 0.1105 Rio Grande 4771 0.0021
PROVINCE TOTAL 15021 0.1246 PROVINCE TOTAL 8832 0.0489
25
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).
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Brazilian Argentinean
NE Brazil E Brazil SE Brazil Rio Grande
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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
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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
28
Figure 4. Taxon-level variation in drilling frequency across provinces a) including all data and b)
restricted to size-standardized data.
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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).
30
Figure 5. Taxon-level variation in drilling frequency across ecoregions a) including all data and
b) restricted to size-standardized data.
0
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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
32
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
33
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
34
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.
35
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
36
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
37
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
38
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
39
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.
40
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).
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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
42
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
43
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
44
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.
45
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.
46
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
47
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-
48
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
49
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).
50
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
51
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
52
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
53
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
54
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
55
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.
56
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
0.05
0.1
0.15
0.2
0.25
0.3
0.35
-45 -35 -25 -15 -5 5 15 25 35 45
Dri
llin
g Fr
equ
ency
(Northern Hemisphere) Latitude (Southern Hemisphere)
EQ
UA
TO
R
57
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
58
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
59
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
60
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
61
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
62
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
63
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
64
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
65
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)
66
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
67
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.
68
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York.
Absalão, R.S., 1989. Padrões distributivos e zoogeografia dos moluscos da plataforma
continental Brasileira. Parte III. Comissão oceanográfica Espírito Santo I. Mem. Inst. Osweldo
Cruz. 84, 1–6.
Absalão, R.S., 1991. Environmental discrimination among soft-bottom mollusc associations off
Lagoa dos Patos, south Brazil. Estuar. Coast. Shelf Sci. 32, 71–85.
Aguirre, M.L., 1993. Palaeobiogeography of the Holocene molluscan fauna from northeastern
Buenos Aires Province, Argentina: its relation to coastal evolution and sea level changes.
Palaeogeogr. Palaeocl. 102, 1–26.
Aguirre, M.L., Donato, M., Richiano, S., Farinati, E.A., 2011. Pleistocene and Holocene
interglacial molluscan assemblages from Patagonian and Bonaerensian littoral (Argentina, SW
Atlantic): Palaeobiodiversity and palaeobiogeography. Palaeogeogr. Palaeocl. 308, 277–292.
Aguirre, M.L., Farinati, E.A., 1999. Paleobiogeografía de las faunas de moluscos marinos del
Neógeno y Cuaternario del Atlántico suboccidental. Rev. Soc. Geol. España. 12, 93–112.
Alexander, R.R., Dietl, G.P., 2001. Latitudinal trends in naticid predation on Anadara ovalis
(Bruguière, 1789) and Divalinga quadrisulcata (Orbingy, 1842) from New Jersey to the Florida
Keys. Am. Malacol. Bulletin. 16, 179–194.
Allmon, W.D., Nieh, J.C., Norris, R.D., 1990. Predation in time and space revisited: drilling and
peeling in turritelline gastropods. Palaeontology. 33, 595–611.
Balech, E., 1954. Division zoogeografica del litoral sudamericano. Rev. Biol. Mar. 4, 184–195.
Benkendorfer, G., Soares-Gomes, A., 2009. Biogeography and biodiversity of gastropod
molluscs from the eastern Brazilian continental shelf and slope. Lat. Am. J. Aquat. Res. 37, 143–
159.
Boschi, E., 2000. Species of decapod crustaceans and their distribution in the American marine
*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.
102
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 Type
Naticid Species & Size
Prey & Size Temperatures & (Clams Eaten Per Day)
Time of Year Location Reference
Field - Caged Lunatia lewisii 72.4–95 mm
Venerupis philippinarum Protothaca staminea Nuttalia obscurata >38 mm
NP (0.09) May–September BC, Canada
Cook & Bendell-Young (2010)
Field - Caged Lunatia lewisii 89.3–95 mm
Protothaca staminea 10–65 mm
18°C (0.06) 6°C (0.014)
Summer & Winter BC, Canada
Peitso et al. (1994)
Lab - Flow Through
Euspira pulchella 4–15.9 mm
Cerastoderma edule 2–16 mm (H)
4–18°C (0.12–0.50) February–November
Wales Kingsley-Smith et al. (2003a)
Lab - Controlled
Lunatia heros (Various)
(Mixed) 19–24°C (0.13) NA: June–October CA, USA Aronowsky (2003)
Glossaulax reclusiana CA & OR, USA Olivella biplicata Olivellidae n/a Inc Both* Edwards, 1969
Lunatia heros
NB, Canada Mya arenaria Myidae Y Un, Inc Shells Thurber, 1949; Medcof & Thurber, 1958
NS, Canada Mya arenaria Myidae Y Un Both Wheatley, 1947
PE, Canada Spisula solidissima Mactridae S Un Obs Wheatley, 1947; Medcof & Thurber, 1958
ME, USA Mya arenaria Myidae Y Un Shells Vencile, 1997
Lunatia triseriata NS, Canada Mya arenaria Myidae Y Un Both Wheatley, 1947
ME, USA Mya arenaria Myidae Y Un Shells Vencile, 1997
Lunatia lewisii
BC, Canada Tresus nuttallii Mactridae Y Un Obs Grey, 2001
BC, Canada Saxidomus giganteus
Veneridae S Un, Inc Both* Bernard, 1967
WA, USA Tresus nuttallii Mactridae Y Un Obs Reid & Freisen, 1980
WA, USA
Mya arenaria Myidae Y Un Obs
Agersborg, 1920
Protothaca staminea
Veneridae N Un Obs
Clinocardium nuttallii
Cardiidae N Un Obs
Neverita duplicata
MA, USA Ensis directus Pharidae Y Un Shells Edwards, 1974
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
138
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 Taxon
Size Collected (Exp)
Prey Taxon Prey Size
Prey Family % #/Total Gape Un/ Inc
Sed Depth
Monitored Reference
Conuber melastoma
~27.5 Hong Kong
Venerupis philippinarum
20–40 Veneridae 13% 3/23 N Un SL daily Ansell & Morton, 1985
Glossaulax didyma
47–52 Hong Kong
Venerupis philippinarum
30–39 Veneridae 50% 8/16 N Un, Inc
SL daily Ansell & Morton, 1987
Anomalocardia squamosa
Veneridae 78% 7/9 N Un
Atactodea striata
n/p Mesodesmatidae 25% 1/4 N Un
Coecella chinensis
Mesodesmatidae 13% 3/23 N Un
Glauconome chinensis
Glauconomidae 57% 4/7 N Un
Glossaulax reclusiana
~29.5 CA & OR, USA
Olivella biplicata
18–28 Olivellidae 81% 17/21 n/a Un, Inc
SL n/p Edwards, 1969
Lunatia heros
24.5–47.5
NJ (NC), USA
Mercenaria mercenaria
25–43 Veneridae 27% 13/48 N Inc 3 cm 1–2 days Friend, 2011
large MA (CA), USA
Venerupis philippinarum
20–40 Veneridae 38% (Un), 16% (Inc)^
42/111 (Un), 18/111 (Inc)^
N Un, Inc
10–15 cm
daily Aronowsky, 2003
Mercenaria mercenaria
~40 Veneridae N Un, Inc
Macoma spp. 8–45 Tellinidae N Un, Inc
139
n/p NJ, USA Spisula solidissima
larger Mactridae n/p n/p S Un n/p n/p Weissberger & Grassle, 2003
30–60 NB (ON), Canada
Protothaca staminea
20–60 Veneridae 9% (Un),
21% (Inc)^
N Un, Inc
10 cm n/p Grey, 2001
Lunatia lewisii
50– 100
BC (ON), Canada
Protothaca staminea
20–60 Veneridae N 10 cm n/p Grey, 2001
n/p BC, Canada
Saxidomus giganteus
n/p Veneridae > 25% n/p S Un 7.6 cm
daily Bernard, 1967
n/p BC (AB), Canada
Venerupis philippinarum
37–57 Veneridae 54% 917/ 1687
N Un, Inc
SL n/p Newel & Bourne, 2012
Natica gualteriana
20.9 Guam Tellina robusta n/p Tellinidae 11% 2/19 N Un 1.4–3.5 cm
n/p Vermeij, 1980
Natica unifasciata
25–34 (H)
Panama Olivella volutella
15–20 Olivellidae 100% 3/3 n/a Un 5 cm hourly –daily
Hughes, 1985
Neverita duplicata
33–37 NC, USA Neverita duplicata
17–23 Naticidae 6% 7/126 n/a Un, Inc
7.6 cm
3 days Siao et al., 2010
15–26 NC, USA Mercenaria mercenaria
7–23 Veneridae 10% 81/807 N Un 7.6 cm
2–3 days Gould, 2010
medium –small
Macoma spp. ~25 Tellinidae 4% (Un),
11/265 (Un),
N Un, Inc
10–15 cm
daily Aronowsky, 2003
MA (CA), USA
Venerupis philippinarum
~37 Veneridae 12% (Inc)^
32/265 (Inc)^ N
Un, Inc
Neverita duplicata
smaller Naticidae 100% 1/1 n/a Inc
Polinices mammilla
~28 Hong Kong
Venerupis philippinarum
10–40 Veneridae 36% 44/114 N Un SL daily Ansell & Morton, 1985
(continued)
140
larger Hong Kong
Venerupis philippinarum
n/p
Veneridae 55% 78/142 N Un
SL daily Ansell & Morton, 1987
Anomalocardia squamosa
Veneridae 44% 10/23 N Un
Atactodea striata
Mesodesmatidae 14% 4/28 N Un
Coecella chinensis
Mesodesmatidae 20% 10/49 N Un
Donax faba Donacidae 16% 3/19 N Un
Glauconome chinensis
Glauconomidae 15% 5/34 N Un
25.7– 35.4
Guam
Gafrarium pectinatum
n/p
Veneridae 13% 1/8 N Un
1.4–3.5 cm
n/p Vermeij, 1980
Timoclea marica
Veneridae 100% 4/4 N Un
Tellina robusta Tellinidae 21% 4/19 N Un
Quidnipagus palatam
Tellinidae 60% 6/10 N Un
^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).
(continued)
141
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
SU Agersborg, 1920 "In the case of Mya, the gasteropod sucks itself over the syphon down into the sand until its victim is dead from suffocation, and then when the clam has opened, Polynices simply sends its proboscis between the valves and devours the content." p. 421
SU Edwards, 1969 "Although Polinices may occasionally force its prey's operculum, the incomplete bore holes suggest another explanation, viz., that O. biplicata suffocates while wrapped in the predator's foot and relaxes." p. 327
SU Vermeij, 1980 "...Arcopagia robusta and Quidnipagus palatam which can be eaten by naticids without drilling. It is likely that these clams suffocate while being enveloped by the predator's foot before drilling has proceeded very far." p. 332
SU Hughes, 1985 "Since in the present study, N. unifasciata consumed O. volutella within 12 h, a forceful entry through or round the edges of the flimsy operculum seems a more likely method than suffocation." p. 334
SU Ansell & Morton, 1987 "The immediate cause of gaping of the prey is interpreted here as suffocation, but it is also possible that the process is facilitated by the presence in the pedal mucus or other secretion of the predator of a narcotizing toxin." p. 117
SU Reid & Gustafson, 1989 "We explored the possibility... secretion might have a pharmacological effect [...] There was no such effect, 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
SU Vermeij et al., 1989 "… but Ansell & Morton (1987) have shown in laboratory trials with Venerupis japonica eaten by various 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]
SU Calvet i Catà, 1992 "Naticid gastropods use several strategies to feed on their prey <…> suffocation in snails with a large mesopodium (Ansell & Morton 1987), and non-boring predation as observed in razor clams (Schneider 1981). p. 58
SU Peitso et at., 1994 “Large Glossaulax didiyma begin boring their prey, but consume it after the prey suffocates, before boring is complete (Ansell and Morton 1987)." p. 323
143
SM Leighton, 2001 "Vermeij (1980) noted that many of the smaller prey species in his study might have been killed by smothering before drilling was necessary." p. 57
SM Leighton, 2002 "Also, some naticids may be capable of smothering, rather than drilling, their prey (Ansell and Morton 1987)." p. 333
SU Weissberger & Grassle, 2003 "A naticid may kill a bivalve to large by suffocating it with its foot (Ansell & Morton, 1987; E. Weissberger personal observation), leaving no trace of predation on the bivalve's shell." p. 680
SU Kingsley-Smith et al., 2003 "Shell valves cleaned of tissue that lacked evidence of drilling were not recovered from aquaria, such that P. pulchellus did not appear to employ any non-drilling methods of subjugating prey, such as suffocation." p. 182
SU Kowalewski, 2004 "Similarly, Ansell & Morton (1987) observed in aquarium experiments that the naticid Glossaulax didyma abandoned incomplete drill holes and consumed some of its prey, which suffocated during initial phases of drilling, without penetrating the shell." p. 365
SU Harper, 2006 "Ansell and Morton (1987) observed that some individuals of the naticid Glossaulax didyma feeding on 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
SM Harries & Schopf, 2007 "Ansell and Morton (1987) have documented a range of feeding modes, such as smothering […] Because smothering predation leaves no discernable signature in the fossil record…" p. 42–43
SU Morton, 2008 "Ansell & Morton (1987) also showed that Polinices tumidus Swainson, 1840, held its prey with the rear of its foot and, as a consequence, sometimes suffocated it such that there were no drill holes to identify the predation event." p. 317
SM Hasegawa & Sato, 2009 "…four successive phases of behaviour: (1) capture, (2) smothering, (3) rotation and (4) drilling. […] pedal mucus, which enveloped and hardened around the prey, immobilizing it for a few days…" p.149
SU Baumiller et al., 2010 "It has been shown, however, that some extant boring predators can subdue their prey by suffocating them (Kowalewski, 1994)…" p. 639
SM Klompmaker, 2012 "…how often smothering or rasping into the tube via the aperture to kill the organism was employed by naticids cannot be addressed." p. 117
144
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,
145
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
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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
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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