MARINE AND FISHERY SCIENCES 36 (2): 165-178 (2023)

https://doi.org/10.47193/mafis.3622023010509

ABSTRACT. Assessing the extinction risk in marine invertebrates poses serious challenges to

conservation biology, due to the magnitude of marine biodiversity, the inaccessibility of most of the

marine realm, and the lack of appropriate data on population dynamics and ecology for most

species. However, simple life history traits have a huge potential for preliminary screening criteria

for assessing large numbers of species whose status is harsh or impossible to evaluate. Body size

and trophic position could be strong predictors of extinction risk providing a general framework for

the assessment of species vulnerability. We analyzed the Body Size-Trophic Position (BS-TP) rela-

tionship along 1,067 genera representing 4,256 nominal species of western Atlantic benthic gas-

tropods. We found that a carnivore diet characterizes 67% of the genera and that, supporting theo-

retical predictions, the probability of being carnivores as a function of size showed a unimodal

trend. For species with adult body sizes larger than 5 cm, a negative association between trophic

position and body size was detected. This result points to an energetic restriction for the viability of

large species, implying that organisms placed near the BS-TP boundary are extremely vulnerable to

environmental changes. With this result, 109 genera from 42 families of carnivore gastropods and

33 genera from 19 families of herbivore gastropods that may be more vulnerable from the analyzed

perspective were identified and ranked. Supporting these results, while the most vulnerable genera

are not represented in global IUCN assessments, all our ‘top 10’ vulnerable families are being con-

sidered in National or Regional Red Lists. Prior to conducting regional or global conservation

assessments for invertebrate taxa, screening methods should be strongly considered.

Key words: Extinction risk, body size-trophic position relationship, conservation biology.

Evaluación de la vulnerabilidad ecológica de los gasterópodos bentónicos marinos del Atlántico

Occidental

RESUMEN. Evaluar el riesgo de extinción de los invertebrados marinos plantea serios desafíos

para la biología de la conservación, debido a la magnitud de la biodiversidad marina, la inaccesibili-

dad de la mayor parte del ámbito marino y la falta de datos apropiados sobre la dinámica de población

y la ecología de la mayoría de las especies. Sin embargo, los rasgos simples de la historia de vida tie-

nen un gran potencial como criterios preliminares de selección para evaluar un gran número de espe-

cies cuyo estado es difícil o imposible de evaluar. El tamaño del cuerpo y la posición trófica podrían

ser fuertes predictores del riesgo de extinción proporcionando un marco general para la evaluación

de la vulnerabilidad de las especies. Analizamos la relación Tamaño Corporal-Posición Trófica (BS-

TP) a lo largo de 1.067 géneros que representan 4.256 especies nominales de gasterópodos bentóni-

cos del Atlántico Occidental. Encontramos que una dieta carnívora caracteriza al 67% de los géneros

y que, apoyando las predicciones teóricas, la probabilidad de ser carnívoros en función del tamaño

mostró una tendencia unimodal. Para especies con tamaños corporales adultos mayores de 5 cm, se

165

*Correspondence:

alvardoc@fcien.edu.uy

Received: 2 February 2023

Accepted: 31 March 2023

ISSN 2683-7595 (print)

ISSN 2683-7951 (online)

https://ojs.inidep.edu.ar

Journal of the Instituto Nacional de

Investigación y Desarrollo Pesquero

(INIDEP)

This work is licensed under a Creative

Commons Attribution-

NonCommercial-ShareAlike 4.0

International License

Marine and

Fishery Sciences

MAFIS

ORIGINAL RESEARCH

Assessing the ecological vulnerability of Western Atlantic marine benthic

gastropods

ALVAR CARRANZA1, 2, * and MATÍAS ARIM1

1Departamento de Ecología y Gestión Ambiental, Centro Universitario Regional del Este (CURE), Universidad de la República, Av.

Cachimba del Rey e/ Bvar. Artigas y Av. Aparicio Saravia, Maldonado, Uruguay. 2Museo Nacional de Historia Natural, Montevideo, Uruguay.

ORCID Alvar Carranza https://orcid.org/0000-0003-3016-7955

INTRODUCTION

Despite the widespread global threats to marine

ecosystems (Halpern et al. 2007), rates of regis-

tered marine neo-extinctions have been so far rel-

atively low, with a 9-fold lower marine extinction

rate compared to terrestrial systems (Webb and

Mindel 2015). In fact, only five marine mollusc

species or subspecies have been mentioned as

possible extinct in recent historical times (Dong et

al. 2015). However, the pace of marine habitat

deterioration is accelerating, thus increasing

already apparent threats to marine biodiversity,

with nearly 66% of the ocean and 77% of national

jurisdictions showing increased human impact

(Halpern et al. 2015). Further, it should be noticed

that only a small number of marine animals has

been evaluated by the IUCN, and many assessed

species were determined to be data deficient.

Thus, reported numbers of extinct and endangered

marine fauna should be considered as conserva-

tive (Régnier et al. 2009; Pimm et al. 2014).

Gastropods are an incredibly diverse and wide-

spread group, with representatives found in virtu-

ally all aquatic and terrestrial environments, rang-

ing from shallow to deep regions of the ocean,

freshwater, and most land areas. Nevertheless, the

ocean remains their predominant habitat, with the

highest number of species concentrated in marine

benthic environments. Gastropod species have a

variety of different feeding styles. Some species

are seaweed-eating herbivores or suspension

feeders, while others are predatory carnivores or

internal parasites (Todd 2001). Most aquatic gas-

tropods spend adult life in the benthic realm, from

intertidal rocky shores to abyssal plains and

hydrothermal vents. The evolutionary success of

gastropods can be largely attributed to the struc-

tural and functional plasticity of the feeding appa-

ratus (Purchon 1977; Kohn 1983).

To date, only 11,2% species of gastropods in

the IUCN red list are marine. Most of these

species are represented in the Red List owing to

the first comprehensive global assessment of a

marine taxon, namely the 632 valid species of the

tropical marine gastropod Genus Conus (Peters et

al. 2013). However, there is a huge potential for

simple life history traits to be used as preliminary

screening criteria for the assessment of large

numbers of species whose status is harsh or

impossible to evaluate, such as the 32,000-40,000

known described species and the estimated

85,000-105,000 undescribed species in marine

Gastropoda (Appeltans et al. 2012).

In this vein, body size is closely and pre-

dictably related to a wide array of species traits,

thus synthesizing a large amount of biological

information (Brown et al. 2004). Larger animals

live longer, expend more energy, and have higher

metabolic rates, affecting resource demands and

population growth rate and density (McNab

2002; Brown et al. 2004; White et al. 2007).

Additionally, the hierarchy in trophic interac-

tions, in which free-living predators consume

smaller prey, is a well-reported empirical pattern

and a main determinant of food web structure

166 MARINE AND FISHERY SCIENCES 36 (2): 165-178 (2023)

detectó una asociación negativa entre la posición trófica y el tamaño corporal. Este resultado apunta a una restricción energética para la

viabilidad de las especies grandes, lo que implica que los organismos ubicados cerca del límite BS-TP son extremadamente vulnerables a

los cambios ambientales. Con este resultado, se identificaron y clasificaron 109 géneros de 42 familias de gasterópodos carnívoros y 33

géneros de 19 familias de gasterópodos herbívoros que pueden ser más vulnerables desde la perspectiva analizada. Respaldando estos

resultados, mientras que los géneros más vulnerables no están representados en las evaluaciones globales de la UICN, todas nuestras “10

principales” familias vulnerables están siendo consideradas en las Listas Rojas Nacionales o Regionales. Antes de realizar evaluaciones

de conservación regionales o globales para taxones de invertebrados, se deben considerar seriamente los métodos de detección.

Palabras clave: Riego de extinción, relación tamaño corporal-posición trófica, biología de la conservación.

(Brose et al. 2006a, 2006b). Congruently, it was

found that extinction threat for molluscs in mod-

ern oceans is strongly associated with large body

size, whereas past extinction events were non-

selective or preferentially affected smaller-bodied

taxa (Payne et al. 2016). In addition, whereas

habitat zone and feeding mode do not appear to

be associated with threats in the modern ocean,

previous mass extinctions have disproportionate-

ly removed pelagic species. This suggests that

organisms that live in the benthic realm may face

the same threats as their open sea nektonic and

planktonic counterparts.

When the phylogenetic, temporal or spatial

scales are large enough, a hump-shaped relation-

ship between trophic position and body size is

expected (Arim et al. 2007a) and reported (Bur-

ness et al. 2001, 2016; Segura et al. 2015a, 2016).

Despite this, there have been numerous reports of

positive relationships within taxonomic groups.

(Arim et al. 2010; Romanuk et al. 2011). The BS-

TP relationship would be positive as morphologi-

cal restrictions on consumption disappear at larger

sizes; however, the relationship would be negative

because high trophic positions have increased

energetic demands and decreased resources (Arim

et al. 2007a). Positive correlations arise since larg-

er sizes can provide several advantages, including

scape from predation and/or the ability to engage

in more ‘daring’ behaviours, which can expand

the range of available prey. With body size comes

an increase in the ability to capture and dominate

prey, the maximum distance between meals (in

space or time), and the length of the digestive tract

(resulting in longer digestion times and more

resources extracted per gram of prey consumed),

which translates into greater processing opportu-

nities. (McNab 2002). This may be enhanced by

the also increasing absolute size of the organs

associated with prey (and predator) identification

and thus the species ability to differentiate

between resources and distances and detection

thresholds in the environment (Pawar 2015). All

these factors led to an important expansion of the

quantity and quality of resources that can be

exploited. However, the negative relationship

often found at the extreme of body-size distribu-

tions may imply that species placed near the

boundary are extremely vulnerable to any shift in

resource availability, which could drive these

species to extinction. This is of utmost importance

for conservation biologists, since most processes

related with biodiversity loss (e.g. fragmentation,

pollution, overfishing, etc.) produce said shifts in

resource availability and quality (Segura et al.

2015b, 2016). In this sense, there may be impor-

tant conservation applications for identifying

species and/or clades that are susceptible to ener-

getic constraints.

Most of the published examples on BS-TP

focus on taxonomically restricted assemblages,

typically freshwater or marine fishes (e.g. Layman

et al. 2005; Akin and Winemiller 2008; Lucifora et

al. 2009; Arim et al. 2010; Romanuk et al. 2011;

Segura et al. 2015b; Burress et al. 2016; Ou et al.

2017; Dantas et al. 2019). Further, BS-TP curves

may show non-trivial idiosyncratic patterns

according to clade identity, feeding ecologies and

the broader environmental setting. However, no

study has analysed the BS-TP relationship for

marine gastropods to date. Gastropods span four

orders of magnitude in linear dimensions and

eight orders in mass (volume). From Triphoridae,

presenting adult sizes generally ranging between

2-10 mm, with a few species exceptionally reach-

ing 40-50 mm (Albano et al. 2011), to Srynx

aruanus, the largest living gastropod (more than

90 cm maximum adult size), marine gastropods

are a remarkably well suited group to study the

BS-TP relationship. Further, gastropods exploit a

wide array of feeding ecologies, often very con-

served at genus, family, or even superfamily level.

This implies that a feeding strategy may be more

that reasonably inferred given the taxonomic iden-

tity of a given species. In the present study, we

evaluated the relationship between body size and

trophic position along genera of western Atlantic

marine benthic gastropods. By detecting a hump-

167

CARRANZA AND ARIM: VULNERABILITY OF WESTERN ATLANTIC MARINE GASTROPODS

shaped pattern that support energetic constraints,

species prone to be affected by the ongoing

change in the energetic scenario, e.g. productivity,

resource diversity and distribution, temperature,

pollutants, among others, were identified. Finally,

results were contrasted to the existing conserva-

tion assessments for marine gastropods.

MATERIAL AND METHODS

Database structure

Species-level data and associated taxonomy for

western Atlantic benthic gastropods were obtained

from Malacolog 4.1.1, a database created for

research on the systematics, biogeography and

diversity of molluscs (Rosenberg 2009). Mala-

colog geographical coverage ranges from Green-

land to Antarctica, attempting to document all

names that have ever been applied to marine mol-

luscs in the western Atlantic and providing species

identity and taxonomy, maximum adult length

(hereafter body size), bathymetric and geographic

ranges and relevant references supporting each

assignment. However, there is no currently avail-

able dietary information in this database.

Dietary information

Species-level information derived from Mala-

colog was later combined with dietary informa-

tion based on Todd (2001), derived and modified

from the trophic classifications of Hughes (1980)

and Taylor and Reid (1984) for Neogene Neotrop-

ical Gastropds. This trophic classification recog-

nizes seven categories: Predatory carnivores,

browsing carnivores, herbivorous omnivores, her-

bivores, herbivores on rock, rubble or coral sub-

strates, herbivores on plant or algal substrates, and

suspension feeders (Table 1). Each species in the

Malacolog database was assigned to one of the

above-described categories combining them on

the general categories of Carnivore-Non Carni-

vore (Arim et al. 2007b, 2010; Segura et al. 2016).

Data analysis

Considering that the feeding ecology is highly

conserved at generic level, the BS-TP analysis

was analysed at this taxonomic resolution. The

trophic position of each genera (carnivorous ver-

sus non-carnivorous) was linked to the mean

body size of the genera. The occurrence of car-

nivorous genera was related to the average body

size using a logistic regression (Zuur et al. 2009).

Three logistic models were fitted to: i) a model

considering only a constant intercept, in which

diet and body size are independent; ii) a model

that included the effect of body size, reflecting a

monotonic association between variables; and iii)

a model with body size and its quadratic value as

independent variables, considering the theoretical

expectation of a humped association between the

probability of being carnivorous and body size

(Arim et al. 2007a). Models were ranked from

their AIC values and the weight of evidence: wi=

exp(-0.5 · (AICi- min(AIC))/∑ exp(-0.5 · (AICi-

min(AIC)) (Burnham and Anderson 2002). Model

weights indicate the probability that the model is

the best for the data in comparison to the other

models considered.

Priorities for conservation

Genera were ranked in order to identify conser-

vation priorities. The first component of the rank-

ing was based on the difference between the max-

imum body size in the dataset and the mean body

size for each genus. Specifically, the calculation

involves subtracting the mean body size from the

maximum body size, resulting in a numerical

value that represents the difference between the

two measurements. This difference was calculat-

ed for each genus, allowing for comparisons of

the size variation within and between different

genera. Thus, the largest carnivorous or non-car-

168 MARINE AND FISHERY SCIENCES 36 (2): 165-178 (2023)

nivorous genus was assigned a rank value of 1.

The ranking then proceeds with the assumption

that the number of species within genera is nega-

tively correlated with extinction risk and takes

into account the species richness within each gen-

era. As a result, less speciose genera will be

ranked higher at any given body size. The analy-

sis was done for both carnivores and non-carni-

vores separately.

Online search on conservation status

Finally, the overlap between genera/families

here identified was assessed 1) on a global scale

with the IUCN red Lists Global Assessment, and

2) on a regional scale with other non-IUCN

national or regional assessments or national red

lists from countries within the western Atlantic

Ocean, when available.

RESULTS

The database included data on maximum

reported adult body size and dietary information

for 4,256 species belonging to 1,067 genera of

western Atlantic benthic gastropods. Once the

holoplanktonic gastropods were removed, the

database consisted of 1,047 genera, with 350 gen-

169

CARRANZA AND ARIM: VULNERABILITY OF WESTERN ATLANTIC MARINE GASTROPODS

Table 1. Diet categories for Gastropoda used in this study, based in Hughes (1980), Taylor and Reid (1984), and Todd (2001).

Non carnivores

Herbivorous omnivores: browsing macroherbivores

with unselective omnivory, typically of epifauna

attached to macroalgae.

Herbivores on fine-grained substrates: microalgivores,

detritivores, microphages and unselective deposit

feeder. Also included here is a miscellany of herbivo-

rous non-HR and HP categories, including those liv-

ing on wood or mangrove substrates.

Herbivores on rock, rubble or coral substrates: microal-

givores.

Herbivores on plant or algal substrates: micro-and

macroalgivores and detritivores on macroalgal and

seagrass substrates.

Suspension feeders: includes taxa feeding solely or

dominantly upon suspended particles, including

mucociliary feeders.

Carnivores

Predatory carnivores: predators that consume entire

sedentary or mobile macro-organisms, killing them in

the process and also selective foraminifera ingesters

(foraminiferivores). Include scavengers which, with

scant exceptions, display predatory characteristics.

These organisms possess the ability to modulate their

feeding behaviour in response to the availability of

carrion.

Browsing carnivores: predators that consume sedentary,

clonal animals such as corals and cnidarians, sponges,

and ascidians, without causing their immediate death,

fall under this category. Additionally, the group

includes ectoparasites that live on larger sedentary or

mobile prey.

era (33%) classified as non-carnivores and 697

genera (67%) classified as carnivores. The distri-

bution of species richness within genera was

highly skewed, with approximately 43% of the

genera being monospecific, while the maximum

generic diversity corresponded to Conus, with

some 121 species.

Both carnivorous and non-carnivorous species

covered a large range of overlapping body sizes

(Figure 1 A). However, the probability density of

carnivorous genera surpassed that of herbivorous

at intermediate body sizes. This trend is particu-

larly evident in the logistic regression analysis

(Figure 1 B). A quadratic model in which carniv-

orous incidence is maximum at intermediate body

sizes was the one that best matched the data. This

model presented the lower AIC values and it asso-

ciated weight of evidence outperformed alterna-

tive lineal or monotonic models (wquadratic =0.999;

wlinear =7.2e-06; wintercept =5.9e-26). This result

supports the existence of an association between

the incidence of carnivorous genera and body

size, and also that this association involves a

hump-shaped relationship (Figure 1 B).

Once identified the theoretical threshold after

which energetic constraints operate (around 5 cm

maximum adult body size) and ranked species as

previously described, 109 genera from 42 fami-

lies of carnivore gastropods and 33 genera from

19 families of herbivore gastropods that may be

more vulnerable from the analyzed perspective

were classified. Among the overall ranking, seven

out of 10 genera assigned top priorities were car-

nivorous, the exception being Titanostrombus,

Aliger and Syphonota (Table 2). Titanostrombus,

Syphonota, Aliger,Lentigo,Cittarium,Bursatel-

la,Macrocypraea,Dolabrifera,Entemnotrochus

and Aplysia were the most vulnerable of the her-

bivorous genera (Table 3). Triplofusus,Charonia,

Zidona,Pachycymbiola,Turbinella, Adelomelon,

Cassis, Pugilina,Platydoris and Pleuroploca

species ranked amongst the more threatened car-

nivorous genera.

Online search on conservation status

The IUCN currently lists 643 species of marine

gastropods. From these, as mentioned above, 617

species belong to the Genus Conus (Peters et al.

2013). Data deficient and least concern species

170 MARINE AND FISHERY SCIENCES 36 (2): 165-178 (2023)

Carnivores

Non carnivores

Body size log(mm)

1.0 1.5 2.0 2.50.0 0.5

0.0

0.2

0.4

0.6

0.8

1.0 A

Genera probability density

1.0 1.5 2.0 2.50.0 0.5

B

1.0

0.8

0.6

0.4

0.2

0.0

120

60

0

120

60

0

Px: 2.01e-13

Px2: 2.3e-07

Probability of carnivore diet

Number of genera

Body size log(mm)

Figure 1. Size-frequency distribution for carnivorous and non-carnivorous gastropod genera (A) and the probability density of a

carnivorous diet from logistic regression analysis (B).

accounts for ca. 90% of the assessed species. Tax-

onomically, nine families are represented (Table

4), although most of the families include mainly

freshwater and/or brackish species (e.g.

Stenothyridae and Hydrobiidae). However, 39

species from 16 families are represented in

regional and/or national assessments (Table 5).

Results were retrieved from Rio Grande do Sul,

Brazil (ICMBio 2018), Guatemala (CONAP no

date), Colombia (Ardila et al. 2002) and

Venezuela (Rodríguez et al. 2015). Scientific

names provided in Table 5 were updated using the

latest nomenclature available in the World Regis-

ter of Marine Species WORMS (Ahyong et al.

2023), and some names may differ from those uti-

lized in the original publication.

171

CARRANZA AND ARIM: VULNERABILITY OF WESTERN ATLANTIC MARINE GASTROPODS

Table 2. Marine gastropod genera most affected by energetic constraints, based in species richness (SR) within genera and aver-

age maximum adult size. C =carnivores; H =non-carnivores.

Family Genus Species richness Mean size (cm) Diet Rank

Fasciolariidae Triplofusus 1 609 C 1

Strombidae Titanostrombus 1 380 H 2

Charoniidae Charonia 2 382 C 3

Volutidae Zidona 1 270 C 4

Volutidae Pachycymbiola 2 200 C 5

Volutidae Adelomelon 3 362 C 6

Turbinellidae Turbinella 2 280 C 7

Cassidae Cassis 3 288 C 8

Aplysiidae Syphonota 1 170 H 9

Strombidae Aliger 2 274 H 10

Table 3. Non-carnivore marine gastropod genera most affected by energetic constraints.

Higher clade Number of families Family Genus Species richness

Aplysioidea 2 Aplysiidae Syphonota 1

Bursatella 1

Aplysia 6

Dolabriferidae Dolabrifera 1

Cypraeoidea 1 Cypraeidae Macrocypraea 2

Pleutotomarioidea 1 Pleurotomariidae Entemnotrochus 2

Stromboidea 1 Strombidae Titanostrombus 1

Aliger 2

Lentigo 1

Trochoidea 1 Trochidae Cittarium 1

Total 6 18

172 MARINE AND FISHERY SCIENCES 36 (2): 165-178 (2023)

Table 5. Western Atlantic Marine Gastropods species included in available national assessments as data deficient (DD), least con-

cern (LC), near threatened (NT), vulnerable (VU), endangered (EN) and critically endangered (CR). Scientific names

may differ from those originally published. See references in the text.

Family Species Red list category Country

Cassidae Cassis flammea VU Colombia

Cassidae Cassis madagascariensis VU Colombia

Cassidae Cassis madagascariensis EN Guatemala

Cassidae Cassis tuberosa VU Colombia

Charoniidae Charonia variegata DD Brazil

Charoniidae Charonia variegata VU Colombia

Columbellidae Anachis coseli VU Colombia

Cypraeidae Muracypraea mus VU Venezuela

Cypraeidae Propustularia surinamensis VU Colombia

Fasciolaridae Fasciolaria tulipa EN Guatemala

Melongenidae Melongena melongena VU Guatemala

Melongenidae Melongena patula VU Guatemala

Melongenidae Pugilina morio LC Brazil

Olividae Olivancillaria contortuplicata CR Brazil

Olividae Olivancillaria teaguei CR Brazil

Olividae Olivancillaria vesica vesica NT Brazil

Olividae Olivancillaria auricularia DD Brazil

Olividae Olivella formicacorsii DD Brazil

Cymatiidae Cymatium femorale DD Brazil

Table 4. Families of marine gastropods represented in the IUCN Red List as data deficient (DD), least concern (LC), near threat-

ened (NT), vulnerable (VU), endangered (EN), and critically endangered (CR).

Family DD LC NT VU EN CR Total

Assimineidae 2 2 0 0 0 0 5

Conidae 85 465 25 25 11 3 617

Ellobiidae 3 0 0 0 0 0 3

Haliotidae 0 0 0 0 0 1 1

Hydrobiidae 0 1 0 0 0 0 1

Iravadiidae 0 1 0 0 0 0 1

Neritidae 1 7 0 0 0 0 8

Stenothyridae 1 4 0 0 0 0 5

Thiaridae 0 2 0 0 0 0 2

Total 92 482 25 25 11 4 643

DISCUSSION

The present study contributes to both applied

marine conservation initiatives and food web the-

ory. A complementary approach useful for the

identification and prioritization of a number of

gastropod genera was derived from the empirical

evidence supporting the predicted humped trend

between organism trophic position and body size

in benthic marine gastropods.

Theoretical implications

The expected trophic position trend along the

body size gradient was significant and covered a

large variation in the proportion of carnivorous

species. However, it has to be noted that carnivo-

rous diets do not reach a zero incidence among

173

CARRANZA AND ARIM: VULNERABILITY OF WESTERN ATLANTIC MARINE GASTROPODS

Strombidae Aliger gallus DD Brazil

Strombidae Aliger gigas VU Colombia

Strombidae Aliger gigas VU Guatemala

Strombidae Aliger gigas VU Venezuela

Strombidae Titanostrombus goliath VU Brazil

Strombidae Macrostrombus costatus VU Brazil

Strombidae Macrostrombus costatus VU Guatemala

Strombidae Macrostrombus costatus VU Brazil

Strombidae Strombus pugilis VU Guatemala

Strombidae Titanostrombus goliath VU Brazil

Tegulidae Cittarium pica VU Colombia

Tegulidae Cittarium pica VU Venezuela

Terebridae Hastula cinerea LC Brazil

Tonnidae Tonna galea LC Brazil

Tonnidae Tonna pennata DD Brazil

Turbinellidae Turbinella angulata EN Guatemala

Turbinellidae Turbinella laevigata DD Brazil

Vermetidae Petaloconchus myrakeenae CR Brazil

Volutidae Adelomelon beckii DD Brazil

Volutidae Adelomelon riosi DD Brazil

Volutidae Adelomelon ancilla NA Brazil

Volutidae Odontocymbiola americana LC Brazil

Volutidae Odontocymbiola simulatrix DD Brazil

Volutidae Pachycymbiola brasiliana LC Brazil

Volutidae Voluta ebraea DD Brazil

Volutidae Voluta musica VU Venezuela

Volutidae Zidona dufresnei LC Brazil

Table 5. Continued.

Family Species Red list category Country

larger gastropods, as reported for other taxa as

mammals, birds, and fishes (Arim et al. 2011;

Segura et al. 2016). This suggests that in spite of

being a strategy that became progressively more

difficult to sustain, it represents a frequent strate-

gy even among the larger gastropod species.

It was concluded that larger species were con-

sidered as particularly vulnerable to extinction.

The claim that large consumer at higher trophic

position are particularly vulnerable to extinction

is not new (May et al. 1995). However, trophic

position and body size were considered as posi-

tively related, thus providing redundant informa-

tion for vulnerability assessments. Still, the detec-

tion of a humped trophic position-body size asso-

ciation supports the opposite pattern, showing a

negative association between trophic position and

body size among large and vulnerable species.

This implies that large herbivorous could be

equally or more vulnerable to environmental

change than carnivorous species (Segura et al.

2016). More generally, the negative trophic posi-

tion-body size association along intermediate to

lager body sizes involves an explicit mechanistic

understanding of the energetic constrain, poten-

tially affecting species local persistence or extinc-

tion susceptibility (Burness et al. 2001; Valken-

burgh et al. 2004; Arim et al. 2007a).

So far it is known, the negative association

between trophic position and body size emerge

from the balance between energetic population

demands and the available energy in the environ-

ment for each population (Brown et al. 1993;

Marquet and Taper 1998; Burness et al. 2001;

Arim et al. 2007a, 2016). This balance is affected

by environmental variables such as temperature

due to its effects on metabolism (Arim et al.

2007a). Similarly, since more energy has to be

incorporate into the population to reach the mini-

mum viable population size, predation rates are

expected to increase energetic constrains (Arim et

al. 2011). The total amount of local energy in the

food web is determined by the interaction

between area and productivity at the community

174 MARINE AND FISHERY SCIENCES 36 (2): 165-178 (2023)

or ecosystem level (Schoener 1989), and land-

scape features determines how individuals move

among local populations, integrating spatial

patches of resources (Urban and Keitt 2001;

McCann 2005, 2012). Finally, pollutants nega-

tively affect individual’s metabolism, energetic

demands and resource allocation (Garay-Narváez

et al. 2013). Consequently, the negative associa-

tion between trophic position and body size herein

reported is likely to encompass multiple drivers of

energetic imbalance at individual, population,

community and ecosystem levels. The observed

pattern is therefore connecting ongoing environ-

mental trends with the persistence of particular

species close to the ‘boundary’ of energetic con-

straints. However, it should be noticed that these

mechanisms cannot be equally invoked if there is

no positive association between trophic position

and body size (Dantas et al. 2019).

Practical implications

This being said, we found a poor match

between the genera identified here as being close

to the energetic imbalance and the IUCN Red List

marine gastropods. Not only is none of the fami-

lies currently assessed by the IUCN present in our

‘top 10’ assessment, but our analysis suggests that

most species listed may not be affected by ener-

getic constraints. In contrast, all of our ‘top 10’

vulnerable families and genera are much often

represented on the national or regional list. We are

not saying, in any case, that species listed in the

IUCN are not genuine conservation targets, yet

rather suggesting new avenues for identifying

endangered species. In this line, a new addition to

the IUCN Red List, the scaly-foot snail or sea

pangolin (Chrysomallon squamiferum), exempli-

fies how Red List criteria can be applied to organ-

isms in deep water, poorly known habitats without

baseline population data (Sigwart et al. 2019).

However, it is worth noting that several species

included in national or regional Red Lists does not

rank high in our vulnerability assessment, such as

the olivid gastropods Olivancillaria teaguei and

O. contortuplicata (see e.g. Scarabino 2004),

highlighting that the causes of species declines

are complex and often interconnected, and

encouraging more local or regional assessment of

gastropod species.

Caveats

This approach aims to provide an initial screen-

ing for a large number of species and therefore it

is beyond the scope of this paper to carefully

review the nomenclature provided in the database.

This may have important implications, since the

establishment of a new genera, the description of

new species, and the identification of synonymies

may modify our ranking. Further, taking into con-

sideration that most species are probably micro-

gastropods (Albano et al. 2011), the database can

be regarded as biased towards large-sized species.

For example, in an unprecedented massive collect-

ing effort involving 400 person-days at a single

site in New Caledonia, SW Pacific, 2,738 species

of marine molluscs were recorded (Bouchet et al.

2002). Small-sized species made up the majority

of the diversity, while over 50% of the species had

adult sizes below 10 mm. Top five families in

terms of species richness were ‘Turridae’ (special-

ist polychaete hunters), Eulimidae (echinoderm

parasites), Pyramidellidae (invertebrate ectopara-

sites), Triphoridae and Cerithiopsidae (specialist

feeders on sponges). These five families together

accounting for 29.5% of the mollusc diversity at

the study site. There are thus reasons to expect that

any in-depth study of the diversity of gastropods

in the western Atlantic should also follow this pat-

tern. However, even taking into account the large

number of unreported small gastropods and asso-

ciated taxonomic uncertainties (e.g. genus or fam-

ily-level assignment of species), our results should

be robust since no changes in the shape of the

curve are expected unless a large number of previ-

ously unknown large carnivore gastropods species

is discovered.

CONCLUSIONS

Mechanistic theories provide a better frame-

work for the management of applied problems

with comparatively less demand of empirical

information. The humped trend in trophic posi-

tion with body size support the existence of both

morphological restriction to trophic position

among smaller species and an energetic constrain

for large species. It is interesting to note that few

empirical evidence support the humped associa-

tion when was originally proposed. However, the

analysis at large taxonomic and spatial scale is

progressively supporting its occurrence in differ-

ent ecosystems. Equally or more important, when

the humped pattern is not observed, the operation

of additional mechanisms become evident. In this

sense, a theory based on basic principle provides

a mechanist understanding of biodiversity pat-

terns, even when it fails. The taxonomic biases in

the analysis of the TP-BS relationship and more

generally on the environmental determinants of

food chain length are a matter of concern. The

bulk of evidence about the trophic position-body

size relationship is based on fishes. The analysis

of different organisms, with different traits and

inhabiting different environment is essential for

the validation of general mechanisms and/or the

identification of novel mechanisms to be includ-

ed on theory. Our analysis of the trophic position-

body size relationship for marine gastropods

attempts to be a step in this direction, which pro-

vide in this case, mechanistic based suggestions

for the identification of species of conservation

concern.

ACKNOWLEDGEMENTS

Financial support from CSIC-grupos (ID 657

725) to MA is acknowledged.

175

CARRANZA AND ARIM: VULNERABILITY OF WESTERN ATLANTIC MARINE GASTROPODS

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