New records of old species: some pelagic polychaetes along the Italian coast

Abstract

Holoplanktonic polychaetes constitute an exception within this taxon, which as adults colonize all the whole variety of brackish water and marine habitats. Nevertheless, they form a distinctive group in marine zooplankton and play an important role in the pelagic trophic nets. Pelagic worms are little studied, especially in the Mediterranean Sea, while information regarding the distribution of the families Typhloscolecidae and Iospilidae along Italian coasts is a century out of date. This paper deals with the state of knowledge of these polychaetes; it summarizes the previous records, updating them with the new records here reported from Tyrrhenian Sea, in order to check whether they have a bearing on Italian fauna. The findings reported in this paper confirm the presence of the Typhloscolecidae, with the species Sagitella kowalewskyi and Typhloscolex muelleri, and of the Iospilidae, with the species Phalacrophorus pictus and Iospilus phalacroides, along the Italian coasts, validating, in each case, their current presence in the Italian fauna. The main morphological features of these species and a dichotomous key for their identification are also reported.

Keywords:

• Planktonic worms
• Typhloscolecidae
• Iospilidae
• holoplankton
• Mediterranean Sea

Introduction

Holoplanktonic polychaetes, which complete their entire life cycle in the water column, constitute an exception within this taxon, which typically includes a very high number of species, that as adults colonize all the variety of brackish water and marine bottoms. Nevertheless, they form a distinctive group in marine zooplankton and play the important role of predator in the pelagic trophic nets. Traditionally, pelagic polychaetes include seven families: Alciopidae, Lopadorhynchidae, Pontodoridae, Iospilidae, Tomopteridae, Poeobiidae and Typhloscolecidae (Fauchald 1977; Rouse & Pleijel 2001); the families Yndolacidae and Flotidae are not included here due to their uncertain phylogenetic relationship (Rouse & Pleijel 2001). Such exclusively pelagic worms are poorly studied, especially in the Mediterranean Sea, being seldom collected among plankton samples.

This paper deals with the state of knowledge of the Typhloscolecidae and the Iospilidae of the Italian fauna: it summarizes old records and updates them with the present records. This is in response to a recent editorial by Boero (2011), which asked zoologists to address questions regarding “new species” as well as “old” ones and to check whether, in either case, they are still being found or have gone “missing”, all this to better assess regional biodiversity. The species from the Italian seas are here characterized with their main morphological features, and a dichotomous key for their identification is also provided.

The Typhloscolecidae consists of only three recognized genera: Sagitella Wagner, Typhloscolex Bush and Travisiopsis Levinsen, the first with only one species, the last two with six species, respectively (Fauchald 1977; Rouse & Pleijel 2001). They are holoplanktonic polychaetes characterized by a tapered, transparent body ranging from 2 to 40 mm in length with up to 50 segments, generally 20–25. Prostomium small, indistinct with a digitiform tip, typical nucal organs; segments with rudimentary lobes bearing a few simple chetae and pygidium with a pair of flattened anal cirri. Most studies relate to their systematics and distribution (Day 1967; Pleijel & Dales 1991; Fernández-Álamo 2004, 2006; Márquez-Rojas et al. 2013), while even basic knowledge about their biology and ecology remains lacking. Therefore, very little information is available on the distribution of the species of this family from the Italian seas: the only recorded data date back to the nineteenth century and to the 1920s (Bush 1851; Reibisch 1895; Lo Bianco 1904; Fauvel 1923).

The Iospilidae include pelagic polychaetes distinguished by slender and small size, prostomium without antennae, peristomium bearing a pair of ventral palps, all composite chaetae and an eversible pharynx, in some cases armed. Four genera are included in this family: Phalacrophorus Greeff, Iospilus Viguier, Pariospilus Viguier and Iospilopsis Augener, the first two genera with three and two species, respectively, and the latter two with only one species each, according to Fauchald (1977) and Rouse and Pleijel (2001). However, other authors (Day 1967; Dales & Peter 1972; Fernández-Álamo 2009a) recognized only the genera Phalacrophorus Greeff and Iospilus Viguier in the family, including Pariospilus Viguier in the genus Iospilus and Iospilopsis antillensis Augener as synonymous with Phalacrophorus uniformis Reibisch, 1895. Some papers deal with their geographical distribution and new records in Atlantic and Pacific oceans, but very few data concerning the Mediterranean Sea are available. In the case of the Italian seas, the records of Iospilidae also date back to the early 1900s (Lo Bianco 1904; Fauvel 1923).

Materials and methods

Plankton samples were collected by means of a net with a 40 cm mouth diameter and constructed throughout of nylon with a mesh aperture of 100 μm, with horizontal hauls in superficial waters in areas of 20–50 m depth along the northwestern coast of Isola d’Elba (Tuscany, Italy), from 2011 to 2015. The net was gently rinsed and samples were transferred to Petri plates containing sea water for sorting and observation in vivo. Identification of specimens was carried out under stereo and light microscopes. Sampling was carried out by Dr Marco Lucarelli (University of Rome “Tor Vergata”).

Results

Two species of Typholscolecidae for a total of 15 individuals were collected: five belonging to Sagitella kowalewskyi and 10 to Typhloscolex muelleri. They were recorded over 3 years between August and April. Two species of Iospilidae were also collected: Phalacrophorus pictus, with five individuals, and Iospilus phalachroides, with 18 individuals, respectively.

Class Polychaeta

Order Phyllodocida

Family Typhloscolecidae

Genus Sagitella Wagner, 1872

Type species: Sagitella kowalewskyi Wagner, 1872

Sagitella kowalewskyi Wagner, 1872

(Figure 1)

Figure 1. Dorsal view of an entire specimen of Sagitella kowalewskyi. Scale bar: 1 mm.

Main morphological features

Body slender, cylindrical, tapered at both ends, transparent, with around 25–50 segments and 5–15 mm in length. Prostomium conical, anteriorly pointed, ending with a slender palpode. Eyes absent. Large ciliated flaps occurring to both sides of the prostomial end. A retort-shaped organ underneath the pharynx under a dorsal thickening. Behind this, two nuchal organs forming two semi-circular ridges curved in towards their posterior ends. The anteriormost two segments with a pair of foliaceous cirri; the following segments bearing rounded dorsal and ventral cirri. Parapodia slightly pronounced with rudimentary chaetigerous lobes with a single acicula and few simple chaetae, appearing at the third segment. Two large foliaceous anal cirri.

Type locality: Mediterranean (Gulf of Naples).

Geographic distribution

S. kowalewskyi is widely distributed in the Atlantic Ocean in northeastern, tropical and southern waters (Southern 1910; Fauvel 1916, 1923; Støp-Bowitz 1951; Day 1967; Orensanz & Ramirez 1973; Pleijel & Dales 1991; Fernández-Álamo 2006; Márquez-Rojas et al. 2013); in the Pacific Ocean in tropical and subtropical regions, along the north to southeastern coast and in northwestern waters (Chamberlin 1919; Okuda 1938; Dales 1957; Berkeley & Berkeley 1960; Tebble 1962; Ushakov 1974; Fernández-Álamo 2004; Fernández-Álamo & Sanvincente-Añorve 2005); and in the southwest Indian Ocean (Day 1967).

Mediterranean distribution

Tyrrhenian Sea, Gulf of Naples (Lo Bianco 1904), Corsica, Calvi (Fauvel 1916).

Genus Typhloscolex Bush, 1851

Type species: Typhloscolex muelleri Bush, 1851

Typhloscolex muelleri Bush, 1851

(Figure 2a and b)

Figure 2. a, Dorsal view of an entire specimen of Typhloscolex muelleri. b, lateral view of an entire specimen of T. muelleri. Scale bar: 500 µm.

Main morphological features

Body anteriorly wide and posteriorly tapering, transparent, with around 15–25 segments and 2–5 mm long. Prostomium bearing a filiform palpode with a ventral cilindrical swelling. Broad semicircular ciliated lobes dorsally and ventrally on the prostomium, which looks like a plate perpendicular to the length axis of the body ending with the filiform palpode. Sides of head enfolded by a pair of flattened sinous cirri. A pair of similar flattened cirri on the two following segments; the others with foliaceous dorsal and ventral cirri. Small, not clearly differentiated parapodia. Two or three short acicular chaetae from the fifth segment, but usually present only in the posterior segments and rarely projecting beyond the parapodial lobe. Small and ovate anal cirri.

Type locality: Adriatic Sea, Trieste.

Geographic distribution

Common species in the Pacific Ocean, both in tropical sub-tropical regions and in Artic and Antartic waters (Chamberlin 1919; Fauvel 1936; Dales 1957; Berkeley & Berkeley 1960; Tebble 1962; Reish 1968; Ushakov 1974; Fernández-Álamo 2004; Fernández-Álamo & Sanvincente-Añorve 2005; Bilbao et al. 2008; Gagayev & Kosobokova 2012); Atlantic Ocean from northern to southern regions and Antartic waters (Treadwell 1943; Tebble 1960; Day 1967; Orensanz & Ramirez 1973; Ushakov 1974; Fernández-Álamo 2006, 2009b; Márquez-Rojas et al. 2013); and in the southwestern Indian Ocean (Day 1967, 1975).

Mediterranean distribution

North Adriatic Sea, Tyrrhenian Sea, Gulf of Naples (Lo Bianco 1904); Monaco, Gulf of Marseilles (Fauvel 1923; Peres 1954).

Family Iospilidae

Genus Phalacrophorus Greeff, 1879

Type species: Phalacrophorus pictus Greeff, 1879

Phalacrophorus pictus Greef, 1879

(Figure 3)

Figure 3. Dorsal view of an entire specimen of Phalacrophorus pictus. Scale bar: 250 µm.

Main morphological features

Body cylindrical, transparent, 3–6 mm long with 15–30 segments. Prostomium rounded without antennae and with one pair of brown eyes. First and second segments fused and bearing two pair of small tentacular cirri, the first pair much shorter than the second pair, the second segment only with setae. Two and three anterior segments with reduced parapodia with very few setae and without dorsal and ventral cirri. At fourth segment and posteriorly parapodia increasing in size. Dorsal and ventral cirri rounded, shorter than the podial lobes. Compound chaetae spinigerous with long pointed shaft-blades. Muscular pharynx armed with two curved chitinized jaws at the anterior end. Branched chromatophores ventral to the parapodia. Pygidium without appendages.

Type locality: Atlantic Ocean Canary Islands.

Geographic distribution

Atlantic Ocean from northern to southern regions and Arctic area (Reibisch 1895; Fauvel 1916, 1923; Friedrich 1950; Støp-Bowitz 1951; Orensanz & Ramirez 1973; Ushakov 1974; Druzhkov et al. 2000; Fernández-Álamo 2009a; Tovar-Faro et al. 2013); Pacific Ocean tropical, Arctic and Antarctic sectors (Ehlers 1913; Fauvel 1936; Treadwell 1943; Dales 1957; Tebble 1962; Ushakov 1974; Fernández-Álamo & Sanvincente-Añorve 2005; Fernández-Álamo 2006; Bilbao et al. 2008); Indian Ocean (Day 1975).

Mediterranean distribution

Bay of Alger (Viguier 1886), Tyrrhenian Sea, Gulf of Naples (Lo Bianco 1904), Gulf of Marseille (Peres 1954).

Genus Iospilus Viguier, 1886

Type species: Iospilus phalacroides Viguier, 1886

Iospilus phalacroides Viguier, 1886

(Figure 4)

Figure 4. Dorsal view of an entire specimen of Iospilus phalachroides. Scale bar: 250 µm.

Main morphological features

Small, transparent and slender body, 2–3 mm long with 15–20 segments. Prostomium rounded without antennae but with one pair of short palps. Two eyes. Four anterior segments with reduced parapodia. First and second segments fused and bearing two pairs of small tentacular cirri, the first much shorter than the second pair, and one pair of tufts of 2–3 chaetae. Parapodia of segments two and three with reduced chaetigerous lobes without dorsal and ventral cirri. Posterior segments with uniramous parapodia with short dorsal and ventral cirri and chaetigerous lobes with compound chaetae. All compound chaetae spinigerous with long shaft ending pointed. Eversible muscular pharynx unarmed. Starlike chromatophores. Pygidium large without appendages.

Type locality: Mediterranean Sea, Bay of Algiers.

Geographic distribution

Atlantic Ocean (Fauvel 1916; Jiménez-Cueto et al. 2006; Fernández-Álamo 2009a); Pacific Ocean (Treadwell 1943; Dales 1957; Fernández-Álamo & Sanvincente-Añorve 2005); Indian Ocean (Day 1967, 1975).

Mediterranean distribution

Bay of Algiers; Tyrrhenian Sea, Gulf of Naples (Lo Bianco 1904); southern Spanish coast (Fauvel 1916).

Discussion

Studies on biodiversity deal with different aspects of species – biogeographic, evolutive, genetic, ecological – but most of them quote descriptions of new species, suggesting an increase in biodiversity. Such additions extend the checklists of our fauna, but rarely do we pause to consider the “old” species, or the species listed as being present in a given geographical area in the past and now supposed to be still present (Boero 2011).

Typhloscolecidae and Iospilidae represent an interesting case study regarding this issue, being the records of the species belonging to these families from Italian seas published approximately a century ago. The same outdated records have been also reported in the checklist of Italian fauna of polychaetes (Castelli et al. 1995). Only a few recent data are available from the literature (Batistić et al. 2012), but extracted from the faunal list published for other purposes and missing any observations about the record of such polychaetes; these neglected species have hence passed unnoticed.

Holoplanktonic polychaetes prove to be widely distributed in all the oceans of the world; in particular, their distribution throughout the Atlantic and Pacific Oceans and in Arctic and Antarctic waters reflects the course of campaigns of oceanographic exploration. By contrast little is known on the distribution of pelagic polychaetes in the coastal and neritic environments. Subsequently, a lot of them are considered cosmopolitan (Tebble 1962; Ushakov 1974; Rouse & Pleijel 2001) and typical species of open sea waters (Støp-Bowitz 1948; Day 1967). Only recently have detailed studies focused on particular distributions of pelagic polychaetes in inshore localities of the Pacific and Atlantic Oceans. In fact, Fernández-Álamo (1987, 2006) and Fernández-Álamo and Sanvincente-Añorve (2005) explained the distribution pattern of the neritic assemblages of Typhloscolecidae and Iospilidae found along the Mexican Pacific coasts, suggesting that specific feeding habits and different tolerance to the variability in environmental conditions may influence these species along coastal waters.

In fact, notwithstanding their low abundance in the neritic waters, such pelagic polychaetes play an important role in the plankton food web. Some Typhloscolecidae are reported as predators on chaetognaths, while also being considered ectoparasites of such a zooplanktonic group (Øresland & Pleijel 1991; Øresland & Bray 2005). The same authors registered their maximum abundance in the areas with abundant neritic animals, such as preys or possible hosts; they also investigated the role of Typhloscolecidae as being possibly responsible for the headless chaetognaths frequently recorded in plankton samples from the Indian Ocean. Likewise, Márquez-Rojas et al. (2013) recorded some Typhloscolecids and other pelagic polychaetes along the Atlantic continental shelf of the Venezuela coasts, where the mixing processes at the edge of the shelf cause nutrients to arise and promote a general increase in zooplankton abundance, this being a food supply for such carnivorous pelagic polychaetes. Regarding the phytophagous Iospilus phalacroides, which was reported to feed on diatoms (Orensanz & Ramirez 1973), Fernández-Álamo and Sanvincente-Añorve (2005) explained its distribution in the neritic region according to the higher concentrations of phytoplankton along the Mexican Pacific coasts.

In recent years, studies of such holoplanktonic polychaetes have been undertaken in tropical Atlantic and Pacific areas (Fernández-Álamo & Sanvincente-Añorve 2005, 2006; Márquez-Rojas et al. 2013; Tovar-Faro et al. 2013), while no-up-to date information on their distribution in Mediterranean Sea is available for these families of polychates.

Our present data reported in this paper confirm the occurrence of the Typhloscolecidae, with the species Sagitella kowalewskyi and Typhloscolex muelleri, and of the Iospilidae, with the species Phalacrophorus pictus and Iospilus phalacroides, along the Italian coasts, proving the current presence of these species in the Italian fauna and validating the old records. Therefore, the findings of individuals of such pelagic polychaetes in the space of 4 years suggests that these species are a current and real component of the Italian fauna, and not just an occasional record.

The finding of such neglected species confirms that old records represent significant data in the monitoring on biodiversity. Investigation of the “old” species to check whether they are still being found remains a useful task for zoologists interested in examining the state of the fauna and changes in biodiversity (Boero 2011).

Key to families, genera and species

1. Pelagic polychaetes with the prostomium without appendages and eyes but ending with a median palpode; all chaetae simple Typhloscolecidae 2

   -Pelagic polychaetes with the prostomium with two short palps and two eyes, without other appendages and palpode; all chaetae compound Iospilidae. 4

2. Prostomium with large transverse ciliated lobes dorsally and ventrally. Typholscolex muelleri

   - Large transverse ciliated lobes absent 3

3. A pair of nuchal organs forming two semi-circular ridges posteriorly curved without projecting lobes; caruncle absent. Sagitella kowalewskii

   - A pair of nuchal organs with free posteriorly projecting lobes; a caruncle between them usually present Travisiopsis*

4. Eversible pharynx unarmed . Iospilus phalacroides

   - Eversible pharynx armed with a pair of curved jaws. 5

5. First 2–3 segments with reduced parapodia without dorsal and ventral cirri. Phalacrophorus pictus

   - Up to 11 anterior segments with reduced parapodia without dorsal and ventral cirri. Phalacrophorus uniformis**

*Species of this genus are not included in Italian fauna.

**Species not included in Italian fauna.