The cotton bollworm, Helicoverpa zea (Boddie) (Lepidoptera: Noctuidae), is a cosmopolitan pest that feeds on numerous wild and cultivated crops. This insect pest causes economic damage on many vegetable and commercial row cropping systems across the Western Hemisphere (Cohen et al. 1988; Blanco & Houston 2005). Helicoverpa zea is documented to infest > 20 cultivated plant species and > 75 wild non-cultivated hosts (Stadelbacher 1980; Stadelbacher et al. 1986; King 1994; Hardwick 1996; Blanco et al. 2002). Larvae of H. zea feed on different parts of host plants such as flowers, buds, stems, and leaves (Garcia 2006). Infestations and outbreak populations of H. zea cause significant economic damage to 2 major crop hosts in the southern US: corn (Zea mays L.; Poaceae) and cotton (Gossypium hirsutum L.; Malvaceae). Corn is considered significantly more attractive to H. zea when compared to other widely grown row crops including sorghum (Sorghum bicolor L.; Poaceae), soybean (Glycine max L. Merr.; Fabaceae), and tobacco (Nicotiana tobacum L.; Solanaceae) (Hardwick 1965; Johnson et al. 1975; Luttrell 1994; Capinera 2001; Luttrell & Jackson 2012, Rhino et al. 2014). Host plants have been well documented to have significant effects on insect development, reproductive capability, and survivorship including many noctuid species (Ellsbury et al. 1989; Razmjou et al. 2014; Barbosa et al. 2016; Fathipour et al. 2020).

Many studies have investigated the larval developmental differences in H. zea, primarily for standardized moth diets commonly used in laboratories for mass rearing and on a variety of crops producing Bacillus thuringiensis Berliner (Bacillales: Bacillaceae) (Bt) toxin such as corn and cotton (Little et al. 2019). Life tables and demographic data have been collected for many cultivated crops such as chickpea (Cicer arietinum L.; Fabaceae), tomato (Solanum lycopersicum L.; Solanaceae), and tobacco (Blanco et al. 2007; Anderson et al. 2013; Barbosa et al. 2016). A considerable body of work describing the influence of abiotic factors including temperature, d length, and humidity have been studied for H. zea (Harrell et al. 1979; Pullen et al. 1992; Parajulee et al. 1998; Morey et al. 2012; Chen et al. 2014). Research investigating the factors regulating diapause induction and termination of H. zea and other related species within the heliothine complex also have been well studied (Phillips & Newsom 1966; Benschoter 1968).

However, few studies have compared biological parameters of H. zea when reared on common weedy hosts. Baseline biological data for H. zea on different weedy plants will help identify risk in agroeco-systems and questions associated with H. zea survival and fecundity on hosts common across the mid-south. Crimson clover (Trifolium incarnatum L.; Fabaceae) and Japanese honeysuckle (Lonicera japonica Thunb.; Caprifoliaceae) are documented early season hosts of H. zea (Ellsbury et al. 1989; Pair 1994). Crimson clover is an early, cool season, annually grown cover crop throughout the southeastern US (Ellsbury et al. 1989). Historically, crimson clover has been cultivated across the southeastern US to control soil erosion and to stabilize highway rights of way (Power 1987). Across the mid-south, this practice continues and is actively managed by the state department of transportation providing an annual source of wild, first filial generation of field-collected H. zea (F₁) larvae. Japanese honeysuckle is a vining evergreen perennial weed that blooms twice a yr primarily from Apr to May and Sep to Nov across the mid-south. Japanese honeysuckle was introduced in about 1806 as an ornamental that escaped from cultivation around 1890, and subsequently has established throughout the eastern US (Hardt 1986; Pair 1994).

The availability and attractiveness of various non-cultivated hosts (i.e., weedy hosts) change through space and time across the landscape influencing local insect populations (Neunzig 1963; Sudbrink & Grant 1995; Kennedy & Storer 2000). Integrated pest management (IPM) programs require a detailed understanding of a pest's life cycle (Kogan 1998). These data may lead to identification of potential fitness costs associated with select host plants that may have detrimental impacts on H. zea in a given agroecosystem, such as increased developmental times and larval mortality, in addition to potential reductions in fecundity that may be exploited for decision making purposes (Cunningham & Zalucki 2014).

Therefore, the objectives of this study were to assess and compare biological parameters of H. zea when reared to pupation on crimson clover, white clover (Trifolium repens L.; Fabaceae), hairy vetch (Vicia villosa Roth; Fabaceae), kudzu (Pueraria montana (Lour.) Merr.; Fabaceae), and Japanese honeysuckle. In this study, we directly measured the average number of d until hatch, larval development, pupal development and biomass, percent adult emergence and survival, adult longevity, and fecundity for H. zea when reared to pupation (i.e., all life stages) on 5 different non-cultivated host plants commonly found across the mid-south.

Materials and Methods

DATA ANALYSIS

All measures of larval developmental time, pupal weight, emergence, and fecundity data were used to examine host plant effects by using analysis of variance (ANOVA) (SAS Institute 2013) and used the t-test to evaluate differences in gender. A Tukey's mean separation test (α = 0.05) was used to compare results among host plant species averaged across developmental measures when the host plant species was significant (Neter et al. 1985).

Table 1.

Mean (± SEM) of egg and larval developmental times (d), pupal weights (mg), and percentage survivorship of Helicoverpa zea reared on 5 different weedy hosts plants at 27 °C.

Results

Discussion

In this study the biological performance of H. zea was influenced significantly by the host plant. Based on our results, host plant played a significant role in all developmental stages of H. zea larvae, longevity of adults, and reproductive capability. However, results from our study indicated no significant differences across sex for any of the biological parameters measured. These results are consistent with many previous studies on biological parameters of important noctuid species when reared on cultivated, non-cultivated (i.e., weedy hosts), and meridic diets (Nutri-Soy, Archer Daniels Midland Co., Decatur, Illinois, USA; and wheat germ, Anacon Foods, Atkinson, Kansas, USA) (Ellsbury et al. 1989; Liu et al. 2004; Barbosa et al. 2016).

The experimental data presented in this study have some limitations. The original cohort used to measure egg hatching rate was lost due to an equipment malfunction. As a result, only neonates were available from the host plant specific colonies and new groups of 500 individuals were selected randomly and used for determining larval development periods. Last, within-instar mortality was not recorded, and larval mortality was calculated as the number of individuals that were unable to successfully pupate.

Table. 2.

Mean (± SEM) longevity of females and males (d), and fecundity (total) of Helicoverpa zea reared on 5 different weedy host plants at 27 °C.

Host plant suitability, measured in terms of mortality and fecundity are known to have significant variation on insects. Shorter developmental times and greater reproductive capability reflect the suitability of a given host (Tsai & Wang 2001). Larvae experienced significantly different developmental times when reared on each of the host plant species in this study (Table 1). When reared on hairy vetch and kudzu host plants, larvae took considerably less time to develop compared to all other hosts in this study. Similar variation was observed in the average time spent in the pupal stage. The combined developmental stages for larvae reared on honeysuckle had the shortest developmental period of 30 d, while larvae reared on other hosts took as long as 39 d to emerge (Table 1).

Pupal biomass of larvae that were reared on white clover, honeysuckle, and kudzu were among the heaviest observed (Table 1). Helicoverpa zea larvae reared on hairy vetch had among the lowest pupal weights observed of all host plant species. The developmental periods and pupal weights of H. zea observed in this study are comparable to those found in another study using the hosts crimson clover and wild honeysuckle (Gross & Young 1977; Ellsbury et al. 1989). Larval mortality was the lowest when reared on crimson and white clover with less than 42.1% and 27%, respectively. However, for all other host plant species larval mortality was in excess of 49% and reached 66% for H. zea when reared on hairy vetch. Emergence rates for larvae reared on crimson clover where the highest of all host plants (> 85%) (Table 1).

Longevity was highest for larvae reared on crimson clover and honeysuckle (> 8 d), and significantly limited when reared on kudzu (< 5 d) (Table 2). Significant differences in fecundity as measured by the total number of eggs laid per female were detected across each weedy host plant species (P < 0.05) (Table 2). The average number of eggs laid when reared on crimson clover, white clover, hairy vetch, honeysuckle, and kudzu were 553.5, 512.3, 288.2, 194.7, and 142.2, respectively.

Host plant antibiosis effects may have led to the reduced fitness and survival of H. zea observed in these studies and prolonged its developmental time frame. The increased larval development and pupal time may increase H. zea exposure to predation by natural enemies and other mortality factors (i.e., extreme temperatures or desiccation) (Sarfraz et al. 2006). Larval host plant experience has been shown to affect mate finding and oviposition substrate selection (Anderson et al. 2013). Variation observed across plant species may be explained by the nutritional quality of host plant tissue offered to insects (Awmack & Leather 2002). Previous research has shown that components of host plant quality such as nitrogen, free amino acids, and defensive metabolites are known to directly affect biological development and reproduction. Ellsbury et al. (1989) demonstrated the differences associated between crimson clover flowers and leaf tissue when offered to H. zea.

Larval development for H. zea reared on kudzu was among the shortest, pupal weights among the highest, and had the least number of eggs deposited (Table 2). This observation may be of particular importance given the vast geographic host range and aggressive nature of kudzu across the mid-south (Forseth & Innis 2004). Ellsbury et al. (1989) demonstrated that first to third instar H. zea readily bored into and fed upon crimson clover terminals and buds taking significantly more time to adult emergence, whereas larger instars who fed externally on flowers alone pupated and emerged faster. Conversely, our findings in this specific study indicate larvae reared from egg hatch exclusively on crimson clover flowers took significantly longer to hatch, having the longest larval and combined developmental periods across the study. A comparison of our crimson clover experiments with those of Ellsbury et al. (1989) suggest that the extended developmental duration observed in this study for early instars may be explained by a diet solely comprised of fresh crimson flowers and the absence of predators. However, when reared on either crimson or white clover flowers H. zea had the highest emergence and fecundity rates observed over the course of these experiments. When reared on honeysuckle, larvae had the shortest larval and combined developmental stages and the highest pupal biomass but suffered considerable mortality similar to kudzu and hairy vetch. Larvae reared on honeysuckle laid significantly more eggs than those reared on kudzu. Helicoverpa zea reared on hairy vetch were among the first to hatch and had the shortest developmental periods. However, this group had the smallest pupal weights observed across the study and experienced significant mortality (> 65%) (Table 1).

Implications from this study suggest that of the 5 weed species used in these experiments, white clover, hairy vetch, and honeysuckle may support H. zea populations in the wild. However, significant larval mortality, low adult emergence rates, and marked reductions in fecundity were repeatedly observed for individuals reared on these select weed species, suggesting the nominal role they play on H. zea field populations. Furthermore, the ephemeral nature of these select species complicate weed management and make selective weed suppression time consuming and impractical. Given the significant reductions in fitness associated with these candidate weed species, populations of larvae may build; however, it is unlikely that a significant proportion of these individuals will successfully pupate or emerge as an adult.

Individuals reared to adult emergence on white clover were among the most fecund second to larvae reared on crimson clover. However, these individuals took significantly more time to complete development and emerge while experiencing significant larval mortality (> 40%). These factors combined suggest crimson clover is among the most suitable of weedy hosts investigated in this study in terms of overall fitness. Crimson clover and kudzu are 2 of the most widespread and abundant weeds species commonly found across the mid-south that may significantly affect H. zea establishment.

When reared solely on kudzu, H. zea took on average 3 d to hatch similar to all treatments. However, these individuals had the shortest life span between 4 and 5 d and among the highest larval mortality (> 55%) observed across the study. Kudzu currently covers approximately 3,000,000 ha throughout the eastern US and continues to aggressively spread by 50,000 ha per yr (Forseth & Innis 2010). The ability to remove plant stands of kudzu for weed management is likely not feasible given the weed's aggressive growth habit colonizing large contiguous tracts of land. Large stands of kudzu also may play an indirect role in regional suppression of field populations. The aggressive growth of kudzu is known to displace other vegetation, ultimately decreasing plant richness and abundance. Plant competition from kudzu potentially may reduce suitable oviposition substrate in the field.

Results from this study strongly indicate crimson clover is among the most important species to be targeted for weed management. Annual plantings of crimson clover as a soil stabilizer have the potential to have a significant impact on H. zea field populations. Cultural integrated pest management strategies including planting date manipulation to disrupt H. zea populations may provide a useful management tool in addition to chemical control measures. Insect managers can use this information to make informed decisions concerning sampling and potential weed management efforts for species that are more advantageous to H. zea establishment.

The resulting fitness of H. zea on a given weedy host plant may help prioritize cultural and chemical integrated pest management strategies including the timely application of herbicides, biopesticides, and modulated planting date to desynchronize plant-insect phenological events. Increased understanding of H. zea host plant source-sink relationships may help to better explain the potential survival, outbreak, and migratory capability across a given landscape. Understanding the impact that different host plants have on a population's growth potential and biology are important tools used in integrated pest management programs. Future research should examine the quality of various host plant tissues such as vegetative growth compared to floral parts, because the nutritional quality may affect survival and fecundity.

Further investigation of larval diet breadth and its effects on mating behavior, generational fitness, and host finding behavior may offer additional useful information when assessing the potential contribution of migrant individuals. Such information may help to increase our knowledge regarding its population dynamics and management in a given landscape. These findings improve our understanding and provide insights on the potential impact of 5 weedy host plants common across the mid-south and fill a gap by providing baseline biological data for H. zea.