Month: October 2020

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

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

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

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.

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American beech, Fagus grandifolia, an iconic stalwart of North American deciduous forests, is prized for its massive size at maturity, dark glossy green foliage, and smooth grey bark. While wandering in a forest here in the DMV, I was startled to find an American beech with dingy black leaves and strange growths on its branches, several of which were flocked with a pulsating blanket of brilliant white wax. What mischief befell this paragon of the woods? The answer lies within the coat of white wax on the branches. A strange aphid called the woolly beech aphid, a.k.a. beech blight aphid and boogie-woogie aphid, makes American beech its home. This aphid is capable of producing incredible amounts of fluffy white wax from specialized wax glands lining its abdomen.

Life for a beech blight aphid begins with an egg that has survived winter’s chill on the bark of a beech tree. From this egg hatches a nymph that eventually develops into a wingless adult capable of producing legions of offspring. These youngsters develop into winged adults, some of which remain on the host while others depart to find a swamp cypress tree. Here they enter the soil, settle on the tree’s roots and develop by removing sap from the vascular bundles of the roots. How strange is that? Those that remain on beech trees will be parthenogenetic; a legion of Amazonian females reproducing in the absence of males. You go girls!

The colony will grow from just a few in spring to thousands by late autumn. Like other members of their clan, these aphids suck nutrient rich phloem sap from the vascular tissues of the beech. Excess fluid is excreted as a sugar rich product called honeydew. Vast amounts of honeydew rain down on leaves and branches below the colony. This sticky coating serves as a substrate for the growth of a unique sooty mold fungus, Scorias spongiosa, which, at first, is a thin black coating on leaves and bark. Later, as honeydew accumulates from thousands of aphids, the fungus forms a large dark sponge-like mass that may be crowned with yellow fruiting bodies of the fungus. Although sooty mold is not believed to be directly pathogenic, it may cloak leaves and reduce photosynthesis. Luxuriant honeydew and attendant sooty mold beneath infested beech trees may reduce survival of beech seedlings struggling to grow below.   

While taking a photograph of the colony I disturbed a branch, which instantly sent the aphids into paroxysms, with myriad aphids waving their wax covered rear ends up in the air. The rhythmic swaying of aphid posteriors gives rise to the moniker boogie-woogie aphid. This remarkable behavior is thought to confuse predators considering an attack on members of the colony. It certainly confused me. So, when someone is watching, aphids may dance.

Brilliant white wax produced by thousands of beech woolly aphids turn small beech branches snowy white. When disturbed, aphids break into a massive swaying dance routine with abdomens and wax held high. This group reaction is thought to confuse or distract predators. Or could it be that ladies just like to dance?

Ah, but the aphid has one more defensive trick up its sleeve or, should we say, at the end of its nose. The piercing mouthparts inserted into the vascular tissue of the tree to remove sap are comprised of tiny needle-like stylets. Researchers discovered that when caterpillars were introduced to the colony, squads of hostile female soldiers attacked and stabbed the caterpillars causing them to fall from the branch. A colleague tempted the ferocity of the aphid defense when he unwittingly grasped a branch infested with aphids. He described the encounter as “…something like a cross between a burning and stinging sensation.” In the waning days of autumn, take a walk in the woods and see if you can discover a colony of boogie-woogie aphids. Maybe bust a move with them. Dance like no one’s watching.       

Acknowledgements

Bug of the Week thanks Joe Boggs for providing inspiration for this episode after enduring an attack by beech woolly aphids. His Bug Bytes Blog “Attack of the Boogie-Woogie Aphids” and two fascinating studies, “Colony defense by wingpadded nymphs in Grylloprociphilus  imbricator (HEMIPTERA: APHIDIDAE)” by Shigeyuki Aoki, Utako Kurosu, and Carol D. von Dohlen, and “Cascading effects of a highly specialized beech-aphid–fungus interaction on forest regeneration” by Susan C. Cook-Patton, Lauren Maynard, Nathan P. Lemoine , Jessica Shue, and John D. Parker were consulted to prepare this episode.

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The waning weeks of summer and first few weeks of autumn are times when many six and eight-legged critters begin to invade homes here in the DMV. Previous episodes of home invasions featured nefarious brown marmorated stink bugs and multicolored Asian lady beetles lurking on walls and windows, a wolf spider wandering in a sink, camel crickets and house centipedes milling around bathtubs, and a velvety soldier beetle larva that somehow find its way indoors. Many of these creatures, like spiders and larval soldier beetles, are predators on the prowl for a tasty arthropod to eat. Others, like stink bugs and lady beetles, are simply trying to find a safe place to chill out and spend the winter until food returns in spring.  

Several days ago, I received a fine image of a striking predator known as the big-headed ground beetle, Scarites subterraneus. This beauty had been found trespassing in a friend’s kitchen. The big-headed ground beetle is part of a very large family of beetles called ground beetles, a clan more than 40,000 species strong. Scarites is a fierce predator both as larva and adult. I often find them under mulch or beneath rocks lining my flower beds. On several occasions I have seen Scarites larvae dashing across patios and walkways as they move from one planting bed to the next. Both life stages attack and kill a wide variety of pests that frequent our gardens and landscapes, including ground dwelling caterpillars such as cutworms and armyworms, as well as wireworms, fly larvae, ants, aphids, snails and slugs.

Ground beetles are super important predators in gardens and landscapes as both adults and larvae. They hunt and kill a wide variety of pests including snails, slugs, grubs, and soil dwelling caterpillars like cutworms and armyworms. Both adults and larvae are fast movers and are often seen beneath stones, mulch, logs, and sometimes running across sidewalks, roadways, and patios. It is not unusual to have them as guests entering your home in autumn. Simply collect them in a jar or water glass and release them back into your landscape where they enhance sustainability by reducing populations of pests.

As their common name implies, most species of ground beetles forage and live at the interface of soil and air. However, a few species such as the fiery hunter, Calosoma scrutator, and its smaller cousin, Calosoma wilcoxi, trend arboreal. They devour gypsy moth caterpillars and cankerworms in the treetops and feast on unlucky inchworms that fall to the ground.  Ecosystem services provided by ground beetles don’t stop at demolishing insect pests. Many ground beetles are omnivores and when not consuming meat, they feed as granivores on the seeds of weeds. Harpalus pensylvanicus and Anisodactylus sanctaecrucis are two common granivorous ground beetles that occur throughout much of North America. Scientists have found Anisodactylus and Harpalus adept at removing seeds of important agricultural, lawn, and garden weeds including lambsquarter, pigweed, foxtail, crabgrass, and velvetleaf.  After snapping a shot of Scarites, my friend scooped up his unusual house guest and released it back into the landscape. In its natural surroundings it will continue to provide excellent service by removing pests from the garden, just as Mother Nature intended.

References

Special thanks to Dr. Shrewsbury for providing insights and references for this episode. We also thank Frank Roylance for providing the great image of Scarites that inspired this episode. The fascinating study “Ground beetles as weed control agents: effects of farm management on granivory” by Jonathan G. Lundgren was consulted in preparation of this episode.

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In a previous episode we lamented the unusual paucity of large swallowtail butterflies in our gardens this year. But 2020 has not been a rotten season for all of our six and eight legged friends. Over the past few weeks, I have received several images and a few videos of black and yellow garden spiders who have made their homes in flower beds and gardens here in the DMV. Some of us have shared the experience of wandering along a path through a meadow and bumbling into an enormous spider web ruled by a fearsome yellow and black spider.

Argiope aurantia, the so-called black and yellow garden spider, is extraordinarily common this year in some locations. Webs of the black and yellow garden spider can be gargantuan, often spanning several feet. Fortunately for Bug of the Week and for the first time in several years, one of these gorgeous arachnids, a female by the name of Sylvia, has taken up residence amongst my zinnias where she helps to keep blow flies, stink bugs, and other less desirable arthropods at bay.

One of our past resident black and yellow garden spiders, Charlotte, demonstrates her skill at immobilizing and capturing prey. A brown marmorated stink bug stands no chance once it encounters the sticky strands of the web. Charlotte’s attack is eerily reminiscent of Frodo’s unfortunate encounter with Shelob in route to Mount Doom. After immobilizing the stink bug, she returns to feast on the remains of a former, now unrecognizable, victim. Spiders, along with many other home-grown predators, are part of the reason stink bugs are not the problem they once were here in the DMV.

One of the signature features of Sylvia’s web and those of other orb weavers is the construction of a zigzagging band of dense silk called a stabilimentum near the center of her web. The function of the stabilimentum is a topic of debate among arachnologists. Some suggest that the band helps disguise the spider from its predators by providing a form of camouflage as the spider rests in the center of its web. Others believe that the silk may act as a tiny parasol shielding the spider from intense rays of the sun. One fascinating study revealed that the conspicuous bands of silk acted as a visual warning to low flying birds, reducing the likelihood of devastating web-destroying crashes much the same way an image of an owl on a large plate glass window dissuades misguided birds from crashing and breaking their necks. Of course, the spider cares not for the welfare of the bird, but repairing bird-damaged webs takes time away from important projects like capturing and eating insects.

One recent misty morning, more of a rule than an exception this year, provided a grand opportunity to witness another curious behavior of Sylvia the orb weaver, her skill at web-flexing. While stationed near her stabilimentum and grasping strands of silk, Sylvia flexed and extended her front legs repeatedly. Her rhythmic gyrations set the entire web rocking back and forth. Swaying the web in rhythmic motion is called web-flexing, a behavior often observed in orb weavers. Web-flexing has been reported as a way to dislodge potential predators, or to cause prey to become entangled in sticky capture-threads in the web. Flexing may serve other defensive purposes as well. Enemies of the orb weaver include predatory lizards, toads, and other spiders that rely on keen eyesight to locate and capture prey. In an interesting treatise on orb weavers, Wayne Tolbert suggested that web-flexing might be a clever way for the spider to conceal its exact location, thereby confounding hungry predators. On this rainy morning I wondered if Sylvia’s vigorous web-flexing might be a way to shed raindrops from the silken capture-threads of her orb. When you see orb weavers and other spiders in your gardens and landscapes, please avoid any urge to destroy them. We have found spiders to be one of the most important group of predators putting a beat-down on common pests of ornamental plants in residential landscapes.

On a rainy morning, Sylvia, a black and yellow garden spider, uses her forelegs to rock her web back and forth. This behavior known as web-flexing may help her snare prey, dodge predators, or, perhaps, shed raindrops that accumulate on capture-threads of her web. Another black and yellow garden spider has had a very successful season producing two marble-sized egg cases from her harvest of prey. Video credits: Michael Raupp and Ann Payne

Acknowledgements

Bug of the Week thanks Anne Payne, Jill Moore, Steve Hand and Gene Ferrick for sending images and videos and for donating black and yellow garden spiders, inspiriting this episode. Three great articles, “Predator avoidance behaviors and web defense structures in the orb weavers Argiope aurantia and Argiope trifasciata” by W. Tolbert, “Do stabilimenta in orb webs attract prey or defend spiders?” by T.A. Blackledge and J.W. Wenzel, and “Do top-down or bottom-up forces determine Stephanitis pyrioides abundance in urban landscapes?” by Paula Shrewsbury and M.J. Raupp, were consulted for this episode.

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