Exp Appl Acarol (2014) 64:309–319 DOI 10.1007/s10493-014-9828-5
Population dynamics of Aceodromus convolvuli (Acari: Mesostigmata: Blattisociidae) on spontaneous plants associated with Jatropha curcas in central Brazil Wilton P. Cruz • Renato A. Sarmento • Marc¸al Pedro-Neto • Adenir V. Teodoro • Diego M. Rodrigues • Gilberto J. de Moraes
Received: 5 December 2013 / Accepted: 5 June 2014 / Published online: 19 June 2014 Ó Springer International Publishing Switzerland 2014
Abstract Spontaneously growing plants are commonly considered competitors of cultivated plants. Owing to the lack of specificity of many arthropods, spontaneous plants may be attacked by the same arthropods that attack cultivated plants and they may also harbor natural enemies of organisms harmful to cultivated plants. Aceodromus convolvuli Muma (Blattisociidae) has been reported recently in relatively large numbers in Tocantins state, central Brazil, mostly on Helicteres guazumifolia Kunth (Malvaceae). Very little has been reported about the population dynamics of blattisociid mites under field conditions. The objective of this work was to study the population dynamics of A. convolvuli in Gurupi, Tocantins state, to evaluate its possible interaction with associated mites. Monthly samples were taken from leaves of the 11 most abundant and frequent spontaneous plants in a Jatropha curcas L. (Euphorbiaceae) plantation. About 96.5 % of the specimens of A. convolvuli were collected in the rainy season. The patterns of variation of the population of A. convolvuli and of predators belonging to the family Phytoseiidae were similar, but A. convolvuli was much more numerous than all phytoseiid specimens combined. Highly
W. P. Cruz R. A. Sarmento (&) M. Pedro-Neto Universidade Federal de Tocantins (UFT), PO Box 66, Gurupi, State of Tocantins, Brazil e-mail:
[email protected] W. P. Cruz G. J. de Moraes Programa de Po´s-graduac¸a˜o em Entomologia Agrı´cola, Universidade Estadual Paulista Ju´lio de Mesquita Filho, UNESP, Jaboticabal, State of Sa˜o Paulo, Brazil A. V. Teodoro Embrapa Tabuleiros Costeiros, Av. Beira Mar 3250, PO Box 44, Jardins, Aracaju, State of Sergipe, Brazil D. M. Rodrigues Departamento de Cieˆncias Agra´rias, Universidade Federal do Para´ (UFPA), Maraba´, State of Para´, Brazil G. J. de Moraes Departamento de Entomologia e Acarologia, Escola Superior de Agricultura ‘‘Luiz de Queiroz’’, Universidade de Sa˜o Paulo (ESALQ/USP), Piracicaba, State of Sa˜o Paulo, Brazil
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significant correlations were observed between A. convolvuli densities and relative humidity or diversity of spontaneous plants. When only mites on H. guazumifolia were considered, highly significant correlation was also observed between densities of A. convolvuli and of mites of the family Tetranychidae. The results suggested that A. convolvuli could be a predator of tenuipalpid and/or tetranychid mites. Studies about its biology are needed to determine its preferred food sources and potential as biological control agent. Keywords
Ecology Predation Biological control Blattisociid mite
Introduction Spontaneously growing plants are often considered competitors of cultivated plants, able to reduce the yield of the latter, being in those cases referred to as invasive plants or weeds. Because of the lack of specificity of many arthropods, spontaneous plants may be attacked by the same arthropods that attack cultivated plants and could thus serve as reservoirs of pest organisms. However, they may also harbor natural enemies of organisms that are harmful to cultivated plants (Altieri et al. 2003; Bellini et al. 2005). The main mites of the order Mesostigmata found on plants are predators belonging to the family Phytoseiidae. Some species of this family are considered to be important to the control of several plant pests (McMurtry and Croft 1997; Gerson et al. 2003). Much less common on plants are the members of the family Blattisociidae, which were previously included in the family Ascidae (Lindquist and Evans 1965; Halliday et al. 1998; Lindquist et al. 2009). Several blattisociids have been mentioned to prey on arthropods (Gerson et al. 2003; Lindquist et al. 2009). Aceodromus Muma is a mite genus originally included in Phytoseiidae (Muma 1961) and later transferred to Blattisociidae (Lindquist and Chant 1964). Aceodromus convolvuli Muma was described from specimens collected in Florida, United States of America, on leaves of Convolvulus sp. (Muma, 1961). It was later reported by Lindquist and Chant (1964) in Jamaica on leaves of eggplant and Crotalaria sp., and by Fadamiro et al. (2009) in Alabama, USA, on unidentified plants in citrus orchards. Aceodromus convolvuli was first reported in Brazil by Moraes et al. (1993), on spontaneous plants growing in several states of the northeastern part of the country. It was also reported on coffee in Sa˜o Paulo State, Brazil (Mineiro et al. 2006). More recently, A. convolvuli was reported from Tocantins state, in central Brazil, in a study conducted by Cruz et al. (2012) on the mite fauna of physic nut Jatropha curcas L. (Euphorbiaceae) and associated spontaneous plants. Jatropha curcas has been considered for extended cultivation in several tropical countries, mainly for biodiesel production (Openshaw, 2000). In the work conducted by Cruz et al. (2012), 1,141 specimens of A. convolvuli were collected on samples of 11 species of spontaneous plants. About 69 % of those specimens were found on Helicteres guazumifolia Kunth (Malvaceae). This plant has been reported from southern Mexico to the central region of Brazil, in open, secondary and semideciduous forests, gallery forests, pastures, zones of periodic fires and clearings, dry or moist thickets and grassy or bushy slopes (Goldberg 2009). In Venezuela, this plant has been reported mainly in open habitats with dry, sandy and rocky soils (Rondo´n and CumanaCampos 2007).
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The objective of this work was to conduct an analysis of the population dynamics of A. convolvuli, based on the samplings conducted by Cruz et al. (2012), evaluating its possible interaction with the associated mites on those 11 spontaneous plant species. This work is one of the rare efforts to evaluate the population dynamics of species of the ascid sense Lindquist and Evans (1965). Apparently, the only other study of this type refers to the blattisociid Lasioseius parberlesei Bhattacharyya in Taiwan (Tseng 1984), where it was considered an effective predator of Steneotarsonemus spinki Smiley (Tarsonemidae) on rice. Thus, not much can be anticipated in terms of the response of A. convolvuli to the varying climatic factors, or in terms of its possible natural prey. However, as other blattisociid mites have a preference for humid environments, we anticipated that the same occurs with A. convolvuli.
Materials and methods The data used for the analysis presented here were collected in the study conducted by Cruz et al. (2012). The work involved the evaluation of A. convolvuli and associated mite species on spontaneous plants from a 4-year old cultivation of J. curcas of about 0.5 ha, in Gurupi (11°480 2900 S, 48°560 3900 W; 280 m altitude), Tocantins state, in a subtropical region with well defined rainy (November–April) and dry (May–October) seasons. The natural vegetation of this locality is classified as ‘‘Cerrado’’, a very diverse savannah type of biome covering slightly over 20 % of the Brazilian territory, where annual rainfall ranges between 800 and 2,000 mm, but with a pronounced dry season (Ratter et al. 1997). The experimental field was mainly surrounded by pasture (mostly Brachiaria sp., Poaceae), except for one side, edging an area of natural vegetation. The height of the spontaneous plants varied from about 15 cm (dry season) to about 120 cm (wet season). They were not controlled during the conduction of the study or in the previous year. No fertilization or pesticide spray was done during the study or in the period of 2.5 years before it started (Cruz et al. 2012). Mite sampling Samples were taken from 15 sites (9 m2 each) randomly delimited within the experimental field. Eleven plant species were selected for the evaluations, based on their abundance and frequency in the area (Cruz et al. 2012). The selection was done by counting the plants of each species within two quadrats (0.25 m2) randomly thrown in each sampling site (Mueller-Dombois and Ellenberg 1974; Cruz et al. 2012). Selected species were those with abundance of at least 2.5 plants per quadrat and which were present with a frequency of at least 10 % of the quadrats. The same selected plant species were sampled throughout the work, regardless of the variation in their abundance or frequency along the time. Identification of spontaneous plants was conducted with the use of a manual (Lorenzi 2006) and the help of M. Ignacio, a botanist. The selected plants were: Fabaceae—Calopogonium mucunoides Desv.; Lamiaceae—Hyptis suaveolens (L.) Poit.; Malvaceae—Peltaea riedelii (Gu¨rke) Standl., Sida urens L., Sida cordifolia L., Sida rhombifolia L., Urena lobata L., H. guazumifolia, Waltheria americana L.; Poaceae—Andropogon gayanus Kunth and Urochloa mutica (Forssk.) T.Q. Nguyen (Angiosperm Phylogeny Group 2009). The diversity of spontaneous plants was estimated at each sampling date by calculating the Shannon–Wiener (H0 ) index with DIVES software version 2.0. Sampling of spontaneous plants for diversity estimation was conducted using the methodology proposed for Mueller-
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Dombois and Ellenberg (1974), described above. Subsequently, the spontaneous plants’ richness and abundance were obtained. The samples were collected once between the 20th and 25th of each month, from February 2010 to January 2011. At each sampling date, 10 (Fabaceae, Lamiaceae and Malvaceae) or 20 (Poaceae) leaves of each selected plant species present in each sampling site were collected, constituting a sample. Thus, for each species, the number of samples taken at each sampling date varied according to its respective frequency at that sampling date, for a minimum of two and a maximum of 11 samples. The leaves of each species from each sampling site were placed in a plastic bag that in turn was placed in a cool box (about 20 °C) and transferred to the laboratory, where they were maintained in a refrigerator (about 10 °C) for up to 5 days, until examined under a stereomicroscope. For quantification and identification, mites were mounted in Hoyer’s medium; however, when a certain species was too abundant, the mites were counted and only part of the specimens was mounted for confirmation of the identification. Identification of mite species was carried out by the third and the last authors, using the original descriptions and relevant complementary descriptions of the species of each group. Leaf area was estimated at each sampling date. Climatic data (daily temperature, relative humidity and rainfall) were obtained from ‘‘Estac¸a˜o Meteorolo´gica de Gurupi (INMET)’’, at Universidade Federal do Tocantins campus, about 20 km from the experimental site. The analyses were conducted by taking into account monthly average temperature and relative humidity and monthly total rainfall, in all cases for the period preceding each sampling date (i.e., the most recent monthly reading was taken). Statistical analysis To estimate the main factors related to the fluctuation of A. convolvuli throughout the work, data distribution was initially checked with Shapiro–Wilk normality test, using the Shapiro.test function procedure of R program. Since many of the variables did not have normal distribution, Spearman’s test was used to determine simple correlations between variables (population densities of A. convolvuli, phytoseiids, tetranychids and tenuipalpids, as well as indexes of plant diversity, rainfall, relative humidity and temperature). This was done with the use of the Spearman’s rank correlation (rho) function procedure or R program. A multiple regression analysis relating the population densities of A. convolvuli with the variables showing significant simple correlation with densities of A. convolvuli and not related among themselves was performed, using ‘‘model’’ of R to obtain the coefficients of the function and Summary (model) to determine the level of significance of the variables and of the model as a whole, and R2 of the model (R Development Core Team 2006).
Results A re-examination of the mites collected showed the need to correct or complement the identification reported in Cruz et al. (2012), as indicated in Table 1. Relation between Aceodromus convolvuli and environmental factors in rainy and dry seasons Considering all plants together, about 96.5 % of the specimens of A. convolvuli were collected in the rainy season (Table 2). In the dry season, that species was only found on H.
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Table 1 Correction and complementation of the identification of the mite species reported by Cruz et al. (2012), based on a re-examination of the specimens Reported by Cruz et al. (2012)
Corrected identification
Tetranychidae Mononychellus sp. Panonychus sp.
Mononychellus planki (McGregor) Neotetranychus granifer Feres & Flechtmann
Phytoseiidae Neoseiulus aff. mumai Neoseiulus fallacis
Neoseiulus benjamini (Schicha) Neoseiulus pluridentatus Lofego & Moraes
Phytoseiulus sp. Typhlodromalus clavicus
Phytoseius guianensis De Leon Amblydromalus sp.
guazumifolia and C. mucunoides, at very low numbers. Total rainfall, average temperature and average relative humidity were 964 mm, 26 ± 0.6 °C and 80 ± 1.1 % in the wet season, and 80 mm, 26 ± 1.6 °C and 59 ± 3.9 % in the dry season, respectively. Dynamics of Aceodromus convolvuli on all spontaneous plants When all spontaneous plant species were considered together, the densities of A. convolvuli increased between February and April, when the maximum level was reached (Fig. 1a). Densities reduced drastically to nearly zero in June, remaining so until September; it again increased progressively but slightly until November, remaining about the same level until next January. The pattern of variation of the phytoseiid population was similar, except that the decline of the population after reaching a peak density in April was more gradual. Among other mite groups, the highest densities were attained by the Tydeoidea (including Tydeidae and Iolinidae), which peaked in March, followed by the Tetranychidae and the Tenuipalpidae, both reaching the maximum level in June (Fig. 1b). The highest densities of A. convolvuli and phytoseiids coincided with the highest levels of plant diversity and with the end of the rainy season (Fig. 1c). Highly significant correlations were observed between the densities of A. convolvuli and phytoseiids, as well as between the former and plant diversity indexes (Table 3); significant correlations were observed between A. convolvuli densities and relative humidity. No significant correlation between A. convolvuli densities and any of the remaining independent variables was observed. Owing to the significant correlations between phytoseiid densities and plant diversity as well as between levels of relative humidity and plant diversity (Table 3), the latter parameter was not included in the multiple regression analysis. In that analysis, the only significant factor of the generated equation corresponded to phytoseiid densities, and the coefficient of determination (R2) of the equation was 0.78. Dynamics of Aceodromus convolvuli on Helicteres guazumifolia The patterns of variation of the densities of A. convolvuli and phytoseiids were similar to those when all spontaneous plant species were considered together (Fig. 2a). However, the peak population density of A. convolvuli was much higher, while that of the phytoseiids was only slightly higher. Differently from what was observed when all plants were considered together, densities of Tydeoidea were low during the whole observation period
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Table 2 Seasonal occurrence of Aceodromus convolvuli on spontaneous plants, in the dry and rainy seasons, in Gurupi, Tocantins state, Brazil, from February 2010 to January 2011 Spontaneous plants
Dry season (May–October)
Helicteres guazumifolia
Rainfall season (November–April)
Total
38
746
784
Calopogonium mucunoides
2
135
137
Sida urens
0
48
48
Ureda lobata
0
41
41
Waltheria americana
0
41
41
Andropogon gayanus
0
23
23
Hyptis suaveolens
0
19
19
Sida cordifolia
0
18
18
Urochloa mutica
0
16
16
Peltaea riedelii
0
8
8
Sida rhombifolia
0
6
6
40
1,101
1,141
Total
(Fig. 2b). Among the remaining mite groups, the highest levels were attained by the tetranychids and the tenuipalpids, also in June, being these about twice as high as determined for all plants together. Yet, variations in the populations of mites other than A. convolvuli and phytoseiids were much more erratic than observed when all plants were considered together. Significant correlations (Table 3) were observed between A. convolvuli densities and phytoseiid densities, tetranychid densities, relative humidity, and plant diversity. No significant correlation was observed between the remaining independent variables with A. convolvuli densities. Because of the significant correlations between phytoseiid and tetranychid densities, phytoseiid densities and plant diversity, relative humidity and plant diversity, and tetranychid densities and plant diversity (Table 3), the multiple regression analysis included only phytoseiid and tenuipalpid densities, temperature and rainfall. Similarly to what was determined when all spontaneous plant species were considered together, the only significant factor of the generated equation was phytoseiid densities, and the coefficient of determination of the equation was 0.58.
Discussion The analyses of the numbers of A. convolvuli in each of the two distinct seasons prevailing in Gurupi as well as of the dynamics of each variable along the evaluation period suggested a strong influence of rainfall and relative humidity on the densities of A. convolvuli. The significant correlation between the population level of A. convolvuli and the levels of relative humidity confirmed that assumption, but the non-significant correlation between the first parameter and rainfall seemed not to support it. This apparent contradiction could be due to the non-linear relation between A. convolvuli population densities and rainfall; in this sense, there might be a minimum rainfall threshold level below which A. convolvuli is about uniformly and negatively affected, independent of the amount of rain. Hence, absence or incidence of very low rainfall between May and September resulted in very low
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Fig. 1 Population densities of Aceodromus convolvuli and associated mite species on all sampled plants as well as monthly mean levels of plant diversity and abiotic parameters, in Gurupi, Tocantins state, between February 2010 and January 2011
levels or total absence of A. convolvuli in the study area. In addition, the sudden occurrence of high rainfall after the dry season was not followed by a corresponding proportional increase in A. convolvuli population levels, possibly because of a natural time lag required for the food sources (possibly prey organisms) of A. convolvuli to increase with increasing rainfall, which would then allow the subsequent increase of the population of the latter.
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Table 3 Significant correlations between the population densities of Aceodromus convolvuli and biotic and abiotic factors as well as between other combinations of factors for all spontaneous plants and on Helicteres guazumifolia alone, in Gurupi, Tocantins State, Brazil, from February 2010 to January 2011 Factors
Spontaneous plants
Helicteres guazumifolia
r
r
P
P
Phytoseiidae
0.93
0.000009
0.80
0.002
Plant diversity
0.92
0.00001
0.87
0.0002
Relative humidity
0.66
0.01
0.71
0.01
Tetranychidae Phytoseiidae 9 plant diversity
Tetranychidae 9 plant diversity
0.01 0.0007
0.87
0.003
0.83 0.78
0.03
0.60
0.04
0.61
0.04
0.61
0.03
Phytoseiidae 9 Tetranychidae Relative humidity 9 plant diversity
0.66
Fig. 2 Population densities of Aceodromus convolvuli and associated mite species on Helicteres guazumifolia, in Gurupi, Tocantins state, between February 2010 and January 2011
With the onset of the dry season, the sharper decline of A. convolvuli population in comparison with the phytoseiid population suggest the former to be more sensitive to lower humidity than the latter. This pattern would be expected, as members of Ascidae sensu lato
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Lindquist and Evans (1965) are usually found on aerial plant parts only in regions of prevailing high levels of relative humidity. In a study conducted in northeastern Brazil, Rodrigues et al. (1996) determined the significant level of association A. convolvuli with several other mites and plants. They determined the association to be negative with the phytoseiid Neoseiulus (=Amblyseius) idaeus Denmark & Muma and positive with the phytoseiid Amblydromalus (=Typhlodromalus) manihoti (Moraes), species that predominate respectively under conditions of low and high humidity levels (Moraes et al. 1990). As commonly observed in areas of the Cerrado vegetation, the region where the study was conducted has marked alternations of very dry and very humid seasons. Thus, the prevalence of A. convolvuli during part of the year in Gurupi leads to the conclusion that it has an efficient mechanism to allow survival in the dry season, though at very low population levels (Cruz et al. 2013). Faunistic surveys on leaves of cultivated plants or plants of the natural vegetation have usually shown outstandingly higher abundance of phytoseiids in comparison with other mesostigmatid mites. Thus, the finding of a larger population density of A. convolvuli in comparison with that of all phytoseiid species combined is uncommon, deserving detailed analysis. A question to be answered is why A. convolvuli is so abundant in the region where the study was conducted. Among other reasons, the relatively high abundance could be related to the presence of H. guazumifolia, onto which A. convolvuli was by far the most common Mesostigmata. However, in which way the plant affects the mite could not be determined, because of the absence of information about its biology. The higher proportion of A. convolvuli than of phytoseiids was not related to a conceivable more intense surveying effort on this plant, as at each sampling date the examined leaf area of that plant species corresponded to only about 20 % of all examined leaves. Although not rare, H. guazumifolia was not one of the most common plants considered in this study. It was only the eighth on the list of the most abundant, with a patchy distribution in the study area. This species is a shrub whose leaves are covered by starshaped trichomes, under which A. convolvuli were found. Those structures seem to offer some protection to the predators, as suggested by the fact that it was rather difficult to collect them with a brush during the evaluations. Several factors have been related to the presence of trichomes, including the maintenance of lower temperature on the leaf surface, protection from the effect of UV light and the retention of a thicker boundary layer of higher relative humidity over the leaf surface (Wagner et al. 2004; Coder and Warnell 2013). These characteristics might favor A. convolvuli. As reported by Ordaz et al. (2011), several studies have been conducted on the morphology, phenology, ecology and biochemical characteristics of H. guazumifolia, a plant of medicinal importance in South America. Characteristics about patterns of nectar production, morphology of floral nectaries, nectar composition and hummingbird association were reported by Goldberg (2009). The chemical composition of essential oils of leaves of H. guazumifolia was studied by Ordaz et al. (2011). The authors reported that the predominant compounds were non-terpenoid volatile secondary metabolites. The role of alternative food such as nectar and secondary compounds to the predominance of A. convolvuli on H. guazumifolia in this study has not been determined. To our knowledge this is the first study of the mite fauna of this plant. Considering the possibility of using A. convolvuli for the control of pest organisms, future studies should include detailed evaluations on its accepted food sources. The results of the present study suggest that items to be investigated should include tetranychid and tenuipalpid mites. The relatively low correlation between the densities of A. convolvuli and tetranychids as well as the non significant correlation between the densities of A.
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convolvuli and tenuipalpids might not necessarily indicate that they do not interact. Instead, that could be a function of a complex predator–prey interactions, with non-synchronous population fluctuations, and/or due to the concurrent confusing effect of other environmental factors. The inverse patterns of variation of A. convolvuli and tenuipalpids graphically distinguishable between February and June further supports this possibility, with an increase in the population level of the former being followed by a (slower) reduction of the population of the latter during the end of the rainy season, and an inverse trend at the onset of the dry season, which, as previously discussed, seems to disfavor A. convolvuli. Detailed studies of predator–prey interactions should be stimulated, especially in areas where mites have been barely investigated, as in central Brazil. These may lead to the discovery of new prospective biological control agents of this relatively little known group of mesostigmatid mites. Considering that another blattisociid mite, Lasioseius lindquisti Nasr & Abou-Awad, has been reported to develop and reproduce when offered pollen of Phoenix dactylifera as food source (Momen et al. 2011), pollen of H. guazumifolia should also be investigated as a possible food source for this mite. Acknowledgments The authors thank the National Council for Scientific and Technological Development (CNPq) for financial support (Projects 620028/2008-4 and 475408/2008-0) and Coordination of Improvement of Higher Education Personnel CAPES-Brazil for providing scholarships to the first and third authors (Projects: PROCAD-NF and CAPES-PNPD). We thank M. Ignacio (Universidade Federal do Tocantins, Brazil) for help with the identification of part of the plants collected in this study.
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