Classification

Noctuoidea: Noctuidae: Heliothinae: Helicoverpa armigera (Hübner)

Common name

cotton bollworm, Old World bollworm, scarce bordered straw

Synonyms

Heliothis armigera, H. obsoleta, H. pulverosa, H. uniformis, H. armiger

Prior to the mid-20th century, the name armigera was often used to refer to H. zea in the New World. See the Detailed Information tab for specifics.

Larval diagnosis (Detailed)

Prior to the mid-20th century, the name armigera was often used to refer to H. zea in the New World. Only in 1955 were the two names considered separate species and H. zea used for the New World populations. Based on Heliothis being considered masculine, the species name was shortened to "H. armiger" to be in agreement with the gender of the genus. This is not currently followed. Consult King (1994)King (1994):
King, A. B. S. 1994. Heliothis/Helicoverpa (Lepidoptera: Noctuidae). In Insect Pests of Cotton. Mathews G. A. and J. P. Turnstall (eds.). Commonwealth Agricultural Bureaux International. Wallingford, Great Britain. 593 pp. for a discussion of these points.

In spite of the pest status of H. armigera, there appears to be few detailed larval morphological studies with complete setal maps of the mature larvalarva:
the stages between the egg and pupa of those insects having complete metamorphosis
(e.g., Kirkpatrick 1961Kirkpatrick 1961:
Kirkpatrick, T. H. 1961. Comparative morphological studies of Heliothis species (Lepidoptera: Noctuidae) in Queensland. Queensland Journal of Agricultural Science 18: 179-194., Chu et al. 1965Chu et al. 1965:
Chu, H. F., C. L. Fang and L. Y. Wang. 1965. Fauna of Chinese Economic Insects. Volume 7. Lepidoptera, Noctuidae (immature stages). [China] Science Publishing House. 120 pp., Thakar and Srivastava 1983Thakar and Srivastava 1983:
Thakar, A. V. and R. P. Srivastava. 1983. Chaetotaxy of eight noctuid caterpillars. Bulletin of Entomological Research 24: 83-94., Sri et al. 2010Sri et al. 2010:
Sri, I. A., V. R. Rao, P. R. Sekhar and M .S. V. Chalam. 2010. Taxonomic studies on different lepidopteran caterpillars on cotton, chilli and pulses. Annals of Plant Protection Sciences 18: 104-107.). Toguebaye and Couilloud (1982)Toguebaye and Couilloud (1982):
Toguebaye, B. S. and R. Couilloud. 1982. Etude descriptive de l'oeuf et des stades larvaires d'Heliothis armigera (Hubner 1908) (Lepidoptera, Noctuidae) en microscopie electronique a balayage. Coton et fibres tropicales 37: 197-209. [date incorrectly listed as 1908 - should be Hubner 1809] studied the first instarinstar:
the stage between molts
of H. amigera in detail. Various, often conflicted diagnoses, have been published; the major ones are reviewed here organized by geographical regions. Although complicated, listing the suite of characters used to identify H. armigera will result in a better understanding of morphological variation and provide backup characters that might be useful in doubtful cases. Neither Weisman (1986)Weisman (1986):
Weisman, D. M. 1986. Keys for the identification of some frequently intercepted lepidopterous larvae. U.S. Department of Agriculture, Animal and Plant Health Inspection Service, Plant Protection and Quarantine series 81-47. 64 pp. nor Venette et al. (2003)Venette et al. (2003):
Venette, R. C., E. E. Davis, J. Zaspel, H. Heisler and M. Larson. 2003. Mini Risk Assessment. Old World bollworm, Helicoverpa armigera Hubner [Lepidoptera: Noctuidae]. Department of Entomology, University of Minnesota for the U. S. Department of Agriculture Cooperative Agricultural Pest Survey program. 36 pp. treated larval identification of H. armigera at United States ports; there is certainly a need to address this topic in some detail.

Hardwick (1965)Hardwick (1965):
Hardwick, D. F. 1965. The corn earworm complex. Memoirs of the Entomological Society of Canada 40: 1-247. presented a morphometric key to Helicoverpa larvae based on origins. For Australia, he noted H. armigera usually had spiracles with dark brown rims and a central light or medium brown area. There was often orange shading around the D and SD pinaculapinaculum:
a small, flat, or slightly elevated chitinized area bearing a seta or setae
, but no orange spot. The vertical diameter of SD1 on A7 was equal or less than the diameter of the corresponding spiracle in H. armigera from Australia (Kirkpatrick 1961Kirkpatrick 1961:
Kirkpatrick, T. H. 1961. Comparative morphological studies of Heliothis species (Lepidoptera: Noctuidae) in Queensland. Queensland Journal of Agricultural Science 18: 179-194.). Bejakovich and Dugdale (1998)Bejakovich and Dugdale (1998):
Bejakovich D. and J. Dugdale. [1998]. Keys to late-instar larvae and adults of Noctuidae (Lepidoptera) encountered in field surveys and border control in New Zealand. MAF Quality Management and Manaaki Whenua Landcare Research. Lincoln, New Zealand. 55 pp., working in New Zealand, noted H. armigera has three longitudinal bands of microspinesmicrospines:
minute spines on the body, usually visible only under magnification
: one on the dorsaldorsal:
at the top or back or above
midline, one between D2 and L2 and a final one between L1 and L3. In addition, the rim of the spiracle is black in all instars, the microspinesmicrospines:
minute spines on the body, usually visible only under magnification
have a broad round base, the cuticle appears "cobblestoned" between the spines and microspinesmicrospines:
minute spines on the body, usually visible only under magnification
are present below SD1 on A1-8. Matthews (1999: figs. 415, 416) illustrated the cuticle texture of H. armigera on A1 and A9 with scanning electron micrographs. He noted late instar H. armigera often have "saddle markings" (enlarged pinaculapinaculum:
a small, flat, or slightly elevated chitinized area bearing a seta or setae
connected by a black bar) on A1 and A2. These tend to be absent in H. punctigera (Matthews 1999: plateplate:
a larger sclerotized area of the body; = shield
21). Another difference is prothoracic setaeseta:
a hairlike projection of the body wall that is articulated in a socket; compare to spine
behind the head. These tend to be pale in H. armigera but dark in H. puntigera. Hosts can also provide a clue. Helicoverpa punctigera is not as common on members of the grass family as is H. armigera (Department of Primary Industries and Fisheries 2005).

Chu et al. (1965), studying Helicoverpa in China, noted that H. armigera and H. assulta both have a small inner mandibular tooth. Helicoverpa armigera has cone shaped pinaculapinaculum:
a small, flat, or slightly elevated chitinized area bearing a seta or setae
on A1 and A8 and more spines near the dorsaldorsal:
at the top or back or above
line on A1 and A8 than H. assulta. The spines of H. armigera are pointed, easy to see "inside the legs" and the head has P1 slightly higher than AF2. Gardner (1946) put H. armigera in his A IV group noting that these species have a trisetosetrisetose:
three setae
SV group on A2, a bisetosebisetose:
two setae
SV group on A7, SD1 on A8 directly above the spiracle and microspinesmicrospines:
minute spines on the body, usually visible only under magnification
becoming hairlike ventrally. Gardner (1946) did not find an inner tooth on the mandible of H. armigera. Yoshimatsu (2002)Yoshimatsu (2002):
Yoshimatsu, S. 2002. Identification of similar species in 4 groups of Japanese noctuid (Insecta: Lepidoptera) pests from their immature stages. Annual Report 2001/2002. National Institute for Agro-Environmental Sciences. Japan. http://www.niaes.affrc.go.jp/annual/r2001/html/no46.html, working in Japan, illustrated the mandibles of both H. armigera and H. assulta. They were nearly identical but H. armigera was said to have microspinesmicrospines:
minute spines on the body, usually visible only under magnification
on the anal shieldanal shield:
the dorsal shieldlike covering of the last abdominal segment (= anal plate)
that are lacking in H. assulta. In addition, the diameter of the SD1 pinaculapinaculum:
a small, flat, or slightly elevated chitinized area bearing a seta or setae
on A7 is about equal to the spiracle length in H. armigera. The SD1 pinaculapinaculum:
a small, flat, or slightly elevated chitinized area bearing a seta or setae
on A7 in H. assulta is much larger, about 1.4-2 times the length of the spiracle. There are also minor differences in spiracle sizes on A7 compared to A8 between these species.

Hardwick (1965)Hardwick (1965):
Hardwick, D. F. 1965. The corn earworm complex. Memoirs of the Entomological Society of Canada 40: 1-247. used measurements and ratios to separate H. armigera from H. assulta in Africa without other morphological details. Ahola and Silvonen (2005)Ahola and Silvonen (2005):
Ahola, M. and K. Silvonen. 2005. Larvae of Northern European Noctuidae. Volume 1. KuvaSeppala Group Limited. Vaasa, Finland. 657 pp. gave a detailed description of the mouthparts of H. armigera, but no keys to related species in northern Europe. Beck (1999: 291-293) did provide a key to European Heliothinae. He illustrated the chaetotaxychaetotaxy:
the arrangement and nomenclature of setae; see setal map
of the first abdominal segment, noted the D pinaculapinaculum:
a small, flat, or slightly elevated chitinized area bearing a seta or setae
of A1 and A8 are joined by a black bar and that the D pinaculapinaculum:
a small, flat, or slightly elevated chitinized area bearing a seta or setae
of A1 are relatively large and closely spaced (Beck 1999: 501b, Beck 2000: 174). He illustrated the mandible of H. armigera with a small inner tooth (Beck 1999: 512c). Sannino et al. (1993) included H. armigera in his study of Lepidoptera associated with tobacco. He called attention to the sinuate striations and well developed pinaculapinaculum:
a small, flat, or slightly elevated chitinized area bearing a seta or setae
in H. armigera.

Given the documented larval variation in North American species of Chloridea, Heliothis, and Helicoverpa, we have little or no confidence in morphological identification of larval H. armigera in some parts of its range. Neunzig (1969: figs 9-12) showed that the pinaculapinaculum:
a small, flat, or slightly elevated chitinized area bearing a seta or setae
height of both H. zea and C. virescens varies according to age within an instarinstar:
the stage between molts
. As a larvalarva:
the stages between the egg and pupa of those insects having complete metamorphosis
grows, the cuticle tightens which tends to stretch and shrink the pinaculapinaculum:
a small, flat, or slightly elevated chitinized area bearing a seta or setae
. Obviously, it becomes hard to trust pinaculapinaculum:
a small, flat, or slightly elevated chitinized area bearing a seta or setae
size as a key character, although several authors cite conical pinaculapinaculum:
a small, flat, or slightly elevated chitinized area bearing a seta or setae
as a feature of H. armigera. Another problem is mandible wear. Chloridea virescens can have a well developed inner tooth or just a scar (Neunzig 1969: figs 6, 7). This may explain why some authors see a tooth on H. armigera while others do not.

Unfortunately, the quarantine significance of H. armigera forces us to evaluate conflicting literature and attempt a diagnosis. In New Zealand, the black spiracles and three bands of microspinesmicrospines:
minute spines on the body, usually visible only under magnification
will separate H. armigera from H. puntigera (with brown spiracles) and H. assulta (with microspinesmicrospines:
minute spines on the body, usually visible only under magnification
not in obvious bands) (Bejakovich and Dugdale 1998: 10, 11). Kirkpatrick (1961)Kirkpatrick (1961):
Kirkpatrick, T. H. 1961. Comparative morphological studies of Heliothis species (Lepidoptera: Noctuidae) in Queensland. Queensland Journal of Agricultural Science 18: 179-194. was unable to separate H. armigera from H. punctigera in Australia, and given doubt about the spiracular color of H. armigera being black or brown in areas outside of New Zealand, it is better to stop at genus for interceptions in Australia. Color characters (saddle markings, etc.) will be a clue but are not definitive. Yamaskaki et al (2009: Fig. 1) illustrated four color forms of H. armigera: completely green, green with stripes, brown and black. This helps document at least some of the expected variation for this pest.

For European interceptions, when present, large conical pinaculapinaculum:
a small, flat, or slightly elevated chitinized area bearing a seta or setae
will separate H. armigera from related genera of Heliothinae, but not all specimens are expected to show this character. Perhaps scattered spines on the distaldistal:
toward the tip or end; farthest from the body
region of the hypopharyngeal complexhypopharyngeal complex:
a structure consisting of the Hypopharynx, Labial palpi, and Spinneret
(Ahola and Silvonen 2005: fig. 1106) is the most distinctive mouthpart character for H. armigera in northern Europe. The final problem is separating H. armigera from H. assulta. Helicoverpa assulta is normally associated only with only Solanaceae (but see Mathews 1999: 117, 118) whereas H. armigera is polyphagous. Differences in cuticular texture will separate the two species on solanaceous hosts. Sannino et al (1996) compared H. peltigera to H. armigera and noted major differences in the larval mandibles.

Identification Authority (Detailed)

Helicoverpa armigera was first reported as established in Brazil in early 2013 in the states of Goias, Bahia, and Mato Grosso (Czepak et al. 2013Czepak et al. 2013:
Czepak, C., K. C. Albernaz, L. M. Vivan, H. O. Guimaraes and T. Carvalhais. 2013. Research note. First reported occurrence of Helicoverpa armigera (Hubner) (Lepidoptera: Noctuidae) in Brazil. Pesquisa Agropecuaria Tropical, Goiania 43: 110-113.). It has since been reported from the Distrito Federal, the southern state of Parana (Specht et al. 2013Specht et al. 2013:
Specht, A., D. R. Sosa-Gomez, S. V. de Paula-Moraes and S. A. Cavaguchi Yano. 2013. Identificacao morfologica e molecular de Helicoverpa armigera (Lepidoptera: Noctuidae) e ampliacao de seu registro de ocorrencia no Brasil. Pesquisa Agropecuaria Brasileira 48: 689-692., Tay et al. 2013Tay et al. 2013:
Tay, W. T., M. F. Soria, T. Walsh, D. Thomazoni, P. Silvie, G. T. Behere, C. Anderson and S. Downes. 2013. A brave New World for an Old World pest: Helicoverpa armigera (Lepidoptera: Noctuidae) in Brazil. Plos One 8(11): e80134. doi:10.1371/journal.pone.0080134.), and also Roraima and Piaui (Mastrangelo et al. 2014Mastrangelo et al. 2014:
Mastrangelo, T., D. F. Paulo, L. W. Bergamo, E. G. F. Morais, M. Silva, G. Bezerra-Silva and A. M. L. Azeredo-Espin. 2014. Detection and genetic diversity of a heliothine invader (Lepidoptera: Noctuidae) From North and Northeast of Brazil. Journal of Economic Entomology 107: 970-980.). Individuals of H. armigera have also been confirmed from Paraguay and the Tucuman Province in Argentina (Murua et al. 2014Murua et al. 2014:
Murua, M. G., F. S. Scalora, F. R. Navarro, L. E. Cazado, A. Casmuz, M. E. Villagran, E. Lobos and G. Gastaminza. 2014. First record of Helicoverpa armigera (Lepidoptera: Noctuidae) in Argentina. Florida Entomologist 97: 854-856.). This is the first instance of this important pest establishing in the New World. Because we have not identified any morphological characters to reliably separate H. zea from H. armigera, interceptions from many locations in South America will require molecular methods. There is also occasional evidence of Old World cargo or produce being shipped through Mexico to the United States. This is another potential pathway for introduction of H. armigera into the New World.

A second problem area is Australia and New Zealand. Do not identify H. armigera to species in Australia and do so in New Zealand only with caution using well preserved mature larvalarva:
the stages between the egg and pupa of those insects having complete metamorphosis
. Helicoverpa puntigera is restricted to Australia, or occasionally New Zealand where it does not overwinter (Bejakovich and Dugdale 1998: 52), and therefore it is not a consideration when identifying H. armigera from other regions.

For quarantine purposes, it may be best to assume H. assulta eats only Solanaceae until more records from other plant families are published from regions outside of Australia. Therefore, we can assume Helicoverpa interceptions from non-solanaceous plants are more likely to be H. armigera than H. assulta. Body color is another clue. Hardwick (1965:28) stated that H. assulta is primarily a green larvalarva:
the stages between the egg and pupa of those insects having complete metamorphosis
whereas H. armigera tends to be darkly colored. This difference between the two species was illustrated by Li et al. (2013)Li et al. (2013):
Li, H., H. Zhang, R. Guan and X. Miao. 2013. Identification of differential expression genes associated with host selection and adaptation between two sibling insect species by transcriptional profile analysis. Biomedical Central Genomics 14: 582. along with other morphological characters needing confirmation (crochet pattern) or clarification (prothoracic chaetotaxychaetotaxy:
the arrangement and nomenclature of setae; see setal map
). Therefore, green larvaelarva:
the stages between the egg and pupa of those insects having complete metamorphosis
on Solanaceae from the Old World need to be examined carefully as H. assulta suspects instead of rapidly confirming them as H. armigera.

Identification of H. armigera from Europe and Northern Africa is relatively straightforward. Heliothis nubigera is the only species almost colored like H. armigera (Beck 1999-2000Beck 1999-2000:
Beck, H. 1999-2000. Die Larven der Europaischen Noctuidae. Revision der Systematik der Noctuidae (Lepidoptera, Noctuidae). Herbipoliana 5/1(1): 1-864; 5/1(2): 1-448; 5/3(3): 1-512; 5/3(4): 1-336., Ahola and Silvonen 2005Ahola and Silvonen 2005:
Ahola, M. and K. Silvonen. 2005. Larvae of Northern European Noctuidae. Volume 1. KuvaSeppala Group Limited. Vaasa, Finland. 657 pp.) from this region. The literature is good and sibling species like H. assulta do not occur in those regions. Netherlands vegetables are assumed to be grown in country, other host are of uncertain origin and therefore it is best not to attempt a species identification for Helicoverpa from this pathway. Sibling species of Helicoverpa in Central Africa prevent recognition of H. armigera in that part of the world.

NOTE: Due to the continuing spread of H. armigera in South America, exercise caution when attempting identifications from that continent. There are no morphological characters to separate the larvaelarva:
the stages between the egg and pupa of those insects having complete metamorphosis
of H. armigera from H. zea. When in doubt, default to "Helicoverpa sp." instead of attempting a species-level ID. The following keys may not reflect the most recent H. armigera distribution in South America.

Key to the identification of Helicoverpa armigera suspects intercepted at U.S. ports of entry

Identification guide to larval Heliothinae (Lepidoptera: Noctuidae) of quarantine significance

Origin records

Helicoverpa armigera has been intercepted from the following locations:

Albania, Bosnia and Herzegovina, Bulgaria, Burkina Faso, Cape Verde, China, Egypt, Eritrea, France, Gambia, Germany, Ghana, Guatemala, Hong Kong, India, Iraq, Israel, Italy, Japan, Jordan, Kenya, Lebanon, Malaysia, Mali, Morocco, Mozambique, Netherlands, New Zealand, Nigeria, Pakistan, Palestinian Territory, Philippines, Portugal, Senegal, South Africa, South Korea, Spain, Tanzania, Thailand, Togo, Trinidad and Tobago, Tunisia, Turkey, Ukraine, United Arab Emirates, United Kingdom of Great Britain and N. Ireland, Yugoslavia, Zimbabwe

Records from Guatemala needs confirmation and likely represent misidentifications.

Host records

Helicoverpa armigera has been intercepted on the following hosts:

Abelmoschus esculentus, Achillea, Allium, Amaranthus, Ammi, Anemone coronaria, Anemone, Anethum, Anigozanthos, Antirrhinum, Artemisia, Asclepias, Asclepias tuberosa, Asparagus, Aster, Astilbe, Astrantia, Bellis, Bouvardia, Brassica oleracea, Brassica oleracea var. acephala, Brassica rapa, Brassica, Brunia, Bupleurum griffithii, Bupleurum, Cajanus cajan, Calendula, Capsicum annuum, Capsicum, Carthamus, Celosia, Cestrum, Chamelaucium, Chrysanthemum, Cicer arietinum, Cicer, Cichorium intybus, Citrus, Clematis, Coriandrum sativum, Cosmos, Craspedia, Cucurbita, Cucurbitaceae, Cynara scolymus, Dahlia, Delphinium, Dendrobium, Dianthus, Echinops, Eryngium, Eustoma grandiflorum, Eustoma, Fabaceae, Fragaria, Gentiana, Gerbera, Gladiolus, Gomphrena, Grevillea, Gypsophila, Helianthus, Hibiscus, Hydrangea, Hypericum, Jasminum sambac, Jasminum, Lablab purpureus, Lathyrus sativus, Leucadendron, Leucospermum cordifolium, Leucospermum, Limonium, Lippia graveolens, Lippia, Lisianthus, Lysianthus, Lysimachia, Malus, Malvaceae, Matricaria, Mentha longifolia, Mentha, Minthostachys, Moluccella, Musa, Nerium, Ocimum basilicum, Ocimum, Oleaceae, Oncidium, Origanum majorana, Origanum, Origanum vulgare, Ornithogalum arabicum, Ornithogalum, Oxypetalum, Phaseolus coccineus, Phaseolus, Pisum sativum, Pisum, Polianthes tuberosa, Polyanthus, Protea, Ranunculus, Rosa, Rosmarinus officinalis, Rosmarinus, Rudbeckia, Salvia officinalis, Salvia, Satureja hortensis, Satureja, Scabiosa, Setaria italica, Solanaceae, Solanum aethiopicum, Solanum melongena, Solanum, Statice, Tagetes erecta, Tagetes, Tetrapleura, Thymus citriodorus, Thymus, Thymus vulgaris, Trachelium, Tuberosa, Tulipa, Vernonia amygdalina, Veronica, Zea mays