Original article

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

0000-0001-5136-2974Esteban Isrrael Moreira-Rivas^{1  *}  , 0000-0003-4629-8255Maura Isabel Díaz-Lezcano² 

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

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

ABSTRACT

Paraguay ecosystems are home to a great diversity of organisms in urban trees that include fungus-plant interactions, commonly called mycorrhizae. These mycorrhizaes 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 one exotic Bauhinia variegata L. associated with the fungus Phlebopus sp.

Key words: Mycorrhizae; Native Forest species; Exotic forest species; Macrofungi.

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 

Family	scientific name	common name
Altingiaceae	Liquidambar styraciflua	liquidámbar
Anacardiaceae	Mangifera indica L.	mango
Annonaceae	Rollinia emarginata	aratiku
Annonaceae	Annona muricata	corazon de india
Apocynaceae	Tabernaemontana catharinensis.	sapirangy
Apocynaceae	Plumeria rubra	jazmín magno
Arecaceae	Roystonea regia	palmera real
Arecaceae	Arecaceae sp.	palmera
Arecaceae	Acrocomia aculeata	mbokaja
Arecaceae	Copernicia alba	karanda
Bignoniaceae	Handroanthus albus	lapacho amarillo
Bignoniaceae	Handroanthus heptaphyllus	lapacho negro
Bignoniaceae	Jacaranda mimosifolia	jacaranda
Bignoniaceae	Tecoma stans	tecoma
Bignoniaceae	Spathodea campanulata	tulipán de la India
Boraginaceae	Cordia americana	guajayvi
Boraginaceae	Cordia ecalyculata	colita
Cecropiaceae	Cecropia pachystachya	amba
Clusiaceae	Rheedia brasiliensi	pakuri
Combretaceae	Terminalia catappa	sombrilla de playa
Euphorbiaceae	Sapium haematospermum	kurupika'y
Euphorbiaceae	Actinostemon concolor	yvyra hu
Fabaceae	Delonix regia	chivato
Fabaceae	Bauhinia variegata	lluvia de orquídea
Fabaceae	Caesalpinia ferrea	granadillo brasileño
Fabaceae	Peltophorum dubium	yvyra pyta
Fabaceae	Parapiptadenia rigida	kurupa'y
Fabaceae	Anadenanthera colubrina	kurupa'y kuru
Fabaceae	Triplaris gardneriana	villetana
Fabaceae	Geoffroea spinosa	manduvira
Fabaceae	Enterolobium contortisiliquum	timbo
Fabaceae	Tipuana tipu	tipa
Fabaceae	Inga marginata	inga
Fabaceae	Albizia niopoides	yvyraju
Fabaceae	Leucaena leucocephala	leucaena
Fabaceae	Cassia fistula	lluvia de oro
Fabaceae	Acacia mangium	acacia
Fabaceae	Pterogyne nitens	yvyra ro
Fabaceae	Bauhinia forficata	lluvia de orquídeas
Fabaceae	Albizia niopoides	yvyraju
Lamiaceae	Vitex megapotamica	taruma
Lauraceae	Ocotea sp.	laurel
Malpighiaceae	Malpighia emarginata	acerola
Malvaceae	Ceiba chodatii	samu'u
Malvaceae	Guasuma ulmifolia	kamba aka
Meliaceae	Melia azedarach	paraiso
Meliaceae	Cedrela fissilis	cedro
Moraceae	Ficus luschnathiana	ybapoy
Moraceae	Ficus benjamina	ficus
Moraceae	Morus alba	mora
Moraceae	Ficus enormis	guapo y
Moringaceae	Moringa oleifera	moringa
Myrtaceae	Eucalyptus grandis	eucalipto
Myrtaceae	Eugenia uniflora	ñangapiry
Myrtaceae	Myrtus communis	mirto
Myrtaceae	Psidium guajava	guayaba
Proteaceae	Grevillea robusta	grevillea
Rhamnaceae	Hovenia dulcis	hovenia
Rutaceae	Citrus limonia	limon
Rutaceae	Citrus aurantiun	apepu
Sapindaceae	Sapinduous saponaria	casita
Sapindaceae	Melicoccus lepidopetalus	yvapovo
Sapotaceae	Chrysophyllum gonocarpum	agua'i
Ulmaceae	Phyllostylon rhamnoides	juasy'y
Urticaceae	Cecropia pachystachya	amba'y

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)}.

C) Basidiocarp color when old. D) Cross section of Phlebopus sp. associated with Bauhinia variegate

Fig. 1.  - A) Observation of the pores. B) Entire basidiocarps with a gregarious growth habit. 

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. 

Botanical family	Scientific name	Source	Location
Bignoniaceae	Handroanthus heptaphyllus	native	Americas Square (-25.2938788, -57.581541.16z)
Bignoniaceae	Jacaranda mimosifolia	native	Infante Rivarola Square (-25.294579, -57.5775188.15z)
Fabaceae	Bauhinia variegate	exotic	Carlos Antonio López Park (-25.2869366,-57.6510244.15z)

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).

Fig. 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 ^{Kumlaet 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.

Fig. 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).

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Received: January 26, 2022; Accepted: June 16, 2022

^*Autor para la correspondencia: [e-mail]

Los autores declaran no tener conflictos de intereses.

Esteban Isrrael Moreira-Rivas: Concepción de la idea, búsqueda y revisión de literatura, confección de instrumentos, aplicación de instrumentos, recopilación de la información resultado de los instrumentos aplicados, análisis estadístico, confección de tablas, gráficos e imágenes, confección de base de datos, asesoramiento general por la temática abordada, redacción del original (primera versión), revisión y versión final del artículo, corrección del artículo, coordinador de la autoría, traducción de términos o información obtenida, revisión de la aplicación de la norma bibliográfica aplicada.

Maura Isabel Díaz-Lezcano: Concepción de la idea, búsqueda y revisión de literatura, confección de instrumentos, aplicación de instrumentos, recopilación de la información resultado de los instrumentos aplicados, análisis estadístico, confección de tablas, gráficos e imágenes, confección de base de datos, asesoramiento general por la temática abordada, redacción del original (primera versión), revisión y versión final del artículo, corrección del artículo, coordinador de la autoría, traducción de términos o información obtenida, revisión de la aplicación de la norma bibliográfica aplicada.