Cerruti R2 Hooks$ and Anahí Espíndola*
$Associate Professor and Extension Specialist and *Assistant Professor, CMNS, Department of Entomology
University of Maryland
Insect pollinators play an essential role in the maintenance of wild plant diversity and agricultural productivity. Indeed, global studies have shown that the vast majority of plants require animal pollination to produce fruit and seed. In temperate regions, major pollinator groups include bees (Hymenoptera), syrphid (Diptera), as well as butterflies and moths (Lepidoptera). In contrast to bees, Lepidoptera are not considered efficient pollinators of most cultivated plants. Nevertheless, they are vital pollinators of many flowering plants, especially in the wild as well as managed lands such as parks and yards.
The pollinating taxa of Lepidoptera are mainly in the moth families Sphingidae (hawk moths; Fig. 1), Noctuidae (owlet moths) and Geometridae (geometer moths), and the butterfly families Hesperiidae (skippers) and Papilionoidea (common butterflies). The adult stage of these lepidopterans obtains their nutrients and water from nectar of various flowers; and while exploiting flowers for food, pollination may occur. Moths and butterflies have different pollinator niches, as butterflies are very active during the day (diurnal) and visit open flowers during the morning hours and under full sunlight. Contrarily, moths are more active during the evening and night hours (nocturnal). As a response to this, some flowers may seek to increase pollination by changing color during a 24-hour period to attract butterflies during the day and moths at night. For example, Quisqualis indica flowers change color from white to pink to red which may be associated with a shift from moth to butterfly pollination (Fig. 2). A study conducted in China verified that different pollinators are attracted to each floral color stage; primarily moths at night and bees and butterflies during the day. Further, fruit set was higher for white than pink or red flowers indicating that moths contributed more to its reproductive success. While adult butterflies and moths are important pollinators, their larvae – often called caterpillars – may be economically important pests in agricultural, forest and urban environments. In some instances, their status as agricultural villains as caterpillars override their positive image as ecosystem service providers as adults.
Nectar and pollen consumption
Adult butterflies diet choice varies between species, populations, generations, sexes, age groups and individuals. Most adult lepidopterans feed on fluid resources such as nectar, decomposing animals, dung and fruit sap (Fig. 3) and others may not feed at all as adults. Butterflies consume nectar by active suction using their elongated mouthparts (called proboscis), and usually avoid highly concentrated nectar because of its high viscosity.
Nutritionally, nectar serves as a source of water, carbohydrates and amino acids; the latter allowing butterflies to meet their nitrogen requirements. Interestingly, butterfly-pollinated flowers tend to have higher concentrations of amino acids than do flowers pollinated by bees and other animals. This is remarkable since insects like butterflies, whose larval stages feed on plant foliage and adult stages on nectar have long been assumed to obtain most or all of their nitrogen-rich compounds needed for reproduction from larval feeding. Going against this assumption, it has been shown that both nectar consumption and larval food intake can affect the life span and fecundity (number of offsprings produced) of some butterfly species. For example, a recent study found that nitrogen-rich compounds (amino acids) present in nectar significantly increased the fecundity of the nectar-feeding butterfly Araschnia levana. However, their fecundity was enhanced only if the female fed on a poor-quality plant as a larva. This suggests that nectar can act as a necessary dietary complement if a butterfly fed on a nitrogen-poor plant as a larva.
Another nitrogen-rich floral reward is pollen. Nectar-consuming butterflies come into contact with pollen while visiting flowers, but the vast majority of butterflies is unable to feed on pollen. However, butterflies of the neotropical genera Heliconius and Laparus (Lepidoptera: Nymphalidae; Fig. 4) evolved a feeding technique in which amino acids are extracted from pollen grains, rather than fortuitously during their pursuit of nectar. These butterflies collect and accumulate large pollen loads, and the production of saliva helps keep it attached to their proboscis while they gently chew the pollen to consume its amino acids. Pollen feeding is thought to increase Heliconius longevity and egg production.
Butterflies efficiency as pollinators
It has been suggested that for most plant species, butterflies visit flowers less frequently than bees and deposit less pollen per visit. With a few notable exceptions such as yucca moths, adult lepidopterans show little floral specialization, preferring flowers with large landing surfaces, deep, narrow corollas that can accommodate their elongated mouths, and plants displaying many flowers in close proximity. Butterflies prefer visiting large flower heads, and when searching flowers for nectar, pollen grains attach to various body extremities (e.g., mouth parts, head) depending on the plant’s floral architecture. However, because butterflies’ legs and mouth parts are elongated, most of their body does not enter in direct contact with the plant’s pollen. Consequently, butterflies pick up less pollen on their bodies than bees, and most of it is usually deposited on or around their heads and mouth parts. This pollen is then transferred to the surface of the stigma when the butterfly reaches for nectar in a new flower. Because little pollen is usually carried by butterflies, and the fact that – unlike bees – they don’t have specialized structures for carrying pollen, butterflies are less successful than bees at moving pollen between flowers. Although not as efficient as bees, butterflies can be very effective pollinators, and among the insect fauna they qualify as essential pollinators. In many instances, a decline in the butterfly fauna is attributed to a decrease in nectar-rich and economically or culturally important wild plant species. Further, butterflies can be important in agricultural systems. For example, a survey of pollinators associated with macadamia in NE Brazil found that macadamia yields mainly benefited from pollination by butterflies rather than bees. Consequently, butterflies were responsible for > 50% of floral visits to macadamia flower. Moreover, their pollination of some vegetable crops contributes strongly to seed production.
Many flowers, including some orchids, are completely dependent on butterflies for pollination, and a member of the pea family, the peacock flower (Caesalpinia pulcherrima; Fig. 5) is largely dependent on butterflies for pollination, with pollen being mainly carried on their wings. In addition to butterflies, some moths have a special relationship with specific plants. For example, the yucca plant (Hesperoyucca whipplei) is pollinated by the yucca moth (Tegeticula maculata) with which it has a symbiotic relationship. The gravid female moth gathers pollen grains from flowers at night and forms them into a ball. She carries the ball in her mouth to another yucca flower. She then inserts her ovipositor into the ovary wall of the flower and deposits a single egg and then pushes the pollen into the stigma, thus pollinating the flower. The larva hatches in late spring or summer, and feeds on some of the developing seeds. Emergence of the adult moth occurs while yucca plants are again in bloom, allowing the cycle to continue.
Flower structure and mouthparts
The body architecture (e.g., body size, mouth shape) and behavior of pollinators with respect to the flower’s dimension and morphology, are some of the factors that define which floral visitors are effective pollinators. Many studies of plant-pollinator interactions provide evidence that the morphological match between the flower shape and size, and the length of pollinators’ mouthparts influences pollination success. In relation to this, it has been observed that flowers and their pollinators engage in a series of reciprocal adaptive or coevolutionary cycles. In these cycles, plants that have the “best” floral shape for a specific pollinator are capable of producing more seeds, while pollinators that are capable of obtaining more nectar from an individual flower visit will also obtain greater energy required to produce more offsprings. When the pollinator and plant requirements align like this, plants tend to evolve floral shapes that match their “best” pollinator, while pollinators tend to evolve specific floral preferences and morphologies that match the plant. Over many generations, this leads to the establishment of floral preferences in pollinators, and a convergence in floral shapes of flowers visited by a given type of pollinator. It is for this reason that butterflies and hummingbirds are seen more often visiting long-necked or trumpet shaped flowers, than other pollinators; and these flower types are better pollinated by butterflies or hummingbirds than other pollinator groups. The result of these coevolutionary processes can be seen in many cases of pollination, but some of the most impressive examples are those having led to the evolution of extremely long proboscides (up to 14 inches) in some lepidopterans (Fig. 6), which match the length of the floral tube of their preferred flowers.
How do moths and butterflies locate flowers
In order to locate floral resources, lepidopterans use a series of cues, such as specific colors, shapes, sizes and odors. As stated previously, moths are major nocturnal pollinators of a diverse range of plant species but have been historically considered to contribute little to overall pollination. However, recent research has rejected this notion, demonstrating that nocturnal moths contribute strongly to pollination, even to the point of compensating for poor pollination by diurnal pollinators. Moths are attracted to pale or white flowers with an open cup or tubular shape, heavy with fragrance and dilute nectar, and typically open in late afternoon to night. In turn, these plants are also specialized in pollination by moths, with these attractive traits having evolved through millions of years of coevolution. An example of these plants includes the creeping buttercup or honeysuckle, which tend to emit a strong fragrance at night.
Unlike moths, butterflies are diurnal and typically visit flowers under heavy sunlight, preferring those displayed in clusters and offering large nectar rewards (Fig. 7). Flowers specialized in pollination by butterflies are often brightly colored (red, yellow, orange), lack an apparent scent and secrete relatively dilute nectar in narrow elongated floral tubes. Examples of butterfly flowers are goldenrods and Asters, which provide a large landing surface as well as abundant and accessible nectar. Some of these preferences in butterflies are due to the butterfly’s good perception of color, which in most cases covers a wider range of the spectrum than human vision. Indeed, various studies have demonstrated that some pollinators rely strongly on color to make their foraging decisions, and this is certainly the case of butterflies. Similar to hummingbirds, butterflies have a good perception of the color red and as such, are attracted to red flowers. Further, many lepidopterans are able to distinguish various shades of yellow. To this point, an experiment consisting of potted daylily and nightlily showed that swallowtail butterflies preferentially visited reddish or orange-colored flowers and hawkmoths favored yellowish flowers. Similar to many insects, butterflies are capable of seeing ultraviolet light, which allows them to follow special nectar markings present on flowers that are only visible under that type of light. Correspondingly to how butterflies and moths are able to sense odors of their preferred flowers, studies have shown that butterflies may also sense the nectar amino acid content of different flowers, preferring those with high versus low amino acid content. For instance, studies found that, when given the choice, the cabbage white butterfly (Pieris rapae) preferred feeding on artificial flowers containing sugar-amino acid mixes, versus sugar-only nectar of Lantana camara (a perennial shrub).
Butterfly flower avoidance
As with all organisms, butterflies have their own natural enemies at the immature and adult stages. Egg, larva and pupa of butterflies and moths are vulnerable to parasitism and predation. Adult stages may suffer mortality from mammalian and arthropod predation. For instance, when visiting flowers, butterflies may be vulnerable to arthropod predators such as mantises and spiders (Fig. 8). Studies have shown that butterflies are capable of avoiding flowers with predator cues. For example, similar to bees, they have been shown to avoid flowers with artificial spiders and models of spider forelimbs. In another study conducted in a butterfly pavilion, visiting butterflies stayed away from flowers containing dead mantises.
Howbeit, it is debatable whether butterflies were responding to the mantis’s cues or were simply avoiding flowers containing foreign objects. Still, some studies seem to agree that at least some avoidance is due to visual recognition. Interestingly, the degree of avoidance recorded in these studies indicated that it was weaker in butterflies reared in the pavilion than in wild butterflies. This tends to indicate that a part of this avoidance is learned and a reflection of previous predation experiences.
Drivers of pollinator and butterfly losses. Many insect pollinators that provide vital services are declining and multiple factors have been implicated. In Europe, noticeable drops have been observed for butterflies, wild bees and hoverflies. Similarly, lepidopterists in the US are reporting that butterflies are in decline. Butterflies face a wide range of threats including habitat loss, changes in land management and land use, climate change, disease, pesticides and invasive organisms. Another driver of pollinator decline is agriculture intensification, which results in loss and fragmentation of pollinator-diverse habitats such as semi-natural grasslands, and is also associated with increased chemical use. Other factors associated with human activity have also been identified as contributors to pollinator loss. For instance, pollutants and urbanization can negatively affect the richness and abundance of native plant species used by pollinators, and thus lead to poor pollinator communities. Anthropogenic changes in the landscape can sometimes affect pollinators in surprising and indirect ways. For instance, changes in land use can lead to increased encroachment of plants such as some shrubs that are not congenial to butterflies and an associated decrease in butterfly richness and abundance by negatively impacting herbaceous plant cover and diversity. Further, enhanced shrub covering may indirectly affect pollinators by increasing their predation by perching birds.
Should bee and butterfly conservation plans be the same? The ecology of lepidopterans differs from that of bees. For example, bees require nectar and pollen throughout their life, while butterflies only utilize nectar as adults. Further, most caterpillars are leaf-feeders and do not require any parental care, while bees must collect pollen and nectar to support their brood and themselves. Moreover, while most bee species develop in relatively protected habitats (i.e., their nests), caterpillars are exposed while feeding on their host plants, vulnerable to predation, parasitism and climatic factors. These differences may require some alterations in conservation efforts aimed at protecting butterflies and bees. For example, butterfly-friendly environments must contain plants that support the larval and adult stages, and land management practices need to be appropriate for preserving plant species needed in caterpillar diets. Failing to do so would lead to low caterpillar survival or death, and the eventual loss of the butterfly population.
Conserving butterflies. To help save butterflies and other pollinators, it is recommended that a diversity of colorful, wildlife-friendly plants full of nectar be planted in gardens, yards, urban and recreational areas and on/nearby arable lands. Floral diversity is a pre-requisite for enhancing butterfly conservation, especially in urban environments. To better ensure butterflies have access to resources throughout the year, flowers with a range of bloom time (early spring through fall) and morphological features should be planted. Further, a habitat hospitable to butterflies and moths provides food for caterpillars, nectar-bearing flowers for adults, and consists of at least some native species. Indeed, although a few can feed on exotic plants, most caterpillar species are specialized on native plant species. Likewise, although some caterpillars are polyphagous, most are restricted to a few or just one plant species. Protecting land for butterflies does not equate to transforming all land into a fully protected area. Indeed, land in public settings, such as roadway medians, roadsides, landscaped parks, and even railway embankments have the potential to support large populations of pollinators. Confirming this, studies found that bee and butterfly species richness and abundance were higher in railway embankments than in grasslands. Further, they demonstrated that in that context non-vegetated ground negatively affected butterfly populations, since their diversity positively depended on species richness of native plants. For this same reason, open forests also tend to harbor higher pollinator diversity than forests with a very closed canopy. Further, actions can be taken to improve the pollinator friendliness of different public lands. For instance, roadside management plans can be designed to benefit pollinators (Fig. 9). Roadsides with abundant and diverse native wildflowers managed with judicious mowing and herbicide use can become diverse pollinator habitats. Furthermore, research indicates that roadsides with high-quality habitat reduce pollinator mortality as insects remain in the roadside as opposed to leaving in search of flowers.
Land management tactics for increasing plant diversity (intercropping, cover cropping, insectary plants, flower borders, etc.) are often used to enhance populations of natural enemies in cropping systems. When this practice is used to augment natural enemy efficacy, it is often called conservation biological control. However, this same tactic can be used to concomitantly conserve biocontrol agents and pollinators, while enhancing other services to cropping system (i.e., pest suppression). In a similar context, the idea of companion planting can also represent a way to combine production with pollinator protection in agricultural landscapes. Companion planting is a traditional husbandry practice whereby a second plant species is planted alongside a crop with the goal of improving yield. Using a flowering species as a companion plant can make arable lands more congenial to pollinators resulting in improved pollination services and crop yield. A recent study examined the use of borage, Borago officinalis (Fig. 10), as a companion plant in strawberry. Borage plants were found to significantly increase yield and quality of strawberries, suggesting an increase in insect pollination per plant.
Immature stages of some moths and butterflies are viewed negatively because of their harm to agriculture. However, adult lepidopterans are mostly cherished for their aesthetic beauty, and less recognized for their contribution to pollination. Howbeit, lepidopterans are vital contributors to the pollination of wild plants and domesticated crops; and though their efficiency at crop pollination does not reach the level of bees in most systems, there are instances in which their services are of greater value (as for pollination of macadamia nuts), or compensating diurnal pollination (as shown for nocturnal moths). Moreover, while bees are more likely to pollinate fruit crops, butterflies are primary pollinators for many vegetables and herbs, especially those in the carrot, sunflower, legume, mint and Brassica family. Although pollination of these vegetable crops is not needed for producing the edible portion of the crop, it is required for seed production, in which future plantings require. This suggests that efforts being directed to protect bee pollinators should similarly integrate moth and butterfly conservation. To this point, because the ecology of bees and lepidopterans differ especially with respect to resource requirements during their immature stage, plans directed at conserving bee and lepidopteran pollinators should take these differences into consideration. Financial support for the publication of this article is via USDA NIFA EIPM grant award numbers 2017-70006-27171.