Acessibilidade / Reportar erro
Article • Bragantia 80 • 2021 • https://doi.org/10.1590/1678-4499.20190459   copy

Evidence for coabundance of leafminer flies and whiteflies in melon crops

Authorship SCIMAGO INSTITUTIONS RANKINGS

ABSTRACT

Interspecific competitions are important mechanisms in structuring ecological communities, including agroecosystems, in which different species may share the same food resource. In melons, two major pests coexist in time and space, Liriomyza sativae Blanchard (Diptera: Agromyzidae) and Bemisia tabaci (Gennadius) (Hemiptera: Aleyrodidae). The former feeds on the leaf mesophyll, while the latter on the phloem sap. Therefore, the same niche exploitation can trigger interactive processes between both populations. The present research aimed to determine if there are positive or negative interactions between whiteflies and leafminers under field conditions. The experiment was conducted in four commercial melon fields in northeast Brazil in two planting seasons. Thirty random plants were weekly selected for detection of whitefly nymphs and leafminer larvae throughout the entire crop cycle. The data was organized and analyzed considering the species abundance of L. sativae (larvae) and B. tabaci (nymphs and adults) in the same plant. Thus, the coabundance of species was investigated by using regressions with Poisson errors. The results suggest different fractions of negative, positive and neutral (not significant relationships) coabundance between the two species. Among 34 significant interactions, 56% were negative, suggesting that more than half of significant interactions are due to interspecific competition with negative coabundance.

Key words
Liriomyza sativae Blanchard; Bemisia tabaci (Gennadius); Cucumis melo L. semi-arid

INTRODUCTION

Interspecific interactions between populations of organisms describe relationships capable of regulating patterns of distribution, abundance and species diversity within ecological communities (Kaplan et al. 2011Kaplan, I., Sardanelli, S., Rehill, B. J., and Denno, R. F. (2011). Toward a mechanistic understanding of competition in vascular-feeding herbivores: an empirical test of the sink competition hypothesis. Oecologia, 166, 627-636. https://doi.org/10.1007/s00442-010-1885-9
https://doi.org/10.1007/s00442-010-1885-... ). Particularly, competition could be defined as a reduction in the survival rate of a particular species, affecting its population growth through interference from another or even by resource competition, in which an organism is displaced by a more aggressive one (Begon et al. 2005Begon, M., Townseed, C. R., and Harper, J. L. (2005). Ecology: From Individuals to Ecosystems. Oxford: Wiley-Blackwell.). Strategies are also used by species to coexist and avoid competition, such as niche segregation and spatial or temporal resource partitioning (Chesson 2000Chesson, P. (2000). Mechanisms of Maintenance of Species Diversity. Annual Review of Ecolog, and Systematics, 31, 343-366. https://doi.org/10.1146/annurev.ecolsys.31.1.343
https://doi.org/10.1146/annurev.ecolsys.... ; Di Bitetti et al. 2009Di Bitetti, M. S., Di Blanco, Y. E., Pereira, J. A., Paviolo, A., and Pírez, I. J. (2009). Time partitioning favors the coexistence of sympatric crab-eating foxes (Cerdocyon thous and Pampas foxes (Lycalopex gymnocercus). Journal of Mammalogy, 90, 479-490. https://doi.org/10.1644/08-MAMM-A-113.1
https://doi.org/10.1644/08-MAMM-A-113.1... ).

Co-occurrence patterns have been a central concern in community ecology, particularly to investigate segregation and/or grouping in animal communities (Gotelli 2000Gotelli, N. J. (2000). Null model analysis of species co-occurrence patterns. Ecology, 81, 2606-2621. https://doi.org/10.1890/0012-9658(2000)081[2606:NMAOSC]2.0.CO;2
https://doi.org/10.1890/0012-9658(2000)0... ). However, this approach is characterized particularly by analysis of presence–absence matrices with “null model” randomization tests (Gotelli 2000Gotelli, N. J. (2000). Null model analysis of species co-occurrence patterns. Ecology, 81, 2606-2621. https://doi.org/10.1890/0012-9658(2000)081[2606:NMAOSC]2.0.CO;2
https://doi.org/10.1890/0012-9658(2000)0... ), structure that does not allow considering the abundance of species, an important aspect to evaluate interactive processes in local scale (Brodie et al. 2018Brodie, J. F., Helmy, O. E., Mohd-Azlan, J., Granados, A., Bernard, H., Giordano, A. J., and Zipkin, E. (2018). Models for assessing local-scale co-abundance of animal species while accounting for differential detectabilit and varied responses to the environment. Biotropica, 50, 5-15. https://doi.org/10.1111/btp.12500
https://doi.org/10.1111/btp.12500... ).

Bemisia tabaci (Gennadius) and Liriomyza sativae Blanchard are the main pests of melon in northeast Brazil (Chagas et al. 2019Chagas, M. C. M., Costa-Lima, T. C., and Silva, J. R. (2019). Manejo de pragas. In C. Nic., and A. Borém (Eds.), Melão do plantio à colheita (p. 118-146). Viçosa: UFV.). The whitefly nymphs and adults feed by inserting their mouthpieces in the leaf and sucking the phloem sap (Jahan et al. 2014Jahan, S. M. H., Lee, G.-S., Lee, S., and Lee, K.-Y. (2014). Upregulation of probin., and feeding related behavioural frequencies in Bemisia tabaci upon acquisition of Tomato yellow leaf curl virus. Pest Management Science, 70, 1497-1502. https://doi.org/10.1002/ps.3828
https://doi.org/10.1002/ps.3828... ), while the leafminer larvae use their mouth hooks to feed in the mesophyll inside the leaves (Wei et al. 2000Wei, J., Zou, L., Kuang, R., and He, L. (2000). Influence of leaf tissue structure on host feeding selection by pea leafminer Liriomyza huidobrensis (Diptera: Agromyzidae). Zoological Studies, 39, 295-300.). The leafminer larvae and whitefly nymphs occur mainly on the basal and medium leaves of the melon’s branch (Chagas et al. 2019Chagas, M. C. M., Costa-Lima, T. C., and Silva, J. R. (2019). Manejo de pragas. In C. Nic., and A. Borém (Eds.), Melão do plantio à colheita (p. 118-146). Viçosa: UFV.). Therefore, both species coexist by feeding on the melon plants and their damage results in large economic losses in this agroecosystem (Baldin et al. 2012Baldin, E. L. L., Silva, J. P. G. F., and Pannuti, L. E. R. (2012). Resistance of melon cultivars to Bemisia tabaci biotype B. Horticultura Brasileira, 30, 600-606. https://doi.org/10.1590/S0102-05362012000400007
https://doi.org/10.1590/S0102-0536201200... ; Costa-Lima et al. 2019Costa-Lima, T. C., Chagas, M. C. M., and Parra, J. R. P. (2019). Comparing Potential as Biocontrol Agents of Two Neotropical Parasitoids of Liriomyza sativae. Neotropical Entomology, 48, 660-667. https://doi.org/10.1007/s13744-018-00667-0
https://doi.org/10.1007/s13744-018-00667... ).

In tomatoes, B. tabaci infestation modifies the expression of proteins that may exert influence on other herbivores (Mayer et al. 2002Mayer, R. T., Inbar, M., McKenzie, C. L., Shatters, R., Borowicz, V., Albrecht, U., Powell, C. A., and Doostdar, H. (2002). Multitrophic interactions of the silverleaf whitefly, host plants, competing herbivore and phytopathogens. Archives of Insect Biochemistr and Physiology, 51, 151-169. https://doi.org/10.1002/arch.10065
https://doi.org/10.1002/arch.10065... ). Field and laboratory studies showed that B. tabaci has a negative impact on the biological parameters of Liriomyza trifolii Burgess in tomatoes (Inbar et al. 1999Inbar, M., Doostdar, H., Leibee, G. L., and Mayer, R. T. (1999). The role of plant rapidly induced responses in asymmetric interspecific interactions among insect herbivores. Journal of Chemical Ecology, 25, 1961-1979. https://doi.org/10.1023/A:1020998219928
https://doi.org/10.1023/A:1020998219928... ). A similar result was obtained in cucumber and pumpkin plants infested with B. tabaci, in which the biological performance of L. sativae was low when compared to plants free from whiteflies (Zhang et al. 2005Zhang, L.-P., Zhang, G.-Y., Zhang, Y.-J., Zhang, W.-J., and Liu, Z. (2005). Interspecific interactions between Bemisia tabaci (Hem., Aleyrodidae and Liriomyza sativae (Dipt Agromyzidae). Journal of Applied Entomology, 129, 443-446. https://doi.org/10.1111/j.1439-0418.2005.00991.x
https://doi.org/10.1111/j.1439-0418.2005... ).

Melon crops in Brazilian semi-arid region becomes perfect models to test open field interactions, because whiteflies and leafminers are major pests of this crop, exploiting the same niche. Thus, the present research aimed to determine if there are positive or negative interactions between L. sativae and B. tabaci under field conditions.

MATERIAL AND METHODS

The study was conducted in Floresta, Pernambuco (PE), located in the semi-arid region of northeast Brazil. The city has a BSw’h’ climate (very warm, semi-arid, steppe type), according to the Köppen classification, and 4aTh (warm tropical with severe drought) according to the Guassen classification (Jacomine et al. 1973Jacomine, P. K. T., Cavalcanti, A. C., Burgos, N., and Pessoa, S. C. P. (1973). Levantamento exploratório: reconhecimento de solos do estado de Pernambuco. Recife: DNPEA.).

Surveys were conducted in four commercial melon fields during two different periods. The first was from August to September of 2015 (A1 and A2) and the second was from March to May of 2016 (B1 and B2). The geographical coordinates of the studied areas were A1 (8°47’14,1”S and 38°34’54,7”W), A2 (8°36’49,9”S and 38° 35’ 00,2”W), B1 (8°38’16,5”S and 38°34’30,6”W) and B2 (8°39’09,4”S and 38°36’53,8”W).

The studied fields ranged from 0.7 to 1.3 ha, all cultivated with yellow type melons. The crop was established with seeds, drip irrigation and without plastic mulching. In general, the fertilizer foundation was made with NPK (6-24-12). Other information about the crop management can be found in Table 1. In field A1, the phytosanitary measures were conducted until the fourth week. However, monitoring proceeded until the tenth week, when fruits were at harvest point.

Thumbnail
Table 1
Melon crop management information about the four fields used in the experiments, Floresta (PE), Brazil.

The samplings were carried out weekly during the entire crop cycle. Eight to 10 samplings were done in each field, according to the harvest period. In each sampling, a total of 30 plants were randomly selected in each field and the tenth leaf (counted from the apex) was detached. The number of B. tabaci nymphs and L. sativae larvae were recorded. For the whiteflies, a 5 cm2 area was focused with a hand lens (10×), in the leaf lower margin close to the midrib. Only fourth instar nymphs (red-eye presence) were registered. For L. sativae, live larvae (yellow colored) inside the mines in the entire leaf area were recorded. For the B. tabaci adults count, the melon apex branch (third leaf from the apex) was sampled on the leaf abaxial side.

The Shapiro-Wilk test was used to evaluate the normality of errors, with results suggesting the data does not follow a normal distribution. Therefore, generalized linear models (GLM) with a Poisson distribution of errors were used to analyze the influence of L. sativae larvae on B. tabaci nymphs or adults and vice-versa. This was done because the interest of this research was to explore the bidirectional relationship between the two insect species. For this reason, to investigate the negative, positive or neutral (not significant) coabundance, L. sativae and B. tabaci (nymphs or adults) were established both as dependent and independent variables. The statistical significance was evaluated with p < 0.05. The regression coefficient was used to estimate the positive or negative coabundance between species. Regression coefficients have been regularly used as a competition coefficient in several studies, emphasizing interspecific interaction and evidencing the competitive abilities of organisms (Hallett and Pimm 1979Hallet, J. G., and Pimm, S. L. (1979). Direct estimation of competition. The American Naturalist, 113, 593-600. https://doi.org/10.1086/283415
https://doi.org/10.1086/283415... ; Luo et al. 1998Luo, J., Monamy, V., and Fox, B. J. (1998). Competition between two Australian rodent species: a regression analysis. Journal of Mammalogy, 79, 962-971. https://doi.org/10.2307/1383104
https://doi.org/10.2307/1383104... ; Hart et al. 2018Hart, S. P., Freckleton, R. P., and Levine, J. M. (2018). How to quantify competitive ability. Journal of Ecology, 106, 1902-1909. https://doi.org/10.1111/1365-2745.12954
https://doi.org/10.1111/1365-2745.12954... ).

RESULTS AND DISCUSSION

Results show three relationship scenarios estimating coabundance patterns between L. sativae and B. tabaci (nymphs or adults) by using Poisson regression coefficients: neutral, positive and negative coabundance. The neutral pattern indicates no relationship between species (Tables 2 to 5), positive coabundance reveals an increasing trend between species (Fig. 1) and the negative shows a decreasing trend between species (Fig. 2). In the current study, it was chosen to present just two figures to illustrate these relationships between species, since the graphs represent the several other analyzed interactions very well. Tables 2 to 5 show the significance of the coabundance between the two species, as well as the coabundance effect given by the Poisson regression coefficient in four different fields described in Table 1.

Thumbnail
Table 2
Association between L. sativae (larvae) and B. tabaci (nymphs and adults) in melon field A1, June to August 2015, Floresta, Brazil.
Thumbnail
Table 3
Association between L. sativae (larvae) and B. tabaci (nymphs and adults) in melon field A2, June to August 2015, Floresta, Brazil.
Thumbnail
Table 4
Association between L. sativae (larvae) and B. tabaci (nymphs and adults) in melon field B1, March to May 2016, Floresta, Brazil.
Thumbnail
Table 5
Association between Liriomyza sativae (larvae) and Bemisia tabaci (nymphs and adults) in melon field B1, March to May 2016, Floresta, Brazil.
Figure 1
Influence of L. sativae larvae on B. tabaci nymphs indicating positive coabundance from collections obtained in melon field A1, August 27, 2015.
Figure 2
Influence of L. sativae larvae on B. tabaci adults indicating negative coabundance from collections obtained in melon field A1, August 13, 2015.

In field A1 with among 29 interactions, 10 exhibited an absence of significance between dependent and independent variables (Table 2). Twelve interactions exhibited a positive coabundance between L. sativae and B. tabaci, with 10 showing leafminers versus whitefly nymphs and two for L. sativae and B. tabaci adults (Table 2). Seven interactions showed a negative coabundance in field A1 and, among them, just one exhibited unidirectional negative impact on the other competitor (Table 2).

Among 19 interactions were observed in field A2, 13 of them exhibited not significant coabundance, one showed a positive interaction between L. sativae and nymphs and five indicated negative interactions, with three involving adults of B. tabaci and two showing interactions with nymphs (Table 3). Only one negative coabundance took place in a unidirectional way (Table 3).

In field B1 there were among 18 interactions, 13 were not significant, two positives and three negatives (Table 4). The positive ones occurred between L. sativae and B. tabaci adults. For the negatives, two involved whiteflies adults and one for the nymphs (Table 4) and one of them exhibited a unidirectional interaction (Table 4). In B2 there were among 19 interactions, 15 were not significant, four exhibited a negative coabundance and none were positive (Table 5). Among the negative interactions, just one was observed involving nymphs of B. tabaci, while the other three involved interactions between L. sativae and B. tabaci adults (Table 5).

The results suggest the occurrence of negative, positive and neutral coabundance between the two species. The negative coabundance indicates the occurrence of interspecific competition, while the positive relationships suggest no competition. Among 85 interactions were investigated, 19 were negative, 15 were positive and 51 were not significant or neutral. Among the 34 significant interactions, 56% were negative, suggesting that more than half of the significant interactions are due to interspecific competition. The results obtained indicate that competition can occur between L. sativae and B. tabaci in melon crops in the studied conditions. Based on the Poisson regressions, only 22% of the interactions suggest the occurrence of competition with negative effect, 18% indicates the existence of positive interactions and 60% are neutral interactions. Negative coabundance comes from the ability of a species to negatively impact its competitor by consuming the shared resources in an uneven way and, in this study, it is represented by the significant negative regression slope value (Crowell and Pimm 1976Crowell, K. L., and Pimm, S. L. (1976). Competitio and niche shifts of mice introduced onto small islands. Oikos, 27, 251-258. https://doi.org/10.2307/3543903
https://doi.org/10.2307/3543903... ; Hallett and Pimm 1979Hallet, J. G., and Pimm, S. L. (1979). Direct estimation of competition. The American Naturalist, 113, 593-600. https://doi.org/10.1086/283415
https://doi.org/10.1086/283415... ; Luo et al. 1998Luo, J., Monamy, V., and Fox, B. J. (1998). Competition between two Australian rodent species: a regression analysis. Journal of Mammalogy, 79, 962-971. https://doi.org/10.2307/1383104
https://doi.org/10.2307/1383104... ). Positive coabundance comes from the ability of two species to use shared resources without causing a negative impact into each other and, in this study, it was indicated by a positive slope value. In neutral coabundance, species are totally independent of each other and is currently determined by the absence of significance between the species abundances.

Although the two species have distinct feeding behavior, both share the same host plant, coexisting in time and space, increasing the likelihood of competition (Schoener 1974Schoener, T. W. (1974). Resource partitioning in ecological communities. Science, 185, 27-39. https://doi.org/10.1126/science.185.4145.27
https://doi.org/10.1126/science.185.4145... ; Connell 1980Connell, J. H. (1980). Diversit and the coevolution of competitors, or the ghost of competition past. Oikos, 35, 131-138. https://doi.org/10.2307/3544421
https://doi.org/10.2307/3544421... ). Among the 19 negative effects, 11 were caused by L. sativae and eight by B. tabaci. Although results indicate a slight advantage for L. sativae, the difference between the number of negative effects among the two species is not high. In tomatoes, a reduction in L. trifolii oviposition, feeding puncture and larval viability was observed in plants previously infested with B. tabaci, whereas this effect did not occur in the reverse order (Inbar et al. 1999Inbar, M., Doostdar, H., Leibee, G. L., and Mayer, R. T. (1999). The role of plant rapidly induced responses in asymmetric interspecific interactions among insect herbivores. Journal of Chemical Ecology, 25, 1961-1979. https://doi.org/10.1023/A:1020998219928
https://doi.org/10.1023/A:1020998219928... ). Negative effects on L. sativae were also observed in pumpkin and cucumber previously infested with B. tabaci, which reduced the number of mines number and the weight of fly pupae (Zhang et al. 2005Zhang, L.-P., Zhang, G.-Y., Zhang, Y.-J., Zhang, W.-J., and Liu, Z. (2005). Interspecific interactions between Bemisia tabaci (Hem., Aleyrodidae and Liriomyza sativae (Dipt Agromyzidae). Journal of Applied Entomology, 129, 443-446. https://doi.org/10.1111/j.1439-0418.2005.00991.x
https://doi.org/10.1111/j.1439-0418.2005... ). Defense mechanisms of plants, triggered by the insects feeding, may be involved in these cases. It has been observed that tomato plants infested with B. tabaci and L. trifolii produce proteins related to the pathogenesis (PR-proteins), some restricted to the feeding site, others in a systemic way (Inbar and Gerling 2008Inbar, M., and Gerling, D. (2008). Plant-mediated interactions between whiteflies, herbivore., and natural enemies. Annual Review of Entomology, 53, 431-448. https://doi.org/10.1146/annurev.ento.53.032107.122456
https://doi.org/10.1146/annurev.ento.53.... ). These proteins, such as chitinases, β-1,3-glucanase and peroxidases, may express insecticidal and antimicrobial activity (Mayer et al. 2002Mayer, R. T., Inbar, M., McKenzie, C. L., Shatters, R., Borowicz, V., Albrecht, U., Powell, C. A., and Doostdar, H. (2002). Multitrophic interactions of the silverleaf whitefly, host plants, competing herbivore and phytopathogens. Archives of Insect Biochemistr and Physiology, 51, 151-169. https://doi.org/10.1002/arch.10065
https://doi.org/10.1002/arch.10065... ). However, these proteins or secondary plant metabolites are usually not found in the phloem, making chewing insects more susceptible to these compounds compared to sucking insects (Zhang et al. 2005Zhang, L.-P., Zhang, G.-Y., Zhang, Y.-J., Zhang, W.-J., and Liu, Z. (2005). Interspecific interactions between Bemisia tabaci (Hem., Aleyrodidae and Liriomyza sativae (Dipt Agromyzidae). Journal of Applied Entomology, 129, 443-446. https://doi.org/10.1111/j.1439-0418.2005.00991.x
https://doi.org/10.1111/j.1439-0418.2005... ). Also, the whiteflies secrete a viscous saliva that forms a sheath that lubricates the stylet pathway and protects against these compounds when penetrating the plant (Mayer et al. 2002Mayer, R. T., Inbar, M., McKenzie, C. L., Shatters, R., Borowicz, V., Albrecht, U., Powell, C. A., and Doostdar, H. (2002). Multitrophic interactions of the silverleaf whitefly, host plants, competing herbivore and phytopathogens. Archives of Insect Biochemistr and Physiology, 51, 151-169. https://doi.org/10.1002/arch.10065
https://doi.org/10.1002/arch.10065... ). Thus, B. tabaci can induce plant defenses without being affected, overcoming other herbivores in competition (Mayer et al. 1996Mayer, R. T., McCollum, T. G., McDonald, R. E., Polston, J. E., and Doostdar, H. (1996). Bemisia feeding induces pathogenesis-related proteins in tomato. In D. Gerlin., and R. T. Mayer (Eds.), Bemisia 1995: Taxonomy, Biology, Damage, Contro and Management (p. 179-188)., andover: Intercept Ltd., 2002Mayer, R. T., Inbar, M., McKenzie, C. L., Shatters, R., Borowicz, V., Albrecht, U., Powell, C. A., and Doostdar, H. (2002). Multitrophic interactions of the silverleaf whitefly, host plants, competing herbivore and phytopathogens. Archives of Insect Biochemistr and Physiology, 51, 151-169. https://doi.org/10.1002/arch.10065
https://doi.org/10.1002/arch.10065... ). Considering the PR-proteins expression, these are generally more intense at the site where the injury occurred immediately after feeding (Karban and Baldwin 1997Karban, R., and Baldwin, I. T. (1997) Induced responses to herbivory. Chicago: University of Chicago Press. https://doi.org/10.7208/chicago/9780226424972.001.0001
https://doi.org/10.7208/chicago/97802264... ). In melon plants, L. sativae larvae and B. tabaci more developed nymphs occur predominantly in the branch middle region (Chagas et al. 2019Chagas, M. C. M., Costa-Lima, T. C., and Silva, J. R. (2019). Manejo de pragas. In C. Nic., and A. Borém (Eds.), Melão do plantio à colheita (p. 118-146). Viçosa: UFV.). Therefore, the whitefly may trigger more intense plant defense responses at the feeding site and possibly interferes in the leafminers’ development. On the other hand, a recent study identified a protein (Bt56) inserted by B. tabaci in tobacco plants that elicits the salicylic acid signaling pathway and, consequently, suppresses the effective jasmonic acid defenses (Xu et al. 2019Xu, H.-X., Qian, L.-X., Wang, X.-W., Shao, R.-X., Hong, Y., Liu, S.-S., and Wang, X.-W. (2019). A salivary effector enables whitefly to feed on host plants by eliciting salicylic acid-signaling pathway. Proceedings of the National Academy of Sciences of United States of America, 116, 490-495. https://doi.org/10.1073/pnas.1714990116
https://doi.org/10.1073/pnas.1714990116... ).

The current results clearly show a higher number of interactions taking place in A1 than other fields, in addition to a lower number of non-significant interactions. Field A1 had phytosanitary measures applied only during the first four weeks, while the other melon fields had a weekly use of insecticides. Thus, a higher number of each pest was observed, mainly L. sativae. Consequently, the probability of finding B. tabaci also increased.

CONCLUSION

Most interactions between L. sativae and B. tabaci in melon crops in the Brazilian semi-arid region are neutral. Among the significant interactions most are negative, suggesting that these interactions are due to interspecific competition with negative coabundance.

ACKNOWLEDGEMENTS

To Túlio Silva for the aid in the field work and to the melon producers of Floresta for allowing to use their areas in the experiments.

REFERENCES

  • Baldin, E. L. L., Silva, J. P. G. F., and Pannuti, L. E. R. (2012). Resistance of melon cultivars to Bemisia tabaci biotype B. Horticultura Brasileira, 30, 600-606. https://doi.org/10.1590/S0102-05362012000400007
    » https://doi.org/10.1590/S0102-05362012000400007
  • Begon, M., Townseed, C. R., and Harper, J. L. (2005). Ecology: From Individuals to Ecosystems. Oxford: Wiley-Blackwell.
  • Brodie, J. F., Helmy, O. E., Mohd-Azlan, J., Granados, A., Bernard, H., Giordano, A. J., and Zipkin, E. (2018). Models for assessing local-scale co-abundance of animal species while accounting for differential detectabilit and varied responses to the environment. Biotropica, 50, 5-15. https://doi.org/10.1111/btp.12500
    » https://doi.org/10.1111/btp.12500
  • Chagas, M. C. M., Costa-Lima, T. C., and Silva, J. R. (2019). Manejo de pragas. In C. Nic., and A. Borém (Eds.), Melão do plantio à colheita (p. 118-146). Viçosa: UFV.
  • Chesson, P. (2000). Mechanisms of Maintenance of Species Diversity. Annual Review of Ecolog, and Systematics, 31, 343-366. https://doi.org/10.1146/annurev.ecolsys.31.1.343
    » https://doi.org/10.1146/annurev.ecolsys.31.1.343
  • Connell, J. H. (1980). Diversit and the coevolution of competitors, or the ghost of competition past. Oikos, 35, 131-138. https://doi.org/10.2307/3544421
    » https://doi.org/10.2307/3544421
  • Costa-Lima, T. C., Chagas, M. C. M., and Parra, J. R. P. (2019). Comparing Potential as Biocontrol Agents of Two Neotropical Parasitoids of Liriomyza sativae Neotropical Entomology, 48, 660-667. https://doi.org/10.1007/s13744-018-00667-0
    » https://doi.org/10.1007/s13744-018-00667-0
  • Crowell, K. L., and Pimm, S. L. (1976). Competitio and niche shifts of mice introduced onto small islands. Oikos, 27, 251-258. https://doi.org/10.2307/3543903
    » https://doi.org/10.2307/3543903
  • Di Bitetti, M. S., Di Blanco, Y. E., Pereira, J. A., Paviolo, A., and Pírez, I. J. (2009). Time partitioning favors the coexistence of sympatric crab-eating foxes (Cerdocyon thous and Pampas foxes (Lycalopex gymnocercus). Journal of Mammalogy, 90, 479-490. https://doi.org/10.1644/08-MAMM-A-113.1
    » https://doi.org/10.1644/08-MAMM-A-113.1
  • Gotelli, N. J. (2000). Null model analysis of species co-occurrence patterns. Ecology, 81, 2606-2621. https://doi.org/10.1890/0012-9658(2000)081[2606:NMAOSC]2.0.CO;2
    » https://doi.org/10.1890/0012-9658(2000)081[2606:NMAOSC]2.0.CO;2
  • Hallet, J. G., and Pimm, S. L. (1979). Direct estimation of competition. The American Naturalist, 113, 593-600. https://doi.org/10.1086/283415
    » https://doi.org/10.1086/283415
  • Hart, S. P., Freckleton, R. P., and Levine, J. M. (2018). How to quantify competitive ability. Journal of Ecology, 106, 1902-1909. https://doi.org/10.1111/1365-2745.12954
    » https://doi.org/10.1111/1365-2745.12954
  • Inbar, M., Doostdar, H., Leibee, G. L., and Mayer, R. T. (1999). The role of plant rapidly induced responses in asymmetric interspecific interactions among insect herbivores. Journal of Chemical Ecology, 25, 1961-1979. https://doi.org/10.1023/A:1020998219928
    » https://doi.org/10.1023/A:1020998219928
  • Inbar, M., and Gerling, D. (2008). Plant-mediated interactions between whiteflies, herbivore., and natural enemies. Annual Review of Entomology, 53, 431-448. https://doi.org/10.1146/annurev.ento.53.032107.122456
    » https://doi.org/10.1146/annurev.ento.53.032107.122456
  • Jacomine, P. K. T., Cavalcanti, A. C., Burgos, N., and Pessoa, S. C. P. (1973). Levantamento exploratório: reconhecimento de solos do estado de Pernambuco. Recife: DNPEA.
  • Jahan, S. M. H., Lee, G.-S., Lee, S., and Lee, K.-Y. (2014). Upregulation of probin., and feeding related behavioural frequencies in Bemisia tabaci upon acquisition of Tomato yellow leaf curl virus Pest Management Science, 70, 1497-1502. https://doi.org/10.1002/ps.3828
    » https://doi.org/10.1002/ps.3828
  • Kaplan, I., Sardanelli, S., Rehill, B. J., and Denno, R. F. (2011). Toward a mechanistic understanding of competition in vascular-feeding herbivores: an empirical test of the sink competition hypothesis. Oecologia, 166, 627-636. https://doi.org/10.1007/s00442-010-1885-9
    » https://doi.org/10.1007/s00442-010-1885-9
  • Karban, R., and Baldwin, I. T. (1997) Induced responses to herbivory. Chicago: University of Chicago Press. https://doi.org/10.7208/chicago/9780226424972.001.0001
    » https://doi.org/10.7208/chicago/9780226424972.001.0001
  • Luo, J., Monamy, V., and Fox, B. J. (1998). Competition between two Australian rodent species: a regression analysis. Journal of Mammalogy, 79, 962-971. https://doi.org/10.2307/1383104
    » https://doi.org/10.2307/1383104
  • Mayer, R. T., McCollum, T. G., McDonald, R. E., Polston, J. E., and Doostdar, H. (1996). Bemisia feeding induces pathogenesis-related proteins in tomato. In D. Gerlin., and R. T. Mayer (Eds.), Bemisia 1995: Taxonomy, Biology, Damage, Contro and Management (p. 179-188)., andover: Intercept Ltd.
  • Mayer, R. T., Inbar, M., McKenzie, C. L., Shatters, R., Borowicz, V., Albrecht, U., Powell, C. A., and Doostdar, H. (2002). Multitrophic interactions of the silverleaf whitefly, host plants, competing herbivore and phytopathogens. Archives of Insect Biochemistr and Physiology, 51, 151-169. https://doi.org/10.1002/arch.10065
    » https://doi.org/10.1002/arch.10065
  • Schoener, T. W. (1974). Resource partitioning in ecological communities. Science, 185, 27-39. https://doi.org/10.1126/science.185.4145.27
    » https://doi.org/10.1126/science.185.4145.27
  • Wei, J., Zou, L., Kuang, R., and He, L. (2000). Influence of leaf tissue structure on host feeding selection by pea leafminer Liriomyza huidobrensis (Diptera: Agromyzidae). Zoological Studies, 39, 295-300.
  • Xu, H.-X., Qian, L.-X., Wang, X.-W., Shao, R.-X., Hong, Y., Liu, S.-S., and Wang, X.-W. (2019). A salivary effector enables whitefly to feed on host plants by eliciting salicylic acid-signaling pathway. Proceedings of the National Academy of Sciences of United States of America, 116, 490-495. https://doi.org/10.1073/pnas.1714990116
    » https://doi.org/10.1073/pnas.1714990116
  • Zhang, L.-P., Zhang, G.-Y., Zhang, Y.-J., Zhang, W.-J., and Liu, Z. (2005). Interspecific interactions between Bemisia tabaci (Hem., Aleyrodidae and Liriomyza sativae (Dipt Agromyzidae). Journal of Applied Entomology, 129, 443-446. https://doi.org/10.1111/j.1439-0418.2005.00991.x
    » https://doi.org/10.1111/j.1439-0418.2005.00991.x

Edited by

Section Editor:

Luís Garrigós Leite

Publication Dates

  • Publication in this collection
    15 Jan 2021
  • Date of issue
    2021

History

  • Received
    14 Nov 2019
  • Accepted
    06 Oct 2020
Creative Common - by 4.0
This is an Open Access article distributed under the terms of the Creative Commons Attribution License, which permits unrestricted use, distribution, and reproduction in any medium, provided the original work is properly cited.
Instituto Agronômico de Campinas Avenida Barão de Itapura, 1481, 13020-902, Tel.: +55 19 2137-0653, Fax: +55 19 2137-0666 - Campinas - SP - Brazil
E-mail: bragantia@iac.sp.gov.br
Acompanhe os números deste periódico no seu leitor de RSS