NOTES ON GEOGRAPHIC DISTRIBUTION the journal of Check List Check List 13(1): 2028, 4 January 2017 doi: https://doi.org/10.15560/12.1.2028 ISSN 1809-127X ©2017 Check List and Authors Parasites on the spot: the rediscovery of a presumably extinct Apodanthaceae in Sao Paulo state, Brazil Danilo Soares Gissi’* & Milton Groppo’ ‘Universidade de Sao Paulo, Instituto de Biociéncias, Departamento de Botanica, , Rua do Matao 277, CEP 05508-900, Sao Paulo, SP, Brazil *Faculdade de Filosofia, Ciéncias e Letras de Ribeirao Preto (FFCLRP-USP), Departamento de Biologia, CEP 14051-070, Ribeirao Preto, SP, Brazil ° Corresponding author. E-mail: dsgissi@gmail.com Abstract: Apodanthaceae are achlorophyllous herbs holoparasitic on the stems and roots of species of Fabaceae or Salicaceae (Casearia and Xylosma). The family consists of two genera, Apodanthes Poit. and Pilostyles Guill. Although one species of each genus occurs in several states of Brazil, we report a new record of Pilostyles blanchetti (Gardner) R.Br. in the state of Sao Paulo, the first in 50 years. Comments on the distribution of species, hypothetic pollinators, and color images are presented. Key words: Atlantic Rainforest; Fabaceae; Holoparasite; Salicaceae Apodanthaceae is composed of achlorophyllous herba- ceous holoparasites on the stems and roots of members of Fabaceae and Salicaceae (Casearia and Xylosma). BELLOT & RENNER (2014) recognized two genera within Apodantha- ceae: Apodanthes Poit. and Pilostyles Guill. The ten species of the family (nine of them in Pilostyles) are distributed throughout the Americas, Africa, Asia and Australia. The species currently circumscribed in Apodanthaceae have traditionally been included as a tribe (Apodantheae) in Rafflesiaceae (besides Rafflesieae, Cytineae, and Mitraste- moneae); however, recent analyses suggest the recognition of four different families, each one corresponding to the tribes cited above (Rafflesiaceae sensu stricto, Cytinaceae, Mitrastemonaceae, and Apodanthaceae; APG IV 2016), none of them closely related to each other. As a conse- quence, holoparasitism should be interpreted as convergent in these families. Apodanthaceae is now positioned within the Cucurbitales (NICKRENT et al. 2004; FILIPOWICZ & RENNER 2010; APG IV 2016). Only two species occur in Brazil, Apodanthes caseariae Poit., and Pilostyles blanchetti (Gardner) R.Br. (Groppo 2016). Apodanthaceae includes plants with unique char- acteristics, including a vegetative body reduced to a haustorial system, whose parenchymatic and tracheary elements invade the host stem (GROPPO et al. 2007). The main plant body remains hidden within the host tissue, except when flowering. This feature makes it difficult to find the species in the field, and therefore Apodanthaceae is likely underrepresented in herbaria. While collecting plants in the municipality of Buri (Sao Paulo, Brazil), we found a species of Apodanthaceae parasitizing trees of Bauhinia forficata Link (Fabaceae). Host branches were covered with emerging flowers from the parasite, which was identified as Pilostyles blanchetii. Images of the species, as well as comments on taxonomy, biology and geographic distribution are presented. Specimens were collected from of Bauhinia trees grow- ing on a forest border located on private property owned by the family of the first author in the municipality of Buri, in the southwestern region of the state of S4o Paulo (23°45'36.8"S, 048°38'55.3" W and 674 m above sea level; Figure 1). Collections were deposited at ESA (Herbarium, Escola Superior de Agricultura “Luiz de Queiroz”, Universi- dade de Sao Paulo, Piracicaba, Brazil). Material examined: Brazil, Sao Paulo, Buri: Gissi, D.S. 02 (ESA114052); Gissi, D.S. 49 (ESA126572). The plants were identified using the keys and descrip- tions of VATTIMO (1971), and BELLOT & RENNER (2014). Pilostyles differs from Apodanthes for parasitizing Fabaceae and for its pistillate flowers less than 5 mm long, while Apodanthes parasites Salicaceae, with the inner whorl of petals easily deciduous and pistillate flowers more than 5 mm long. VATTIMO (1971) referred 15 species of Pilostyles in Brazil, distinguished by the host and small details of the flowers; however, BELLOT & RENNER (2014) recognized a single species of the genus in this country, P. blanchetii. This species can be distinguished from other Neotropical Pilo- styles by presenting anthers in two whorls, tepals purple to brown sometimes with clearer margins and the middle ones mostly diamond-shaped (BELLOT & RENNER 2014). The host species was identified as Bauhinia forficata Link ssp. pruinosa (Vogel) Fortunato & Wunderlin (Fabaceae) using the keys and descriptions of VAZ & TOZZI (2005). The site where the specimen was collected is located in the municipality of Buri, southwestern Sao Paulo state biodiversity data Gissi & Groppo | The rediscovery of Apodanthaceae in Sao Paulo, Brazil 50°0'0"W 20°0'0"S Phytogeographic Domains ' Atlantic Forest 25°0'0"S Cerrado 50°0'0"W 45°0'0"W 20°0'0"S 25°0'0"S 200 300 45°0'0"W Figure 1. Geographic distribution of Pilostyles blanchetti in the state of Sao Paulo, Brazil. and within in the transition of Cerrado and Atlantic For- est phytogeographical domains, both Brazilian hotspots (MYERS et al. 2000). The property is a farm with intense agricultural land use with some small forest remnants along streams. Nearby in other forest fragments in the same property, additional individuals of infected B. forfi- cata were found on saplings to fully grown trees. Personal field observations indicate that the parasites bloom every year during the summer (December to February). Gissi 02 was collected in 20 February 2011 and bears only fruits or late pistillate flowers. A new record was made in 1 January 2014 (Gissi 49), with staminate flowers (Figure 2). Pilostyles blanchetii occurs in several Brazilian states (Groppo 2016), including Minas Gerais and Parana, both bordering Sao Paulo. It occurs in other countries in south America, including Colombia, Venezuela, Guyana, Argentina and Uruguay, as well as in Central America and the Caribbean, including Jamaica, the Cayman Islands, Costa Rica, and Panama (BELLOT & RENNER 2014). Until the discovery of this population in Buri, the only known record of Apodanthaceae in Sao Paulo dates from 1961 (Araraquara, 28 January 1961, M. Kuhlman s.n., IPA 12303), and since then, there are no literature or herbarium records of the family in the state. The species could be considered presumably extirpated in the state of Sao Paulo according to the criteria used for the list of endangered Check List | www.biotaxa.org/cl species in the state (SOUZA et al. 2007), because it has not been collected or observed in the wild for over 50 years. Therefore, this new record sheds light to the conservation of this species, which now can be considered Endangered (EN) in the state due to a restricted distribution not within the limits of a conservation area; it should be included in the official list of endangered species (SMA 2016). This record also shows the importance of search effort, even in areas that are thought to be satisfactorily collected, or even over-collected, such as this state. The absence of regular collections of Pilostyles (or any other species of Apodanthaceae) from Sao Paulo can be a result of an insufficient sampling, given the invisibility of these parasites when not in flower. It is possible that P. blanchetii is more common in Sao Paulo than what herbarium records suggest. On the other hand, collections of P. blanchetti are scarce from localities from southernmost latitudes, with some exceptions from Parana and Santa Catarina states. Perhaps a latitudinal gradient (colder climates in the south) plays a role in the distribution of the species. Our field observations revealed the flowering phenology of Pilostyles follows the seasonal cycle of host plant senescence and growth. Bauhinia forficata loses its leaves during the dry season and starts producing new branches when the rainy season comes (around December); at that Volume 13 | Issue1 | Article 2028 Gissi & Groppo | The rediscovery of Apodanthaceae in Sao Paulo, Brazil Figure 2. Staminate flowers of Pilostyles blanchetti on the stems of the host Bauhinia forficata. Photo by Danilo Soares Gissi. ve Figure 3. Beetles visiting the flowers of Pilostyles, perhaps nourishing of the nectar produced on the nectaries. Photo by Danilo Soares Gissi. © Check List | www.biotaxa.org/cl 3 Volume 13 | Issue 1 | Article 2028 Gissi & Groppo | The rediscovery of Apodanthaceae in Sao Paulo, Brazil point, the parasite’s flowers emerge. We observed ants and beetles visiting the flowers (Figure 3). BELLOT & RENNER (2013) stated the small sessile flowers offer nectar in minute quantities from a shallow nectary cushion at their bases. This nectar may be collected by the ants and beetles, which may be the effective pollinators. However, further studies are necessary to test this hypothesis. ACKNOWLEDGEMENTS We are grateful to Dr. Vinicius Castro Souza for all the support to this study at Herbarium ESA. We also thank Ana Faraco for the distribution map and Dr. Chris Randle for the English review. MG thanks FAPESP (grants #2006/03170-0, #2011/10446-0, #2015/09458-6) and CNPq (grant #309994/2012-8) for financial support. LITERATURE CITED APG IV. 2016. An update of the Angiosperm Phylogeny Group classification for the orders and families of flowering plants: APG IV. Botanical Journal of the Linnean Society 181: 1-20 doi: 10.1111/bo0j.12385 BELLOT, S. & S.S. RENNER. 2013. Pollination and mating systems of Apodanthaceae and the distribution of reproductive traits in parasitic angiosperms. American Journal of Botany 100: 1083- 1094. doi: 10.3732/ajb.1200627 BELLOT, S. & S.S. RENNER. 2014. The systematic of the worldwide endoparasite family Apodanthaceae (Cucurbitales), with a key, a map, and color photos of most species. Phytokeys 36: 41-57. doi: 10.3897/phytokeys.36.7385 FILIPOWICZ, N. & S.S. RENNER. 2010. The worldwide holoparasitic Apodanthaceae confidently placed in the Cucurbitales by nuclear and mitochondrial gene trees. BMC Evolutionary Biology 10: 219. doi: 10.1186/1471-2148-10-219 GRoppo, M., M.M. AMARAL & G.T. CECCANTINI. 2007. Flora da Serra do Cipé, Minas Gerais: Apodanthaceae. Boletim de Botanica da © Check List | www.biotaxa.org/cl Universidade de Sao Paulo 25: 87-92. doi: 10.11606/issn.2316- 9052.v25i1p87-94 Groppo, M. 2016. Apodanthaceae in Flora do Brasil 2020 em con- stru¢do. Jardim Botanico do Rio de Janeiro. Accessed at http:// floradobrasil.jbrj.gov.br/reflora/floradobrasil/FB49, 18 January 2016. MYERS, N., R.A. MITTERMEIER, C.G. MITERMEIER, G.A. FONSECA & J. KENT. 2000. Biodiversity hotspots for conservation priorities. Nature 403: 853-858. doi: 10.1038/35002501 NICKRENT, D.L., A. BLARER, Y.-L. Qiu, R. VIDAL-RUSSELL & EE. ANDERSON. 2004. Phylogenetic inference in Rafflesiales: The influence of rate heterogeneity and horizontal gene transfer. BMC Evolutionary Biology 4: 40. doi: 10.1186/1471-2148-4-40 SMA (SECRETARIA DO ESTADO DO MEIO AMBIENTE DE SAO PAULO). 2016. Lista oficial das espécies da flora do Estado de Sao Paulo ameacadas de extincdo. Resolugdo n° 57, de 5 de Junho de 2016. Accessed at http://www.ambiente.sp.gov.br/wp-content/ uploads/2016/06/pg_0073.pdf, 12 November 2016. SOUZA, V. C., M.C.H. MAMEDE, I. CORDEIRO, J. PRADO, F. BARROS, M.G.L.W. WANDERLEY, P.Y. KAGEYAMA, G. CECCANTINI & J.G. RANDO. 2007. Critérios utilizados na elaboracdo da Lista de Espé- cies da Flora Ameagadas de Extin¢do no estado de Sao Paulo; pp. 15-20, in: M.C.H. Mamede, V.C. Souza, J. Prado, FE Barros, M.G.L. Wanderley and J.G. Rando (org.). Livro Vermelho das espécies vegetais ameacadas do estado de Sao Paulo. Vol. 1.1 ed. Sao Paulo: Instituto de Botanica. Vaz, A.M.S.F. & A.M.G.A. TOZZI. 2005. Sinopse de Bauhinia sect. Pauletia (Cav.) DC. (Leguminosae: Caesalpinioideae: Cercideae) no Brasil. Brazilian Journal of Botany 28(3): 477-491. doi: 10.1590/ S0100-84042005000300006 VATTIMO, I. 1971. Contribuigaéo ao conhecimento da tribo Apod- antheae R. Br. parte 1 — conspecto das espécies (Rafflesiaceae). Rodriguésia 26(38): 37-62. Author contributions: DG collected the specimens, DG and MG wrote the text, and identified the material. Received: 4 May 2016 Accepted: 18 November 2016 Academic editor: Juliana de Paula-Souza Volume 13 | Issue1 | Article 2028