Abstracts
The objective of this work was to compare the biology of Chinavia impicticornis and C. ubica (Hemiptera: Pentatomidae), two species of stinkbugs that occur as secondary pests in soybean. Life table procedures were used for evaluating nymphs, and fecundity tables for evaluating adults, in order to establish the demographics of the two species. The two species have similar demographic parameters, and the development of immature stages, from egg to adult, had similar duration periods of approximately 30 days. In both species, eggs and second-instar nymphs were the stages with higher mortality. Total egg production did not differ between females of both species. Fecundity and survival curves for adults showed similar trends in both species. However, C. ubica had greater potential to increase its populations, since its fecundity parameters were significantly higher than those of C. impicticornis. Moreover, the generational time and the time required to double the population size were shorter in C. ubica. Prolonged longevity, long oviposition period, high fecundity, and the ability to rapidly increase their populations indicate that both species can become potential pests in favorable environments.
Glycine max ; age-specific fecundity; life table; mass rearing; reproductive potential; stinkbugs.
O objetivo deste trabalho foi comparar a biologia de Chinavia impicticornis e de C. ubica (Hemiptera: Pentatomidae), duas espécies de percevejos que ocorrem como pragas secundárias em soja. Foram utilizados procedimentos de tabelas de vida para a avaliação de ninfas, e tabelas de fertilidade para a de adultos, no intuito de estabelecer os parâmetros demográficos das duas espécies. As duas espécies apresentam parâmetros demográficos similares, e o desenvolvimento dos estágios imaturos, de ovo a adulto, apresentou duração similar, de aproximadamente 30 dias. Nas duas espécies, ovos e ninfas do segundo instar foram os estágios com maior mortalidade. A produção total de ovos não diferiu entre as fêmeas de ambas as espécies. As curvas de fecundidade e de sobrevivência para adultos mostraram tendências semelhantes nas duas espécies. Entretanto, C. ubica apresentou maior potencial de aumentar suas populações, uma vez que seus parâmetros de fecundidade foram significativamente maiores do que os de C. impicticornis. Além disso, o tempo generacional e o tempo necessário para dobrar a população em tamanho foram mais curtos em C. ubica. A longevidade prolongada, o longo período de oviposição, a alta fertilidade e a capacidade de aumentar rapidamente suas populações indicam que ambas as espécies podem tornar-se pragas potenciais, em ambientes favoráveis.
Glycine max ; fecundidade por idade; tabela de vida; criação em massa; potencial reprodutivo; percevejos.
Introduction
Chinavia impicticornis (Stål, 1872) and Chinavia
ubica (Rolston, 1983) (Hemiptera: Pentatomidae) are sympatric species of
pentatomids known as green stinkbugs. They have been reported as minor components of the
stinkbug pest complex, which is economically important in many crops, mainly Solanaceae
and Leguminosae (Panizzi et al., 2000PANIZZI, A.R.; MCPHERSON, J.E.; JAMES, D.G.; JAVAHERY, M.; MCPHERSON,
R.M.Stink bugs (Pentatomidae). In: SCHAEFER, C.W.; PANIZZI, A.R. (Ed.). Heteroptera
of economic importance. Boca Ratón: CRC Press, 2000. p.421-474.). These
species were formerly considered to belong to the genus Acrosternum
Fieber, 1860, but the taxonomic position of some Afrotropical species and of all
Nearctic and Neotropical species was reviewed, which reorganized the subgenus
Chinavia as a valid genus (Schwertner &
Grazia, 2006SCHWERTNER, C.F.; GRAZIA, J.Descrição de seis espécies de Chinavia
(Hemiptera, Pentatomidae, Pentatominae) da América do Sul. Iheringia. Série Zoologia,
v.96, p.237-248, 2006. DOI: 10.1590/S0073-47212006000200015.
https://doi.org/10.1590/S0073-4721200600...
).
In Brazil, 32 Chinavia species have been recorded, from which 18 are
considered potential pests, exploiting a large number of plant families (Panizzi et al., 2000PANIZZI, A.R.; MCPHERSON, J.E.; JAMES, D.G.; JAVAHERY, M.; MCPHERSON,
R.M.Stink bugs (Pentatomidae). In: SCHAEFER, C.W.; PANIZZI, A.R. (Ed.). Heteroptera
of economic importance. Boca Ratón: CRC Press, 2000. p.421-474.; Schwertner & Grazia, 2006SCHWERTNER, C.F.; GRAZIA, J.Descrição de seis espécies de Chinavia
(Hemiptera, Pentatomidae, Pentatominae) da América do Sul. Iheringia. Série Zoologia,
v.96, p.237-248, 2006. DOI: 10.1590/S0073-47212006000200015.
https://doi.org/10.1590/S0073-4721200600...
, 2007SCHWERTNER, C.F.; GRAZIA, J.O gênero Chinavia Orian (Hemiptera,
Pentatomidae, Pentatominae) no Brasil, com chave pictórica para os adultos. Revista
Brasileira de Entomologia, v.51, p.416-435, 2007. DOI:
10.1590/S0085-56262007000400005.
https://doi.org/10.1590/S0085-5626200700...
; Panizzi, 2007PANIZZI, A.R. Nutritional ecology of plant feeding arthropods and IPM.
In: KOGAN, M.; JEPSON, P. (Ed.). Perspectives in ecological theory and integrated
pest management. New York: Cambridge University Press, 2007. p.170-222. DOI:
10.1017/CBO9780511752353.007.
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). Chinavia
impicticornis and C. ubica have wide
geographical distribution, being found in all Brazilian regions (Schwertner & Grazia, 2007SCHWERTNER, C.F.; GRAZIA, J.O gênero Chinavia Orian (Hemiptera,
Pentatomidae, Pentatominae) no Brasil, com chave pictórica para os adultos. Revista
Brasileira de Entomologia, v.51, p.416-435, 2007. DOI:
10.1590/S0085-56262007000400005.
https://doi.org/10.1590/S0085-5626200700...
). In crops, both species are recorded
mainly in soybean (Panizzi et al., 2000PANIZZI, A.R.; MCPHERSON, J.E.; JAMES, D.G.; JAVAHERY, M.; MCPHERSON,
R.M.Stink bugs (Pentatomidae). In: SCHAEFER, C.W.; PANIZZI, A.R. (Ed.). Heteroptera
of economic importance. Boca Ratón: CRC Press, 2000. p.421-474.).
Although they have not yet been reported as major pests, C.
impicticornis and C. ubica may become
increasingly destructive secondary pests, since they are found feeding and ovipositing
in several important crops (Panizzi et al.,
2000;PANIZZI, A.R.; MCPHERSON, J.E.; JAMES, D.G.; JAVAHERY, M.; MCPHERSON,
R.M.Stink bugs (Pentatomidae). In: SCHAEFER, C.W.; PANIZZI, A.R. (Ed.). Heteroptera
of economic importance. Boca Ratón: CRC Press, 2000. p.421-474.)Panizzi, 2007PANIZZI, A.R. Nutritional ecology of plant feeding arthropods and IPM.
In: KOGAN, M.; JEPSON, P. (Ed.). Perspectives in ecological theory and integrated
pest management. New York: Cambridge University Press, 2007. p.170-222. DOI:
10.1017/CBO9780511752353.007.
https://doi.org/10.1017/CBO9780511752353...
.
In Central Brazil, populations of stinkbugs should be evaluated in monitoring programs
in order to avoid an epidemic growth that may result in economic damage to soybean crops
(Corrêa-Ferreira & Azevedo, 2002CORRÊA-FERREIRA, B.S.; AZEVEDO, J. de. Soybean seed damage by different
species of stink bugs. Agricultural Forest Entomology, v.4, p.145-150, 2002. DOI:
10.1046/j.1461-9563.2002.00136.x.
https://doi.org/10.1046/j.1461-9563.2002...
). In
addition to direct feeding damage, stinkbugs are known to facilitate infection by plant
pathogens such as bacteria and yeast (Daugherty,
1967DAUGHERTY, D.M. Pentatomidae as vectors of yeast-spot disease of
soybeans. Journal of Economic Entomology, v.60, p.147-152, 1967. DOI:
10.1093/jee/60.1.147.
https://doi.org/10.1093/jee/60.1.147....
; Clarke & Wilde, 1970CLARKE, R.G.; WILDE, G.E. Association of the green stink bug and the
yeast-spot disease organism of soybeans. I. Length of retention, effect of molting,
isolation from feces and saliva. Journal of Economic Entomology, v.63, p.200-204,
1970. DOI: 10.1093/jee/63.1.200.
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).
The morphology of the immature stages and some biological aspects of these two
Chinavia species have already been reported (Grazia et al., 1982GRAZIA, J.; DEL VECCHIO, M.C.; HILDEBRAND, R. Estudo das ninfas de
pentatomídeos (Heteroptera) que vivem sobre soja [Glycine max (L.) Merrill]: IV -
Acrosternum impicticorne (Stal, 1872). Anais da Sociedade Entomológica do Brasil,
v.11, p.261-268, 1982., Schwertner et
al., 2002SCHWERTNER, C.F.; ALBUQUERQUE, G.S.; GRAZIA, J.Descrição dos estágios
imaturos de Acrosternum (Chinavia) ubicum Rolston (Heteroptera: Pentatomidae) e
efeito do alimento no tamanho e coloração das ninfas. Neotropical Entomology, v.31,
p.571-579, 2002. DOI: 10.1590/S1519-566X2002000400009.
https://doi.org/10.1590/S1519-566X200200...
), and a preliminary laboratory study showed that
C. impicticornis and C.
ubica have similar development time, high fecundity (Laumann et al., 2006LAUMANN, R.A.; AQUINO, M.F.S.; MOTTA, L.S.M.; SANTOS, H.M.; MORAES,
M.C.B.; BORGES, M.Parâmetros biológicos de populações de Chinavia ubica e Chinavia
impicticornis (Hemíptera: Pentatomidae) do Distrito Federal. Brasília: Embrapa
Recursos Genéticos e Biotecnologia, 2006. (Comunicado técnico, 150).), and an efficient intraspecific communication
during the reproductive stage, by means of chemical and vibratory signals (Moraes et al., 2005MORAES, M.C.B.; LAUMANN, R.A.; COKL, A.; BORGES, M.Vibratory signals of
four Neotroprical stink bug species. Physiological Entomology, v.30, p.175-188, 2005.
DOI: 10.1111/j.1365-3032.2005.00446.
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), 2008MORAES, M.C.B.; PAREJA, M.; LAUMANN, R.A.; BORGES, M.The chemical
volatiles (semiochemicals) produced by neotropical stink bugs (Hemiptera:
Pentatomidae). Neotropical Entomology, v.37, p.489-505, 2008. DOI:
10.1590/S1519-566X2008000500001.
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.
The reasons and the means by which insect populations increase are central questions in
basic and applied ecology (Laughlin, 1965LAUGHLIN, R. Capacity for increase: a useful population statistic.
Journal of Animal Ecology, v.34, p.77-91, 1965. DOI: 10.2307/2370.; Royama, 1981ROYAMA, T. Evaluation of mortality factors in insect life table
analysis. Ecological Monographs, v.51, p.495-505, 1981. DOI:
10.2307/2937326.
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; Peterson et al., 2009PETERSON, R.K.D.; DAVIS, R.S.; HIGLEY, L.G.; FERNANDES, O.A. Mortality
risk in insects. Environmental Entomology, v.38, p.2-10, 2009. DOI:
10.1603/022.038.0102.
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). Life table studies from laboratory data can help
answering these questions (Royama, 1981ROYAMA, T. Evaluation of mortality factors in insect life table
analysis. Ecological Monographs, v.51, p.495-505, 1981. DOI:
10.2307/2937326.
https://doi.org/10.2307/2937326....
). Life
table studies give basic information on survivorship, development, and reproduction rate
of insect species, and can reveal their most vulnerable stage under specified
conditions. These information help identifying specific events, such as death of
immatures and reproductive rates, which can be used to improve rearing techniques.
Moreover, they provide population growth indicators that could help establishing control
strategies (Southwood, 2000SOUTHWOOD, T.R.E. The construction, description and analysis of
age-specific life tables. In: SOUTHWOOD, T.R.E.; HENDERSON, P.A. (Ed.). Ecological
methods. 3rd ed. Oxford: Blackwell Science, 2000. p.404-436. DOI:
10.1007/978-94-009-1225-0.
https://doi.org/10.1007/978-94-009-1225-...
; Yu et al., 2005YU, J.-Z.; CHI, H.; CHEN, B.-H. Life table and predation of Lemnia
biplagiata (Coleoptera: Coccinellidae) fed on Aphis gossypii (Homoptera: Aphididae)
with a proof on relationship among gross reproduction rate, net reproduction rate,
and preadult survivorship. Annals of the Entomological Society of America, v.98,
p.475-482, 2005. DOI: 10.1603/0013-8746.
https://doi.org/10.1603/0013-8746....
; Polanco et al., 2011POLANCO, A.M.; BREWSTER, C.C.; MILLER, D.M. Population growth potential
of the bed bug, Cimex lectularius L.: a life table analysis. Insects, v.2, p.173-185,
2011. DOI: 10.3390/insects2020173.
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). For example, short developmental time together with
high fecundity and longevity, on a given host plant, usually indicate greater
suitability of the host to support infestation and increasing population of the species
(Southwood, 2000SOUTHWOOD, T.R.E. The construction, description and analysis of
age-specific life tables. In: SOUTHWOOD, T.R.E.; HENDERSON, P.A. (Ed.). Ecological
methods. 3rd ed. Oxford: Blackwell Science, 2000. p.404-436. DOI:
10.1007/978-94-009-1225-0.
https://doi.org/10.1007/978-94-009-1225-...
).
The objective of this work was to compare the biology of C. impicticornis and C. ubica, two species that occur as secondary pests in soybean.
Materials and Methods
Adults of C. impicticornis and C. ubica came from colonies maintained for five generations in the Semiochemical Laboratory of Embrapa Recursos Genéticos e Biotecnologia, located in Brasília, Distrito Federal, Brazil; and voucher specimen were deposited in the institution's insect collection. The insects were reared in 8-L transparent plastic containers, and fed a standard diet composed of green bean pods (Phaseolus vulgaris L.), dry soybean seeds (Glycine max L.), raw peanuts (Arachis hypogaea L.), sunflower seeds (Helianthus annuus L.), and water. A 15-cm2 plastic mesh (~40 meshes) was placed against the inner wall of each container to serve as oviposition substrate and shelter for the bugs. The containers were covered with voile and kept at 26±1ºC and at 65±10% relative humidity.
In order to build a stage-specific life table, egg masses from each species (78 egg masses with 993 eggs for C. impicticornis, and 73 egg masses with 1,945 eggs for C. ubica) were collected from the colony, placed in Petri dishes (9 cm in diameter x 2 cm in height) at the density of 100 eggs per dish, and inspected daily for egg hatching, survival, and development progress, from first to second instar. As food supply and source of humidity, a green bean pod was offered inside the Petri dishes. After the second instar was reached, nymphs of C. impicticornis (n=248) and C. ubica (n=470) were transferred to the 8-L transparent plastic containers in groups of ~100 nymphs per container, which represented the jointed nymphs from 2 to 5 Petri dishes, in order to complete their development. The food source was the standard diet described before. Development time (time when half + 1 of the nymphs from each group molt into the following instar) and survival rate (lx = proportion of individuals alive in each instar, calculated as the proportion from the initial number of individuals, i.e. eggs) of each immature stage were calculated for each species. Survivorship curves were drawn from egg to adult stage.
Males and females - emerged on the same day from the nymphs reared in the above conditions - were paired (1 female and 1 male) and transferred to 250-mL capacity oviposition cages, with the same food substrate previously described. A total of 50 couples of C. impicticornis and 45 couples of C. ubica were observed daily, and sexual maturity, age at first oviposition, oviposition period, and longevity were recorded. The number of egg masses, the number of eggs per mass, and the total lifetime fecundity (total eggs per female) were also quantified. Age-specific fecundity (mx = mean number of females per female per day) was estimated for each species, as the product between the mean number of eggs per female per day, the mean immature survivorship (from the estimation of immature survivorship), and the female rate (0,5), considering the typical sex rate of the species (1:1, female: male).
Curves of the immature stages of each species were compared with the Kaplan-Meier (1958)KAPLAN, E.L.; MEIER, P. Nonparametric estimation from incomplete
observations. Journal of the American Statistical Association, v.53, p.457-481, 1958.
DOI: 10.1080/01621459.1958.10501452.
https://doi.org/10.1080/01621459.1958.10...
survival analysis and log-rank
test. The development time of each immature stage and the total developmental time of
each species were compared by generalized linear models (GLMs) and deviance analyses,
using models with inverse Gaussian error distribution and the F test. The same
procedures were used to compare the longevity of males and females between species. The
total number of egg masses per female and the total number of eggs per female were
compared between species by the GLM and deviance analyses, using models with Poisson and
quasi-Poisson error distribution, respectively, and the c2 test. The number
of eggs per egg mass was compared between species with a GLM, using species as fixed
factor and individual as a random factor, as well as Poisson distribution of errors for
the models.
Data from female age (x = computed as days in adult life + mean development time of
immature stages), survivorship (lx), and specific fecundity (mx)
were used to estimate the mean and standard deviation of fecundity table parameters
using the Life Table computer program (Maia et al.,
2000MAIA, A. de H.N.; LUIZ, A.J.B.; CAMPANHOLA, C. Statistical inference on
associated fertility life table parameters using jackknife technique: computational
aspects. Journal of Economic Entomology, v.93, p.511-518, 2000. DOI:
10.1603/0022-0493-93.2.511.
https://doi.org/10.1603/0022-0493-93.2.5...
), with functions and procedures embedded on the SAS System for Windows
(SAS Institute, Cary, NC, USA). This program uses the jackknife technique to estimate
life table parameters (Meyer et al., 1986MEYER, J.S.; INGERSOLL, C.G.; MCDONALD, L.L.; BOYCE, M.S. Estimating
uncertainty in population growth rates: jackknife vs. bootstrap techniques. Ecology,
v.67, p.1156-1166, 1986. DOI: 10.2307/1938671.
https://doi.org/10.2307/1938671....
). The
estimated parameters, following the definitions of Birch
(1948)BIRCH, L.C. The intrinsic rate of natural increase of an insect
population. Journal of Animal Ecology, v.17, p.15-26, 1948. DOI:
10.2307/1605.
https://doi.org/10.2307/1605....
and Southwood (2000)SOUTHWOOD, T.R.E. The construction, description and analysis of
age-specific life tables. In: SOUTHWOOD, T.R.E.; HENDERSON, P.A. (Ed.). Ecological
methods. 3rd ed. Oxford: Blackwell Science, 2000. p.404-436. DOI:
10.1007/978-94-009-1225-0.
https://doi.org/10.1007/978-94-009-1225-...
, were: net
reproductive rate (Ro = ∑lxmx), which represents the number
of females per female per generation; intrinsic rate of increase (rm =
lnRo/T), which expresses the instantaneous production of females per female; daily
finite rate of increase (λ = rm, in females per female per day); mean
generation time (T = ∑mxlxx/Ro); and time to double
population in size (DT = In(2)/rm).
Life Table parameters estimated for each species were compared by t tests, using the mean from the jackknife estimates of their respective variances. All statistical tests were performed at 5% probability.
Results and Discussion
The total development time from egg hatching to adult emergency did not differ between C. impicticornis and C. ubica (Table 1). Chinavia impicticornis took less time to complete its initial development stages (eggs and first- and second-instar nymphs) than C. ubica; however, the time length required to complete the third and the fourth nymphal stages was higher in the former species, and the development time of the fifth nymphal stage did not show statistical differences between species.
Development time of immature stages, male and female longevity, and female fecundity of Chinavia impicticornis and Chinavia ubica fed on green bean pods, dry soybean seeds, raw peanuts, and sunflower seeds, at 26±1ºC, 65±10% relative humidity, and photoperiod of 14:10 hours light:dark.
Similar egg development time was reported for other Chinavia species:
6.8 days for C. marginatum Palisot de Beauvois, 1817; 8 days
for C. apicicornis Spinola, 1852; 6 days for C. bella
Rolston, 1983; 6.7 days for C. longicorialis Breddin, 1901;
8.4 days for C. obstinata Stål, 1860; and 8 days for C.
pengue Rolston, 1983 (La Porta & Avalos,
1993LA PORTA, N.C.; AVALOS, D.S.Aspectos biológicos de Acrosternum
apicicorne (Spinola, 1862) (Hemiptera, Pentatomidae). Agriscientia, v.10, p.45-49,
1993.; Avalos & La Porta, 1996AVALOS, D.S.; LA PORTA, N.C. Biología de Acrosternum bellum Rolston,
1983 (Hemiptera: Pentatomidae). Agriscientia, v.13, p.25-30, 1996.;
Matesco et al., 2007MATESCO, V.C.; SCHWERTNER, C.F.; GRAZIA, J.Descrição dos estágios
imaturos e biologia de Chinavia pengue (Rolston) (Hemiptera, Pentatomidae). Revista
Brasileira de Entomologia, v.51, p.93-100, 2007. DOI:
10.1590/S0085-56262007000100016.
https://doi.org/10.1590/S0085-5626200700...
, 2009MATESCO, V.C.; SCHWERTNER C.F.; GRAZIA, J.Morphology of the immatures
and biology of Chinavia longicorialis (Breddin) (Hemiptera: Pentatomidae).
Neotropical Entomology, v.38, p.74-82, 2009. DOI:
10.1590/S1519-566X2009000100007.
https://doi.org/10.1590/S1519-566X200900...
). However, the development time from egg to adult registered
for these species was longer than those obtained for C. impicticornis
and C. ubica: 42 days for C. marginatum; 45.3 days
for C. apicicornis; 38.5 days for C. bella; 86 days
for C. obstinate; 45.7 days for C. pengue; and 39
days for C. longicorialis (Hallman et
al., 1992HALLMAN, G.J.; MORALES, C.G.; DUQUE, M.C. Biology of Acrosternum
marginatum (Heteroptera: Pentatomidae) on common beans. Florida Entomologist, v.75,
p.190-196, 1992.; La Porta & Avalos, 1993LA PORTA, N.C.; AVALOS, D.S.Aspectos biológicos de Acrosternum
apicicorne (Spinola, 1862) (Hemiptera, Pentatomidae). Agriscientia, v.10, p.45-49,
1993.;
Avalos & La Porta, 1996AVALOS, D.S.; LA PORTA, N.C. Biología de Acrosternum bellum Rolston,
1983 (Hemiptera: Pentatomidae). Agriscientia, v.13, p.25-30, 1996.; Matesco et al., 2003MATESCO, V.C.; SCHWERTNER, C.F.; GRAZIA, J.Imaturos de pentatomídeos
(Hemiptera, Heteroptera): morfologia e biologia de Acrosternum obstinatum. Iheringia.
Série Zoologia, v.93, p.81-88, 2003. DOI:
10.1590/S0073-47212003000100009.
https://doi.org/10.1590/S0073-4721200300...
, 2007MATESCO, V.C.; SCHWERTNER, C.F.; GRAZIA, J.Descrição dos estágios
imaturos e biologia de Chinavia pengue (Rolston) (Hemiptera, Pentatomidae). Revista
Brasileira de Entomologia, v.51, p.93-100, 2007. DOI:
10.1590/S0085-56262007000100016.
https://doi.org/10.1590/S0085-5626200700...
, 2009MATESCO, V.C.; SCHWERTNER C.F.; GRAZIA, J.Morphology of the immatures
and biology of Chinavia longicorialis (Breddin) (Hemiptera: Pentatomidae).
Neotropical Entomology, v.38, p.74-82, 2009. DOI:
10.1590/S1519-566X2009000100007.
https://doi.org/10.1590/S1519-566X200900...
). Besides
physiological particularities of each species, the differences observed between them may
also be due to: food sources, time (number of generations) in laboratory rearing,
environmental conditions, or rearing procedures.
The survival curves for the immature stages showed similar patterns for both species
(Figure 1), but differed statistically through
comparative analysis of the curves by the Kaplan-Meier survival analysis and log-rank
test (S=7.43, df=1, p=0.006). From the original cohort of C.
impicticornis (n = 993 eggs), the mortality rate was highest in the egg
stage (37.6%), followed by second-instar nymphs (47.4%); whereas in C.
ubica (starting with n=1,945 eggs), the mortality was 42.80% for eggs and
34.2% for fourth-instar nymphs. Since the insects were reared under controlled
conditions, where many environmental mortality factors present in the field - such as
temperature variations, precipitations, and presence of competitors or predators - are
absent, the mortality observed may be due to natural intrinsic mortality. However, even
in this case, rearing conditions cannot be disregarded. In general, diet composition and
environmental conditions influence insect performance (Parra, 2001PARRA, J.R.P.Técnicas de criação de insetos para programas de controle
biológico. 6.ed. Piracicaba: Fundação de Estudos Agrários Luiz Queiroz, 2001.
134p.; Cohen, 2004COHEN, A.C. Insects diets: science and technology. Boca Ratón: CRC
Press, 2004.; Parra et al., 2012PARRA, J.R.P.; PANIZZI, A.R.; HADDAD, M.L. Nutritional indices for
measuring insect food intake and utilization. In: PANIZZI, A.R.; PARRA, J.R.P. (Ed.).
Insect bioecology and nutrition for integrated pest management. Boca Ratón: CRC
Press, 2012. p.13-49.), particularly for the
Pentatomidae family (Panizzi, 1997PANIZZI, A.R.Wild hosts of pentatomids: ecological significance and role
in their pest status on crops. Annual Review of Entomology, v.42, p.99-122,
1997.; Silva et al., 2008SILVA, C.C.; LAUMANN, R.A.; BLASSIOLI, M.C.; PAREJA, M.; BORGES,
M.Euschistus heros mass rearing technique for the multiplication of Telenomus podisi.
Pesquisa Agropecuária Brasileira, v.43, p.575-580, 2008. DOI:
10.1590/S0100-204X2008000500004.
https://doi.org/10.1590/S0100-204X200800...
; Silva et al., 2011SILVA, F.A.C.; CALIZOTTI, G.S.; PANIZZI, A.R.Survivorship and egg
production of phytophagous pentatomids in laboratory rearing. Neotropical Entomology,
v.40, p.35-38, 2011. DOI: 10.1590/S1519-566X2011000100005.
https://doi.org/10.1590/S1519-566X201100...
), in laboratory colonies. Since the optimal rearing
conditions are not know for C. ubica and C.
impicticornis, a negative influence of the procedures and environmental
conditions adopted in the present work could still have had a significant influence on
their development.
Age-specific survivorship of immature stages of Chinavia impicticornis and C. ubica, fed on green bean pods, dry soybean seeds, raw peanuts, and sunflower seeds at 26±1°C, 80±10% relative humidity, and photoperiod of 14:10 hours light:dark. lx is the survivorship, calculated as the proportion from the initial number of individuals, i.e. eggs, in this case n=993 for C. impicticornis and n=1,945 for C. ubica. N I to N V refer to first- to fifth-instar nymphs, respectively.
Therefore, for C. ubica and C. impicticornis mass
rearing purposes, nymphal mortality should be properly addressed and minimized.
According to Nath & Rai (2010)NATH, S.; RAI, A. Study of life table of Ceracris nigricornis laeta
(Orthoptera: Acrididae) in laboratory conditions. Romanian Journal of Biology -
Zoology, v.55, p.159-165, 2010., reduced
survival in early stages, with mortality prior to sexual maturity, plays a key role in
decreasing the population size. Matesco et al.
(2009)MATESCO, V.C.; SCHWERTNER C.F.; GRAZIA, J.Morphology of the immatures
and biology of Chinavia longicorialis (Breddin) (Hemiptera: Pentatomidae).
Neotropical Entomology, v.38, p.74-82, 2009. DOI:
10.1590/S1519-566X2009000100007.
https://doi.org/10.1590/S1519-566X200900...
observed high mortality (82%) of C. longicornis from
first- to fifth-instar nymphs, which made it impossible to keep the insects in the
laboratory up to the second generation. Moreover, females of this species did not
display copulatory behavior and egg-laying activity. The authors suggest a clear
influence of the diet on the mortality of immature stages of C.
longicornis because egg and first-instar nymph showed lower mortality (Matesco et al., 2009MATESCO, V.C.; SCHWERTNER C.F.; GRAZIA, J.Morphology of the immatures
and biology of Chinavia longicorialis (Breddin) (Hemiptera: Pentatomidae).
Neotropical Entomology, v.38, p.74-82, 2009. DOI:
10.1590/S1519-566X2009000100007.
https://doi.org/10.1590/S1519-566X200900...
). Wild hosts, besides some
other cultivated plants, are fundamental for immature and adult performance of stinkbugs
(Panizzi, 1997PANIZZI, A.R.Wild hosts of pentatomids: ecological significance and role
in their pest status on crops. Annual Review of Entomology, v.42, p.99-122,
1997.). Therefore, one alternative
for reducing the mortality of immature instars of C. ubica and
C. impicticornis could be the incorporation of some wild plants in
their diets.
The species differed as to mean adult longevity of males and females. Chinavia
impicticornis had higher longevity, with its males living 31.5% more than
C. ubica males, and its females living 38% more than C.
ubica females (Table 1). As
C. impicticornis and C. ubica were reared under the
same diet and environmental conditions, the differences observed in adult longevity
could represent natural differences between the species or a better adaptation of
C. impicticornis adults to laboratory conditions. Maximal life span
of females differed between both species: 121 days for C. impicticornis
and 80 days for C. ubica (Figure
2). Mean adult longevity of C. impicticornis (78.0±29.8
days for males and 66.8±26.3 days for females) and C. ubica
(53.4±35.4 days for males and 41.4±29.1 days for females) was similar to the
ones reported for other pentatomid species under the same diet and laboratory
conditions, such as Euschistus heros (46.5±19.7 days for males and
52.2±19.7 days for females) (Costa et al.,
1998COSTA, M.L.M.; BORGES, M.; VILELA, E.F. Biologia reprodutiva de
Euschistus heros (F.) (Heteroptera: Pentatomidae). Anais da Sociedade Entomológica do
Brasil, v.27, p.559-568, 1998. DOI: 10.1590/S0301-80591998000400008.
https://doi.org/10.1590/S0301-8059199800...
) and Edessa meditabunda (63.3±8.0 days for males
and 60.5±9.9 days for females) (Silva et al.,
2012SILVA, C.C.A.; LAUMANN, R.A.; FERREIRA, J.B.C.; MORAES, M.C.B.; BORGES,
M.; ČOKL, A. Reproductive biology, mating behavior, and vibratory communication of
the brown-winged stink bug, Edessa meditabunda (Fabr.) (Heteroptera: Pentatomidae).
Psyche, article ID 598086, 2012. DOI: 10.1155/2012/598086.
https://doi.org/10.1155/2012/598086....
).
Age-specific survivorship and fecundity of Chinavia impicticornis (A) and C. ubica (B) females fed on green bean pods, dry soybean seeds, raw peanuts, and sunflower seeds, at 26±1ºC, 65±10% relative humidity, and photoperiod of 14:10 hours light:dark. lx is the survivorship, calculated as the proportion from the initial number of individuals, i.e. eggs, in this case n=50; and mx is the age-specific fecundity, determined as the mean number of females per female per day.
Mated females of C. impicticornis started laying eggs at the age of
9.8±2 days from the final molt, and over the course of their lifetime an average of
13.5±7.3 egg masses were laid. Mated females of C. ubica started
ovipositing at the age of 10.3±1.8 days, and laid an average of 6.07±5.5 egg
masses, significantly lower than that of C. impicticornis
(c2
1,94 = 3, 30; p<0.001). The period required to reach sexual maturity,
between the final molt and the first copula, for both species, was shorter than those
reported for other Chinavia species, which took between 12.4 to 13.8
days (La Porta & Avalos, 1993LA PORTA, N.C.; AVALOS, D.S.Aspectos biológicos de Acrosternum
apicicorne (Spinola, 1862) (Hemiptera, Pentatomidae). Agriscientia, v.10, p.45-49,
1993.; Avalos & La Porta, 1996AVALOS, D.S.; LA PORTA, N.C. Biología de Acrosternum bellum Rolston,
1983 (Hemiptera: Pentatomidae). Agriscientia, v.13, p.25-30, 1996.). Chinavia
impicticornis laid egg masses with significant lower number of eggs
(14.3±1.7) than C. ubica (23.4±7.0) (GLM z=9.95; p<0.001).
Despite the differences in the number of eggs per egg mass, total egg production per
female between species did not show statistical differences (Table 1), because the lower number of egg masses in C.
ubica is offset by a higher number of eggs per egg mass.
Other species of Chinavia (C.
obstinata, C. pengue, and C.
longicorialis) showed similar fecundity values (Matesco et al., 2003MATESCO, V.C.; SCHWERTNER, C.F.; GRAZIA, J.Imaturos de pentatomídeos
(Hemiptera, Heteroptera): morfologia e biologia de Acrosternum obstinatum. Iheringia.
Série Zoologia, v.93, p.81-88, 2003. DOI:
10.1590/S0073-47212003000100009.
https://doi.org/10.1590/S0073-4721200300...
, 2007MATESCO, V.C.; SCHWERTNER, C.F.; GRAZIA, J.Descrição dos estágios
imaturos e biologia de Chinavia pengue (Rolston) (Hemiptera, Pentatomidae). Revista
Brasileira de Entomologia, v.51, p.93-100, 2007. DOI:
10.1590/S0085-56262007000100016.
https://doi.org/10.1590/S0085-5626200700...
, 2008MATESCO, V.C.; SCHWERTNER, C.F.; GRAZIA, J.Immature stages of Chinavia
musiva (Berg, 1878): a unique pattern in the morphology of Chinavia Orian, 1965
(Hemiptera, Pentatomidae). Journal of Natural History, v.42, p.1749-1763, 2008. DOI:
10.1080/00222930802124297.
https://doi.org/10.1080/0022293080212429...
) to those reported here.
Fecundity and survival curves for adults of both species showed similar trends (Figure 2). Female mortality showed lower rates in C. impicticornis than in C. ubica. Fecundity rate (mx) peaks showed similar values in both species, but in C. ubica, peaks were maintained with a lower number of oscillations and concentrated in a shorter period of time.
The net reproduction rate (Ro) did not differ significantly between species (Table 2), and both of them were able to increase in number, which reveals that laboratory conditions and food were adequate for rearing. However, the following parameters of fecundity tables differed significantly between species: intrinsic rate of natural increase (rm), finite rate of increase (λ), generation time (T), and doubling time (DT). According to these results, C. ubica had a higher capacity to increase its population in a shorter time, compared to C. impicticornis. The similarity in survivorship of immature stages and in fecundity of females of both species probably influenced this result, but C. ubica had progeny production centered in a shorter time (Figure 2). Therefore, if the species preserves this behavior in field conditions, C. ubica would have a higher capacity to increase its population in a shorter time and at higher rates than C. impicticornis.
Mean±standard deviation of fecundity life table parameters of Chinavia impicticornis and C. ubica fed on green bean pods, dry soybean seeds, raw peanuts, and sunflower seeds, at 26±1ºC, 80±10% relative humidity, and photoperiod of 14:10 hours light:dark.
The biologic potential of both species (i.e., the number of offspring produced in the
subsequent generation) is comparable to the ones observed in other pentatomid species,
such as the brown stinkbug, E. heros, reared under the
same laboratory conditions (Silva et al.,
2008SILVA, C.C.; LAUMANN, R.A.; BLASSIOLI, M.C.; PAREJA, M.; BORGES,
M.Euschistus heros mass rearing technique for the multiplication of Telenomus podisi.
Pesquisa Agropecuária Brasileira, v.43, p.575-580, 2008. DOI:
10.1590/S0100-204X2008000500004.
https://doi.org/10.1590/S0100-204X200800...
).
The results obtained in the present study indicate that both Chinavia species evaluated should be included in monitoring programs of stinkbugs in crops such as soybean and common beans.
Conclusions
-
The two congeneric species of stinkbugs, Chinavia impicticornis and C. ubica, have similar biological traits under laboratory conditions.
-
Prolonged longevity, long oviposition period, high fecundity, and the ability to rapidly increase their populations indicate that these species can become potential crop pests in favorable environments (climate and access to food).
-
Both species can be mass reared successfully under laboratory conditions.
-
Eggs and second-instar nymphs are the most susceptible and the key stages to focus on when thinking in mass rearing.
Acknowledgments
To International Foundation for Science (IFS), to Conselho Nacional de Desenvolvimento Científico e Tecnológico (CNPq), and to Fundação de Amparo à Pesquisa do Distrito Federal (FAPDF), for financial support; and to Dr. Jocelia Grazia from Universidade Federal do Rio Grande do Sul (UFRGS) and to Dr. Cristiano Feldens Schwertner from Universidade Federal de São Paulo (Unifesp), for their help on the identification of the insects.
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Publication Dates
-
Publication in this collection
May 2015
History
-
Received
30 May 2014 -
Accepted
31 Mar 2015