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An Updated List of the Plants Associated with Plant-Parasitic Aphelenchoides (Nematoda: Aphelenchoididae) and Its Implications for Plant-Parasitism Within This Genus

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An Updated List of the Plants Associated with Plant-Parasitic Aphelenchoides (Nematoda: Aphelenchoididae) and Its Implications for Plant-Parasitism Within This Genus Zootaxa 4013 (2): 207–224 ISSN 1175-5326 (print edition) www.mapress.com/zootaxa/ Article ZOOTAXA Copyright © 2015 Magnolia Press ISSN 1175-5334 (online edition) http://dx.doi.org/10.11646/zootaxa.4013.2.3 http://zoobank.org/urn:lsid:zoobank.org:pub:78D07882-590D-44D6-A765-23BE9A6999ED An updated list of the plants associated with plant-parasitic Aphelenchoides (Nematoda: Aphelenchoididae) and its implications for plant-parasitism within this genus ALCIDES SÁNCHEZ-MONGE1,2, LORENA FLORES3, LUIS SALAZAR3, SUE HOCKLAND4 & WIM BERT1 1 Ghent University, Department of Biology, Nematology Research Unit, Ledeganckstraat 35, B-9000 Ghent, Belgium. 2 Universidad de Costa Rica, Escuela de Estudios Generales, 2060, Costa Rica 3 Universidad de Costa Rica, Laboratorio de Nematología, Centro de Investigación en Protección de Cultivos (CIPROC), 2060, Costa Rica 4 Independent Plant Nematology Consultant, Harrogate, North Yorkshire, England, UK. www.plantparasiticnematodes.com Abstract Few Aphelenchoides spp. are facultative plant-parasites (foliar and bulb nematodes); three of them are well known in ag- ricultural systems, namely Aphelenchoides besseyi, A. fragariae and A. ritzemabosi. Ten other plant-parasitic species, A. arachidis, A. bicaudatus, A. blastophthorus, A. dalianensis, A. ensete, A. nechaleos, A. paranechaleos, A. saprophilus, A. sphaerocephalus and A. subtenuis, have been reported from a limited number of plant species. We compiled a new data- base of the associated plants for these thirteen species, a comprehensive list that includes 1104 reports from 126 botanical families. A. besseyi, A. fragariae and A. ritzemabosi represent 94% of the reports, circa 83% and 16% of the total reports correspond to flowering plants and ferns, respectively, with three records on conifers and two from other botanical groups also listed. Most plant-parasitic Aphelenchoides show a remarkably broad diversity of associated plants. Most species ap- pear to have no specific plant hosts (i.e. are generalists). The broad host ranges of these species and absence of more inti- mate interactions with the associated plants highlights the primitive mode of parasitism in Aphelenchoides species, making them potentially interesting in the study of the evolution of plant parasitism. Even though the compiled list of as- sociated plants is long, it probably only represents a fraction of the potential range. The complete compilation has been uploaded to http://nematodes.myspecies.info/. Key words: crops, evolution, ferns, flowering plants, foliar nematodes, phylogeny Resumen: Pocas especies de Aphelenchoides son parásitos facultativos de plantas (nematodos foliares y del bulbo), tres de ellas: Aph- elenchoides besseyi, A. fragariae y A. ritzemabosi son muy importantes en sistemas agrícolas. Otras diez especies; A. arachidis, A. bicaudatus, A. blastophthorus, A. dalianensis, A. ensete, A. nechaleos, A. paranechaleos, A. saprophilus, A. sphaerocephalus y A. subtenuis, han sido informadas en un número reducido de especies de plantas. Se compiló una nueva base de datos de plantas asociadas a las trece especies, e incluye 1104 registros de 126 familias botánicas. A. besseyi, A. fragariae and A. ritzemabosi representan el 94% de los registros, cerca del 83% y 16% del total de los mismos correspon- den a plantas con flores y helechos, respectivamente, tres registros en coníferas y dos en otros grupos botánicos fueron también enlistados. La mayoría de los Aphelenchoides fitófagos muestran una amplia diversidad de plantas asociadas. La mayoría de las especies no tienen hospederos específicos (generalistas). Los amplios rangos de estas especies y la ausencia de relaciones más íntimas con sus plantas asociadas destacan el modo primitivo de parasitismo de Aphelenchoides, haci- éndolos potencialmente interesantes en el estudio de la evolución del fitoparasitismo. A pesar de la amplitud de la lista compilada, es probable que solo represente una parte de la potencial diversidad de asociaciones. Este listado está di- sponible en http://nematodes.myspecies.info/. Palabras clave: cultivos, evolución, filogenia, helechos, nematodos foliares, plantas con flores Accepted by P. Mullin: 18 Aug. 2015; published: 8 Sept. 2015 207 Introduction Around 4000 species of nematodes have been described as plant-parasitic i.e., those that can feed on plant tissue (Decraemer & Hunt 2013) and some of them have a serious economic impact on crops. Plant-parasitism has arisen independently several times in Nematoda: in Trichodoridae Thorne, 1935, Longidoridae Thorne, 1935 (Meyl, 1961) and in the order Panagrolaimida Hodda, 2007 specifically in the suborders Tylenchina Chitwood, 1950 and Aphelenchina Geraert, 1966 (sensu Hodda 2011). However, the position of “tylenchs” (=Tylenchina Chitwood, 1950 sensu Hodda 2011 or Tylenchida Thorne, 1949 sensu Siddiqi 1980) versus “aphelenchs” (=Aphelenchina Geraert, 1966 sensu Hodda 2011 or Aphelenchida Siddiqi, 1980) is controversial, and thus the point at which plant- parasitism arose remains hypothetical. Phylogenetic hypotheses based on nuclear SSU rDNA (Bert et al. 2008, van Megen et al. 2009) suggested that Aphelenchoidea Fuchs, 1937 (Thorne, 1949) is a sister to tylenchs while Aphelenchoidoidea Skarbilovich, 1947 (Siddiqi, 1980) have an independent origin. However, a recent phylogenetic analysis based on mitochondrial genomes (Kim et al. 2015) indicate a monophyletic status for aphelenchs, independent from the tylenchs. The superfamily Aphelenchoidoidea (sensu Hodda 2011) comprises 7 families and includes mainly fungal- feeding species, insect parasites, predators but also some damaging plant pathogens in the genera Bursaphelenchus Fuchs, 1937 and Aphelenchoides Fischer, 1894 (Nickle, 1970). Although most species of Aphelenchoides are fungivores or predators (Kanzaki & Giblin-Davis 2012), thirteen species have been reported as plant-parasitic in a wide variety of plants. Special attention has been paid to three predominantly plant-parasitic species within the “foliar and bulb nematodes” (Aphelenchoididae Skarbilovich, 1947 (Paramonov, 1953)) namely Aphelenchoides besseyi Christie, 1942, A. fragariae (Ritzema Bos, 1890) Christie, 1932 and A. ritzemabosi (Schwartz, 1911) Steiner & Buhrer, 1932, that have been extensively studied due to their economic impact and yield losses. Notably, A. besseyi was listed within the top ten plant-parasitic nematodes (PPN) according to its scientific and economic importance (Jones et al. 2013) while A. fragariae and A. ritzemabosi are the most common parasitic nematodes on aerial parts of ornamental plants (McCuiston et al. 2007). In addition to the plant-parasitic Aphelenchoides, a few mycophagous species have gained a quarantine status, i.e. A. agarici Seth & Sharma, 1986, A. composticola Franklin, 1957, A. sacchari Hooper, 1958 and A. swarupi Seth & Sharma, 1986 (Singh et al. 2013). The number of plants associated with Aphelenchoides has increased in recent years and this genus shows a broad host range compared to other PPN, with over 700 species from 85 botanical families being reported (Kohl 2008, 2011). However, Koch's Postulates i.e., the four criteria to identify the causal agent of a disease, have not been fulfilled in most cases and the term “associated host” is preferred to denote a possible parasitic relationship (Kohl 2011). The high number of nominal species of Aphelenchoides (circa 200), of which the majority have not been described sufficiently to enable reliable identification, has led to notorious determination problems. Moreover, in addition to a large intra-specific variation and minimal inter-specific relationships, most taxa are not yet associated with discriminating molecular data, muddling the taxonomic work on this genus (Zhao 2006). By the beginning of 2015, the databases of the International Nucleotide Sequence Database Collaboration (INSDC) had more than 600 nucleotide sequences (mostly mitochondrial DNA and RNA subunits) that belonged to Aphelenchoides samples, but for only 17 named species while the number of taxa tagged only as “Aphelenchoides sp.” was 34. Some of these taxa are represented only by a single sequence. Based on the number of their hosts, parasites are either classified as specialists or generalists (Koprivnikar & Randhawa 2013). Both feeding strategies are probably present in the genus Aphelenchoides as some species have been reported only on one or two related plant species while others have been reported on plant groups not closely related. In this paper, we present a compiled list of the plant species associated with plant-parasitic Aphelenchoides to appraise the potential/overlapping ranges that a single or a specific combination of species could have. Based on the compiled data of Aphelenchoides records and relationships, respectively plotted on a plant and Aphelenchoides spp. phylogenetic framework, we also provide some insights on plant-parasitism of this genus. Materials and methods Data on Aphelenchoides species and their associated plants were compiled from the available literature (papers, bulletins, theses, datasheets), on-line publications (Kohl 2011) and the University of California Davis on-line 208 · Zootaxa 4013 (2) © 2015 Magnolia Press SÁNCHEZ-MONGE ET AL. database (http://plpnemweb.ucdavis.edu). Reports considered by the source as “Doubtful” or “Mistake” were excluded from the list as well as those that originated from soil samples. When the nematodes were found in roots, only those plants explicitly described as hosts or associated hosts were listed to avoid
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