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NOCTUIDAE  -  Helicoverpa armigera (Hübner)

Taxonomy

Noctuoidea: Noctuidae: Heliothinae: Helicoverpa armigera (Hübner)

Common names: 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 (Summary)

  • D setae of A1-8 inserted on large conical chalazae, those of A1, A2 or A8 often larger than the rest
  • Body color highly variable, but usually with lines and stripes and sometimes a black bar joining the D setae of A1 or A2
  • If setal bases are small, then the mandible has a minute tooth on the inner rib and no large retinaculum
  • Larvae of H. armigera are difficult to separate from those of other species of Helicoverpa (H. assulta, H. puntigera); see the detailed larval diagnosis for more information.
  • There are no consistent morphological characters that can be used to separate the larvae of H. armigera and H. zea.

 

Host/origin information

Helicoverpa armigera is highly polyphagous and has been recorded feeding on plants in more than 45 families. Larvae are intercepted on a variety of hosts from many locations. The origins and hosts listed here are the most common combinations; however, it is possible that larvae may be intercepted on any host originating from within this species' recorded distribution.

Origin Host(s)
IndiaTagetes
Israelvarious
Kenyavarious
NetherlandsBupleurum, Leucospermum, Ornithogalum, Veronica
Zimbabwevarious

 

Recorded distribution

Helicoverpa armigera is widely distributed throughout the Old World (Africa, Asia, Europe), Australasia, and Oceania.

In early 2013, H. armigera was first reported from Brazil. This is the first report of H. armigera establishing in the New World. It has since been reported from the Brazilian states of Mato Grosso, Goias, Bahia, Distrito Federal, Parana, Roraima, and Piaui. In late 2013, it was reported from Paraguay, and in 2014 from the Tucuman Province of Argentina (Viclos and La Chocha).

 

Identification authority (Summary)

Larvae of H. armigera are usually intercepted from locations in the Old World. In the New World, H. armigera has been recorded from Brazil (see list of states above), Paraguay, and Argentina. See the Detailed Information tab for specific identification recommendations for various regions.

 

Pest characterization

(Based on Cavey 2001, Venette et al. 2003)

  • Taxonomy: Medium. Species identification is often difficult.
  • Distribution: High. Helicoverpa armigera is not present in the U.S.
  • Potential Impact: High. This species is a serious threat to agriculture and the environment.

This ranking characterizes H. armigera as quarantine significant.

NOCTUIDAE  -  Helicoverpa armigera (Hübner)

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) 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 larva (e.g., Kirkpatrick 1961, Chu et al. 1965, Thakar and Srivastava 1983, Sri et al. 2010). Toguebaye and Couilloud (1982) studied the first instar 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) nor Venette et al. (2003) treated larval identification of H. armigera at United States ports; there is certainly a need to address this topic in some detail.

Hardwick (1965) 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 pinacula, 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 1961). Bejakovich and Dugdale (1998), working in New Zealand, noted H. armigera has three longitudinal bands of microspines: one on the dorsal 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 microspines have a broad round base, the cuticle appears "cobblestoned" between the spines and microspines 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 pinacula connected by a black bar) on A1 and A2. These tend to be absent in H. punctigera (Matthews 1999: plate 21). Another difference is prothoracic setae 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 pinacula on A1 and A8 and more spines near the dorsal 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 trisetose SV group on A2, a bisetose SV group on A7, SD1 on A8 directly above the spiracle and microspines becoming hairlike ventrally. Gardner (1946) did not find an inner tooth on the mandible of H. armigera. Yoshimatsu (2002), working in Japan, illustrated the mandibles of both H. armigera and H. assulta. They were nearly identical but H. armigera was said to have microspines on the anal shield that are lacking in H. assulta. In addition, the diameter of the SD1 pinacula on A7 is about equal to the spiracle length in H. armigera. The SD1 pinacula 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) used measurements and ratios to separate H. armigera from H. assulta in Africa without other morphological details. Ahola and Silvonen (2005) 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 chaetotaxy of the first abdominal segment, noted the D pinacula of A1 and A8 are joined by a black bar and that the D pinacula 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 pinacula 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 pinacula height of both H. zea and C. virescens varies according to age within an instar. As a larva grows, the cuticle tightens which tends to stretch and shrink the pinacula. Obviously, it becomes hard to trust pinacula size as a key character, although several authors cite conical pinacula 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 microspines will separate H. armigera from H. puntigera (with brown spiracles) and H. assulta (with microspines not in obvious bands) (Bejakovich and Dugdale 1998: 10, 11). Kirkpatrick (1961) 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 pinacula will separate H. armigera from related genera of Heliothinae, but not all specimens are expected to show this character. Perhaps scattered spines on the distal region of the hypopharyngeal complex (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. 2013). It has since been reported from the Distrito Federal, the southern state of Parana (Specht et al. 2013, Tay et al. 2013), and also Roraima and Piaui (Mastrangelo et al. 2014). Individuals of H. armigera have also been confirmed from Paraguay and the Tucuman Province in Argentina (Murua et al. 2014). 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 larva. 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 larva whereas H. armigera tends to be darkly colored. This difference between the two species was illustrated by Li et al. (2013) along with other morphological characters needing confirmation (crochet pattern) or clarification (prothoracic chaetotaxy). Therefore, green larvae 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 1999-2000, Ahola and Silvonen 2005) 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 larvae 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

NOCTUIDAE  -  Helicoverpa armigera (Hübner)

Because larvae of H. armigera are difficult to identify to species, many are likely listed in PestID under "Helicoverpa spp."

 

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

NOCTUIDAE  -  Helicoverpa armigera (Hübner)

Setal map

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Helicoverpa armigera setal map

Helicoverpa armigera setal map

Click here to download a full-size printable PDF of this larval setal map

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Fig. 1: Late instar larva, lateral view


Fig. 1: Late instar larva, lateral view
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Fig. 2: Late instar larva, dorsal view


Fig. 2: Late instar larva, dorsal view
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Fig. 3: Late instar larva, lateral view


Fig. 3: Late instar larva, lateral view
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Fig. 4: Late instar larva, dorsal view


Fig. 4: Late instar larva, dorsal view
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Fig. 5: Mid- to late instar larva, lateral view


Fig. 5: Mid- to late instar larva, lateral view
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Fig. 6: Mid- to late instar larva, dorsal view


Fig. 6: Mid- to late instar larva, dorsal view
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Fig. 7: Mid-instar larva, lateral view


Fig. 7: Mid-instar larva, lateral view
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Fig. 8: Early instar larva, lateral view


Fig. 8: Early instar larva, lateral view
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Fig. 9: Early instar larva, lateral view


Fig. 9: Early instar larva, lateral view
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Fig. 10: Mid-instar


Fig. 10: Mid-instar
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Fig. 11: Head and thorax


Fig. 11: Head, thorax
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Fig. 12: Conical pinacula on A1


Fig. 12: Pinacula on A1
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Fig. 13: Crochets


Fig. 13: Crochets
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Fig. 14: Head (cleared)


Fig. 14: Head (cleared)
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Fig. 15: Hypopharyngeal complex, lateral view


Fig. 15: Hypo. complex
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Fig. 16: Hypopharyngeal complex, dorsal view


Fig. 16: Hypopharyngeal complex, dorsal view
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Fig. 17: Mandible


Fig. 17: Mandible
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Fig. 18: Mandible


Fig. 18: Mandible
  LepIntercept - An identification resource for intercepted Lepidoptera larvae
  by Todd M. Gilligan and Steven C. Passoa
  Identification Technology Program (ITP), Fort Collins, CO. Last updated February 2014.