Termites are soil-living arthropods that cause serious losses to most dryland
crops, including rainfed upland rice (Wood and Cowie, 1988).
They dig underground tunnels with minimum connection to the above-ground environment
(Noirot and Darlington, 2000) through which they reach
and attack host plants. Since the major constituent of the diet of termites
is cellulose, they can cause damage directly in many ways to the host (Femi-Ola
et al., 2007; Kumar and Pardeshi, 2011).
In Africa, most of the termite species that cause serious damage to crops belong
to the subfamily Macrotermitinae (Wood et al., 1980).
In the dry and semi-arid tropics, many food and industrial crops and many forest
trees are attacked by termites leading to economic losses. In general, the level
of damage depends on termite species and population size. It can also depend
on the susceptibility of the host plants. Factors such as drought, cellulosic
food availability, soil aeration and soil moisture stability increase the proliferation
of Isoptera. Also, the presence of biotic and abiotic elements in the ecosystem
plays a major role in the abundance and distribution of termites (Bong
et al., 2012). Aslam et al. (2000)
report that the presence of termites in a region depends on the vegetation type.
Taking into account this basic knowledge from previous research, the present
study investigated the biodiversity of termites in an upland rice ecosystem,
including seeking to establish the periods of their occurrence and the level
of damage inflicted on rice varieties. Many studies report high levels of damage
due to termites on upland rice (Heinrichs and Barrion, 2004;
Nwilene et al., 2008; Agunbiade
et al., 2009), but the species responsible are not indicated in all
cases. Knowledge of termite diversity associated with upland rice and the exact
situation concerning their damage will constitute an important base for better
control of these pests. Furthermore, information on the occurrence of each species
would be crucial for deciding the appropriate period of applying control measures
against these insects.
MATERIAL AND METHODS
Site of experiment: The experiment was carried out in Niaouli (Benin), identified as a hot spot for termites. This site is characterized by bimodal rainfall with an average annual of 1200 mm per year. The main rainy season runs from March to July and the short rainy season from September to November. The soil is a ferralitic upland that is sandy in its upper horizon (0-25 cm) and clayey in the lower horizon (25-50 cm). The vegetation type is Guinean humid savannah covered with monocotyledons and dicotyledonous weeds, with some forest trees.
Planting techniques: Ten upland rice varieties - 7 NERICA varieties (1, 2, 3, 4, 6, 7 and 10), one Oryza glaberrima (CG14, African parent of the NERICA lines), two Oryza sativa (WAB56-104, Asian parent and LAC23, a variety resistant to many biotic stress) were sown at random on individual plots separated from each other by a 2-m alley.
The varieties were sown at a plant spacing of 20x20 cm, and gaps were filled at 7 days after emergence. Three seedlings per hill were kept throughout the experiment. A basal dose of NPK (15-15-15) at a rate of 150 kg ha-1 was applied before sowing. A top-dressing of urea (50 kg ha-1) was applied twice during the weeding periods at 21 and 42 Days After Sowing (DAS). The experimental design was a randomized complete block with three replications.
Sampling of population and damage parameters: Termite populations and damage were sampled at three phenological stages of rice: tillering (40 DAS), heading (60 DAS) and maturation (90 DAS). Population sampling was carried out in two environments - (1) the rice field and (2) the surrounding natural savannah-while damage was recorded only in rice plots.
In rice plots, five sampling points 0.5 m apart were chosen following plot diagonals. Holes of 0.25x0.25 m (0.06 m2) surface area were made between hills. For each new sampling period new holes were dug a few centimeters from the previous sampling points. Damage sampling consisted of harvesting 10 hills within the rice plot. For selected hills, all plant organs were checked to identify termite species and their damage.
The sampling in natural savannah consisted of evaluating the termite populations in the landscape surrounding the experimental field. Sampling holes of 0.25x0.25 m (0.06 m2) surface area were dug at random in the delimited space at the same time as the field sampling. A distance of 2 m was maintained between holes.
The extracted soils were placed in plastic bags for laboratory investigation, during which termite species were separated and conserved in vials containing 70% alcohol.
Identification of termites species: Termites species were identified
in the laboratory using several identification methods (Sands,
1965; Harris, 1968; Pearce et
Data collection and statistical analysis: The specific diversity in
both rice field and natural savannah was calculated from the diversity index
formula established by Simpson (1949):
where, S represents the number of termite species (species richness), N represents the total population and n represents the total number of individuals per species.
This index is negatively correlated with the diversity, i.e. diversity is higher
when D = 0 and lower when D = 1. From this formula we can calculate the Derived
Index of Simpson (Es) as:
Mean termite population per plot was analyzed by analysis of variance (ANOVA)
with SAS statistical software 8.2 (SAS Institute, 2002).
Significant differences between termite populations were compared by the Student
Newman-Keuls (SNK) test at 5% probability level.
Six termite species were identified namely: Microtermes sp., Microcerotermes parvus Haviland, 1898; Pseudacanthotermes militaris Hagen, 1858; Amitermes evuncifer Silvestri, 1912; Trinervitermes oeconomus Trägardh, 1904 and Macrotermes bellicosus Smeathman, 1781. These species belong to the family of Termitidae and the subfamilies Macrotermitinae, Termitinae and Nasutitermitinae (Table 1).
Specific diversity and abundance of termites: The abundance and diversity of termite species varied across infested environments and according to phonological stage of rice.
Six termite species were recorded in the rice field, while four species were found in the natural savannah (Table 2). The termite population was also denser in the rice field than in the natural savannah. In rice, six species of termite were observed at tillering and heading stages, while five species were inventoried at maturity. The specific diversity was greater at heading stage (D = 0.23; Es = 0.77) than at tillering (D = 0.31; Es = 0.69) and maturity stages (D = 0.34; Es = 0.66) (Table 3).
At tillering stage six termite species were present on rice. While NERICA 10
and NERICA 6 had the highest specific richness of termites (5 species), population
densities on these varieties were moderately low (3.8 and 7.9 individuals per
sampling hole, respectively).
|| Termite species found in upland ecology at Niaouli, Benin
|| Termite specific diversity in rice field and natural savannah
|| Termite specific diversity in each stage of rice phenology
|| Population of termites on rice varieties at tillering stage
The lowest specific richness was found on WAB56-104 (3 species), but the total
density on this variety was moderately high (14.1 individuals per sampling hole).
The dominant species were M. parvus, followed by P. militaris
and Microtermes sp. (Table 4).
|| Population of termites on rice varieties at heading stage
|Means followed by the same letter are not significantly different
at the 5% level according to SNK test
|| Population of termites on rice varieties at maturity
|Means with the same letter are not significantly different
at the 5% level according to SNK test
At heading stage, six termite species were present on rice, but the specific diversity and density differed considerably among rice varieties. However, the populations of the various termite species increased (compared to tillering stage) on all varieties except WAB56-104 and LAC23 (Table 5).
Finally, at maturity stage the density of termites was greater than at the two earlier stages but at that stage only five species infested rice (Table 6). Microtermes sp. was by far the most abundant species overall. It was followed by M. parvus and A. evuncifer. Populations of P. militaris and M. bellicosus were less important at this stage.
Mode of attack and damage on rice: The site of termite attack was highly dependent on the species of termites (Table 7). In most of the cases, the presence of a specific termite species was coincident with evidence of severe damage on rice, but in a few cases the termite was present without the associated damage. The occurrence of termite species varied according to rice phenological stages and the symptoms of damage were specific for each type of termite.
Microtermes sp. occurred at all phenological stages, but its damage
was very low at the beginning of the crop growth cycle and gradually increased
to maturity stage, except NERICA 10 and CG14 on which species peaked at heading.
The species was found in the ground especially in the rhizosphere (root area).
|| Termite damage localization and plant status
|Damage level: - = low or nothing; + = medium; +++ = high
The damage was primarily cutting of roots and making tunnels along the stems.
The tunnels were often filled with soil. The attack was more frequent on wilted
and dry plants.
Microcerotermes parvus was also found at all cropping stages. Its damage increased from tillering to maturity. It was not only found in the rhizosphere, but also on the dried plants. Its damage was either stem cutting, especially on the collar leaving characteristic furrows at the end of the stems, or root cutting and making tunnels along the stems. Its attack was particularly evident on wilted and dried plants and a little on fresh seedlings.
Amitermes evuncifer was uniformly present in the rice field throughout the growth period. It was often found in built nests or in underground galleries. It was also found in the nest of T. oeconomus. Its presence was strongly associated with damage, recognized by black furrows inside the infested organs (stems or roots). The attack also took place outside the stem especially on the external cortex of the collar.
Pseudocanthotermes militaris was present in the field throughout the cropping cycle, but its population was abundant only at tillering and heading stages. This species was also found in the soil surface (without apparent nests) as well in underground horizon. Its presence in the field was rarely associated with damage. Dried grasses (in natural savannah) and lodged rice stems were primarily infested and damage was minor on normal rice plants. In a few cases, small furrows were observed on the base of rice seedlings without any serious impact.
Trinervitermes oeconomus was present in the field at low densities from tillering to heading, and absent at maturity stage. An abundant colony of this species was found in a nest built 10-30 cm above the soil. It was also seen in small groups in underground galleries. Its presence was not related to any serious damage. Only a few furrows were noted on the stems, leaves and panicles, leaving small openings on these organs without any severe consequences. Some nests were built next to rice hills creating a physical constraint to seedling growth.
Finally, M. bellicosus, like the previous species, was present at low density in the field throughout the cropping cycle. However, its presence was very often associated with damage. Indeed, in the infested hills, all the stems were cut on the side of the collar. The infested seedlings lodged and dried out.
The study revealed the presence of six species of termite in the rice field
and only four species in the natural savannah. All the species found in natural
savannah were found on rice. This suggests that field infestation can originate
from natural savannah. Akpesse et al. (2008)
reports that termites found in natural vegetation are able to colonize crops
and fruit trees. Litsinger et al. (1987) found
that termites have some preference for rice over perennial vegetation. This
could explain the greater diversity of termites in the rice field than in the
natural environment. Among the species collected on rice, the fungus-growing
termites (Microtermes sp. and P. militaris) and the dry-wood termites
(M. parvus and A. evuncifer) were the most abundant. These termites
constitute the main part of soil macrofauna attacking dryland crops (Akpesse
et al., 2001). The establishment of their colonies in cropping areas
should be favored by the availability of food that promotes the termites
activity (Kumar and Pardeshi, 2011). Microtermes
sp., A. evuncifer and P. militaris have been identified on rice
in Côte dIvoire (Akpesse et al., 2008),
while M. bellicosus, Microtermes sp. and T. oeconomus have
been found on rice in Nigeria (Harris, 1969; International
Institute of Tropical Agriculture, IITA, 1971; Malaka,
1973). Also, most of the species recorded in our study have also been found
on other tropical crops such as yam and cassava (Atu, 1993),
sugar cane (Sands, 1977), groundnut (Johnson
and Gumel, 1981), sorghum (Logan et al., 1990),
maize (Wood et al., 1980; Akpesse
et al., 2008), as well as many forest trees (Anani
Kotoklo et al., 2010).
Microcerotermes parvus and P. militaris were the most abundant
species at tillering stage, M. parvus, A. evuncifer, P. militaris
and Microtermes sp. the most abundant at heading stage, and Microtermes
sp., M. parvus and A. evuncifer were the most common at maturity.
The termite population was not very important at the beginning of the cropping
cycle (tillering), but increased during heading and maturity stages, probably
because of the abundance of the cellulosic resources (wilted and dried plants)
in that period. Agunbiade et al. (2009) report
that termites attack living rice when dead material is not available. Heinrichs
and Barrion (2004) explain that termites are attracted by plants being stressed
by biotic or abiotic factors such as drought, diseases and nutrient deficiency.
Microtermes sp. appeared to be the dominant and most harmful species
at maturity. Indeed, this species builds underground nests located in the deep
soil horizon (Wood, 1996), where it stores food to feed
a growing population over a long period of time.
All of the rice varieties were infested by the six termite species, but the specific densities were different among varieties. NERICA 6, CG14, NERICA 10 and NERICA 3 were less infested even at maturity, while NERICA 4 and LAC23 were heavily infested at maturity.
The attack modes of termite species were also specific. The three most harmful
species were Microtermes sp., M. parvus and A. evuncifer.
These species are known to be responsible for major damage on dryland crops
(Akpesse et al., 2008). Their attack is commonly
made on roots and stems. The attack of P. militaris and M. bellicosus
was sporadic and very low. Trinervitermes oeconomus had no effect on
upland rice, contrary to what is reported by Wood and Cowie
(1988) on its role in rice damage.
Finally, it is important to know that termites can be secondary pests on plants that are primarily stressed by other biotic or abiotic constraints. So, not all the damage met in the field is caused by termites.
This study has identified the main termite species that attack upland rice. A total of six species was found on rice against four in the natural savannah. The dominant species were xylophagous termites (fungus-growing termites and dry-wood termites). The specific diversity varied not only according to the environment, but also according to rice phenological stage. These results can be useful to undertake targeted measures against key termite species.