Monstrilla grandis Giesbrecht, 1891

Suárez-Morales, Eduardo, Goruppi, Alenka, de Olazabal, Alessandra & Tirelli, Valentina, 2017, Monstrilloids (Crustacea: Copepoda) from the Mediterranean Sea (Northern Adriatic Sea), with a description of six new species, Journal of Natural History (J. Nat. Hist.) 51 (31 - 32), pp. 1795-1834 : 1822-1827

Monstrilla grandis Giesbrecht, 1891

( Figures 9 (d – f) and 10 – 13)

Material examined

Adult male from NIS collected on 20 July 2016 at station 6 ( Figure 1 ), harbour of Trieste , North Adriatic Sea, specimen partially dissected, mounted on slides in glycerine, sealed with Entellan ®. Slide deposited in ECO-CHZ-009527. Adult male and adult female from station 1 collected 12 May 2014 from same locality, specimen partially dissected, mounted on slides in glycerine, sealed with Entellan ®. Slide deposited in ECO-CHZ- 009528. Adult male and adult female from station PALOMA ( Figure 1 ) collected 22 August 2014 from the Gulf of Trieste , specimen partially dissected, mounted on slides in glycerine, sealed with Entellan ®. Slide deposited in ECO-CHZ-009529. Four adult males and adult female from station 3 ( Figure 1 ) collected 13 July 2010, harbour of Trieste , specimen undissected, ethanol-preserved, vial deposited in ECO-CHZ-009530 . Three adult females from station 1 collected 30 June 2014, harbour of Trieste , specimen undissected, ethanol-preserved, vial deposited in ECO-CHZ-009531 . Twelve adult males, eight adult females from station 1, same locality, collected 15 July 2015, same locality, three specimens partially dissected, mounted on slides in glycerine, sealed with Entellan ®, slides deposited in ECO-CHZ-009532; remaining specimens undissected, ethanol-preserved (ECO-CHZ-009533) . Five adult males, one adult female from station 3 ( Figure 1 ) collected 8 July 2009, harbour of Trieste , Adriatic Sea, undissected, ethanolpreserved, vial deposited in ECO-CHZ-009534 .

Remarks

The male and female specimens from Trieste were easily identified as M. grandis following the valuable illustrated reports of the species by Dolgopolskaya (1948), Shen and Bai (1956), Ramírez (1971) and Suárez-Morales (2000c). Our specimens have the same body shape, proportions, fifth leg structure and armature as described and depicted in previous taxonomic reports ( Shen and Bai 1956; Ramírez 1971; Suárez- Morales 2000c; Suárez-Morales et al. 2013).

This presumably widespread species was originally described from the southwestern Atlantic at 49S, 65W by Giesbrecht (1891), but only a brief diagnosis was published at that time; the male was depicted from specimens collected at the Gulf of Naples ( Giesbrecht 1893). Based on specimens from Toulon Bay, in the Mediterranean, Suárez- Morales (2000c) described the male following upgraded standards. The species has been recorded from different geographic areas of the world, including the Black Sea ( Dolgopolskaya 1948), the China Seas ( Shen and Bai 1956), the Caribbean area ( Fish 1962; Nutt and Yeaman 1975), Argentina ( Ramírez 1971), the Mediterranean ( Rose 1933; Isaac 1974, 1975), Chile ( Marín and Antezana 1985), Costa Rica ( Suárez-Morales et al. 2013) and Korea ( Chang 2014). The record by Ramírez (1971) is the geographically closest to the type locality. Based on the analysis of our male and female specimens from Trieste, we provide additional comparative data and notes on the variability of this species in order to contribute to completing the morphologic background of the nominal M. grandis . This information is expected to support an eventual distinction of new species.

In their respective reports on M. grandis from Costa Rica and Korea, Suárez-Morales et al. (2013) and Chang (2014) recognised that the apparently cosmopolitan distribution of this species could be concealing a complex of cryptic species. Rose (1933) recognised that the report of the male of M. grandis by Scott (1904) could refer to a different species. Suárez-Morales et al. (2013) detected some differences in the males from different geographic areas, to which we add our analysis of the male specimens. These characters include the relative length of the cephalothorax with respect to the total body length: the shortest cephalothorax (43% of body length) is known in the Costa Rica population ( Suárez-Morales et al. 2013, fig. 2B), followed by specimens reported by Giesbrecht (1893) from Naples and by Ramírez (1971) from Argentina (47%), by Suárez-Morales (2000c) from Toulon (48%), Dolgopolskaya (1948) from the Black Sea (48.7%), Shen and Bai (1956) from China (49%) and a range of 49.2 – 50.5% was observed in the male specimens from Trieste ( Figures 10a and 11a ). The antennule length with respect to the total body length shows some variation: 48% (Naples), 55% ( Argentina), 56% ( China), 57% (Black Sea), 60% ( Costa Rica), 61% (Toulon), 59.3% – 64.8 % (Trieste). There are subtle differences on the position of the oral papilla along the cephalothorax: 44% (Naples), 45 – 43% (Trieste), 46% ( Costa Rica), 49% ( China), 53% (Toulon); and in the relative lengths of the male fourth antennular segment: 20% (Black Sea), 23% ( China), 24.4% ( Argentina), 26% (Naples), 26.6% (Toulon), 27% ( Costa Rica) and 28 – 32% in our specimens from Trieste. The body size is also remarkably variable, less than 0.8 mm (Naples, Black Sea, Costa Rica) up to more than 1.5 mm (Naples, Barbados, Argentina, Brazil, Scotland) (see Scott 1904; Dolgopolskaya 1948; Fish 1962; Ramírez 1971; Suárez-Morales 2000c; Razouls et al. 2005 – 2017). In the samples from Trieste, the male specimens length ranged between 0.64 – 1.05 mm (average = 0.86 mm, n = 15). The cuticular ornamentation of the ventral surface of the cephalothorax was described only in the specimens from Toulon Bay ( Suárez-Morales 2000c) and the pattern differs from the Costarrican male ( Suárez-Morales et al. 2013); in the former specimens, there is only one pair of strongly chitinised nipple-like processes vs three pairs of such structures (plus an additional medial one) in the Costarrican specimen, these arranged in a relatively tight pattern ( Suárez-Morales et al. 2013, fig. 2E). In our specimens from Trieste the ornamentation resembles that of the Costarrican specimens, with three pairs of nipple-like processes, but in our specimens these are arranged in a more separate pattern and, instead of having a single medial papilla-like structure posterior to this group, there are additional bud-like structures grouped either in a transverse row of three (arrows in Figure 9 (b, e, f)) or in two symmetrical inclined rows each with 2 – 4 such elements ( Figure 11 (b – d)). These bud-like groups are associated to a ventral cephalic protuberance, which is pronounced in our specimens (arrows in Figures 9 (f) and 11(b)) and in those reported by Giesbrecht (1893), but is weakly developed in the specimens from Toulon ( Suárez-Morales 2000c, fig. 2C) and Costa Rica (Suárez- Morales et al. 2013, fig. 2D). Also, the Toulon male specimens have a pair of protuberant processes on the inner and outer margins of the caudal rami ( Suárez-Morales 2000c, fig. 3G); these have not been reported in any other of the examined records, including the males from Trieste ( Figures 10 (f) and 11(g)). The length of the single fifth leg seta is similar in all cases, reaching midlength of the caudal rami or even slightly beyond it when stretched backwards ( Figures 10 (f, g) and 11(g, i)). Details of the male antennulary armature ( Grygier and Ohtsuka 1995) of our specimens can be compared only with records from Toulon ( Suárez-Morales 2000c) and Costa Rica ( Suárez-Morales et al. 2013). In the first segment, element 1 has some variation, even in individuals from Trieste; it can be as long a segment ( Figure 10 (b)) as in the Toulon specimens ( Suárez-Morales 2000c, fig. 2E) or about half its length ( Figure 11 (e)) as in the Costarrican specimen ( Suárez-Morales et al. 2013, fig. 2C). In the three groups compared, elements 2v2,3 are the longest of group 2v-d. This is also discernible from illustrations by Giesbrecht (1893) (Naples), Shen and Bai (1956) ( China) and Ramírez (1971) ( Argentina). On the fourth segment, element 4v1 is consistently the longest of the setal group 4v-d in the populations compared ( Giesbrecht 1893; Ramírez 1971; Suárez-Morales 2000c; Suárez-Morales et al. 2013), but showed some variation in size among the specimens from Trieste ( Figures 10 (b) and 11(e)). At least two of the males from Trieste showed a modified (proximally expanded) caudal seta ( Figure 10 (d, e)), but the other specimens observed have normal caudal setae ( Figure 10 (a, f) and 11(a, g)). It is noteworthy to mention that some female specimens showed an expansion on two caudal setae (arrows in Figure 13 (i)). In addition, the leg 3 basipodal seta is relatively longer in our specimens ( Figure 11 (f)) than in the specimen from Costa Rica ( Suárez-Morales et al. 2013, fig. 3C).

A comparison of the females of M. grandis was presented by Chang (2014), who correctly concluded that a complete redescription of the type specimens or topotypic specimens of both sexes should be performed in order to fully compare them with the European and Asian specimens to clarify the taxonomic status of this species. Molecular studies should also be used to determine if there is in fact a divergence among these populations. We noticed a certain degree of variation among the female specimens from Trieste; their size ranged between 1.3 – 1.9 mm (average = 1.55, n = 14), they are longer than the Korean specimen (1.3 mm excluding caudal rami) ( Chang 2014), the Toulon specimens, exhibiting a wide size range (0.8 – 1.5 mm) ( Suárez-Morales 2000c), but smaller than the Argentinian specimens (2.6 mm) and those reported from Barbados ( Fish 1962) (4.2 mm). The comparative analysis of the cephalic ornamentation showed some variation among specimens from Trieste, always resembling the pattern observed in the males, with an anteriormost set of bud-like processes arranged in two vertical rows, with 4 or 5 elements on each row ( Figures 12 (c) and 13(c)) or with an asymmetrical alignment of these rows ( Figure 12 (d)), the latter pattern depicted also by Huys and Boxshall (1991) and Chang (2014). A similar, but tighter pattern of these elements was observed by Suárez-Morales (2000c) in material from Toulon. The presence of frontal sensilla ( Figures 12 (c) and 13(g)) is also a variable intra-population character, it was absent in some specimens from Trieste ( Figure 12 (d)). In all populations compared female M. grandis lack a cephalic ventral protuberance ( Figures 12 (b) and 13(c)) described in some males of this species. The female antennule armature of our specimens from Trieste showed some coincidences when compared with that of the male in pre-geniculation segments; elements 2v2,3 are the longest of group 2v-d ( Figures 12 (a) and 13(b)) and element 4v1 is the longest of group 4v-d. Also, the female genital double-somite has an incomplete suture visible on dorsal view and reaching halfway around the lateral margin ( Figures 12 (f) and 13(d)) and observed in other populations as well ( Dolgopolskaya 1948; Huys and Boxshall 1991; Suárez-Morales 2000c; Chang 2014), but not in the report on the Argentinian specimens, in which the suture appears to be more extended around the ventral surface of the somite ( Ramírez 1971, figs. 2 and 4). The female fifth leg has, in all the populations compared, a thumb-like inner process on the exopodal lobe; it was clearly present in the specimens from Trieste (arrows in Figures 12 (h) and 13(d – f, h, i)). As noticed by Chang (2014), Giesbrecht ’ s (1893) illustration of this appendage could be deemed as incomplete, because this is a species character.

As mentioned by Suárez-Morales et al. (2013), part of the morphometric variations revealed in this analysis could be attributed to the different techniques of observation, preservation or illustration processes related to these records. The size and morphometric variations found in male and female M. grandis , even in geographically adjacent areas (i.e. the Mediterranean, the Aegean), its wide distribution in three geographic separate regions (Mediterranean – Black Sea – Europe, Southwestern Atlantic and Western Pacific) and the degree of intraspecific variability in the same locality as observed in the Gulf of Trieste (the northernmost gulf of the Mediterranean) strengthens the need to define if this nominal species represents a species complex, as has been proved in other ‘ cosmopolitan ’ nominal species. This is probably one of those cases in which molecular evidence is needed to solve a taxonomic problem in which morphological patterns are not informative enough.

Figures

Figure 1. Location of zooplankton sampling stations in the Gulf of Trieste (Italy), where monstrilloid copepods were obtained during the surveyed period.

Figure 9. Monstrilla ghirardellii sp. nov., holotype adult male from Trieste. (a) leg 1 with intercoxal sclerite; (b) leg 2 with intercoxal sclerite; (c) leg 3. Monstrilla grandis Giesbrecht, 1891, adult male, specimen A, from Trieste. (d) urosome and fifth legs, ventral view; (e) cephalic region, ventral view showing anteriormost row of bud-like processes (arrowed); (f) same, lateral view (protuberance arrowed). Scale bars: 100 µm.

Figure 10. Monstrilla grandis Giesbrecht, 1891, adult male, specimen ‘A’ from Trieste. (a) habitus, dorsal view; (b) same, right antennule, dorsal view; (c) same, urosome, dorsal view; (d) specimen ‘B’ lateral view of urosome showing modified caudal seta; (e) detail of modified caudal seta view; (f) male specimen ‘C’, urosome with fifth legs and genital complex, ventral view; (g) same, lateral view. Scale bars: 100 µm (a), 100 µm (b–d, f, g), 50 µm (e).

Figure 11. Monstrilla grandis Giesbrecht, 1891, adult male, specimen ‘C’ from Trieste. (a) habitus, dorsal view; (b) cephalic region showing preoral ornamentation and protuberance, lateral view; (c) same, ventral view of cephalic region; (d) male specimen ‘D’, ventral view of cephalic region; (e) left antennule with armature, dorsal view; (f) leg 3; (g) urosome and genital complex, dorsal view; (h) same, lateral view; (i) same, ventral view. Scale bars: 200 µm (a), 100 µm (b–i).

Figure 12. Monstrilla grandis Giesbrecht, 1891, female specimen ‘A’, from Trieste. (a) right antennule with armature; (b) cephalic area showing cuticular ornamentation, lateral view; (c) same, dorsal view; (d) female specimen ‘B’, cephalic area showing ventral ornamentation; (e) specimen ‘A’, urosome with fifth legs, ventral view; (f) urosome with fifth legs, lateral view; (g) same, ventral view, fifth legs omitted; (h) fifth leg, ventral view, thumb-like processes arrowed. Scale bars: 100 µm (a, e–g), 50 µm (b–d, h).

Figure 13. Monstrilla grandis Giesbrecht, 1891, adult female, specimen ‘C’ from Trieste. (a) habitus, dorsal view, one caudal ramus omitted; (b) right antennule with armature, dorsal view; (c) cephalic region, lateral view; (d) urosome with fifth legs, lateral view; (e) same, ventral view; (f) same, dorsal view; (g) frontal area, dorsal view; (h) urosome of specimen ‘D’ with fifth legs, ventral view; (i) same, dorsal view. Scale bars: 200 µm (a), 100 µm (b, d–f, h, i), 50 µm (c, g).