Population biology of Nassarius vibex (say, 1822) on a sheltered beach in Southeastern Brazil.
Article Type: Report
Subject: Snails (Distribution)
Home range (Research)
Authors: Cabrini, Tatiana Medeiros Barbosa
Cardoso, Ricardo Silva
Pub Date: 08/01/2012
Publication: Name: Journal of Shellfish Research Publisher: National Shellfisheries Association, Inc. Audience: Academic Format: Magazine/Journal Subject: Biological sciences; Zoology and wildlife conservation Copyright: COPYRIGHT 2012 National Shellfisheries Association, Inc. ISSN: 0730-8000
Issue: Date: August, 2012 Source Volume: 31 Source Issue: 3
Topic: Event Code: 690 Goods & services distribution; 310 Science & research Advertising Code: 59 Channels of Distribution Computer Subject: Company distribution practices
Geographic: Geographic Scope: Brazil Geographic Code: 3BRAZ Brazil
Accession Number: 303011406
Full Text: ABSTRACT Nassariids have a worldwide distribution and are most often found in sheltered embayments in tropical, subtropical, and temperate zones occurring in intertidal and subtidal areas. Species of this genus are scavengers, constituting a major link in the energy flow between carrion, independent of trophic levels, and the environment. The aims of this study are to compare the distribution pattern and the population biology (growth and mortality) of males and females of Nassarius vibex. Sampling was carried out monthly, at spring low tide, from September 2007 through February 2009 at Flexeiras Beach, located in Rio de Janeiro state (22[degrees]), southeastern Brazil. Sampling was conducted according to a systematic design in which biological samples were taken along 6 transects spaced equally and perpendicular to the shoreline. On each transect, 10 equally spaced sampling units (SUs) were established: the first (SU1) at the waterline, the second last (SU9) on the drift line, and the last (SU 10) 3 m above the drift line (supralittoral). Highest population abundances were observed in spring for both sexes. There were significant differences in abundance among the levels in both sexes. Females of N. vibex had lower abundance, grew faster, and had higher mortality and shorter life spans than males. Variations in the population parameters of N. vibex might be regulated by phenotypic adjustment in local conditions, food availability, and, apparently, in this case, by exposure to organotin compounds inducing to the imposex.

KEY WORDS: Nassariids, population biology, Nassarius vibex, sheltered beach, Brazil

INTRODUCTION

Among small invertebrates, which account for part of the macrofauna in beaches, molluscs can reach an astonishingly high biomass in mudflats (Cannicci et al. 2008) and sand beaches (McLachlan & Brown 2006), occupying different trophic levels of the ecosystem food web (Arruda et al. 2003). In this group, nassariids have received special attention because they are one of the faunal dominants (Britton & Morton 1994a) and play an important role in the recycling and reincorporation of decaying matter into the trophic chain of local estuarine ecosystems (Britton & Morton 1994b).

The genus Nassarius has a worldwide distribution on the seabed and on soft shores, and is most often found in sheltered embayments in tropical, subtropical, and temperate zones, occurring in intertidal and subtidal areas (Morton & Chan 1999). Most of the studies of this genus are related to systematic (Cernohorsky 1984) feeding behavior (Morton & Chan 1999, Morton & Chan 2003, Harasewych 1998) and reproductive biology (Houston 1978, Barnett et al. 1980). This genus is used as a bioindicator of pollution by tributyltin (TBT; compound used in antifouling paints applied on ships) by the degree of imposex development (i.e., imposition of male sexual characters in females) in the coastal waters of Europe (Barreiro et al. 2001, Barroso et al. 2005).

There are few studies concerning the life span and population dynamics of nassariids species (Morton & Chan 2003). Among the species most studied are highlighted Nassarius reticulatus (Linnaeus, 1758) (Tallmark 1980, Barroso et al. 2005, Chatzinikolaou & Richardson 2008) and Nassarius festivus (Powys, 1835) (Chan & Morton 2001, Morton & Chan 2003), but few studies have focused on Nassarius species of the South America coast (Demaintenon 2001a, Demaintenon 2001b, Cardoso et al. 2009, Lima-Verde et al. 2010).

Nassarius vibex (Say, 1822) is one of the most important species in the macrofaunal intertidal communities of sheltered sand-muddy beaches on the Silo Paulo and Rio de Janeiro coast (Brazil) (Denadai et al. 2005, Cardoso et al. 2011) and constitutes a major link in the energy flow between carrion, independent of trophic levels, and the environment (Britton & Morton 1994a). There are few studies of this species, and available information refers to feeding behavior (Hurst 1965), response to escape (Gore 1966), and ontogeny of reproductive system (Demaintenon 2001 a, Demaintenon 2001 b). Concurrent studies have reported the incidence of imposex in different populations of N. vibex (Cardoso et al. 2009, Cardoso et al. 2010, Lima-Verde et al. 2010, Cardoso et al. 2011), and feeding behavior (Cabrini & Cardoso, submitted). Apart from these studies, there is no further information about this species on the Atlantic coast of South America. This study compares the abundance, distribution pattern, and population biology of male and female N. vibex, a common and abundant species in the sheltered beaches of Rio de Janeiro state.

MATERIALS AND METHODS

Study Area, and Sampling and Laboratory Procedures

Flexeiras Beach (22[degrees]56' S, 43[degrees]53' W), located on Itacuruca Island, Sepetiba Bay, on the south coast of Rio de Janeiro state, Brazil, is characterized as a sheltered beach using the McLachlan (1980) ranking system. This beach has a microtidal regime with a mean tidal range of 1.5 m, is 350 m long, and is about 30 m wide. The beach slope is of 1/30.6 m. The salinity of the water is nearly constant at 35.

Sampling was carried out monthly at spring low tide in September 2007 through February 2009. Biological samples were taken along 6 transects, spaced equally and perpendicular to the shoreline. On each transect, 10 equally spaced sampling units (SUs) were established: the first (SU1) at the waterline, the second last (SU9) on the drift line, and the last (SU 10) 3 m above the drift line (supralittoral). One sample was taken with a 0.04-[m.sup.2] quadrat sampler to a depth of 25 cm. Each SU was sieved through a 0.5-mm mesh. All individuals were preserved in 70% ethanol. Sediment samples for particle size analysis were taken with a plastic corer with a 3.5-cm diameter to a depth of 10 cm at SU10 (supra), SU5 (middle), and SU1 (infra) in transects 2 and 5.

In the laboratory, shell length of N. vibex was measured with calipers (0.01-mm precision), with the results being grouped into 0.5-mm size classes. The shells were cracked posterially in a vice, and the animals were removed and examined for sex determination. Individuals with a seminal vesicle were identified as male whereas those animals without a seminal vesicle were classified as female (Demaintenon, 2001b).

Sediment samples were dried in an oven at 70[degrees]C and sieved through graded screens to determine mean particle size and sorting parameters for each level (Folk & Ward, 1957). After that, the mean particle size was calculated for these 3 strata. The beach face slope of each transect was measured by the height difference between drift line and waterline (Emery 1961).

Data Analysis

To perform the growth analysis, the monthly length-frequency distributions discriminated by sex were used according to procedures suggested by G6mez and Defeo (1999). Their procedure consists of (1) separating normally distributed components of length frequency distributions through the NORMSEP routine of the FISAT program (Gayanillo et al. 1996), (2) assigning absolute ages to respective cohorts (lengths) and building an age-length key, (3) using the resulting age-length key for each sex to fit the von Bertalanffy growth function (VBGF) for seasonality (Gayanillo et al. 1996) by nonlinear least squares:

[MATHEMATICAL EXPRESSION NOT REPRODUCIBLE IN ASCII]

where [L.sub.t] is length at time t (in millimeters), [L.sub.[infinity]] is the theoretical maximum length attained by the species, K is the curvature parameter, C accounts for the intensity of seasonal growth oscillations, [t.sub.0] is theoretical age at 0 length, and wp is the winter point (i.e., period of growth reduction, expressed as a decimal fraction of the year). To compare the VBGF fitted for each sex, an analysis of the residual sum of squares (ARSS) was performed (Chen et al. 1992).

The standard growth index [phi] (Pauly & Munro 1984) was used as a measure of overall growth performance: [phi] - 2 log10 ([L.sub.[infinity]]) + log10 (K). [phi] has been used successfully as a growth index in sandy beach populations (Defeo et al 1992).

The instantaneous mortality rate (Z) was calculated by the single, negative exponential model using the length-converted catch curve method (Pauly et al. 1995) of the FISAT program (Gayanillo et al. 1996). Life span was estimated by an inverse von Bertalanffy growth equation, considering maximum length (Cardoso & Veloso 1996).

Student's t-test was used to compare abundance of males with females as well as to determine whether there were significant differences between the shell heights of males and females of N. vibex. Nested ANOVA was used to test the null hypothesis that there was no significant difference in the abundance of males and females of N. vibex between months nested within years and also between levels nested within transects. Year and transect were fixed factors, and month and stratum were random factors in the model. One-way ANOVA was performed to compare the spatial variability of mean grain size. Tukey's HSD test was used a posteriori to assess significant differences. Normality and homogeneity of variance was assessed using the Cochran test.

The comparison test of slopes was used to compare mortality rates between males and females of N. vibex (Zar 1999). In all statistical analyses, a significance level of 5% was adopted (Zar 1999).

RESULTS

Habitat Characterization

The mean grain size ranged from 0.25 (medium sand)-l. 30 mm (very coarse sand). One-way ANOVA indicated significant differences of mean grain size among strata (F = 4.57, df = 2/159, P < 0.05), and Tukey's test detected differences only in upper strata (P < 0.05). The beach had a gentle slope, ranging from 1/20 1/40 m.

Population Structure

The greatest population abundance of males and females of N. vibex were registered in the spring (October 2007 and November 2008; Fig. 1). The sex ratio between males and females differed significantly from 1:1 (t-test = 4.73, P < 0.05). The males of N. vibex had greater abundance than females in most months. Between-month variation in population abundance was greater in males of N. vibex, ranging from 5.0-33.3 individuals/[m.sup.2], and in females ranged from to 3.3 21.5 individuals/[m.sup.2]. There was no significant difference in shell length between females and males N. vibex (t-test = 0.47, P < 0.64).

Distribution

The across-shore distribution of females and males N. vibex extended 40 m from the base of a boulder wall to the lower limits of the swash zone (30-cm water layer; Fig. 2). Nested ANOVA indicated no significant differences between abundance of males and females N. vibex between months nested within years (years: [F.sub.(males)11.18] = 1.51, P = 0.4098; months (years): [F.sub.(males)6,18] = 1.54, P = 0.3468), and (years: [F.sub.(females)12,18] = 1.48, P - 0.2468; months (years): [F.sub.(males)3,18] = 0.47, P = 0.8483), but significant differences between levels nested within transects were indicated (levels (transect): [F.sub.(males)50,60] = 14.23, P = 0.0000 and [F.sub.(females)11,60] = 13.19, P = 0.0004). Tukey's test showed that maximum abundance occurred closer to the lower part of the midlittoral (levels 4, 5, and 6), decreasing smoothly toward both extremes of the beach in both sexes.

Populations Parameters

The analysis of growth parameters revealed that there is significant variation in individual growth between the sexes. Female N. vibex grew significantly faster than male, as verified by ARSS analysis ([F.sub.3,151] = 63.7, P < 0.05) and a variation of growth performance ([phi]). The model VBGF with seasonal oscillation through nonlinear fitting explained more than 96% of the variance in females and more than 97% in males of N. vibex. The striking similarity between estimates of the VBGF determined that the statistical comparison via the ARSS did differ between sexes (F ratio = 63.7, P < 0.0000).

[FIGURE 1 OMITTED]

Estimated growth parameters were statistically significant (P < 0.0000; Table 1), with the exception of [t.sub.0] in males and females N. vibex. Weak intra-annual oscillations in growth reflected slower growth in the summer (December) in males (C = 0.36, wp = 1.00), and moderate intra-annual oscillations in growth-reflected minimal growth in the autumn (April and May) in females of the scavenger (C = 0.66, WP = 0.40; Fig. 3). The size of the smallest male individual (shell length (SL)) was 5.33 mm, whereas that recorded in females was smaller (i.e., 4.28 mm in SL). The largest values were 17.44 mm and 17.56 mm in males and females, respectively. The life span ([t.sub.max]) corresponding to these estimates was more than 3.5 y in males and approximately 3 y in females.

A comparison test of slopes showed that the mortality rate showed significant differences between the sexes (t-test = 4.15, P < 0.05). Females N. vibex (Z = 3.61 [+ or -] 0.43/y) had significantly greater mortality than males (Z = 3.44 [+ or -] 0.37/y; Table 2, Fig. 4).

DISCUSSION

Population biology of both sexes of N. vibex differed significantly. Females had a lower abundance, grew faster, had a greater mortality, and a shorter life span than males. However, both sexes showed similar spatial distribution. These patterns were consistent in time.

[FIGURE 2 OMITTED]

The abundance peaks of male and female N. vibex were recorded in spring. However, most studies of Nassarius species observed these peaks in summer (i.e., N. reticulatus (Tallmark 1980, Chatzinikolaou & Richardson 2008) and N. Jestivus (Morton &Chan 2004)). All these studies registered only 1 peak per year. We believe that these unimodal peaks can be related to (1) the well-defined seasons in temperate zones or high-latitude regions or (2) increased activity and feeding response during the warmer months and a decreased activity and response toward the catch during the winter. Tallmark (1980) observed that N. reticulatus became immobile in winter (temperatures <4[degrees]C) and, thus, less vulnerable to predation. Therefore, fluctuations in population abundance can indicate periods of intense reproduction and recruitment, which is frequent in benthic organisms.

The populations of N. vibex in Flexeiras beach were male biased. Torres and Drummond (1999) suggested that if reproductive conditions are deteriorating, the differential costs between males and females may increase. This concept can be related to the environmental conditions typical of the study site. Sepetiba Bay should be regarded as the most dynamic, variable, and organically polluted area (Gomes et al. 2009), thereby accounting for the greatest deviation in the sex ratio from 1:1. Cardoso et al. (2011) observed in this area, on beaches with a high percentage of imposex (considered highly polluted), the sex ratio revealed significant deviations from 1:1 at 3 beaches of the 5 analyzed.

[FIGURE 3 OMITTED]

Greater abundance of males and females N. vibex occurred closer to the lower part of the midlittoral, decreasing smoothly toward both extremes of the beach. This distribution could be associated with grain size, because the middle and lower strata did not showed statistical differences, suggesting that N. vibex occur most abundantly in coarse sands. However, Nassarius iodes (Dall, 1917) no showed preference by sediment type, occurring in fine sand and coarse sand (Cupul-Magana & Te11ez-Duarte 1997). According to Cupul-Magana and Tellez-Duarte (1997), N. iodes are governed more by their feeding habits than by their substrate preferences. Behavior can also influence the distribution, because N. vibex population showed a wide range over the surface of tidally exposed sandflats, in response to active foraging behavior. McKillup and McKillup (1997) also verified the same distribution in other nassariids.

The high SD in abundance of males and females N. vibex by sampling levels (Fig. 2) suggest a clumped distribution of this species, mainly in the intermediate area. Clumped distribution of an N. vibex population can be explained by aggregation around carrion in the intertidal zone, because this food is rarely available naturally and, when it is available, it is found in this zone (Britton & Morton 1994b).

There was no significant difference in shell height between females and males N. vibex, corroborating observations for N. reticulatus (under laboratory conditions) and N. festivus (Chan & Morton 2005, Chatzinikolaou & Richardson 2008).

Analysis of the estimated parameters for male and female N. vibex, and the growth curves derived from them (Table 1, Fig. 3) show that females grew faster than males, corroborating the results of Barroso et al. (2005) with N. reticulatus in Portugal and Chatzinikolaou and Richardson, (2008) with N. reticulatus in North Wales (under laboratory conditions). A possible explanation may be the result of the high percentage of females N. vibex affected by imposex, like that observed in the studied population (approximately 85% of females are affected by imposex; Cabrini unpubl.). The low percentage of non imposex females impeded the construction of a growth curve. Son and Hughe (2000) observed that shell growth of imposex female Nucella lapillus (Linnaeus, 1758) populations was much more accentuated than for normal females. According to these same authors, this difference was a result of the energy meant for reproduction, which was used instead for the growth of the shell, because TBT affects gonadic activity.

[FIGURE 4 OMITTED]

Males N. vibex displayed a seasonal growth pattern--slower growth during the summer. Large males N. vibex showed slower shell growth during the summer months, and this is attributed to the onset of sexual maturity, when energy is diverted from shell growth to reproduction, and this same pattern was also observed in N. reticulatus (Chatzinikolaou & Richardson 2008). Female N. vibex displayed growth reduction during the autumn which was caused by the gonadal cycle of nassariids that matured progressively in autumn, with maturity being achieved in winter (Chan & Morton 2005). Female N. vibex have few energy reserves during maturation: the bulk of energy gained by feeding is channeled into reproduction, not growth. This is common in molluscs, which have a short life cycle, high fecundity, and a sigmoidal growth curve (Chia & Skeel 1973).

Male N. vibex showed weak growth oscillation whereas female N. vibex showed moderate to high oscillation. Seasonal growth was also observed for N. reticulatus at a beach and a lagoon of North Wales, and for N. festivus at 3 beaches in Hong Kong (Morton & Chan 2003). The interruption of growth of these species may be ca used by ranges of ocean temperatures, onshore currents, and climate. Other factors such as food availability have been observed to affect the growth of nassariids (McKillup & McKillup 1997). Some authors suggest that rates of food supply or frequency of feeding opportunities influence feeding behavior of carnivorous snails, because carrion is generally a scarce source in mudflats and sandflats (McKillup & Buttler 1983, McKillup & McKillup 1997).

Growth parameters of the VBGF [L.sub.[infinity]] and K correlated significantly with latitude (Table 3). Some geographical trends emerged from the 12 growth estimates compiled from the literature. There is evidence for latitudinal gradients in both parameters, with [L.sub.[infinity]] positively (r = 0.62, P < 0.0306) and K inversely (r = 0.56, P < 0.0478) correlated with latitude. Some 12-mm differences in [L.sub.[infinity]] were found between the boreal species (carapace length, 28.6 ram) and subtropical species (carapace length, 16.6 mm).

Bivalves and crustaceans (Maze & Laborda 1988, Defeo & Cardoso 2002, Cardoso & Defeo 2004) grow faster at low latitudes--a consequence of an increased metabolic rate (higher oxygen consumption) observed at lower latitudes (Longhurst & Pauly 1987). However, the genus Nassarius show no consistent geographical pattern to growth performance ([phi]). Because N. vibex is localized at a low latitude (22[degrees]S), it has a lower [phi]' than N. festivus (2.81 2.87) (Morton & Chan 2003) at the same latitude, and lower than N. reticulatus (2.76) at a higher latitude (51[degrees]S) (Chatzinikolaou & Richardson 2008). This may be the result of a greater plasticity in life history traits, which enables these species to survive under diverse environmental conditions (Brown 1996).

Natural mortality in females was higher than in males of the N. vibex population. This can be explained by the female N. vibex population of Flexeiras beach, which shows a high incidence of imposex (Cabrini unpubl.), suggesting that TBT is related to sterility and female mortality. This was also seen in Nassarius kraussianus (Dunker, 1846) populations in South Africa (Marshall & Rajkumar 2003).

The greater number of males than females of N. vibex, in almost all months, can be explained by the longer life span of males over females (3.52 y and 2.57 y, respectively), and thus they remain in the population longer. Life span differs within and among species of Nassariidae; male and female N. vibex have a life span similar to N. festivus (22-29 too) in Hong Kong (Morton &Chan 2004) and both have a shorter growing period than N. reticulatus (15 y) in Sweden (Tallmark 1980), and 4-5y in North Wales (Chatzinikolaou & Richardson 2008). These data suggest that tropical species of Nassarius have shorter life spans than boreal species (Table 3).

CONCLUSION

We conclude that the population biology of N. vibex seems to be affected by imposex. Because females N. vibex had a lower abundance, grew faster, and had greater mortality and shorter life span than males. These results can be explained by alterations in gonadic activity caused by the possible presence of TBT or other chemical products that induce the occurrence of imposex.

Results obtained from examining a database of studies with other Nassarius species provided strong support for the latitudinal gradient hypothesis (Defeo & Cardoso 2002): Nassarius species from tropical and subtropical beaches exhibited greater growth and mortality rates, and shorter life spans than species from temperate beaches. These latitudinal trends could be related to variations in temperature, which constitutes an aggregate variable correlated with different simultaneous effects in the nearshore surface zone environment (e.g., food availability).

ACKNOWLEDGMENTS

This article appeared as a dissertation submitted by T. M. B. C. to the Universidade Federal do Estado do Rio de Janeiro in partial fulfillment of the requirements for an MS degree in biological science. We thank Dr. M. Petracco for critically reading the manuscript. This study was supported by Coordenacao de Aperfeicoamento de Pessoal de Nivel Superior (CAPES) postgraduate research studentships. R. S. C. was supported by the Conselho Nacional de Desenvolvimento Cientifico e Tecnologico and by the Fundacao de Amparo a Pesquisa do Estado do Rio de Janeiro.

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TATIANA MEDEIROS BARBOSA CABRINI (1,2) * AND RICARDO SILVA CARDOSO (2)

(1) Programa de Pos-Graducao em Ciencias Biologicas (Biodiversidade Neotropical), Universidade Federal do Estado do Rio de Janeiro (UNIRIO), Rio de Janeiro, RJ, CEP 22290-240, Brazil; (2) Laboratorio de Ecologia Marinha, Depto Ecologia e Recursos Marinhos, Universidade Federal do Estado do Rio de Janeiro (UNIRIO), Av. Pasteur no. 458, Urca, Rio de Janeiro, RJ, CEP 22290-240, Brazil

* Corresponding author. E-mail: taticabrini@hotmail.com

DOI: 10.2983/035.031.0327
TABLE 1.
Growth parameters estimated by nonlinear least squares fit
of the von Bertalanffy function for males and females
of Nassarius vibex.

                                  Males              Females
    Nassarius vibex
       Parameter          Mean (SE)     P      Mean (SE)     P

[L.sub.[infinity]] (mm)       19.20   0.0000       18.11   0.0000
K                              0.68   0.0000        1.25   0.0000
C                              0.36   0.0018        0.66   0.0030
WP                             1.00   0.0000        0.40   0.0000
[T.sub.0]                      0.01   0.9173        0.04   0.5671
[r.sup.2]                      0.99   0.0043        0.96   0.0015
[[phi].sup.2]                  2.40                 2.61
Largest (mm)                  17.44                17.62
[t.sub.max] (mo)               3.52                 2.97

TABLE 2.
Mortality estimates (Z) for males and females of
Nassarius vibex.

Parameters     Males           Females

g              11.35 (0.93)    9.71 (1.05)
Z               3.44 (0.38)    3.61 (0.43)
[R.sup.2]       0.96           0.91

Data are mean and SD (in parentheses). g, regression intercept;
[R.sup.2], determination coefficient.

TABLE 3.
Parameters of the growth curve of von Bertalanffy to species
of the family Nassariidae: asymptotic length ([L.sub.[infinity]]),
growth constant (K), and growth performance index ([phi]').

                         [L.sub.[infinity]]
Species            K            (mm)          [phi]   Latitude

Nassarius vibex   0.68         19.20           2.40   22[degrees]56'S
Nassarius vibex   1.25         18.11           2.61   22[degrees]56'S
Nassarius vibex   1.22           18            2.60   23[degrees]37'S
Nassarius vibex   0.58          18.5           2.30   23[degrees]37'S
Nassarius          2.7          16.6           2.87   22[degrees]15'N
  festivus
Nassarius          2.3          17.4           2.84   22[degrees]15'N
  festivus
Nassarius          2.0           18            2.81   22[degrees]15'N
  festivus
Nassarius         0.85          25.5           2.74   53[degrees]13'N
  reticulatus
Nassarius         0.70          28.6           2.76   53[degrees]13'N
  reticulatus
Ilyanassa         0.13          29.8           2.06   38[degrees]37'N
  obsoleta
Buccinanops       0.22          30.8           2.32   40[degrees]45'S
  globulosum
Buccinanops       0.49          51.6           3.12   40[degrees]45'S
  globulosum

Species           Source

Nassarius vibex   Current study
Nassarius vibex   Current study
Nassarius vibex   Yokoyama (2010)
Nassarius vibex   Yokoyama (2010)
Nassarius         Morton and
  festivus          Chan (2004)
Nassarius         Morton and
  festivus          Chan (2004)
Nassarius         Morton and
  festivus          Chan (2004)
Nassarius         Chatzinikolaou and
  reticulatus       Richardson (2008)
Nassarius         Chatzinikolaou and
  reticulatus       Richardson (2008)
Ilyanassa         Curtis et al. (2000)
  obsoleta
Buccinanops       Narvarte et al. (2008)
  globulosum
Buccinanops       Narvarte et al. (2008)
  globulosum
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