The genus Terschellingia de Man, 1888

The genus belongs to the family Linhomoeidae (Monhysterida), a taxon of heterogeneous nature without known holapomorphy (Lorenzen, Reference Lorenzen1994). Three subfamilies are recognized: Desmolaiminae Schneider, Reference Schneider1926, Eleutherolaiminae Gerlach & Riemann, Reference Gerlach and Riemann1973 and Linhomoeinae Filipjev, Reference Filipjev1922. The genus Terschellingia belongs to the Desmolaiminae, a subfamily mainly characterized by (modified from Schneider, Reference Schneider1926): cuticle smooth or faintly annulated, second and third circle of anterior sensilla close (6 + 10) or separate (6 + 6 + 4), amphidial fovea circular, buccal cavity conical and presence of cardia between pharynx and intestine.

Terschellingia, emended diagnosis. Desmolaiminae. Cuticle faintly striated (may appear smooth under light microscope); amphidial fovea rounded. Buccal cavity absent or minute, cuticularized structures (i.e. teeth) rarely present. Pattern of anterior sensilla: 6 + 6 + 4; the labial sensilla only detectable in larger specimens at high magnification and they are almost in the same level that cephalic sensilla; the four cephalic sensilla setiform, submedian and non-jointed. Pharynx shape variable (with or without set off bulb). Cardia valve rather well developed. Secretory–excretory pore located posterior to the nerve ring. Male diorchic, posterior testis reflexed; spicules curved; gubernaculum with apophyses (poorly developed in one species). Female didelphic–amphidelphic (rarely monodelphic–prodelphic), ovaries outstretched, vulva at about mid-body. Tail anteriorly largely conical, posterior part cylindrical and tail tip rounded, without terminal setae.

Type species: Terschellingia communis de Man Reference De Man1888.

Evaluation of taxonomic diagnostic characters among Terschellingia species

The examination of six morphological (=qualitative) and 17 morphometric features allowed to detect the characters of diagnostic value within the genus. Scatter plots of selected morphometric features were analysed in order to look for those which discriminate among groups of species (Figure 1). The features related to body size (length and de Man's ratios a and b) not only showed poor discrimination among species but also tend to show high correlation (Fortuner, Reference Fortuner1990). In addition, the significant relationship between body dimensions and food availability (dos Santos et al., Reference Dos Santos, Derycke, Fonsêca-Genevois, Coelho, Correia and Moens2008) suggested the lesser diagnostic value. Features related to relative position and size of amphidial fovea, length of the tail (relative to anal body diameter) and length and shape of spicules allowed discrimination of groups of species (Figure 1) and were therefore considered of diagnostic value.

Fig. 1. Scatter plots of morphometric features of valid species of the genus Terschellingia. Measurements correspond to holotype. Labels defined as 3–4 first types of the specific names in Table 3 (except for T. longisoma = lonm). Dashed lines indicate possible cut-values for discriminating among species.

Morphological characters would be highly useful in diagnosis of species. We selected six features: presence/absence of teeth, shape of cephalic setae (papilliform and setiform), presence/position of cervical setae (absent, at level of or posterior to amphidial fovea), presence/absence of pharyngeal bulb, developed/reduced apophysis and shape of the tail (conical portion less or more than 50% of total length of tail). The number of developed ovaries appears to be a feature with taxonomic value, but it is not always described, mainly in old studies. The presence/pattern of precloacal supplements has been used extensively as a taxonomic character; although supplements are present in at least one species (T. longicaudata) they are hard to observe with light microscope, and thus less useful as a diagnostic character.

Discrimination of species within the genus Terschellingia

Within the genus, 38 nominal species have been described. However, according to our results only 15 of them are considered as valid. From the 23 non-valid species, 14 are species inquirendae and nine are junior synonyms of one of the valid former species (see Table 2 for explanations). Pictorial (Figure 2) and tabular (Table 3) keys summarize the main diagnostic characters for discrimination among valid species of Terschellingia and an explanation follows below.

Fig. 2. Outline of 15 valid species of the genus Terschellingia. Drawings not to same scale and reproduced from original description (except for T. communis, reproduced from Gerlach, Reference Gerlach1963).

Table 2. Outline of non-valid Terschellingia species. Abbreviations: sp. inq., species inquirend a; syn., synonymy. For additional abbreviations see Table 1. The numbers of specimens used in the original descriptions are indicated.

The presence of small teeth in the buccal cavity is the main taxonomic feature that distinguishes T. elegans and T. sulfidrica from the other species of the genus. Both species can be differentiated from one another by shape and length of spicules (more curved and larger in T. sulfidrica; Figures 1 & 2), tail shape (>50% conical in T. sulfidrica versus >50% filiform in T. elegans), and the presence of a single ovary in T. sulfidrica. According to Gagarin & Vu-Thanh (Reference Gagarin and Vu-Thanh2003), T. elegans closely resembles T. supplementata (here synonymized with T. longicaudata) but mainly differs from it and in extension also from T. longicaudata by the presence of a tooth, the shorter cephalic setae and the absence of cervical setae.

Three species of Terschellingia have the amphidial fovea located relatively far from the anterior body end: T. capitata, T. distalamphida and T. longisoma (Figures 1 & 2). Terschellingia distalamphida can be distinguished from the other two species by the presence of cervical setae and a filiforme tail (<50% conical and more than 12 anal diameters length). Terschellingia capitata is characterized by a large and muscular pharyngeal bulb (bar 3.4 versus 1.3 and 1.9 in T. distalamphida and T. longisoma respectively). Terschellingia longisoma is characterized by a very long and thin body (total length holotype: 2156 µm, a = 90); also it has a tail very poorly attenuated to the terminus (Gagarin & Vu-Thanh, 2006).

Terschellingia papillata is the only species of the genus with cephalic setae papilliforme. The spicules of T. papillata are very similar to those in T. longicaudata (Figure 2), but the former lacks the cervical setae and it has a larger conical portion of the tail.

On the basis of presence/absence of pharyngeal bulb, two groups of species can be distinguished: a group of ten species with clear set-off pharyngeal bulb (six of them already characterized above). The remaining four species (i.e. T. communis, T. lissa, T. longicaudata and T. vestigia) differ from each other by a combination of characters (Table 3).

Table 3. Main diagnostic characters differentiating the valid species of the genus Terschellingia de Man Reference De Man1888. Abbreviations in Table 1; additional abbreviations: ceph. setae, shape of cephalic setae; cerv. setae, presence/position of cervical setae (first somatic setae) with respect to amphidial fovea; phar. bulb, pharyngeal bulb; post., posterior. States of character: 0 = absence; 1 = presence. *No females described.

Terschellingia lissa can be differentiated from the other three Terschellingia species by a larger size of amphidial fovea (>0.5 cbd), conical portion of the tail is less than 50% of total length and lack of cervical setae. In addition T. lissa has a relatively small body length within the genus (<1000 µm).

The main differences between T. communis and T. longicaudata rest on the length of the conical portion of the tail. The length of the tail appears to be useful for differentiating most of the specimens (i.e. T. communis c′: <12; T. longicaudata c′: >12; Figure 1). However, we recorded in Cienfuegos Bay some unusually large male specimens of T. longicaudata with ‘short tail’ (c′: 5.5–8.8); and some females of T. communis can have a relatively long tail (c′: 10–12). The original description by de Man (Reference De Man1888) of T. communis showed a completely conical tail with pointed tip, not found in any other description of the species; the latter feature was discussed by Timm (Reference Timm1962) as ‘problematic’. Reviewing the literature and based upon our own material, we found that the tail tip is rounded. The length of spicules appears to be an important feature for differentiating between the holotypes of T. communis and T. longicaudata (Figure 1). However, there are not clear differences between T. communis and T. longicaudata regarding spicule length on the basis of the few studies including absolute measurements: 54–61 µm (1.6–1.9 abd) versus 47–48 µm (1.7 abd) in Warwick et al. (Reference Warwick, Platt and Somerfield1998); 38–44 µm (1.2–1.4 abd) versus 38–113 µm (1.4–1.9 abd) in specimens from Cienfuegos Bay. However, since Figure 1 shows a clear cut-value around 1.7 abd for holotypes, we include the spicule length as a useful character for diagnosis.

Other important, but more difficult to standardize, differences between T. communis and T. longicaudata are regarding to cervical setae, shape of cardia, and shape of spicules and gubernaculum apophysis. So far, the main difference with respect to the pattern of cervical setae is the position (at level of amphidial fovea in T. longicaudata; posterior to the fovea in T. communis). However, the number of cervical setae and their relative position in the anterior region is variable in specimens of T. longicaudata as has been reported by other authors (e.g. Chitwood, Reference Chitwood1951; Timm, Reference Timm1961; Wieser & Hopper, Reference Wieser and Hopper1967; Bhadury et al., Reference Bhadury, Austen, Bilton, Lambshead, Rogers and Smerdon2008) and from specimens from Cienfuegos Bay. The cardia is larger, rounded and without pericardiac cells in T. communis versus cylindrical and rounded by intestinal cells in T. longicaudata; nevertheless the shape would be affected by the processes of preservation and mounting for the specimen. In relation to accessorial reproductive structures, T. communis has a proximal end of spicules non-cephalated and the apophysis of gubernaculum wide and cuticularized in ventral border; T. longicaudata has a cephalated spicule with central septum in manubrium and a narrower apophysis of the gubernaculum. However, intraspecific variability in spicule shape and gubernaculum has been observed (i.e. compare T. communis in Figures 2E & 3E).

Fig. 3. Species of the genus Terschellingia recorded in Cienfuegos Bay, Caribbean Sea. T. gourbaultae: (A) anterior part; (B) tail; (G) spicular apparatus; T. communis: (C) anterior part; (D) tail; (E) spicular apparatus; T. longicaudata: (F) anterior part; (G) tail; (H) spicular apparatus.

The high number of junior synonymies of T. longicaudata (in total five; see Table 2) could be explained by: (i) high abundance and cosmopolitan distribution leading to numerous descriptions by different authors; and (ii) high morphological plasticity. There are, for instance: large variation in body habitus (de Man's ratio a ranged 29–40 after Timm, Reference Timm1962), sexual dimorphism in size of amphidial fovea (♂ 0.3 cbd; ♀ 0.5 cbd after Wieser, Reference Wieser1956) and in relative position of amphidial fovea (Amp ♂ 0.5; ♀ 0.9 after Vitiello, Reference Vitiello1969), different aspect of spicular apparatus (Vitiello, Reference Vitiello1969) and presence or absence of precloacal supplements.

The diagnosis of T. vestigia is based on the presence of a reduced dorsal apophysis of the gubernaculum. However, since only one male was described, putative intraspecific variability cannot be assessed. We prefer to maintain this species as valid given that it is relatively easy to check this diagnostic character.

Five species of Terschellingia lack a set-off pharyngeal bulb; the table elaborated by Austen (Reference Austen1989) and summarizing main differences among these species has been updated by Guo & Zhang (Reference Guo and Zhang2000) and Huang & Zhang (Reference Huang and Zhang2005) with addition of one species respectively but without further discussion. We found that some of the proposed diagnostic characters are less useful for species differentiation. Length-related measurements (total body length, de Man's ratio a and tail length) were notably overlapping among species. The body length is not a good main diagnostic character, even for species with extreme body sizes (T. austenae <950 µm; T. major > 3436 µm) since in some monhysterids, body size is influenced by environmental factors such as food availability (dos Santos et al., Reference Dos Santos, Derycke, Fonsêca-Genevois, Coelho, Correia and Moens2008). In addition, the length of spicules in five specimens of T. gourbaultae from Cienfuegos Bay was shorter (59–66 µm) than specimens from the Tamar Estuary, England reported by Austen (Reference Austen1989) (80–88 µm), suggesting high variability in this character.

Two species (T. austenae and T. claviger) have less than 50% of total tail length conical, with the distal third portion filiforme. These species can be differentiated from each other by the relative size of amphidial fovea and the position of cervical setae; in addition, the length and shape of spicules and apophysis of gubernaculum would be useful diagnostic characters (Table 3).

Differences among T. brevicauda, T. gourbaultae and T. major are more subtle on the basis of taxonomic characters currently proposed. Austen (Reference Austen1989) pointed out that the shorter tail in T. brevicauda (c′ 3.5–4.3) allows its differentiation from other species; the tail of T. gourbaultae is effectively larger (c′: 5.5–8.0 after Austen; 5.1–9.4 in specimens from Cienfuegos Bay). An additional feature, maybe less variable (and so more useful), is the position of the cervical setae (Table 3). The spicular apparatus is different in appearance (Figure 2) and in absolute measures (spicule length: 47–53 µm for T. brevicauda versus 80–88 µm for T. gourbaultae), but other morphometric measures such as relative length and shape of spicules failed to show differences (Figure 1). The unique record of T. brevicauda in North Carolina, USA (Ott, Reference Ott1972) does not allow to assess possible intraspecific variability.

Two conspicuous features allow to identify specimens belonging to T. major; i.e. large body size (>3000 µm), and presence of precloacal supplements (>30). The latter character has been recorded in T. sulfidrica; but in specimens described from several geographical regions (e.g. T. longicaudata) the presence and number of supplements appeared variable. On the basis of the proposed differential diagnosis for species of Terschellingia (Table 3) the discrimination between T. gourbaultae and T. major would become problematic if high intraspecific variability exists in the latter species. The differences in relative length of spicules between holotypes suggest the usefulness of this feature for discrimination (Figure 1).

Description of Terschellingia species from Cienfuegos Bay

For most of the features measured on specimens from Cienfuegos Bay they were relatively different from the data for the holotypes. This suggests a continuum in the size of body structures and a high morphological plasticity in the three species analysed. The high morphological plasticity in some nematode genera with numerical dominance (e.g. Daptonema, Sabatieria and Terschellingia) could adjust in a more general model relating morphological plasticity and ecological success (Hollander, Reference Hollander2008 and references herein). It should be interesting to assess the level of intraspecific variability (i.e. morphological plasticity) in rarer species of nematodes; and also to test for relationships between morphological plasticity and ecological dominance in free-living marine nematodes.

The morphometric data are presented in Table 4 and illustrations in Figure 3. We only include in this section those features with some variation compared to older descriptions of the species.

Table 4. Morphometric data (minimum–maximum) for males and females of Cuban specimens of the genus Terschellingia. Abbreviations in Table 1; additional abbreviations: amph Ø, diameter of amphidial fovea; amp.dist, distance of amphidial fovea to anterior end; gubern., gubernaculum; spic.arc and spic.cor, length of spicules as arc and cord respectively.