Journal of South American Earth Sciences 110 (2021) 103352

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Journal of South American Earth Sciences

journal homepage: www.elsevier.com/locate/jsames

Drilling predation on juvenile and adult gastropod shells during the

Pliocene in the eastern Pacific, southern Mexico
Claudia Gabriela Ortiz-Jerónimo a, Ma Catalina Gómez-Espinosa b, *, Frank Raúl Gío-Argáez c,
Oscar Talavera-Mendoza b, Luis Antonio Flores de Dios b, Brenda Berenice Martínez-Villa c
a
Escuela Superior de Ecología Marina, Universidad Autónoma de Guerrero, Gran Vía Tropical 20 Playas, 39390, Acapulco de Juárez, Guerrero, Mexico
b
Escuela Superior de Ciencias de La Tierra, Universidad Autónoma de Guerrero, Exhacienda San Juan Bautista, Taxco El Viejo, 40323, Guerrero, Mexico
c
Instituto de Ciencias Del Mar y Limnología, Universidad Nacional Autónoma de México, Circuito Exterior CU, Ciudad Universitaria, Alcaldía Coyoacán, 04510, Ciudad
de México, Mexico

A R T I C L E I N F O A B S T R A C T

Keywords: Quantifying the effects of drilling predation on juvenile and adult gastropods is important for understanding the
Durophagy paleoecology of communities. Although numerous studies have examined predation on adult shells, virtually no
Fossil reports cover juvenile specimens. We compare predation frequency and prey effectiveness between juvenile and
Predator-prey relationship
adult gastropods in a Pliocene assemblage from the eastern Pacific of Mexico. Evidence of predation in the
Marine gastropods
Neogene
sample was confirmed by the presence of drilling in the shells, ascribed to Oichnus simplex Bromley, 1981 and
O. paraboloides Bromley, 1981, which showed active predation by caenogastropods. The occurrence of drilling
gastropods in the same locality reveals the possible predators as naticids (Polinices intermeratus (Philippi, 1853),
and Natica broderipiana Récluz, 1844) and muricids (Eupleura vokesorum Herbert, 2005 and Thypina sp.). Some
differences were found in predatory patterns between drilling gastropods, naticids drilled at a higher frequency
than muricids in adults, while the opposite occurs in juveniles. Prey Effectiveness (PE) values were 0.00 for
juveniles and 0.02 for adults.

1. Introduction patterns (Klompmaker et al., 2017) and influence of environmental

In evolutionary and theoretical ecology, the lethal and nonlethal
effects of predation have largely been studied using mostly small-bodied
and abundant organisms. The fossil record has been widely used to test
these ecological and evolutionary hypotheses and theories (Vermeij,
1987; Klompmaker et al., 2019). Predator–prey interactions through
time have been studied using trace fossil evidence because predators are
infrequently preserved in the process of hunting their prey (Kelley and
Hansen, 2003; Kowalewski et al., 1998; Ottens et al., 2012; Kong et al.,
2015; Tackett and Tintori, 2019). Most reports of predation in the fossil
record come from Europe, the United States and Japan, with isolated
reports worldwide (eg., see Klompmaker et al., 2019).
Other studies have used organismal remains to understand the
taphonomic aspects of predation in the fossil records to establish
guidelines to identify taphonomically altered assemblages (Kowalewski,
2002). Recently, a database on this topic has been of interest to infer
gradients (Klompmaker et al., 2019). Many publications have described
the quantitative study of drilling predation (Hoffmeister, 2002;
Klompmaker et al., 2016; Archuby and Gordillo, 2018; Tackett and
Tintori, 2019).
Some molluscivory strategies include whole organism ingestion,
insertion, and extraction, pre-ingestive breakage, and penetration of the
prey’s skeleton, leaving behind a hole in the shell. The study of preda­
tion in the fossil record focuses on the last two types as indirect evidence
of predation, recognizable as trace fossils (Klompmaker et al., 2019).
Most studies of gastropod predation on mollusk fossils have mainly
focused on adult mortality (see Klompmaker et al., 2019). Research
covering earlier ages (juvenile and larvae) has been included only in
experimental neontological studies, testing recent organisms under
controlled laboratory conditions and for target taxa (Brenchley, 1982;
Hayakawa et al., 2012; Hickman, 2001; Pechenik et al., 2010; Solas
et al., 2015). Studies of fossil molluscs by Kelley and Hansen used a sieve

* Corresponding author.
E-mail addresses: ortizclaudia168@yahoo.com.mx (C.G. Ortiz-Jerónimo), c_gomez@ciencias.unam.mx (M.C. Gómez-Espinosa), raulgioargaez@cmarl.unam.mx
(F.R. Gío-Argáez), otalavera.uagro@gmail.com (O. Talavera-Mendoza), afloresdd@yahoo.com.mx (L.A. Flores de Dios), brendamavi@ciencias.unam.mx
(B.B. Martínez-Villa).

https://doi.org/10.1016/j.jsames.2021.103352
Received 9 October 2020; Received in revised form 19 April 2021; Accepted 20 April 2021
Available online 23 April 2021
0895-9811/© 2021 Elsevier Ltd. All rights reserved.
C.G. Ortiz-Jerónimo et al.
size of 1 mm, so that juveniles were likely included in their data, but
juveniles were not analyzed separately from adults (see summary in
Kelley and Hansen 2006).
Chattopadhyay et al. (2020) consider that the nature of drilling
predation is well documented for molluscan fossils, but understudied for
micromolluscs (<5 mm). So far, no information has been available
regarding predation on juvenile fossil gastropods, and there is only one
study about fossil microbivalves (Chattopadhyay et al., 2020).
Drill holes on shelled organisms are one of the most common
paleoecological observations used to evaluate specific aspects of biotic
interactions, including research on gastropod predators (Chattopadhyay
et al., 2014; Kitchell et al., 1981). In addition to morphological diversity
in gastropods, the fossil record for these organisms covers the Phaner­
ozoic, and has been commonly used to study predation in paleontolog­
ical (Kelley and Hansen, 2003) and neontological studies (Solas et al.,
2015) of prey and predators (Klompmaker et al., 2019).
Although it is widely argued that identifying specific predators
without direct observation is difficult (Kelley and Hansen, 2003), evi­
dence of some drilling predators has been documented in neontological
studies by direct observation in modern marine environments or by
laboratory experiments (Kong et al., 2015). Among the predatory gas­
tropods, several families include shell drillers that excavate a hole in the
prey shell to provide access to the prey flesh (Kabat, 1990). Drilling
gastropods belong to Capulidae, Cassididae, Eulimidae, Marginellidae,
Muricidae, Nassaridae, Naticidae, Okadaiidae, Dotiidae, and Platycer­
atidae, each manifesting perforations of particular morphology (Car­
riker, 1981; Klompmaker et al., 2019).
Muricid and naticid gastropods are common drilling predators that
leave round and smooth perforations on the shells of their prey (Car­
riker, 1981). The prey can be other mollusks (bivalves, gastropods, and
scaphopods), brachiopods, barnacles, serpulids, small crabs, ostracods,
carrion of fish, and other groups (Carriker, 1981; Klompmaker et al.,
2015; Mondal et al., 2017). Muricid and naticid gastropods have
different modes of predatory behavior and drill holes of different shapes
(Kelley and Hansen, 2003). The holes usually drilled by muricids are
cylindrical with nearly straight edges, but some holes have an irregular
outline with jagged margins; these features are associated with Oichnus
simplex (Kabat, 1990). The holes drilled by naticids tend to have a
greater diameter than those of muricids. They are more strongly conical,
often with a tendency to develop countersunk walls (Kabat, 1990),
resembling a wall with a parabolic outline (Kong et al., 2015); this shape
is associated with Oichnus paraboloides (Archuby and Gordillo, 2018).
In incomplete drill holes, the muricids leave a hole with a concave or
flat bottom, surrounded by a circular edge (Archuby and Gordillo 2018).
These features are not present in the naticids, naticids’ incomplete drill
holes tend to have a central boss (Kabat, 1990). Another difference be­
tween them is that naticids attack only living organisms, whereas
muricids feed on both living and dead animals (Reyment, 1967). These
represent a generality but we need to consider that there are some
exceptions.
The goal of this study was to evaluate the predator–prey interactions
in Pliocene marine gastropods, using indirect evidence of predation
(drill holes) on juvenile and adult shells from the eastern Pacific,
southern Mexico, evaluating quantitatively the frequency of predation
(Lower Taxon Frequency-LTF) and prey effectiveness (PE). LTF esti­
mates taxon-specific (species, genus, or family) predation intensity,
particularly important in this study because it is biologically and
ecologically more meaningful (Paul et al., 2013). PE is a measure of
prey’s ability to resist predation (Sawyer and Zuschin, 2011), unsuc­
cessful predation attempts (Dietl, 2003) or predator failure (Kowa­
lewski, 2004).
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Journal of South American Earth Sciences 110 (2021) 103352
2. Materials and methods
2.1. Study area
Punta Maldonado is on the southeastern coast of Mexico, at the
boundaries of the states of Guerrero and Oaxaca, 206 km southeast from
Acapulco and almost 52 km northeast from Pinotepa Nacional. Punta
Maldonado consists of an area of 7711 km2 within the Cuajinicuilapa
municipality (Fig. 1).
The Punta Maldonado Formation is a highly fossiliferous marine
siliciclastic sandstone deposit within the foreshore and offshore transi­
tion zones of a storm-dominated siliciclastic shelf (Juárez-Arriaga et al.,
2005). It is divided into six lithostratigraphic units designated from the
base to top as I to VI and a paleosol deposit affected by intense erosive
activity.
The Punta Maldonado Formation was previously dated based on
foraminiferan assemblages and oceanographic reconstructions (see
Durham et al., 1981; Malpica-Cruz and Padilla-Arredondo, 1994; Cam­
pa-Uranga and González-Morán, 2002). Juárez-Arriaga et al. (2005)
assigned the Punta Maldonado Formation an Early Pliocene age based
on foraminifera and ostracod assemblages. They were the first to report
Pliocene marine rocks in the southwestern coast of Mexico.
A new proposal on the stratigraphy of Punta Maldonado Formation
was recently published (Gómez-Espinosa et al., 2021). They divided the
formation into seven informal lithostratigraphic units (Fig. 2). To avoid
confusion to identify the units, they changed the Arabic number pro­
posed originally by Juárez-Arriaga et al. (2005), by Roman numbers.
The principal change was the addition of a unit 4 wedged throughout the
entire sequence, cutting units 2 and 3 and consisting of rhodolith beds
composed of a medium-grain sand matrix, approximately 1.5 m thick.
The unit 4 was previously interpreted by Juárez-Arriaga et al. (2005) as
a paleochannel filled with conglomeratic material cut into unit II.
Fossils preserved in the Punta Maldonado Formation include rho­
dolith algae, foraminifers, bryozoans, corals, mollusks (bivalves, gas­
tropods, and scaphopods), regular echinoderms, ostracods, barnacles,
and vertebrate remains such as shark teeth (Gío-Argaez et al., 2019;
Gómez-Espinosa et al., 2019). Gastropods and bivalves are so well pre­
served that some of them retain their original color.
2.2. Sample collection
We tabulated drilling predation data for bulk collected gastropod
and sediment samples from Unit 7 (according to Gómez-Espinosa et al.,
2021) of the Punta Maldonado Formation. Samples were collected at “El
Faro” fishing village outcrops located at X = 546,308, Y = 1,804,856
UTM, and at “El rastro” outcrops located at X = 548,061, Y = 1,803,754
UTM. “El rastro” is an informal name used only by local people.
For adult shell sampling, three bulk samples were collected and
sieved through a 4 mm mesh size following the technique suggested by
Anderson et al. (1998). Bioclasts >4 mm are recommended to sample
molluscan remains because smaller fractions display significantly lower
damage than larger fractions. After being sieved, the shells were
hand-picked.
Juvenile gastropods were recovered by means of micropaleontolog­
ical techniques, processing one sample of 100 g of sediment and sieving
the sediment in the U.S. STD sieve series for microfossils from no. 20
(850 μm mesh size) to no. 100 (149 μm mesh size). The sample was
processed in the Laboratory of Environmental Micropaleontology,
ICMyL-UNAM and juvenile shells were mainly recovered from the sieve
no. 60 (250 μm mesh size) sediments below 25 μm sieve size did not
contain gastropods.
Predation evidence (drill holes) was examined under a dissecting
stereomicroscope at Escuela Superior de Ciencias de la Tierra. Complete
and relatively complete adult and juvenile gastropods shells were
included in the present analysis, considering as complete shells with
more than 90% of their original form (Davies et al., 1989), and relatively
C.G. Ortiz-Jerónimo et al.
Fig. 1. Geologic map of the study area (Gómez-Espinosa et al., 2021).
complete shells with more than 75% of their original form preserved.
The drill holes were studied, described, and taxonomically identified to
ichnospecies level. Location of drill holes on the shell surface was
determined with respect to two areas: body whorl and spire (Fig. 3).
Apex was not considered because some studies have shown that drill
holes at the extreme end may not allow the complete consumption of the
prey; because the apex is not a preferential place to drill by predators
(Kabat, 1990).
Representative juvenile gastropod shells were mounted on an
aluminium stub by double-sided sticky tape and coated with carbon for
SEM imaging at the Scanning Electron Microscopy and Microanalysis
3
Journal of South American Earth Sciences 110 (2021) 103352
Laboratory of the Universidad Autónoma de Guerrero.
2.3. Predation frequency
Lethal and sublethal damage were evaluated to calculate predation
frequency using the Lower Taxon Frequency (LTF) method (Kowa­
lewski, 2002):
LTF = DK /NK (1)
where K is a lower taxon target in the analysis, DK is the number of
specimens displaying complete drill holes, and NK is the total number of
C.G. Ortiz-Jerónimo et al. Journal of South American Earth Sciences 110 (2021) 103352

Fig. 2. Stratigraphic column from Punta Maldonado Formation (Gómez-Espinosa et al., 2021).

specimens of that taxon in the sample. Multiply-drilled specimens were

computed as a single attack.

2.4. Prey effectiveness

Prey effectiveness (PE) was defined by Vermeij (1987) as the ratio of

the number of incomplete drill holes to the total number of attempted
holes. PE is a parameter that estimates a predator’s failure by doc­
umenting unsuccessful attacks or healed drill holes (Kowalewski, 2002),
as follows:
PE = TF /TT (2)

where TF is the number of particular trace fossils of predatory origin that

record failed attacks, and TT is the total number of these trace fossils.

2.5. Statistical analysis

We used the Chi2 test to compare drilling frequency in groups cate­

gorized by family and species level in adult life stages and to compare
predation patterns between families in both adult and juvenile life
Fig. 3. Areas considered for the location of the drillhole in the shell. stages. The Chi2 test was also used to compare potential drilling

4
C.G. Ortiz-Jerónimo et al. Journal of South American Earth Sciences 110 (2021) 103352

predators in life stages, as well as their drilling site selectivity. Table 2

Summary of drilling predation on juvenile gastropods of Punta Maldonado,
3. Results México.
Family n Ichnospecies LTF PE
In total, 2907 shells were recovered, including 1067 adults and 1847 O. O. a
juvenile gastropods. Adult gastropods corresponding to 66 species simplex paraboloides
included in 23 families from these 26 species in 13 families show drilling Columbellidae Swainson, 72 25 2 0 0.38 0.00
predation (Supplementary data, Table 1). 1840
Species from the families Turritellidae, Epitoniidae, Calyptraeidae, Cancellariidae Forbes and 123 68 37 0 0.85 0.00
Ovulidae, Personidae, Bursidae, Hipponicidae, Pisaniidae, Fasciolar­ Hanley, 1848
Pyramidellidae Gray, 598 90 60 0 0.25 0.00
iidae, and Volutidae do not display drilled individuals. Taxonomic 1840
identification for juvenile gastropods was only possible at 16 family Turridae H. Adams & A. 270 97 11 0 0.40 0.00
levels for some samples (Table 2) because microgastropods are not well Adams and Adams, 1853
developed and lack distinguishing adult characteristics. Relative abun­ (1838)
Rissoidae Gray, 1847 10 5 3 0 0.80 0.00
dance varies across family and species levels.
Terebridae Mörch, 1852 244 37 21 0 0.24 0.00
Epitoniidae Berry, 1910 16 6 0 0 0.38 0.00
(1812)
3.1. Trace fossil morphology and ichnospecies assignment Olividae Latreille, 1825 17 3 3 0 0.35 0.00
Cystiscidae Stimpson, 50 7 5 0 0.24 0.00
Two different types of drill holes were found in both juvenile and 1865
Pisaniidae Gray, 1857 145 69 19 0 0.61 0.00
adult gastropods. The holes were perpendicular or sub-perpendicular to
Pseudomelatomidae J.P.E. 13 4 5 0 0.69 0.00
the shell surface, with a cylindrical or paraboloid cross-section. Walls Morrison, 1966
were smooth without any etched relief. Naticidae Guilding, 1834 73 9 3 0 0.16 0.00
Trace fossils were identified as ichnogenus Oichnus Bromley, 1981, Conidae J. Fleming, 1822 3 1 1 0 0.67 0.00
with two species: O. simplex Bromley, 1981 and O. paraboloides Bromley, Planaxidae Gray, 1850 1 0 0 0 0.00 0.00
Architectonicidae Gray, 3 1 1 0 0.67 0.00
1850
Table 1 Calyptraeidae Lamarck, 5 0 0 0 0.00 0.00
Summary of drilling predation by family on adult gastropods of Punta Maldo­ 1809
nado, México. Sp 1 (Unidentified family) 1 0 1 0 1.00 0.00
Sp 2 (Unidentified family) 20 5 0 0 0.25 0.00
Family n Ichnospecies a LTF PE Sp 3 (Unidentified family) 4 2 0 0 0.50 0.00
O. O. Sp 4 (Unidentified family) 5 2 0 0 0.40 0.00
simplex paraboloides Sp 5 (Unidentified family) 66 44 0 0 0.67 0.00
Sp 6 (Unidentified family) 52 2 0 0 0.04 0.00
Turritellidae Lovén, 1847 42 0 0 0 0.00 0.00 Sp 7 (Unidentified family) 1 0 0 0 0.00 0.00
Epitoniidae Berry, 1910 8 0 0 0 0.00 0.00 Sp 8 (Unidentified family) 22 2 0 0 0.09 0.00
(1812) Sp 9 (Unidentified family) 6 1 0 0 0.17 0.00
Calyptraeidae Lamarck, 38 0 0 0 0.00 0.00 Sp 10 (Unidentified 21 5 2 0 0.33 0.00
1809 family)
Ovulidae J. Fleming 2 0 0 0 0.00 0.00 Sp 11 (Unidentified 1 0 0 0 0.00 0.00
(1822) family)
Naticidae Guilding, 1834 70 1 5 0 0.08 0.00 Sp 12 (Unidentified 4 1 1 0 0.50 0.00
Personidae Gray, 1825 9 0 0 0 0.00 0.00 family)
Bursidae Thiele, 1925 21 0 0 0 0.00 0.00 Sp 13 (Unidentified 1 0 1 0 1.00 0.00
Hipponicidae Troschel, 8 0 0 0 0.00 0.00 family)
1861
Pisaniidae Gray, 1857 21 0 0 0 0.00 0.00 n-abundance at family level, LTF- Lower Taxon Frequency, PE- Prey Effective­
Nassariidae Iredale, 1916 46 2 6 0 0.17 0.00 ness, a-aborted drill holes.
(1835)
Columbellidae Swainson, 47 5 1 1 0.13 0.17
1840
1981. O. simplex was indicated by a drill hole commonly perpendicular
Fasciolariidae Gray, 5 0 0 0 0.00 0.00 to the shell surface with a cylindrical or subcylindrical cross section
1853a,b (Fig. 5 A-E, Fig. 6A–I). In contrast, O. paraboloides was indicated by a
Conidae J. Fleming (1822) 93 2 1 1 0.03 0.33 paraboloid cross-sectional shape (Nielsen and Nielsen, 2001) (Fig. 5 F-L,
Pseudomelatomidae J. P. 262 15 41 1 0.21 0.02
Fig. 6J–O). Aborted drill holes end as a pit (in incomplete penetration),
E. Morrison (1966)
Turridae H. Adams & A. 55 4 7 0 0.20 0.00 wider than deep (Wisshak et al., 2015) (Fig. 5M–N).
Adams and Adams, 1853
(1838)
Terebridae Mörch, 1852 85 7 14 0 0.25 0.00
3.2. LTF and PE
Olividae Latreille, 1825 116 3 3 0 0.05 0.00
Muricidae Rafinesque, 7 1 0 0 0.14 0.00 LTF values for adult and juvenile organisms are 0.13 and 0.36,
1815 respectively. PE values are 0.02 in adult shells and 0.00 in juvenile shells
Mitridae Swainson, 1831 24 2 3 0 0.21 0.00
(Tables 1 and 2).
Cystiscidae Stimpson, 29 0 4 0 0.14 0.00
1865
Cancellariidae Forbes and 51 5 2 0 0.14 0.00
3.3. Prey selectivity
Hanley, 1848
Volutidae Rafinesque, 3 0 0 0 0.00 0.00
1815 Drilling predation in the sample was observed occurring only in
Architectonicidae Gray, 25 4 2 0 0.24 0.00 mollusks, including gastropods, bivalves and scaphopods, both in adult
1850 and juvenile stages. Juvenile mollusks were mixed with a great diversity
n-abundance at family level, a-aborted drill holes, LTF- Lower Taxon Frequency, of shelly microfossils (foraminifers and ostracods), which showed no
PE- Prey Effectiveness. evidence of predatory drill holes.

5
C.G. Ortiz-Jerónimo et al.
Fig. 4. Abundance of Oichnus ichnospecies in adult and juvenile gastropods
by family.
At the family level, juvenile Pyramidellidae were primarily attacked
predominantly by muricids. Conversely, adult shells of the Pseudome­
latomidae family (species Compsodrillia duplicata) were more frequently
attacked, mainly from naticids (Fig. 4).
3.4. Statistical analysis
The total number of successful drilling attacks between adult and
juvenile stages are significantly different (Chi2 = 172.71, p < 0.001).
140 of 1060 adult shells show complete drilled holes caused by preda­
tors and only 3 display evidence of a failed (aborted) attack. In contrast,
6
Journal of South American Earth Sciences 110 (2021) 103352
662 of 1847 juvenile shells showed complete drill holes and no aborted
attacks, meaning drilling predation was typically successful.
A comparison between families displaying successful drilling attacks
in both juvenile and adult shells indicate significant differences (Chi2 =
121.25, p < 0.001) per life stage, suggesting organisms from families in
juvenile stages were attacked more frequently.
4. Discussion
Molluscan shells possess characteristics that reduce predation risk,
such as thickened walls, narrow shell apertures, axial shell sculptures,
and short spires (Vermeij, 1987; Bertness and Cunningham, 1981;
Lively, 1986). Nevertheless, they are an easy target for predators and
represent the most common marine prey in the late Cenozoic (Klomp­
maker et al., 2019).
4.1. Potential drilling predators
Three families of molluscivorous gastropods are present in the
Pliocene of Punta Maldonado: Naticidae, Conidae and Muricidae.
Predatory marine gastropods of the Conidae family use venom to
capture their prey (Weese and Duda Jr., 2019), commonly worms, fish
and other mollusks (Prashanth et al., 2017). Conidae predation does not
leave a trace in the fossil record.
The Muricidae is a diverse family containing a variety of predators,
including shell drillers, carrion feeders, other specialized predators, and
herbivores. Nevertheless, most muricids are shell drillers (Kabat, 1990).
Naticidae are major predators in marine soft substrates, preying mainly
on shelled mollusks by drilling predation (Huelsken, 2011).
Our results suggest naticids and muricids are common predators of
gastropods in Punta Maldonado during the Pliocene. Species in the
assemblage representing drilling predators correspond to Natica bro­
deripiana (Récluz, 1844), Polinices intemeratus (Philippi, 1853) (nati­
cids), Eupleura vokesorum (Herbert, 2005), and Typhina sp. (muricids)
(Fig. 7).
Recent works considered gastropod predation based on the abun­
dance of the potential drilling predators (Martinell et al., 2013). This
assessment is consistent with our results for adults, which show higher
predation by naticids than muricids (Chi2 = 38.64, p < 0.001), because
naticids are ten times more abundant (n = 70) than muricids (n = 7)
(Fig. 4). We cannot support this statement in juveniles because we were
only able to identify Naticidae family, while Muricidae members were
not possible to identify between the microgastropods.
Naticids commonly prey on benthic, infaunal shelled mollusks,
consuming their prey within the sediment, while the epifaunal and
rocky-habitat generally escape naticid predation. Muricids, on the other
side, hunt the epifauna and also eat carrion. They are known to attack on
the surface (Kabat, 1990).
Difference in predation between muricids and naticids has been
explained by the life habits (Klompmaker, 2009) - in our assemblage
most adult gastropods lived in the sediments, and some on the top of the
sediment. The assemblage studied contains gastropods that exhibited a
range of epifaunal, infaunal, and epibiont species; showing a predomi­
nance of infauna over epifauna gastropods (Table 3). This represents an
abundance of infaunal prey for naticids and less epifaunal prey for
muricids.
Comparisons between habitat and life mode of Muricidae (epifaunal)
and Naticidae (infaunal) indicate they could not possibly meet each
other (Hoffman et al., 1974). To genus level Strombina Mörch, 1852 was
exclusively preyed by muricids, while Polinices Montfort, 1810, Carino­
drillia Dall, 1919 and Eupleura H. Adams & A. Adams and Adams, 1853
were preyed upon by naticids; but the rest of the genera (n = 14) were
preyed upon by muricids and naticids (Supplementary data), then
specimens studied do not resemble this marked difference. Even more,
the muricid Eupleura vokesorum has an O. paraboloides trace (Fig. 6H).
This proves predation of muricids by naticids. While naticid Natica
C.G. Ortiz-Jerónimo et al. Journal of South American Earth Sciences 110 (2021) 103352

Fig. 5. Evidence of drilling predation in adult gastropod shells. Oichnus simplex ichnospecies in A) Architectonica nobilis B) Natica broderipiana C) Subcancilla attenuata
D) Cancellaria ventricosa E) Trajana perideris; Oichnus paraboloides ichnospecies in F) Carinodrillia hexagona G) Polystira picta H) Eupleura vokesorum I) Compsodrillia
duplicata J) Neoterebra armillata K) Cancelaria jayana L) Hindsiclava militaris. Aborted drill holes in M) Conasprella aff. C. roberti N) Strombina fusinoidea. Scale bar 5
mm, close up 2.5 mm.

Fig. 6. Evidence of drilling predation in juvenile gastropod shells showing ichnospecies A-I Oichnus simplex, and J-O O. paraboloides. Families A-B Turridae E, J, O
Naticidae, F cf. Architectonicidae, N Olividae. Scale bar 500 μ.

Fig. 7. Drilling predator gastropods represented in the assemblage A) Natica broderipiana B) Polinices intermeratus C) Eupleura vokesorum D) Typhina sp. Scale bar
5 mm.

broderipiana displays a drill hole that resembles O. simplex (Fig. 5B), even Relative availability of the prey may determine the diet of predators
so we need to consider that holes in very-thin shells do not display the (Kabat, 1990). At genus level, there was no evidence of prey preference
difference between naticids and muricids holes (Kelley and Hansen, for naticids or muricids, which probably results from the great diversity
2003). of gastropods in the assemblage studied (both predators as prey), and a

7
C.G. Ortiz-Jerónimo et al. Journal of South American Earth Sciences 110 (2021) 103352

Table 3 including variation in latitude, depositional environment (including

Life habits per family. bathymetry, substrate and temperature, and taphonomic bias).
Family Life habits Regarding PE, naticids and muricids were apparently efficient
predators in the Pliocene of Punta Maldonado, with only 3 of 143 drill
Turritellidae Most species may be mostly sedentary and infaunal or semi-
infaunal in relatively soft substrate, many are also epifaunal holes incomplete (2.1%). This is almost half the effectiveness than PE
on coarser or harder substrates (Allmon, 1988) reported by Klompmaker (2009) for naticids on Pliocene bivalves from
Epitoniidae More or less adapted to parasitic mode of life on Cnidaria ( The Netherlands (<4%). In juvenile shells all the drill holes were
Harlog, 1987) complete.
Calyptraeidae Usually living stacked on top of one another, on rocks, on
horseshoe crabs, hermit crabs, other gastropods and on dock
Prey effectiveness may also show latitudinal patterns that could
pilings (Vermeij, 2020) affect interpretation in failed drilling (e.g., Kelley et al., 2001). A greater
Ovulidae Living in association with various coelenterates such as true aggregate prey effectiveness has been also reported in assemblages from
corals, gorgonians or soft corals (Chiappone et al., 2003) tropical and subtropical environments than from higher latitudes (Ver­
Naticidae Infaunal, sand or mud-dwelling (Carriker, 1981)
meij, 2002).
Personidae Natural history is poorly known, mainly subtidal, often
associated with coral reef area (Poutiers, 1998)
Bursidae Epifaunal, living in coral reefs or rocky shores. Some inhabit 4.3. Drilling location selectivity
deeper waters in sand or mud bottoms (Poutiers, 1998)
Hipponicidae Usually living stacked on top of one another, on rocks, on Modern and fossil molluscan assemblages have shown non-random
horseshoe crabs, hermit crabs, other gastropods and on dock
pilings (Vermeij, 2020)
distributions of drill hole sites on the prey shell (Berg and Nishenko
Pisaniidae Epifaunal (no known sand-burrowing species) (Vermeij, 1975; Kabat and Kohn 1986; Mallick et al., 2013, 2014).
2017b) For naticids it was suggested that drill hole siting is primarily a
Nassariidae Occur on soft substrates, and many are infaunal, some are function of the manipulation of the prey during boring and may depend
epifaunal (Vermeij, 2017b)
on the prey shell morphology (Kabat, 1990), while muricids have no
Columbellidae This family includes infaunal and epifaunal members (
Vermeij, 2017a) drilling stereotypy because they do not wrap their foot around their prey
Fasciolariidae Epifaunal, inhabiting sand bottoms, mud or rubble (Poutiers, so that shell manipulation is more difficult (Goswami et al., 2020).
1998) Our results show that drilling in adults is not random in a vertical
Conidae This family includes infaunal (sand-burying) and epifaunal profile (Chi2 = 113.4, p < 0.001). This could be because of the size of
members (Vermeij, 2017a)
Pseudomelatomidae Infaunal (Vermeij, 2017b)
these areas, since drill holes are mainly located in the body whorl in
Turridae Infaunal (Vermeij, 2017b) ovoid or low spire shells (e.g., Naticidae, Olividae, Conidae), while in
Terebridae Infaunal (Vermeij, 2017b) high spires or turrid shells the drill holes were located preferentially in
Olividae Infaunal. All shallow-water Olividae members are active the spire at the third whorl (e.g. Turridae), with no difference between
sand-burrowing (Vermeij, 2017b)
O. simplex and O. paraboloides (Supplementary data). A high selectivity
Muricidae Epifaunal (Carriker, 1981)
Mitridae Infaunal, active sand-burrowing (Vermeij, 2017a) of drill hole sites on gastropods has also been registered from the
Cystiscidae Epifaunal, rocky bottom (Coovert, 1987) Cretaceous to the Oligocene, showing a strong preference for drilling
Cancellariidae Infaunal soft-bottom dwelling (Modica, 2015) near the middle-shell position (Kelley and Hansen, 1996). Our results
Volutidae Infaunal, sandy or muddy bottoms, active sand-burrowing ( are comparable to those obtained for the Miocene gastropods from
Poutiers, 1998; Vermeij, 2017b)
Architectonicidae Infaunal, sand burying (Bieler, 1993; Vermeij, 2017b)
Western India, where a site selectivity was found at mid-height of the
shells in turritelline gastropods and restricted towards the lower part of
the body whorl in naticids (Goswami et al., 2020).
hierarchy can not be established.
Drilling predator gastropods’ abundance is higher than the abun­ 4.4. Other controlling factors of possible predation
dance reported for other gastropod assemblages, muricids and naticids
representing 7.2% of the total sample. For example, in the Miocene of There are families that have parasitic (Epitoniidae) and epibiontic
India the abundance reported was 3.4% (Goswami et al., 2020), and for (Ovulidae, Calyptraeidae, Hipponicidae) habits (Table 3). Members of
the same period in the European Paratethys, predators’ abundance these families do not display drilling predation evidence (Table 1),
represented 2.27% of the sample (Sawyer and Zuschin, 2011). because their mode of life prevents them from being preyed upon by
Higher predation by naticids than muricids has been reported in muricid or naticids. When alive, the Ovulidae family members have a
other Pliocene areas such as in Muddy Creek assemblage, Victoria, mantle covering the shell and the mantle is unpalatable and therefore is
Australia, where it was determined that 75% of the drill holes were rejected or ignored by some predators (Gerhart, 1986). In this case it is
naticid and the other 25% corresponded to muricid (Hingston, 1985). not only the habitat that prevents predation by drilling gastropods.
In our results, Calyptraeidae and Hipponicidae members did not
4.2. LTF and PE show drilling predation. This agrees with the statement that limpets
have low predation risk because of their life habits and shell morphology
Cenozoic drilling frequencies are typically considered much higher - “like small pebbles. Shells are difficult for small crawling predators to
than for other eras, up to 40% for the Paleogene and Neogene (Kowa­ ascend, providing a degree of safety for epibionts from potential en­
lewski et al., 1998). emies” (Vermeij, 2020 p. 94). Nevertheless, this usually occurs in
According to results of juvenile and adult gastropods, a higher dril­ tropical regions where the intensity of predation is high and shells are
ling frequency in smaller specimens has been evidenced in previous abundant, as in the case of the locality studied in Punta Maldonado. But
studies of the fossil record (Arua and Haque, 1989). This higher drilling in higher latitudes, even specialized guest limpets might not be safe
frequency in smaller specimens may be for several reasons; juvenile (Vermeij, 2020), as is shown for recent limpets from Patagonia,
predators (probably more abundant than adults) may target young in­ Argentina, where limpets are common prey for muricid gastropods
dividuals for easy manipulation of prey, or it may be a change in the life (Archuby and Gordillo, 2018).
mode of the prey during ontogeny (Paul et al., 2013). In some species, Another general trend considered the idea that ornamented shells are
younger individuals may be infaunal, while the larger individuals may less vulnerable to predation, compared with not ornamented shells
be epifaunal. This can result in higher predation on juveniles (Paul et al., (Vermeij, 1982). Strong ornamentation on gastropods could make it
2013; Sawyer and Zuschin, 2011; Waite and Strasser, 2011). difficult for a drilling predator to grip and attack (Dudley and Vermeij,
Variation of drilling intensity has been attributed to many causes 1978), increasing gastropods’ shells resistance to predation. Advantage

8
C.G. Ortiz-Jerónimo et al.
of ornamented shells over predation can be because the ornamentation
acts as an armor in gastropods or by an increase in the cost-benefit of
predatory attack (Vermeij, 1982).
We observed this trend, because in adult gastropods, strongly orna­
mented forms do not have drill holes as in Bursidae (Bursa rugosa,
Marsupina nana) and Personidae (Distorsio decussata) families. While the
species that lack sculpture increase vulnerability as Columbella sp., or the
ones with relatively weaker ornamentation as Neoterebra elata,
N. armillata, Hinsiclava militarias, Carinodrillia hexagona and Archi­
tectonica nobilis, wich display a higher drilling frequencies. This is clearly
observed in the genus Polystyira where P. picta has a drilling frequency of
0.64 against 0.00 in P. tuberculosa, possessing the first one a weaker
ornamented shell than the second one. Nevertheless, one of exceptions
to this trend is Cyphoma emarginatum (Ovulidae), a species without
sculpture in the shell, this species is not preyed by drilling gastropods
because of its epibiontic life habit and unpalatability.
4.5. Further considerations
Although no evidence of size selectivity was found, we are assuming
that juvenile gastropods were preyed upon by juvenile gastropod
predators and that the adults followed the same pattern. The successful
predation attacks among adults and juveniles was significantly different
(Chi2 = 172.71, p < 0.001), suggesting better adaptation against pre­
dation by adult organisms.
Nonetheless, it must be considered that predation patterns by gas­
tropods can be controlled by biotic factors such as predator availability,
prey avoidance, prey preference, and the diversity and abundance of
both predators and prey (Paul et al., 2013). Other controlling factors
that can affect predation patterns include the number of samples per
location, predators competing against each other and the abundance of
durophagous predators that crush the undrilled shells, and other po­
tential prey (Smith, 2018).
Considering other prey, in the assemblage studied bivalves and
scaphopods are abundant, and ostracods are present as well. Bivalves
and scaphopods have drilling predation traces but have not been stud­
ied. Ostracods do not show these traces.
Ostracods are reported as potentially important prey for juvenile
naticids (Reyment, 1967; Maddocks, 1988) and muricids (Reyment and
Elewa, 2003). But in an environment rich in bivalves, ostracods are not
the main target for predation (Reyment and Elewa, 2003). This prefer­
ence is not determined by abundance because no significant correlation
was found between species abundance and drilling percentages in
Paleocene ostracods from Argentina (Villegas-Martín et al., 2019).
5. Conclusion
This research was performed on 2907 shells. Juvenile and adult
gastropods from the Pliocene of Punta Maldonado, Guerrero, in the
Pacific Coast of Mexico, have predatory drill holes associated with the
ichnospecies Oichnus simplex and O. paraboloides. These drills coincide
with the presence in the fossil assemblage of Eupleura vokesorum,
Typhina sp. (muricids), Natica broderipiana and Polinices intemeratus
(naticids).
Oichnus paraboloides was more abundant than O. simplex, showing a
higher level of predation by naticids than muricid gastropods in adult
stages. The opposite happens in juvenile stages where O. simplex was
predominant, and muricids were the principal predators.
The most likely factor explaining the predation pattern on adults is
the higher abundance of Naticidae over Muricidae in the assemblage.
This assessment can not be applied to juvenile species. It is not possible
to compare the abundance between juvenile predatory families because
only members of the Naticidae were able to be identified, while muricids
are part of the unidentified families.
The record of predatory drill holes in the Pliocene fossil gastropods
studied here indicated a significantly higher (Chi2 = 172.71, p < 0.001)
9
Journal of South American Earth Sciences 110 (2021) 103352
occurrence in juvenile than adult stages. Nevertheless, PE values for
juvenile (0.00) compared to adult stages (0.02) do not show significant
difference (Chi2 = 0.82).
Funding sources
This study was supported by the Secretaria de Educación Pública
(SEP-PROMEP) Project. The first author was supported by a master’s
scholarship from Consejo Nacional de Ciencia y Tecnología (CONACyT).
Author statement
All authors of this research paper have directly participated in the
planning, execution, or analysis of this study, as mentioned below with
their responsibility in the research.
1. Claudia Gabriela Ortíz-Jerónimo: contributed with the methodology,
validation, formal analysis, and writing-original draft preparation.
2. Catalina Gómez-Espinosa contributed with the conceptualization,
supervision, writing-original draft preparation, and Funding
acquisition.
3. F. Raúl Gío-Argaez contributed with the resources and Funding
acquisition
4. Oscar Talevera Mendoza contributed with the resources and
supervision
5. Luis A. Flores de Dios contributed with the resources
6. Brenda Martinez Villa contributed with the resources.
Declaration of competing interest
The authors declare that they have no known competing financial
interests or personal relationships that could have appeared to influence
the work reported in this paper.
Acknowledgments
We thank the Scanning Electron Microscopy and Microanalysis
Laboratory of the Universidad Autónoma de Guerrero (CONACYT, grant
231511) and Jazmín López-Díaz who provided the scanning electron
images. We are grateful to reviewers Adiël A. Klompmaker and Patricia
H. Kelley, and editors Pablo J. Pazos and Diana E. Fernández, for their
valuable suggestions and advice to improve this paper.
Appendix A. Supplementary data
Supplementary data to this article can be found online at https://doi.
org/10.1016/j.jsames.2021.103352.
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