Keywords

1 Introduction

The native Quercus humboldtii is a dominant species in the Colombian Andean mountains, expanding from the Darien in Panama (8° N) to the southern montane cordilleras in Colombia (1° N) (Pulido et al. 2006; Cárdenas and Salinas 2006; Orwa et al. 2009), within a wide altitudinal range from 750 to 3450 m asl (Fundación Natura 2007; Avella and Cárdenas 2010). These ecosystems occupy small continuous and discontinuous relicts in the Colombian departments of Antioquia, Boyacá, Caldas, Cauca, Cundinamarca, Chocó, Huila, Nariño, Quindio, Santander, Valle del Cauca, and Tolima (Myers and Lynch 1997; Pulido et al. 2006; Fundación Natura 2007).

Oak forests establish symbiotic relationships with ectomycorrhizal mushrooms (ECM). This beneficial ecological interaction is established between plant roots and fungal mycelium, playing an essential role in the dynamics of forest ecosystems. The association allows the exchange of nutrients, especially phosphorus and nitrogen, from the fungi to the host plant and carbohydrates from the host to the fungi, and it constitutes an overall communication system among several trees by translocating nutrients (Read 1998; Pérez-Moreno and Read 2004).

Most studies related to macrofungi in Colombia have focused on oak forests (Q. humboldtii), because it is estimated that fungal diversity in these ecosystems is high (Franco-Molano et al. 2000). Nearly 99% of the local fungal diversity has been reported in the Andean Mountains, including saprotrophic, pathogenic, entomopathogenic, and ectomycorrhizal fungi (Vasco-Palacio and Franco-Molano 2013).Moreover, native oak forests are the habitat for many ectomycorrhizal species with a potential high value, because of their nutritive and medicinal characteristics and their importance to local people as an economic income (Boa 2004, Pérez-Moreno 2012). This fact raises the attention on managing good practices of the ecosystem products.

In this chapter, we compile information on ECM species and their distribution in Colombia, based on national reports of specimens collected in Q. humboldtii forests. Regarding the use of mushrooms, we provide references in which the edibility of some ectomycorrhizal mushrooms was reported. We include 2 national and 16 local species records from the departments of Boyacá, Cundinamarca, and Santander. We suggest that more studies aiming to assess the regional fungal diversity are key components to move forward in the knowledge of the Colombian fungi and their conservation.

2 Methods

2.1 Sampling

Fruiting bodies of ECM associated with Quercus humboldtii were collected in the forests of Boyacá and Santander. The departments distributed along the Andean mountains present two highest precipitation seasons during the year (Guzmán et al. 2014): April–June and October–December, which favour the fructification of fungal species. We collected specimens during the rainy season of April–May 2014 and 2015 in the departments of Boyacá (Municipio de Villa de Leyva, Vereda Capilla 05°39′ 26.78″ N, 73°30′ 46.41″ O; Municipio de Arcabuco, Vereda Piedras Blancas, 05°48.546″ N, 73°28.751″ O; Municipio de Arcabuco, 5°45′ 35.38″ N, 73°26′ 47.10″ O) and Santander (Vereda San José de La Montaña 06°02′ 29.82″ N, 73°00′ 02.8″ O). We included records from Cundinamarca based on previously collected specimens stored in the ANDES Herbarium (Universidad de los Andes, Bogotá) and registered in the SPECIFY database version 6.6.02 software (www.specifysoftware.org).

2.2 Descriptions

Macroscopic and microscopic features were analyzed for each collected sample. Fruit bodies were dried and packaged in plastic bags, stored in the ANDES Herbarium (Universidad de los Andes, Bogotá), and registered in the SPECIFY database. We used taxonomic keys and guides by Arora (1986), Halling (1989), Halling and Mueller (1999), Franco-Molano et al. (2000), Tulloss (2000, 2002, 2005), Mata et al. (2003), Halling and Mueller (2005), and Phillips (2005).

2.3 Search for ECM Reports in Colombia, the Mycorrhizal Trophic Status and the Edibility of Wild Mushrooms

We made an extensive literature search on fungal diversity lists for the country, with the earliest record by Hooker and Kunth in 1822 and until 2018. We included reports from published papers, field guides, and books. Articles showing the ectomycorrhizal trophic status of fungal genera included in our ECM checklist were searched in the ISI Web of Knowledge (www.webofknowledge.com). The family and author of each species followed Index Fungorum (http://www.indexfungorum.org/names/names.asp). Finally, we provide references in which the edibility of some ectomycorrhizal species is reported (Smith 1964, Arnolds 1995, Polese and Lamaison 1999, Boa 2004, Phillips 2005, Pérez-Moreno et al. 2010, Burrola-Aguilar et al. 2012, Eyssartier et al. 2011, Smith and Bonito 2012).

3 Results and Discussion

A total of 120 ECM species were compiled from reports indicating their association to Q. humboldtii forests (Table 16.1). Figure 16.1 shows a map of Colombia with the number of ECM species per family and per department. About 11 out of 14 departments located in the Andean mountain system have records of ECM species, except Risaralda, Chocó, and Norte de Santander. Caldas, Quindio, and Tolima are among the departments with the lowest number of ECM reports. The department with the highest number of repords is Antioquia, followed by Boyacá and Cundinamarca. The fungal families with the major number of ECM species per department were Boletaceae (in five departments), Amanitaceae (in two departments), and Russulaceae (in two departments).

Table 16.1 Ectomycorrhizal species reported in Q. humboldtii in Colombia. Species reported as edible are indicated
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Fig. 16.1
figure 1

The departments of Colombia where ECM species have been reported with Quercus humboldtii. The number of ECM species per family is indicated inside each pie chart. The delineated departments in the map encompass the Andean cordillera and are a part of the total departments in Colombia

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Information on the ectomycorrhizal trophic status of fungal genera was confirmed by literature regarding anatomical, chemical, and/or molecular analyses (Table 16.2).

Table 16.2 References reporting the ectomycorrhizal characteristic of fungal genera included in this study
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A total of 18 species are new records: 2 national and 16 local records for the departments of Boyacá, Cundinamarca, and Santander (Table 16.3, Fig. 16.2)

Table 16.3 New records of ECM fungi collected in Q. humboldtii forests, in the departments of Boyacá, Cundinamarca, and Santander
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Fig. 16.2
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Basidiome and microscopy of new national and some local records. (a) Basidiomes of Inocybe tahquamenonensis, (a1) Spores of I. tahquamenonensis, (a2) Basidia of I. tahquamenonensis; (b) Cortinarius violaceus; (c) Basidiome of Russula sardonia, (c1) Spores, basidia and pleurocystidia of R. sardonia; (d) Phylloporus centroamericanus; (e) Boletus neoregius; (f) Calostoma cinnabarinum; (g) Xerocomellus chrysenteron; (h) Craterellus fallax; (i) Amanita fuligineodisca. White scale bars correspond to 1 cm. Black scale bars correspond to 10 μm

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3.1 Morphological Description of the Two National Records

Inocybe tahquamenonensis D.E. Stuntz 1954. Material studied NVE 303 ANDES_F802 Fig. 2A, A1, A2—Colombia, Boyacá, Municipio de Arcabuco, Vereda Peñas Blancas, 20 May 2012, in Q. humboldtii. This species occurs in north temperate regions in eastern North America (Phillips 2005; Matheny and Moreau 2009). Pileus: 1.5–4 cm cm wide, convex to plano-convex to decurved when mature, dark purplish-brown to reddish or blackish-brown, with pronounced scales concolorus with the pileus surface; margin even with scales. Context reddish-purple, 4 mm wide. Lamellae adnexed to adnated, concolorous with the pileus surface, close to slightly distant. Spore print brown. Stipe 3–6 × 0.4–0.7 cm, concolorus with the pileus surface, cylindrical, with abrupt scales. Basidiospores: 6–9 × 5–7.5 μm, cruciform. Basidia: 24–31 × 13–16 μm. Hymenophoral trama interwoven hyphae.

Russula sardonia Fr. 1838. Material studied NVE 633 ANDES_F650 Fig. 2C, C1—Colombia, Boyacá, Municipio de Arcabuco, km 5 via Arcabuco-Gachantiva. 15 Dec. 2013, in Q. humboldtii. This species occurs in north temperate regions, found in Europe and western North America (Phillips 2005).

Pileus: 4–6.5 cm wide, convex, to flat in mature specimens and with a depression, violet, purplish or brownish-red, greenish or ochre to yellowish, hard, glabrous. Context white, 1–2 cm wide. Lamellae adnexed to slightly decurrent, at first cream to pale golden yellow, narrow. Stipe: 3.0–8.0 cm long × 1.0–1.5 cm wide, whitish to very pale lilac upper half, to greyish dark lilac in the lower half, uniform; surface fibrillose to slightly pruinose. Spore print cream. Basidiospores: 7–9 × 6–8 μm, ovoid with warts up to 0.5 μm high, joined into ridges forming fine irregular lines or rugose ornamentation. Basidia: 50–60 × 10–14 μm. Hymenophoral trama: ovoid cells up to 30 μm long, regularly arranged. Pleurocystidia spindle-shaped or cylindrical, without septa.

3.2 Notes on Some Taxa Not Included in the Checklist

3.2.1 Basidiomycota

Amanitaceae: All the species in Colombia, with the exception of A. savannae (described from a wet savanna by Tulloss and Franco-Molano, 2008), belong to a clade of symbiotic species (Subgenera Lepidella and Amanita) (Wolfe et al. 2012). We did not include the species A. ceciliae in the list, because the Colombian and Mesoamerican species for “A. ceciliae” probably is A. sororcula Tulloss, Ovrebo & Halling (http://amanitaceae.org/?Amanita%20ceciliae). The species A. muscaria has been widely reported in exotic pine plantations (Pulido 1983; Franco-Molano et al. 2000; Franco-Molano and Uribe-Calle 2000; Montoya et al. 2005), but Vargas et al. (2019) reported it in association with Q. humboldtii in Santander.

Cortinariaceae: The genus Cortinarius is one of the most diverse genera containing over 2000 spp. (Kirk et al. 2008), and a large number of taxa occurring in Colombia have not been determined yet to species level.

Entolomataceae: The species E. ferrugineogranulatum reported by Soto-Medina and Bolaños-Rojas (2013) and Horak (1977) was not included in the checklist , since it was reported in open lands (potreros) and on rotten wood in rain forests. The same occurs for the species E. lyophylliforme reported by Horak (1977) in a tropical rain forest near Buenaventura at 180 m asl. The species E. venezuelanum (Dennis) E. Horak 1978 was collected in forests dominated by Colombobalanus excelsa (Soto-Medina and Bolaños-Rojas 2013) and was not included in the checklist. The genus Entoloma is reported to have ectomycorrhizal species (Rinaldi et al. 2008; Tedersoo et al. 2010); however, the subgenera Nolanea and Leptonia are nonmycorrhizal (Tedersoo et al. 2010).

Hydnangiaceae: The species Laccaria ohiensis has been collected in forests dominated by the native oak species Colombobalanus excelsa in the department Valle del Cauca (Soto-Medina and Bolaños-Rojas 2013). A report of Laccaria laccata was made by Sánchez (2006) in Norte de Santander; however, there is no specification on its host.

Boletaceae: the species Boletus orquidianus (=Xerocomus orquidianus) was reported for the country but not associated with Fagaceae (Halling 1989). However, it was later collected in an oak forest in Antioquia (Franco-Molano et al. 2000). The species Boletus pavonius and B. purpurascens are reported from Santander (Hooker and Kunth 1822; Vasco-Palacio and Franco-Molano 2013) on the banks of the Magdalena river growing on decomposed wood (Hooker and Kunth 1822), and was not included in this checklist. A specimen identified as B. reticulatus was collected in a temperate region between Popayán and Almaguer (Hooker and Kunth 1822), probably in oak forests; however, no vegetation information for this specimen was reported.

We did not include species in the genus Phlebopus, since the ecology of the genus is ambiguous showing some species cultivated as saprotrophs (Thoen and Ducousso 1990; Wilson et al. 2012) or engaging in multipartite symbiotic interactions (Zhang et al. 2015).

The genus Chalciporus has been reported as ectomycorrhizal by Rinaldi et al. (2008); however, Tedersoo et al. (2010) concluded that there is not enough evidence to show its mycorrhizal habit. For this reason, we did not include in the checklist two species reported in Colombia: Chalciporus piperatus (Bull.) Bataille and Chalciporus caribaeus Pegler reported by López-Quintero et al. (2007) and Franco-Molano et al. (2010), respectively.

Suillus luteus NVE425 Andes_F925, was collected in Q. humboldtii in the department of Boyacá. However, species in this genus are restricted to Pinaceae, and therefore S. luteus was not included in the present ECM checklist. Anatomical, chemical, and molecular analyses must be performed to confirm the association with Q. humboldtii. Previous studies have reported this species in Colombia associated with conifers (Franco-Molano et al. 2000) and introduced with Pinus spp. (Guzmán and Varela 1978) in Antioquia, Caldas, and Cundinamarca.

Cantharellaceae: the species Cantharellus cinereus was previously reported by Vasco-Palacio and Franco-Molano (2013), but was not included in this checklist, since the study by Guzmán and Varela (1978) did not report it.

Gomphales: Species in the genus Ramaria are reported both as ectomycorrhizal and saprotroph (Humpert et al. 2001; Tedersoo et al. 2010). We include in the checklist the species R. cyaneigranosa whose mycorrhizal status was confirmed by Nouhra et al. (2005); it belongs to the subgenus Laeticolora characterized by a terricolous habit (Humpert et al. 2001). Other species included in the checklist (Table 16.1) belong to the subgenera Ramaria (R. botrytis, R. secunda, R. flava) and the subgenus Laeticolora (R. formosa), have terricoluos habit, and are suggested to be mycorrhizal (Humpert et al. 2001; Hobbie et al. 2002; Smith and Read 2008). In contrast, the saprotrophic species Ramaria stricta grows on wood debris (Hosaka et al. 2006), belongs to a phylogenetic clade of lignicolous taxa (Humpert et al. 2001), and is not included in the checklist.

3.2.2 Ascomycota

Pezizales: Within this order several species are expected to form ectomycorrhizal symbiosis including species in the genera Humaria, Genea, Trichophaea, Geopora, Helvella, Hydnotria, Peziza, and Sarcosphaera (Tedersoo et al. 2006). The species Peziza patena has been reported in Colombia by Vasco-Palacios and Franco-Molano (2013), but there is no specific data on its distribution or host.

3.3 Notes on Other Orders

Geastrales: According to the studies referenced by Rinaldi et al. (2008) and the phylogenetic analysis by Hosaka et al. (2006), we did not included Geastrum as ECM.

Trechisporales: Dunham et al. (2007) observed some traits that characterize ECM formation in species from the genus Trechispora. In Colombia, eight species of this genus are reported, but they were not included here; further analyses on the trophic status must be made for this particular genus.

3.4 Edible Ectomycorrhizal Fungi in Native Oak Forests

Regarding our search on previous reports on edibility of wild fungi, 37 ectomycorrhizal species associated with Q. humboldtii forests in the Andean mountains in Colombia are potentially edible (Table 16.1). Among them, some are locally reported as edible for the department of Boyacá: Ramaria secunda and Lacifluus indigo by Ruíz and Henao-Mejía (2006), Tylopilus indecisus, Ramaria flava, R. cyaneigranosa, R. botrytis, and the other five species of Ramaria by Peña-Cañon and Henao-Mejía (2014), Lactifluus deceptivus (pers. comm. Yeina Niño Fernández, March 2014) and Russula cyanoxantha (pers. comm. Angélica Ruíz, May 2012).

Given that the native oak forests provide environmental benefits and services, their maintainance and protection are vital (Chaves et al. 2007). Encouraging public awareness on the importance of fungal diversity and its conservation, in localities where its edibility is traditionally known, might allow a sustainable production. In countries such as the United States, and some countries in Europe, conservation activities have been proposed based on the impact of intense harvesting of edible mushrooms over long time periods (Pilz and Molina 2002).

4 Concluding Remarks

The conservation of ectomycorrhizal fungi associated to oak ecosystems is a priority, regarding that oak forests suffered habitat loss, rare fungal species are associated with this host, and a potential use of ECM species is known. Moreover, ectomycorrhizal fungi play a key role in sequestering carbon in soils (Soudzilovskaia et al. 2019), hence their conservation and restoration might be one strategy to act on when considering actions for climate change mitigation.

Following the evaluation criteria provided by the Micheli Guide to Fungal Conservation (http://www.fungal-conservation.org/micheli.htm), in this report we accomplished the following citeria: mentioning ECM fungi in a conservation context, listing departments in the Colombian Andes where ECM fungal species occur with native Q. humboldtii, and showing different regions in the Andean cordillera where there is a lack of knowledge on fungal diversity and where exploration of ECM diversity should be enhanced.