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The cabbage looper (Trichoplusia ni) is a moth in the family Noctuidae, a family commonly referred to as owlet moths. It is a migratory moth found across North America and Eurasia, as far south as Florida and as far north as British Columbia.[1] Cruciferous vegetables; such as cabbage, bok choy, and broccoli; are its main host plant, hence the reference to cabbage in its common name. While these plants are preferred, over 160 plants can serve as hosts for the cabbage looper. Its migratory behavior and wide range of host plants attribute to its broad distribution. The cabbage looper population is generally greatest in the fall, but they can be found in any season. [2][3]

The cabbage looper larva is most notable for being a vegetable pest, especially for crucifers. While it is not extremely destructive, it is becoming difficult to manage, as this species has already developed resistance to many insecticides.[3][4] Numerous methods are being researched in order to manage this species.

Taxonomy

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The cabbage looper larva is considered to be a type of cabbage worm for its appearance and primary consumption of cabbages. While cabbage worms are all similar in appearance and host plants, they are not closely related in terms of phylogeny. In fact, none of the cabbage worms bear close phylogenetic relations, as they are all from different families.[4] The cabbage looper is a member of the family Noctuidae, one of the largest families in Lepidoptera.[5] It is related to other infamous vegetable pests, like the cutworm and armyworm.[3]

Description and Life Cycle

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Cabbage looper larva

Egg

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The cabbage looper eggs are generally yellow-white in color, dome-shaped, and patterned with ridges. They are 0.6mm in diameter and 0.4mm in height, and usually laid singly on the underside of leaves.[6]

  • In one day, 40-50 females can lay 1000-2000 viable eggs. Viable eggs generally hatch after three days, with unviable eggs failing to develop and collapsing in that time.[7]

Larva

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Cabbage looper pupa

Cabbage looper larvae are a type of cabbage worm, green in color with a white stripe on the side. After hatching, they are white and hairy, but eventually turn green and lose the hair, leaving only a few bristles. They can be identified by their unique looping behavior, in which they arch their body in a loop when they crawl.

  • Larvae are generally 3-4cm long, and can have four to seven instars within 9-14 days.[3] Larvae initially consume little, but increase their consumption during their lifetime until they are consuming three times their weight daily.[7]

Pupa

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When they pupate, they attach to the undersides of leaves and form a silky cocoon.[4] This stage can last 4-13 days, depending on the temperature of the environment.[3]

  • Male pupae are slightly larger than female.[7]

Adult

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The adult form is a moth with gray-brown front wings and light brown back wings.[3] Males can be distinguished from females by light brown hairs that lie flat against their abdomen.[8]

  • They are about 2.5 cm long and have a wingspan of 3.8 cm. As they are nocturnal, adults spend their days protected by their host plants and begin activity 30min before sunset.

Mating occurs 3 or 4 days after metamorphosis, during which 300-1400 eggs are oviposited. [2] The cabbage looper's life cycle is generally 24-33 days long, from egg to adulthood.[6]

Migration

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Cabbage looper populations in North America migrate from Mexico to Canada, depending on the seasons. It generally overwinters in Mexico or southern California, where temperatures are above 16ºC even during winter. It used to be found frequently in Florida, but this has lessened due to fewer cabbage crops.[1] As northern regions of North America grow warmer, the cabbage looper gradually moves upward, only migrating if the region is above 16ºC. [9] During summer, it is less commonly found in southern regions, due to high temperatures. Similar to the monarch butterfly, populations presumably migrate in groups, as there is little genetic difference between source and migrating populations.[10]

Similar seasonal distributions were found in Europe. There, the cabbage looper can be found from England to southeastern Europe.[9]

Temperature

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The cabbage looper migration patterns are highly temperature dependent, as temperature can impact development. It has the greatest impact on pupation, where pupae often cease to finish metamorphosis if grown at 10ºC. Even if pupae are transferred from 10ºC to 12.7ºC, they often emerge deformed, sometimes developing an extra instar. Temperatures above 35ºC also result in physical deformations in adults, such as poor wing development. Mating and flight are negatively impacted by temperatures above 32ºC and below 16ºC, which may explain why cabbage loopers migrate to northern regions once temperatures reach 16ºC.[9] The time between female calling and male response increases as temperature increases, but when the temperature reaches 27ºC, mating increases. At the same time, oviposition and longevity decrease, with hatching almost ceasing at 32ºC.[2] The embryo itself is actually quite resilient, as it is able to develop at 10ºC and at 40ºC. However, although it is developed, it is unable to hatch.[11]

  • Temperature does not affect the receptor neurons.[12]

Host Plants

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The cabbage looper is a generalist insect that can reside on over 160 host plants. The looper's variety of hosts is partially due to the ability of its salivary glands to differentially express based on the host. For example, cabbage and tomato plants use defensive strategies involving different compounds, and cabbage looper can combat either by upregulating the appropriate gene. The gland's high responsiveness to the diet allows for considerable flexibility in host plants. The cabbage looper's preferred hosts are crucifers like cabbage and broccoli, because it grows faster on these plants, possibly due to nutritional or chemical differences.[13] Tobacco can also be a host for the cabbage looper, although it is not preferred due its gum production and trichomes that negatively impact early larvae survival. However, older larvae are more resistant to these issues.[14] The number of caterpillars on a plant depends on plant's foliage, maturity, and height.[15]

Attraction to odors

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Cabbage loopers detect plant odors in order to seek food resources and suitable host plants for oviposition. Mated females respond faster to plant odors compared to their unmated female and male counterparts, which makes sense given that they have motivations of both food and oviposition.[16] Studies have shown that the cabbage looper is attracted to the floral compounds phenylacetaldehyde, methyl salicylate, 2-phenylethanol, benzaldehyde, benzyl alcohol, benzyl acetate, and methyl-2-methoxy benzoate, with the strongest attractor being phenylacetaldehyde.[17] The cabbage looper is more attracted to a blend of odors than phenylacetaldehyde alone.[18]

Pheromones

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Synthesis

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The cabbage looper is unique in that it does not hormonally regulate pheromone production. In fact, pheromones are constantly being produced, upon complete development of the pheromone glands at the adult stage. Studies suggest that there are stage specific proteins that correspond to the development of the gland. In particular, the immature gland lacks numerous enzymes crucial to pheromone biosynthesis, such as fatty acid synthetase and acetyltransferase, which is why the looper cannot produce pheromones prior to the adult stage.[19]

Similar to other pheromone biosynthesis reactions, female cabbage looper pheromone production initiates with synthesis of 16 and 18-carbon fatty acids. This is followed by desaturation at C!1 and chain shortening by two or four carbons. Finally, the fatty acid is reduced and acetylated to form an acetate ester. The result is a blend of different female pheromone compounds at a consistent ratio. This ratio can be highly altered by mutations in chain shortening proteins, demonstrating that the chain shortening step is important for determining the ratio of pheromones in the final blend.[20]

Male

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Although males engage in mate searching behavior more often than females, making pheromone production more important for females, male cabbage loopers also produce pheromones. As with female cabbage loopers, males around host plants are more attractive to females, because plant odor enhances the attractiveness of the male pheromone. This is advantageous to females because it helps with mate choice, as plant odor-enhanced males are more likely to be near a host plant.

  • The male pheromone may also be related to food-finding behavior, as both males and females are more attracted to the male pheromone when starving.[21]

Although there is no direct evidence that supports the notion that males release pheromones in response to host plant odor, there remains a likelihood that such behavior occurs, and that the lack of results from one scientific study is due to either the choice of host plant or the experimental setup. [22] The male pheromones are d-linalool, m-cresol, and p-cresol, and they are produced from hair pencils on the abdomen.[23] Studies suggest that the cresol is particularly important for attractiveness to females, while linalool is found in floral odors and is believed to attract individuals searching for nutrients. [24]

Female

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Cabbage loopers are unique in that both females and males release pheromones in order to seek a mate. Generally, females release pheromones from the tips of their abdomens, and males seek females upon detection. [2][25] Females around host plants are more attractive to males, possibly because females release more pheromones in the presence of host plant odor. Although it is not clear why host plant odor incites female pheromone production, scientists believe that this response may help to reduce time wasted spent searching for a mate and therefore increase the chance of mating. [22] Female cabbage loopers usually attract the male, as females have more to lose by spending energy and time on searching for a mate. That being said, occasionally the reverse occurs, where females will seek males. This, however, only happens under particular selection conditions, such as a shortage of males or host plants. [23]

  • The female pheromones are cis-7-dodecenyl acetate, cis-5-dodecenyl acetate, 11-dodecenyl acetate, cis-7-tetradecenyl acetate, cis-9-tetradecenyl acetate, and dodecyl acetate.[26][27]

Detection

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Cabbage loopers possess olfactory receptor neurons on their antennae for detecting pheromones. The neurons are specifically located on two sensory structures called sensilla that differ in length and pore density. Male loopers have two types of neurons, and depending on which sensilla they are present, the neurons will detect female pheromones at varying sensitivities to each of the six pheromones. The neurons are most sensitive to the main component of the female pheromone blend, cis-7-dodecenyl acetate, and the male inhibitory signal, cis-7-dodecenol. The presence of cis-7-dodecenyl acetate is crucial for male response to female pheromones, as it is 80% of the entire blend. In fact, the proximal region of antennae, where receptor neurons for this pheromone are located, has more sensory structures compared to the distal region. The proximal region is also less likely to experience damage, showing the importance of detecting the pheromone.[28] It is not clear why the inhibitory compound is detected, as it does not seem to be produced by females, but scientists speculate that its presence in the blend may be too small to be undetectable by scientific equipment.[29] The inhibitory signal only elicits a response when delivered alongside female pheromones to avoid mixing signals from other species.[30]

These neurons are also capable of recognizing and responding to cis-7-tetradecenyl acetate and cis-9-tetradecenyl acetate. There are no specialized neurons for the other three pheromones.[28] Instead, these minor pheromones can cross-stimulate neurons, which is why partial blends that lack one or two of the minor pheromones can still fully stimulate the male receptors.[31]

Other mating behaviors

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Copulation

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Cabbage loopers ready to mate were observed elevating their abdomen and fanning their wings. Males also fan out their abdominal hairs, open their genital claspers, and partially stick out their spermatophores. Males gradually expose more of their spermatophores as they wait for a mate. Upon interest, a potential mate examines the other's abdomen with antennae, and mating occurs if both agree.[8] Mating on average occurs at 2am, but has been observed occurring between 12 and 4am.[25] Mating generally occurs 3-4 days after emergence, but can occur up to 16 days afterwards. Mating generally doesn't occur before the third day, as eggs are not fully developed upon emergence and require a few days to reach maturity.[2]

Multiple Matings

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Cabbage loopers engage in multiple matings, a behavior that is beneficial for both males and females. For females, rate of oviposition increases with the number of matings, and ultimately lay more eggs total. While it was once believed that multiple matings were necessary to fertilize all eggs, evidence shows that only one mating is needed to fertilize almost all eggs. Instead, it is more likely that the spermatophore provides nutrients to the female that confers reproductive benefits. This may explain why males produce female-attracting pheromones, as females may be seeking nutrient-rich spermatophores. For males, multiple matings did not affect the quality of their spermatophores, suggesting that they can maximize reproductive opportunities without decreasing fecundity. [32]

Oviposition

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Oviposition can occur upon emerging, but the eggs are not fertile, as they do not mature until the third day of adulthood.[2][8] Eggs are mostly found on the mainstem leaves of plants. As the plant grows, eggs are also found higher.[33] Host plant of choice for oviposition will depend on larval experience, known as learned host behavior. It was shown that moths unfamiliar with a host plant will avoid ovipositing on said plant. Moths grown on a host plant, and therefore familiar, will preferentially oviposit on the host, even if the host produces unappetizing chemicals. This demonstrates that larvae and moths develop host preferences and that the species is slow to determine whether a plant chemical is toxic. [6] This choice is also influenced by larval frass, as its presence serves as a chemical deterrent for potential mothers. Larval frass indicates that the site is already occupied, therefore avoiding overcrowding. [34]

Enemies

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Nucleopolyhedrovirus (NPV)

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From the family Baculoviridae, NPVs are naturally occurring viruses that are commonly used as pesticides for the cabbage looper. There are numerous NPVs, many of which were isolated from the cabbage looper or the alfalfa looper. NPVs vary in infectivity and virulence. For example, the AcMNPV isolates are more infectious than the TnSNPV isolates in the first instar, while the TnSNPV isolates produced more occlusion bodies, protein structures that protect the virus and increase long term infectivity.[35] TnSNPVs are their most lethal during the third and fourth instars have detrimental effects, such as delayed development, reduced egg production, and fewer hatched eggs. These effects are significantly diminished when the larvae are infected during the fifth instar, suggesting that the earlier infection is more effective.[36]

Parasitism

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While the cabbage looper frequently encounters parasites, its most common parasite is the tachinid fly. In one study, 90% of the parasitized larvae were due to the tachinid fly.[37] It parasitizes most often in the late fall and winter, but it is capable of parasitizing year-round. Cabbage loopers at their third or fourth instar yield the most parasites. It is early enough in the larval stage that the maggots still have time to feed and grow before pupation can prevent parasite emergence. It is also late enough that the caterpillars are large enough to support the maggots. Fly oviposition is often triggered by the larva thrashing to repel the fly, regardless of whether the larvae are already parasitized. As a result, larvae are often overparasitized, overwhelming and killing smaller larvae. Oviposition glues the egg to the host and helps the maggot burrow into the larva, where it remains until the third day. The maggot cuts a slit into the back and eats its way out of the larva. [38]

Predators

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General predators like spiders, ants, and lady beetles prey on cabbage looper eggs and larvae, removing 50% of the eggs and 25% of the larvae within three days. Lady beetles consume at the highest rate.[39] Other common predators of cabbage looper larva include Orius tristicolor, Nabis americoferus, and Geocoris pallens.[40]

Damage

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The cabbage looper is infamous for being a pest, and is considered to be one of the most problematic cabbage pests. The larvae eat large holes into the underside of leaves and consume developing cabbage heads. In addition, they leave behind sticky frass, thereby contaminating the plants. It can also consume the leaves of a myriad of host plants beyond cabbages. Although it is a damaging pest, the cabbage looper is actually not as destructive as some may claim. In fact, plant seedlings can tolerate the cabbage looper, but it becomes more problematic once the plant begins heading. [4] This pest's infamous reputation likely stems from its ability to easily infest a variety of crops and growing difficulty managing it, for the cabbage looper is growing resistant to biological insecticides and synthetic insecticides are not condoned. [3][41]

Management

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Sex pheromones

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The extensive research in cabbage looper pheromones and their attractive qualities was for the purpose of developing traps for the moth. Initial research involved isolation of the female pheromone to identify the compounds and potentially synthetically replicate the natural female pheromone. Scientists were successfully able to develop a synthetic version that functions biologically similarly to the natural form. [26] The synthetic female pheromone has been used with black light traps to study cabbage looper populations in various regions of the US.[9] Synthetic male pheromone has also been developed and was found to be effective in attracting and trapping both male and female cabbage loopers. The blend of male pheromones helped to trap females seeking mates and individuals seeking food.[24] Further studies in Arizona showed that pheromone baited black light traps are not effective in managing the cabbage looper. The traps did capture some males, which resulted in less mating and therefore fewer eggs laid. However, the effect was not large enough to cease using insecticides, as farming standards require crops that are basically insect-free.[42]

Insecticides

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Scientists are actively seeking methods for controlling the cabbage looper. Synthetic insecticides are relatively effective; however, many of them are banned for their toxicity.[43] One exception is AmbushTM. Studies have shown that this pyrethroid insecticide is effective at killing cabbage looper eggs, and its usage is permitted in the US.[44] Other studies have explored the usage of biological insecticides; for example, Nucleopolyhedrosis virus was shown to be effective. Unfortunately, managing large quantities of this virus would a hassle, so it is ultimately not a feasible option.[45] An effective option is to use synthetic and biological insecticides together; this method seems to both control the population and slow the development of resistance, but it still requires the usage of toxic chemicals. [46] Currently, spraying Bacillus thuringiensis is considered to be the best option, possibly with NPV for an added benefit.[4][47] Unfortunately, the cabbage looper is growing increasingly more resistant to B. thuringiensis. Recent studies, however, have demonstrated that cabbage loopers resistant to B. thuringiensis are twice as susceptible to NPVs, which provides insight into novel biological control methods.[48]

Baculovirus-insect cell expression

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Baculovirus-insect cell expression involves the engineering of a baculovirus vector to produce a desired protein in an insect cell.[49] Numerous insect cells have been developed into a cell line, such as fruit flies, mosquitoes, and silkworms. The tissue of the cabbage looper has also been used to develop a cell line. It is particularly useful for its fast growth rate and less reliance upon insect haemolymph in the medium.[50] More recently, the cabbage looper cell line has been engineered to grow in serum-free media. Although serum helps insect cell growth, it is very expensive and can hinder subsequent experimental procedures. As a result, the development of the cell line to grow independently of serum means that the cell line could be used to produce viruses and proteins in a more affordable, efficient, and productive manner.[51]

References

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