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A NEW SPECIES OF (MYXOMYCETES) FROM CHIHUAHUA, MEXICO

G. MORENO 1, M. LIZÁRRAGA 2, I. FLORES-ROMERO 2 & F. JIMÉNEZ-VEGA 2

1 Dpto. Ciencias de la Vida (Botánica), Edificio de Biología, Univ. Alcalá, 28805 Madrid, España [email protected] 2 Dpto. Ciencias Químico Biológicas, Instituto de Ciencias Biomédicas, Univ. Autónoma de Ciudad Juárez, Anillo Envolvente Pronaf y Estocolmo s/n, Ciudad Juárez, Chihuahua 32300, México [email protected]

Summary. Moreno, G., M. LIZÁRRAGA, I. FLORES-ROMERO & F. JIMÉNEZ-VEGA (2018). A new species of Physarum (Myxomycetes) from Chihuahua, Mexico. Bol. Soc. Micol. Madrid 42: 21–26. Physarum pauciverrucosum, a new species which has profusely fructified on barks from Populus deltoides and Ulmus pumila in moist chamber, is described. Samples come from Juárez city urban area. Photographs of its most relevant macro and microscopic features are provided.

Key words: , myxobiota, , slime moulds, .

Resumen. MORENO, G., M. LIZÁRRAGA, I. FLORES-ROMERO & F. JIMÉNEZ-VEGA (2018). Una nueva especie de Physarum (Myxomycetes) de Chihuahua, Mexico. Bol. Soc. Micol. Madrid 42: 21–26. Se describe Physarum pauciverrucosum, una nueva especie que ha fructificado abundantemente sobre cortezas de Populus deltoides y Ulmus pumila en cámara húmeda. Las muestras proceden del área urbana de Ciudad Juárez. Se aportan fotografías de sus características macro y microscópicas más relevantes.

Palabras clave: Amoebozoa, hongos mucilaginosos, mixobiota, Physarales, taxonomía.

INTRODUCTION ornamentation (LADO, 2005–2018). The genus Physarum is located in the family In a study about bark-dweller Myxomycetes Chevall., inside the order Physarales T. Macbr. from urban zones conducted by FLORES- According to MARTIN & ALEXOPOULOS ROMERO (2017), abundant material fructifying (1969), this order is characterized by the on Ulmus pumila L. and Populus deltoides presence of lime, usually abundant on some Bartram ex Marshall barks, has been collected. parts, and frequently on the entire fructification, Is proposed a species belonging to the genus spores black, deep purplish or violaceus, brown Physarum Pers., which does not fit properly in any in mass, deep purplish brown to violaceus by of the species currently recognized for this genus, transmitted light, and assimilative stage of due to its morphological characteristics and spore phaneroplasmodium. Inside this order, several

Bol. Soc. Micol. Madrid 42. 2018 21 G. MORENO, M. LIZÁRRAGA, I. FLORES-ROMERO & F. JIMÉNEZ-VEGA genera, in which lime presence is not conspicuous, MATERIALS AND METHODS are included, like Protophysarum M. Blackw. & Alexop. Despite of sharing characteristics All material (32 samples) was obtained from with Rostaf., the latter genus moist chamber cultures, between the years 2015 was included in the family Physaraceae by and 2018. For the microscopic study, permanent BLACKWELL & ALEXOPOULOS (1975), who slides with Hoyer media were prepared according considered it a primitive form of Physarales. to MORENO & MANJÓN (2010). Photographs Later, molecular studies carried out by FIORE- were taken with Nikon SMZ800 stereoscope and DONNO & al. (2008), concluded the genus is Nikon eclipse 80i microscope, equipped with a better located within the order Physarales, in DS-5M automatic photographic system. SEM a clade that is independent from micrographs were taken with a Zeiss DSM-950 Rostaf. ex Cooke and Physarales Rostaf. ex microscope, samples were previously prepared Cooke. CASTILLO & al. (1998), proposed the with critical point technique (MORENO & al., new family Protophysaraceae A. Castillo, Illana 2017). Samples are deposited in the herbarium & G. Moreno for this taxon, inside the order AH (Universidad de Alcalá) and in the herbarium Physarales. UACJ (Departamento de Ciencias Químico Something similar happened with Licea Biológicas of the Universidad Autónoma de fimicola Dearn. & Bisby, initially proposed as a Ciudad Juárez). species within the order Jahn, and later, due to its blackish spores, located in the order DESCRIPTION Physarales and newly created genus Kelleromyxa Eliasson (ELIASSON & al., 1991). Molecular Physarum pauciverrucosum G. Moreno, M. studies performed by ERASTOVA & al. (2013) Lizárraga & Flores-Romero, sp. nov. Figs. 1–11 confirmed its permanence in the order Physarales, and proposed the new family Kelleromyxaceae D. MycoBank MB 826868 Erastova, M. Okun, A.M. Fiore-Donno, Novosh. & Schnittler. Etymology: pauciverrucosum from latin pauci = Other organisms that have been located few and verrucosum = warts. The name is due in the class Caval.-Sm. based to scattered warts on spore surface. on molecular studies belong to the genus Hyperamoeba Alexeieff. FIORE-DONNO & Typus. Mexico: Chihuahua, Juárez City, federal al. (2010) indicate the genus was established public park El Chamizal, on Populus deltoides to accommodate an aerobic exhibiting bark, leg. I. Flores-Romero & M. Lizárraga, three life stages, amoeba, flagellate, and cyst. placed into cultivation 16–VIII–2016, sporocarps However, the genus is invalid and its species obtained 7–IX–2016, UACJ 3058 in AH 49089 occupy different positions inside this class, as Holotypus. for example Physarum flagellatum (Alexeieff) Fiore-Donno, Kamono & Caval.-Sm. Additional specimens examined. Mexico: Chihuahua, Juárez According to LADO (1995–2018) the genus City, Parque Público Federal El Chamizal, on Populus Physarum consists of 145 species worldwide. In deltoides bark, leg. I. Flores-Romero & M. Lizárraga, placed Mexico 60 taxa are recognized (58 species and into cultivation 2–IX–2015, sporocarps obtained 20–X–2015, 2 varieties) MORENO & al. (2007); LADO & UACJ 2914. Ibidem, placed into cultivation 16–VIII–2016, WRIGLEY DE BASANTA (2008); ESTRADA- sporocarps obtained 20–IX–2016, UACJ 3271. Ibidem, TORRES & al. (2009); LIZÁRRAGA & al. sporocarps obtained 27–IX–2016, UACJ 3025. Ibidem, (2008, 2015 and 2016). Only 17 species have placed into cultivation 18–X–2016, sporocarps obtained been recorded for the Chihuahua state MORENO 14–XI–2016, UACJ 3070 in AH 49090. Ibidem, sporocarps & al. (2007); SALAZAR-MARQUEZ & al. obtained 2–XII–2016, UACJ 3114. Ibidem, sporocarps (2014); LIZÁRRAGA & al. (2015). obtained 12–XII–2016, UACJ 2858. Ibidem, placed into

22 Bol. Soc. Micol. Madrid 42. 2018 A NEW SPECIES OF PHYSARUM (MYXOMYCETES) FROM CHIHUAHUA, MEXICO

Figs. 1–11.– Physarum pauciverrucosum G. Moreno, M. Lizárraga & Flores-Romero, AH 49089 Holotype. 1–3. Variation of sporocars with multi-lobulated and gyrose sporothecae. 4. Stipe. 5. Whitish capillitium. 6–7. Detail of capillitium under LM. 8. Spores under LM. 9–11. Detail of spore ornamentation under SEM.

Scale bars: 1, 3–4 = 1 mm, 2, 5 = 0.5 mm, 6–7 = 50 µm, 8 = 10 µm, 9–11 = 2 µm

Bol. Soc. Micol. Madrid 42. 2018 23 G. MORENO, M. LIZÁRRAGA, I. FLORES-ROMERO & F. JIMÉNEZ-VEGA

cultivation 3–VII–2017, sporocarps obtained 18–VIII–2017, 4). Pseudocolumella usually absent, occasionally UACJ 3312. Institutos de: Ingeniería y Tecnología (IIT) can develop a whitish, subglobose to somewhat and Arquitectura, Diseño y Arte (IADA), on Ulmus pumila elongated, calcium carbonate pseudocolumella bark, leg. I. Flores-Romero & M. Lizárraga, placed into like Physarum robustum (Lister) Nann.-Bremek. cultivation 12–X–2015, sporocarps obtained 10–XI–2015, Hypothallus brownish, barely conspicuous. UACJ 3056 in AH 49112. Ibidem, placed into cultivation Plasmodium not observed. Capillitium abundant, 19–VIII–2016, sporocarps obtained 3–IX–2016, UACJ filamentous, branched, reticulated, with many 3102. Ibidem, sporocarps obtained 8–IX–2016, UACJ calcareous nodules, elongated, straight to 3252. Ibidem, sporocarps obtained 9–IX–2016, UACJ 3253 fusiform (Figs. 5–7). Spores 10–11.5 (–12) µm in AH 49091 and UACJ 3291. Ibidem, sporocarps obtained diam., globose to subglobose, blackish brown 20–IX–2016, UACJ 3270 in AH 49092. Ibidem, sporocarps in mass, dark violaceous brown under de LM, obtained 23–IX–2016, UACJ 3092. Ibidem, sporocarps with a paler area and a characteristic spore obtained 29–IX–2016, UACJ 3099 in AH 49092. Ibidem, ornamentation, formed by scarce and thick sporocarps obtained 4–X–2016, UACJ 3106. Ibidem, warts up to 1 µm diam., very scattered on the sporocarps obtained 5–X–2016, UACJ 3116 and UACJ spore surface, which is smooth (Fig. 8). Under 3117, Ibidem, sporocarps obtained 10–X–2016, UACJ SEM, spore ornamentation is formed by scarce 3125. Ibidem, sporocarps obtained 12–X–2016, UACJ and thick warts or bacula which are isolated or 3128. Ibidem, sporocarps obtained 14–X–2016, UACJ 3165 forming small groups (Figs. 9–11). and UACJ 3176. Ibidem, sporocarps obtained 20–X–2016, UACJ 3267. Ibidem, sporocarps obtained 24–X–2016, Observations: Physarum pauciverrucosum is UACJ 3275. Ibidem, placed into cultivation 3–VIII–2017, characterized by its usually stipitate fructifications, sporocarps obtained 18–VIII–2017, UACJ 3316. Ibidem, isolated to gathered, due to joined sporothecae sporocarps obtained 8–IX–2017, UACJ 3315. Instituto de presenting a multi-lobulated morphology, gyrose Ciencias Biomédicas, on Ulmus pumila bark, leg. I. Flores- confluent, capillitium with abundant, elongate Romero & M. Lizárraga, placed into cultivation 15–VIII– and straight to fusiform calcareous nodules; and 2017, sporocarps obtained 30–VIII–2017, UACJ 3314 in AH its spores with scattered and thick warts on the 49113, duplo in herbarium M. Meyer. Ibidem, placed into surface. cultivation 9–IV–2018, sporocarps obtained 18–IV–2018, Physarum gyrosum has a similar morphology UACJ 3331 in AH 49094 duplo in BPI. Ibidem, sporocarps of the sporotheca, but can be distinguished by the obtained 7–V–2018, UACJ 3336. absence of a stipe, or being simply a hypothallus extension, and its spores with abundant small Sporocarpic fructifications, stipitate to rarely warts on the entire surface. sessile, single to gregarious, occasionally gathered, Physarum nicaraguense T. Macbr., is 0.5–2.25 mm height (Fig. 1). Sporotheca 0.5–1.2 according to MARTIN & ALEXOPOULOS × 0.2–0.5 mm, whitish, reniform, sinuous, rarely (1969) and LISTER (1925) a common species subglobose, frequently joined together, multi- in the American tropics. It also presents multi- lobulated, gyrose confluent, resembling Physarum lobulated sporothecae with stipe, dense white gyrosum Rostaf., sometimes sporothecae are capillitium with thick and angular nodules, joined laterally, taking an umbilicate morphology sometimes forming a whitish pseudocolumella, at the apex, sometimes laterally compressed also fructifying on dead wood. Nevertheless it is (Figs. 2–3). Peridium membranous, encrusted clearly distinguished by its closely and distinctly with white lime, which allows to see the inner warted or spinulose spores. nodules of calcium carbonate, taking a marked Schwein. also granular to reticulate morphology that resembles possess irregular to gyrose confluent sporothecae, the surface of Physarum decipiens M.A. Curtis yellow, grey or rarely white; the stipe is usually (Fig. 4). Stipe 0.2–0.8 mm height, reddish brown long, yellow, translucent, slender, flexuous, often to date brown, turning blackish brown towards confluent and its spores are minutely spinulose. the base, sometimes attached to other stipes (Fig. There are only a few species of Myxomycetes

24 Bol. Soc. Micol. Madrid 42. 2018 A NEW SPECIES OF PHYSARUM (MYXOMYCETES) FROM CHIHUAHUA, MEXICO that present a spore ornamentation formed position of the enigmatic myxomycete by scarce and scattered warts, like genus Kelleromyxa revealed by SSU rDNA luteonitens L.G. Krieglst. & Nowotny, whose sequences. Mycol Progress 12: 599–608 DOI spore ornamentation under SEM is presented in 10.1007/s11557-013-0892-8. NEUBERT & al. (1995). ESTRADA-TORRES, A., D. WRIGLEY DE BASANTA, E. CONDE & C. LADO ACKNOWLEDGEMENTS (2009). Myxomycetes associated with drylan ecosystems of the Tehuacán-Cuicatlán Valley We would like to express our gratitude Biosphere Reserve, Mexico. Fungal Diversity to A. Priego and J.A. Pérez of the Electron 36: 17–56. Microscopy Service of the University of FIORE-DONNO, A.M., M. MEYER, S.L. Alcalá for their invaluable help producing the BALDAUF & J. PAWLOWSK (2008). SEM images. We also thank Luis Monje and Evolution of dark-spored Myxomycetes A. Pueblas of the Department of Drawing and (slime-molds): Molecules versus morphology. Scientific Photography at the Alcalá University Molecular Phylogenetics and Evolution 46: for his help in the digital preparation of the 878–889. photographs, we are grateful to J. Rejos, curator FIORE-DONNO, A.M., A. KAMONO, E.E of the AH herbarium for his assistance with the CHAO, M. FUKUI & T. CAVALIER-SMITH examined specimens in the present study. We (2010). Invalidation of Hyperamoeba by want to express our gratitude to M. Meyer for transferring its species to other genera of the revision of this manuscript. We also thank D. Myxogastria. J. Eukaryot. Microbiol. 57: 189– López-Peña and H. Singer for his help with the 196. doi:10.1111/j.1550-7408.2009.00466. manuscript translation. M. Lizárraga extends his FLORES-ROMERO, I. (2017). Estudio thanks to Antonio de la Mora Covarrubias and taxonómico de Myxomycetes corticicolas Alberto Constance (DCQB-ICB, Universidad del Parque publico Federal el Chamizal e Autónoma of Ciudad Juárez) for his economic Institutos de la UACJ. Tesis de Maestría support. I. Flores-Romero thanks CONACYT for en ciencias con orientación Genómica, the scholarship given to carry out her master’s Universidad Autónoma de Ciudad Juárez, studies. Chihuahua, Mexico. 121 pp. LADO, C. (2005–2015). An online nomenclatural BIBLIOGRAPHY information system of Eumycetozoa. Real Jardín Botánico, CSIC. Madrid, BLACKWELL, M. & C.J. ALEXOPOULOS Spain. Available from: http://www.nomen. (1975). Taxonomic studies in the Myxomycetes. eumycetozoa.com (accessed 22 May 2018) IV. Protophysarum phloiogenum, a new genus LADO, C. & D. WRIGLEY DE BASANTA species of Physaraceae. Mycologia 67: 32– (2008). A review of neotropical myxomycetes 37. (1828–2008). Anal. J. Bot. Madrid 65(2): CASTILLO, A., C. ILLANA & G. MORENO 211–254. (1998). Protophysarum phloiogenum and a http://dx.doi.org/10.3989/ajbm.2008.v65.i2.293 new family in the Physarales. Mycol. Res. LADO, C., M. RODRIGUEZ-PALMA & A. 102(7): 838–842. ESTRADA-TORRES (1999). Myxomycetes ELIASSON, U., H.W. KELLER & J.D. from a seasonal tropical forest on the pacific SCHOKNECHT (1991). Kelleromyxa, a new coast of Mexico. Mycotaxon 71: 307–321. generic name for Licea fimicola (Myxomy­ LISTER, A. (1925). A Monograph of the cetes). Mycol. Res. 95: 1201–1207. (ed. 3. rev. G. Lister). British ERASTOVA, D.A., M.B. OKUN, A.M. Museum Nat. Hist. London, 296 pp. FIORE-DONNO, Y.K. NOVOZHILOV & LIZÁRRAGA, M., G. MORENO, M. ESQUE- M. SCHNITTLER (2013). Phylogenetic DA, M. CORONADO (2008). Myxomycetes

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of Sonora, México. 4: Sierra de Alamos-Rio Omega S.A., Barcelona, 1417 pp. Cuchujaqui Biosphere Reserve. Mycotaxon MORENO, G., M. LIZÁRRAGA & C. ILLANA 103: 153–170. (2007). Catálogo de los myxomycetes de LIZÁRRAGA, M., G. MORENO, M. México. Bol. Soc. Micol. Madrid 31: 187– ESQUEDA, C.I. SALAZAR-MÁRQUEZ & 229. M.L. CORONADO (2015). Myxomycetes of MORENO, G., A. CASTILLO, A. LÓPEZ- Chihuahuha (Mexico) 4. Central plains of the VILLALBA & A. SÁNCHEZ (2017). A new Chihuahuan desert. Mycotaxon 130: 1073– species of Hemitrichia in succulent plants. 1101. http://dx.doi.org/10.5248/130.1073 Bol. Soc. Micol. Madrid 41: 31–35. LIZÁRRAGA, M., G. MORENO & M. ESQUEDA NEUBERT, H., W. NOWOTNY, K. BAUMANN (2016). New records of myxomycetes from & H. MARX (1995). Die Myxomyceten, Band México. Mycotaxon 131: 511–520. http:// 2 Physarales. Karlheinz Baumann Verlag dx.doi.org/10.5248/131.511 Gomaringen, 368 pp. MARTIN G.W. & C. J. ALEXOPOULOS (1969). SALAZAR-MÁRQUEZ, C., M. LIZÁRRAGA, The Myxomycetes. University of Iowa Press. G. MORENO (2014). Myxomycetes de Iowa. USA. matorral xerófilo del municipio de Juárez, MORENO, G. & J.L. MANJÓN (2010). Guía Chihuahua, México. Bol. Soc. Micol. Madrid de hongos de la Península Ibérica. Ediciones 38: 67–77.

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