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Zootaxa 3085: 4154 (2011) www.mapress.com / zootaxa/ Copyright 2011 Magnolia Press
ISSN 1175-5326 (print edition)

Article

ZOOTAXA
ISSN 1175-5334 (online edition)

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
1 Laboratorio de Biologa Marina, Facultad de Ciencias y Filosofa, Universidad Peruana Cayetano Heredia, Calle Honorio Delgado 430, Lima 31, Lima, Per. E-mail: karemaguirre@gmail.com, hookery@yahoo.com 2 Department of Invertebrates, Section Malacology, Royal Belgian Institute of Natural Sciences (RBINSC), Rue Vautier 29, B1000, Brussels, Belgium. E-mail: philippe.willenz@naturalsciences.be 3 Museu Nacional, Departamento de Invertebrados, Universidade Federal do Rio de Janeiro, Quinta da Boa Vista, s/n, 20940040, Rio de Janeiro, RJ, Brazil. E-mail: eduardo.hajdu@gmail.com 4 Corresponding author

Abstract
Southeastern Pacific sponges (Phylum Porifera) range among the worlds least known faunas, with only 13 species reported to date from the entire Peruvian coast. This state of affairs motivated the onset of two large, cooperative, exploratory initiatives, with the aim of mapping sponge richness and distribution in the area: Proyectos ESPER and EsponjAS. Over 800 specimens have been collected in Peru since 2007, with identifications still in progress. Among these, a sponge species originally thought to be an exclusive epibiont on Eucidaris thouarsii sea urchins, relatively conspicuous on Perus Punta 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 18.2 and 75.7. There appears to be only a slight tendency for increased sponge coverage on larger sea urchins, so there may be factors, other than sea urchin age, shaping this association. Clathria (Microciona) aculeofila sp. nov. can be markedly dominant as an epibiont on E. thouarsii, albeit the great sponge richness in the area. This is in contrast to the allegedly opportunistic, 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 biological, chemical and pharmaceutical properties, Southeastern Pacific species range among the least known in the world (Hajdu and DesqueyrouxFandez 2008). Only 13 species belonging to the Demospongiae (4) and Hexactinellida (9) are this far known from Peru, with no Calcarea yet recorded. The complete list comprises the demosponges Acarnus peruanus van Soest et al., 1991; Dysidea ligneana (Hyatt, 1877); Myxilla asymmetrica DesqueyrouxFandez and van Soest, 1996; Myxilla dracula DesqueyrouxFandez and van Soest, 1996; and the hexactinellids Bathydorus spinosissimus Lendenfeld, 1915; Eurete spinosum Lendenfeld, 1915; Holascus edwardsi Lendenfeld, 1915; Hyalonema agassizi Lendenfeld, 1915; H. agujanum Lendenfeld, 1915; H. bianchoratum pinulina Lendenfeld, 1915; H. tenuifusum Lendenfeld, 1915; H. tylostylum Lendenfeld, 1915 and Sympagella cantharellus Lendenfeld, 1915. With the exception of Acarnus peruanus and Dysidea ligneana, all these sponges come from deep waters. This meager list was the main reason to start the ESPER Project (Esponjas del Per) in 2007 and Proyecto EsponjAS (Esponjas da Amrica do Sul) in 2008, with the aim of mapping sponge richness and distribution along the Peruvian coast. This is also a natural follow up for Hajdu, Willenz et al.'s taxonomic studies of Chilean sponges (e.g. Azevedo et al., 2009; Willenz et al., 2009).

Accepted by J. Hooper: 22 Sep. 2011; published: 31 Oct. 2011

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The recent intensive collecting undertaken along Perus coastline yielded over 800 specimens and thousands of underwater images of sponges and their habitats, which are now sorted into major taxonomic groups, providing the basis for ongoing taxonomic study undertaken in Brussels, Geneva, Lima and Rio de Janeiro. In this work we describe 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 of these sea urchins, the frequency and intensity of the association between Clathria sp. nov. and the sea urchins spines as well as the gutcontents 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 dimensions, depth and temperature of the habitat recorded at the same time. Collecting localities were Lobos de Afuera Islands, Cancas, El uro, Mncora and Punta Sal, indicated in the map shown in Figure 1. This area is located at the transition zone between the Guayaquil and Central Peru marine ecoregions (Panamic Region), being thus subject to the alternating effects of the Panama (Tropical/Subtropical) and Humboldt (Subtropical/Temperate) currents systems. Water temperatures in this zone can be as cold as 1213C and warmer than 25C, depending on the time of the year and prevailing current system. The density and distribution of sea urchins, as well as frequency and intensity of the sponge association were evaluated in three linetransects with 10 x 2 m at the spots known as Bajo El Cardo (035853.9S, 805920.5W) and Balneario I (035720.3S, 805756.2W) (Punta Sal). Ten sea urchins were collected randomly at 10 m depth (19C) for calculation of quantitative traits of the sponge association, and extensive visual counts were undertaken along the transect. A third sampling was conducted at Balneario II (035716.9S, 805756.4W) at 15 m depth (19C). Sea urchins had the height and width of their tests, as well as percentage of spongecovered spines recorded. Immediately afterwards, sea urchins still in seawater-filled buckets, had their guts and Aristotle lanterns removed and preserved in 96% ethanol. Materials used for the identification, apart from dozens of underwater images, were a few collected specimens from Lobos de Afuera Islands and Punta Sal. The identification of the sea urchins was based on comparisons to the descriptions of Mortensen (1910), Clark (1948), Caso (1979), and Lessios (2005, and in litt. 2010). Sponges were identified on the basis of their dissociated spicules and thick sections, under light as well as scanning electron microscopy. In general, procedures followed standards presented by Rtzler (1978) and Mothes de Moraes (1985), with some additions which are presented below. A spongecovered spine was prepared for SEM study according to the papain enzymatic protocol outlined by Pinheiro and Hajdu (2001), which consisted of sectioning 2 cm out from a spine, adding this and 30 ml digestion buffer (100 mM sodium acetate, pH 5.0; cisteine 5 mM; 5 mM EDTA) to a Falcon tube kept for 24 hours at 4C. Subsequently, 1 ml of a 3 % papain solution (freshly made in digestion buffer) was added to the sponge digestion tube and incubated at 60C for 24 h. The digested fragment was then gently washed with water jets to finish the cleaning of its spiculofibers. The preparation was then dehydrated back in ethanol 96 % for 1 h, dried under a warm lamp, attached to a stub with doublesided carbon tape, and vacuumcoated with evaporated gold prior to SEM. Another section from a sea urchin spine has been obtained by sawing specimens embedded in low viscosity epoxy resin (Spurr Low Viscosity Embedding Media, Polysciences, Inc) with a lowspeed saw (Labcut 1010, Agar Scientific Ltd.) using a diamond wafering blade, and wetground on polishing discs. Abbreviations used: CZA (Coleccin de Zoologa Acutica, Universidad Peruana Cayetano Heredia, Lima, Peru), MHNG (Museum dHistoire naturelle, Geneva, Switzerland), MNRJ (Museu Nacional, Universidade Federal do Rio de Janeiro, Rio de Janeiro, Brazil), RBINS (Royal Belgian Institute of Natural Sciences, Brussels, Belgium), STRI (Smithsonian Tropical Research Institute, Balboa, Panama).

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FIGURE 1. Map of Peru with collection localities of Clathria (Microciona) aculeofila sp. nov. and details of the Punta Sal region. 1 = Cancas; 2 = Punta Sal, Punta Sal Balneario I and Punta Sal Balneario II; 3 = Mncora; 4 = El uro; 5 = Lobos de Afuera Islands.

Systematics Class Demospongiae Sollas Order Poecilosclerida Topsent Suborder Microcionina Hajdu, van Soest and Hooper Family Microcionidae Carter

CLATHRIA (MICROCIONA) ACULEOFILA SP. NOV.

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Genus Clathria Schmidt Subgenus Clathria (Microciona) Bowerbank Clathria (Microciona) aculeofila sp. nov. (Figs 16; Tabs 12)
Type material. Holotype CZA 13317 (schizotypes MNRJ 13317, RBINS POR 2000, MHNG 76056) Bajo El Cardo (Punta Sal035716.90S, 805756.40W, 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 Quebrada Verde (El uro041322.30S, 811224.10W, Piura, Peru), 45 m deep, coll. Y. Hooker and M. Rios, 14.Oct.2007. CZA 11332 (schizotypes MNRJ 11332, RBINS POR 2001, MHNG 76058), Islote El Lagarto (Lobos de Afuera Islands065601.20S, 804219.90W, 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 Islands065452.50S, 804255.90W, 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 uro041330.40S, 811231.60W, Piura, Peru), 10.0 m deep, Y. Hooker and M. Rios, 14.Oct.2007. CZA 11453 (schizotypes MNRJ 11453, RBINS POR 2005, MHNG 76146, Baja de Quebrada Verde (El uro 041322.30S, 811224.10W, Piura, Peru), 45 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 uro041322.30S, 811224.10W, Piura, Peru), 8 m deep, coll. Y. Hooker and M. Rios, 18.Oct.2007. CZA 12955 (schizotypes MNRJ 12955, RBINS POR 2007, MHNG 76149), the fishermens pier (Mncora040635.65S, 810402.50W, 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 Sal035834.10S, 805906.00W, Piura, Peru), 13.2 m deep, coll. Y. Hooker and B. Ibaez, 21.Nov.2009. CZA 12982 (schizotypes MNRJ 12982, RBINS POR 2009, MHNG 76151), Balneario anchorage (Punta Sal035804.10S, 805809.30W, Piura, Peru), ca. 10.0 m deep, coll. Y. Hooker and C. Segami, 21.Nov.2009. CZA 12989 (schizotypes MNRJ 12989, RBINS POR 2010, MHNG 76152), (El uro04141.00S, 811246.00W, 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 fishermens pier (El uro041300.00S, 811050.10WPiura, 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 (Cancas035514.10S, 805429.90WPiura, 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, with principal megascleres mostly bearing spines only at the base, auxiliary megascleres which are either smooth or paucispined at the base, smooth toxas in one or two length categories frequently over 100 m long, and palmate isochelae in a single category, normally smaller than 15 m long. Description. Habit. Sponges are usually thinly encrusting (< 1 mm thick), but slightly thicker sponges can be found 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 34 cm2 in area epibiont coverage, and specimens were not seen stretching from one spine into another. Larger specimens were found on rocky substrate, in this case reaching over 16 x 14 cm in area (e.g. CZA 11490). Surface is hispid and texture velvety. Consistency soft, but in parts it is the hard substrate that one feels when touching the sponge. Colour in life brightred (CZA 11332, 11380, 11437, 11449, 11453, 11490, 12981, 12955, 12989) or yellow (CZA 12982, 13031, 13066), turning into beige after preservation with ethanol. Meandering subectosomal canals are clearly visible in yellow specimens only, and scattered oscules could only be seen in the pictures taken from CZA 11490 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 (2030 m across) from which short, echinated fibres arise (up to 600 m high). Principal megascleres stand erect on the substrate, held erect by the basal layer of spongin, but also slightly above, coring or echinating the fibres. Auxiliary megascleres arranged in disorganized (sub)ectosomal bouquets, frequently piercing the surface. Spicules in these bouquets are frequently laying tangential to the surface. Microscleres of variable abundance are scattered.

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Spicules. Megascleres (Fig. 5AR; Fig. 6AN, Table 1). Principal subtylostyles (Fig. 5AF; Fig. 6AH), variably stout, slightly curved, slightly fusiform, tapering gradually to a sharp apex; base slightly swollen, roundish, irregularly acanthose, with variably sharp (blunt verrucose to pointy thorn), straight or bent spines; smooth shaft. Auxiliary subtylostyles (Fig. 5KR; Fig. 6IN), smooth, slender, straight, tapering gradually to a sharp apex; base barely swollen, elliptical, smooth or bearing a crown of sharp, straight spines; smooth shaft. Accessory acanthostyles (Fig. 5GJ; Fig. 6FH), variably stout, slightly curved, slightly fusiform, tapering gradually to a sharp 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 additional comparative materials. Values are in micrometres.
CZA # Color / Sub- Principal subtylostyles strate 11332 11380 11437 11449 11453 11490 12955 12981 12982 12989 13031 13066 13317 Red / Eucidaris Red / Eucidaris Red / Rock Red / Eucidaris Red / Rock Red / Rock Red / Rock Red / Eucidaris Yellow / Eucidaris Red / Spondylus Yellow / Rock Yellow / Eucidaris Red / Eucidaris 172-307-607 / 7-15.7-28 Auxiliary sub- Accessory acanthostyles tylostyles 125-263.3-407 86-90-103 / 7-7.9-9 Isochelae 13-13.8-15 16 10-13.6-18 9-13.2-17 8-13.2-17 10-14-30 15-35.5-45 11-14.1-16 12-12.4-14 10-13.1-17 10-13.6-16 12 Toxas 20-57.1-110 40-65.6-123 16-52.4-109 38-74.5-132 67-112.9-153 41-80.7-140 38-52.2-110 38-48.8-77 24-49.2-74 42-83.3-146 19-49.9-101 60-69-72 33-69.7-114

132-231.4-418 / 9.4-15.3-22 162-227.8-308 85-100.9-128 / 6-3.5-13 78-142.2-324 / 6-10-16 75-215.4-428 / 7-13-20 68-115.5-239 / 5-7.5-11 101-205.7-283 / 6-11.2-20 74-259-588 / 4-12-24 71-169.4-254 / 9-10.9-15 312-455.7-760 83-85.3-91 / 7-7.5-8 116-240.2-350 67-74-78 / 7-7.1-8 113-208-327 114-218-310 71-76.4-80 / 6-7.1-9 79-88.5-101 / 6-8-9

229-295.1-379 72-80.8-89 / 5-6-7 144-191.7-220 73-77-81 / 7-6.9-7

69.6-138.2-300 / 2.4-5.7-9.6 182-224.5-258 84-86.4-91 / 5-6.4-7 95-188-465 / 7-13-26 215-274.8-413 / 10-13.6-18 145-240-319 104-175-295 51-84.6-96 / 5-6.8-9 76-94.3-131 / 6-8.2-11

64.8-124.4-432 / 2.4-5.3-9.6 130-230.5-304 65-86.4-109 / 6-7.6-9 111-184-318 / 5-9.5-13 115-178-258

103-121.8-132.8 / 7.4-9.7- 10-13.7-15 11.7

Microscleres (Fig. 5ST; Fig. 6OP). Palmate isochelae (Fig. 5T; Fig. 6P), mostly with nearly straight, slender shafts, only seldom slightly twisted or curved, claws 3845 % the entire spicule length. Toxas (Fig. 5S; Fig. 6O), smooth, common, Vtype (gentle central curve and nearly no curves on extremities); the smallest ones are usually 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 temperatures of 14 to 23C. In Cancas, El uro, Mncora, Punta Sal and Lobos de Afuera cidarid sea urchins were relatively common and these had nearly always their spines covered by the Clathria aculeofila sp. nov. Apparently most, 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 distinguish 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 new species described here. Only 12 species of these subgenera are this far known from provinces adjacent to the type locality of the new species, viz. the Warm Temperate Northeast Pacific, the Tropical East Pacific, the Juan Fernn-

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dez and Desventuradas, the Warm Temperate Southeast Pacific and the Magellanic provinces (Table 2). Among these, 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 distinction in 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 m long, which are much larger than the largest megascleres observed here in the new species. The latter differs further through its smaller megascleres and toxas, and apparent lack of accessory acanthostyles. The four remaining species appear closer 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) and encrusting rocky substrates (e, f). a, b = CZA 11332, c = CZA 12981, d = CZA 12982, e = CZA 11437, f = CZA 13031. White arrows indicate the sponge; black arrows indicate bare spines or bare tips of the spines. Scale bars: a = 3 cm; b = 2 cm; c = 3 cm; d - f = 2 cm.

Clathria (M.) discreta has fully spined acanthostyles as principal megascleres, relatively rare toxas, which consequently have an unknown length range [ca. 80 m according to Thiele (1905)], and isochelae, which are smaller than 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, de Laubenfels (1932) did not report toxas smaller than 60 m in the former, nor isochelae smaller than 24 m in the latter. Finally, C. (T.) membranacea needs a revision, as Desqueyroux (1972) described materials divergent from Thieles (1905) original description. Thieles material differs from the new species by its considerably shorter principal spicules, accessory acanthostyles which appear to be absent, and toxas reported to reach only 70 m in length. On the other hand, Desqueyrouxs sponges come closer to the new species because of their larger and stouter principal spicules, but they also have smaller toxas, and no accessory acanthostyles, and above all, the reported occurrence of anisochelae suggests better placement elsewhere, possibly in C. (Cornulotrocha). A formal decision on this matter has to await a detailed revision of all relevant material. This far, the only Chilean Clathria with anisochelae is C. (Cornulotrocha) rosetafiordica Hajdu et al. 2006 from the fjords region. This species differs from the

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new one, as pointed out above, and also from Desqueyrouxs sponges in having smaller anisochelae and lack of toxas. 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. (Microciona) and C. (Thalysias) known from the Warm Temperate Northeast Pacific, Tropical East Pacific, Juan Fernndez and Desventuradas, Warm Temperate Southeast Pacific and Magellanic provinces. Values are in micrometres. (adapted from Hajdu et al., 2006). Species (M., Microciona; T., Thalysias) Microscleres Megascleres c, chelae; t, toxas aa, access. acanthostyles; as, auxil. (subtylo)styles; at, access. tylostyles; ba, basally acanthose; ps, princ. styles; pt, princ. tylostyles ps (acant. the length), 253 x 9 c, 13 (in rosettes) as, 241 x 4 aa, 101 x 6 ps (acant. the length), 115238.8-525 x 11-14 as, 176-223.6-240 x 4 aa, 101 x 6 ps, 293-509.1-676 x 9-13.2-22 as, 213-392.9-899 x 4-8.9-16 aa, 52-120.5-265 x 2.5-7.8-11 ps, 350-900 x 11-12 as, 240-600 x 4-10 aa, 77-280 x 5-10 c, 10-13 (in rosettes) Distribution - Habit Recorded Depth

Clathria (Cornulotrocha) spp. C. (M. ?) polita (Ridley, 1881) (orig. descr., as Hymedesmia p.; transferred here to C. (Cornulotrocha)) C. (C.) rosetafiordica Hajdu et al., 2006 (descrip. orig.) Magellan Area (Sandy Point) thin crust, 0.6mm thick - 13-18 m depth North of the Fjords Region of Chile (Quintupeu Fjord) - thin crust, 0.6 mm thick - 13-18 m depth Gough I., Antarctica - thick crust, cushion-shaped, subspherical - 18-200 m depth

Clathria (Microciona) spp. C. (M.) antarctica (Topsent, 1917) (sensu Hooper, 1996 - data on holotypes of Stylostichon toxiferum Topsent, 1913 & Microciona basispinosa Burton, 1934, compiled) C. (M.) antarctica (Topsent, 1917) (sensu Desqueyroux, 1972, as Microciona basispinosa) t, 18-37.0-84 x 0.8-2.1-4.0

t, 28-44

Chile (ca. 37-42 S) - cushionshaped - 6-10 m depth

C. (M. ?) brepha (de Laubenfels, ps (acant.), 95-130 x 8 1930) (sensu de Laubenfels, as, 190-210 x 3 1932, as Anaata b.) C. (M.) californiana (de Lauben- pt, 215-261 x 17-22 fels, 1930) (sensu de Laubenat, 140 x 2 (originally not fels, 1932, as Ophlitaspongia reported as a second category) pennata var. c.) C. (M.) discreta (Thiele, 1905) (orig. descr., as Microciona d.) C. (M.) discreta (Thiele, 1905) (holotype remeasured) ps (acant.), ca. 250 x 15 as, ca. 200 x 3 aa, ca. 125 x 7

c, 17-21 (arcuate ?)

California, Bor. E. Pac. salmon-red, thin crust - intertidal California, NW Pac. - scarlet, 2.5 mm crust - intertidal

t, 45-55

c, ca. 6 t, ca. 80

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

ps (acant.), 257-313.5-446 x 10- c, 7-10 t, not found 21-24 as (ba), 178-267.8-337 x 3.6-5.3 aa, 120-139.9-158 x 14-19 ps (acant), 210-280 x 16 as (ba), 170-240 x 3-5 aa, 90-130 x 8 c, 8 t, 50-300 c, 12-16 t, 60-140 Chile (ca. 37-53 S) - thin crust - 0-10 m depth California, Bor. E. Pac. - brilliant scarlet or rich pink, cushion-shaped - intertidal (?) to 18 m depth continued next page

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

C. (M.) microjoanna (de Lauben- ps, 280-330 x 20-27 as, 205-260 x 3-4 fels, 1930) (sensu de Laubenaa, 85-100 x 5-10 fels, 1932, as Microciona m.)

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TABLE 2. (continued) Species (M., Microciona; T., Thalysias) Microscleres Megascleres c, chelae; t, toxas aa, access. acanthostyles; as, auxil. (subtylo)styles; at, access. tylostyles; ba, basally acanthose; ps, princ. styles; pt, princ. tylostyles c, 24-28 t I, 40-72 x 3-7 t II, 14-22 c I, 42-50 (arcuate?) c II, 23-25 (arcuate?) Distribution - Habit Recorded Depth

C. (M.) parthena (de Laubenfels, ps, 350-475 x 27-33 1930) (sensu de Laubenfels, as, 260-300 x 3-5 1932, as Microciona p.) aa, 100-108 x 5-8 C. (M.) spongigartina (de Laubenfels, 1930) (sensu de Laubenfels, 1932, as Anaata s.) Clathria (Thalysias) spp. C. (T.) amabilis (Thiele, 1905) ps, 300 x 7 (descrip. orig., como Stylotellop- as (acant.), 270 x 10 sis a.) aa, 150-160 x 10 ps (acant.), 115-390 x 13 as, 190-210 x 5-6

California, Bor. E. Pac. - red, cushion-shaped - 26-45 m depth California - rich brown slightly reddish, crust 5 mm intertidal Punta Arenas, SW Atl. (Tierra del Fuego, Falklands/ Malvinas), Antarctica red-pink, 34 mm, firm and solid 19 m depth Isls. Juan Fernandez, SW Atl. (Uruguai, Falklands/Malvinas) thin crust, 0.7 mm

absent

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

ps, 150 x 9 as. I, 390 x 9 as. II, up to 420 x 3 aa, absent ps (?), 406-430.7-465 x 7-10 as I (?), 127-280.9-384 x 2-4 as II, (?) 127-154.5-264 x 6-7 aa, absent ps, 360-510 x 13-28 as. I (ba), 240-300 x 3-6 as. II, absent aa, absent

c, 17 t, 70

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

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

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

Palmate anisochelae, 9- Chile (ca. 37S) - crust 10 m 21 depth t (sometimes microspined tips), 4279 c, 13-16 California, Pac. L. Bor. light brownish-red, thick layer intertidal

C. (T.) originalis (de Laubenfels, pt, 150-155 x 12-13 1930) (sensu de Laubenfels, at, present 1932, as Esperiopsis o.)

The genetic homogeneity of Clathria sponges occurring in distinct spines of the same sea urchin remains to be investigated. We preferred to be on the safe side, following the advice by van Soest (in litt.), and nominate the holotype from a single spine. Sea urchin abundance and dimensions at Punta Sal. The three transects evaluated had a total of 377 sea urchins, thus 6.28 sea urchins/m2. The mean density ranged from 1.5 to 12 sea urchins/m2, calculated from six obtained counts (each 10 x 2 m transect had 50% evaluation by each of two divers). Test dimensions ranged from 3.2 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 spongesea urchin association. Total number of spines for each collected sea urchin ranged from 68 to 96, with a sponge coverage percentage ranging from 18.2 to 75.7. As expected, the smallest sea urchins, presumably the younger, had the least sponge coverage, but this is not striking. Sea urchins with tests only up to 4.4 cm in diameter (N = 20) had mean sponge coverage of 45.5%, while those with tests ranging from 4.5 to 5.6 cm (N = 10) had mean coverage of 49.5%. Nevertheless, densely covered small sea urchins were also observed (4 cm test, 75.7% coverage), as well as slight coverage of large individuals (5.6 cm test, 18.9% coverage). 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) and the Greek word 'philos' (= love), and refers to the species observed abundance as an epibiont on cidaroid spines.

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FIGURE 3. Transversal fracture of a spine of the sea urchin Eucidaris thouarsii (SEM) showing the structure of the skeleton of Clathria (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 antifouling, except for cidarids which are provided with muscle and collagen, only in the basal part of the thorns. The microstructure of their spines also facilitates the settlement of epibiont fauna (David et al., 2009). Actually, epibiosis on cidarid spines is reported at least from the Upper Pennsylvanian (ca. 300 MA; Schneider, 2003), where no size difference between sea urchins with epibionts and those without could be found, which matches our observed slight difference only (see above), and supports the idea that epibiosis in cidarids might not be directly correlated with sea urchin age. Htrier et al. (2004) found 25 species of sponges occurring as epibionts (ectosymbionts) on the spines of Ctenocidaris spinosa (Koehler, 1926) and ten on those of Rhynchocidaris triplopora (Mortensen, 1909) in the Weddell Sea. Only five species occurred on both sea urchins. Given that sponges range among the most common inhabitants of this area, Htrier et al. (2008) suggested the association with cidarid spines might be an opportunistic one, albeit shaped by sponge preference, as only a small subset of epibiontic sponge species are shared between the two cidarid species considered. This is in marked contrast with our observations on Eucidaris thouarsii, where a single, notably dominant epibiontic sponge species is found, notwithstanding the rich sponge coenosis observed in the same area (Willenz et al., in prep.). The epibiontic sponge, Clathria (Microciona) aculeofila sp. nov., is far from being a dominant sponge in the Punta Sal region, if its epibiontic occurrence is not computed. Accordingly, it appears quite obvious that this species has a strong preference for the sea urchin habitat, and also a way of reaching this habitat first, and defending it from other possible space competitors.

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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 m.

Htrier 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 Ctenocidaris speciosa Mortensen, 1910. This induced modification was inferred from the observation that different stations showed comparatively similar rockdwelling fauna, while rather distinct assemblages were found when comparing cidarids and rocks in the same station. They also found that different communities were associated to each 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 by far the dominant epibiontic organism on Eucidaris thouarsiis spines in the Punta Sal area (including Cancas, El uro, Mncora), while only a 'merely common' epibiont in the Lobos de Afuera Islands, where the biota is more frequently subjected to subtropical climatic conditions. On the other hand, it is important to highlight that the new Clathria has only been found outside sea urchin spines in the Punta Sal Region, not in the islands. Thus, its marked dominance 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 Ctenocidaris perrieri Koehler, 1912, an association which differs from the present one in its non-specificity, as well as that the main sponge epibiont is erect, rather than encrusting (Cerrano et al., 2009). This latter trait probably reflects the fact that the specimens studied by Cerrano et al. (2009) were collected in a low energy deepsea mimicking environment. 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 encrusting epibionts would have a greater chance of success. Several species of Clathria are known to be facultative epibionts. Hooper (1996) listed 11 species classified in subgenera Clathria (Clathria) Schmidt, 1862; C. (Wilsonella) Carter, 1885; C. (Microciona), C. (Dendrocia) Hallmann, 1920 and C. (Thalysias) Duchassaing and Michelotti, 1864. Nevertheless, none of these have been reported to be a dominant and nearly exclusive epibiont on their biological substrates, which comprised algae, bivalves, corals, 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 to spongecovered Eucidaris thouarsii in northern Peru renders this an ideal target for future deeper studies of factors determining recruitment on and colonization of new spines. Description of the sponge associate was an important first step in this direction.

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FIGURE 5. Spicule composition of a red Clathria (Microciona) aculeofila sp. nov. (MNRJ 11449) in SEM. AC, principal subtylostyles; DF, details of respectively AC; GI, accessory acanthostyles; J, detail of I; KM auxillary styles and subtylostyles; NP, details of the base of KM; QR, details of the extremities of LM; S, toxas; T, isochelae. Scale bars: AC = 100 m; GI = 20 m; J = 5 m; KM = 50 m; NR = 10 m; S = 20 m; T = 5 m.

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FIGURE 6. Spicule composition of a yellow Clathria (Microciona) aculeofila sp. nov. (MNRJ 12982) in SEM. AC, principal subtylostyles; DE, details of respectively AB; FG, accessory acanthostyles; H, detail of G; IJ auxillary styles and subtylostyles; KN, details of various auxillary styles and subtylostyles; O, toxas; P, isochelae. Scale bars: AC = 100 m; D E = 10 m; FG = 20 m; H = 5 m; IJ = 50 m; KN = 10 m; O = 20 m; P = 5 m.

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Acknowledgements
Comparative materials (isolated, spongecovered 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 literature on sea urchins; to L. Despontin, J. Cillis and E. de Lima for technical assistance with sample preparation and scanning 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 Cooperation; the Proyecto EsponjAS was funded by Conselho Nacional de Desenvolvimento Cientfico e Tecnolgico (CNPq/PROSUL). K. Aguirre received a grant from Consejo Nacional de Ciencia, Tecnologa e Innovacin Tecnolgica (CONCYTEC). The Servicio Nacional de Areas Naturales Protegidas (SERNANP), Agrorural (ex Proabonos) and the Direccin de Hidrografa y Navegacin del Per are acknowledged for permitting access to Isla Lobos de Afuera and for logistical support.

References
Agassiz, A. (1898) Reports on the dredging operations off the west coast of Central America to the Galapagos, to the West coast of Mexico, and in the Gulf of California, in charge of Alexander Agassiz, carried on by the U.S. Fish Commission Steamer "Albatros", during 1891, Lieut. Commander Z.L. Tanner, U.S.N., commanding. Bulletin of the Museum of Comparative Zoology at Harvard College, 33, 7186, pls IXIII, 71 map. Azevedo, F., Hajdu, E., Willenz, Ph. & Klautau, M. (2009) New records of Calcareous sponges (Porifera, Calcarea) from the Chilean coast. Zootaxa, 2072, 130. Carter, H.J. (1885) Descriptions of Sponges from the Neighbourhood of Port Phillip Heads, South Australia. Annals and Magazine of Natural History (5), 16, 277294. Caso, M.E. (1979) Los Equinodermos de la Bahia de Mazatln, Sinaloa. Cerrano, C., Bertolino, M., Valisano, L., Bavestrello, G. & Calcinai, B. (2009) Epibiotic demosponges on the Antarctic scallop Adamussium colbecki (Smith, 1902) and the cidaroid urchins Ctenocidaris perrieri Koehler, 1912 in the nearshore habitats of the Victoria Land, Ross Sea, Antarctica. Polar Biology, 32, 10671076. Clark, H.L. (1948) A report of the echini of the warmer eastern Pacific, based on the collections of the Velero III. Allan Hancock Pacific Expedition, 8, 225252. David, B., Stock, S.R., Carlo, F., Htrier, V. & De Ridder, C. (2009) Microstructures of Antarctic cidaroid spines: diversity of shapes and ectosymbiont attachments. Marine Biology, 156, 15591572. Desqueyroux, R.P. (1972) Demospongiae (Porifera) de la costa de Chile. Gayana, 20, 171. Desqueyroux-Fandez, R. & van Soest, R.W.M. (1996) A review of Iophonidae, Myxillidae and Tedaniidae occurring in the South East Pacific (Porifera: Poecilosclerida). Revue Suisse de Zoologie, 103, 379. Duchassaing de Fonbressin, P. & Michelotti, G. (1864) Spongiaires de la mer Carabe. Natuurkundige verhandelingen van de Hollandsche maatschappij der wetenschappen te Haarlem, 21, 1124, pls IXXV. Hajdu, E. & Desqueyroux-Fandez, R. (2008) A reassessment of the phylogeny and biogeography of Rhabderemia Topsent, 1890 (Rhabderemiidae, Poecilosclerida, Demospongiae). Revue Suisse de Zoologie, 115, 377395. Hajdu, E., Desqueyroux-Fandez, R. & Willenz, Ph. (2006) Clathria (Cornulotrocha) rosetafiordica sp. nov. from a south-east Pacific fjord (Chilean Patagonia) (Microcionidae: Poecilosclerida: Demospongiae: Porifera). Journal of the Marine Biological Association of the United Kingdom, 86, 957961. Hallmann, E.F. (1920) New genera of Monaxonid sponges related to the genus Clathria. Proceedings of the Linnean Society of New South Wales, 44, 767792, pls XXXVIXL. Htrier, V., David, B., De Ridder, C. & Rigaud, T. (2008) Ectosymbiosis is a critical factor in the local benthic biodiversity of the Antarctic deep sea. Marine Ecology Progress Series, 364, 6776. Htrier, V. & De Ridder, C. (2004) Comparative biodiversity of ectosymbionts in two Antarctic cidaroid echinoids, Ctenocidaris spinosa and Rhynchocidaris triplopora. In: T. Heinzeller & J.H. Nebelsick (Eds), Echinoderms Mnchen. Taylor & Francis, London, 201205. Hooper, J.N.A. (1996) Revision of Microcionidae (Porifera: Poecilosclerida: Demospongiae), with description of Australian species. Memoirs of the Queensland Museum, 40, 1626. Hyatt, A. (1877) Revision of the North American Poriferae; with remarks upon foreign species. Part II. Memoirs of the Boston Society of Natural History, 2, 481554, pls XVXVII. Koehler, R. (1912) Echinodermes (astries, ophiures et chinides). In: Deuxieme Expdition Antarctique Franaise 19081910. Masson, Paris, pp. 272, 216 pls. Koehler, R. (1926) Description d'un Psammechinus liliaris anormal et fortement dform, provenant de Luc-sur-Mer. Bulletin de l'Institut Ocanographique (Monaco), 472, 110. Laubenfels, M.W. de (1932) The marine and fresh-water sponges of California. Proceedings of the United States National Museum, 81, 1140.

CLATHRIA (MICROCIONA) ACULEOFILA SP. NOV.

Zootaxa 3085 2011 Magnolia Press

53

TERMS OF USE This pdf is provided by Magnolia Press for private/research use. Commercial sale or deposition in a public library or website is prohibited.
Lendenfeld, R. von (1915) The Sponges. 3. Hexactinellida. In: Reports on the Scientific Results of the Expedition to the Eastern Tropical Pacific, in charge of Alexander Agassiz, by the U.S. Fish Commission Steamer 'Albatross', from October, 1904, to March, 1905, Lieut. Commander L.M. Garrett, U.S.N., Commanding, and of other Expeditions of the 'Albatross', 18911899. (29). Memoirs of the Museum of Comparative Zoology at Harvard College, 42, 1396, pls 391109. Lessios, H.A. (2005) Echinoids of the Pacific waters of Panama: Status of knowledge and new records. Revista de Biologia Tropical, 53, 147170. Mortensen, T. (1909) Echinological notes. Videnskabelige Meddelelser fra Dansk Naturhistorisk Forening, 65, 211251. Mortensen, T. (1910) The Echinoidea of the Swedish South Polar Expedition. Wissenscaftliche Ergebnisse der Schwedischen Sdpolar-Expedition 19011903 (Vol. 6). Stockholm. Mothes-de-Moraes, B. (1985) Esponjas Marinhas. In: Manual de Tcnicas para Preparao de Colees Zoolgicas. Sociedade Brasileira de Zoologia, So Paulo, pp. 13. Pinheiro, U.S. & Hajdu, E. (2001) Shallow-water Aplysina Nardo (Aplysinidae, Verongida, Demospongiae) from the So Sebastio Channel and its environs (Tropical southwestern Atlantic), with the description of a new species and a literature review of other Brazilian records of the genus. Revista Brasileira de Zoologica, 18, 143160. Rtzler, K. (1978) Sponges in coral reefs. In: D.R. Stoddart & R E. Johannes (Eds), Research methods. Monographs on oceanographic methodology. UNESCO. Coral Reefs, pp. 5, 299313. Schmidt, O. (1862) Die Spongien des adriatischen Meeres. Leipzig: Wilhelm Engelmann. Schneider, C.L. (2003) Hitchhiking on Pennsylvanian echinoids: Epibionts on Archaeocidaris. Palaios, 18, 435444. Soest, R.W.M. van, Hooper, J.N.A. & Hiemstra, F. (1991) Taxonomy, phylogeny and biogeography of the marine sponge genus Acarnus (Porifera: Poecilosclerida). Beaufortia, 42, 4988. Thiele, J. (1905) Die Kiesel- und Hornschwmme der Sammlung Plate. Supplement 6(Fauna Chiliensis III). Zoologische Jahrbcher, 1905, 407496, pls 427433. Topsent, E. (1913) Spongiaires de l'Expdition Antarctique Nationale Ecossaise. Transactions of the Royal Society of Edinburgh, 49, 579 643, pls IVI. Valenciennes, A. (1846) In: Agassiz, L. & Desor, E. (1846) Catalogue raisonn des familles des genres et des espces de la Classe de Echinodermes. Annales des Sciences Naturelles, Zoologie, 36, 305374. Willenz, Ph., Hajdu, E., Desqueyroux-Fandez, R., Lbo-Hajdu, G. & M. Carvalho, M. (2009) Porifera - Sponges. In: V. Hussermann & G. Frstera (Eds), Marine Benthic Fauna of Chilean Patagonia. Nature in Focus, Santiago de Chile, pp. 93170.

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