Marine Biology

, 165:81 | Cite as

Egg masses and development of Falsilunatia eltanini (Mollusca: Gastropoda): a deep-sea naticid from a Southwestern Atlantic Canyon

  • Andres Averbuj
  • Pablo E. Penchaszadeh
  • Guido Pastorino
Original paper

Abstract

A series of cruises to the Mar del Plata Submarine Canyon (38°S/54°W) off Argentina in 2012–2013 have provided biological material that enables insights into the various modes of development of deep-sea invertebrates at depths up to 3500 m. This study describes the unusually large encapsulated embryos of the globose moon snail, Falsilunatia eltanini Dell, 1990 (Naticidae), and compares them with another direct-developing naticid from the same collections, Bulbus carcellesi. Embryos of F. eltanini develop in sand ribbon egg masses that contain up to 6 conspicuous egg capsules, 5.0–8.5 mm diameter. Each F. eltanini egg capsule contains a single, ~ 170-µm diameter egg and abundant, white, supplementary food. This allows the crawling pre-hatching juveniles to grow to 4.7 mm shell diameter. Different stages of development were found among multiple egg collars collected on the same date, which suggests a long reproductive season that could be continuous or periodic (lasting more than a year). The number of whorls in the hatchling juvenile shells and the significant size they attain confirm the occurrence of a long period of embryonic development. This reproductive strategy requires a large maternal investment in the very large egg capsules and abundant supplementary food. Within Naticidae, this extraordinary modality is only observed in several species inhabiting deep-sea and boreal cold waters.

Introduction

There are few developmental studies that can help understand the reproductive mode and general biology of deep-sea gastropods (Bouchet and Warén 1993; Montgomery et al. 2016). In particular, there were few studies on the reproduction of deep-sea naticids, only one from the Southern hemisphere (Hain and Arnaud 1992), until a recent study on Bulbus carcellesi from a Southwest Atlantic Canyon off the Argentine north coast (Penchaszadeh et al. 2016).

Egg masses of Naticidae are typically sand-encrusted rings or collars (Ankel 1930; Lebour 1936; Thorson 1935, 1940, 1946; Giglioli 1955; Natarajan 1957; Amio 1963; Gohar and Eisawy 1967; Bouchet and Warén 1993; Huelsken et al. 2008; Pastorino et al. 2009) with the exception of the Australian genus Conuber (Polinicinae), which has gelatinous egg masses different from those of other known naticids (Murray 1966). Giglioli (1955) reviewed the variability in egg masses and egg capsule spaces (the cavity or chamber where the egg capsules are laid) in Naticidae. Naticid egg capsule spaces were described for the first time by Thorson (1935) as globular egg cavities, and classified according to internal features such as rigidity of the walls and conspicuity of the egg capsules.

Most naticid eggs develop within the egg capsules until hatching as planktonic veliger larvae, but in some species hatchlings emerge as crawling juveniles (Ankel 1930; Thorson 1935; Lebour 1936; Thorson 1936, 1940, 1946; Giglioli 1955; Natarajan 1957; Amio 1963). In direct-developing naticids, i.e., no pelagic larval stage, the egg capsule contains a considerable amount of an albumen-like, white dense substance (henceforth referred to as supplementary food) in the intracapsular fluid, the only known exception being Euspira catena which has nurse eggs (Ankel 1930; Hertling 1932; Lebour 1936; Thorson 1946; Giglioli 1955). These are non-developing (or arrested in early development) eggs consumed by the offspring (Lardies and Fernández 2002; Perry and Roitberg 2006).

To study the reproductive mode of deep-sea invertebrates from the Southwest Atlantic, a series of cruises were scheduled for the Project ‘Invertebrates of abyssal bottoms (submarine canyons) up to 3500 m depth’ (BID—PICT 2013 2504). This region of the world was poorly known, but some previous studies led to the prediction that a great number of invertebrates have protected development, and lack a free-swimming larvae stage (Tyler and Young 1992; Pearse and Lockhart 2004). Recent studies have provided a significant increase in the knowledge of the development of some gastropod species, and several Classes of Echinodermata and Cnidaria (Pastorino 2016; Penchaszadeh et al. 2016, 2017; Berecoechea et al. 2017; Lauretta and Penchaszadeh 2017; Martinez and Penchaszadeh 2017; Rivadeneira et al. 2017). In the present study we describe the egg mass of Falsilunatia eltanini Dell, 1990, a moon snail collected from the deep-sea waters (up to 2400-m depth) off Buenos Aires province, Argentina, including a characterization of its egg capsule spaces and embryonic development.

Materials and methods

Adult F. eltanini were collected in 2012 and 2013 by dredge trawl and bottom trawl fishing net from 21 of 66 sampling stations in the Mar del Plata Submarine Canyon area (38°S/54°W), Argentina, during three cruises to the Argentine Continental Slope aboard R/V ‘Puerto Deseado’ (Table 1).
Table 1

Stations of R/V ‘Puerto Deseado’ in Mar del Plata Submarine Canyon area where Falsilunatia eltanini egg masses and individuals were collected in 2012 and 2013, indicating sampling site information and collected material

Station

Latitude, S

Longitude, W

Depth, m

Fishing gear

# of egg masses (range of capsules per mass)

Date

Specimens of F. eltanini

1

37°58.0´

55°12.7´

201

Dredge trawl

1 (2)

10 Aug 2012

 

2

37°57.2´

55°11.1´

291

Dredge trawl

2 (1–2)

10 Aug 2012

 

24

37°54.2´

54°02.6´

2420

Fishing net

28 (1–6)

14 Aug 2012

18L + 14D

32

37°59.8´

55°12.5´

319

Dredge trawl

1 (4)

17 Aug 2012

7L + 20D

53

37°52.6´

53°54.2´

1763

Fishing net

7 (1–2)

8 Sept 2013

 

55

37°52.2´

53°51.6´

1712

Fishing net

2 (1–2)

8 Sept 2013

13L + 2D

60

37°51.7´

54°4.6´

1584

Dredge trawl

1 (5)

10 Sept 2013

 

L live, D dead

Complete or fragmented egg masses were found at only 7 of the 21 stations. These were preserved in 4% formalin-sea water solution, and examined under a stereomicroscope and measured (length, width and thickness) with a caliper. Measurements were recorded for complete egg masses only. The longest axes of eggs, embryos and shells were measured using a 0.01-mm precision ocular micrometer.

Species identification of the embryos used shell, radular and opercular features, as well as calcified shells. Radulae were prepared according to the method described in Pastorino (2005). Radulae of embryos were obtained by dissolving the entire specimen in sodium hypochlorite. The main developmental features of each stage were described. Images of the egg masses and adult shells were recorded using a Nikon D100 digital camera with a 60-mm macro lens. All images were digitally processed. After the study, the material was deposited in the Invertebrate Collection of IBIOMAR, CCT CONICET—CENPAT (CNP-Inv 2749, 2750, 2751, 2752, 2753, 2754, 2755) and Museo Argentino de Ciencias Naturales ‘Bernardino Rivadavia’ (MACN-In 41474, 41475, 41476, 41477, 41478, 41479).

Results

Species identification

Only adult shells of F. eltanini were used by Dell (1990) to describe this species from the deep-sea just west of South Georgia Island. The species has a characteristic rounded outline and solid shell, with very weak spiral ornamentation consisting of fine striae and axial growth lines all over the surface (Fig. 1e). The periostracum is thick and brownish. An interesting feature is the corneous, suboval, paucispiral operculum with closely spaced growth lines and distinctive ridged suture. A characteristic ornamentation of the operculum consists of irregular and sometimes oblique spiral microridges clearly seen in the embryonic opercula and close to the suture in the adults (Fig. 1e). The radulae obtained from the embryos and adults of F. eltanini are illustrated in this study for the first time, confirming the generic allocation by Dell (1990). The radulae have a hemispherical, triangular rachidian tooth, with only one large cusp and two lateral processes and conspicuous denticles in the rachidian base (Fig. 2).
Fig. 1

Falsilunatia eltanini: adult shell in apertural (a), lateral (b) and adapertural (c) view. Operculum of adult (d). SEM of an embryonic operculum (e). Operculum of adult of Bulbus carcellesi (f) and SEM of the embryonic  operculum (g) of B. carcellesi. Scale bars 1 cm (ad, f), 1 mm (e, g)

Fig. 2

Falsilunatia eltanini: SEM photograph of radulae from adult (a) and embryo (b). Arrowheads indicate the denticles on the sides of rachidian that are distinctive of F. eltanini, in adult and embryo. Bulbus carcellesi: SEM photograph of radulae from adult (c) and embryo (d). Scale bars 100 µm (a), 50 µm (b, d), 200 µm (c)

A sympatric naticid species, Bulbus carcellesi, was collected at some of the same stations but more frequently at shallower depths. The adult shell is larger, more globose and thinner than that of F. eltanini with a wide aperture and low spire. In addition, while the latter is always chalky white, F. eltanini has a dark brownish periostracum that clearly identifies the species. Moreover, differences between adults of these species include the denticles on each side of the rachidian cusps and on the laterals, present in F. eltanini and absent in B. carcellesi. Concurrently, the marginals are more elongated and thinner in B carcellesi than in F. eltanini, and the inner is always bicuspid. These features are already present in the embryonic radula and together with those of the corneous operculum leave no doubt about the species identification. They are particularly useful when the calcification of the embryos is weak and the shell is still not completely formed.

Characteristics of the egg mass

The egg masses were identified as belonging to F. eltanini, based on the similarity in the radulae, operculum and shell morphology of late embryos and adults. Falsilunatia eltanini spawn flat, slightly curved egg masses, with narrow non-undulating margins and sand grains embedded in a gelatinous matrix, forming a short ribbon. In this study, egg masses were 7.4–28.2 mm long, 6.7–13.6 mm wide and 3.1–5.9 mm thick (n = 27). Egg masses contained 1–6 egg capsule spaces in a single row within their rigid walls. Most egg masses collected were clearly fragments of 1–4 egg capsule spaces. These spaces were globular chambers made of sand grains glued together, which bulged prominently on the external face of the egg mass, clearly visible to the naked eye (Fig. 3a–f). Each space contained a single egg capsule (4.1–8.5 mm diameter; n = 59) with only one egg/embryo inside, which was immersed in the supplementary food completely filling the capsule early in development (Fig. 4a). No nurse eggs or sibling embryos were found.
Fig. 3

Falsilunatia eltanini: egg masses. Dorsal (a, c, e) and ventral (b, d, f) view of three egg masses. Bulbus carcellesi: dorsal (g) and ventral (h) views of comparable egg masses. Scale bar 1 cm (ah)

Fig. 4

Falsilunatia eltanini: developmental stages. Dissected egg capsule space showing egg capsule with supplementary food content (a), blastula/gastrula (b), early ‘veliger’ with incipient ciliated velum (c), ‘veliger’ with tentacles, developed ciliated velum and ciliated foot (d), ‘pediveliger’ showing a translucent developed flexible shell and a thick operculum, note supplementary food (e, f), pre-hatching stage inside the egg capsule with scarce supplementary food (g), pre-hatching with 2.5-whorls shell and thick operculum (h) and pre-hatching with a calcified extremely thin shell, which broke during manipulation (i). ec egg capsule, f foot, m mantle, o operculum, ss sand egg capsule space, sf supplementary food, sh shell, t tentacle, v velum. Scale bars 1 mm (a, fi), 200 µm (bd), 500 µm (e)

General features of developmental stages

The earliest embryonic stage observed in Falsilunatia eltanini corresponded to early cell divisions (several micromeres and macromeres) and blastulae and gastrulae (Fig. 4b), measuring on average 190.0 ± 26.9 (mean ± SD) µm. The supplementary food substance was dense and abundant. The early ‘veliger’ stage was characterized by an antero-posterior elongation of the embryo (320.2 ± 72.3 µm in diameter), with the ciliated mouth in antero-ventral position. The anterior (cephalic) part of the embryo was characterized by the development of a ciliated incipient velum (Fig. 4c). In the ‘veliger’ stage, embryonic growth showed an incipient spiralization together with the formation of a translucent organic matrix of the future shell. At this stage, the embryo (798.0 ± 449.2 µm) was more elongated, and a bi-lobed ciliated velum was completely developed. The intracapsular food was still abundant. At the ‘pediveliger’ stage, a developing foot could be distinguished. The velum was still visible, but as the embryo increased in size, the velum showed signs of resorption (Fig. 4d). The embryo had now consumed a considerable portion of the intracapsular material and had increased in size with a shell of up to1 ½ whorls and 1.57 ± 0.39 µm in diameter. The pre-hatching stage was the largest and had 1 ½–2 ¾ whorls. It had a developed foot, and a translucent, birefringent shell that was somewhat flexible. Late embryos were slightly calcified. The velum was completely reabsorbed, and a thick, rigid operculum had developed. Embryos at this stage were 2.80 ± 1.08 mm in shell diameter with a maximum observed size of 4.70 mm (Fig. 4e–i). Intracapsular food was scarce. Eyes were not observed in F. eltanini embryos at any stage, consistent with the absence of eyes in the adults. Table 2 shows the features and measurements for each embryonic stage.
Table 2

Distinctive features of embryonic stages of Falsilunatia eltanini

Stage

Description

Mean (SD) embryo (µm) or shell diameter (mm)

Range in embryo (µm) or shell diameter (mm)

Whorls

N egg capsules (n egg masses)

Early embryo

Roundish egg to blastula/gastrula

190.0 ± 26.9 µm

171–209 µm

2 (2)

Early ‘veliger’

Incipient velum, stomodeum antero-ventral

320.2 ± 72.3 µm

228–437 µm

6 (6)

‘Veliger’

Bi-lobed, ciliated velum

798.0 ± 449.2 µm

380–1273 µm

3 (3)

‘Pediveliger’

Foot developed, partially reabsorbed velum, growing shell

1.57 ± 0.39 mm

1.05–1.97 mm

0.25–1.5

5 (5)

Pre-Hatching

Foot fully developed, velum completely resorbed, shell with whorls

2.80 ± 1.08 mm

1.44–4.70 mm

1.5–2.75

11 (11)

One egg capsule was studied from each egg masses, thus numbers in the last column are coincident

Discussion

Studies on the reproductive modalities of ~ 30 species of Naticidae show that most of them hatch as planktonic veliger larvae, as reviewed by Pastorino et al. (2009). However, complete intracapsular (direct) development was documented in ten species in which hatchlings are crawling juveniles (Ankel 1930; Thorson 1935, 1940; Giglioli 1955; Amio 1963; Penchaszadeh et al. 2016). Among them, four species share similarities with features of Falsilunatia eltanini egg masses, all found in cold or deep habitats (Table 3). These species were grouped by Giglioli (1955) as ‘Division I’ based on the internal features of the egg masses such as the rigid walls and large egg capsules (900–3000 µm). They live either in North Atlantic cold waters, as Cryptonatica affinis and Euspira pallida that have two to four bands of egg capsules in the walls of the sand ribbons, or in the deep-sea, as Bulbus carcellesi and F. eltanini that have a single row of giant egg capsules (Thorson 1935; Penchaszadeh et al. 2016). In all cases non-undulating margins are present. Northern species have a semi-circular egg mass, while the southern species are only slightly curved (Thorson 1935; Giglioli 1955; Penchaszadeh et al. 2016). Additionally, Hain and Arnaud (1992) included some data for ‘Falsilunatia notorcadensis’ from the Weddell Sea, Antarctica, recording an egg mass with at least 6 egg capsules, with a single hatchling per capsule and a shell height of 4.7 mm; no other characteristics were reported. Two egg masses from another naticid species from Antarctica (74°41′S, 35°04′W and 74°30′S, 26°24′W; depths of 500 and 483 m, respectively) with a developmental modality similar to F. eltanini were reported by Hain (1990). These egg capsules were assigned to Kerguelenatica delicatula as Amauropsis (Kerguelenatica) grisea in Hain (1990) (Engl 2012). Hain (1990) found a single embryo per egg capsule space, at the veliger stage (1–2 mm in shell diameter), surrounded by ‘white’ substance (supplementary food). In a list of Alaskan mollusks, Baxter (1987) stated that records of Cryptonatica clausa from the Arctic also included C. aleutica and C. russa. According to the author these species could not be distinguished by shape, morphometrics, nor apparently by their radulae, but differed primarily in the shape of the egg case. Cryptonatica clausa and C. russa appear to have features that fit into Giglioli’s Division I or II (direct development) as conspicuous swellings of 2–5 mm in 2–5 rows were observed (Giglioli 1955). In contrast, the egg mass of C. aleutica was smooth, which suggests the possibility of a planktonic veliger larval development. Baxter’s list has neither illustrations nor other information, which hampers further discussion.
Table 3

Comparison of egg masses of cold water naticid species with direct development

Species

Capsules egg mass−1

Range in capsule diameter (μm)

Embryos capsule−1

Egg diameter (μm)

Embryo nutrition

Hatchling diameter (μm)

Maximum # of whorls at hatching

Source

Euspira pallida, as E. groenlandica

13–38

2500–3000

1

2250

‘White’

1500–1700

1.5–2

Thorson (1935)

Cryptonatica clausa

13–24

2000–2250

1

 

‘White’

1500

1.75–2

Thorson (1935)

Bulbus carcellesi

1–6

8780–14,140

1

< 200

‘White’

4250–6000

3.25

Penchaszadeh et al. (2016)

‘Falsilunatia notorcadensis’

> 6

 

1

  

4700

 

Hain and Arnaud (1992)

Falsilunatia eltanini

1–6

5000–8500

1

171–209

‘White’

1440–4700

2.5

Present study

‘White’ = supplementary food

Most egg masses collected in this study were fragments of 1 or 2 egg capsules. Considering the fragments and complete egg masses it is likely that the egg masses of F. eltanini would normally contain 4–6 egg capsules. Falsilunatia eltanini egg capsules and embryos are the second largest in the family, after the recently described B. carcellesi which also had up to 6 egg capsules per mass, 8.8–14.1 mm in diameter (Penchaszadeh et al. 2016). The egg masses of F. eltanini are smaller than those of B. carcellesi, and they lack the wide sand-encrusted margins surrounding the egg capsules in the latter. Falsilunatia eltanini is the only species in this genus inhabiting this particular area and depth range. Some authors have included B. carcellesi in the genus Falsilunatia (Torigoe and Inaba 2011). Bulbus carcellesi co-occurred at some sample sites, but was more abundant at 201–1275 m (egg masses present at 201–1006 m), while F. eltanini was more abundant at 1144–2934 m (egg masses present at 1584–2934 m). Moreover, the two species are distinguishable from each other based on morphological characters already present in the embryos. The larval radulae in F. eltanini and B. carcellesi are very similar in structure to the adult radulae. Minor differences are usually the size, particularly length and thickness, of marginal and lateral teeth. Wether this character, similar radulae in embryos and adults, extends to the whole family is unknown. Other deep-sea neogastropods, such as some Volutidae, show a similar pattern between radulae of larvae and adults (Penchaszadeh et al. 2017).

The egg size of marine gastropods has been related to particular developmental modalities: small eggs species develop into planktonic (either planktotrophic or lecithotrophic) larvae that hatch in a shorter time and attain smaller hatching sizes. The opposite reproductive features are observed in larger egg species with benthic or direct development, which according to Thorson prevail towards higher latitudes (Thorson 1946, 1950; Levitan 2000; Gallardo and Penchaszadeh 2001, Kohn 2012). However, extraembryonic resources, such as intracapsular fluid and nurse eggs allow direct development in species that have smaller egg (Fioroni 1982; Rivest 1986; Penchaszadeh 1988; Young 2003) which would be a third developmental modality. Among Naticidae the three developmental modalities occur. Occasionally, two different life history patterns have been reported for a single naticid species (Pedersen and Page 2000). However, the literature on naticid development includes the entire range of modes of larval development, including planktonic veliger larvae that are either lecithotrophic or planktotrophic.

There is great variation in the size of uncleaved eggs in the family Naticidae, ranging from less than ~ 100 μm (Natarajan 1957) to ~ 1000 μm in diameter (Thorson 1940). Other naticid species with a similar egg size to that of F. eltanini (~ 170–200 µm in diameter) hatch as planktonic veligers (Thorson 1940; Amio 1963). Falsilunatia eltanini produces a single egg capsule per space with only one embryo inside as in B. carcellesi, F. notorcadensis, E. pallida and C. affinis. The embryo is surrounded by a dense mass of albumen-like substance in the early stages of development (Thorson 1935) and as development proceeds this supplementary food decreases in abundance. These supplementary extraembryonic resources enable larger hatchling sizes associated with higher survival rates (Spight 1976; Moran 1999; Moran and Emlet 2001), which appears important for reproductive success in extreme environments such as the deep-sea (Montgomery et al. 2016). The reproductive modality observed in these five species may be explained as a case of convergence that provides a great amount of supplementary food (filling the enormous egg capsules with it) and optimizes chances of embryo survival in an extreme environment with limited food resources. Albumen-like substances are found in all the directly developing Naticidae, with the exception of Euspira catena. Egg capsules in that species have another intracapsular nutritive source very uncommon in the Naticidae: nurse eggs (Ankel 1930; Hertling 1932; Lebour 1936; Thorson 1946; Giglioli 1955; Pastorino et al. 2009). The large size of F. eltanini egg capsules allows for an enormous quantity of supplementary food within it. This supplementary food was depleted before hatching.

The smallest embryo found for F. eltanini measured 171 μm and corresponded to early cell division. The egg capsule volume is five-fold less in F. eltanini than in B. carcellesi (in both species filled with similar supplementary food), representing an enormous difference in the amount of nutritive resources for the developing embryos. This characteristic may explain the smaller pre-hatching size of F. eltanini compared with the giant hatchling (up to 6-mm diameter) in B. carcellesi (Penchaszadeh et al. 2016). It is likely that we did not observe the hatching stage, as we found embryos with very thin calcified shells, but no older embryos. The adults of F. eltanini and B. carcellesi have calcified shells, those of F. eltanini being thicker.

The deep-sea has often been considered a constant environment, with little to no seasonal variation (Tyler and Young 1992). Moreover, fluctuations of productivity or other parameters do not necessarily relate to reproductive seasonality among deep-sea molluscs (Scheltema 1994). This stability enables certain species to reproduce asynchronously or continuously throughout the year (Rokop 1974; Giese and Kanatani 1987; Tyler and Young 1992). Species showing high synchronicity or apparent seasonality in their reproduction generally do not occur in deep-sea habitats (Rokop 1974), and often have small eggs and planktonic larval development (Tyler et al. 1982). Different stages of development were found among multiple egg collars collected on the same date (early stages as well as enormous crawling juveniles), which suggests a long reproductive season. This has been observed for various other deep-sea gastropods, for example, the Rissoidae, Benthonella tenella (Rex et al. 1979), the Buccinidae, Colus jeffreysianus (Colman et al. 1986) and the Calliotropidae, Calliotropis ottoi (Colman and Tyler 1988). Reproduction in F. eltanini may be continuous or periodic if the gametogenic cycle lasts more than one year, with different overlapping generations of oocytes as reported for the deep-sea sea star Ctenodiscus australis (Rivadeneira et al. 2017). A recent study of the deep-sea buccinid Buccinum escalariforme in mesocosms [i.e., darkened tanks with chilled running seawater to resemble seasonal fluctuations in the study area (0–5 °C) and fluctuation in particulate organic matter deposition] was reported to spawn in March 2014, September 2014, and March 2015, possibly the first evidence for seasonality of reproduction in a deep-sea gastropod (Montgomery et al. 2016). This reproductive behavior was correlated with seasonal inputs of deposited organic matter that might provide stimuli for oogenesis in this species (Montgomery et al. 2016). However, further studies including the gametogenic cycle would be needed to confirm such seasonal reproduction.

The dominance of non-planktonic larvae in gastropod species inhabiting deep-sea and other cold water environments compared to planktonic gastropod larvae from other (i.e., shallow) environments is remarkable (Clarke 1992; Young 2003). Non-planktonic development includes not only encapsulation, but also provision of nutritive resources as intracapsular fluid (Colman and Tyler 1988), nurse eggs (Giglioli 1955; Colman and Tyler 1988; Montgomery et al. 2016) or albumen-like or ‘white’ substance (Penchaszadeh et al. 2016). A similar trend of protection of the offspring was observed in echinoderms, in the form of large eggs (Tyler et al. 1982) and brooding (Rivadeneira et al. 2017). In semelparous mysid crustaceans (Childress and Price 1978; Brandt et al. 2004) and octopus (Robison et al. 2014), females guard the egg mass until the embryos hatch as adult-like individuals. As reviewed by Pearse and Lockhart (2004), species of the major species-rich clades in the Antarctic often brood their young. In contrast, most clades of brooders are not present in the Arctic; brooding species in this environment are exceptional since most species have pelagic larvae. Therefore, a ubiquitous pattern is not found for cold water environments and the diversity of clades living in these environments. As more knowledge becomes available on the reproduction of invertebrates inhabiting such physically extreme environments, previous interpretations will require revision (Pearse and Lockhart 2004).

The occurrence of a convergent embryonic developmental modality among naticid species in very cold environments (deep-sea and cold boreal Atlantic and even Antarctic waters) is suggested, including encapsulation in large (visible to the naked eye) capsules and abundant extraembryonic nutrition (Hain 1990; Penchaszadeh et al. 2016). In most marine invertebrates, embryonic development takes longer at lower environmental temperatures (Childress and Price 1978; Robison et al. 2014). A successful direct development mode in such environments requires a large maternal investment that is expressed in F. eltanini in extremely large egg capsules, abundant nutritive content, and large embryo size, which are unique in the Naticidae (Thorson 1935; Hain and Arnaud 1992; Penchaszadeh et al. 2016). The number of whorls in the hatchling juvenile shell and the size they attain could be indicative of a long period of embryonic development in F. eltanini.

Notes

Acknowledgments

Special thanks are due to Alan Kabat for his thoughtful suggestions that highly improved the manuscript, to the Editors and to Juan Pablo Livore for reviewing the final manuscript. We thank Melina Atencio and Valeria Teso and the people involved in the ‘Talud Continental’ expeditions. This work was funded by PICT 2013–2504 from Agencia Nacional de Promoción Científica y Tecnológica, and PIP 0253 from Consejo Nacional de Investigaciones Científicas y Técnicas. This is publication #99 of LARBIM.

Compliance with ethical standards

Conflict of interest

Andres Averbuj, Guido Pastorino and Pablo E. Penchaszadeh declare that they have no conflict of interest.

Ethical approval

All applicable international, national, and/or institutional guidelines for the care and use of animals were followed.

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Copyright information

© Springer-Verlag GmbH Germany, part of Springer Nature 2018

Authors and Affiliations

  1. 1.LARBIM (IBIOMAR), CCT CONICET, CENPATPuerto MadrynArgentina
  2. 2.Laboratorio de Ecosistemas Costeros-MalacologíaMuseo Argentino de Ciencias Naturales CONICETBuenos AiresArgentina

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