Effects of larval host plants on over-wintering preparedness and survival of the cotton bollworm, Helicoverpa armigera (Hübner) (Lepidoptera: Noctuidae)
Introduction
The cotton bollworm, Helicoverpa armigera (Hübner) (Lepidoptera: Noctuidae), is one of the most serious insect pests in China, Australia and India. This species has a wide range of host plants, including both cultivated and wild species, about one hundred and seventy two species of host plants from 40 families in Australia (Zalucki et al., 1994) and about 200 species from 30 families in China (Xu et al., 1958). Every year, the larvae of this species cause substantial damage to cotton, corn, tomato, kidney bean and other vegetable crops. In China alone, this insect caused several billion RMB losses per year during the 1990s, about 10 billion RMB of which (about 1.25 billion USA dollars) was a direct loss of plants in 1992 (www.stdaily.com/gb/stdaily/2005-10/20/content_444994.htm), before Bt plants had been planted widely. Over most of its range in China, this species produces four or five generations a year and over-winters as a diapausing pupa.
Diapause is an important strategy by which insects avoid unfavorable environmental conditions (Tauber et al., 1986; Danks, 1987). The main factors associated with diapause in insects are photoperiod and temperature (Hodkova and Socha, 1995; Nakai and Takeda, 1995). Other environmental factors, such as food quality (Tzanakakis et al., 1992), have received limited attention. Research on cold hardiness has emphasized the contribution of diapause (Tauber et al., 1986; Jiang and Zhang, 1997; Slachta et al., 2002), to the exclusion of possible host plant effects. Nonetheless, food has been shown to be a major factor regulating diapause for a few species of insects (Tauber et al., 1986), influencing the accumulation of energy needed for over-wintering (Zvereva, 2002). Host plant quality affects larval growth rate, the sensitive stage for diapause induction, and cold hardiness (Hunter and McNeil, 1997), which are particularly obvious in polyphagous insects. For example, Zvereva (2002) reported that host plant quality can disturb over-wintering preparedness and thus affect the over-wintering success of the leaf beetle, Chrysomela lapponica.
It is well known that insects must accumulate reserves of glycogen before they enter winter diapause (Sakurai et al., 1992). Moreover the accumulated low-molecular-weight sugars and/or sugar-alcohols during over-wintering (Storey and Storey, 1991) are closely correlated with the nutritive quality of host plants (Zvereva, 2002). In this paper, we confirmed that diapausing cotton bollworm pupae weighed more than non-diapausing pupae that had been raised under the same environmental conditions. Clearly, the potential for accumulating reserves is related to the nutritional quality of host plants. Our previous research, which agrees with results reported by Kidd and Orr (2001), suggested that host plants had a significant effect on the development of the immature stage and body weight of pupae of the cotton bollworm (Liu et al., 2004).
Host plants of the cotton bollworm have different nutritive values, which may affect the rate of development of larvae that feed on them and therefore influence the population dynamics of this pest (Ruan and Wu, 2001). The contributions of host plants to developing generations of the cotton bollworm are clear. The suitability of host plants can be ranked as follows: cotton > corn > legume > tobacco > tomato > hot pepper (Liu et al., 2004). To date, the influences of host plants on pupal survival and the cold-hardiness of over-wintering populations remain unclear.
In China, under natural conditions, the fourth or fifth over-wintering generation of the cotton bollworm has a wide range of potential host plants. Changes in cultivation practices have resulted in summer corn being planted on a large scale; corn and concurrently grown cotton, tobacco, and tomato crops supply food of differing quality for the larvae of the over-wintering generation (Lu and Xu, 1998). Differences in the nutritional levels of host plants in the field may affect the over-wintering potential, the over-wintering survival, and the intensity of outbreaks of this pest in the subsequent years. Diapause in the cotton bollworm, Helicoverpa armigera, is induced by the short photoperiod and low temperatures of autumn (Li and Xie, 1981; Wu and Guo, 1995) and is terminated by either high or low temperatures (Wu and Guo, 1995). In China, only diapausing pupae can successfully over-winter in the temperate zone. In the field, the cotton bollworm enters winter diapause in October and emerges from this state in late December, after which temperatures below the lowest threshold for pupal development prevent any activity until April of the following year (Jiang and Zhang, 1997). For insect herbivores, growth and development are often intimately linked to host plant quality (Bernays, 1990). Thus differences in the quality of host plants for the cotton bollworm might be expected to influence diapause occurrence and cold-hardiness of over-wintering pupae.
In this study, we reared newly hatched H. armigera larvae on five host plants, using artificial diet as a control. We measured the effects of larvae host plants on the over-wintering preparedness of pupae at the beginning of over-wintering (November). This information is essential to the development of a theoretical foundation for managing over-wintering populations and for improving forecasts of the population dynamics of this pest.
Section snippets
Insects, criteria for determining diapause, and host plants
A laboratory population of H. armigera was established by collecting full-grown larvae from cotton plants growing in the suburbs of Changsha, in the province of Hunan. The larvae were reared on an artificial diet with wheat germ as the main component (Wu and Gong, 1997) at 27 °C under a photoperiod of L:D=14:10 to prevent diapause. Newly hatched larvae were reared in groups until the 3rd instar, after which they were separated in individual glass tubes (2.0 cm dia.×8.0 cm high) to prevent
Effects of host plants on over-wintering preparedness of diapausing and non-diapausing pupae
Both fresh and dry mass of diapausing pupae were much heavier than the fresh and dry mass of non-diapausing pupae, and the diapausing pupae contained more lipids (mg/pupa) than did non-diapausing pupae (Table 1), which showed that larvae destined for diapause accumulate and store energy for over-wintering. The pupal weight and lipid gained, in both non-diapausing and diapausing pupae, varied significantly on different host plants (Table 1).
Over-winter reserve storage for diapausing pupae among different host plants
The pupal weight of the over-wintering population was
Discussion
Different host plants contain various nutrient levels, which may affect the ability of H. armigera pupae to over-winter. This study showed that for all the tested host plants, diapausing pupae of H. armigera are much heavier than non-diapausing pupae; this results is supported by our previous study on summer-diapausing pupae (Liu et al., 2006). Clearly, larvae destined to become diapausing pupae accumulate energy before diapause is induced, confirming that H. armigera belongs to the category of
Acknowledgements
The work was supported by National Basic Research Program of China (973 Program, No. 2006CB102006), the Chinese National Key Basic Research Development Program (No. G2000016210), Chinese Academy of Sciences Program (No. KSCX2-SW-103, No. KSCX2-1-02), the National Nature Sciences Fund (No. 30070128), and CAS Innovation Program. The authors thank Mr. Zeng Liangbin for his assistance in the laboratory and Emily Wheeler for editorial assistance.
References (48)
- et al.
Metabolic reserves associated with pupal diapause in the flesh fly, Sarcophaga crassipalpis
Journal of Insect Physiology
(1985) - et al.
Cold hardiness of Habrobracon hebetor (Say) (Hymenoptera: Braconidae), a parasitoid of pyralid moths
Journal of Insect Physiology
(2005) Dehydration in dormant insect
Journal of Insect Physiology
(2000)- et al.
Physiological and biochemical changes in summer and winter diapause and non-diapause pupae of the cabbage armyworm, Mamestra brassicae L. during long-term cold acclimation
Journal Insect Physiology
(2003) - et al.
A simple method for the isolation and purification of total lipids from animal tissues
Journal of Biological Chemistry
(1957) - et al.
Biochemistry and physiology of aestivo-hibernation in the adult apple blossom weevil, Anthonomus pomorum (Coleoptera: Curculionidae)
J. Insect Physiol.
(1996) - et al.
Physiology of drought tolerance and cold hardiness of the Mediterranean tiger moth Cymbalophora pudica during summer diapause
J. Insect Physiol.
(1998) - et al.
A true summer diapause induced by high temperature in the cotton bollworm, Helicoverpa armigera (Lepidoptera: Noctuidae)
Journal of Insect Physiology
(2006) - et al.
Feeding glucose or sucrose, but not trehalose, suppresses the starvation-induced premature pupation in the yellow-spotted longicorn beetle, Psacothes hilaris
Journal of Insect Physiology
(2005) - et al.
The effect of diet quality on physiological and life-history traits in the harvetman Pachylus paessleri
Journal of Insect Physiology
(2007)
Entering diapause is a prerequisite for successful cold-acclimation in adult Graphosoma lineatum (Heteroptera: Pentatomidae)
J. Insect Physiol.
Factors that influence freezing in the sub-Antarctic springtail Tullbergia Antarctica
Journal of Insect Physiology
Loss of supercooling ability in Cryptopygus antarcticus (Collembola: Isotomidae) associated with water uptake
Cryoletters
Evolution of phenotype variance: non-Mendelian parental influences on the phenotypic and genotypic components of the life-history traits in a generalist herbivore
Heredity
Colorimetric method for determination of sugars and related substances
Analytical Chemistry
Multiple range and multiple F tests
Biometrics
Timing of diapause initiation, metabolic changes and overwintering survival of the spruce budworm, Choristoneura fumiferana
Ecol. Entomol.
Effect of temperature on photoperiodic response in a selected nondiapause strain of Pyrrhocoris apterus (Heteroptera)
Physiol. Entomol.
Overwintering survival and spring emergence in Meligethes aeneus: effects of body weight, crowding, and soil treatment with Beauveria bassiana
Entomol. Exp. Appl.
Host-plant quality influences diapause and voltinism in a polyphagous insect herbivore
Ecology
Study of cold hardiness for diapaused pupae of cotton bollworm, Helicoverpa armigera
Journal of Nanjing Agricultural University
Comparative feeding and development of Pseudoplusia includens (Lepidoptera: Noctuidae) on kudzu and soybean foliage
Ann. Entomol. Soc. Am.
Cited by (74)
Different diets affecting biology, physiology and cold tolerance of Trogoderma granarium Everts (Coleoptera: Dermestidae)
2018, Journal of Stored Products ResearchCitation Excerpt :In many insect groups, the production and accumulation of sugars and polyhydric alcohols (polyols) mainly depended on energy reserves of insect as a result of its food quality (Storey and Storey, 1991). The results of present study showed a higher accumulation of trehalose and sorbitol in larvae reared on triticale and rye (as suitable diets), which is similar to Liu et al. (2007) results, who reported that larval diets affected the amount of energy reserves, such differences further influence the production of low-molecular-weight cryo-protectants, leading to differences in cold hardiness depending on their larval host plants. As it is evident from Tables 5 and 6, a strong supercooling capacity found among T. granarium larvae fed on triticale was perhaps related to the higher levels of low molecular weight cryoprotectants, especially trehalose, that were converted from glycogen.
Cold tolerance of the invasive oak lace bug, Corythucha arcuata
2023, Agricultural and Forest EntomologyPupae survival following fire in the frosted elfin (Callophrys irus)
2023, Agricultural and Forest Entomology