Vulcanolepas Southward & Jones, 2003

Buckeridge, John S., Linse, Katrin & Jackson, Jennifer A., 2013, Vulcanolepas scotiaensis sp. nov., a new deep-sea scalpelliform barnacle (Eolepadidae: Neolepadinae) from hydrothermal vents in the Scotia Sea, Antarctica, Zootaxa 3745 (5), pp. 551-568 : 556-566

Genus Vulcanolepas Southward & Jones, 2003

Diagnosis (emend.) Neolepadini with capitular plates contiguous, adults having a ratio of peduncle length to capitulum length of between 1:1 and 20:1; peduncle armed with numerous small scales, between 15–30 per whorl.

Type species. Neolepas osheai Buckeridge, 2000 . From hydrothermal vents at depth 1200–700 metres, Brothers Caldera, Kermadec Ridge, SW Pacific.

Distribution. Kermadec Ridge, SW Pacific; Pacific-Antarctic Ridge; East Scotia Ridge, Antarctica (depth range: 1200–2627m).

Remarks. This description adds a third species to the genus Vulcanolepas , although as noted below, the morphological diversity of this new species is remarkable, and if only a few specimens had been recovered (and these had represented the greatest divergence in the morphological envelope of the taxon), it is likely that two species would have been proposed. Fortunately we have both an extensive collection of this species plus molecular analyses of the CO1 and 28S genes, which place V. scotiaensis sp. nov. as a strongly supported monophyletic group relative to available related Neoverruca species ( Figure 3).

CO1 was amplified from 19 V. scotiaensis sp. nov. specimens (657bp, Genbank Accession # KF39820- KF739838 ) and contained 8 variable sites: 7 transitions and 2 transversions (one site has three different bases). Four were phylogenetically informative (including both transitions). Eight 28S Vulcanolepas scotiaensis sp. nov. specimens (1,824bp, Genbank Accession # KF39812-KF39819) were all genetically identical. The 18S specimen (1885bp, Genbank Accession # KF39811) is identical to previously published sequences ( EU082393 , EU082394 )

Both partitioned and RY coded analysis of CO1 yielded the same sister taxon relationship between Vulcanolepas and Neoverruca but differed in the phylogenetic relationships among other scalpellomorphs (data not shown). There was no evidence of population structuring based on locality. Uncorrected genetic distances within Vulcanolepas scotiaensis sp. nov. ranged from 0–0.76% while genetic distances from these to other Neolepas species ranged from 16.1–17.5%, about 15x higher.

Analysis of 28S yielded identical phylogenies using ML and Bayesian approaches. Both strongly supported a monophyletic clustering of Vulcanolepas scotiaensis sp. nov. with other Neolepa s species, with>90% support from both analytical approaches (see Figure 4 ). Likelihood support for this 28S ML phylogeny (LnL = -3887, Figure 4 ) was found by SH testing to be a significantly better fit to the data (p<0.05) than the phylogeny constrained to a monophyletic ‘ Vulcanolepas ’ group (LnL = -3911). Support was not significant at 1% however, so we interpret this result with caution until additional related taxa and genes can be analysed in concert to better evaluate these relationships.

At a very fine scale, genetic analysis places V. scotiaensis sp. nov. with Neolepas spp. rather than with the other two species of Vulcanolepas —which in turn are grouped with Leucolepas longa ( Figure 4 ). This assessment, although a little at variance with morphological observations, is considered acceptable. Any taxonomy at generic level, within a tribe of very closely related species, is likely to demonstrate some degrees of transition. Uncertainty here could be solved by calling all species Neolepas —i.e. by reverting to the situation prior to Southward and Jones (2003), who split Neolepas into these three genera. However morphology dictates that the proposals of Southward and Jones (2003) are reasonable: Leucolepas is very distinct, and although V. scotiaensis sp. nov. has some characters, such as a very long peduncle, that conform to Leucolepas , in most aspects it conforms best to Vulcanolepas ( Table 2). Nonetheless, some minor adjustments to the diagnosis of Vulcanolepas are required.

Vulcanolepas scotiaensis Buckeridge and Linse sp. nov.

( Figure 5a–b ; Figure 6a–f ; Figure 7a–f ; Figure 8a–g ; Figure 9a–c )

Vulcanolepas sp. Marsh et al., 2012: 10.

Vulcanolepas sp. Rogers et al., 2012: Table 2. Material examined. Holotype: NHMUK 2013.1031 ( Figure 5a ) a complete specimen (capitulum length 20.5mm, peduncle length 17.0mm); E9 vent field, Stn. JC 42-F0396, 60º02.559S, 29º58.922W, 2402 m, coll. 30.01.2010.

Paratypes: NHMUK 2013.1032; NMV J.61011, J.61012, J.61013 ; NIWA 81215 ; all paratypes have same collection data as holotype .

Other material: E2 Stn. JC42-F066– 56º05.313S, 30º19.087W, 2605 m, 4 specimens (‘robust’ variety), coll. 20.01.2010; E2 Stn. JC42-F122– 56º05.335S, 30º19.1W, 2627 m, 8 specimens (‘robust’ variety) and 2 specimens (‘gracile’ variety), coll. 23.01.2010; E2 Stn. JC42-F160– 56º05.335S, 30º19.1W, 2627 m, 15 specimens (‘gracile’ variety), coll. 23.01.2010; E2 Stn. JC42-F170– 56º05.335S, 30º19.1W, 2627 m, 12 specimens (‘robust’ variety), coll. 23.01.2010; E2 Stn. JC42-F247– 56º05.277S, 30º19.1W, 2603 m, 4 specimens (‘robust’ variety), coll. 24.01.2010; E2 Stn. JC42-F296– 56º05.27S, 30º19.102W, 2605 m, 3 specimens (‘robust’ variety), coll. 24.01.2010; E9 Stn. JC42-F301– 60º02.599S, 29º58.922W, 2402 m,> 100 specimens (‘gracile’ variety), coll. 30.01.2010; E9 Stn. JC42-F350– 60º02.599S, 29º58.922W, 2402 m, 7 specimens (‘gracile’ variety), coll. 30.01.2010; E9 Stn. JC42- F386– 60º02.599S, 29º58.922W, 2402 m, 7 specimens (‘gracile’ variety), coll. 30.01.2010; E9 Stn. JC42-F0396– 60º02.559S, 29º58.922W, 2402 m,> 50 specimens (‘gracile’ variety), coll. 30.01.2010; E9 Stn. JC42-F0500– 60º02.807S, 29º58.708W, 2394 m, 11 specimens (‘gracile’ variety), coll. 30.01.2010; E9 Stn. JC42-F0501– 60º02.823S, 29º58.696W, 2396 m, 46 specimens (‘gracile’ variety), coll. 02.02.2010; Kemp Caldera Stn. JC42- F0621– 59º41.677S, 28º21.086W, 1420 m, 1 specimen (‘gracile’ variety), coll. 02.09.2010.

Types are listed with the institutional abbreviations preceding the relevant registration number, i.e., NHMUK (Natural History Museum, London), NIWA (National Institute of Water and Atmospheric Research, Auckland), NMV (Museum Victoria, Melbourne).

Diagnosis. Vulcanolepas with capitular height to width ratio of c. 9:8; apex of rostrum extending freely beyond basal angle of scutum; plates with weak to moderate apico-basal ridges crossed by moderately weak, transverse growth lines; medial latus slightly wider than high; ratio of length of peduncle to capitulum in adults up to 20:1; peduncular scales in middle portion protruding for c. 1.2 mm, each with a fine, acicular termination.

Description. Vulcanolepas with capitular height to width ratio of c. 9:8; capitulum comprising eight approximate, calcareous plates: carina, rostrum, and paired terga, scuta and medial latera ( Figure 5 ); capitulum laterally compressed to slightly less than diameter of peduncle; plates with transverse growth ridges weakly to moderately defined, crossed by fine but well-formed apico-basal striae; incurved apices of carina and rostrum extending beyond capitulum for up to 10% of length, becoming more arcuate in adults; carina with umbone apical, tectum strongly arched transversely, with narrow ridge along their tergal margins; in profile may appear weakly toothed due to intersection of transverse growth lines and striae ( Figure 5b ); rostrum with tectum broadly rounded, scutal margins weakly concave, apex acute; tergum quadrangular, with sharp medial apico-basal ridge and faint secondary ridge extending from tergal apex to apex of medial latus, crossed by weak growth striae; scutum quadrangular, tergal margin concave, gently incurved, occludent margin convex, basal angle sharp—generally about 85º but ranging from 75–95º, medial apicobasal ridge rounded, stronger apically, fine apico-basal ridges crossed by weak growth striae; medial latus triangular, apical angle c. 70º, generally 1.5x wider than high, weak apico-basal striae crossed by stronger transverse growth ridges parallel to capitulum-peduncle margin ( Figures 5 , 6 , 7 ); peduncle-capitulum ratio varies from 1:1 to c. 20:1.

Peduncle with up to 30 acicular scales per whorl (measured ~ 10 mm below the capitulum in adults), those near capitulum smallest, about 2x longer than wide, with apices protruding laterally for up to 1.2 mm; abundance of scales greatest near capitulum where they are closely approximate ( Figure 9c ). Scales becoming more widely spaced basally, a quarter of distance above basal attachment, scales about as wide as long, separated from each other by as much as four times their own width ( Figure 9a ).

Internally, capitular plates unremarkable ( Figure 7b, d, f ). Mostly smooth except for where a plate extends beyond the soft tissue: here a zone of fine growth lines parallel the plate margin, e.g. in the tergum, develops as a 1.5mm strip from apex to occludent angle, and down to point adjacent to apex of the carina; scutum with shallow, smoothly rounded depression in upper half of plate for adductor muscle attachment, just below the apex there is a very short groove marking where it interlocks with the tergum; median latus smooth; carina and rostrum smooth, except for fine growth lines in apical region where plate extends beyond capitulum.

Trophi and appendages: Labrum with single row of minute teeth on crest, flanked by pair of relatively small mandibular palps; mandibles tridentoid, comprising a larger superior tooth and two lesser-formed, lower teeth, the lower teeth and the inferior angle are modified into neolepadine comb-structures ( Figure 8e ); first maxillae (maxillule) relatively large compared with second maxillae, hatchet-shaped, inferior angle protruded into a blunt triangle, densely covered with setae (figure 8d); second maxillae with moderately flat cutting edge possessing abundant fine spines ( Figure 8c ); cirri in the ‘gracile’ forms in particular, moderately long, filamentous and delicate; cirri I and II with robust proximal segments ( Figure 8a, b ); intermediate segments of cirrus VI with six pairs of long simple setae distally plus three pairs of progressively finer and shorter proximal setae ( Figure 8f ). Caudal appendages small, blunt, uni-articulate, about half the length of the basal segment of cirrus VI ( Figure 8g ); penis with annulated appearance and numerous short, fine, terminal setae.

Morphotypes:The extremes of the two morphotypes are characteristic of the optimal environment (‘gracile’) and least preferred environment (‘robust’), with the population of the former being overwhelmingly abundant. There is a gradation in morphology and not surprisingly, this relates directly to the environment. Typical representatives of each morphotype differ in their p:c ratios, sculpture and to some degree with the cirri ( Table 3). However the feeding cirri in the ‘robust’ forms are almost always terminated through heavy predation, making comparison of appendages difficult.

Southward & Newman (1998) noted that the feeding cirri (III–VI) on some neolepadines from Lau were particularly filamentous and “white”—a coloration resulting from a coating of bacteria, which they interpreted as evidence of symbiosis; the barnacle being dependent on the bacteria as a food source. No bacteria were observed on the cirri of V. scotiaensis sp. nov., and although this absence may reflect the methodology of collection, preservation and subsequent handling, the cirri of V. scotiaensis sp. nov. are much shorter and less filamentous than the Lau specimens. Southward & Newman (1998: 261) observed that the ratio of article length to setae length in the feeding cirri of the Lau specimens was 1:14.0. This is very much greater than V. scotiaensis sp. nov., where the ratio is from 1:3.5–4.0 (in ‘robust’ forms) to 1:2.7–3.4 (in ‘gracile’ forms), making V. scotiaensis sp. nov. one of the least filamentous of the neolepadines for which this measurement has been made. ( Southward & Newman (1998: 261) recorded ratios of between 1:6.2 and 1:6.7 for three other neolepadines). The ratio of setae length to article length was initially considered sufficiently informative to include in the diagnosis of V. scotiaensis sp. nov.; however in a recent paper by Hoch (2011: 402), it is shown that for the balanomorph barnacle Semibalanus balanoides , there is a good correlation between the hydrodynamic environment and cirral length. Wider observation is required before the significance of this character within the neolepadines is clarified; in the interim, the article length to setae length ratio for V. scotiaensis sp. nov. remains a ‘useful observation’.

Juveniles: Many of the adults (established hermaphrodites) had juveniles attached to their peduncles. Juveniles were most commonly attached to the lower half of the peduncle ( Figure 6f ). As with other scalpelliformes, peduncle development follows that of the capitulum, with the smallest specimens measured (2.0 mm) having a capitulum length of at least twice that of the peduncle. Surprisingly, none of the specimens dissected were ovigerous.

Colour: Specimens growing near active venting, and warmer waters such as “Car Wash” in E9 possess straw coloured peduncles; the capitular plates are pales cream, but covered with an orange-brown integument ( Figures 6 , 7 , 9 ). Specimens near dying or less active venting sites ( Figure 12 ) tend to be encrusted with black-brown minerals (manganiferous Fe oxy-hydroxides?).

Etymology. Geographic (of, or pertaining to the Scotia Sea).

Distribution. Hydrothermal vent seeps at circa 1400 to 2600 metres, from the ESR, Antarctic-South American Ocean Ridge Complex (56.05ºS to 60.02ºS, 29.58ºW to 30.19ºW).

Remarks. The three species of Vulcanolepas are all characterized by approximate capitular plates with weak to moderate external ornamentation. The protruding peduncular scales of V. scotiaensis sp. nov. are a particularly distinctive feature of this species, as is the free extension of the apex of the rostrum, (and sometimes the carina). The imbricating scales on the peduncle are generated in a zone immediately below the capitulum, where they are both very small, and very numerous. Determining the exact number per whorl is difficult at this junction, so instead the number of imbricating scales per whorl is measured at a distance of approximately 10 mm below the base of the capitulum.

The most common morphotype of V. scotiaensis sp. nov. is the ‘gracile’ form (figure 5a). At sites of active diffuse venting, where temperatures range between 5–19ºC (such as “Car Wash” at E9), dense populations of>1500 individuals per square metre ( Figure 11 ) have been recorded; see Marsh et al. (2012). The two morphotypes appear to be a function of environment, with specimens living close to sites with low hydrothermal activity such as is found at E2 on the chimney base of the “Dog’s Head” vents described as ‘robust’. The ‘robust’ forms are characterised by noticeably more ornate capitular plates and very much shorter peduncles ( Figure 5b ) and at sites like the chimney base of “Dog’s Head” the peduncle to capitulum ratio approaches to 1:1 ( Figures 10a, 10b ). Specimens at sites such as the chimney base of “Dog’s Head” or in the neighbouring pillow basalts are closely confined to narrow hydrothermal fissures ( Figure 12 ).

A comparison of peduncle to capitulum length is provided in Figures 10a and 10b , demonstrating that the ratio varies from 8.6/1 to 18.6/1. Specimens with a capitulum that is longer than the peduncle are either juveniles, or adults that are growing in less than suitable conditions, such as at the chimney base of “Dog’s Head” or the pillow basalt fields with low diffuse flow in E2, where venting is significantly reduced. The resultant low temperatures are less supportive of the growth of micro-organisms—the primary food source of cirripedes ( Figure 12 ). Vulcanolepas scotiaensis sp. nov. in these localities is not only ‘stunted’, it is generally heavily encrusted with minerals, suggesting that these specimens may be relatively aged ( Figure 12 ).

V. scotiaensis sp. nov. may be distinguished from other species Vulcanolepas by the much greater length of the peduncle in adults. The p:c in V. osheai is typically ~8:1, and in V. parensis ~6:1. Importantly, V. scotiaensis sp. nov. has a median-latus that is wider than high (the opposite occurs in the other two taxa), and the apices of the rostrum commonly extend freely beyond the capitulum. The carina of V. scotiaensis sp. nov. may also extend freely; in addition, these plates are often less incurved than in V. parensis and V. osheai .

Feeding and Vulcanolepas scotiaensis sp. nov. Like all neolepadines, V. scotiaensis sp. nov. is characterized by relatively long, delicate, filamentous cirri—which are interpreted as an adaptation to maximize food capture in a moderately low energy, abyssal environment ( Newman, 1979: 157; Buckeridge, 2000: 417). In vent communities, the food source of larger filter feeders, such as cirripedes, comprises both chemosynthetic and photosynthetic micro-organisms. Marsh et al., (2012: 13) postulate that as with other neolepadines, V. scotiaensis sp. nov. gains nutrition from epibionts attached to its cirri as well as from traditional filter feeding.

Cirripedes too are an important food source within the vent fauna trophic web—as many of the cirri in specimens that have been dissected are incomplete ( Table 4). Cirral damage to cirripedes appears to have occurred following grazing by macro-consumers such as asterozoans (e.g. as observed in Rogers et al., 2012: Figure 3E).

Reid et al. (2013) have undertaken an analysis of different isotopic levels in the tissue of a range of taxa from the ESR, including V. scotiaensis sp. nov., and have found that macro-consumers (such as cirripedes, crabs and anemones) have C, N and S isotopic signatures that demonstrate varying input in the ratio of epipelagic photosynthetic micro-organisms and vent microbial micro-organisms, and further that this ratio varies between E2 and E9. In particular Reid et al. (2013) and Suzuki et al., (2009) demonstrate that there is a greater range of 34 S isotope values in the tissue of organisms at E2 than at E9. They interpret this as reflecting a greater variability in the food source at E2, with proportionately more epipelagic photosynthetic autotrophs than at the chemoautotroph dominated E9.

Differences in the chemistry of each site are expected in an active region of hydrothermal venting, where vents may close abruptly and new ones quickly form. Indeed, even small changes in vent activity are likely to result in significant variations in feeding activity (and growth), and this supports our interpretation that the broad morphologic envelope demonstrated by the ‘gracile’ and ‘robust’ forms of V. scotiaensis sp. nov. is a function of a dynamically evolving benthic environment.

Apparently V. scotiaensis nov. has a high resilience to environmental change—or a capacity to continue to function when conditions drop to less than optimal. The barnacle population density is much less at E2 sites such as at the chimney base of “Dog’s Head” ( Figure 12 ), where conditions are less than optimal; and this lack of crowding permits acceptable feeding without a need to divert resources to produce longer peduncles. The specimens at “Dog’s Head” are also heavily encrusted with minerals and as hydrothermal activity is much reduced at E2, it is likely that this build-up represents prolonged exposure to vent fluids, suggesting that these individuals may be older than their E9 counterparts.

Figures

FIGURE 4. Genetic relationship of V. scotiaensis sp. nov. with other neolepadines: 28S Bayesian majority-rule consensus phylogeny. Bayesian posterior support and maximum likelihood bootstrap support are respectively shown next to each tree node.

FIGURE 5. Morphotypes of Vulcanolepas scotiaensis sp. nov. a: The “gracile” form. Holotype NHMUK 2013.1031. The capitulum comprises eight approximate, calcareous plates: carina (c), rostrum (r) and paired terga (t), scuta (s) and medial latera (ml); is = imbricating scale of the peduncle. Note the broadly arched profile of the carina (compared with b), and on the tergum, the weak longitudinal ridge on the scutal side that extends to a point near the apex of the medial latus. The peduncle has been truncated in this diagram (see Figure 6f for an appreciation of the relative peduncle to capitulum length). b: The “robust” form. Paratype NHMUK 2013.1032. Note the nodose pattern on the plates, produced by intersection of strong growth lines with longitudinal ribs. The peduncle, although truncated for this diagram, is approximately the same length as the capitulum.

FIGURE 6. Vulcanolepas scotiaensis sp. nov., external morphology. a: Capitulum (left side, exterior), “gracile” form, peduncle truncated, from JC42-F-0396; b: Capitulum (left side, exterior), more heavily sculpted “robust” form (peduncle truncated), from JC42-F-0122; c: Complete animal (left side, exterior), more heavily sculpted “robust” form, showing a capitulum that is slightly longer than the peduncle, from JC42-F-0122; d: Complete animal (left side, exterior), “gracile” form, from JC42-F-0396; e: Complete animal (left side, exterior), “gracile” form (juvenile), from JC42-F-0396; f: Complete animal (right side, exterior), “gracile” form (adult) showing a peduncle that is at least ten times the length of the capitulum, from JC42-F-0396.

FIGURE 7. Vulcanolepas scotiaensis Plate morphology. a: Capitulum (left side, exterior) showing plate arrangement (carina, rostrum and peduncle removed); b: Capitulum (interior) showing plate arrangement; c: Carina (exterior); d: Carina (interior); e: Rostrum (exterior); f: Rostrum (interior). From JC42-F-0396.

FIGURE 8. Vulcanolepas scotiaensis Appendages and trophi. a: Cirrus I; b: Cirrus II. c Right second maxilla; d: Right maxilla (or maxillule); e: Right mandible, showing modification of the two lower teeth and the inferior angle into a comb-like structure, a characteristic feature of the neolepadines noted in Southward & Newman, (1998: 261). f: Intermediate segment of cirrus VI, showing six pairs of long, simple setae and below these, three pairs of successively shorter, finer setae (setae truncated). g: Uni-articulate caudal appendage. (Note that in these diagrams, the density of the setae on the trophi is reduced). From JC42-F-0396.

FIGURE 9. Vulcanolepas scotiaensis Peduncular scale arrangement. From peduncle of a mature “gracile” specimen, oriented with capitulum to top (capitulum length: 20 mm, peduncle length: 170mm). a: Arrangement immediately above the base of the peduncle; b: Arrangement mid-length along the peduncle, showing widely spaced scales and an attached juvenile; c:. Arrangement close to the capitulum, showing close proximity of small scales, (lower part of capitulum visible). Specimen from JC42-F-0396.

FIGURE 10a. Ratios of peduncle to capitulum length. The “gracile” form (shown as series 1, a diamond) is the less ornamented variety, and by far the most abundant in the collections. During growth, the peduncle can grow up to 20 times the length of the capitulum. The trend line included is for the “gracile” form only; the R2 correlation of this regression at 0.72518 confirms a reasonable correlation—i.e. that with growth, the pedun11 cle can be expected to become proportionately longer. However, the “robust” variety (shown here as series 2, a square) has subequal p:c ratios, and this apparently changes little with growth (= age), such that some larger specimens may even possess a capitulum that is slightly longer than the peduncle. This part of the graph is isolated and used in Figure 10b. Data base 57 specimens (“gracile” from JC42 F-0396 (34), JC42 F386 (10); “robust” 13 from JC42-F0122). p = peduncle length, c = capitulum length.

FIGURE 11. Benthic Ecology: The V. scotiaensis sp. nov. assemblage at the “Carwash” vent chimney in the E9 vent field (60°02.809S, 29°58904W), East Scotia Ridge Back-Arc Basin. a: Photograph DSCN9734, showing V. scotiaensis sp. nov. as the dominant organism living at this site. a specimen of the decapod Kiwa (arrowed) may be seen above and slightly to the right of the letter ‘a’; a larger, pink anemone, Pacmanactis sp. (arrowed), is on the left margin. Image taken by the Scorpio stills camera on Isis, Dive 138. b: Photograph DSCN0191, showing detail of V. scotiaensis sp. nov. in feeding mode with extended, delicate, filamentous cirri. A specimen of the limpet Lepetodrilus sp. was grazing on the exterior of one of the larger peduncles (arrowed). Image taken by the Scorpio stills camera on Isis, Dive 140. Only the ‘gracile variety’ of V. scotiaensis sp. nov. is present in these two photographs, both taken at circa 2400 metres, where temperatures in the barnacle assemblage zone ranges between 5 and 19°C (Marsh et al., 2012). Scale: diameter of largest peduncle (arrowed) circa 6mm.

FIGURE 12. Benthic Ecology: The V. scotiaensis sp. nov. assemblage at the “Dog’s Head” vent in E2. The morphotype present here is predominantly the ‘robust’ variety of V. scotiaensis sp. nov., and specimens are generally heavily encrusted with blackish Fe/Mn minerals. The greatest density of organisms is found along what is interpreted as an old, or dying active vent. The bio-density in this reduced energy environment is significantly lower than at “Carwash” (Figure 11).