But a few millimeters in length, tiny, handsome carpet beetles sometimes appear in my home on wintry days.
As we say good riddance to 2020, and welcome in a hopeful 2021, Bug of the Week will spend some time catching up with a few fascinating, fearsome, and funny creatures found in and around our homes. This week we visit tiny recyclers of organic matter called carpet beetles that can sometimes become pests. On a warmish winter day, I occasionally spot a rather lovely small beetle scaling a wall or scooting across a countertop in my home. Carpet beetles get their name from their proclivity to breed in a wide variety of natural substrates containing the protein keratin, which is found in felt, silk, feathers, pet hair, animal hides and carcasses, and, yes, woolen carpets. They become pests when colonizing a drawer, closet, or box where sweaters or other garments are stored. Adult beetles deposit eggs that hatch into hungry, tiny larvae which nibble away fibers, creating holes or sinuous trails in fabrics.
Hairs on dermestid larvae can cause dermatitis to some people.
The larvae are very hairy little beasts, covered with long hairs or setae. Prolonged exposure to these hairs festooning the bodies of carpet beetle larvae has caused dermatitis in some people. Carpet beetles belong to a larger clan of recyclers called dermestids, or hide beetles. Hide beetles provide an important service to museum curators by virtue of their ability to strip skeletons of virtually all muscle and sinew, producing lovely bare bones. However, dermestids create problems for professional and amateur entomologists when they invade collections of pinned and preserved specimens. Larvae bore into dead insects and consume proteinaceous tissue within. As they feed, small pellets of waste products called frass litter the area beneath the infested specimen. This is the classic hallmark of a dermestid attack.
During winter, pretty carpet beetle adults and their very hairy larvae sometimes wander about my desk, table, and walls. In the wild, other dermestids are some of the last visitors to animal carcasses. Larvae like this one can remove skin, muscle, and other connective tissue, leaving behind nothing but bone.
Uh oh, ragged holes in my woolen cap look like the handiwork of carpet beetles.
Thwarting carpet beetle infestations is relatively straightforward. Before storing any garment made of natural fibers be sure it is laundered or dry cleaned and stored in a sealable bin or bag. If these rascals have already established a foothold somewhere in your home, try to ferret out their location. This could be a seldom used woolen rug in the basement, a box of sweaters in the attic, or a blanket, dress, or sport coat in a closet. Carpet beetles can also breed in carcasses of dead insects so maybe a pile of dead stink bugs in the attic is the source of an infestation. Some species of dermestids breed in stored products like grains, pet food, nuts, and spices. We met a caterpillar with similar habits, the Indian meal moth larva, in a recent episode. Once you locate the infestation, discard or destroy the material serving as the source of the infestation. In the case of carpets and rugs, vacuuming and deep cleaning will help. A lightly infested blanket or scarf can be salvaged by either placing the item in a deep freezer that is below 0 degrees Fahrenheit for several days, or by heating it above 130 degrees Fahrenheit for several hours. Temperature extremes can kill eggs, larvae, pupae, and adult carpet beetles. But please don’t set the item on fire or burn your house down.
An untidy pile of frass behind a dead insect specimen is a sure indication of a dermestid beetle infestation.
How does a person who should know better wind up with carpet beetles in a home? The answer lies in the back of a closet where show-and-tell bugs used in STEM outreach are stored. In a tray of preserved scarab beetles, one unfortunate specimen bears an untidy deposit of frass attending its rear-end. Since dead beetles don’t engage in post-mortem voiding of waste, the pile of frass is the tell-tale signature of carpet beetle larvae dining inside the dead scarab. Bad luck for the scarab translates to good luck for sharing a tale of carpet beetles.
Bug of the Week wishes everyone a happy and healthy New Year free of all plagues!
Acknowledgements
Information in this episode originated in great articles written by Whitney Cranshaw at Colorado State University and Michael Potter at the University of Kentucky. Learn more about these creatures at the following websites:
And what to my wondering eyes should appear, but a colony of whiteflies, bringing holiday cheer.
One of the real delights of the holiday season is adding festive plants to the home décor. As we have seen in previous episodes of Bug of the Week, this often means that some six and eight-legged creatures including mantises, adelgids, and spiders sometimes accompany a Christmas tree when it arrives indoors. These plant-related holiday surprises are not limited to Christmas trees, oh no. This week, let’s visit another fascinating but dastardly insect that sometimes makes its presence known on one of my favorite holiday plants, poinsettia. Decorating the home with poinsettias is a holiday tradition that likely originated in Mexico, where poinsettias add beauty to holiday nativity crèches. According to legend, in the town of Cuernavaca a young girl had no flowers to adorn the nativity at her church. Instead, she collected a weed growing by the roadside. An angel transformed the weed into the beautiful poinsettia, and ever since, poinsettias have been used as a seasonal decoration. Poinsettias are as much of a holiday tradition as mistletoe, holly, and an evergreen tree in many homes.
Yellow patches on poinsettia leaves may be a sign of whiteflies feeding below.
As I browse displays of poinsettias that have sprung up in every hardware and grocery store, I’m on the lookout not just for holiday decorations, but for holiday whiteflies. Whiteflies are small sucking insects and relatives of more commonly known sap-suckers such as beech and woolly alder aphids we met in recent previous episodes. To spot a whitefly-infested poinsettia, first look at the color of the plant’s leaves – not the red, yellow, or speckled bracts comprising the blossom. The leaves on most varieties should be a clear deep green with no evidence of yellow patches or streaks. Leaves with yellow patches that are undersized, twisted, puckered, or curled can be the ghost of holiday problems yet to come. Whiteflies are usually found on the underside of leaves where they insert tiny beaks into the plant’s vascular system to extract sugar-rich sap from a vascular element called phloem. Plant sap contains nutrients needed for their growth and development. Large populations of whiteflies can cause leaves to drop prematurely. As whiteflies feed, they excrete a sugary waste product called honeydew. This sticky liquid can become a substrate for the growth of an ugly fungus known as sooty mold.
Whiteflies have four stages in their lives, egg, nymph, pupa, and adult. An adult female whitefly lays eggs on the undersurface of a leaf. After several days, eggs hatch and mobile nymphs, called crawlers, move about the leaf surface until they find a suitable place to feed. Nymphs hunker down, shed their skin, and become stationary for the remainder of their youth. After several molts, a pupa forms, and from this pupa emerges the adult whitefly. Shed pupal skins often festoon the undersides of leaves. Adult whiteflies look like tiny white moths. They too have sucking mouthparts and suck the sap of poinsettias. If disturbed, they flutter from the leaf surface. The nymphs and pupae are usually yellowish or whitish and translucent. Red eyespots can be seen on the pupa shortly before the adult whitefly emerges.
With wings yet to unfold, an adult whitefly emerges from its pupal case. A bit later with wings now fully expanded, polishing up the thorax and antennae is the next order of business to get ready for the holidays.
Droplets of sweet sticky honeydew are produced as a waste product when whiteflies feed.
For the folks that grow poinsettias, whiteflies can be a very serious problem. If populations become too great, entire crops are lost. The most common whiteflies that come home with poinsettias are the greenhouse whitefly, Trialeurodes vaporariorum, and the silverleaf whitefly depicted in this Bug of the Week. A strain of silverleaf whitefly, the dastardly “Q biotype”, has been found in several states in the US. This strain is resistant to many of the pesticides formerly used to control whiteflies and causes headaches not only for the greenhouse industry but also for growers of some of our most important agricultural crops including tomato, peppers, squash, cucumber, beans, eggplant, watermelon, cabbage, potato, peanut, soybean, and cotton. Fortunately, entomologists are finding new ways to control whiteflies using tiny wasps that attack them, predatory beetles that eat them, and pathogens that give them lethal infections.
If this Bug of the Week sounds a bit like the Nightmare before Christmas, try not to panic. Don’t let a few whiteflies on your poinsettia spoil the holiday. A few whiteflies will not ransack your poinsettia between now and the New Year and, hey, many poinsettias will join other decomposing vegetation in the compost well before Valentine’s Day. However, if whiteflies are numerous and your poinsettia looks whipped, and you had planned to keep your poinsettia going with the other house plants, it may be best to toss it out and replace it with one not bearing tiny six-legged gifts. Many fine, pest-free poinsettias can still be had in retail markets large and small. So, Happy Holidays to poinsettias, whiteflies and all!
Despite some chilly weather, peach-clematis aphids keep on keeping on the leaves of my sweet autumn clematis.
With winter fast upon us and most deciduous trees and shrubs already naked, my sweet autumn clematis, Clematis terniflora, still shines like a beacon of green as it engulfs a lamppost in the front yard. After rewarding me with fragrant blossoms for much of the fall, this non-native invader is hosting an entire food web of alien insects. Let’s start with the herbivores, a flock of peach-clematis aphids. During spring and summer, through Thanksgiving, and, in this era of climate change perhaps all winter, my clematis will be home to peach-clematis aphids. Several species of clematis and peaches serve as food for this now cosmopolitan vagabond. Beneath each leaf, scores to hundreds of aphids suck nutritious phloem sap. Over the past several months and in years past, the aphid horde is so abundant that clematis leaves drip with honeydew, which in turn serves as a substrate for the growth of sooty mold. This type of non-pathogenic fungus, akin to one produced by boogie woogie aphids and woolly alder aphids we met in previous episodes, blackens leaves and may interfere with photosynthesis.
The saga of the peach-clematis aphids began earlier this year in the spring when winged aphids migrated from a tree in the peach clan (Prunus) to the clematis vine clinging to my lamppost. During the warm months of summer and fall, surviving females begin reproducing without assistance of males. This form of reproduction, called parthenogenesis, produces only females, thus enabling aphid populations to increase rapidly. As I examined my colony of aphids recently, I noticed several winged adults mixed with the parthenogenetic females. In cold regions like Maryland, when temperatures turn chilly, male and female winged adults are produced and leave the clematis, returning to Prunus to mate and lay eggs that will spend the winter on the bark of the tree. Sexual reproduction in the fall produces eggs, the overwintering stage of the aphids. In spring, the eggs hatch and the complex life cycle of the aphid resumes.
Another fact of life contributing to explosive population growth of aphids is their ability to skip the usual insect-like business of laying eggs. Many species of aphids dispense with the egg stage and, like humans, give live birth to their babes. This blessed event takes only a few minutes but appears to be fraught with significant drama. Birthing aphids do lots of posturing and pushing. Fortunately, aphids have sucking mouthparts and loud vocalizations such as those accompanying human births are conspicuously absent. To further accelerate the process of filling the world with their kind, female aphids carry embryos of their grandchildren within their bodies even before they are born (i.e. their daughters are born already pregnant). This further compresses the generation time for aphids and is part of the reason aphid populations rapidly grow from a few to thousands.
With Thanksgiving in the rear view mirror and the rest of Holiday Season just around the corner, peach-clematis aphids are still living it up on sweet autumn clematis. On a leaf blade a mother is surrounded by her daughters, and on a petiole aphids suck sap from phloem. Just for fun, watch the live birth of an aphid (five times actual speed). Note that aphid births are breech. At the end of the clip, is that older sister coming to see how mom and little sister are doing? Dance of the Sugar Plum Fairy by Kevin MacLeod is licensed under a Creative Commons Attribution 4.0 license, https://incompetech.com/music/royalty-free/index.html?isrc=USUAN1100270. Artist: http://incompetech.com/
Just as my clematis serves as a feast for aphids, so too will the aphids and their honeydew serve as dinner for guests higher up the food chain. Roaming around my clematis, multicolored Asian lady beetle larvae snack on aphids. Their alligator-like larvae patrol leaves and stems searching for tasty aphids. Without much stealth or finesse, larvae capture aphids in their jaws and proceeded to munch their hapless prey. Small aphids disappear in just a minute or two, but large, plump aphids required several minutes to eat. A single larva of the multicolored Asian lady beetle may devour 1,200 aphids during the course of development. Adults of this species can also kill hundreds of aphids during their lifetime. This capacity to eat so many aphids makes the multicolored Asian lady beetle one of the most effective biological control agents in our gardens.
In this microcosmic food web, clematis is food for the peach-clematis aphid, and aphids will become food for both adult and larval lady beetles. A yellowjacket laps up carbohydrate rich honeydew produced by the aphids. This rich source of carbohydrates may help yellowjackets fatten up to survive a wicked winter. Dance of the Sugar Plum Fairy by Kevin MacLeod is licensed under a Creative Commons Attribution 4.0 license: https://creativecommons.org/licenses/by/4.0/, Source: http://incompetech.com/music/royalty-free/index.html?isrc=USUAN1100270, Artist: http://incompetech.com/
And during this season of Holiday feasts, what banquet would be complete without dessert? With gobs of sweet honeydew on leaves, dozens of hungry yellowjackets recently visited the clematis to lap up a carbohydrate rich meal to fatten up for their winter rest. So, in this festive season, while we devour turkey and savor pumpkin pie, reflect on the happy feasts underway on greenery like an autumn clematis where aphids dine and serve dinner to other creatures higher up the food web.
Acknowledgements
Bug of the Week thanks Roger Blackman and his amazing website, Aphids on the World’s Plants: An online identification and information guide at http://www.aphidsonworldsplants.info/ which served as a reference for this episode. The fact-filled leaflet “Multicolored Asian Lady Beetle” by Janet Knodel, E. Richard Hoebeke, and Carolyn Klass, Dept. of Entomology, Cornell University provided great information on the ladybeetle. Many thanks to Dr. Gary Miller of USDA’s Systematic Entomology Laboratory for his help in identifying the tiny star of this episode.
No ho ho ho for this boxwood leaf loaded with larvae of boxwood leafminer.
Glossy, dark green leaves of a healthy boxwood are conspicuously absent when infestations of boxwood leafminer give boxwoods a bad case of the blues.
One of the most interesting and charming woody plants in our landscapes is the boxwood. This evergreen shrub has been domesticated by gardeners since the time of the Roman Empire. Pliny wrote about the uses of boxwoods as a garden hedge and as a source of wood for the construction of musical instruments. Boxwoods are featured in the Holiday season in North America and Europe where their glossy, deep green leaves grace wreaths, centerpieces, and garlands in homes. This week on a trip to my favorite market, I passed a boxwood hedge that looked anything but charming. The usually deep green leaves of the boxwood were mottled yellow and orange and disfigured with bumps and blisters. The plants appeared to have a bad case of pox. What misfortune had befallen these noble shrubs? After plucking a few leaves from the embattled boxwoods, and carefully removing the lower surface of a leaf, I discovered several tiny, squirming, yellow maggots just beneath the surface. These were the larvae of the diabolical boxwood leafminer.
The boxwood’s blues began last spring in early May when adult boxwood leafminers emerged from leaves, exiting their leafy nursery. On the way out, the adult flies left behind the shed skin of their former pupal case. The papery skins, called exuviae, protrude from the bottom surface of the leaf for many days before dropping from the plant. Adult boxwood leafminers are delicate orange flies closely resembling mosquitoes. After mating, the female fly seeks the undersurface of a young boxwood leaf. Using a small drill-like structure at the tip of her abdomen, she punches a tiny hole in the surface and lays eggs in the soft tissue beneath. From these eggs tiny yellow boxwood leafminer larvae hatch. During summer and autumn, as the larvae grow, boxwood leaves produce small circles of cells surrounding developing larvae. These cells serve as a source of food for the maggots and produce abnormal swellings of the leaf, called galls. Development slows during the chilly months of winter and early spring, but by April, with the return of warmer temperatures, larvae grow rapidly as the boxwood ramps-up its activity. To escape the protected confines of its mine, the leafminer has a clever trick. Just before pupating, the maggot moves to the lower surface of the leaf and carefully removes almost all of the leaf tissue until only a thin layer is left. This layer forms a window that will be used by the pupa as an escape hatch. With a successful exit strategy in place, the larva pupates and in a few short weeks the pupa pushes through the window, enabling the adult fly to escape.
Peeling back the lower epidermis of a boxwood leaf reveals boxwood leafminer maggots nestled within, ready for a long winter’s nap. Fast forward to next spring, when larvae have completed development and pupated. As they emerge from leaves, shed pupal cases mark the exit sites of adult midges. With jazzy twisting motions, the rockin’ female drills into a tender new leaf to deposit eggs.
Managing leafminers
If you are troubled by boxwood leafminers, then a good, non-insecticidal way to thwart this uninvited guest is to plant varieties of boxwoods resistant to attack by this fiend. Years ago, we discovered that a variety of boxwood from the highlands of Macedonia was highly resistant to the boxwood leafminer. This variety is called Buxus sempervirens ‘Vardar Valley’. You can find it in several nurseries in the DMV. Here’s hoping your boxwoods don’t suffer holiday blues courtesy of the boxwood leafminer.
References
A wealth of information on boxwoods can be found in Lynn Batdorf’s wonderful “Boxwood Handbook”, used as a reference for this story. Information on resistant boxwood varieties came from the article entitled “Integrated approaches for managing the boxwood leafminer, Monarthropalpus flavus” by M.J. Raupp, I.H. Mars, and G. d’Eustachio, the abstract of which can be found at this link: https://www.actahort.org/members/showpdf?booknrarnr=630_6
Sparkling scales of brown, black, and silver give the Indian meal moth a rather comely appearance.
Holiday season is baking season. Pies, cookies, cakes, and breads are comfort foods many crave on chilly days. During this season of culinary delight, cupboards and pantries receive lots of attention and activity. On a recent socially-distanced visit to a friend’s home, we noticed tiny moths flitting about the kitchen. A peek inside the pantry revealed more than a minor swarm of said moths. During this holiday season, many hopeful bakers will open pantries and be greeted by clouds of these small wonders, a cosmopolitan raider of the pantry, the Indian meal moth, Plodia interpunctella. While fascinating for entomologists, this is an unwelcome surprise for most folks.
Silk inside plastic bags or containers is a pretty sure sign of a meal moth infestation.
The adult stage of this insect is a rather small moth just slightly larger than ½ inch in length, with wings banded white and rusty red. They flit about the pantry or cupboard in search of mates and tasty products rich in carbohydrates, fats, and proteins. One recent infestation in my cupboard raged in a package of organic cashews. Within the package, small cream colored caterpillars spun silken webs and sallied forth to consume the nutritious nuts. In addition to spinning silken galleries, larvae deposited frass, the digested remains of their meal. The voided frass was entangled in silken strands to form a nasty messy web. Two excellent clues signaling the presence of meal moths are the presence of silk and frass within a bag of flour, grain, seeds, or pet food. After larvae complete development, they may gnaw holes and escape their plastic prisons. Nomadic caterpillars are often found wandering about the walls and ceiling of the pantry in search of a protected spot to spin cocoons and develop into pupae. Sometimes vagabond larvae enter cracks between shelves, lids of jars, electrical sockets, or seams behind baseboards to pupate. Soon the next generation of adults will appear, intent on finding new bags and boxes of stored products to infest.
Within a plastic bag, scads of meal moth caterpillars spin silken webs and deposit frass while devouring my once tasty organically grown cashews. While caterpillars are a rich source of protein, this much extra protein with my nuts I don’t need.
How do meal moths colonize pantries in the first place? It is possible that original infestations of meal moths arrive with cereal, seeds, dried fruit, or grain as a few tiny eggs within a package from the store. After hatching from eggs, small caterpillars in a bag of seeds in the back of a closet could go unnoticed, but this vanguard is capable of generating sufficient moths to initiate a full blown mothagedon. Meal moths also survive outdoors and are commonly found in caches of nuts or seeds stored by squirrels or rodents. Adult moths originating outdoors can invade indoor pantries during warm weather when doors and windows are wide open. Mice often enter homes in autumn and winter seeking shelter and bringing stockpiles of seeds with them. These seeds might arrive contaminated with the associated moth eggs and may become a source of infestations indoors.
Indian meal moth caterpillars can chew through plastic and invade other bags of grain, seeds, and fruit.
What should you do if you find these rascals in a pantry or cupboard? First, remove all goods and products from the storage area. Vacuum the cupboard, pantry, or cabinet like there is no tomorrow. Carefully inspect all cracks, corners, crevices, and seams in the cupboard and remove any larvae or pupae you find. Seal as many of these refuges as possible with caulk. Remove and replace loose paper used to line shelves. Inspect any pots, pans, glasses or other items occupying the pantry where food will be stored and remove any meal moths on these items as well. Inspect opened and unopened bags and boxes of food for signs of silk, frass, larvae, or moths. If in doubt, toss it out. My pantry pest guru recommends the “deep chill” treatment for unopened packages you might want to salvage, but are suspect by association. Place unopened bags in the freezer for one week, remove them for one week, and then freeze again for a final week. The intermittent week of thaw tricks eggs into hatching and the tiny caterpillars are then killed by the second trip to subzero land. When you purchase items that might serve as food for meal moths, seal them in strong plastic storage containers with tightly fitting lids. This will help prevent any moths you might have missed during the crusade from laying eggs that hatch into larvae capable of infesting your food. Try not to store prime foods like grain or dried fruit for very long periods of time. The longer stored products remain on a shelf, the more likely they are to be infested by an itinerant moth that happens by.
Pheromone traps can be used to capture male meal moths and gage their activity and numbers.
One approach useful in alerting you to an incipient invasion of meal moths is to purchase and deploy pheromone traps. These small triangular boxes are placed inside your pantry or cupboard. Inside the box is a sex pheromone bait that attracts the male meal moth from many feet away. The ever-hopeful male senses the pheromone, a chemical signal released by a female, and is tricked into believing that a receptive beauty waits inside the open-ended trap. He flies inside to find his mate, but instead becomes ensnared by a sticky substance lining the inside of the trap. By placing these traps within a pantry, you can detect the emergence of male moths that may be the harbingers of a burgeoning population of moths in your cupboard. This advanced warning serves as a signal to initiate a search and destroy mission. Good luck hunting moths and protecting your baking supplies during this season of culinary delight.
Acknowledgements
We thank Linda and Jeff for sharing their relentless Indian meal moths with Bug of the Week and Dr. Nancy Breisch for the wealth of information and advice about bugs. The Handbook of Pest Control, Ninth Edition, by Arnold Mallis was used as a resource.
Fruit flies like this African fig fly may join Thanksgiving festivities in your home. Photo credit: Maggie Lewis
Just before Thanksgiving kicks off the holiday season, scads of questions show up in my mailbox about hordes of tiny flies buzzing around fruit bowls, kitchen sinks, and counters tops. They seem to appear from nowhere and lend credence to Aristotle’s notion of spontaneous generation, the theory that living organisms like flies somehow originate spontaneously from non-living or putrefying things. To help untangle this mystery, consider the change of seasons. Late autumn in the DMV and many other parts of our land is characterized by cool damp weather. Moist evenings and mornings punctuated by warmish days are nearly ideal for decomposing tons of leaves, fruits, and other vegetable matter, the accumulated bounty of Mother Nature’s efforts during spring and summer. This week of Thanksgiving, my compost pile is a writhing mass of invertebrates intent on converting vegetable protein into animal biomass as quickly as possible. On warm days, a cloud of fruit flies hovers over my compost and some of these winged raiders undoubtedly infiltrate my home when doors open.
Like many kitchens, mine is home to a bowl of fruit that occasionally contains one item gone a little squidgy. Yeasty odors of acetic acid and ethanol emanating from an over-ripe banana serve as powerful attractants for fruit flies. After arriving at a slightly brown banana, the female fruit fly deposits eggs. Each gal lays roughly 500 eggs during the course of her life time. Small translucent larvae hatch from the eggs. They glide through the overripe fruit slurping-up nutritious fermenting fluids as they develop and grow. With warm ambient temperatures, fruit flies can complete a generation in less than two weeks. With their capacity for reproduction, populations around the fruit bowl can explode seemingly overnight. One careless week, I neglected to empty the stainless steel compost bin on my kitchen counter and I was rewarded with several hundred fruit fly maggots happily growing in the bin. Yikes!
Dozens of fruit flies could not escape the irresistible odors of vinegar. Once inside the jar, a perforated plastic cover prevented escape and sealed their fate. Photo credit: Ingalisa Schrobsdorff
Fruit flies can also enter home as stowaways with overripe fruits or vegetables from the market or garden. These goods may arrive preloaded with a complement of eggs or tiny larvae. To reduce chances of bringing home an infestation, inspect your produce carefully and wash fruits or vegetables before you set them out in a bowl. If fruit is unrefrigerated and displayed in a bowl, check it out regularly and toss over-the-hill items before they generate flies. Fruit flies often breed in sink or floor drains, garbage pails, or recycling containers in homes, restaurants, and offices where decomposing organic material accumulates. Inspect these areas regularly, clean up spills, and disinfect surfaces. For the cloud of fruit flies wafting around your home, consider building a vinegar trap to catch and kill these noisome rascals. Traps can be purchased commercially and several trap designs are available on the internet. My do-it-yourself vinegar trap consists of an 8 oz. clear plastic tumbler filled with 4 oz. of apple cider vinegar or wine vinegar and a few drops of dish detergent. Within 24 hours of placing the trap on the counter, more than 100 fruit flies were lured to their death. One clever modification of the trap includes fastening a bit of plastic wrap over the lid of the vessel with rubber bands a poking a few holes in the plastic. Apparently, this allows fruit flies to enter but confounds attempts to escape should they change their tiny minds about a vinegary death by drowning.
More than just an indoor nuisance, several invasive species of fruit flies have now established in our region. The spotted-wing drosophila, Drosophila suzukii, first detected in the US in 2008 in California, has now spread from coast to coast and border to border. It is a major pest of strawberries, blueberries, raspberries, black berries, and cherries, and crop losses in the United Sates alone are estimated to exceed hundreds of millions of dollars annually. If spotted-wing drosophila was not enough, a second dastardly fruit fly, the African fig fly, Zaprionus indianus, first detected in Florida in 2005, has now spread to the Canadian border and can also be found here in the DMV. African fig flies infest a broad range of plants, including berry crops as well as figs, grapes, and cherries. Unlike spotted-wing drosophila, female African fig flies generally cannot cut through intact fruit skin to lay eggs; they instead are thought to oviposit (deposit eggs) into or near pre-existing cracks and wounds. In some varieties of grapes, the African fig fly may actually out-compete its Asian relative, the spotted-wing drosophila.
African fig fly is an invasive fruit fly species that was first detected in the United States in 2005 and has since established in Maryland. Adults can be identified by the white and black stripes running longitudinally down their back. While spotting an adult is easy, spotting a larva swimming in a raspberry is a bit harder and somewhat disconcerting if the raspberry is in your cereal. Video credit: Maggie Lewis
African fig fly eggs are strange things with several long filaments at one end. These filaments help the egg obtain oxygen. Photo credit: Maggie Lewis
Ah, but fruit flies are not all bad. The most famous fruit fly of all is, of course, Drosophila melanogaster. This tiny workhorse of scientific studies, a hero many of us met for the first time in high school biology, brought the 1933 Nobel Prize in Physiology or Medicine to Thomas Hunt Morgan for his pioneering work on mechanisms of heredity and the location of genes on chromosomes. Fruit flies have ventured to the International Space Station to help scientists study the effects of zero gravity on cardiac function and immune responses to disease. Closer to home and in my compost bin, they provide a vital ecological service by unlocking nutrients tied up in vegetable waste and returning these nutrients to food webs. So for good or bad, hail the tiny but mighty fruit fly.
On this unprecedented Thanksgiving in the time of COVID-19, Bug of the Week wishes you a happy one. Be sure to share some of your unwanted vegetables with ever-grateful fruit flies in your compost!
References
The wonderful video, images, and ideas for this week’s episode were created by doctoral candidate Maggie Lewis of the Department of Entomology, University of Maryland, College Park. We thank Ingalisa and Sahar Schrobsdorff for providing inspiration for this story and sharing an image of their clever fruit fly trap. The interesting references “Trapping spotted wing drosophila, Drosophila suzukii (Matsumura) (Diptera: Drosophilidae), with combinations of vinegar and wine, and acetic acid and ethanol” by P. J. Landolt, T. Adams, and H. Rogg, “Spotted Wing Drosophila: Potential Economic Impact of a Newly Established Pest” by M. Bolda, R. Goodhue, and F. Zalom, “Effects of Interspecific Larval Competition on Developmental Parameters in Nutrient Sources Between Drosophila suzukii (Diptera: Drosophilidae) and Zaprionus indianus” by M. Edana Shrader, H. J. Burrack, and D. G. Pfeiffer, and “Flies, gnats, and midges” by W. A. Kolbe in “The Handbook of Pest Control” were used in preparing this Bug of the Week. To learn more about the African fig fly, please visit the following website: https://academic.oup.com/jipm/article/10/1/20/5514212#136729274
Twisted gnarly leaves on my pretty Nyssa are the handiwork of a tiny gall-making insect.
The range of color in Nyssa’s autumn display is hard to beat.
Some call it tupelo, others call it black or sour gum, but I call it drop-dead gorgeous, Nyssa sylvatica. Of all the trees in the forest, I think this one takes home first prize in autumn with shades of scarlet, orange, yellow, and green swirled together in a raucous mix. A common native of eastern North American forests, this beauty is almost pest free and thrives in managed landscapes.
One summer’s day while enjoying my Nyssa’s deep glossy leaves, I was miffed by several gnarly leaves at the tips of branches. Along the margins of said leaves were numerous yellowish-white crescent shaped galls. Galls are abnormal plant growths often associated with an insect, mite, nematode, or microbial pathogen. To get a closer look at this aberration, I plucked a few leaves and dissected the galls under the lens of a powerful microscope. The galls were hollow pockets packed with hordes of tiny yellow sucking insects known as phylloxerids, close kin to woolly aphids we met on beech trees and alder branches. These suckers are tiny, about a millimeter in length. Within each gall several of these gals were surrounded by dozens of pill-shaped translucent eggs, offspring produced asexually, without contributions from males.
Early in the growing season, phylloxerids induce small crescent-shaped galls along the margins of leaves.
How do they make galls? Well, galls form when an invading biotic agent, in this case a tiny insect, takes control of the genetic machinery of the undifferentiated cells in the developing leaf. Compounds released by the insect as it feeds tell the cells of the leaf something like this, “don’t expand to form a normal flat leaf, curl over along the margin and form a nice hollow pocket, a home where I can lay eggs and my children and I can dine unseen and unmolested by hungry predators.” How clever is that! Pretty clever indeed, but one small problem exists. During autumn when my Nyssa drops its gnarly leaves, surely these leaf-bound gall-dwellers do not fare well in the soil. Where do the tiny phylloxerids go?
Early in the season, marginal galls created the phylloxerid twist and distort young leaves at the tips of Nyssa’s branches. Within each gall are female phylloxerids laying dozens of pill-shaped eggs. Phylloxerids are strange looking creatures. Between the first set of legs in the center of the body are sucking mouthparts used to initiate gall formation and to remove sap from the leaf’s cells.
Up in the treetop, flocculant tufts of wax mark the location of tiny insects. Are these overwintering phylloxerids that will lay claim to my Nyssa next spring?
In a remarkable treatise on all things phylloxerid published some 116 years ago, Theo Pergande of Cornell University described the overwintering stages of the phylloxerid. He observed tiny wax covered phylloxerids in protected locations on the bark of the Nyssa. This week I scaled my Nyssa and several meters up in craggy folds along the trunk and in rough patches of bark were small white tufts of wax housing tiny sucking insects, presumably the overwintering generation of phylloxerids. While the exact molecular mechanisms by which gall-makers control their plant-hosts remain largely unknown, hundreds of species of insects and mites have discovered astonishing ways to alter the plants they live on and in during millions of years of intimate association.
Acknowledgements
We thank Drs. Fredericka Hamilton and Gary Miller of USDA for help in identifying the tiny creature featured in this episode. “North American Phylloxerinae Affecting Hicoria (Carya) and Other Trees” by Theo Pergande, and the amazing ‘Aphids on Worlds Plants’ website were used as references for this episode.
Adult euonymus leaf-notcher moths fly in autumn and mimic wasps. This one was found less than 10 miles from the Pennsylvania boarder in Hampstead, Maryland. Photo credit: Charles Krause
Followers of Bug of the Week have witnessed the tale of spotted lanternfly unfold from its first discovery in Berks County, PA in 2014 to its spread across states lines, including Maryland’s border in 2018. With a recent sighting of euonymus leaf-notcher adults in Hampstead, MD less than 10 miles from the PA border, it looks like some of Maryland’s troubles may be heading Pennsylvania’s way. Let’s review how we got here. Back in 2002 a new pest was discovered in Fairfax, VA when a homeowner noticed a voracious caterpillar munching her ornamental euonymus. The caterpillars were sent to Eric Day at the Insect Identification Laboratory in Blacksburg, VA. Eric reared the larvae and sent the unknown moths to specialist John Brown at the Systematic Entomology Laboratory, USDA. Dr. Brown identified the moth as one not known to occur in the US – a new, exotic, invader. The scientific name of this alien is Pryeria sinica. Prior to its discovery in Fairfax, this pest was only known from eastern Russia and China through Korea, Japan, and Taiwan.
Hordes of caterpillars strip leaves and create frass fouled foliage (repeat three times fast).
In 2003 more moths were collected in Northern Virginia and on May 28, 2003 Gaye Williams at the Maryland Department of Agriculture identified specimens of Pryeria sinica from Anne Arundel County, Maryland. Somewhere along the way the new pest was dubbed the euonymus leaf-notcher due to the distinctive pattern of feeding caused by the caterpillar. As the large caterpillars eat, sections of leaf along the margin disappear down their gullets, hence the name leaf-notcher. The leaf-notcher passes winter as taupe colored eggs deposited in clusters of 150 or more on pencil-sized twigs near terminals of branches. Eggs hatch in mid-March and early April, and tiny caterpillars first feed in tight silken webs spun around unfolded leaves at terminals. As larvae grow, they move to expanded leaves to feed and are often found in large groups. Their presence is easily recognized by marginal notches and coarsely shredded leaves on the ground below. When abundant, these caterpillars can entirely strip shrubs.
After completing development in early summer, larvae wander from the plants seeking protected locations to pupate. Large numbers of wandering caterpillars may alarm homeowners, but citizens should remain calm as caterpillars are not known to eat humans or pets. Caterpillars spin pupal cocoons amidst fallen leaves and adult moths appear in the autumn to fly, mate, and lay eggs on the terminals of euonymus branches. Unlike many moths, these are day fliers. They have unique patterns and colors on their body and wings that make them closely resemble wasps. The fact that they mimic wasps may help them avoid being eaten by day feeding predators such as birds. In North America, the leaf-notcher has been reported on Euonymus japonicus and E. kiautschovicus ‘Manhattan’. In its native range in Asia, the pest has been reported feeding on E. sieboldianus,E. japonicus, and E. alatus. Moreover, other members of the Celastraceae such as Celastrus punctatus and C. orbiculatus are recorded as hosts for this pest.
In early spring, euonymus leaf-notchers hatched from eggs and scores of caterpillars began to strip leaves of euonymus. After completing development in spring, caterpillars spun silken cocoons in protected locations. In late October and November, adult moths emerged from very cute pupae, mated, and deposited overwintering eggs on twigs of euonymus.
The pest has two obvious weak points that provide excellent opportunities for management. From the time that egg laying ends in December until eggs hatch in spring, eggs can be crushed on the plant or simply removed by pruning off the terminal and disposing of it. If larvae are small or in restricted areas on a plant, then they too may be removed by a gloved hand or pruner. If larvae are widely distributed, abundant, or otherwise difficult to control manually, then several insecticides should perform well. Some of the most “environmentally friendly” insecticides for killing caterpillars contain Bacillus thuringiensis kurstaki (Btk) or the active ingredient called spinosad. Btk destroys cells in the gut of the caterpillar, a slow and painful death to be sure. Spinosad acts on the nervous system of the caterpillar, inducing a more rapid, twitchy form of death.
In 2009, surveys conducted by the Maryland Department of Agriculture discovered euonymus leaf-notcher in Anne Arundel and Prince Georges Counties in Maryland. Image credit: Maryland Department of Agriculture
Euonymus leaf notcher, where are you now? While no formal records are being kept at the present time by most state agencies, if you think you have spotted this pest you are always welcome to send an image to Bug of the Week care of Mike Raupp at [email protected]. Of course, you can also contact your state Department of Agriculture or University Extension Service and give them a heads-up. Happy leaf-notcher hunting!
Acknowledgements
Many thanks to Charles Krause for sharing his wonderful images of euonymus leaf-notcher and providing the inspiration for this episode. Thanks also to Gaye Williams of the Maryland Department of Agriculture for confirming the identity of the adult moth.
Marbled orb weavers can be found in residential landscapes, fields, and forests from spring until late autumn in Maryland. Despite its scary appearance this orb-weaver poses little threat to humans greater than 2 inches tall. Photo credit: Frederic Zeldow
A few weeks ago, we visited a rockin’ orb weaving spider, the black and yellow garden spider, and watched it dispatch a dastardly brown marmorated stink bug. This week we meet another amazing orb weaver, the beautiful marbled orb-weaver. Usually in mid-autumn Bug of the Week begins to receive images of these fantastic predators and this year was no exception. I had the good fortune to bump into one of these beauties while wandering a trail along the Patuxent River in Columbia, MD. One look at the ornate coloration and patterns on the abdomen of this spider leave no doubt about how this beguiling spider got its name. The marbled orb-weaver is found throughout the contiguous lower 48 states and as far north as Alaska. It is also a common denizen of forests and fields in Europe.
Markings of this immature marbled orb-weaver are stunning.
Like other members of its clan, the marbled orb-weaver spins a web of radial threads like the spokes of a wheel upon which spiral sticky capture-threads are placed. Capture-threads are remarkable evolutionary products of millions of years of bioengineering. Each capture-thread has a core of silk bearing scores of tiny droplets of viscous glycoproteins. These glycoproteins give the web its stickiness. Hapless insects that blunder into the web are trapped by the sticky silk until the spider zooms to its future meal, where it delivers a lethal paralyzing bite. The marbled orb-weaver has a clever strategy to capture prey while limiting exposure to its own enemies. After constructing its amazing web of death, the marbled orb-weaver hides in a retreat near the web. The retreat might be a cluster of dead leaves or a piece of loose bark. A strand of silk called a signal thread runs from the web to the retreat. When a potential victim is snared by the web, vibrations travel along the thread and alert the orb-weaver to the presence of its prey. The message is simple and clear – dinner is about to be served.
Hiding in a folded leaf near its intricate web, a marbled orb-weaver awaits a victim. In a flash that even slow motion fails to capture, the orb-weaver descends to the center of the web to find its prey. Good fortune befalls a small wasp that strikes the web as it somehow manages to escape. Just to share what the orb-weaver might have done, I included a short clip to show how its cousin, the spotted orb-weaver, wraps up its prey.
Acknowledgements
“The National Audubon Field Guide to North American Insects and Spiders”, by Lorus and Margery Milne, and “Estimating the Stickiness of Individual Adhesive Capture Threads in Spider Orb Webs”, by Brent D. Opell, were used as references for this episode. Bug of the Week gives special thanks to Frederic Zeldow for the nice picture of a marbled orb-weaver and inspiration for this episode.
Next spring Massospora fungi will zombiefy periodical cicadas, taking control of their minds and behaviors while turning their abdomens into buff-colored fungus gardens.
For a variety of reasons, Halloween is one of Bug of the Week’s favorite holidays. In years past we have visited many bugs dressed in orange and black including monarch and Gulf fritillary butterflies, milkweed bugs, assassin bugs, and milkweed tiger moths not to mention several scary spiders like black widows, recluse spiders, and tarantulas. But what could be more fun and in sync in the year of the pandemic than a visit with some zombie insects? These are not the kind of Haitian voodoo zombies where a corpse is reanimated by a bokor to conduct some dastardly deeds. Nor are these the ilk of George Romero’s zombies intent on consuming flesh of other insects, as in the Night of the Living Dead Insect. Nah, insect zombies are more akin to zombie apocalypse creatures, hapless victims of a mind-altering pathogen directing deadly actions to further the spread of its own kind. In a delightfully ghoulish paper, D. Donald Steinkraus and colleagues define zombie insects as “… insects infected with an entomopathogen or parasite that alters their behaviors and morphology in ways that benefit the pathogen or parasite.” Boom, insect zombie apocalypse!
Crickets committing suicide
Crickets become “suicidal” after being infected by horsehair nematode worms. Click here to see images of horsehair worms.
One amazing case of an insect zombie involves a European cricket called Nemobius and a horsehair worm called Paragordius. To breed, the horsehair worm must encounter its mate in water. However, the nematode’s eggs are laid near riverbanks where they are often ingested by hosts in which they will develop, arthropods including Nemobius. Inside the cricket, the parasitic nematode grows to its full extent which may be more than 5 inches. To complete its life cycle, the parasite must return to water and here is where the zombification part of the story happens. By a mechanism not yet fully understood, the nematode takes control of the cricket’s mind and alters its behavior, forcing the cricket to wander from its usual dank habitat into open, brighter areas until It encounters a body of water. The water body could be natural such as a stream or pond or human-made such as a swimming pool. The latter is where scientists documented a second bizarre behavior. Upon encountering the swimming pool, infected crickets took a “suicidal” leap into the water. By making the cricket take a plunge, the nematode can escape from its cricket host and seek a water-bound mate to complete its life cycle.
Ants take a drive from treetops and lock-jaws on leaves
Ready to release their spores, parasol-like fruiting bodies of Ophiocordyceps rise from the corpse of their zombie ant host. Photo courtesy of David P. Hughes
Several species of fungi also play mind games with their insect hosts. Zombie ants often make splashes in the news. These unfortunate creatures were first described by famed naturalist Alfred Wallace more than a century and a half ago. Zombie ants are found in tropical forests on many continents and in temperate forests in South Carolina and Florida. Zombie ants are members of the genus Camponotus, commonly known as carpenter ants. The carpenter ant destined to be a zombie is arboreal, spending most of its time high in the canopy of a tree. Occasionally, to get from one tree to the next, it must descend to the earth where spores of the fungus Ophiocordyceps lie in wait. Upon contacting the surface of the ant, these spores awaken and bore into their host. As the ant ascends back into the treetop the fungus, which has now reached the brain, causes the ant to spasm and tumble to the ground. Like the slow moving, foot dragging ghouls in Romero’s films, the fungus causes the zombie ant to seek a microhabitat with just the right conditions of temperature and humidity for the fungus to survive. Once the location is found, zombie ants ascend a plant and use their powerful jaws to lock onto the midvein of a leaf in a “death grip.” Some 4 – 10 days later a fungal fruiting body erupts from the body of the dead ant and releases infective spores into the environment to await the next victim. Widespread infections by Ophiocordyceps sometimes produce massive graveyards of zombie ants.
A soldier beetle’s last salute
Other species of fungi gain mind control over other insects including flies, beetles, and cicadas. Soldier beetles, a.k.a. leatherwings, are cousins of fireflies. Like other members of this clan, soldier beetles are natural born killers in both adult and juvenile stages and are highly beneficial insects to have around the garden. But it is not all fun and games for soldier beetles in the garden during cool moist seasons. A fungal pathogen called Eryniopsis lampyridarum lurks in the landscape waiting to infect soldier beetles. Once the beetle unwittingly picks up a spore from the landscape, the spore germinates and penetrates the exoskeleton of the hapless beetle. Inside the beetle it multiples and takes control of the beetle’s nervous and muscular system, turning it into a zombie. The fungus causes the soldier beetle to march to the upper leaves of a plant in a behavior called summiting. There the beetle clamps onto a leaf with its jaws and dies. Spore producing structures within the cadaver cause the beetle’s abdomen to swell and in a grisly final act, the wings of the beetles open to expose the swollen abdomen, a final postmortem salute. This allows fruiting bodies to erupt from the upper surface of the beetle and spew their spores into the environment, where they disperse and infect other victims.
When normally active soldier beetles become infected with Eryniopsis, they do a zombie walk to the tips of leaves, grab onto leaves with their jaws, and die. After death, the fungus within causes their wings to spread, facilitating the release of spores into the environment.
Dead flies deceiving hapless suitors
Seedcorn flies infected with Entomophthora climb high on plants. Their grotesquely swollen abdomens are attractive to male flies that will attempt to mate with them, thereby becoming infected and furthering the spread of Entomophthora.
Cool, wet springs also spawn legions of seedcorn maggots, a pest of many horticultural and food crops including soybeans, corn, peas, onions, potatoes and beans. As temperatures warm, peril awaits adult seedcorn maggot flies. Hiding on the springtime vegetation are infective spores of a fungus called Entomophthora muscae. When the fly alights on vegetation, unseen spores attach to the surface of its exoskeleton. When the right combination of temperature and humidity conspire, spores hatch and fungal hyphae penetrate the skin of the fly, establishing a lethal infection. Once inside its host, the fungus invades the fly’s tiny mind and body transforming it into a fly zombie. By taking control of the fly’s nervous system, Entomophthora causes the doomed, but inherently fidgety fly to move ever more slowly upward and outward on a plant until it creeps to its final resting spot at the tip of a leaf or branch. From this elevated perch, the fungus erupts from the skin of the fly and spews spores into the air, all the better to distribute its spawn on vegetation where other flies will inadvertently become infected. In a related species of fly, the common house fly, Musca domestica, another strange twist happens in this zombie insect tale. The fungus infection causes the abdomen of a fly to swell dramatically. This large abdomen is highly attractive to male houseflies seeking a mate. Large abdomens may be an indicator of higher fecundity in a potential mate and, yes, just like Sir Mix A Lot, male houseflies like big butts. Causing the abdomen to swell may increase the chances of attracting a randy suitor that will become infected, further helping the fungus to multiply and disperse.
Male cicadas get in touch with their feminine side
One of the strangest twists in the zombie insect genre is set to take place in millions of backyards next spring with the return of the Big Brood, Brood X periodical cicadas. Beneath trees where cicadas spend their youth sipping sap, spores of the fungal pathogen Massospora cicadina have been waiting for 17 years. During April and May as cicada nymphs escape from the earth, resting spores of Massospora adhere to their exoskeletons. Compounds on the surface of the cicada send a signal to the spores that dinner is served and it is time to germinate. The fungus penetrates the skin of the cicada and multiplies, turning the cicada into a fungus garden. Spores of Massospora are then released into the environment where a second, more sinister wave of infection takes place. At this stage of their cycle, thousands of newly molted adult cicadas populate the landscape to begin their courtship rituals. Ubiquitous spores of the fungus spewed from the nymphs adhere to the skin of adult cicadas, germinate, and begin to infect the airborne legions. The infection sterilizes both male and female cicadas, but does nothing to quell the libido of sex-crazed male cicadas. Infected males continue to seek and attempt to mate with females despite their contagious infection. In a game of tit for tat, female cicadas infected with Massospora remain attractive to healthy males that soon become infected and then mate with other cicadas. If this was not weird enough, Massospora twists the minds of infected male cicadas. Male cicadas adopt female courtship behaviors including a coy wing flick, the female’s signal that she is ready to accept a mate. This results in hyper-sexed uninfected males attempting to mate with infected drag queen males, further enhancing the spread of Massospora.Massospora becomes a cicada STD as it moves from one cicada to another by the behavior modifying process called Active Host Transmission or AHT. As the fungus develops within its host the abdomen of the cicada disintegrates, leaving behind a buff-colored mass of fungus. Infected cicadas are flight capable and their peregrinations carry the fungus to new habitats as they fly about. A second wave of infections produce resting spores that inoculate the soil with Massospora that will await the return of the cicadas in 17 years. While the loss of an abdomen spells instant death for a human, this is not the case for a cicada. Throughout cicada land male and female Massospora zombies walk and fly about missing their abdomens, macabre reminders of a very clever fungus.
As cicada nymphs emerge from their galleries next spring, Massospora spores lurking in the soil for 17 years will germinate on their exoskeleton, bore their way in, and multiply within the cicadas. Soon the cicada’s abdomen will disintegrate, enabling fungal fruiting bodies to disperse spores. Sterile but still randy males spread Massospora to other cicadas in futile mating attempts. In a mind control coup, infected male cicadas mimic female courtship behaviors that entice uninfected males to mate with them, further accelerating the active transmission of Massospora in the cicada population.
Bug of the Week hopes you have a happy and safe Halloween without any worms or fungi trying to make you a zombie unless, of course, you wish to be one.
Acknowledgements
Bug of the Week thanks Bronwyn Mitchell-Strong for providing the inspiration for this episode and for affording the opportunity to share insect zombie stories with the Natural History Society of Maryland. Many thanks to Dr. David P. Hughes for sharing his gruesome image of an ant infected with Ophiocordyceps. The following fascinating studies were consulted in preparation for this episode: “Do hairworms (Nematomorpha) manipulate the water seeking behaviour of their terrestrial hosts?” by F. Thomas, A. Schmidt-Rhaesa, G. Martin, C. Manu, P. Durand & F. Renaud; “Water-seeking behavior in worm-infected crickets and reversibility of parasitic manipulation” by Fleur Ponton, Fernando Otálora-Luna, Thierry Lefèvre, Patrick M. Guerin, Camille Lebarbenchon, David Duneau, David G. Biron, and Frédéric Thomas; “Zombie soldier beetles: Epizootics in the goldenrod soldier beetle, Chauliognathus pensylvanicus (Coleoptera: Cantharidae) caused by Eryniopsis lampyridarum (Entomophthoromycotina: Entomophthoraceae)” by Donald C. Steinkraus, Ann E. Hajek, and Jim K. Liebherr; “A fungus infecting domestic flies manipulates sexual behaviour of its host” by Anders Pape Møller; “Behavioral betrayal: How select fungal parasites enlist living insects to do their bidding” by Brian Lovett, Angie Macias, Jason E. Stajich, John Cooley, Jørgen Eilenberg, Henrik H. de Fine Licht, and Matt T. Kasson; and “A specialized fungal parasite (Massospora cicadina) hijacks the sexual signals of periodical cicadas (Hemiptera: Cicadidae: Magicicada)” by John R. Cooley, David C. Marshall Kathy B. R. Hill.
