bs_bs_banner Zoological Journal of the Linnean Society, 2015, 173, 787–817. With 12 figures Integrative taxonomy of calcareous sponges (subclass Calcinea) from the Peruvian coast: morphology, molecules, and biogeography FERNANDA AZEVEDO1, BÁSLAVI CÓNDOR-LUJÁN1, PHILIPPE WILLENZ2, EDUARDO HAJDU3, YURI HOOKER4 and MICHELLE KLAUTAU1* 1Universidade Federal do Rio de Janeiro, Instituto de Biologia, Departamento de Zoologia, Avenida Carlos Chagas Filho, 373, 21941-902, Rio de Janeiro, RJ, Brazil 2Royal Belgian Institute of Natural Sciences, Taxonomy and Phylogeny, Rue Vautier 29, B – 1000, Bruxelles, Belgium 3Universidade Federal do Rio de Janeiro, Museu Nacional, Departamento de Invertebrados, Quinta da Boa Vista, S/N, 20940-040, Rio de Janeiro, RJ, Brazil 4Universidad Peruana Cayetano Heredia, Laboratorio de Biología Marina, Lima, Avenida Honorio Delgado, 430, Urbanización Ingeniería, San Martín de Porres, Lima, Perú Received 6 May 2014; revised 2 September 2014; accepted for publication 7 September 2014 Understanding of evolution and systematics of Calcarea (Porifera) have not yet met a corresponding increase in the knowledge of diversity and distribution of these sponges in several parts of the world. Peru is an emblematic example of this lack of taxonomic knowledge, as only three shallow-water species of sponges have hitherto been reported from its 3000 km coast. With the aim of studying sponges of Peru, an integrative taxonomy approach (morphology, molecules, and biogeography) was used in order to achieve sound species identifications. The first findings of Peruvian calcareous sponges are presented here. Eight species are described in the subclass Calcinea, of which five are new to science. The retrieved biogeographical patterns are either locally endemic, widespread, or discontinuous over large areas. Clathrina antofagastensis was previously known from Chile, while C. aurea and Ernstia tetractina had been reported from the Atlantic (Brazil), and thus represent the first genetically confirmed tropical amphi- American distributions of species not yet found on both sides of the Isthmus of Panama. Our results reveal a richer Tropical East Pacific sponge fauna than the Warm Temperate South-Eastern Pacific one. © 2015 The Linnean Society of London, Zoological Journal of the Linnean Society, 2015, 173, 787–817. doi: 10.1111/zoj.12213 ADDITIONAL KEYWORDS: internal transcribed spacer – marine biodiversity – molecular systematics – Pacific Ocean – Peru − Porifera. INTRODUCTION et al., 2010). This is especially so when organisms have a limited number of easily assessable characters or Integrative taxonomy involves the use of multiple and possess markedly changing morphologies, as is the case complementary disciplines (morphology, and molecu- for sponges (Dohrmann et al., 2008, 2011, 2012; Rossi lar or chemical taxonomy) to evaluate the statuses of et al., 2011; Cárdenas, Pérez & Boury-Esnault, 2012; taxa (Dayrat et al., 2008; Schlick-Steiner et al., 2010). Gazave et al., 2012; Voigt, Wülfing & Wörheide, 2012; Today, it appears to be the best approach for produc- Klautau et al., 2013). ing reliable systematics and phylogenetic studies, and In the molecular era, the first studies on calcare- achieve a more natural system of classification (Padial ous sponges performed under an integrative perspec- tive aimed to verify the taxonomic status of allegedly cosmopolitan species (Solé-Cava et al., 1991; Klautau, *Corresponding author. E-mail: [email protected] Solé-Cava & Borojevic, 1994; Valderrama et al., 2009). © 2015 The Linnean Society of London, Zoological Journal of the Linnean Society, 2015, 173, 787–817 787 788 F. AZEVEDO ET AL. However, phylogenetic relationships soon started to Tarazona & Valle, 1998; Tarazona et al., 2003; Paredes, become investigated (Manuel et al., 2003, 2004; Cardoso & Tarazona, 2004; Chavez et al., 2008). Rossi et al., 2011; Voigt et al., 2012). In a recent Traditionally, the most investigated marine fauna com- study, species and genera belonging to the order prises groups of animals with economic value, and this Clathrinida (subclass Calcinea) were re-evaluated based is also the case in Peru (Tarazona et al., 2003). One on morphological and molecular data, which resulted exception relates to the Polychaeta (Tarazona, 1974), in the genera Ascandra and Clathrina being rede- which is one of the taxonomically best known benthic fined, and the erection of four new genera (i.e. Arthuria, animals in Peru (Costello et al., 2010; Miloslavich et al., Borojevia, Brattegardia, and Ernstia; Klautau et al., 2011). By contrast, sponges are one of the least studied 2013). In addition, some species of Guancha, with groups of animals in Peru, despite their numerous func- triactines and no tetractines, were transferred to tional and structural roles in marine ecosystems (e.g. Clathrina, in spite of their possession of a peduncle provision of microhabitat, release of chemicals, en- (Klautau et al., 2013). An integrative taxonomy ap- hancement of primary production; Wulff, 2001; Cerrano proach was also used to strengthen the description of et al., 2006; Bell, 2008; de Goeij et al., 2013). With more four Clathrina species from the Adriatic Sea (Imešek than 3000 km of shoreline, Peru still represents a large et al., 2013). Somewhat contradictorily, recent ad- hiatus in the South American sponge biodiversity in- vances in understanding the evolution and systemat- ventory, with only 14 species reported; five Demospongiae ics of Calcarea by applying molecular tools have not from shallow waters (Hyatt, 1877; van Soest, Hooper yet resulted in a corresponding increase in the knowl- & Hiemstra, 1991; Desqueyroux-Faúndez & van Soest, edge of diversity and distribution of calcarean species 1996; Aguirre et al., 2011), and nine Hexactinellida, in several parts of the world. Peru represents a clear all from the deep sea (von Lendenfeld, 1915). No Calcarea example of this lack of taxonomic information, not just have ever been reported from the Peruvian coast. for Calcarea, but also for the entire phylum Porifera, The aim of this paper was to reduce this lack of with only three shallow-water species described from knowledge, by determining the species composition and its coast. geographical range of calcinean calcareous sponges (sub- In response to future needs and challenges in study- class Calcinea) from Peru’s shallow waters using an ing marine biodiversity, several international efforts integrative taxonomic approach. This goal was pursued (e.g. Global Taxonomy Initiative) have started with the by an international cooperation set up in 2007 amongst purpose of strategically inventorying particular under- Belgium (RBINS), Brazil (MNRJ), Peru (UPCH), estimated taxa, filling the gaps in regions considered and Switzerland (MHNG), in the form of two re- to be poorly known, and developing new taxonomic ex- search projects: ESponjas del PERú and Capacitação pertise in countries where it is weak or non-existent para Pesquisa em Taxonomia, Filogenia e Biogeografia (Costello et al., 2010; van Soest et al., 2012; Hooper et al., de Poríferos da América do Sul. The first findings of 2013). The present study is the result of one of these Peruvian calcareous sponges are presented here. collaborations. The Peruvian coast (south-east Pacific) holds one of MATERIAL AND METHODS the four major upwelling systems in the world, the Humboldt Current System, which is characterized by SAMPLING PROCEDURE its moderate to extremely high primary productivity, A total of 43 specimens of calcareous sponges (sub- and its particularly productive fisheries (Bakun & class Calcinea) was collected in 28 of the 90 localities Weeks, 2008; Chavez & Messié, 2009). According to the investigated along the Peruvian coast, from Tumbes Marine Ecoregions of the World system (Spalding et al., (3°S) to Tacna (18°S) (Fig. 1, Table 1). Several inves- 2007), the Peruvian marine ecosystem stretches over tigated localities are within protected areas (i.e. Paracas two biogeographical provinces, the southern part of the National Reserve; Guano Islands and Capes Nation- Tropical East Pacific (TEP), which extends from 3 to al Reserve System; Tumbes Mangroves National Sanc- 6°S, and the northern sector of the Warm Temperate tuary) or identified as priorities for nature conservation South-eastern Pacific (WTSP), which extends from 6 (Foca Island; El Ñuro; Punta Sal). Consequently, this to 42°S. However, there are no sharp boundaries study received the support of the Protected Natural between biogeographical provinces and at a finer reso- Areas National Service (SERNANP) to access several lution; adjacent biotas may share a transition zone with sites and in obtaining permits for scientific studies. considerable overlap (Spalding et al., 2007). In addi- Samples were collected between 2007 and 2009 at tion, the Peruvian ecosystem is subject to high depths varying from the intertidal zone to 30 m by scuba interannual environmental variability caused by the diving. Sponges were photographed in situ, along with El Niño Southern Oscillation (ENSO), which causes a 5-cm scale bar and an inventory number. Depth and temporary changes in the composition and abun- water temperature were recorded by photographing dance of biological communities (Paredes et al., 1998; depth gauges at the time of each sampling. © 2015 The Linnean Society of London, Zoological Journal of the Linnean Society, 2015, 173, 787–817 CALCINEAN SPONGES FROM PERU 789 Figure 1. Location of Peru and its seven main regions along the coast. SPECIMEN PREPARATION