Translator Disclaimer
1 September 2013 Survival of a Lepidopteran Defoliator of Eucalyptus is Influenced by Local Hillside and Forest Remnants in Brazil
Luiz Eduardo Macedo-Reis, Luiz Gustavo Souto Soares, Maurício Lopes De Faria, Mario Marcos Do Espírito Santo, José Cola Zanuncio
Author Affiliations +
Abstract

We tested the hypothesis that Euselasia eucerus (Lepidoptera: Riodinidae) the intensities of mortality factors in eucalyptus plantations in xeric environments are greater near fragments of native forest and they diminish with increasing distance from the latter. Samples were collected along a transect crossing a 70-ha planting of Eucalyptus urophylla x Eucalyptus grandis hybrid extending from adjacent native vegetation to a hilltop. Sampling was completed along an elevation and distance gradient from the native forest in three environments, near the native forest (base), intermediate (mid way between the native forest and the hilltop) and distant from the native forest (hilltop) ones. Fungi, parasites and predators caused mortality of E. eucerus pupae. Damage to E. urophylla x E. grandis hybrid by E. eucerus was greater at the more distant location possibly because of plant water deficits and/ or increased E. eucerus survival. Mortality of E. eucerus in all ontogenetic stages was greater in areas near the native forest. Proximity to native vegetation appeared to be a key factor that influenced survival of local E. eucerus populations in E. urophylla x E. grandis hybrid plantations. The results presented here reinforce the concept that native vegetation near eucalyptus plantations exerts a local effect supporting the maintenance of natural enemies of E. eucerus, and favoring infections by entomopathogenic fungi during the pupal stage of this insect.

Lepidopteran defoliators are important pests of cultivated eucalyptus (Myrtales: Myrtaceae) due to the intensity and persistence of damage they cause (Zanuncio et al. 2003; Bernardino et al. 2007). Infestations of these species can occur throughout the year or in sporadic population explosions (Zanuncio et al. 1998, 2000). Euselasia eucerus (Lepidoptera: Riodinidae) is one of a few butterfly pest species of eucalyptus in Brazil (Zanuncio et al. 2000). This lepidopteran originated in South America and is a known defoliator of eucalyptus. It is found in Minas Gerais, São Paulo, Santa Catarina and Rio Grande do Sul states, Brazil (Zanuncio et al. 2000). Euselasia eucerus increases in density, especially during the driest months of the yr, and it has multiple generations per yr in eucalyptus plantations (Sousa et al. 2010).

Euselasia eucerus has 5 well-defined stages, and it completes its life-cycle from egg hatch to the adult in 27 to 28 days. Its clutches contain 50 eggs on average (Murta et al. 2008; Zanuncio et al. 2009). The first few instars are social (aggregated), but the last two instars are found in smaller or isolated groups. The first few instars have weak jaws not capable of perforating the leaf cuticle, and they scrape the leaf surface, while the last few instars consume the leaves entirely. Benefits of aggregation disappear or are balanced by the costs associated with intraspecies competition of the last few instars (Reader & Hochuli 2003).

A number of factors contribute to the mortality of E. eucerus. Its eggs are parasitized by Trichogramma maxacali, Voegelé and Pointel, 1980, T. demoraesi Nagaraja, 1983 and T. acacioi Brun, Moraes & Soares, 1984 (Trichogrammatidae); its larvae and pupae are predated by the pentatomids, Podisus nigrispinus Dallas, 1851, Brontocoris tabidus (Signoret, 1852) and Supputius cincticeps (Stål, 1860); and its pupae are parasitized by Itoplectis sp. (Ichneumonidae), Galeopsomyia sp. (Eulophidae) and the fungus Paecilomyces fumosoroseus (Wizea). The parasitism of E. eucerus eggs was reported to be the main source of mortality of populations of this lepidopteran (Zanuncio 2009). Substantial mortality of E. eucerus larvae and other Lepidopteran can be caused by the predation of birds, ants and many others invertebrates (Greeney et al. 2012). Podisus nigrispinus, a common predator, is used for the biological control of the lepidopteran defoliators (Bortoli et al. 2011), but its effectiveness depends on prey density (Oliveira et al. 2001). Overall predation induces evolutionary responses by prey to that avoid, repel or escape attackers, causing indirect changes in aggregation pattern (Soares et al. 2009; Greeney et al. 2012). The physiological regulation of temperature and water balance are likely to have the greater impact on larval mortality (Allen 2007). However, the dynamics of the effects of entomopathogenic fungi and insect natural enemies on E. eucerus populations in the field are unknown.

The presence of native vegetation bordering plantations may be important on a local scale because it may lead to increased densities of natural enemies (Sperber et al. 2004) possibly because of the greater diversity of resources and niches (Tews et al. 2004). For example, Oxydia vesulia (Lepidoptera: Geometridae), a defoliator of eucalyptus, is more abundant in plantations without native vegetation remnants (Bragança et al. 1998; Murta et al. 2008). This pattern has also been reported for E. eucerus (Murta et al. 2008) and other lepidopteran defoliators with remnants of native vegetation increasing diversity of hymenopteran parasitoids in eucalyptus plantations (Bragança et al. 1998).

Remnants of native vegetation surrounding plantations increase the local availability of soil resources such as moisture, carbon and nitrogen, which are essential for the growth and development of plants (Chen et al. 2013). Therefore, the distance from a remnant forest is a compounding factor because of the decreasing predation/ parasitism (Lill & Marquis 2001) and increased opportunity for herbivory through increased plant stress (White 1984) and/or quantitative reductions of chemical defenses (Ribeiro & Basset 2001).

Remnant forests may also affect the diversity and abundance of natural predators on E. eucerus. The effectiveness of natural enemies can be evaluated with life tables to show mortality rates caused by different factors recorded in each stage of the insect cycle (Silva et al. 2008). Knowledge of these dynamics should facilitate the improvement of strategies to control eucalyptus pests.

The objective of the present study was to test the hypothesis that distance from the remmant forest is a factor affecting the survival and population sizes of different life stages of E. eucerus. We posited that the greatest mortality rate of this insect would be found in the zones where eucalyptus plantations interface with native forest remnants.

MATERIALS AND METHODS

Samplings were performed at a Nipo-Brazilian Cellulose S. A. company plantation (Celulose Nipo-Brasileira S.A. CENIBRA) in the Municipality of Belo Oriente, Minas Gerais State, Brazil (S 19° 29′ 36.7″ W -42° 24′ 62.9″) during an outbreak of E. eucerus butterflies in May and Jun 2005. This region is characterized by sharp relief, average temperature of 24.7 °C and annual rainfall of 1,220 mm (CENIBRA S.A. Meteorological Station, Belo Oriente). The climate according to the Köppen classification is hot and humid, with rainy and hot summers and dry and cold winters. Sampled eucalyptus plantations exhibited original Atlantic Forest biome with semi-deciduous seasonal vegetation structure. Remaining fragments of the native vegetation, mainly at the bottoms of valleys, are parts of legal reserves and permanent preservation areas which accumulate water and maintain lakes, forming the hydrographic Rio Doce basin (Perônico 2009).

Collections were located in a 70-ha plot of a 3-yr-old hybrid eucalyptus (Eucalyptus urophylla × Eucalyptus grandis) plantation. Three 150-m long transects were delimited in this plot simulating a hydric stress gradient. Each transect encompassed the following environments: mesic (close to the native vegetation and at the valley bottom with 230 m elevation; and a high moisture content), intermediate (intermediate elevation at 255 m) and xeric (hilltop at 280 m elevation, with a lower moisture content and greater distance from the native forest). Eight plants 20 m distant one from the other were selected per transect, and 3 lower basal branches were removed from each. We randomly chose 20 terminal branches from these 3 branches as the maximum number to minimize the effect of basal branch size, and transported to the laboratory in individual bags, where the numbers of E. eucerus eggs, larvae and pupae per leaf were counted. The ontogenetic stage of each individual was determined. Pupae infected with fungi were separated from healthy individuals based on the whitened appearance of the mass of fungal filaments, while parasitized pupae were identified based on the characteristic emergence holes left by parasitoids. Finally, pupae were considered to have been predated when the external layer of each was damaged, leaving part of the exoskeleton of the individual, without internal content.

Insect stages with aggregation behavior (L1, L2 and L3) were combined into one category for the life table calculations. Also those stages with mainly solitary individuals (L4 and L5) were combined. These two categories were treated as L1–L3, representing larvae with aggregation behavior, and L4–L5, those with solitary behavior.

The effects of the environments on density and survival of different ontogenetic categories of E. eucerus were tested with generalized linear models in 3 stages: (1) with the abundance of E. eucerus as a changeable response to transect environments (xeric, intermediate and mesic) and the ontogenetic category (eggs, L1–L3 larvae, L4– L5 larvae and pupae) as an explicative variable; (2) with the proportion of E. eucerus per plant as a response variable and the transect environments and ontogenetic categories as explicative variables; and (3) with the proportion of pupae as a response variable and the environments and mortality factors (parasitoids, predators and fungi) as explicative variables. Individuals collected were grouped by plant, with 8 replications per environment. Each complete model was subjected to an analysis of the residues to verify the adequate distribution of residuals and differences between the levels were verified by an analysis of contrast (Crawley 2010).

The numbers of live pupae and adults present in the field were estimated with a static life table (Silva et al. 2008). The L1 to L5 stages were determined according to the lengths of the E. eucerus larvae. In this type of life table, the absolute differences in the numbers per category (from egg to adult) are attributed to the mortality in each stage.

Field data were estimated based on the E. eucerus developmental stages using Kobayashi method (Kobayashi 1968). This method is based on (1) a provisional estimate of the number of individuals that die per stage, assuming a uniform mortality rate in all stages during the sampling interval, and (2) a correction of these estimates, assuming that mortality differs in some stages but is constant for each one. Number of individuals per stage (n) was used to calculate mortality factors (kn).

Mortality factors (Varley & Gradwell 1970) were calculated per phase or stage with the following equation: kn = log N - log Ns, where N = the initial population and Ns = the surviving population at the end of the related stage. The greater the value of the factor, k, the greater the intensity of the mortality factor.

RESULTS

A total of 46,360 E. eucerus individuals were obtained from 3,084 leaves sampled from 408 branches of the Eucalyptus urophylla × E. grandis hybrid (7.5 ± 0.32 SE leaves per branch and 15.6 ± 2.6 SE individuals per leaf), including 37,780 eggs (13.1 ± 2.3 SE eggs per leaf); 7,267 L1–L3 larvae (2.07 ± 0.65 SE larvae per leaf); 973 L4–L5 larvae (0.3 ± 0.11 SE larvae per leaf); and 340 pupae (0.1 ± 0.02 SE pupae per leaf). A total of 26.547 individuals were found on plants in the xeric environment (18.38 ± 1,31 SE eggs per leaf, 5.49 ± 0,84 SE L1–L3 larvae per leaf, 0.68 ± 0.23 L4–L5 larvae per leaf, and 0.2 ± 0,01 pupae per leaf); 12,228 in the intermediate environment (13.24 ± 1.3 SE eggs per leaf, 0.69 ± 0.18 SE L1– L3 larvae per leaf, 0.08 ± 0.3 SE L4–L5 larvae per leaf and 0.07 ± 0.01 pupae per leaf); and 7,624 in the mesic environment (5.69 ± 0.63 SE eggs per leaf, 0.68 ± 0.12 SE L1–L3 larvae per leaf, 0.15 ± 0.04 SE L4–L5 larvae per leaf and 0.04 ± 0.001 pupae per leaf).

The total numbers of eggs (generalized linear model (GLM), quasi-Poisson: Χ;2 [1,22] = 5,648.5, P < 0.001), L1–L3 larvae (GLM quasi-Poisson: χ2[1,22] = 6,989.5, P < 0.001), L4–L5 larvae (GLM quasi-Poisson: χ2 [1.21] = 710.87, P < 0.01) and pupae (GLM quasi-Poisson: χ2 [1,22] = 152.53, P < 0.001) were highest in the xeric environment and there was no significant difference between the intermediate and mesic ones (Fig. 1). The proportion of eggs was greater in the intermediate transect environment (GLM quasi-binomial: F [1,22]= 2,060.9, P < 0.05) than in the xeric and mesic environments (Fig. 2). However, the number of live caterpillars in the L1–L3 stage was higher in the xeric environment (GLM quasi-binomial: F [1,22] = 2,633.7, P < 0.01) than in the mesic and intermediate environments. The proportions of L4–L5 larvae (GLM quasi-binomial: F[2.21]= 482.98, P = 0.12) and pupae (GLM quasi-binomial: F[2.21]= 12.289, P = 0.66) were similar between the environments (Fig. 2). The estimated egg mortalities were high and similar in the mesic and intermediate environments (94% and 88%, respectively), with greater Kn values in these environments (0.925 and 1.284, respectively).

Fig. 1.

Number of eggs (I), L1–L3 larvae (II), L4–L5 larvae (III), and pupae (IV) of Euselasia eucerus (Lepidoptera: Riodinidade) per plant of hybrid Eucalyptus urophylla x Eucalyptus grandis in the xeric, intermediate and mesic environments in Belo Oriente, Minas Gerais State, Brazil. Bars with different letters indicate statistically significant differences between means. Data represented as mean ± standard error.

f01_941.jpg

The number of viable eggs of E. eucerus was greatest in all environments, followed by L1–L3 larvae. However, the survival pattern changed between environments beginning from the L1– L3 stage, with greater numbers of L4–L5 larvae and pupae in the xeric (GLM quasi-binomial: F[1, 30] = 42,455, P < 0.0001) and intermediate environments (GLM quasi-binomial: F [1, 30] = 42,275, P < 0.0001) (Fig. 2), which showed similar values between these ontogenetic phases. Survival between the L1–L3 and L4–L5 stages was similar in the mesic transect environment where a decreased proportion of pupae was found (GLM quasi-binomial: F [2, 29] = 20,471, P < 0.0001) (Fig. 2).

Fig. 2.

Percentage of alive individuals of Euselasia eucerus (Lepidoptera: Riodinidae) per plant of hybrid Eucalyptus grandis × Eucalyptus urophylla in Belo Oriente, Minas Gerais. Analyzes were made by environment and by stage per environment (xeric, mesic and intermediate). Data represented as mean ± standard error.

f02_941.jpg

Compared with the mesic environment, mortality of E. eucerus larvae was lower in the xeric and intermediate environments, with 87.5% mortality for L1–L3 larvae and 69% for L4–L5 larvae in the xeric environment and 88% mortality for L1–L3 larvae and 4% for L4–L5 larvae in the intermediate environment. The Kn was higher for the L1–L3 larvae and lower for the L4–L5 larvae in the xeric and intermediate environments (Table 1). In contrast, larval mortality was higher in the mesic environment, varying from 72% in the L1–L3 stage to 77% in the L4–L5 stage, and with the highest mortality Kn found for the L4–L5 larvae (Table 1).

The L4–L5 larvae to pupae ratio differed in the mesic environment, which had the highest Kn (0.54) and 72% mortality of pupae compared with 48.5% in the intermediate environment and 55.5% in the xeric one (Table 1). Pupal mortality was attributed to parasitoids, predators and fungi, and this last factor represented the principal mortality factor in all environments, i.e., xeric (GLM quasi-binomial: F [2,21] = 24.273, P < 0.04), intermediate (GLM quasi-binomial: F[2,15] = 30.44, P < 0.001) and mesic (GLM quasi-binomial: F [2,18] = 40.247, P < 0.0004) and with a greater impact in the mesic environment (GLM quasi-binomial: F [2,18] = 15.133, P < 0.03) (Fig. 3). Parasitism was similar between the 3 environments (GLM quasibinomial: F [2, 18] = 4.9, P = 0.38), but predation was lower in mesic and in the intermediate environments without any predated pupae (Fig. 3).

TABLE 1.

LIFE TABLE OF EUSELASIA EUCERUS (LEPIDOPTERA: RIODINIDAE) INDICATING THE MORTALITY FACTORS (K) IN 3 DIFFERENT ENVIRONMENTS A TRANSECT DELIMITED IN A PLANTATION OF EUCALYPTUS UROPHYLLA × EUCALYPTUS GRANDIS IN BELO ORIENTE, MINAS GERAIS STATE, BRAZIL DURING MAY AND JUN OF 2005.

t01_941.gif

DISCUSSION

The greater number of E. eucerus individuals in the xeric environment may be associated with the availability of nutrients and water stress in these plants, making them more vulnerable to pests (White 1984; Thies et al. 2003). Moreover, females of this butterfly may prefer to lay eggs in xeric environments because of the lower mortality by parasitoids and fungi compared to other environments.

Egg parasitism is one of the major control factors of E. eucerus in the field, independent of its population density (Matsumoto et al. 2004; Murta et al. 2008). Egg mortality of E. eucerus decreased (70%) with a decreased Kn effect (0.525) in the xeric environment. Mortality at this stage was principally due to parasitism by Trichogramma maxacalii, independent of habitat. This shows the importance of Trichogramma species in the natural biological control of agricultural and forest pests (Zanuncio et al. 2009) and corroborates the reported severe mortality of E.eucerus by T. maxacalli (Oliveira et al. 2000; Murta et al. 2008). Trichogramma, a natural enemy, is broadly distributed, specialized, efficient and crucial for integrated management of this pest (Pratissoli et al. 2005).

Fig. 3.

Mortality rate of Euselasia eucerus pupae, per plant of Eucalyptus urophylla × Eucalyptus grandis in the xeric, intermediate and mesic environments in Belo Oriente, Minas Gerais. Bars with different letters indicate statistically significant differences between means. Data represented as mean ± standard error.

f03_941.jpg

The greater structural complexity and variety of food resources of native vegetation increases the diversity (Thies et al. 2003), longevity and fertility of parasitoids in adjacent plantations (Oliveira et al. 2000). The mesic environment is in contact with a fragment of Atlantic Forest, which may contribute to the natural control of E. eucerus through this forest's positive effect on the parasitism rates of this butterfly in eucalyptus (Lill & Marquis 2001; Murta et al. 2008).

Differences in numbers of E. eucerus individuals per stage can be attributed to predation or parasitism or to mortality due to unknown causes, such as pathogens or climatic factors (Hajek & Leger 1994). Mortality factors of E. eucerus larvae are not well known (Zanuncio et al. 2009), but predation by Pentatomidae was observed during field sampling. These predators attack mainly third and fourth instar larvae (Lemos et al. 2003, Medeiros et al. 2003). Aggregation behavior of E. eucerus caterpillars at early stages can impede predation (Klok & Chown 1999), compared with the increased susceptibility to natural enemies of solitary individuals (Reader & Hochuli 2003). The greater size of E. eucerus caterpillars at third and fourth instars can facilitate their selection by predators as they yield a greater energetic return (Burger & Gochfeld 2001). Finally, the greater voracity of the final instars can increase consumption rates and the release of volatile chemical compounds that indicate the presence of eucalyptus herbivores, and thereby increase the predation risk (Radhika et al. 2003).

The greater number of E. eucerus individuals on eucalyptus plants in xeric areas may be caused by the higher concentration of nitrogen in the tissues of these plants and/or lower levels of chemical defenses (Thies et al. 2003). These factors would allow E. eucereus larvae to reach a larger size and be more susceptible to predation. In contrast, feeding on lower quality plants in mesic areas would render larvae more attractive to predators in later instar life-stages.

The mortality pattern of E. eucerus pupae can also be explained by their distance from the Atlantic Forest remnants, as the efficiency of predators and parasitoids depends on encounters with their hosts (Borer et al. 2007). Euselasia eucerus pupate on eucalyptus leaves and trunks, on other plants in the forest understory (Sousa et al. 2010), and on the ground. This behavior can make predator/parasitoid encounters unpredictable during active searching, and the predation was higher at the higher resource abundance in the xeric environment, but parasitism showed no differences between environments (Fig. 3). The same factors do not affect fungal infections, because fungi exhibit a high capacity to be spread horizontally by wind. Moreover, the greater humidity in mesic environments can favor the proliferation of fungi on E. eucerus pupae (Palmer et al. 1987), and humidity can favor their efficiency against pupae of this butterfly on eucalyptus plants (Zanuncio et al. 2009).

The results presented here reinforce the concept that native vegetation near eucalyptus plantations exerts a local effect supporting the maintenance of natural enemies of E. eucerus, and favoring fungal infection during pupal stage of this insect.

ACKNOWLEDGMENTS

To Nipo-Brazilian Cellulose-CENIBRA SA. for logistical support, particularly Alex Giovanny de Barros Medeiros. We are also very grateful to José B. Sampaio Júnior for helpful comments on the statistical analysis, Wagner Lacerda de Lima Fernandes for field work, and for the comments of anonymous reviewers of this manuscript. This study was completed with funding from the Minas Gerais Foundation for Research Support (Fundação de Amparo à Pesquisa do Estado de Minas Gerais — FAPEMIG) and from the Graduate Program in Biological Sciences (Programa de Pós-Graduação em Ciências Biológicas (PPGCB)) of Montes Claros State University (Universidade Estadual de Montes Claros (UNIMONTES).

REFERENCES CITED

1.

P. E. Allen 2010. Group size effects on survivorship and adult development in the gregarious larvae of Euselasia chrysippe (Lepidoptera: Riodinidae). Insect. Soc. 57: 199–204. Google Scholar

2.

A. S. Bernardino , T. V. Zanuncio , J. C. Zanuncio , E. R. Lima , and J. E. Serrão 2007. Note on gynandromorphism in the eucalyptus defoliator Thyrinteina arnobia (Stoll, 1782) (Lepidoptera: Geometridae). An. Acad. Brasileira de Ciências 79: 235–237. Google Scholar

3.

E. T. Borer , C. J. Briggs , and R. D. Holt 2007. Predators, parasitoids, and pathogens: a cross-cutting examination of intraguild predation theory. Ecology 88: 2681–2688. Google Scholar

4.

S. A. Bortoli , A. K. Otuka , A. M. Vacari , M. I. E. G. Martins , and H. X. L. Volpe 2011. Comparative biology and production costs of Podisus nigrispinus (Hemiptera: Pentatomidae) when fed different types of prey. BioControl. 58: 127–132. Google Scholar

5.

M. A. Bragança , J. C. Zanuncio , M. Picanço , and A. J. Laranjeiro 1998. Effects of environmental heterogeneity on Lepidoptera and Hymenoptera populations in Eucalyptus plantations in Brazil. Forest Ecol. Mgt. 103: 287–292. Google Scholar

6.

J. Burger , and M. Gochfeld 2001. Smooth-billed Ant (Crotophaga ani) predation on butterflies in Mato Grosso, Brazil: Risk decreases with increased group size. Behav. Ecol. Sociobiol. 49: 482–492. Google Scholar

7.

F. Chen , H. Zheng , K. Zhang , Z. Ouyang , J. Lan , H. Li , and Q. Shi 2013. Changes in soil microbial community structure and metabolic activity following conversion from native Pinus massoniana plantations to exotic Eucalyptus plantations. Forest Ecol. Mgt. 291: 65–72. Google Scholar

8.

M. J. Crawley 2007. The R Book. Statistical Papers, vol.50(2): 445–446. Springer Berlin/Heidelberg, Disponível em: < http://dx.doi.org/10.1007/s00362-008-0118-3>. Accessed: 28 Jul 2010. Google Scholar

9.

GreeneyH. F. , L. A. Dyer , and A. M. Smilanich 2012. Feeding by lepidopteran larvae is dangerous: A review of caterpillars chemical, physiological morphological, and behavioral defenses against natural enemies. ISJ. 9: 7–34. Google Scholar

10.

A. E. Hajek , and R. J. St. Leger 1994. Interactions between fungal pathogens and insect hosts. Annu. Rev. Entomol.39: 293–322. Google Scholar

11.

C. J. Klok , and S. L. Chown 1999. Assessing the benefits of aggregation: thermal biology and water relations of anomalous emperor moth caterpillars. Funct. Ecol. 13: 417–427. Google Scholar

12.

S. Kobayashi 1968. Estimation of the individual number entering each developmental stage in an insect population. Res. Popul. Ecol. 10: 40–44. Google Scholar

13.

W. P. Lemos , F. S. Ramalho , J. E. Serrão , and J. C. Zanuncio 2003. Effects of diet on development of Podisus nigrispinus (Dallas) (Het., Pentatomidae), a predator of the cotton leafworm. J. Appl. Entomol. 127: 389–395. Google Scholar

14.

J. T. Lill , and R. J. Marquis 2001. The effects of leaf quality on herbivore performance and attack from natural enemies. Oecologia 126: 418–428. Google Scholar

15.

T. Matsumoto , T. Itioka , and T. Nishida 2004. Is spatial density-dependent parasitism necessary for successful biological control? Testing a stable host-parasitoid system. Entomol. Exp. Appl. 110: 191–200. Google Scholar

16.

R. S. Medeiros , F. S. Ramalho , J. C. Zanuncio , and J. E. Serrão 2003. Effect of temperature on life table parameters of Podisus nigrispinus (Het.: Pentatomidae) fed with Alabama argillacea (Lep., Noctuidae) larvae. J. Appl. Entomol. 127: 209–213. Google Scholar

17.

A. F. Murta , F. T. O. Ker , D. B. Costa , M. M. Espírito-Santo , and M. L. Faria 2008. Controle biológico natural de Euselasia apiasoan (Dahman) (Lepidoptera: Riodinidae) por Trichogramma maxacalii (Voegelé e Pointel) (Hymenoptera: Trichogrammatidae): efeitos de remanescentes de Mata Atlântica e parasitismo independente da densidade. Neotrop. Entomol. 37: 229– 232. Google Scholar

18.

H. N. Oliveira , J. C. Zanuncio , D. Pratissoli , and I. Cruz 2000. Parasitism rate and viability of Trichogramma maxacalii (Hym.: Trichogrammatidae) parasitoid of the Eucalyptus defoliator Euselasia apison (Lep.: Riodinidae), on eggs of Anagasta kuehniella (Lep.: Pyralidae), Forest Ecol. Mgt. 130: 1–6. Google Scholar

19.

F. E. Palmer , D. R. Emery , J. Stemmler , and J. T. Staley 1987. Survival and growth of microcolonial rock fungi as affected by temperature and humidity. New Phytologist 107: 155–162. Google Scholar

20.

C. Perônico 2009. Preenchimento sedimentar de lagos assoreados na região do médio Rio Doce, Minas Gerais. Thesis (Ph.D.). Universidade Federal de Ouro Preto. Departamento de Geologia. 453 pp. Google Scholar

21.

D. Pratissoli , U. R. Vianna , H. B. Zago , and P. L. Pastori 2005. Capacidade de dispersão de Trichogramma em tomateiro estaqueado. Pesquisa Agropecuária Brasileira 40: 613–616. Google Scholar

22.

V. Radhika , C. Kost , S. Bartram , M. Heil , and W. Boland 2008. Testing the optimal defense hypothesis for two indirect defenses: extraforal nectar and volatile organic compounds. Planta 228: 449–457. Google Scholar

23.

T. Reader , and D. F. Hochuli 2003. Understanding gregariousness in a larval Lepidopteran: the roles of host plant, predation, and microclimate. Ecol. Entomol. 28: 729–737. Google Scholar

24.

S. P. Ribeiro , and Y. Basset 2007. Gall-forming and free-feeding herbivory along vertical gradients in a lowland tropical rainforest: the importance of leaf sclerophylly. Ecography 30: 663–672. Google Scholar

25.

R. J. Silva , V. H. P. Bueno , D. B. Silva , and M. V. Sampaio 2008. Tabela de vida de fertilidade de Lysiphlebus testaceipes (Cresson) (Hymenoptera, Braconidae, Aphidiinae) em Rhopalosiphum maidis (Fitch) e Aphis gossypii Glover (Hemiptera, Aphididae). Rev. Brasileira Entomol. 52: 124–130. Google Scholar

26.

M. A. Soares , J. C. Zanuncio , G. L. D. Leite , and J. E. Serrão 2009. Do Thyrinteina arnobia (Lepidoptera: Geometridae) use different defense behaviors against predators? J. Plant Dis. Prot. 116: 30–33. Google Scholar

27.

S. M. Sousa , M. L. Faria , and A. O. Latini 2010. Sobrevivência diferencial de pupas de Euselasia apisaon Dahman (Lepidoptera: Riodinidae) em plantas de subbosque nos plantios de eucalyptus de Belo Oriente, MG. Neotrop. Entomol. 39: 681–685. Google Scholar

28.

C. F. Sperber , K. Nakayama , M. J. Valverde , and F. S. Neves 2004. Tree species richness and density affect parasitoid diversity in cacao agroforestry Basic Appl. Ecol. 5: 241–251. Google Scholar

29.

J. Tews , U. Brose , V. Grimm , K. Tielborger , M. C. Wichmann , M. Schwager , and F. Jeltsch 2004. Animal species diversity driven by habitat heterogeneity/diversity: the importance of keystone structures. J. Biogeogr. 31: 79–92.  Google Scholar

30.

C. Thies , I. Steffan-Dewenter , and T. Tscharntke 2003. Effects of landscape context on herbivory and parasitism at different spatial scales. Oikos 101:18–25. Google Scholar

31.

G. C. Varley , and G. R. Gradwell 1970. Recent advances in insect population dynamics. Annu. Rev. Entomol. 15: 1–24. Google Scholar

32.

T. C. R. White 1984. The abundance of invertebrate herbivores in relation to the availability of nitrogen in stressed food plants. Oecologia 63: 90–105. Google Scholar

33.

T. V. Zanuncio , J. C. Zanuncio , M. M. M. Miranda , and A. G. B. Medeiros 1998. Effect of plantation age on diversity and population fluctuation of Lepidoptera collected in Eucalyptus plantations in Brazil. Forest Ecol. Mgt. 108: 91–98. Google Scholar

34.

J. C. Zanuncio , T. V. Zanuncio , E. F. Teixeira , and F. S. Ramalho 2000. Temporal variations of Lepidoptera collected in an eucalyptus plantation in the State of Goiás, Brasil. Netherlands J. Zool. 50: 435–443. Google Scholar

35.

J. C. Zanuncio , T. V. Zanuncio , F. A. Freitas , and D. Pratissoli 2003. Population density of Lepidoptera in a plantation of Eucalyptus urophylla in the State of Minas Gerais, Brazil. Animal Biol. 53: 17–26. Google Scholar
Luiz Eduardo Macedo-Reis, Luiz Gustavo Souto Soares, Maurício Lopes De Faria, Mario Marcos Do Espírito Santo, and José Cola Zanuncio "Survival of a Lepidopteran Defoliator of Eucalyptus is Influenced by Local Hillside and Forest Remnants in Brazil," Florida Entomologist 96(3), 941-947, (1 September 2013). https://doi.org/10.1653/024.096.0331
Published: 1 September 2013
JOURNAL ARTICLE
7 PAGES


SHARE
ARTICLE IMPACT
Back to Top