CORE Metadata, citation and similar papers at core.ac.uk Provided by Biblioteca Digital da Produção Intelectual da Universidade de São Paulo (BDPI/USP) Universidade de São Paulo Biblioteca Digital da Produção Intelectual - BDPI Centro de Biologia Marinha - CEBIMar Artigos e Materiais de Revistas Científicas - CEBIMar 2015-05 Identifying monophyletic groups within Bugula sensu lato (Bryozoa, Buguloidea) http://www.producao.usp.br/handle/BDPI/49614 Downloaded from: Biblioteca Digital da Produção Intelectual - BDPI, Universidade de São Paulo Zoologica Scripta Identifying monophyletic groups within Bugula sensu lato (Bryozoa, Buguloidea) KARIN H. FEHLAUER-ALE,JUDITH E. WINSTON,KEVIN J. TILBROOK,KARINE B. NASCIMENTO & LEANDRO M. VIEIRA Submitted: 5 December 2014 Fehlauer-Ale, K.H., Winston, J.E., Tilbrook, K.J., Nascimento, K.B. & Vieira, L.M. (2015). Accepted: 8 January 2015 Identifying monophyletic groups within Bugula sensu lato (Bryozoa, Buguloidea). —Zoologica doi:10.1111/zsc.12103 Scripta, 44, 334–347. Species in the genus Bugula are globally distributed. They are most abundant in tropical and temperate shallow waters, but representatives are found in polar regions. Seven species occur in the Arctic and one in the Antarctic and species are represented in continental shelf or greater depths as well. The main characters used to define the genus include bird’s head pedunculate avicularia, erect colonies, embryos brooded in globular ooecia and branches comprising two or more series of zooids. Skeletal morphology has been the primary source of taxonomic information for many calcified bryozoan groups, including the Buguloidea. Several morphological characters, however, have been suggested to be homoplastic at dis- tinct taxonomic levels, in the light of molecular phylogenies. Our purpose was to investigate the phylogenetic interrelationships of the genus Bugula, based on molecular phylogenetics and morphology. A Bayesian molecular phylogeny was constructed using original and previ- ously published sequences of the mitochondrial genes cytochrome c oxidase subunit 1 (COI) and the large ribosomal RNA subunit (16S). Morphological characteristics from scanning electron and light microscopy were used to confirm the clades detected by the molecular phylogeny. Our results suggest that the genus is composed of four clades, for which we pro- vide diagnoses: Bugula sensu stricto (30 species), Bugulina (24 species), Crisularia (23 species) and the monotypic Virididentula gen. n. Ten species could not be assigned to any of those genera, so they remain as genus incertae sedis. Our findings highlight the importance of using molecular phylogenies in association with morphological characters in systematic revi- sions of bryozoan taxa. Corresponding author: Karin H. Fehlauer-Ale, Laboratorio de Bentos, Centro de Estudos do Mar, Universidade Federal do Parana, Avenida Beira-Mar, s/n, Caixa Postal 61, CEP 83255-976, Pontal do Sul, Pontal do Parana, PR, Brazil. E-mail: [email protected] Karin H. Fehlauer-Ale, Laboratorio de Bentos, Centro de Estudos do Mar, Universidade Federal do Parana, Avenida Beira-Mar, s/n, Caixa Postal 61, CEP 83255-976, Pontal do Sul, Pontal do Parana, PR, Brazil and Laboratorio de Sistematica e Evolucß~ao de Bryozoa, Centro de Biologia Marinha, Universidade de S~ao Paulo, Rodovia Manoel Hypolito do Rego, km 131,5 Praia do Cabelo Gordo, CEP 05588-000, S~ao Sebasti~ao, SP, Brazil Judith E. Winston, Smithsonian Marine Station, 701 Seaway Drive, Fort Pierce, FL 34949, USA. E-mail: [email protected] Kevin J. Tilbrook, Oxford University Museum of Natural History, Parks Road, Oxford, OX1 3PW, UK. E-mail: [email protected] Karine B. Nascimento, Laboratorio de Sistematica e Evolucß~ao de Bryozoa, Centro de Biologia Marinha, Universidade de S~ao Paulo, Rodovia Manoel Hypolito do Rego, km 131, 5 Praia do Cabelo Gordo, CEP 05588-000, S~ao Sebasti~ao, SP, Brazil. E-mail: [email protected] Leandro M. Vieira, Departamento de Zoologia, Centro de Ci^encias Biologicas, Universidade Federal de Pernambuco, Av. Prof. Moraes Rego 1235, Cidade Universitaria, CEP 50670-901, Recife, Pernambuco, Brazil and Laboratorio de Sistematica e Evolucß~ao de Bryozoa, Centro de Biologia Marinha, Universidade de S~ao Paulo, Rodovia Manoel Hypolito do Rego, km 131,5 Praia do Cabelo Gordo, CEP 05588-000, S~ao Sebasti~ao, SP, Brazil. E-mail: [email protected] 334 ª 2015 Royal Swedish Academy of Sciences, 44, 3, May 2015, pp 334–347 K. H. Fehlauer-Ale et al. Monophyletic groups within Bugula sensu lato Introduction laid down in the International Code made a decision negat- Bryozoans are suspension feeding, colonial and mostly ses- ing the use of Bugula Oken. Opinion 417 (Hemming 1956) sile aquatic invertebrates, represented by approximately stated that names introduced by Oken (1815) were not 5870 described living (Bock & Gordon 2013) and 15 000 available because Oken’s work was not consistently binomi- fossil species (Gordon 2009). Within the order Cheilosto- nal. To change the long-used name of this speciose and mata, Bugula Oken, 1815 (Buguloidea, Bugulidae) is one of abundant group of bryozoans at this point would have been the most familiar and well-studied genera, represented by disruptive to bryozoan taxonomy. To maintain stability, more than 80 valid species (Bock & Hayward 2014). John Ryland (Ryland 1967) petitioned the Commision of Species in the genus Bugula are globally distributed, Zoological Nomenclature to make the genus name Bugula inhabiting shallow water in tropical to cold water regions Oken available for use. Sertularia neritina Linnaeus, 1758; (Kluge 1962; Hayward 1995; Hayward & Ryland 1998; was subsequently designated the type by the ICZN under Winston & Woollacott 2008; Vieira et al. 2012), with some its plenary powers (Opinion 902); thus, Bugula is an objec- representatives reported from deeper waters of the conti- tive senior synonym of Acamarchis. Since then, the genus nental shelf and beyond (Hayward 1981). Some species are name Bugula has been applied in its broad sense to species known from fouling communities and also may form well- with a variety of morphological character states with established introduced populations (Mackie et al. 2006; respect to branching pattern, spines and ooecia (e.g. Johnson & Woollacott 2012; Karlson & Osman 2012; Hayward & Ryland 1998; Winston & Woollacott 2008; Fehlauer-Ale et al. 2014); others are apparently endemic to Vieira et al. 2012). particular regions (Ryland 1960; Winston & Woollacott The genus has been characterized by bird’s head pedun- 2008; Vieira et al. 2012). culate avicularia, erect colonies and branches comprising The genus Bugula has a long and complicated taxonomic two or more series of boat-shaped zooids (Ryland 1960). history. The name, Bugula, was introduced by Oken (1815) Almost all species have pedunculate bird’s head avicularia, to accommodate three species: Cellularia neritina, Cellularia the type species Bugula neritina (Linnaeus, 1758) being a avicularia and Bugula avicularia (Linnaeus, 1758). Later tax- remarkable exception. The patterns of branch bifurcation onomists used different names or grouped species in differ- in biserial species are usually one of three types described ent ways. Harmer (1923, 1926) synonymized nine generic by Harmer (1923): types 3, 4 or 5 (Fig. 1; see also Harmer names under Bugula: Acamarchis Lamouroux, 1816 (type 1926; Winston & Woollacott 2008; Vieira et al. 2012). species Sertularia neritina Linnaeus, 1758; objective junior The basal and lateral walls of zooids are lightly calcified, symonym of Bugula, see below); Halophila Gray, 1843 (type and most of the frontal wall is membranous, providing flex- species Halophila johnstonae Gray, 1843); Avicularia Gray, ibility to the branches. The majority of species have spines 1848 (junior homonym of spider genus Avicularia Lamarck, on the distal angles of the zooids; in some species, the 1818); Bugulina Gray, 1848 (type species Sertularia avicular- spines are merely pointed extensions of the distal edges of ia Linnaeus, 1758); Crisularia Gray, 1848 (type species zooids, but in others, they are articulated (Winston & Sertularia fastigata Linnaeus, 1758; =Cellularia plumosa Woollacott 2008). The ooecia may be crescentic to globu- Pallas, 1766; see Harmer, 1923); Avicella Van Beneden, lar or helmet shaped (Ramalho et al. 2005; Winston & 1848 (no type species selected); Ornithopora d’Orbigny, Woollacott 2008). 1852 (type species Sertularia avicularia); Ornithoporina Skeletal morphology has been the primary source of taxo- d’Orbigny, 1852 (type species Ornithoporina avicularia nomic information for many calcified bryozoan groups (e.g. d’Orbigny, 1852; =Avicularia flabellata Gray, 1848; see Har- McKinney & Jackson 1989; Jackson & Cheetham 1990; mer 1923); and Dendrobeania Levinsen, 1909 (type species Hayward & Ryland 1998, 1999; Tilbrook 2006; Cheetham Flustra murrayana Johnston, 1847). Two of these genera, et al. 2007; Vieira et al. 2012, 2013, 2014). Several morpho- however, are currently considered distinct genera in Bugu- logical characters, however, have been recently revealed to lidae: Dendrobeania (see Hayward & Ryland 1998) and be homoplastic at distinct taxonomic levels in the light of Halophila (see Winston 2005); although Ornithopora was molecular phylogenies, suggesting that the overall current previously considered as a synonym of Bugula (Harmer bryozoan classification requires revision. Examples include 1923), it is an objective junior synonym of Bugulina (see calcified