Host Range Information

Supplementary information

Host range information

The host range of Heliothisvirescens encompasses a large number of plants in a great many families; some description is provided for of each of the ten hosts chosen for this experiment.

Antirrhinum majus(Scrophulariacae) – H. virescens is widely reported on biocontrol and gardening websites as feeding on snapdragon (e.g. University of Florida IFAS: and a picture of active feeding at though I can find no primary references for it. It is readily accepted by larvae in the laboratory.

Brassica oleracea(Brassicaceae) – Harding (1976) reports larvae of H. virescens on cabbage in cultivation in the Lower Rio Grande Valley of Texas, but notes it is a poor host. Robinson et al. (2010) list it feeding on B. rapa and B. tournefortii.

Capsicum anuum (Solanaceae) – Harding (1976) reports eggs and larvae of H. virescens on bell peppers in cultivation in the Lower Rio Grande Valley of Texas, but notes it is a poor host.

Cicer arietinum (Fabaceae) – Blanco et al (2007) report H. virescens on garbanzo beans in Mississippi and in Tamaulipaus, Mexico. In Davis, California, larvae ate every bean in a small stand of garbanzo beans in the author’s garden, they additionally chewed on leaves and stems (perhaps in food shortage).

Cucumerismelo (Cucurbitaceae) – Harding (1976) reports eggs and larvae on cantaloupe in cultivation in the Lower Rio Grande Valley of Texas, but reports it as a poor host. Interestingly, this contradicts the findings of this study. I have not found it on garden canteloupes in Davis, California, though they were meters away from heavily-infested garbanzo beans.

Datura stramionum (Solanaceae) – Robinson et al (2010) list the genus Datura as a host of H. virescens, I have found larvae on D. stramionum in Davis, CA.

Ipomoea hybrid (Convulvaceae) – Roach (1975) reports it on “Morning glory (Ipomoea spp.)” and on I. pandurata, a native congener of ornamentals. Barber 1937 reports it on I. sp. in Georgia, though it is not clear if this refers to an ornamental, crop (e.g. sweet potato), or wild species.

Mirabilis longifloraNyctaginaceae) – a post to Iowa State’s citizen science website Bug Guide (bugguide.net) showed a late-instar larvae of this species feeding on a Mirabilis sp. leaf with damage and frass evident. (Obviously, we have no knowledge of whether it was feeding on this plant for earlier instars, and the experiment may be interpreted as evidence against this possibility). As this would be a new host family, I decided to test it in this experiment.

Petunia exserta (Solanaceae) – H. virescens is a common pest of petunias (e.g. Davidson et al 1992). P. exserta is a rare wild Petunia species (though cultivated as an ornamental), but I have found H. virescens feeding on it in my garden and it is readily accepted by it in the lab.

Rumexacetosella (Polygonaceae) – Harding (1976) reports larvae on Rumex sp. (or spp.) in the Lower Rio Grande Valley of Texas, Barber (1937) reports it on R. crispus in Georgia, and Sudbrink and Grant (1995) report it on R. obtusifolia in Tennessee. R. acetosella is a common weed in North America.

References

Barber, G. W. 1937. Seasonal availability of food plants of two species of Heliothis in Eastern Georgia. Journal of Economic Entomology 30: 150-158.

Blanco, C.A., Teran-Vargas, A. P., Lopez, J. D., Kauffman, J. V. & X. Wei. 2007. Densities of Heliothisvirescens and Helicoverpazea (Lepidoptera: Noctuidae) in three plant hosts. Florida Entomologist 90: 742-750.

Davidson, N. A., Kinsey, M. G., Ehler, L. E. & G. W. Frankie. 1992. Tobacco budworm, pest of petunias, can be managed with Bt. California Agriculture 46: 7-9.

Harding, J. A. 1976. Heliothis spp.: seasonal occurrence, hosts, and host importance in the lower Rio Grande Valley. Environmental Entomology 5: 666-668.

Roach, S. H. 1975. Heliothis spp.: larvae and associated parasites and diseases on wild host plants in the Pee Dee area of South Carolina. Environmental Entomology 4: 725-728.

Robinson, G. S., P. R. Ackery, I. J. Kitching, G. W. Beccaloni & L. M. Hernández, 2010. HOSTS - A Database of the World's Lepidopteran Hostplants. Natural History Museum, London. (Accessed: 22March 2017).

Sudbrink D. L. & J. F. Grant. Wild host plants of Helicoverpazea and Heliothisvirescens (Lepidoptera: Noctuidae) in Eastern Tennessee. Environmental Entomology 24: 1080-1085.

Omnivory amongst herbivores, a mini-review

The omnivory discussed in this manuscript is consumption of plant and animal matter (i.e. omnivorysensuArim and Marquet 2004). This is a specific type of omnivory, which has been classically defined as the consumption of more than one trophic level (Pimm & Lawton 1978). Most prior research into omnivory has focused on predator guilds that feed on each other and herbivores (intraguild predation, e.g. Polis et al 1989), predators that supplement their diet with plant foods (e.g. Naranjo and Gibson 1996), and, though not trophic omnivory, herbivores which mix plant foods (e.g. Singer and Bernays 2003). Less attention has been paid to “herbivores” which include non-plant food in their diet, though this is very common. Examples of arthropods are detailed in the main manuscript; however, most literature deals with mammals and seem pertinent to include.

Consumption of animal matter is often-noted in vertebrate herbivores; ornithologists have long-noted the consumption of nestling songbirds by deer (Allan 1978; Pietz and Granfors 2000) and cows (Nack and Ribic 2005). Nesting seabirds suffer similarly from deer and sheep (Furness 1988), as do geese from caribou (Abraham, Mineu and Cooke 1977). Lambs are consumed by pigs (Pavolv et al 1981). Red squirrels prey heavily on young hares (O’Donoghue 1994) and rabbits themselves opportunistically scavenge mammalian and avian carrion (Clauss et al 2016). Beavers scavenge salmon carcasses (Gleason et al 2005); similarly, deer scavenge annual die-offs of alewives, a small fish (Case and McCullough 1987). Hippopotamuses consume live birds and smaller mammals and scavenge large mammal carcasses (Dudley et al 2016). American toad tadpoles consume conspecifics, especially when dead, which causes more rapid development (Heinen and Abdella 2005). Mammalian grazers and browsers must also ingest whatever arthropods happen to be on or in the plant matter ingested.

These examples, while mostly noticed in obvious, large animals, demonstrate that omnivory is at least an occasional occurrence for many “herbivores” and the ubiquity suggests an ability to consume, if not process and digest, animal matter is a widespread herbivore trait. Given this remarkable convergence across herbivorous taxa and the results of this caterpillar experiment, while I cannot conclude an adaptive purpose of omnivory, the behavior seems unlikely to be broadly maladaptive and may be ecologically- or evolutionarily-important in more than just caterpillars.

References

Abraham, K., Mineau, P. & Cooke, F. (1977) Unusual predators of snow goose eggs. Canadian Field-Naturalist, 91, 317–318.

Allan, T. (1978) Further evidence of white-tailed deer eating birds in mist nets. Bird Banding, 49, 184.

Arim, M. & Marquet, P. a. (2004) Intraguild predation: A widespread interaction related to species biology. Ecology Letters, 7, 557–564.

Case, D.J. & Mccullough, D.R. (1987) White-Tailed Deer Forage on Alewives. Journal of Mammalogy, 68, 195–198.

Clauss, M., Lischke, A., Botha, H. & Hatt, J.-M. (2016) Carcass consumption by domestic rabbits (Oryctolaguscuniculus). European Journal of Wildlife Research, 62, 143–145.

Dudley, J.P., Hang’Ombe, B.M., Leendertz, F.H., Dorward, L.J., de Castro, J., Subalusky, A.L. & Clauss, M. (2016) Carnivory in the common hippopotamus Hippopotamusamphibius : implications for the ecology and epidemiology of anthrax in African landscapes. Mammal Review, 46,

Furness, R.W. (1988) Predation on ground-nesting seabirds by island populations of red deer Cervuseluphus and sheep Ovis. The Zoological Society of London, 216, 565–573.

Gleason, J.S., Hoffman, R.A. & Wendland, J.M. (2005) Beavers, Castor canadensis, feeding on salmon carcasses: Opportunistic use of a seasonally superabundant food source. Canadian Field-Naturalist, 119, 591–593.

Nack, J.L. & Ribic, C.A. (2005) Apparent Predation by Cattle at Grassland Bird Nests. The Wilson Bulletin, 117, 56–62.

Naranjo, S. & Gibson, R. (1996) Phytophagy in predaceous heteroptera: effects on life history and population dynamics. ZoophytophagousHeteroptera: implications for life history and integrated pest management, pp. 57–93.

O’Donoghue, M. (1994) Early survival of juvenile snowshoe hares. Ecology, 75, 1582–1592.

Pietz, P.J. & Granfors, D.A. (2000) White-tailed deer (Odocoileusvirginianus) predation on grassland songbird nestlings. The American Midland Naturalist, 144, 419–422.

Richardson, M.L., Reagel, P.F., Mitchell, R.F. & Whitman, D.W. (2012) Opportunistic Carnivory by Romaleamicroptera (Orthoptera: Acrididae). Annals of the Entomological Society of America, 105, 28–35.

Singer, M.S. & Bernays, E.A. (2003) Understanding omnivory needs a behavioral perspective. Ecology, 84, 2532–2537.

Eggshell consumption and host breadth

Bernays (1998) noted that cannibalism is common in polyphagous insects; this assertion was not quantified though my own observations also anecdotally bear this out. A problem with truly making this correlation is the paucity of records of cannibalism and even fewer that decisively say cannibalism does not occur in a species. Therefore I sought out another omnivorous behavior that might be correlated with generalism and is reported in the literature. Margaret Brooks’ (1991) rearing records of 77 species of British moths include whether or not the larva ate the eggshell (additional species without a note in either direction were excluded). I then looked up host breadth from the British Natural History Museum’s HOSTS database (Robinson et al 2010). These are combined into Table A1.

A mixed effects model with a fixed effect of eggshell consumption and random effects of both genus and family of caterpillar with a negative-binomial error distribution has a positive and significant coefficient for eggshell consumption (0.78 + 0.25, z = 3.13, df residual = 70, p = 0.002) and this model fits significantly better than the same model without eggshell consumption term (Likelihood ratio test, X2 = 9.4, df=1, p = 0.002). This model predicts 7.44 (5.03 – 10.98) host families consumed for a species which consumes its eggshell versus 3.39 (2.95 – 3.89) for one which does not.

Interestingly, the limited amount of butterfly data from Brooks and Knight (1980) does not show any significant pattern. A mixed effect model including eggshell consumption as a fixed effect and genus and family as random effects does not fit significantly better than a null model with no fixed effect (LR test, X2 = 2.9, df residual = 46, p = 0.09). Unlike in moths, where many families have members which both eat and do not eat eggshells, most butterfly families seem phylogenetically consistent in their eggshell consumption. Notably, like all Lycaenids noted, the predatory Maculiniaarion does not eat its eggshell. In contrast, in moths, 2/3 of families with more than two species noted had both egg-shell consuming and eschewing species allowing a comparison less confounded by phylogeny.

Dave Wagner and Charley Eisemann (pers. comm.) caution against use of the HOSTS database for analyses such as these, because of some various erroneous or misattributed records which exist, and are even expected for such a comprehensive venture. Nevertheless, as a starting point for hypothesis generation and background natural history, as it is used here, it is sufficient, but for a more formal meta-analysis, the references for each species should be checked carefully.

Additional References

Brooks, M., 1991.A complete guide to British moths (Macrolepidoptera). Cape.

Brooks, M. and Knight, C. 1982. A complete guide to British Butterflies. Cape.

Figure 1: Box plot of plant families consumed by Brooks’ 77 moth species, by eggshell consumption (n=56, 21).

Table A1, Brooks eggshell data and HOSTS familial records for 77 species of British moths. Two lichen-feeders are marked “NA” with respect to host plant families consumed.

family / genus / species / eggshell_eaten / num_families
Hepialidae / Korscheltellus / lupulinus / 0 / 10
Cossidae / Zeuzera / pyrina / 0 / 15
Zygaenidae / Adscita / geryon / 0 / 1
Zygaenidae / Zygaena / filipendulae / 0 / 1
Limacodidae / Apoda / limacodes / 0 / 1
Sesiidae / Sesia / bembeciformis / 0 / 2
Lasiocampidae / Malacosoma / neustria / 0 / 6
Lasiocampidae / Lasiocampa / quercus / 0 / 11
Saturniidae / Saturnia / pavonia / 0 / 18
Endromidae / Endromis / versicolora / 0 / 3
Drepanidae / Watsonalla / binaria / 0 / 2
Thyatiridae / Habrosyne / pyritoides / 0 / 2
Thyatiridae / Achlya / flavicornis / 0 / 2
Geometridae / Archiearis / parthenias / 0 / 2
Geometridae / Alsophila / aescularia / 0 / 8
Geometridae / Geometra / papilionaria / 0 / 4
Geometridae / Hemistola / chrysoprasaria / 0 / 1
Geometridae / Cyclophoroa / linearia / 0 / 1
Geometridae / Xanthorhoe / fluctuata / 0 / 1
Geometridae / Anticlea / badiata / 0 / 1
Geometridae / Operophtera / brumata / 0 / 15
Geometridae / Eupithecia / pulchellata / 0 / 1
Geometridae / Eupithecia / venosata / 0 / 1
Geometridae / Abraxas / grossulariata / 0 / 12
Geometridae / Opisthograptis / luteolata / 0 / 4
Geometridae / Selenia / dentaria / 0 / 8
Geometridae / Colotois / pennaria / 0 / 8
Geometridae / Erannis / defoliaria / 0 / 11
Geometridae / Ematurga / atomaria / 0 / 9
Geometridae / Bupalus / pinaria / 0 / 1
Notodontidae / Phalera / bucephela / 0 / 10
Notodontidae / Cerura / vinula / 0 / 2
Notodontidae / Notodonta / dromedarius / 0 / 2
Notodontidae / Peridea / anceps / 0 / 1
Arctiidae / Callimorpha / dominula / 0 / 10
Arctiidae / Tyria / jacobaeae / 0 / 1
Nolidae / Nola / cucullatella / 0 / 1
Noctuidae / Hadena / bicruris / 0 / 1
Noctuidae / Panolis / flammea / 0 / 2
Noctuidae / Cucullia / verbasci / 0 / 2
Noctuidae / Xylocampa / areola / 0 / 1
Noctuidae / Allophyes / oxyacanthae / 0 / 2
Noctuidae / Acronicta / leporina / 0 / 6
Noctuidae / Phlogophora / meticulosa / 0 / 12
Noctuidae / Nonagria / typhae / 0 / 2
Noctuidae / Arenostola / phragmitidis / 0 / 1
Noctuidae / Eustrotia / uncula / 0 / 2
Noctuidae / Earias / clorana / 0 / 1
Noctuidae / Bena / prasinana / 0 / 2
Noctuidae / Colocasia / coryli / 0 / 7
Noctuidae / Diachrysia / chrysitis / 0 / 7
Noctuidae / Polychrysia / moneta / 0 / 1
Noctuidae / Autographa / gamma / 0 / 25
Noctuidae / Catocala / nupta / 0 / 1
Noctuidae / Callistege / mi / 0 / 6
Noctuidae / Hypena / proboscidalis / 0 / 3
Lasiocampidae / Macrothylacia / rubi / 1 / 8
Lasiocampidae / Philudoria / potatoria / 1 / 2
Sphingidae / Hyloicus / pinastri / 1 / 1
Sphingidae / Laothoe / populi / 1 / 4
Sphingidae / Deilephila / porcellus / 1 / 4
Notodontidae / Stauropus / fagi / 1 / 11
Lymantriidae / Orgyia / antiqua / 1 / 24
Lymantriidae / Calliteara / pudibunda / 1 / 11
Lymantriidae / Euproctis / chrysorrhoea / 1 / 19
Lymantriidae / Lymantria / monacha / 1 / 7
Arctiidae / Nudaria / mundana / 1 / NA
Arctiidae / Eilema / lurideola / 1 / NA
Arctiidae / Arctia / caja / 1 / 21
Arctiidae / Diacrisia / sannio / 1 / 9
Arctiidae / Spilosoma / lutea / 1 / 10
Noctuidae / Agrotis / puta / 1 / 5
Noctuidae / Noctua / pronuba / 1 / 14
Noctuidae / Orthosia / gothica / 1 / 17
Noctuidae / Heliothis / maritima / 1 / 4
Noctuidae / Scoliopteryx / libatrix / 1 / 7
Noctuidae / Phytometra / viridaria / 1 / 2

Table A2: Butterfly data from Brooks and Knight (1982) and the HOSTS database (Robinson et al 2010).

Satyridae / Pararge / aegeria / 1 / 1 / foliage
Satyridae / Lasiommata / megera / 1 / 1 / foliage
Satyridae / Erebia / epiphron / 1 / 1 / foliage
Satyridae / Erebia / aethiops / 1 / 1 / foliage
Satyridae / Melanargia / galathea / 1 / 1 / foliage
Satyridae / Pyronia / tithonus / 1 / 1 / foliage
Nymphalidae / Boloria / selene / 1 / 1 / foliage
Nymphalidae / Argynnis / aglaja / 1 / 1 / foliage
Nymphalidae / Argynnis / paphia / 1 / 1 / foliage
Nymphalidae / Vanessa / atalanta / 0 / 2 / foliage
Nymphalidae / Vanessa / cardui / 0 / 17 / foliage
Nymphalidae / Aglais / urticae / 0 / 2 / foliage
Nymphalidae / Nymphalis / polychloros / 0 / 4 / foliage
Nymphalidae / Inachis / io / 0 / 4 / foliage
Nymphalidae / Polygonia / c-album / 0 / 9 / foliage
Nymphalidae / Apatura / iris / 1 / 2 / foliage
Nymphalidae / Ladoga / camilla / 1 / 1 / foliage
Nemeobiidae / Hamearis / lucina / 1 / 1 / foliage
Lycaenidae / Cupido / minimus / 0 / 1 / reproductive
Lycaenidae / Plebejus / argus / 0 / 5 / reproductive
Lycaenidae / Aricia / agestis / 0 / 2 / foliage
Lycaenidae / Aricia / artaxerxes / 0 / 2 / foliage
Lycaenidae / Polyommatus / icarus / 0 / 1 / reproductive
Lycaenidae / Lysandra / coridon / 0 / 1 / foliage
Lycaenidae / Lysandra / bellargus / 0 / 1 / foliage
Lycaenidae / Maculinea / arion / 0 / 1 / reproductive
Lycaenidae / Celastrina / argiolus / 0 / 17 / reproductive
Lycaenidae / Lycaena / phlaeas / 0 / 1 / foliage
Lycaenidae / Lycaena / dispar / 0 / 1 / foliage
Lycaenidae / Callophrys / rubi / 0 / 8 / reproductive
Lycaenidae / Thecla / betulae / 0 / 1 / foliage
Lycaenidae / Quercusia / quercus / 0 / 1 / foliage
Lycaenidae / Satyrium / w-album / 0 / 1 / foliage
Lycaenidae / Satyrium / pruni / 0 / 1 / foliage
Pieridae / Leptidea / sinapis / 1 / 1 / foliage
Pieridae / Pieris / brassicae / 1 / 6 / foliage
Pieridae / Pieris / rapae / 1 / 6 / foliage
Pieridae / Pieris / napi / 1 / 4 / foliage
Pieridae / Anthocharis / cardamines / 1 / 1 / reproductive
Pieridae / Colias / croceus / 1 / 1 / foliage
Pieridae / Gonepteryx / rhamni / 0 / 2 / foliage
Papilionidae / Papilio / machaon / 1 / 5 / foliage
Hesperiidae / Erynnis / tages / 0 / 1 / foliage
Hesperiidae / Pyrgus / malvae / 0 / 1 / foliage
Hesperiidae / Carterocephalus / palaemon / 1 / 1 / foliage
Hesperiidae / Thymelicus / sylvestris / 1 / 1 / foliage
Hesperiidae / Thymelicus / lineola / 0 / 1 / foliage
Hesperiidae / Thymelicus / acteon / 0 / 1 / foliage
Hesperiidae / Hesperia / comma / 0 / 1 / foliage
Hesperiidae / Ochlodes / venata / 1 / 1 / foliage