Mimulus guttatus is a widespread riparian plant native to western North America. Due to its wide distribution and phenotypic variation it has been the subject of many studies incorporating genetic information into ecological and life history evolution studies. Mimulus guttatus defends itself from herbivory with physical defenses (e.g. trichomes) as well as a suite of phytochemical defenses; phenylpropanoid glycosides (PPGs). Despite its importance as a model organism little has been done on the herbivores that feed on this plant. We used literature records as well as field observations to construct a list of the Lepidoptera that utilize M. guttatus as a food plant. Sixteen species of Lepidoptera within five families were recorded as feeding on M. guttatus. Six of these species are classified as generalist herbivores, while the rest have varying degrees of host plant specialization.
Mimulus guttatus D.C. (syn. Erythranthe guttata (Fisch. ex DC.) G.L.Nesom, Family Phrymacea) is a plant species complex native to riparian areas of western North America. This species is an important model organism for studies of evolutionary genomics and ecology having been cited in over 1,000 studies. This use is in part due to its tremendous phenotypic variation, including variation in life history (annual vs. perennial; Hall & Willis 2006), leaf morphology (Wu et al. 2010), and anti-herbivore defenses (Holeski 2007a, Holeski et al. 2013). In addition to its large native range, non-native populations of M. guttatus occur in eastern North America, Europe, and New Zealand (Stace 2010, Webb et al. 1988).
Fig. 1.
A. Mimulus guttatus in a typical habit near flowing water, B. Chemical structure of Conandroside, a phenylpropanoid glycoside (PPG) produced by M. guttatus that acts as a chemical defense. C. glandular M.guttatus trichomes, these act as defense from herbivores. Photos by M. Rotter.
Mimulus guttatus possesses both physical and chemical anti-herbivore defenses (Fig. 1). Physical defenses include trichomes. Although trichomes can serve as both a defense against herbivores and in physiological and abiotic interactions, evidence suggests that they function largely as an anti-herbivore defense within perennial and/or coastal M. guttatus populations (Holeski et al. 2010). Many trichomes produced by the species are glandular with sticky secretions (Holeski 2007a). Mimulus guttatus also produces a suite of foliar secondary compounds, phenylpropanoid glycosides (PPGs). Phenylpropanoid glycosides have been shown to deter feeding by generalist herbivores (Cooper et al. 1980, Mølgaard 1986) while specialist lepidopteran herbivores may use at least some PPGs as feeding stimulants (Holeski et al. 2013). Many plant species within the Schrophulariacea sensu lato (where Phrymacea was once included) contain PPGs (Mølgaard & Ravn 1988). This shared phytochemistry leads to many of the same specialist herbivores feeding from plants across the Schrophulariacea sensu lato (Bowers 1988). Despite its defenses, herbivory on M. guttatus can still be very damaging to plants (Fig. 2).
Lepidoptera have long been an important order in studies of the co-evolution of plants and their insect herbivores (Ehlrich & Raven 1964). The “arms race” between insect herbivores and plants has driven evolution of novel secondary compounds, as well as the means to sequester or detoxify these compounds within many groups of plants and insects, often leading to evolutionary radiations (Cornell & Hawkins 2003, Marquis et al. 2016). For instance, rapid radiation within the Pieridae butterfly family following an adaptive radiation event in its host plant order Brassicales was most likely due to Pieridae specialization on glucosinolates in Brassicales (Braby & Trueman 2006). A clear picture of the evolution within the Lepidoptera thus necessitates a thorough knowledge of host plant use as well as the host plant range of individual species of Lepidoptera. This review uses literature references as well as our own field observations and rearing records to record the diversity of Lepidoptera that feed on M. guttatus. We also discuss the ecological context and chemical ecology of these interactions.
Methods
To locate M. guttatus host records for Lepidoptera we consulted field guides with host records, species catalogues, taxonomic treatments of specific groups, and natural history reports. We checked state and regional field guides from countries where M. guttatus is present in order to find species that may use M. guttatus only locally. This literature search was combined with over three years (2014–2016) of observational records of Lepidoptera feeding on Mimulus guttatus. Over 60 populations of M. guttatus throughout its range in western North America were searched for caterpillars. These searches included both visual and sweep net surveys. To be included in our list of species that utilize M. guttatus as a host, a caterpillar had to be either observed actively feeding on the plant in the field or was collected from the plant and successfully reared to adulthood on a diet of M. guttatus in the lab. To classify the degree of host plant specialization for each Lepidopteran, we recorded a representative list of other species of plants that each Lepidoptera species is known to feed upon
Results and Discussion
We found 16 species of Lepidoptera within five families that utilize M. guttatus as a food plant (Tables 1 & 2). Eight of these species were not previously recorded to feed on M. guttatus (Table 2). Of the 16 total species, six are broad generalists while four would be considered specialists on plants in the same clade of families as M. guttatus (Scrophulariacea sensu lato). One species has been recorded feeding on other plants within the Lamiaceae (Stachys spp.), and for two of the species the only known food plant is M. guttatus.
Generalist Lepidoptera found feeding on Mimulus guttatus.
The six species of generalist herbivores known to feed on M. guttatus are all species with large geographic ranges. For example, Amphipyra tragopoginis (Clerck, 1759) (Noctuidae) is a common moth throughout the Holarctic region and can be found throughout the northern portions of the native M. guttatus range, although the moth itself may have been introduced to North America (Forbes 1954). Trichoplusia ni (Hübner, [1803]) (Noctuidae) is another widespread generalist, with a geographic range covering most of North America, which has been found feeding on M. guttatus. We collected this species feeding on multiple M. guttatus populations from the northern Cascades to the southern Sierra Nevada Mountains. Trichoplusia ni has predilections for members of the Brassicacea but will often feed on any available forb (Powell & Opler 2009; Wagner et al. 2011). Mimulus guttatus often grows with members of Brassicacea particularly the non-native water cress (Nasturtium officinale) (Rotter unpublished data), to which T. ni may be initially attracted to and then utilize other plants in the community.
Fig. 3.
A. Herreshoffia gracea caterpillar from Gila County Arizona. B. Freshly emerged adult. Photo by M. Rotter.
Two generalists that may sequester plant secondary compounds were recorded feeding on M. guttatus. The species Estigmene acrea (Drury, 1773) (Eribidae) is a widespread generalist throughout North America, and is a pest of many cultivated crops. Late instar caterpillars were collected feeding on M. guttatus near Mormon Lake in central Coconino County, Arizona. Estigmene acrea was locally abundant at the time of collection (a likely outbreak year in northern Arizona). Although overall a generalist, E. acrea does exhibit host plant preferences at different times of its life cycle (Casterjon et al. 2006). As a late-instar caterpillar, E. acrea prefer plants that can offer protection from parasitoids via caterpillar sequestration of plant metabolites (Singer et al. 2004). Grammia incurropta (Edwards, 1881) (Eribidae) is a common lab species for investigating the evolution of generalist diets (Wagner & Conner 2008), which is also known to sequester and favor plant metabolites in order to “medicate” itself (Smilanich et al. 2011). Records of this species feeding on M. guttatus in the field are from Arizona (Michael Singer, personal communication), and the species readily consumes M. guttatus in the lab.
Fig. 4.
A. Autographa pasiphaeia caterpillar from Kern county California. B. Freshly emerged adult. Photo by M. Rott
There were three records of Lepidoptera feeding on M. guttatus outside of its native western North American range, with no records of feeding on M. guttatus within its native range. Our records may thus corroborate results of several studies showing that generalist native herbivores may prefer non-native plants (Agrawal & Kotanen 2003, Parker & Hey 2004). The literature record of Amphipyra tragopoginis feeding on M. guttatus comes from the United Kingdom where M. guttatus is a widespread non-native plant (Hancock & Wallace 1986). Nematocampa resistaria (Herrich-Schäffer, [1856]) (Geometridae) and Spodoptera ornithogalli (Guenée, 1852) (Noctuidae) were recorded feeding on an isolated population of M. guttatus (over 1000 km from the next known population of M. guttatus) in the Upper Peninsula of Michigan (Ontonagon County). Both of these species are common in eastern North America where they feed on a wide variety of plants (Wagner et al. 2011, Wagner 2005).
Specialist Lepidoptera feeding on Mimulus guttatus.
Specialist Lepidoptera that feed on Mimulus guttatus also share other host plant species. For instance the two Junonia spp. (Nymphalidae) that feed on M. guttatus, as well as Euphydryas chalcedona (Doubleday, [1847]) (Nymphalidae), feed on plant species within the Scrophulariacea senso lato as well as other related families (e.g., Plantaginacea, Verbenaceae, and Acanthaceae). We hypothesize that this shared specialization on host plants within and related to the Scrophulariacea senso lato is due to overlap in host plant phytochemical profile. For example, the PPG verbascoside has been reported in many plant species in this group (Jimenez & Riguera 1994; Keefover-Ring et al. 2014). Compounds in another phytochemical group, iridoid glycosides, are present in many of these plants (e.g., Plantaginacea and Verbanaceae) but not M. guttatus (M.D. Bowers, personal communication).
Table 1.
Literature references of Lepidoptera feeding on Mimulus guttatus.
The host plants utilized by E. chalcedona populations vary by region, as is the case with many Nymphalidae within the tribe Melitanea. For example, coastal California populations of E. chalcedona often feed primarily on Diplacus aurantiacus (Phrymacea) and populations from the Sonoran Desert feed typically on Keckiella antirrhinoides (Plantaginacea) (Kuussaari et al 2004, Rotter personal observation). Euphydryas chalcedona use of M. guttatus in the wild is likely localized to several populations in California and Nevada, but populations found feeding on other species will oviposit and the larva will feed on M. guttatus in the lab. Chemical variation between host plant populations as well as environmental and biotic factors have likely led to local adaptation of E. chalcedona populations (Bowers 1986).
The genus Annaphila (Noctuidae) contains several species that feed on M. guttatus. Annaphila lithosina Hy. Edwards, 1875 was documented ovipositing on M. guttatus, and its larva feed on flowers of the plant (Buckett 1966). Prior to 1966 the host plant of A. lithosina was unknown, and Buckett speculated that M. guttatus may be the only host plant for A. lithosina. Annaphila casta Hy. Edwards, 1890 (which forms a complex with A. lithosina and A. miona Smith, 1908) was recorded to readily feed on M. guttatus in captivity, and oviposits on M. moschatus in the wild (Henne 1967). Further study of the relationship of Annaphila spp. and M. guttatus, particularly regarding how the moths interact with PPGs could help elucidate the natural history of the beautiful but little-studied Annaphila.
Table 2.
Field and laboratory observations of Lepidoptera feeding on Mimulus guttatus, not previously recorded.
Other host records on Mimulus guttatus.
During the course of this study two particularly interesting records of Lepidoptera feeding on M. guttatus were recorded. The first record is the first documented host plant record for Herreshoffia gracea Sperry, 1949 (Geometridae) (Fig. 3). This moth was originally described from Oak Creek Canyon, Coconino County, Arizona (Sperry 1949). We collected several late instar larval geometrid species from Mimulus guttatus along Fossil Creek, Gila County, Arizona in April of 2015. Both Oak Creek and Fossil Creek are semi-shaded perennial streams running through canyons on the edge of the Mogollon Rim of northern Arizona. We collected mature caterpillars actively feeding on M. guttatus; live caterpillars were also taken back to the lab where they were fed until they pupated. One adult was successfully reared (all other pupae had parasitoid wasps which emerged after 18 days in a chrysalis; Specimen MR 715, Northern Arizona University). Herreshoffia gracea has been recorded in Coconino, Cochise, and now Gila Counties in Arizona and Siskyou County in northern California (Moth Photographers Group, 2016); in every recorded county for this moth M. guttatus is a common riparian plant. Although it is not known if H. gracea utilizes other plants, many other members of the Geometrid tribe Xanthorhioni are limited in their larval diet breadth (Powell & Opler 2009).
We collected late instar caterpillars of Autographa pasiphaeia (Grote, 1873) (Noctuidae) (Fig. 4) from M. guttatus along the Kern River, Kern County, California. These were reared in the lab and had adults successfully emerge (Specimen MR 716 Northern Arizona University). This species ranges throughout California and into Oregon (Powell & Opler 2008). Within this range the common host plant is Stachys spp. (Lamiacea), which shares a common clade with M. guttatus within the order Lamiales (Stevens 2001). Several Stachys species contain verbascoside (Jimenez & Riguera 1994), a PPG that is also present in Mimulus guttatus.
Suspected hosts on Mimulus guttatus.
There are several records of the Nymphalid Phyciodes mylitta (W.H. Edwards, 1861) using M. guttatus as a host plant. More often the host plants of P. mylitta are listed as members of the Asteracea tribe Cynareae (thistle tribe). Mimulus guttatus is thus an odd addition to this group. The first record of P. mylitta on M. guttatus appears in Scott's work on North American butterflies (1986). It appears that this record may simply have been repeated in later citations. However, P. mylitta is common in many areas where M. guttatus is present, so further investigation may be warranted.
Spodoptera exigua (Hübner) (Noctuidae) is a widespread generalist that can utilize a wider array of plants as hosts. This species was reared in the lab on M. guttatus and could likely utilize it in the wild.
Conclusion
The Lepidoptera fauna that utilizes M. guttatus is composed of specialists that also feed on relatively limited numbers of other, related plant species, as well as multiple broad generalists. Although several species have been recorded to have M. guttatus as their sole host, this may merely be due to limited records for these Lepidoptera. We are currently conducting no-choice feeding trials using several of the species listed here to characterize the relationship between M. guttatus defense traits and herbivore performance. Understanding how these defense traits influence herbivores of M. guttatus as well as a thorough knowledge of the diversity feeding on M. guttatus will contribute greatly to understanding the evolutionary and ecological history of this model organism.
Acknowledgments
Funds from the Utah Native Plant Society, Idaho Native Plant Society, and the Michigan Botanical foundation supported sampling efforts. Additional funding was provided by a Northern Arizona University (NAU) fellowship (Rotter) and NAU start-up funds (Holeski).
