Diversity and community composition of

nematode communities in horticultural and

banana crops

Diversidad y composición de la comunidad de nemátodos

en cultivos hortícolas y banano

William E. Rosas Carrera

Jiménez Feijoó M.I.

Piedrahita Piedrahita P.M.

Álava Hidalgo E.I.

Abstract: Horticultural and musaceous crops are of great economic

importance in Ecuador. Although there are studies on the association

of phytopathogenic nematodes and the damage they cause, little

research has been done on the diversity and composition of nematodes

in these crops. The present study evaluates the diversity, composition

and abundance of the nematode community related to soil

physicochemical characteristics, reports Shannon H' diversity and

nematode community structure, based on their trophic groups,

colonizer-persistent (c-p) community structure and maturity index

(MI). This work presents results from soils in horticultural and banana

plantations in the provinces of Azuay (highlands), El Oro and Guayas

(coast), respectively. The results showed average organic matter

(OM%), temperature (T°C) and humidity (H%) variables with

significant differences (P<0.05) between sampling regions. No

organisms of the mycophagous trophic group were found throughout

the study. Genera such as Tylenchus, Helycotylenchus and

Pratylenchus, represented more than 50% of the total of those

collected. However, a notable difference was observed in the

predatory trophic group, with a higher abundance in the coastal region

than in the highlands. In general, the Costa and Sierra growing regions

had a considerable impact on abundance and physicochemical

variables. Climate had an important effect on the distribution and

diversity of nematodes, including those of the predatory trophic

group. The abundance of the herbivore trophic group could be

mediated by the presence of the predator trophic group.

Keywords: Nematode, diversity, abundance, structure, trophic

Resumen: Los cultivos hortícolas y de musáceas representan una

gran importancia económica para el Ecuador. Aunque existen

estudios sobre la asociación de nemátodos fitopatógenos y los

perjuicios que causan, poco se ha investigado sobre la diversidad y

composición de nemátodos en dichos cultivos. El presente estudio

evalúa la diversidad, composición y abundancia de la comunidad de

1 Veterinary Zootechnician, UNIVERSIDAD

AGRARIA DEL ECUADOR: Guayaquil, Guayas,

EC, https://orcid.org/0000-0002-1128-6062,

wrosas@uagraria.edu.ec

2 PhD , Escuela Superior Politécnica del Litoral:

Guayaquil, Guayas, EC, https://orcid.org/0000-

0002-1961-5123, mjimenez@espol.edu.ec

3 PhD (Animal Behaviour), Escuela Superior

Politécnica del Litoral: Guayaquil, Guayas, EC,

https://orcid.org/0000-0002-4403-6326,

ppiedra@espol.edu.ec

4 Ph.D. (Agronomy), Escuela Superior Politécnica

del Litoral: Guayaquil, Guayas, EC,

https://orcid.org/0000-0002-8910-0926,

eialava@espol.edu.ec

Published

Instituto Tecnológico Superior Edwards

Deming. Quito – Ecuador

Periodicity

January-March

Vol. 1, Num. 21, 2024

pp. 57 .-77

http://centrosuragraria.com/index.php/revista

Dates of receipt

Received: December 10, 2023

Approved: February 26, 2024

Correspondence author

wrosas@uagraria.edu.ec

Creative Commons License

Creative Commons License, Attribution-

NonCommercial-ShareAlike 4.0

International.https://creativecommons.org/lice

nses/by-nc-sa/4.0/deed.es

Diversity and community composition of nematode communities in horticultural and banana crops

nemátodos relacionado con las características físico-químicas del

suelo, reporta la diversidad de Shannon H’ y la estructura de la

comunidad de nemátodos, a partir de sus grupos tróficos, estructura

de la comunidad colonizadores – persistentes (c-p) e índice de

madurez (IM). Este trabajo presenta resultados de suelos en

plantaciones hortícolas y de banano en las provincias del Azuay

(sierra), El Oro y Guayas (costa) respectivamente. Los resultados

demostraron promedios en las variables materia orgánica (MO%),

temperatura (T°C) y humedad (H%) con diferencias significativas

(P<0.05) entre las regiones de muestreo. No se encontraron

organismos del grupo trófico micofago en todo el estudio. Géneros

como Tylenchus, Helycotylenchus y Pratylenchus, representaron más

del 50% del total de las colectadas. Pero se pudo observar una notable

diferencia del grupo trófico predador con una abundancia mayor en la

región Costa que en la Sierra. En general, las regiones de cultivo Costa

y Sierra tuvieron un impacto considerable en la abundancia y

variables físico-químicas. El clima presento un efecto importante en

la distribución y diversidad de nemátodos, entre ellos los del grupo

trófico predador. La abundancia del grupo trófico herbívoro pudo

verse mediada por la presencia del grupo trófico predador.

Palabras clave: Nemátodo, diversidad, abundancia, estructura,

trófico

Introduction

Nematodes are among the highest proportion microorganisms as they

account for 80% of multicellular organisms and are also localized in

most terrestrial ecosystems (Bardgett and Van Der Putten, 2014;

Eisenhauer and Guerra, 2019; van den Hoogen et al., 2019).. They are

considered model organisms for understanding soil ecology due to their

trophic behavior and life form (Liu, Hu and Li, 2019). To understand

this ecology, there are tools among which are the study of the diversity

and composition of nematodes (Yan et al., 2021). From this community

structure of nematodes based on their diversity and genus composition,

the behavior of nematode trophic groups during winter seasons has been

studied, but more research is still required (Girgan et al., 2021).. Even

to measure their diversity and composition, variables such as height

above sea level, temperature, humidity, crop type (short cycle or

perennial) and even the level of intensive agriculture, are considered

indicators of community structure (Dong et al., 2017; Emery et al.,

2017)..

April - June vol. 1. Num. 21 - 2024

This specific study of nematode communities has proven to be of great

importance, both to know the richness of these microorganisms in

megadiverse countries such as Ecuador or for the correlation of crop

productivity with the different species that inhabit the soil (Altamirano-

Benavides and Yanez-Moretta, 2016; Fan et al., 2020).. Depending on

the trophic group, nematodes can be considered indicators on soil

quality in crops. Since depending on the species composition, they

provide indirect soil information. (Ney et al., 2019). Hence, nematode

community structure in soil is important for the ecological functioning

of agroecosystems and are a fundamental part in agricultural

sustainability (Sánchez-Moreno et al., 2018).. They detect an imbalance

in the correct biotic structure due to the use of pesticides, fertilizers,

crop rotation, perennial crops, among others (Sánchez-Moreno, 2018).

Among the soils that present the ideal characteristics for the

investigation of nematode diversity are soils with musaceous and

vegetable crops. These are among the most important and economically

interesting crops worldwide as well as a great source of nutrients (Dias,

2012; Pareek, 2015; Brown et al., 2017; Campos and Caligari, 2017)..

These crops can be affected by phytopathogenic nematodes that are

considered as pest organisms of horticultural crops (Parvatha, 2013).

However, for the control of these pests, intensive use of pesticides is

seen to be necessary especially in conventional crops (do Amaral et al.,

2018), affecting the nutritional characteristics in crop products. This use

of pesticides would be justified by the high infestation of nematodes in

crops and the need for effective chemical spraying for the control of this

or other types of pests (Greco et al., 2020). This is why crop

management has a direct effect on soil biology and can be used as an

indicator for proper crop management (Pattison et al., 2020). (Pattison

et al., 2018).. Crops in which different communities can be found either

by their intensive use or even by the location where they are found.

In this research work, an analysis of the diversity and species

composition of nematode species is carried out (Moreno and Talavera

M., 2013). (Moreno and Talavera M., 2013).The objective was to

describe the existing communities of nematodes in horticultural and

banana crops in two zones, the highlands and the coast, respectively.

Diversity and community composition of nematode communities in horticultural and banana crops

Materials and methods

The localities correspond to the Sierra and Costa climatic zones. In the

Sierra region, soil samples were obtained from horticultural crops in the

town of San Joaquín in the city of Cuenca, Azuay province. While in

the coastal region, soil samples were collected from musaceous crops

in the localities of El Triunfo, Naranjito, Puerto Inca and Naranjal in

the province of Guayas, as well as Pasaje in the province of El Oro and

La Troncal in the province of Cañar, Ecuador, as shown in Figure 1.

Figure 1. Map showing the location of the sampling points in the study

area.

The study was developed during the months of February to May 2019.

The study sites were randomly selected present in the locations

mentioned above, this due to the economic importance of the crop in

each region (Maffei et al., 2016).. Soil samples were taken in each farm,

at the same time field interviews were conducted consisting of

questions related to fertilizer management, water source, crop rotation

and pest treatment. The crops were also selected according to their

commercial interest due to the wide diversity of nematodes that use

these plants as hosts and the level of damage they can cause by infecting

the crops (Sivasubramaniam, Sivasubramaniam, et al., 2000).

April - June vol. 1. Num. 21 - 2024

(Sivasubramaniam, Hariharan and Zakeel, 2020).. The crops tested in

the Sierra region were: garlic (Allium sativum), cabbage (Brassica

oleracea Capitata group), broccoli (Brassica oleracea Italica group),

lettuce (Lactuca sativa), carrot (Daucus carota), artichoke (Cynara

cardunculus Scolymus group). In the coastal region, banana (Musa

AAA) was used. In all cases, plantations at different stages of

development were evaluated.

A total of 21 soil samples representing each of the crops sampled were

collected. Twelve subsamples were taken from each sampling site, to

obtain a composite and homogeneous sample of approximately 600 g.

Soil samples were taken at a distance of 10 cm to 30 cm from the base

of the stem at a depth of 20 cm to 30 cm and transported in plastic bags

to the laboratory. The samples were stored in coolers to protect them

from sunlight. Soil properties analyzed included soil temperature (T°C),

percent moisture (H%), pH and soil organic matter (OM). To obtain

OM, 100 g of soil (out of approximately 600 g) were sent to and

analyzed in the soil laboratory of the School of Mechanical Engineering

and Production Sciences, Escuela Superior Politécnica del Litoral,

Gustavo Galindo Velasco campus. Soil T°C and H% were measured

using a ProCheck portable data receiver and reader and a GS3 sensor.

The pH was analyzed using a Luster Leaf 1847 Rapitest Digital Plus

Soil pH Meter.

Nematodes were extracted from 200 g of fresh soil from the initial

sample, divided into 2 extraction trays with 100 g each. The method

used for the extraction of nematodes from the soil was the modified

Whitehead trays (Whitehead and Hemming, 1965). (Whitehead and

Hemming, 1965). It consists of a filter that was placed directly over the

trays containing the water. The bottom of the filter was presented in

such a way as to allow the soil to be completely wetted, then incubated

for 48 hours. The collected suspension was filtered using a 230 mesh

sieve and placed in a conical polypropylene tube. The nematodes in

suspension were selected and sorted using a stereomicroscope.

Nematode abundance was measured as individuals per 200 g of soil.

After extraction, the sediment was transferred to Petri dishes where the

total number of nematodes per sample was counted with a BOECO

model BST-606 stereo-zoom-microscope. Subsequently, the

individuals were fixed with the use of formalin glycerin (40%

formaldehyde 10 ml - Glycerin 1 ml - Distilled water 89 ml) and

subsequent mounting of each individual in the object-holder plates. The

nematodes in each sample were counted with the aid of a motorized

Diversity and community composition of nematode communities in horticultural and banana crops

research microscope OLYMPUS model BX63 and identified by genus

(Bongers, 1989; Hunt, 1989). (Bongers, 1989; Hunt, 2008a, 2008b,

2008c; Andrássy, 2010) and then classified into bacterivore, plant

parasite (herbivore), omnivore and predator feeding groups based on

Yeates et al. (1993). In addition, nematodes were classified into the

persistent colonizers group (cp1 - cp5) as an indicator of ecosystem

structure and function (Bongers, 1990a; De Goede, Bongers and

Ettema, 1993; Yeates et al., 1993)based on the successional state and

functioning of the nematode community in soil (Bongers, 1990b; Ferris,

Bongers and De Goede, 2001)..

Identification was based on examination of the caudal 'tail' and cranial

'head' limbs of each organism, primarily the cranial retractile points

'mouth; denticles; stipe; stoma; internal, dorsal, and ventral teeth',

length and shape of the esophagus, characteristic parts of some genera

(van Wyk and Mayhew, 2013).. In addition, genus-specific taxonomic

keys were used, based on scientific papers on nematode identification

(Odontopharynx and Man, 1989; Bostroêm, 1991; Vovlas, 1992;

Mahato, 1997; Ahmad and Shaheen, 2004; Jana, Chatterjee and Manna,

2008; Tahseen and Rajan, 2009; Andrássy, 2010; Nusrat, Anjum and

Ahmad, 2013; Shokoohi et al., et al., 2013, 2016; Carta and Skantar,

2014; Inserra et al., 2014; Alvarez-Ortega et al., 2016; Kolombia et al.,

2017; Leduc and Zhao, 2017; Phani et al., 2018; Sikora, 2018; Kanzaki,

Ekino and Masuya, 2019)..

The following nematode community indices were calculated: genus

richness, nematode abundance, c-p community structure and IM

maturity index were calculated based on data obtained using the

program NINJA (Sieriebriennikov, Ferris and de Goede, 2014)..

Diversity was calculated using the Shannon-Wienner index (H') which

confers greater weight to uncommon species. It allows the nematode

community to have a very even abundance distribution. In addition, it

minimizes the specific diversity of nematodes in small samples such as

the vegetable crops sampled (Krebs, 1999). (Krebs, 1999).

𝐻

= #𝑝

𝑙𝑜𝑔𝑝

"$%

Where the factor S corresponds to the number of species (species

richness), pi the proportion of individuals of species i with respect to

April - June vol. 1. Num. 21 - 2024

the total number of individuals, ni the number of individuals of species

i, and N the number of all individuals of all species.

ANOVA analysis of variance was performed to compare the difference

(P<0.05) of the results throughout the study and thus observe the effects

of physicochemical variables with diversity indices, nematode

abundance and maturity indices. Significant differences in main effects

were analyzed by paired comparison using Tukey's test. All statistical

tests were performed using InfoStat statistical software version

2020I(www.infostat.com.ar).

3. Result

An average abundance of 29 nematodes was found in the coastal region,

while in the sierra region it was higher with an average of 107

nematodes. Of the total of 29 genera of nematodes in the herbivorous,

omnivorous, predatory and bacterivorous trophic groups, the genera

with the greatest number of individuals were Tylenchus,

Helycotylenchus and Pratylenchus, both in samples of horticultural

crops and bananas. In horticultural crops, the genera Helycotylenchus,

Tylenchus and Pratylenchus had the highest number of individuals with

488, 436 and 111 individuals, respectively. In banana crops, the genus

Helycotylenchus and the genus Radopholus also had the highest

number of individuals with 163 individuals in both cases, while the

genus Tylenchus had 103 individuals. All genera belong to the

herbivorous trophic group.

As shown in Figure 2, no genera of the fungivore trophic guild were

found. In the two sampling regions, only the averages of the bacterivore

(Coast: 7.46 ± 1.47, Highlands: 0.69 ± 1.28) and predator (Coast: 14.01

± 2.85, Highlands: 1.66 ± 2.47) guilds showed significant differences

(P<0.05). Two ranges of significance were found for both the

bacterivore and predator trophic groups.

Diversity and community composition of nematode communities in horticultural and banana crops

Figure 2. Abundance in percentage of the total average of nematodes

of four trophic groups of the sampling regions Coast with horticultural

crops and Highlands with banana crops (individuals per 200 g of soil).

All values are means + ES, n = 21. Letters A, B indicate significant

differences between treatments (Tukey's test α = 0.05).

Of the percentages of c-p structure of free-living nematodes, only c-p1,

c-p2 and c-p4 presented significant differences (P<0.05) with the

following averages according to sampling zone: C-p1 (Coast: 32.16 ±

6.48, Sierra: 0.64 ± 5.62); c-p2 (Coast: 9.44 ± 2.47, Sierra: 0.80 ± 2.14)

and c-p4 (Coast: 45.88 ± 11.94, Sierra: 81.89 ± 10.34). Regarding the

range of significance for the c-p percentages, each region was grouped

in different ranges. The MI, H' and the c-p3 - c-p5 structure did

not present significant differences in their averages (P<0.05) in this

study.

April - June vol. 1. Num. 21 - 2024

Table 1. Abundance of soil nematodes (dominant and frequent genera,

trophic groups), physicochemical variables and ecological indices for

the study of the nematode community. Values are shown with mean and

standard error (mean±SE).

Parameter

Coastal Region

Sierra Region

Banana Crops

Horticultural Crops

Abundance of the most prominent genres

Helycotylenchus

18.11±10.58

40.67±9.17

Tylenchus

11.44±9.82

36.33±8.51

Pratylenchus

8.00±4.06

9.25±3.51

Physical-chemical variables

6.33±0.14

6.55±0.12

MO%1

3.39±0.38A

8.58±0.33B

T°C1

30.56±0.22B

20.78±0.19A

H%1

4.95±0.91A

21.42±0.79B

Shannon Index H'

1.38±0.13

1.13±0.11

Maturity index IM

2.82±0.43

3.30±0.37

C-p11

32.16±6.48B

0.64±5.62A

Diversity and community composition of nematode communities in horticultural and banana crops

C-p21

9.44±2.47B

0.80±2.14A

C-p3

7.41±4.81

0.00±4.16

C-p41

45.88±11.94A

81.89±10.4B

C-p5

5.13±2.83

0.00±2.45

1Values followed by different letters in the same row represent a

significant difference according to Tukey's test (α = 0.05).

The physicochemical variable pH did not show significant differences

(P<0.05) in the sampling zones. On the other hand, organic matter,

temperature and humidity did show significant differences in the two

sampling regions, as shown in Table 1. Temperature is positively

related to diversity, while humidity and organic matter are reflected in

diversity, such is the case that it is related to the regions sampled, since

the significant differences in the averages of the Coast region show that

the lower the percentage of humidity, the better the diversity in

comparison with the humidity of the Sierra region where humidity is

higher but diversity is lower than in the Coast region.

The lower diversity of nematodes in horticultural crops in the Sierra

region compared to the diversity of banana crops in the Costa region

may be due to the altitude of this region. As reported by studies on

species richness, at higher altitudes, species richness generally

decreases, as is the case with most of the soil fauna (McCain and

Grytnes, 2002). (McCain and Grytnes, 2010; Vittoz et al., 2010;

Mumladze et al., 2015).. Contrary to this statement according to K

ergunteuil et al. (2016)., both diversity and abundance of nematodes

increase with altitude. Although nematode abundance is indeed higher

in horticultural crops in the Sierra region compared to banana crops in

the Costa region, diversity is not. It is deduced then that the type of

short-cycle crops such as vegetables does not allow the complete life

cycle of persistent species such as predatory nematodes. In addition, the

increase in H% observed (21%) in the Sierra region is related to the

abundance of nematodes, especially the abundance of herbivorous

species. This is due to the higher frequency and amount of rainfall in

April - June vol. 1. Num. 21 - 2024

the Sierra region (Todd, Blair and Milliken, 2000). (Todd, Blair and

Milliken, 1999; Landesman, Treonis and Dighton, 2011).This is mainly

due to the flow of water in the crop irrigation system, data obtained

from the interviews conducted.

According to work done by. W ardle & Yeates, (1993) and Zhao &

Neher, (2014) concerning competition in food webs and soil energy

pathways, at higher altitude conditions, enhances the flow of fungal

energy within ecosystems. Despite not having found fungivorous

genera, it is believed that they could be present, but in a minimal

amount, perhaps due to the lack of fungivorous organisms that have

been controlled by genera such as Tylenchus spp. and Iotonchus spp.

Species of these genera would also feed on fungi and not only on plants

as reported by certain studies (Okada et al., 2002; Tsuda & Futai, 2000).

Regardless of the region, type of crop or type of management, the

genera of herbivorous nematodes were more abundant, thus

demonstrating their phytopathogenic potential as pests. Even for the

control of phytophagous nematodes such as those of the genus

Tylenchus, Helycotylenchus, Pratylenchus and Radopholus, found in

greater numbers in this study, could justify the possible use of

agrochemicals on crops. Even this trophic group of herbivorous

nematodes could displace other trophic groups due to the abundance

that would occupy space for other organisms as is the case of predatory

nematodes that are important as biological control (Chen et al., 2013).

The values obtained for H' diversity do not represent an optimal

diversity (Shannon H' diversity greater than 2), possibly due to the type

of perennial crop such as musaceae, since they present low organic

carbon inputs from plant residues, as stated by B engtsson et al. (2005).

The relationship between diversity H' with the percentage of humidity,

as well as T (°C) and MO may be due to the climate factor of the

sampling zones, which would indicate greater diversity in the coastal

region compared to the Sierra region. Authors such as Gillingham et al.

(2012) and Suggitt et al. (2011) mention the influence of temperature

directly on the distribution of species, including nematodes, according

to the characteristics of the habitat, which is reflected in the relationship

between temperature and the study areas. Likewise, the results obtained

in relation to temperature and organic matter are related to those

obtained by other studies (Bhusal, Tsiafouro, and others). (Bhusal,

Tsiafouli and Sgardelis, 2015; Kergunteuil et al., 2016; Traunspurger et

al., 2017; Varela Benavides, 2018)where they indicate the importance

Diversity and community composition of nematode communities in horticultural and banana crops

of nematodes in the decomposition of organic matter that could be

higher in areas located at higher altitudes, where temperature is the key

factor to understand this relationship.

Finally, the results obtained on the number of nematodes found in class

c-p4, which refers to nematode genera with a long life cycle, larger and

very sensitive to disturbances, generally encompasses predatory and

omnivorous nematodes (Bongers, 1990a). (Bongers, 1990a). These

results indicate more complex trophic networks in the Sierra region

with short cycle crops than in the Costa region with musaceous crops,

which determines a stability in the nematode community and therefore

soil conservation, giving similar results presented in studies of

nematode community structure in agroecosystems with agroecological

crops (Salas and Achinelly, 1990a). (Salas and Achinelly, 2020)..

4. Conclusions

Differences in the abundance and diversity of nematodes were highly

dependent on the region and its humidity and temperature variables,

together with organic matter, which can have an important effect on the

distribution of nematodes and even on the infestation of herbivorous

nematodes. The abundance of predatory nematodes may be controlled

by the type of short-cycle crop and moist climatic conditions. However,

these conditions can be beneficial for nematodes of the herbivorous

trophic group. The use of nematodes as an environmental indicator

seems to be more promising depending on climatic conditions and crop

type, but they certainly help to understand soil ecology in crops.

Acknowledgments

To the VLIR NETWORK ECUADOR, To Ph.D. Denisse F. Peña,

coordinator of the Molecular Biology Laboratory, Universidad de

Cuenca, Yanuncay Campus, for providing me with all the facilities in

the use of microscopes and digital camera. To the analyst in charge of

the Agrolab agricultural laboratory, Ing. María Landre Jama Ochoa and

all her collaborators for their assistance in the laboratory and field work.

Eduardo Francisco Chávez Navarrete, director of the ESPOL soil

laboratory, as well as the analysts Eduardo Gutiérrez and Martha

Hidalgo, for their technical assistance. Aquiles Javier Delgado Elias for

his collaboration in soil sampling in musaceae crops.

April - June vol. 1. Num. 21 - 2024

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