Association of Phlebopus sp. with arborean species of the urban trees of Asunción, Paraguay

Cuban Journal of Forest Sciences. 2022; May-August 10(2): 182-196

Translated from the original in spanish

Original article

Association of Phlebopus sp. with arborean species of the urban trees of Asunción, Paraguay

Asociación de Phlebopus sp. con especies forestales del arbolado urbano de Asunción, Paraguay

Associação de Phlebopus sp. com espécies florestais das árvores urbanas de Assunção, Paraguai

Esteban Isrrael Moreira-Rivas^1* https://orcid.org/0000-0001-5136-2974

Maura Isabel Díaz-Lezcano² https://orcid.org/0000-0003-4629-8255

¹Universidad Nacional de Asunción, Facultad de Ciencias Agrarias. Paraguay.

²Universidad Nacional de Asunción, Facultad de Ciencias Agrarias, Carrera: Ingeniería Forestal Paraguay.

^*Corresponding author: imisrraelmoreira@gmail.com

Received:26/01/2022.
Approved:16/06/2022.

ABSTRACT

Paraguayan ecosystems are home to a great diversity of organisms in urban trees that include fungus-plant interactions, commonly called mycorrhizae. These mycorrhizae present a number of subterranean hyphae that are difficult to visually appreciate and basidiocarps that grow together with certain forest species. Therefore, the objective of this research was to identify mycorrhizal associations between macrofungi and forest species that interact with each other in the urban trees of Asunción, Paraguay. For this, two squares (De las Américas and Infante Rivarola) and the Carlos Antonio López Park were selected as reference points. A tour was carried out to identify the floristic composition of urban trees in the aforementioned green spaces, and the observation of the existence of microrhizal fungi . The fruiting bodies of the macrofungi found were collected and taken to the Biology Laboratory of the Faculty of Agrarian Sciences of the National University of Asunción, they were dried for microscopic observation and identification. The forest species were identified using taxonomic keys, taking into account the size of the tree, the stem, the wood, the bark and the leaves. Three specimens of macrofungi of the genus Phlebopus were found associated with the trees of the Bignoniaceae and Fabaceae families in Asuncion green spaces. Two native forest species Handroanthus heptaphyllus (Vell.) Mattos, Jacaranda mimosifolia D.Don and an exotic Bauhinia variegate L. with association of the fungus Phlebopus sp .

Keywords: Mycorrhizae; Native forest species; Exotic forest species; Macrofungi.

RESUMEN

Los ecosistemas paraguayos albergan una gran diversidad de organismos en el arbolado urbano que incluyen las interacciones hongo-planta, comúnmente llamadas micorrizas. Estas micorrizas presentan una cantidad de hifas subterráneas de difícil apreciación visual y basidiocarpos que crecen junto a ciertas especies forestales. Por ello, el objetivo de esta investigación fue identificar asociaciones micorrízicas entre macrohongos y especies forestales que interactúan entre de sí en el arbolado urbano de Asunción, Paraguay. Para ello, fueron seleccionados como puntos de referencia dos plazas (De las Américas e Infante Rivarola) y el Parque Carlos Antonio López. Se realizó un recorrido para la identificación de la composición florística del arbolado urbano en los mencionados espacios verdes, y la observación de la existencia de hongos microrrízicos. Los cuerpos fructíferos de los macrohongos encontrados fueron recolectados y llevados al Laboratorio de Biología de la Facultad de Ciencias Agrarias de la Universidad Nacional de Asunción, se procedió al secado de estos para su observación microscópica e identificación. Las especies forestales fueron identificadas mediante las claves taxonómicas teniendo en cuenta el porte del árbol, el fuste, la madera, la corteza y las hojas. Tres ejemplares de macrohongos del género Phlebopus fueron encontrados asociados a los árboles de las familias Bignoniaceae y Fabaceae en los espacios verdes asuncenos. Se identificaron dos especies forestales nativas Handroanthus heptaphyllus (Vell.) Mattos, Jacaranda mimosifolia D. Don y una exótica Bauhinia variegata L. con asociación del hongo Phlebopus sp.

Palabras clave: Micorrizas; Especies forestales nativas; Especies forestales exóticas; Macrohongos.

RSUMO

Os ecossistemas paraguaios abrigam uma grande diversidade de organismos em árvores urbanas que incluem interações fungo-planta, comumente chamadas de micorrizas. Estas micorrizas apresentam uma série de hifas subterrâneas de difícil apreciação visual e basidiocarpos que crescem junto com certas espécies florestais. Portanto, o objetivo desta pesquisa foi identificar associações micorrízicas entre macrofungos e espécies florestais que interagem entre si nas árvores urbanas de Assunção, Paraguai. Para isso, duas praças (De las Américas e Infante Rivarola) e o Parque Carlos Antonio López foram selecionados como pontos de referência. Foi realizado um passeio para identificar a composição florística da arborização urbana nos referidos espaços verdes, e a observação da existência de fungos microrrizais. Os corpos de frutificação dos macrofungos encontrados foram coletados e levados ao Laboratório de Biologia da Faculdade de Ciências Agrárias da Universidade Nacional de Assunção, onde foram secos para observação microscópica e identificação. As espécies florestais foram identificadas por meio de chaves taxonômicas, levando em consideração o tamanho da árvore, o caule, a madeira, a casca e as folhas. Três espécimes de macrofungos do gênero Phlebopus foram encontrados associados às árvores das famílias Bignoniaceae e Fabaceae em espaços verdes de Assunção. Duas espécies florestais nativas Handroanthus heptaphyllus (Vell.) Mattos, Jacaranda mimosifolia D. Don e uma exótica Bauhinia variegata L. com associação do fungo Phlebopus sp.

Palavras-chave: Micorrizas; Espécies florestais nativas; Espécies florestais exóticas; Macrofungos.

INTRODUCTION

The organisms of the Fungi Kingdom have been studied throughout universal history, showing that hundreds of them present a way of life that interacts with the hundreds of hosts of the Plantae Kingdom (Pham et al., 2012).

Castro (2009) mentions that the mycorrhiza is a mutualistic symbiosis where its function is to increase the absorption surface of the roots through hyphal systems. extraradical, since the plant can absorb more water, essential nutrients such as (nitrogen and phosphorus) and less mobile ions such as (copper, zinc, ammonia and phosphoric acid), favoring water balance and nutrition (Barrera 2009).

Therefore, from a nutritional perspective, one of the main contributions of mycorrhizae is the absorption of phosphorus, since this nutrient is assimilated from the root pathways, redistributing throughout the plant as it is a fundamental element for its growth, that reflects a fundamental contribution in the increase of the dry mass, growth and foliar area of the plant (Barrera 2009).

Within the edaphic community, the microbiological activity may be due to the mutualistic associations of the microrhizal fungi, such is the case that these organisms may also interact with other agents, no matter if they are bacteria or fungi, thus contributing to perform synergistic actions for the control of phytopathogens, added all this for a better growth of the plant as mentioned (Cano 2011).

Research carried out by Álvarez-Manjarrez et al. (2018) refer that mycorrhizae have certain preferences for botanical families such as (Pinaceae, Fagaceae and Betulaceae) in the northern hemisphere, since they are families of great importance due to their diversity in species and in relation to the southern hemisphere, the colonized botanical families for ectomycorrhizae are the Nothofagaceae, Myrtaceae, Dipterocarpaceae, and the order Fabales, as they are dominant.

In relation to forest species, also from a positive point of view, they can be a source of improvement in obtaining size and quality in seed production through the use of mycorrhizae through the incorporation of phosphorus and other nutrients Montaño et al. (2007).

Within urban trees, there are also fungi associated with roots in a negative way, such as Ganoderma, Fomitiporia, and Hydnopolyporus, which degrade the quality of the wood, affecting its sanitary measures (Moreira-Rivas and Díaz-Lezcano, 2021).

The objective of the research was to identify mycorrhizal associations between macrofungi and forest species that interact with each other in the urban trees of Asunción, Paraguay.

MATERIALS AND METHODS

Research Location

The fieldwork was carried out in the Plazas de las Américas, and Infante Rivarola and Carlos Antonio López Park, in the city of Asunción, Paraguay (Latitude:-25.2819, Longitude:-57.635 25° 162 553 South, 57° 382 63 West). At the end of January 2021, a tour was carried out to identify the floristic composition of urban trees, in the aforementioned green spaces, and the observation of the existence of microrhizal fungi of the genus Phlebopus. In the city of Asunción, a total rainfall of 300 mm was recorded during the month of January and an average temperature of 26ºC. This temperature is within the range considering, the average maximum temperature of 33 °C and 23 °C as minimum temperature, the warmest month of the year in Asunción is January according to Grassi (2020).

Firstly, the forest species present in the aforementioned plazas and park were identified according to the taxonomic keys of López et al. (2002), Pérez de Molas (2016), consigning the botanical family, the scientific name and the common name. For this, the size of the tree, type of stem bark, type and shape of leaves, presence of lenticels, type of inflorescences and fruiting have been considered.

Direct observations of the phytosanitary status of the trees were made and possible fruiting bodies of mycorrhizal fungi were sought , which were collected, labeled in bags and taken to the Biology Laboratory of the Faculty of Agricultural Sciences of the National University of Asunción (UNA).). Once the samples were collected, following the guidelines proposed by Miller and Miller (1988), they were dried and preserved for later microscopic observation and identification, using the Boeco Germany microscope with assemblies in Lactophenol Blue and 5 % Potassium Hydroxide. The photos were taken with a CANON PowerShot camera. Sx 410. The identification of macroscopic fungal species was carried out using the available taxonomic key (Baroni et al., 2015).

RESULTS AND DISCUSSION

Table 1 lists 27 botanical families and 69 tree species identified in the Plazas de las Américas and Infante Rivarola and the Carlos Antonio López Park in Asunción, capital of the Republic of Paraguay.

Table 1. - Tree floristic composition identified in Plazas de las Américas and Infante Rivarola and Carlos Antonio López Park in Asunción, Paraguay

In all the sites of the urban trees, where the samplings and observations were carried out, the genus Phlebopus was identified (Figure 1). It is a light brown fungus, it has a fleshy basidiocarp, solitary to gregarious in habit, its crown is brown with the central stipe tapering upwards with a yellow apex. glabrous surface. It has an irregular margin, in which it splits when they mature.

At the microscopic level, the hyphal webs are gelatinous, the basidiospores have thin walls, and the basidia are clavate.

On the other hand, the genus Phlebopus is a fungus that lives in tropical areas characterized by basidiomata with typically robust structures with the presence of a thick central stipe, without holes, short and smooth with abundant olive -brown basidiospores, brown cystidia and an immeasurable number of intertwined hyphae. the basidioma with a wide distribution in the southern hemisphere as mentioned by Watling (2008).

Figure 1. - A) Observation of the pores. B) Entire basidiocarps with a gregarious growth habit.
C) Basidiocarp color when old. D) Cross section of Phlebopus sp. associated with Bauhinia variegate

Forest associations with Phlebopus sp.

The specimens of the macrofungus Phlebopus sp. were found associated with three forest species mentioning the description and location of the host forest species of Phlebopus sp. as detailed in (Table 2). Moreira-Rivas and Díaz-Lezcano (2021), mention that in the urban trees of Asunción, species of the Fabaceae family predominate, followed by those of the Bignoniaceae family, being frequent to find in squares, parks and avenues of the city the presence of H. heptaphyllus, J. mimosifolia and B. variegata. Likewise, Díaz Lezcano et al. (2021) report that the floristic composition of forest species for ornamental use in squares and parks in Paraguay is very varied, with the species of the Fabaceae, Bignoniaceae and Arecaceae families being the most representative.

Table 2. - Specimens of the macrofungus Phlebopus sp. were found associated with three forest species, mentioning the description and location of the host forest species of Phlebopus sp.

The fungus-plant association occurs through a series of signals that they present to each other, such is the case of the mycelium that the fungi of the genus Phlebopus present sp., with a worldwide distribution, which is associated with forest species such as eucalyptus (Eucalyptus spp.) and certain legumes (Ducousso et al., 2012).

However, there is evidence that Phlebopus sp. is an edible macrofungus, reports by Cristaldo et al. (2021), which confirm that this fungus has phenolic compounds (26.30 ± 5.06 mg GAE.g^-1) and antioxidants (25.69 ± 3, 00 mg EAA.g ^-1), the latter with an activity of 11 %, which is between the edible and non-toxic parameters for human consumption.

Baroni et al. (2015) comment that this genus has been reported in many American countries such as Bolivia, Brazil, Argentina, Colombia, Ecuador, Costa Rica, Puerto Rico, Venezuela and Mexico.

In the reports mentioned by Vasco et al. (2018), support that mycorrhizae are mostly linked by the environmental conditions of the place, in addition to parameters such as (pH, soil types, availability of phosporous, nitrogen, etc.). However, in environmental conditions such as high relative humidity and intense rains that occurred in Asunción during the month of January 2021, the soil conditions were favorable for the growth of these mycorrhizae, and it can be observed that these soils have abundant organic matter that promotes saprotrophic growth of Phlebopus sp. (Figure 2).

Figure 2. - Complete basidiocarp with stereoscopic view and observation of the macrofungus associated with Jacaranda mimosifolia

The forest species J. mimosifolia is one of the dominant species in the urban trees of Asunción and, also, recommended in the Urban Tree Planting Guide for the Metropolitan Area of Asunción (MADES/PNUD/FMAM 2019), so its representativeness could be emphasizing the possibility of association with the fungus Phlebopus sp.

It was also possible to corroborate the presence of Phlebopus sp. in association with H. heptaphyllus (Figure 3). This reaffirms the evidence that mycorrhizal fungi arbusculares are the most prolific and ubiquitous root symbionts, colonizing 72 % of terrestrial plants ( Brundrett and Tedersoo, 2018). Although the benefits of mycorrhizal symbiosis are well documented, little is known about the effects of urbanization on arbuscular mycorrhizal associations (Buil et al., 2021).

According to Kumla et al. (2016), Phlebopus sp. synthetically forms anatomically complete ectomycorrhizae with Pinus sp. and Acacia sp.; however, Palacio et al. (2015) maintain that species of the genus Phlebopus are facultative fungi. On the other hand, Singer et al. (1983) and Sánchez and Mata (2012) state that they are saprobes, which calls into question the ectomycorrhizal nature of the species. In addition, Flamini et al. ( 2018) and Sánchez and Mata (2012) maintain that species of the genus Phlebopus are food fungi.

Deschamps (2002) highlighted that, in San Luis and Córdoba, Argentina, the relationship between Phlebopus bruchii and the Fagara coco tree (Carrillo 2014), belonging to the Rutaceae family, has its origin in native flora, as well as in the case reported in the present investigation where the association between this genus of fungus and two forest species is recorded. natives, J. mimosifolia and H. heptaphyllus.

Figure 3. - Macroscopic observations associated with Handroanthus heptaphyllus characterized by taxonomic keys

On the other hand, the species Bauhinia variegata is a legume that also presented symbiotic associations with the genus Phlebopus sp., as seen in Figure 1.

In the reports made by (Pérez-Moreno and Read 2004), it is mentioned that the genera Acacia, Aldinia and Inga present certain associations with the genera of the Boletales order, to which Phlebopus belongs sp.

Alexander and Hogberg (1986) have also reported genera of edible fungi associated with the subfamily Caesalpinoideae, these genera are: Afzelia, Brachystegia, Isoberlinia and Julbernardia, this being the first indication of Phlebopus sp.. associated with B. variegata as mycorrhiza.

According to the FAO, (2005) there are many economic benefits produced by fungi from the forest point of view, since these are reflected in rural communities, especially in developing countries.

CONCLUSIONS

Specimens of the macrofungus were identified Phlebopus spp. associated with three forest species of the families Bignoniacea: Handroanthus heptaphyllus and Jacaranda mimosifolia and Fabaceae: Bauhinia variegata, very abundant species in the urban trees of Asunción.

The study suggests the execution of silvicultural management related to the health status of trees in the metropolitan area of Asunción and, above all, a record of fungus-tree interaction that allows further identification of Phlebopus species.

FUNDING

Activities related to laboratory work regarding equipment, instruments and reagents have been financed by the Faculty of Agrarian Sciences of the National University of Asunción, and travel to collect samples with the authors' own resources.

ACKNOWLEDGEMENT

The authors appreciate the support of Dr. Daniel Rivaldi of the (FCQ-UNA) and the Faculty of Agricultural Sciences (FCA-UNA).

REFERENCES

ALEXANDER, I.J. and HOGBERG, P., 1986. Ectomycorrhizas of tropical angiospermous trees. The new phytologist [en línea], vol. 102, no. 4, pp. 541_549. [Consulta: 26 January 2022]. ISSN 0028-646X. DOI 10.1111/j.1469-8137.1986.tb00830.x. Disponible en: https://www.mendeley.com/catalogue/575ca9f4-9fad-3dfa-8311-1f95e62d4dd0/.

ALVAREZ-MANJARREZ, J., GARIBAY-ORIJEL, R. and SMITH, M.E., 2018. Caryophyllales are the main hosts of a unique set of ectomycorrhizal fungi in a Neotropical dry forest. Mycorrhiza [en línea], vol. 28, no. 2, pp. 103_115. ISSN 0940-6360. DOI 10.1007/s00572-017-0807-7. Disponible en: http://dx.doi.org/10.1007/s00572-017-0807-7.

BARONI, T.J., CIFUENTES, J., SANTANA, B.O. and CAPPELLO, S., 2015. A new species of Phlebopus (Boletales, Basidiomycota) from Mexico. North American fungi [en línea], vol. 10, no. 0, pp. 1_13. [Consulta: 26 January 2022]. ISSN 1937-786X. DOI 10.2509/naf2015.010.007. Disponible en: https://openjournals.wsu.edu/index.php/pnwfungi/article/view/1429.

BARRERA B,E., 2009. EL USO DE HONGOS MICORRÍZICOS ARBUSCULARES COMO UNA ALTERNATIVA PARA LA AGRICULTURA. Biotecnoloía en el Sector Agropecuario y Agroindustrial [online]. 2009. vol. 7, no. 1, p. 123_132. [Zugriff am: 26 January 2022]. Verfügbar unter: http://www.scielo.org.co/scielo.php?pid=S1692-35612009000100014&script=sci_abstract&tlng=es

BRUNDRETT, M.C. and TEDERSOO, L., 2018. Evolutionary history of mycorrhizal symbioses and global host plant diversity. The new phytologist [en línea], vol. 220, no. 4, pp. 1108_1115. ISSN 0028-646X. DOI 10.1111/nph.14976. Disponible en: http://dx.doi.org/10.1111/nph.14976.

BUIL, P.A., D, RENISON, y A, BECERRA, 2021. Soil infectivity and arbuscular mycorrhizal fungi communities in four urban green sites in central Argentina. Urban Forestry & Urban Greening, 64, 127285. Researchgate.net [en línea], Disponible en: https://www.researchgate.net/publication/353735072_Soil_infectivity_and_arbuscular_mycorrhizal_fungi_communities_in_four_urban_green_sites_in_central_Argentina.

CANO, M.A. and UNIVERSIDAD DE CIENCIAS APLICADAS Y AMBIENTALES, 2011. Interacción de microorganismos benéficos en plantas: Micorrizas, Trichoderma spp. y Pseudomonas spp. una revisión. Revista Udca Actualidad & Divulgacion Cientifica [online]. 2011. vol. 14, no. 2, p. 15_31. [Zugriff am: 26 January 2022]. DOI 10.31910/rudca.v14.n2.2011.771. Disponible en: http://www.scielo.org.co/scielo.php?pid=S0123-42262011000200003&script=sci_abstract&tlng=es

CARILLO, L., 2014. Los hongos comestibles en el código alimentario Argentino. Revista-AGRARIA. [online]. 2014. vol. 8, no. 15, No15, p. 99-103 [Consulta: 26 January 2022]. ISSN 2362-4035. Disponible en: http://www.fca.unju.edu.ar/investigacion/agraria/2014/8/15.

CRISTALDO, E., CAMPI, M., MANCUELLO, C., y MAUBET, Y, 2021. Perfil químico y biológico del hongo comestible Phlebopus sp. Revista-Steviana. [online]. 2021. vol. 13, no. 1, p. 96 [Consulta: 26 January 2022]. ISSN 2304-2907. Disponible en: http://www.facen.una.py/wp-content/uploads/2021/11/Libro-de-resumenes_IVJPB_2021.pdf

DESCHAMPS, J.R., 2002. Hongos silvestres comestibles del Mercosur con valor gastronómico. [en línea], [Consulta: 26 January 2022]. ISSN 1850-2547. Disponible en: http://repositorio.ub.edu.ar/handle/123456789/433.

DÍAZ-LEZCANO, M.I; GAMARRA-LEZCANO, C.C., Y LEZCANO-ACOSTA, M, 2021. Especies Forestales Ornamentales en Paraguay. Ediciones INTA, [en línea], pp. 29-40. [Consulta: 26 January 2022]. ISBN 978-987-679-312-4. Disponible en: https://repositorio.inta.gob.ar/handle/20.500.12123/10744#

DUCOUSSO, M., DUPONNOIS, R., THOEN, D. and PRIN, Y., 2012. Diversity of ectomycorrhizal fungi associated withEucalyptusin Africa and Madagascar. International journal of forestry research [en línea], vol. 2012, pp. 1_10. [Consulta: 26 January 2022]. ISSN 1687-9368. DOI 10.1155/2012/450715. Disponible en: https://www.hindawi.com/journals/ijfr/2012/450715/.

FAO.(FOOD AND AGRICULTURE ORGANIZATION OF THE UNITED NATIONS), 2005. Los Hongos Silvestres Comestibles: Perspectiva Global de Su USO E Importancia Para La Poblacion (Productos Forestales No Madereros). Food & Agriculture Organization of the United Nations (FAO) [en línea]. [Consulta: 26 January 2022]. Disponible en: https://www.iberlibro.com/9789253051571/Hongos-Silvestres-Comestibles-Perspectiva-Global-9253051574/plp.

FLAMINI, M., SUÁREZ, M.E. and ROBLEDO, G., 2018. Hongos útiles y tóxicos según los yuyeros de La Paz y Loma Bola (Valle de Traslasierra, Córdoba, Argentina). Boletin de la Sociedad Argentina de Botanica. Sociedad Argentina de Botanica [en línea], vol. 53, no. 2, pp. 319_338. [Consulta: 26 January 2022]. ISSN 0373-580X. DOI 10.31055/1851.2372.v53.n2.20588. Disponible en: https://revistas.unc.edu.ar/index.php/BSAB/article/view/20588.

GRASSI, B. 2020. Estado del clima Paraguay 2019 "Cambio climático, evidencias científicas e impactos" [Consulta: 17 April 2022]. Disponible en: https://www.stp.gov.py/v1/wp-content/uploads/2020/11/Presentacio%CC%81n-Estado-del-Clima-Paraguay-2019_compressed.pdf.

KUMLA, J., HOBBIE, E.A., SUWANNARACH, N. and LUMYONG, S., 2016. The ectomycorrhizal status of a tropical black bolete, Phlebopus portentosus, assessed using mycorrhizal synthesis and isotopic analysis. Mycorrhiza [en línea], vol. 26, no. 4, pp. 333_343. [Consulta: 26 January 2022]. ISSN 0940-6360. DOI 10.1007/s00572-015-0672-1. Disponible en: https://pubmed.ncbi.nlm.nih.gov/26671421/.

LOPEZ, J.A., LITTLE, E.L., RITZ, G.F., ROMBOLD, J.S. and HAHN, W.J., 2002. Árboles comunes del Paraguay ñande yvyra mata kuera. [en línea], [Consulta: 26 January 2022]. Disponible en: https://www.agr.una.py/fca/index.php/libros/catalog/book/284.

MADES/PNUD/FMAM. 2019. Guía de ArborizaciónUrbana para el Área Metropolitana de Asunción. Proyec-to"Asunción Ciudad Verde de las Américas _ Vías a la Sustentabilidad". Asunción, Paraguay. 114 p.

MILLER JUNIOR, O.K. & MILLER, H.H. 1988. Gasteromycetes: Morphology and Developmental Features. Eureka, Mac River.

MONTAÑO, N.M, CAMARGO-RICALDE, S.L, GARCÍA-SÁNCHEZ, R. Y MONROY, A, 2009. Micorrizas arbusculares en ecosistemas áridos y semiáridos (Arbuscular mycorrhizae in arid and semiarid ecosystems). Instituto Nacional de Ecología-SEMARNAT, Mundi-Prensa SA de CV, UAM-Iztapalapa, FES Zaragoza, UNAM. Distrito Federal, México. 460 pp. [Consulta: 26 January 2022].Disponible en: https://www.researchgate.net/profile/Arcadio-Monroy-Ata/publication /242595379_MICORRIZAS_ARBUSCULARES_EN_ECOSISTEMAS_ARIDOS_Y_SEMIARIDOS /links/55774cb208aeacff20004a4f/MICORRIZAS-ARBUSCULARES-EN-ECOSISTEMAS-ARIDOS-Y-SEMIARIDOS.pdf

MOREIRA-RIVAS, E.I. and DÍAZ-LEZCANO, M.I., 2021. Arbolado urbano de la zona metropolitana de Asunción (Paraguay) y hongos descomponedores asociados. CEDAMAZ [en línea], vol. 11, no. 2, pp. 93_98. [Consulta: 26 January 2022]. ISSN 1390-5902. DOI 10.54753/cedamaz.v11i2.1176. Disponible en: https://revistas.unl.edu.ec/index.php/cedamaz/article/view/1176.

PALACIO, M., GUTIÉRREZ, Y., FRANCO-MOLANO, A.E. and CALLEJAS-POSADA, R., 2015. Nuevos registros de macrohongos (Basidiomycota) para Colombia procedentes de un bosque seco tropical. Actualidades Biológicas [en línea], vol. 37, no. 102, pp. 319_339. [Consulta: 26 January 2022]. ISSN 0304-3584. Disponible en: http://www.scielo.org.co/scielo.php?script=sci_arttext&pid=S0304-35842015000100008&lng=en&tlng=es.

PÉREZ DE MOLAS, L, 2016. Manual de Familias y Géneros de árboles del Paraguay.[en línea. [Consulta: 26 Enero 2022]. ISBN 978-92-5-309402-8 Disponible en: http://www.infona.gov.py/index.php/noticias/manual-de-familias-y-generos-de-arboles-del-paraguay.

PÉREZ-MORENO, J. and READ, D.J., 2004. Los hongos ectomicorrÍzicos, lazos vivientes que conectan y nutren a los árboles en la naturaleza. Interciencia [en línea], vol. 29, no. 5, pp. 239_247. [Consulta: 26 January 2022]. ISSN 0378-1844. Disponible en: http://ve.scielo.org/scielo.php?script=sci_arttext&pid=S0378-18442004000500004&lng=es&tlng=es.

PHAM, Nguyen-Duc Hoang, Akira SUZUKI, Nguyen-Duc Hoang PHAM, Akiyoshi YAMADA, Kiminori SHIMIZU, Katsuji NODA, Le-Anh Tuan DANG and Akira SUZUKI, 2012. A sheathing mycorrhiza between the tropical bolete Phlebopus spongiosus and Citrus maxima. Mycoscience [online]. 2012. vol. 53, no. 5, p. 347_353. DOI 10.1007/s10267-011-0177-5. Verfügbar unter: https://www.sciencedirect.com/science/article/pii/S1340354012700499

SÁNCHEZ, J.E. and MATA, G., 2012. Hongos comestibles y medicinales en Iberoamérica: investigación y desarrollo en un entorno multicultural. Tapachula, Chiapas, México: El Colegio de la Frontera Sur, Instituto de Ecología. ISBN 9786077637738. https://pesquisa.bvsalud.org/portal/resource/pt/biblio-948657

SINGER, R., ARAUJO, I. and IVORY, M.H., 1983. The electrophically mycorrhizal fungi of the neotropical lowlands, especially Central Amazonia. Vaduz, Liechtenstein: Cramer. ISBN 9783768254779. https://www.worldcat.org/title/ectotrophically-mycorrhizal-fungi-of-the-neotropical-lowlands-especially-central-amazonia/oclc/12947830

VASCO, A., HERNÁNDEZ, J., PENUELA, M., MOLANO, A. y BOEKHOUT, T., 2018. Ectomycorrhizal fungi diversity in a white sand forest in western Amazonia. Fungal Ecology, vol. 31, pp. 9-18. DOI 10.1016/j.funeco.2017.10.003. https://www.sciencedirect.com/science/article/abs/pii/S175450481730123X

WATLING, R., 2008. A Manual and Source Book on the Boletes and their allies. Summerfield Books [en línea]. [Consulta: 26 January 2022]. Disponible en: https://www.summerfieldbooks.com/product/a-manual-and-source-book-on-the-boletes-and-their-allies/.

Conflict of interest:
The authors declare that they have no conflict of interest.

Authors contribution
Esteban Isrrael Moreira-Rivas: Conception of the idea, literature search and review, instrument making, instrument application, compilation of information resulting from the instruments applied, statistic analysis, preparation of tables, graphs, and images, database preparation, general advice on the topic addressed, drafting of the original (first version), review and final version of the article, article correction, authorship coordinator, translation of terms or information obtained, review of the application of the applied bibliographic standard.

Maura Isabel Díaz-Lezcano: Conception of the idea, literature search and review, instrument making, instrument application, compilation of information resulting from the instruments applied, statistic análisis, preparation of tables, graphs, and images, database preparation, general advice on the topic addressed, drafting of the original (first version), review and final version of the article, article correction, authorship coordinator, translation of terms or information obtained, review of the application of the applied bibliographic standard.

This work is licensed under a Creative Commons Attribution-NonCommercial 4.0 International license.
Copyright (c)Esteban Isrrael Moreira-Rivas, Maura Isabel Díaz-Lezcano.