a new clathria (demospongiae, microcionidae) from peru occurring on rocky substrates as well as...

Accepted by J. Hooper: 22 Sep. 2011; published: ?? Month 2011

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A new Clathria (Demospongiae, Microcionidae) from Peru occurring on rocky substrates as well as epibiontic on Eucidaris thouarsii sea urchins

L. KAREM AGUIRRE1, YURI HOOKER1, PHILIPPE WILLENZ2,4 & EDUARDO HAJDU3

1Laboratorio de Biología Marina, Facultad de Ciencias y Filosofía, Universidad Peruana Cayetano Heredia, Calle Honorio Delgado 430, Lima 31, Lima, Perú. E-mail: [email protected], [email protected] 2Department of Invertebrates, Section Malacology, Royal Belgian Institute of Natural Sciences (RBINSC), Rue Vautier 29, B–1000, Brussels, Belgium. E-mail: [email protected] Nacional, Departamento de Invertebrados, Universidade Federal do Rio de Janeiro, Quinta da Boa Vista, s/n, 20940–040, Rio de Janeiro, RJ, Brazil. E-mail: [email protected] author

Abstract

Southeastern Pacific sponges (Phylum Porifera) range among the world’s least known faunas, with only 13 species report-ed to date from the entire Peruvian coast. This state of affairs motivated the onset of two large, cooperative, exploratoryinitiatives, with the aim of mapping sponge richness and distribution in the area: Proyectos ESPER and EsponjAS. Over800 specimens have been collected in Peru since 2007, with identifications still in progress. Among these, a sponge spe-cies originally thought to be an exclusive epibiont on Eucidaris thouarsii sea urchins, relatively conspicuous on Peru’sPunta Sal region. This sponge, latter found to occur on additional substrates too, is described as a new species of Clathria(Microciona). Cidarid density ranged between 1.5 and 12/m2, and largest diameter of the tests between 3.2 and 5.6 cm.Total number of spines on each sea urchin varied between 68 and 96, and percent sponge coverage of these, between 18.2and 75.7. There appears to be only a slight tendency for increased sponge coverage on larger sea urchins, so there may befactors, other than sea urchin age, shaping this association. Clathria (Microciona) aculeofila sp. nov. can be markedlydominant as an epibiont on E. thouarsii, albeit the great sponge richness in the area. This is in contrast to the allegedlyopportunistic, diverse epibiosis by sponges reported previously for Antarctic cidaroids.

Key words: Porifera, new species, epibiosis, Clathria (Microciona)

Introduction

Notwithstanding the ecological importance of sponges (Porifera) in benthic marine ecosystems, and for their bio-logical, chemical and pharmaceutical properties, Southeastern Pacific species range among the least known in theworld (Hajdu and Desqueyroux–Faúndez 2008). Only 13 species belonging to the Demospongiae (4) and Hexacti-nellida (9) are this far known from Peru, with no Calcarea yet recorded. The complete list comprises the demo-sponges Acarnus peruanus van Soest et al., 1991; Dysidea ligneana (Hyatt, 1877); Myxilla asymmetricaDesqueyroux–Faúndez and van Soest, 1996; Myxilla dracula Desqueyroux–Faúndez and van Soest, 1996; and thehexactinellids Bathydorus spinosissimus Lendenfeld, 1915; Eurete spinosum Lendenfeld, 1915; Holascus edwardsiLendenfeld, 1915; Hyalonema agassizi Lendenfeld, 1915; H. agujanum Lendenfeld, 1915; H. bianchoratum pinu-lina Lendenfeld, 1915; H. tenuifusum Lendenfeld, 1915; H. tylostylum Lendenfeld, 1915 and Sympagella canthar-ellus Lendenfeld, 1915. With the exception of Acarnus peruanus and Dysidea ligneana, all these sponges comefrom deep waters. This meager list was the main reason to start the ESPER Project (“Esponjas del Perú”) in 2007and Proyecto EsponjAS (“Esponjas da América do Sul) in 2008, with the aim of mapping sponge richness and dis-tribution along the Peruvian coast. This is also a natural follow up for Hajdu, Willenz et al.'s taxonomic studies ofChilean sponges (e.g. Azevedo et al., 2009; Willenz et al., 2009).

AGUIRRE ET AL.2 · Zootaxa 0000 © 2011 Magnolia Press

The recent intensive collecting undertaken along Peru´s coastline yielded over 800 specimens and thousands ofunderwater images of sponges and their habitats, which are now sorted into major taxonomic groups, providing thebasis for on–going taxonomic study undertaken in Brussels, Geneva, Lima and Rio de Janeiro. In this work wedescribe a new species of Clathria, first thought to be exclusively epibiontic on the sea urchins Eucidaris thouarsii(Valenciennes, 1846), but subsequently found in several hard substrata. The abundance and spatial distribution ofthese sea urchins, the frequency and intensity of the association between Clathria sp. nov. and the sea urchinsspines as well as the gut–contents of the latter were evaluated too.

Material and methods

Sponges and sea urchins were collected by scuba or hookah diving, and photographed in situ, with their dimen-sions, depth and temperature of the habitat recorded at the same time. Collecting localities were Lobos de AfueraIslands, Cancas, El Ñuro, Máncora and Punta Sal, indicated in the map shown in Figure 1. This area is located atthe transition zone between the Guayaquil and Central Peru marine ecoregions (Panamic Region), being thus sub-ject to the alternating effects of the Panama (Tropical/Subtropical) and Humboldt (Subtropical/Temperate) currentssystems. Water temperatures in this zone can be as cold as 12–13°C and warmer than 25°C, depending on the timeof the year and prevailing current system.

The density and distribution of sea urchins, as well as frequency and intensity of the sponge association wereevaluated in three line–transects with 10 x 2 m at the spots known as Bajo El Cardo (03°58’53.9’’S,80°59’20.5’’W) and Balneario I (03°57’20.3”S, 80°57’56.2”W) (Punta Sal). Ten sea urchins were collected ran-domly at 10 m depth (19°C) for calculation of quantitative traits of the sponge association, and extensive visualcounts were undertaken along the transect. A third sampling was conducted at Balneário II (0357’16.9”S,8057’56.4”W) at 15 m depth (19°C). Sea urchins had the height and width of their tests, as well as percentage ofsponge–covered spines recorded. Immediately afterwards, sea urchins still in seawater-filled buckets, had their gutsand Aristotle lanterns removed and preserved in 96% ethanol.

Materials used for the identification, apart from dozens of underwater images, were a few collected specimensfrom Lobos de Afuera Islands and Punta Sal. The identification of the sea urchins was based on comparisons to thedescriptions of Mortensen (1910), Clark (1948), Caso (1979), and Lessios (2005, and in litt. 2010). Sponges wereidentified on the basis of their dissociated spicules and thick sections, under light as well as scanning electronmicroscopy. In general, procedures followed standards presented by Rützler (1978) and Mothes de Moraes (1985),with some additions which are presented below.

A sponge–covered spine was prepared for SEM study according to the papain enzymatic protocol outlined byPinheiro and Hajdu (2001), which consisted of sectioning 2 cm out from a spine, adding this and 30 ml digestionbuffer (100 mM sodium acetate, pH 5.0; cisteine 5 mM; 5 mM EDTA) to a Falcon tube kept for 24 hours at 4°C.Subsequently, 1 ml of a 3 % papain solution (freshly made in digestion buffer) was added to the sponge digestiontube and incubated at 60°C for 24 h. The digested fragment was then gently washed with water jets to finish thecleaning of its spiculofibers. The preparation was then dehydrated back in ethanol 96 % for 1 h, dried under a warmlamp, attached to a stub with double–sided carbon tape, and vacuum–coated with evaporated gold prior to SEM.Another section from a sea urchin spine has been obtained by sawing specimens embedded in low viscosity epoxyresin (Spurr Low Viscosity Embedding Media, Polysciences, Inc) with a low–speed saw (Labcut 1010, Agar Scien-tific Ltd.) using a diamond wafering blade, and wet–ground on polishing discs.

Abbreviations used: CZA (Colección de Zoología Acuática, Universidad Peruana Cayetano Heredia, Lima,Peru), MHNG (Museum d´Histoire naturelle, Geneva, Switzerland), MNRJ (Museu Nacional, Universidade Fed-eral do Rio de Janeiro, Rio de Janeiro, Brazil), RBINS (Royal Belgian Institute of Natural Sciences, Brussels, Bel-gium), STRI (Smithsonian Tropical Research Institute, Balboa, Panama).

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Zootaxa 0000 © 2011 Magnolia Press · 3CLATHRIA (MICROCIONA) ACULEOFILA SP. NOV.

FIGURE 1. Map of Peru with collection localities of Clathria (Microciona) aculeofila sp. nov. and details of the Punta Salregion. 1 = Cancas; 2 = Punta Sal, Punta Sal Balneario I and Punta Sal Balneário II; 3 = Máncora; 4 = El Ñuro; 5 = Lobos deAfuera Islands.

Systematics

Class Demospongiae Sollas

Order Poecilosclerida Topsent

Suborder Microcionina Hajdu, van Soest and Hooper

Family Microcionidae Carter

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Genus Clathria Schmidt

Subgenus Clathria (Microciona) Bowerbank

Clathria (Microciona) aculeofila sp. nov.(Figs 1–6; Tabs 1–2)

Type material. Holotype CZA 13317 (schizotypes MNRJ 13317, RBINS POR 2000, MHNG 76056) Bajo ElCardo (Punta Sal–03°57’16.90’’S, 80°57’56.40’’W, Piura, Peru), 15 m deep, coll Y. Hooker and L.K. Aguirre,13.Feb.2008. Paratypes CZA 11449 (schizotypes MNRJ 11449, RBINS POR 2004, MHNG 76057), Baja de Que-brada Verde (El Ñuro–04°13’22.30”S, 81°12’24.10”W, Piura, Peru), 4–5 m deep, coll. Y. Hooker and M. Rios,14.Oct.2007. CZA 11332 (schizotypes MNRJ 11332, RBINS POR 2001, MHNG 76058), Islote El Lagarto (Lobosde Afuera Islands–06°56’01.20”S, 80°42’19.90”W, Lambayeque, Peru), 8.6 m deep, coll. Ph. Willenz and Y.Hooker, 04.Oct.2007. CZA 11380 (schizotypes MNRJ 11380, RBINS POR 2002, MHNG 76059), San Cristobal(Lobos de Afuera Islands–06°54’52.50”S, 80°42’55.90”W, Lambayeque, Peru), 12.9 m deep, coll. E. Hajdu,07.Oct.2007. CZA 11437 (schizotypes MNRJ 11437, RBINS POR 2003, MHNG 76060, Sur de Quebrada Verde(El Ñuro–04°13’30.40”S, 81°12’31.60”W, Piura, Peru), 10.0 m deep, Y. Hooker and M. Rios, 14.Oct.2007. CZA11453 (schizotypes MNRJ 11453, RBINS POR 2005, MHNG 76146, Baja de Quebrada Verde (El Ñuro–04°13’22.30”S, 81°12’24.10”W, Piura, Peru), 4–5 m deep, coll. Y. Hooker and M. Rios, 14.Oct.2007. CZA 11490(schizotypes MNRJ 11490, RBINS POR 2006, MHNG 76147), Baja de Quebrada Verde (El Ñuro–04°13’22.30”S,81°12’24.10”W, Piura, Peru), 8 m deep, coll. Y. Hooker and M. Rios, 18.Oct.2007. CZA 12955 (schizotypesMNRJ 12955, RBINS POR 2007, MHNG 76149), the fishermen’s pier (Máncora–04°06’35.65”S, 81°04’02.50”W,Piura, Peru), 1.6 m deep, Y. Hooker and F. Menendez, 18.Nov.2009. CZA 12981 (schizotypes MNRJ 12981,RBINS POR 2008, MHNG 76150), Baja El Burro (Punta Sal–03°58’34.10”S, 80°59’06.00”W, Piura, Peru), 13.2m deep, coll. Y. Hooker and B. Ibañez, 21.Nov.2009. CZA 12982 (schizotypes MNRJ 12982, RBINS POR 2009,MHNG 76151), Balneario anchorage (Punta Sal–03°58’04.10”S, 80°58’09.30”W, Piura, Peru), ca. 10.0 m deep,coll. Y. Hooker and C. Segami, 21.Nov.2009. CZA 12989 (schizotypes MNRJ 12989, RBINS POR 2010, MHNG76152), (El Ñuro–04°14’1.00”S, 81°12’46.00”W, Piura, Peru), 15.7 m deep, Y. Hooker and F. Menendez,19.Nov.2009. CZA 13031 (schizotypes MNRJ 13031, RBINS POR 2011, MHNG 76153), the fishermen’s pier (ElÑuro–04°13’00.00”S, 81°10’50.10”W–Piura, Peru), 4.8 m deep, coll. Y. Hooker and C. Segami, 24.Nov.2009.CZA 13066 (schizotypes MNRJ 13066, RBINS POR 2012, MHNG 76154), Chavelera (Cancas–03°55’14.10”S,80°54’29.90”W–Piura, Peru), 11.6 m deep, coll. Y. Hooker, 30.Nov.2009.

Diagnosis. Clathria (Microciona) sp. nov. is the only encrusting Clathria in Peru and neighboring areas, withprincipal megascleres mostly bearing spines only at the base, auxiliary megascleres which are either smooth orpaucispined at the base, smooth toxas in one or two length categories frequently over 100 µm long, and palmateisochelae in a single category, normally smaller than 15 µm long.

Description. Habit. Sponges are usually thinly encrusting (< 1 mm thick), but slightly thicker sponges can befound too (Fig. 2). They frequently occur as the main epibionts on the spines of Eucidaris thouarsii (Valenciennes,1846) (Cidaridae, Echinoidea; CZA 11332, 11380, 11449, 12981, 12982; Fig. 2). Each spine has about 3–4 cm2 inarea epibiont coverage, and specimens were not seen stretching from one spine into another. Larger specimenswere found on rocky substrate, in this case reaching over 16 x 14 cm in area (e.g. CZA 11490). Surface is hispidand texture velvety. Consistency soft, but in parts it is the hard substrate that one feels when touching the sponge.Colour in life bright–red (CZA 11332, 11380, 11437, 11449, 11453, 11490, 12981, 12955, 12989) or yellow (CZA12982, 13031, 13066), turning into beige after preservation with ethanol. Meandering subectosomal canals areclearly visible in yellow specimens only, and scattered oscules could only be seen in the pictures taken from CZA11490 and 12982, all of which smaller than 1 mm in diameter.

Skeleton. (Figs 3, 4). Typical Clathria (Microciona) arrangement, with a basal layer of spongin (20–30 µmacross) from which short, echinated fibres arise (up to 600 µm high). Principal megascleres stand erect on the sub-strate, held erect by the basal layer of spongin, but also slightly above, coring or echinating the fibres. Auxiliarymegascleres arranged in disorganized (sub)ectosomal bouquets, frequently piercing the surface. Spicules in thesebouquets are frequently laying tangential to the surface. Microscleres of variable abundance are scattered.


Spicules. Megascleres (Fig. 5A–R; Fig. 6A–N, Table 1). Principal subtylostyles (Fig. 5A–F; Fig. 6A–H),variably stout, slightly curved, slightly fusiform, tapering gradually to a sharp apex; base slightly swollen, round-ish, irregularly acanthose, with variably sharp (blunt verrucose to pointy thorn), straight or bent spines; smoothshaft. Auxiliary subtylostyles (Fig. 5K–R; Fig. 6I–N), smooth, slender, straight, tapering gradually to a sharpapex; base barely swollen, elliptical, smooth or bearing a crown of sharp, straight spines; smooth shaft. Accessoryacanthostyles (Fig. 5G–J; Fig. 6F–H), variably stout, slightly curved, slightly fusiform, tapering gradually to asharp apex; base frequently styloid, irregularly acanthose, with variably sharp (blunt verrucose to pointy thorn),straight or bent spines; shaft pauci-acanthose, with spines frequently restricted to the central portion.

TABLE 1. Clathria (Microciona) aculeofila sp. nov. Comparative micrometric data for the holotype, paratypes and additionalcomparative materials. Values are in micrometres.

Microscleres (Fig. 5S–T; Fig. 6O–P). Palmate isochelae (Fig. 5T; Fig. 6P), mostly with nearly straight, slen-der shafts, only seldom slightly twisted or curved, claws 38–45 % the entire spicule length. Toxas (Fig. 5S; Fig.6O), smooth, common, V–type (gentle central curve and nearly no curves on extremities); the smallest ones areusually those with the deeper central curves.

Ecology and distribution. (Fig. 1). The sponge material was collected from 1.6 to 15.7 m depth, in water tem-peratures of 14 to 23°C. In Cancas, El Ñuro, Máncora, Punta Sal and Lobos de Afuera cidarid sea urchins were rel-atively common and these had nearly always their spines covered by the Clathria aculeofila sp. nov. Apparentlymost, if not all of these cidarids belong to E. thouarsii. More detailed information is presented below.Remarks. Although there are over 300 described species of Clathria (Hooper, 1996), it is relatively easy to distin-guish the Peruvian species from all others. Among the several subgenera of Clathria, only C. (Cornulotrocha), C.(Microciona) and C. (Thalysias) have comparable architecture and spicule complement when contrasted to the newspecies described here. Only 12 species of these subgenera are this far known from provinces adjacent to the typelocality of the new species, viz. the Warm Temperate Northeast Pacific, the Tropical East Pacific, the Juan Fernán-

CZA # Color / Sub-strate

Principal subtylostyles Auxiliary sub-tylostyles

Accessory acanthostyles Isochelae Toxas

11332 Red /Eucidaris

172-307-607 / 7-15.7-28 125-263.3-407 86-90-103 / 7-7.9-9 13-13.8-15 20-57.1-110


132-231.4-418 / 9.4-15.3-22 162-227.8-308 85-100.9-128 / 6-3.5-13 16 40-65.6-123

11437 Red /Rock

78-142.2-324 / 6-10-16 312-455.7-760 83-85.3-91 / 7-7.5-8 10-13.6-18 16-52.4-109


75-215.4-428 / 7-13-20 116-240.2-350 67-74-78 / 7-7.1-8 9-13.2-17 38-74.5-132

11453 Red /Rock

68-115.5-239 / 5-7.5-11 113-208-327 71-76.4-80 / 6-7.1-9 8-13.2-17 67-112.9-153

11490 Red /Rock

101-205.7-283 / 6-11.2-20 114-218-310 79-88.5-101 / 6-8-9 10-14-30 41-80.7-140

12955 Red /Rock

74-259-588 / 4-12-24 229-295.1-379 72-80.8-89 / 5-6-7 15-35.5-45 38-52.2-110


71-169.4-254 / 9-10.9-15 144-191.7-220 73-77-81 / 7-6.9-7 11-14.1-16 38-48.8-77

12982 Yellow /Eucidaris

69.6-138.2-300 / 2.4-5.7-9.6 182-224.5-258 84-86.4-91 / 5-6.4-7 12-12.4-14 24-49.2-74

12989 Red /Spondylus

95-188-465 / 7-13-26 145-240-319 51-84.6-96 / 5-6.8-9 10-13.1-17 42-83.3-146

13031 Yellow /Rock

215-274.8-413 / 10-13.6-18 104-175-295 76-94.3-131 / 6-8.2-11 10-13.6-16 19-49.9-101

13066 Yellow /Eucidaris

64.8-124.4-432 / 2.4-5.3-9.6 130-230.5-304 65-86.4-109 / 6-7.6-9 12 60-69-72


111-184-318 / 5-9.5-13 115-178-258 103-121.8-132.8 / 7.4-9.7-11.7

10-13.7-15 33-69.7-114


dez and Desventuradas, the Warm Temperate Southeast Pacific and the Magellanic provinces (Table 2). Amongthese, C. (T.) amabilis has no microscleres, and another five species do not have any toxas: C. (C.) polita, C. (C.)rosetafiordica, C. (M. ?) brepha, C. (M.) spongigartina and C. (T.) originalis. Other important points of distinctionin relation to these species are the rosettes observed in C. (Cornulotrocha) and the slightly arcuate isochelae of C.(M. ?) brepha, which suggests this species is probably misidentified in C. (Microciona) (Hajdu et al., in prep.).Within the remaining six species, two do not possess chelae, and are also thus quite distinct from the new species:C. (M.) antarctica and C. (M.) californiana. The first of these, in addition, has styles up to 900 µm long, which aremuch larger than the largest megascleres observed here in the new species. The latter differs further through itssmaller megascleres and toxas, and apparent lack of accessory acanthostyles. The four remaining species appearcloser to the new one, but can also be confidently recognized as distinct, as follows.

FIGURE 2. Clathria (Microciona) aculeofila sp. nov. in situ on spines of the sea urchin Eucidaris thouarsii (a, b, c, d) andencrusting rocky substrates (e, f). a, b = CZA 11332, c = CZA 12981, d = CZA 12982, e = CZA 11437, f = CZA 13031. Whitearrows indicate the sponge; black arrows indicate bare spines or bare tips of the spines. Scale bars: a = 3 cm; b = 2 cm; c = 3cm; d - f = 2 cm.

Clathria (M.) discreta has fully spined acanthostyles as principal megascleres, relatively rare toxas, which con-sequently have an unknown length range [ca. 80 µm according to Thiele (1905)], and isochelae, which are smallerthan those encountered in the new species. Additionally, the Chilean species was described as small round masses(Thiele, 1905) or bearing cylindrical lobes (Desqueyroux, 1972), neither recognized features of the new species.

Clathria (M.) microjoanna and C. (M.) parthena possess totally smooth principal megascleres. Furthermore, deLaubenfels (1932) did not report toxas smaller than 60 µm in the former, nor isochelae smaller than 24 µm in thelatter. Finally, C. (T.) membranacea needs a revision, as Desqueyroux (1972) described materials divergent fromThiele’s (1905) original description. Thiele´s material differs from the new species by its considerably shorter prin-cipal spicules, accessory acanthostyles which appear to be absent, and toxas reported to reach only 70 µm in length.On the other hand, Desqueyroux’s sponges come closer to the new species because of their larger and stouter prin-cipal spicules, but they also have smaller toxas, and no accessory acanthostyles, and above all, the reported occur-rence of anisochelae suggests better placement elsewhere, possibly in C. (Cornulotrocha). A formal decision onthis matter has to await a detailed revision of all relevant material. This far, the only Chilean Clathria with aniso-chelae is C. (Cornulotrocha) rosetafiordica Hajdu et al. 2006 from the fjords region. This species differs from the


new one, as pointed out above, and also from Desqueyroux’s sponges in having smaller anisochelae and lack oftoxas. The new species appears thus well distinguished from allied forms in neighboring biogeographic provinces.

TABLE 2. Comparative micrometric, habit, distribution and depth data for the species of Clathria (Cornulotrocha), C. (Micro-ciona) and C. (Thalysias) known from the Warm Temperate Northeast Pacific, Tropical East Pacific, Juan Fernández and Des-venturadas, Warm Temperate Southeast Pacific and Magellanic provinces. Values are in micrometres. (adapted from Hajdu etal., 2006).

Species(M., Microciona; T., Thalysias)

Megascleresaa, access. acanthostyles; as, auxil. (subtylo)styles; at, access. tylostyles; ba, basally acan-those; ps, princ. styles; pt, princ. tylostyles

Microscleresc, chelae; t, toxas

Distribution - Habit - Recorded Depth

Clathria (Cornulotrocha) spp.

C. (M. ?) polita (Ridley, 1881) (orig. descr., as Hymedesmia p.; transferred here to C. (Cornu-lotrocha))

ps (acant. ¼ the length), 253 x 9as, 241 x 4aa, 101 x 6

c, 13 (in rosettes) Magellan Area (Sandy Point) - thin crust, 0.6mm thick - 13-18 m depth

C. (C.) rosetafiordica Hajdu et al., 2006 (descrip. orig.)

ps (acant. ¼ the length), 115-238.8-525 x 11-14as, 176-223.6-240 x 4aa, 101 x 6

c, 10-13 (in rosettes) North of the Fjords Region of Chile (Quintupeu Fjord) - thin crust, 0.6 mm thick - 13-18 m depth

Clathria (Microciona) spp.

C. (M.) antarctica (Topsent, 1917) (sensu Hooper, 1996 - data on holotypes of Stylostichon tox-iferum Topsent, 1913 & Micro-ciona basispinosa Burton, 1934, compiled)

ps, 293-509.1-676 x 9-13.2-22as, 213-392.9-899 x 4-8.9-16aa, 52-120.5-265 x 2.5-7.8-11

t, 18-37.0-84 x 0.8-2.1-4.0

Gough I., Antarctica - thick crust, cushion-shaped, sub-spherical - 18-200 m depth

C. (M.) antarctica (Topsent, 1917) (sensu Desqueyroux, 1972, as Microciona basis-pinosa)

ps, 350-900 x 11-12as, 240-600 x 4-10aa, 77-280 x 5-10

t, 28-44 Chile (ca. 37-42º S) - cushion-shaped - 6-10 m depth

C. (M. ?) brepha (de Laubenfels, 1930) (sensu de Laubenfels, 1932, as Anaata b.)

ps (acant.), 95-130 x 8as, 190-210 x 3

c, 17-21 (arcuate ?) California, Bor. E. Pac. - salmon-red, thin crust - inter-tidal

C. (M.) californiana (de Lauben-fels, 1930) (sensu de Lauben-fels, 1932, as Ophlitaspongia pennata var. c.)

pt, 215-261 x 17-22at, 140 x 2 (originally not reported as a second category)

t, 45-55 California, NW Pac. - scarlet, 2.5 mm crust - intertidal

C. (M.) discreta (Thiele, 1905) (orig. descr., as Microciona d.)

ps (acant.), ca. 250 x 15as, ca. 200 x 3aa, ca. 125 x 7

c, ca. 6t, ca. 80

Chile (Calbuco, ca. 42º S) - cushion-shaped

C. (M.) discreta (Thiele, 1905) (holotype remeasured)

ps (acant.), 257-313.5-446 x 10-21-24as (ba), 178-267.8-337 x 3.6-5.3aa, 120-139.9-158 x 14-19

c, 7-10t, not found

C. (M.) discreta (Thiele, 1905) (sensu Desqueyroux, 1972, as Dictyociona d.)

ps (acant), 210-280 x 16as (ba), 170-240 x 3-5aa, 90-130 x 8

c, 8t, 50-300

Chile (ca. 37-53º S) - thin crust - 0-10 m depth

C. (M.) microjoanna (de Lauben-fels, 1930) (sensu de Lauben-fels, 1932, as Microciona m.)

ps, 280-330 x 20-27as, 205-260 x 3-4aa, 85-100 x 5-10

c, 12-16t, 60-140

California, Bor. E. Pac. - bril-liant scarlet or rich pink, cush-ion-shaped - intertidal (?) to 18 m depth

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The genetic homogeneity of Clathria sponges occurring in distinct spines of the same sea urchin remains to beinvestigated. We preferred to be on the safe side, following the advice by van Soest (in litt.), and nominate the holo-type from a single spine.

Sea urchin abundance and dimensions at Punta Sal. The three transects evaluated had a total of 377 seaurchins, thus 6.28 sea urchins/m2. The mean density ranged from 1.5 to 12 sea urchins/m2, calculated from sixobtained counts (each 10 x 2 m transect had 50% evaluation by each of two divers). Test dimensions ranged from3.2 to 5.6 cm in greatest diameter and 1.8 to 4.1 cm in height, measured from the 30 collected sea urchins.

Frequency and intensity of sponge–sea urchin association. Total number of spines for each collected seaurchin ranged from 68 to 96, with a sponge coverage percentage ranging from 18.2 to 75.7. As expected, the small-est sea urchins, presumably the younger, had the least sponge coverage, but this is not striking. Sea urchins withtests only up to 4.4 cm in diameter (N = 20) had mean sponge coverage of 45.5%, while those with tests rangingfrom 4.5 to 5.6 cm (N = 10) had mean coverage of 49.5%. Nevertheless, densely covered small sea urchins werealso observed (4 cm test, 75.7% coverage), as well as slight coverage of large individuals (5.6 cm test, 18.9% cov-erage). This suggests that factors other than sea urchin age also play an important role in shaping this association.An important assumption here is that larger sea urchins are older.

Etymology. The species name aculeofila is derived from the Latin word 'aculeus' (= thorn, sting, prickle) andthe Greek word 'philos' (= love), and refers to the species observed abundance as an epibiont on cidaroid spines.

TABLE 2. (continued)

Species(M., Microciona; T., Thalysias)

Megascleresaa, access. acanthostyles; as, auxil. (subtylo)styles; at, access. tylostyles; ba, basally acan-those; ps, princ. styles; pt, princ. tylostyles

Microscleresc, chelae; t, toxas

Distribution - Habit - Recorded Depth

C. (M.) parthena (de Laubenfels, 1930) (sensu de Laubenfels, 1932, as Microciona p.)

ps, 350-475 x 27-33as, 260-300 x 3-5aa, 100-108 x 5-8

c, 24-28t I, 40-72 x 3-7t II, 14-22

California, Bor. E. Pac. - red, cushion-shaped - 26-45 m depth

C. (M.) spongigartina (de Laubenfels, 1930) (sensu de Laubenfels, 1932, as Anaata s.)

ps (acant.), 115-390 x 13as, 190-210 x 5-6

c I, 42-50 (arcuate?)c II, 23-25 (arcuate?)

California - rich brown slightly reddish, crust 5 mm - intertidal

Clathria (Thalysias) spp.

C. (T.) amabilis (Thiele, 1905) (descrip. orig., como Stylotellop-sis a.)

ps, 300 x 7as (acant.), 270 x 10aa, 150-160 x 10

absent Punta Arenas, SW Atl. (Tierra del Fuego, Falklands/ Malvi-nas), Antarctica – red-pink, 3-4 mm, firm and solid – 19 m depth

C. (T.) membranacea (Thiele, 1905) (descrip. orig.)

ps, 150 x 9as. I, 390 x 9as. II, up to 420 x 3aa, absent

c, 17t, 70

Isls. Juan Fernandez, SW Atl. (Uruguai, Falklands/Malvi-nas) – thin crust, 0.7 mm

C. (T.) membranacea (Thiele, 1905) (holotype remeasured)

ps (?), 406-430.7-465 x 7-10as I (?), 127-280.9-384 x 2-4as II, (?) 127-154.5-264 x 6-7aa, absent

c, 17-19t, 46-75.7-125 x 1-2

C. (T.) membranacea (Thiele, 1905) (sensu Desqueyroux, 1972, as Ophlitaspongia m.)

ps, 360-510 x 13-28as. I (ba), 240-300 x 3-6as. II, absentaa, absent

Palmate anisochelae, 9-21t (sometimes microspined tips), 42-79

Chile (ca. 37ºS) - crust – 10 m depth

C. (T.) originalis (de Laubenfels, 1930) (sensu de Laubenfels, 1932, as Esperiopsis o.)

pt, 150-155 x 12-13at, present

c, 13-16 California, Pac. L. Bor. – light brownish-red, thick layer - intertidal


FIGURE 3. Transversal fracture of a spine of the sea urchin Eucidaris thouarsii (SEM) showing the structure of the skeleton ofClathria (Microciona) aculeofila sp. nov. MNRJ 13317. 1 = basal layer of spongin, 2 = echinated paucispicular fibres.

Discussion

The spines of the Echinoidea are characterized by being surrounded by an epidermis which serves as an antifoul-ing, except for cidarids which are provided with muscle and collagen, only in the basal part of the thorns. Themicrostructure of their spines also facilitates the settlement of epibiont fauna (David et al., 2009). Actually, epibio-sis on cidarid spines is reported at least from the Upper Pennsylvanian (ca. 300 MA; Schneider, 2003), where nosize difference between sea urchins with epibionts and those without could be found, which matches our observedslight difference only (see above), and supports the idea that epibiosis in cidarids might not be directly correlatedwith sea urchin age.

Hétérier et al. (2004) found 25 species of sponges occurring as epibionts (ectosymbionts) on the spines ofCtenocidaris spinosa (Koehler, 1926) and ten on those of Rhynchocidaris triplopora (Mortensen, 1909) in theWeddell Sea. Only five species occurred on both sea urchins. Given that sponges range among the most commoninhabitants of this area, Hétérier et al. (2008) suggested the association with cidarid spines might be an opportunis-tic one, albeit shaped by sponge preference, as only a small subset of epibiontic sponge species are shared betweenthe two cidarid species considered. This is in marked contrast with our observations on Eucidaris thouarsii, wherea single, notably dominant epibiontic sponge species is found, notwithstanding the rich sponge coenosis observedin the same area (Willenz et al., in prep.). The epibiontic sponge, Clathria (Microciona) aculeofila sp. nov., is farfrom being a dominant sponge in the Punta Sal region, if its epibiontic occurrence is not computed. Accordingly, itappears quite obvious that this species has a strong preference for the sea urchin habitat, and also a way of reachingthis habitat first, and defending it from other possible space competitors.


FIGURE 4. Ground section of a spine of the sea urchin Eucidaris thouarsii covered by Clathria (Microciona) aculeofila sp.nov. MNRJ 13317. Scale bar = 200 µm.

Hétérier et al. (2008) found that cidarid echinoids modify the local benthic diversity in the deep Weddell Sea.They found cidarids in two sampling stations, one with Aporocidaris milleri Agassiz, 1898, the other with Ctenoci-daris speciosa Mortensen, 1910. This induced modification was inferred from the observation that different sta-tions showed comparatively similar rock–dwelling fauna, while rather distinct assemblages were found whencomparing cidarids and rocks in the same station. They also found that different communities were associated toeach cidarid species, thus inferring that cidarid morphology may determine to a great extent their epibiotic fauna.Our own results point to environmental constraints on epibionts, as Clathria (Microciona) aculeofila sp. nov. is byfar the dominant epibiontic organism on Eucidaris thouarsii’s spines in the Punta Sal area (including Cancas, ElÑuro, Máncora), while only a 'merely common' epibiont in the Lobos de Afuera Islands, where the biota is morefrequently subjected to subtropical climatic conditions. On the other hand, it is important to highlight that the newClathria has only been found outside sea urchin spines in the Punta Sal Region, not in the islands. Thus, its markeddominance as an epibiont in Punta Sal, after all, might be a consequence of its greater density in this area.

Other reported cases of sponge epibiosis on cidarid sea urchins are those of 11 Antarctic species on Ctenoci-daris perrieri Koehler, 1912, an association which differs from the present one in its non-specificity, as well as thatthe main sponge epibiont is erect, rather than encrusting (Cerrano et al., 2009). This latter trait probably reflects thefact that the specimens studied by Cerrano et al. (2009) were collected in a low energy deep–sea mimicking envi-ronment. The moderately shallow areas sampled in our studies in Peru can all be subject to high energy events,locally known as “maretazos, which explain why Eucidaris is mainly found in crevices, as well as why encrustingepibionts would have a greater chance of success.

Several species of Clathria are known to be facultative epibionts. Hooper (1996) listed 11 species classified insubgenera Clathria (Clathria) Schmidt, 1862; C. (Wilsonella) Carter, 1885; C. (Microciona), C. (Dendrocia) Hall-mann, 1920 and C. (Thalysias) Duchassaing and Michelotti, 1864. Nevertheless, none of these have been reportedto be a dominant and nearly exclusive epibiont on their biological substrates, which comprised algae, bivalves, cor-als, gorgonians, hydroids and worm tubes. The single other known Clathria epibiosis on echinoids is that of C. (C.)toxipraedita Topsent, 1913 on Ctenocidaris perrieri reported briefly by Cerrano et al. (2009). The easy access tosponge–covered Eucidaris thouarsii in northern Peru renders this an ideal target for future deeper studies of factorsdetermining recruitment on and colonization of new spines. Description of the sponge associate was an importantfirst step in this direction.


FIGURE 5. Spicule composition of a red Clathria (Microciona) aculeofila sp. nov. (MNRJ 11449) in SEM. A–C, principalsubtylostyles; D–F, details of respectively A–C; G–I, accessory acanthostyles; J, detail of I; K–M auxillary styles and subtylo-styles; N–P, details of the base of K–M; Q–R, details of the extremities of L–M; S, toxas; T, isochelae. Scale bars: A–C = 100ìm; G–I = 20 ìm; J = 5 ìm; K–M = 50 µm; N–R = 10 µm; S = 20 µm; T = 5 µm.


FIGURE 6. Spicule composition of a yellow Clathria (Microciona) aculeofila sp. nov. (MNRJ 12982) in SEM. A–C, principalsubtylostyles; D–E, details of respectively A–B; F–G, accessory acanthostyles; H, detail of G; I–J auxillary styles and subtylo-styles; K–N, details of various auxillary styles and subtylostyles; O, toxas; P, isochelae. Scale bars: A–C = 100 ìm; D–E = 10 ìm; F–G = 20 ìm; H = 5 µm; I–J = 50 µm; K–N = 10 µm; O = 20 µm; P = 5 µm.


Acknowledgements

Comparative materials (isolated, sponge–covered spines of E. thouarsii) were obtained from Pacific Panama,thanks to the generosity of H.A. Lessios. We are grateful to C. De Ridder and R.B. Moura for providing literatureon sea urchins; to L. Despontin, J. Cillis and E. de Lima for technical assistance with sample preparation and scan-ning electron microscopy; and to W.F. Vieira for helping with the field work transects.

The ESPER Project was funded by the Global Taxonomy Initiative from the Belgian Development Coopera-tion; the Proyecto EsponjAS was funded by Conselho Nacional de Desenvolvimento Científico e Tecnológico(CNPq/PROSUL). K. Aguirre received a grant from Consejo Nacional de Ciencia, Tecnología e Innovación Tec-nológica (CONCYTEC). The Servicio Nacional de Areas Naturales Protegidas (SERNANP), Agrorural (ex Proa-bonos) and the Dirección de Hidrografía y Navegación del Perú are acknowledged for permitting access to IslaLobos de Afuera and for logistical support.

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