ORIGINAL ARTICLE

Mycorrhizal colonization and species of arbuscular mycorrhizal fungi in grasses from the Cuenca Pecuaria “El Tablón”, Cienfuegos, Cuba

Colonización micorrízica y especies de hongos micorrizógenos arbusculares en gramíneas de la cuenca pecuaria “El Tablón”, Cienfuegos, Cuba

E. Furrazola,^I L. Ojeda,^II Consuelo Hernández,^III

ABSTRACT

The presence of arbuscular mycorrhizae and communities of arbuscular mycorrhizal fungi (AMF) associated to four grasses established in areas of livestock basin “El Tablón”, belonging to the Estación Experimental "Escambray", Cumanayagua municipality, Cienfuegos province, was determined. Megathyrsus maximuss cv. Likoni, Pennisetum purpureum cv. king grass, Brachiaria decumbens cv. CIAT-606 and Cynodon nlemfuensis vc. Jamaicano grasses were evaluated. A random block design was applied, with four treatments and 15 repetitions. All species showed arbuscular mycorrhizal colonization. The highest value was obtained in Brachiaria decumbens vc. CIAT-606, with 66.27%, while the rootlets of Pennisetum purpureum vc. king grass showed the lowest levels of this variable, with 48.80%. Eight species and five morphotypes of AMF, belonging to eight genera, were observed. The highest density of mycorrhizal fungi spores was associated with Pennisetum purpureum cv. king grass, with 3399 spores/100 g of soil, while the lowest corresponded to Brachiaria decumbens cv. CIAT-606, with only 195 spores/100 g. Arbuscular mycorrhizal  fungi communities were more populated by species belonging to Glomus genus in the four studied pastures.

Key words: pastures, arbuscular mycorrhizae, spore density, morphotype.

RESUMEN

Se determinó la presencia de micorrizas arbusculares y de comunidades de hongos micorrizógenos arbusculares (HMA) asociadas a cuatro pasturas establecidas en áreas de la cuenca pecuaria “El Tablón”, perteneciente a la Estación Experimental “Escambray”, municipio de Cumanayagua, provincia de  Cienfuegos. Se evaluaron las gramíneas Megathyrsus maximuss vc. Likoni, Pennisetum purpureum vc. king grass, Brachiaria decumbens vc. CIAT-606 y Cynodon nlemfuensis vc. Jamaicano. Se aplicó diseño de bloques al  azar, con cuatro tratamientos y 15 repeticiones. Todas las especies mostraron colonización micorrízica arbuscular. El mayor valor se obtuvo en Brachiaria decumbens vc. CIAT-606, con 66.27 %, mientras que las raicillas de Pennisetum purpureum vc. king grass mostraron los menores índices de esta variable, con 48.80 %. Se observaron ocho especies y cinco morfotipos de HMA, pertenecientes a ocho géneros. La mayor densidad de esporas de hongos micorrizógenos estuvo asociada a Pennisetum purpureum vc. king grass, con 3399 esporas/100 g de suelo, mientras la más baja correspondió a Brachiaria decumbens vc. CIAT-606, con solo 195 esporas/100 g. Las comunidades de hongos MA estuvieron dominadas por especies pertenecientes al género Glomus en las cuatro pasturas  estudiadas.

INTRODUCTION

Arbuscular mycorrhizae are an important biological factor for the structure and functioning of soils and influence on the ecological performance, productivity and composition of natural plant communities (van der Heijden et al. 1998) and crops and forest plantations. Fungi forming arbuscular mycorrhizae should be considered as part of the biological diversity of soils and should be included on inventories and biodiversity analyzes at ecosystem and agro-ecosystem level.

As root symbionts, arbuscular mycorrhizal fungi (AMF) are essential components of soil microbial communities, improve its structure, (Piotrowski et al. 2004) help raise the plant productivity (Lekberg & Koide 2005), increase resistance to pathogens (Sikes et al. 2009), and improve water amounts in soil (Neumann & George 2004). These fungi facilitate nutrient uptake and stress tolerance, help the formation of stable aggregates of soil and improve dynamic phosphorus and carbon in the rhizosphere.

Sustainable production of pastures in the tropics is limited by the fragility of soils, which undergo several forms of degradation. Making a better use of these beneficial symbionts may contribute to the increase of sustainability (Pérez et al. 2011). For this purpose, Velez & Sanchez (2015) developed an experiment that combined chemical fertilizers, green manures (Canavalia ensiformis L. and Axonopus scoparius F.), compost and mixture of the latter two in growing white corn to check the performance of mycorrhizae under these conditions. These authors confirmed the highest length, external mycelium activity and percentage of colonization per arbuscules the root system of maize with the addition of green manures mixed with compost, which were inhibited by industrial chemical fertilization.

 In a study conducted in Brazil, to evaluate the association between AM fungi and four native grasses (Axonopus affinis, Paspalum notatum, Andropogon lateralis and Aristida laevis) under phosphate and nitrogen fertilization, Ramos (2014) concluded that the A. laevis and A. lateralis species showed the highest mycorrhizal dependence, while both fertilizations reduced the percentage of mycorrhizal colonization of the least dependent species of mycorrhizae (A. affinis and P. notatum). The number of spores in the soil was not affected by the addition of N and P.

In Cuba, there have been several efforts to demonstrate the positive effect of AMF inoculation on nutrition and productivity of grasses and forage crops (González et al. 2006, Calderón & González 2007). Therefore, it is important to know which AMF species are naturally associated with our grass species. However, there are few studies of AM fungi diversity related to grasses, under the geographical conditions of Cuba.

Monroy et al. (2013) determined that there are 26 morphotypes of AM fungi, in a study with Brachiaria brizantha cv. Toledo, B. dictyoneura cv. Plainsman, Desmodium ovalifolium cv. Maquenque, Panicum maximum (CIAT 36000) and Paspalum notatum as cover of grasses and legumes established in oxisol soils burrowing foot mountain in citrus orchards in Villavicencio, Colombia.

The objective of this study was to define the presence of arbuscular mycorrhizal colonization and species of these fungi, associated with Megathyrsus maximuss cv. Likoni, Pennisetum purpureum cv. king grass, Brachiaria decumbens cv. CIAT-606 and Cynodon nlemfuensis cv. Jamaican. All with more than five years of establishment.

MATERIALS AND METHODS

This research was conducted at the Vaquería Laboratorio Número. 3 from the Estación Experimental “Escambray”, belonging to Empresa Pecuaria “El Tablón”, Cumanayagua municipality, Cienfuegos province. These facilities are locates at 591.00- 260.00 N and 259.00- 250.00 E, in Barajagua cartographic sheet 1: 25 000. The soil is grey brown (Hernández et al. 2015). Table 1 shows some components of soil fertility. 

The study was conducted with a random block design, with four treatments (grass species), 15 replicates (samples) and the following grasses:

1. Megathyrsus maximuss cv. Likoni

2. Pennisetum purpureum cv. king krass

3. Brachiaria decumben cv. CIAT-606

 4. Cynodon nlemfuensis cv. jamaicano

In order to quantify mycorrhizal variables, samples of rootlets were extracted from each species. Therefore, root systems and ryzhospheric soil, associated to a depth of 0-10 cm, were collected. They were dried at the air and they were stored in plastic bags until their processing in the laboratory. Rootlets with less than 2 mm of diameter were washed and cut at around 1 cm. they were dyed with trypan blue, according to the method of Phillips & Hayman (1970).

The percentage of arbuscular mycorrhizal colonization (% MC) was calculated according to the methodology of Giovannetti & Mosse (1980). This procedure consisted on distributing 1.5 g of dyed roots at random over a Petri dish of 8 cm of diameter. The bottom of the dish showed a drawing of a reticule of squares of 0.5 inches (1.27cm). An amount of 100 intersections of roots with lines of this reticule were counted. An amount of 100 intersections with this reticle lines were counted. In each Petri dish, the count was carried ou in three parallel lines. The observed presence of AMF at each intersection represented the mycorrhizal colonization of the root. The intensity of fungal occupation was expressed as percentage of visual density (%VD) and was calculated according to the methodology of Herrera et al. (2004). The scale for assessing the percentage of VD was:

zero: absence of AMF

one: 1 % of visual density

two: 2.5 %

three: 15.5 %

four: 35.5 %

five: 47.5 %

For identifying the associated AMF grass species, 100 grams of soil were taken in each species and mixed with typical soil of the area, which was previously sterilized in an autoclave at 1.5 atmospheres for one hour. Sorghum forage, as indicator crop (trap plants) was sown in pots of 1 kg. Irrigation stopped at four months and the plants were slowly dried for fifteen days. Spores associated with these pastures were quantified using the method of wet sieving and decanting (Gerdemann & Nicolson 1963).

Taxonomic descriptions were performed according to Błaszkowski (2012) and consultation of the specimens was conducted in the Herbarium of the Academy of Sciences, located at the IES-CITMA, where there are more than 3,000 samples of glomeromycetes fungi and a collection of 24,000 images. The results were analyzed by ANOVA of simple classification. When F was significant, the measures were compared according to the multiple range test of Duncan (1955).

RESULTS AND DISCUSSION

All samples of rootlets showed features belonging to the presence of mycorrhizal fungi, being arbuscular or vesicles, typical of this symbiotic association. The two main types of arbuscular mycorrhizal colonization were the Arum-type and Paris-type, illustrated and described by Gallaud (1904). These names correspond to the plants where they were observed for the first time: Arum maculatum L. and Paris quadrifolia L., respectively (Dickson et al., 2007). It is considered that these two types represent the extremes of a structural continuum that characterizes the internal morphology of this association. The type of mycorrhization observed in this study corresponded to the Arum type, which predominates in cultivated species, although, according to the cited authors, both types of mycorrhizal colonization can be observed in grasses.

The highest value of mycorrhizal colonization was found in the Brachiaria decumbens cv. CIAT-606 species, which statistically differed from the rest of the tested species, while Pennisetum purpureum cv. king grass had the lowest percentage of rootlets colonized by the AMF (table 2).

The species Brachiaria decumbens cv. CIAT-606 also had the most visual density of the endophyte in their rootlets, no differences regarding Megathyrsus maximus cv. Likoni. Meanwhile, Cynodon nlemfuensis cv. Jamaicano presented the lowest values of this variable, significantly different from the rest of the evaluated species.

Arbuscular mycorrhizal colonization showed no common pattern on the different studied plant species, as it commonly happens in tropical and temperate ecosystems, because it is known that it depends essentially on the habit of the plant and on environmental conditions (Allen 2001).

According to this author, colonization percentage is a value derived from the growth of two independent organisms, which are different and each tries to maximize their own growth and survival. Therefore, the colonization of roots by AMF depends on two main factors. First, soil resources, essentially phosphorus and nitrogen related to the carbon obtained by the plant, and the mycorrhizal inoculum within the soil, due to its level, composition and distribution. Previous studies have demonstrated that levels of mycorrhizal colonization vary among genotypes of plants within the same species (Tawaraya 2003).

Mycorrhizal colonization values, superior to 50 % and observed in three out of four studied plant species, may be considered as high, according to criteria of Ferrer & Herrera (1980). Nevertheless, in general, these values were considered as moderate, according to criteria of Alarcón (2001), because these species grow under natural conditions in soils with low levels of phosphorus, organic matter and fertility, and it is known that, under these conditions of field, mycorrhizal propagules are not potentiated as well as when mycorrhizal inocula under controlled experimental conditions are used.

In this research, mycorrhizal colonization was evaluated as a result of the presence of thin and thick hyphae.  The value of these last was slightly superior to 40 %, at up to 15 cm deep, while thin hyphae colonized around 30 % of rootlets. The values of visual density obtained in this study are slightly superior to those obtained by Fundora et al. (2011), Terry et al. (2013), who performed AMF inoculations with bio-products and/or chemical fertilization in sown grasses, which varied between 0.34 % and 2.39 %.

Regarding the presence of AMF species, there were eight species and five morphotypes of these fungi, belonging to eight genera: Cetraspora, Claroideoglomus, Dentiscutata, Diversispora, Funneliformis, Glomus,  Paraglomus and Racocetra (table 3).

In a general sense, there were between four and six species associated to each studied pasture, with a predominance of species and morphotypes of Glomus genera (figure 1), although Diversispora spurca produced higher values of propagules in Pennisetum purpureum,Guínea. Likoni and Cynodum nlemfuensis cv. Jamaicano, with 2,033, 325 and 226 spores per 100 g, respectively. Diversispora spurca and Claroideoglomus claroideum were the most important species to be considered for further studies on inoculation, because they were associated to roots of 3 and 2 studied pastures, respectively.

On the other hand, Pennisetum purpureum cv. king grass reproduced the highest number of AMF spores associated to its rootlets, followed by Megathyrsus maximuss cv. Likoni, Cynodum nlenfuenses cv. Jamaicano and Brachiaria decumbens cv. CIAT-606.

AMF are an important part of herbaceous agricultural systems (Sabais et al. 2012, Gibson-Roy et al. 2014). These fungi have equally been used in ecosystem re-vegetation programs, affected by anthropic, as in the case of degraded grasslands (Gao & Guo 2010).

Native communities of AM fungi, associated to grasslands, have been studied by Schnoor et al. (2010), and Busby et al. (2012). The first authors found 38 phylotypes, from which 29 belonged to Glomus A, six to Glomus B and six to Diversisporaceae. The second authors observed 32 species. They found, as in the present study, Claroideoglomus claroideum, Diversispora spurca and Paraglomus occultum species among them. This significant number of species is a result of, besides the traditional isolation techniques of spores from the soil (trap plants and direct counting of spores after centrifugation in sucrose gradient), molecular determinations conducted for fungal communities in roots and soil plus roots in both studies, respectively. Generally, the predominance of Glomus genus was confirmed in these studies, with a similar performance to this study.

Lugo & Cabello (2002) found higher presence of Glomales order, among the 17 species analyzed in the rhizosphere of five grasses associated to mountain grasslands in Sierras de Córdoba. Results of this study coincide with reports of Schnoor et al. (2010), who determined 38 endophyte organisms of AM fungi, associated to Festuca brevipila and Plantago lanceolata, in an experiment for restoring grasslands in the western region of Scania, south of Sweden. From those organisms, 35 belonged to Glomus genus.

As in this study, species of Glomus genus are generally predominant in the communities of AM fungi in agricultural soils from Europe (Mathimaran et al. 2005). Among other reasons, this could be a result of a mechanism of the spores of this genus to repair those damages experienced by hyphae in fungal colonies of soil. According to the cited authors, this mechanism for repairing damages in hyphae varies among Gigaspora, Scutellospora and Glomus genera. In this last, this phenomenon increases the ability of fungus to colonize the roots of the host plant due to proliferation of new hyphae from the apex of the cut hypha. However, it could also reconnect the affected area by the re-connection of several hyphae in a relatively small neighborhood. This mechanism acquires particular importance in soils under agricultural management, due to the disturbance provoked by soil management to fungal colony of these fungi.

It is not surprising the fact that the highest spore density in the soil was associated to Pennisetum purpureum cv. king grass, although this species presents the lowest value of mycorrhizal colonization. Similar results were obtained by Camargo & Dhillion (2002) and Li et al. (2007), because spore production levels do not have necessarily to reflect the abundance of AM fungi within the roots. It is also known that sporulation rates of AM fungi depend on the host (Bever et al. 1996), so it is logical to find different densities of spores per each studied host. Likewise, the different strategies of AM fungi colonization is related to its taxonomical differences at fungal genera level, so each isolation of these fungi show great differences, regarding the degree in which they colonize plant roots (Hart & Reader 2002).  For instance, Aster amellus L., which was an obligated mycotrophic plant species, showed 5 % of mycorrhizal colonization, which is enough to establish an effective mycorrhizal association (Pánková et al. 2008).

It can be concluded that all the species showed arbuscular mycorrhizal colonization. The highest value was observed in Brachiaria decumbens cv. CIAT-606, with 66.27 %, while rootlets of Pennisetum purpureum cv. king grass showed the lowest values of this variable with 48.80 %. There were 13 species and/or morphotypes of AMF. The highest density of spores of mycorrhizal fungi was associated to Pennisetum purpureum cv. king grass, with 3,399 spores/100g of soil, while the lowest value belonged to Brachiaria decumbens cv. CIAT-606, with only 195 spores/100g. AMF communities were dominated by the presence of species from Glomus genus.

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Received: 2/10/2014
Accepted: 15/6/2016

E. Furrazola, Instituto de Ecología y Sistemática. Ministerio de Ciencia, Tecnología y Medio Ambiente. Carretera Varona 11835 e/ Oriente y Lindero, La Habana 19, CP 11900, Calabazar, Boyeros, La Habana, Cuba. Email: eduardof@ecologia.cu