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Maculinea arion

Hey, look at that!  It’s a delicate pale blue butterfly (Maculinea arion) from Europe and northern Asia. What could this ethereal creature have to do with the horror theme which this blog has been following as a lead-up to Halloween?  In fact, what does the butterfly have to do with any of Ferrebeekeeper’s regular themes?  Butterflies are lepidopterans rather than the hymenoptera we favor here.

As it turns out—the butterfly has a lot to do with hymenopterans.  Maculinea arion, or “the large blue butterfly ” to use its not-very-creative English name, may look innocent as a butterfly, but in its larval stage the creature is both appalling and remarkable.   Alcon caterpillars are myrmecophiles—which means the caterpillars live in association with ants.  Despite the Greek meaning of ”myrmecophile”  (to love ants) the relationship is anything but loving on the part of the Alcon caterpillar–unless love is meant in the same way as “to love ham”.

Maculinea arion (Large Blue) larva carried by ant (Drawing by Frohawk)

M. arion caterpillars are relentless predators of ant larvae.  The way they obtain this fragile foodstuff is remarkable for sophistication and ruthless guile.  When a caterpillar hatches, it lives for a few days on wild thyme or marjoram plants.  The caterpillar then secretes a sweet substance which attracts red ants which carry the larva back to their tunnels.

Inside the ant hive, the caterpillar produces pheromones and chemical scents which mimic those of the ant queen.  It also scrapes a small ridge on its first segment to produce the same noise as the ant queen. The ants are deceived by the caterpillar’s mimicry and they take it to the chamber where they rear their own larvae.  The ants wait on the caterpillar as though it were the hive monarch and they even feed it ant larvae—their own undeveloped siblings.  Once it pupates, the butterfly scrapes the inside of its chrysalis to continue the deception.  When the butterfly emerges from its cocoon the hapless ants carry it outside and guard it as its wings harden—whereupon the butterfly departs to mate and lay eggs on wild thyme or marjoram plants.

Phengaris alcon

The Maculinea Arion is not the only caterpillar to make use of this strategy.   The Phengaris alcon butterfly acts in almost exactly the same way.  Here is where the story becomes impressively crazy.   A parasitoid wasp, Ichneumon eumerus, feeds on the alcon caterpillar inside the ant hive.  The wasp infiltrates the hive by spraying a pheromone which causes the ants to attack each other.  While they are busy fighting, the wasp lays its eggs inside the caterpillar.  The wasp larvae hatch into the body of the caterpillar (which the ants think of as a queen) and they eat the caterpillar host safe in the cloak of this deception.

The parasitic wasp Ichneumon eumerus. (Image: J.Thomas/Natural Visions)

If an ant hive becomes too saturated with caterpillars it will die and all three species inside the hive will likewise perish).   The red ants in this scenario are constantly evolving new pheromone signals to outcompete the caterpillars and wasps—which in turn coevolve with the ants.  It’s strange to imagine the troubling world of deception, chemical warfare, and carnage just beneath the ground.

A “Zombee” tattoo (by Josh Herrera of Skin Factory in Las Vegas)

More bad news for honeybees: not only do our hard-working black-and-yellow friends have to contend with blood sucking varroa mites, neonicotinoid insecticides, and giant hungry bears, but a new plague has been spreading from the west coast, claiming the life of domestic honey bees.  The Zombie fly (Apocephalus borealis) is a disgusting little hunchbacked phorid fly which has traditionally preyed on native wasps and bumblebees.  Phorid flies, coincidentally, are a successful family of over 400 species of tiny flies which tend to run very rapidly (although they are capable of flight).  The most famous phorid fly (insomuch as that’s a thing) is probably the coffin fly—although the zombie fly is working its way into the limelight too.  Charming!

The parasitic fly Apocephalus borealis on the back of a bumble bee (photo by Kimberly G. O’Harrow)

Like the horrifying parasitoid wasps, the zombie fly uses its syringe-like ovipositor to inject its eggs inside of its victims.  As the larvae hatch they attack the bee’s brain and cause it to behave in bizarre manners—such as lurching around in a random fashion or flying at night (which gets the bee away from the hive and ensures that the fly lavae are not destroyed by the bee’s concerned colleagues).  Bees so affected are mordantly known as “zombees” for obvious reasons.  Eventually the zombie fly larvae pupate into hard little cocoons which resemble grains of rice.  When they hatch they rip through the bee’s body at the juncture of the head and thorax, frequently decapitating the bee.  Sometimes it is difficult to enjoy the beauty of nature.

Adult female Apocephalus borealis fly (image from Core A, Runckel C, Ivers J, Quock C, Siapno T, et al. (2012). “A new threat to honey bees, the parasitic phorid fly Apocephalus borealis”. PLoS ONE 7 (1))

It is unclear to what extent zombie flies are contributing to the decline of honeybees at large–since the flies have not traditionally attacked domestic bees.  Perhaps the death and decline of other native bees has pushed the zombie flies into this new behavior (or maybe they were getting around to it anyway—they sound like thoroughly repulsive customers).  At any rate, beekeepers have a new problem to worry about, and are tracking confirmed instances of “zombees” online at www.zombeewatch.org.

The Barbados threadsnake–the smallest known snake in the world

The smallest known snake in the world is the Barbados Threadsnake (Leptotyphlops carlae), a species of blind threadsnake so small they were only discovered in 2008 (despite living on a heavily populated, highly studied island).  The adult snakes measure only 10 cm, (4 inches) long.  Herpetologists believe these tiny snakes are at threshold of viable size for snakes: if they were any smaller they would not be able to hunt or reproduce.

Female Barbados threadsnakes lay a single egg which is huge relative to the size of the mother. The newly hatched snakes are already half as large as adults.  Like caecilians or other blind snakes, Barbados threadsnakes are fossorial–they live and hunt underground (which is one of the reasons it took so long to find them).  The little threadsnakes live on the larvae of ants and termites.

The island of Barbados is mostly covered with cities, houses, farms, and roads

Not only are Barbados threadsnakes miniscule.  Their remaining forest territory is tiny. Barbados is heavily developed and no original old growth forests exist.  The threadsnakes live in secondary forests which regrew from the vestiges of long-vanished woods.  Their entire habitat is thought to be no more than a square kilometer or two.

Copidomopsis floridanum injecting its eggs into a caterpillar.

Sometimes horror is a matter of perspective.  For example, parasitoid wasps–some of the most horrifying hymenoptera–are also some of the most beneficial to humankind. The parasitoid wasps are a hugely diverse superfamily among the hymenoptera consisting of more than 6000 different species.  These insects are ancient, successful, and profoundly useful for controlling invasive species or pests (particularly various arthropods), however as soon as one knows what “parasitoid” means it becomes difficult to regard these wasps without revulsion and distaste. A parasitoid is a creature which lives inside another creature (the host) and ultimately kills/destroys that host by consuming it or by bursting out of it.  The detailed dynamics of this relationship are often grisly in the extreme, but they highlight the bizarre (not to say disturbing) mutualism which is such a feature of the natural world.

The emerald cockroach wasp or jewel wasp (Ampulex compressa)

Parasitoid wasps are especially alarming because of the extent to which they can manipulate the behavior of their host.  For example the emerald cockroach wasp (Ampulex compressa) is a solitary hunting wasp which finds a single cockroach and delivers a mildly paralytic sting to the roach’s thorax.  This first sting temporarily incapacitates the roach and allows the wasp to carefully make a second more meaningful sting to a precise spot in the roach’s brain which control’s the roach’s escape response. Not only does the wasp know where to sting, she utilizes a toxin which specifically blocks receptors for the neurotransmitter octopamine. The wasp then chews off a portion of the roach’s antennae and returns to her layer leading the captive roach by holding its damaged antenna like a leash. Inside the wasp’s burrow she plants a single egg on the roach’s belly and then seals the zombified insect inside the chamber with sand and pebbles.  After three days the wasp’s egg hatches and the new larva feeds for 4–5 days on the external portions of the roach.  It then burrow inside the still living roach and devours the creature’s organs in a progression which leaves the roach alive for a maximum length of time.  When the roach is near death the wasp larva builds a cocoon inside it, metamorphoses into an adult, and then bursts out of the roach carcass and flies off.

Aaaagh!

Across the many different parasitoid wasps there are many variations of this behavior involving different arthropod hosts–and specifically targeting the host’s eggs, lava, or adult form.  Additionally there are sundry vectors by which the parasitoid wasps control their hosts.  Not all wasps utilize targeted neuropoisons like the emerald cockroach wasp.  Wikipedia elaborates on how close the biochemical relationship between the parasitoid wasps and their hosts can become:

Endoparasitoid species often display elaborate physiological adaptations to enhance larval survival within the host, such as the co-option of endosymbiotic viruses for compromising host immune defenses. These polydnaviruses are often used by the wasps instead of a venom cocktail. The DNA of the wasp actually contains portions that are the templates for the components of the viral particles and they are assembled in an organ in the female’s abdomen known as the calyx.

In other words some wasps utilize ancient hunks of rogue DNA to directly or indirectly control (and then destroy) their host organisms.

Braconid wasp lavae (Cotesia congregatus) destroying a tomato hornworm

The biochemical sophistication of the parasitoid wasps does not end there.  Certain wasps seem to have a symbiotic relationship with plants.  When these plants are gnawed by harmful insects (especially beetles or caterpillars) the plants release specific chemicals which summon the parasitoid wasps, which, in turn, destroy the insects. An example of this can be found in that most ubiquitous of American staple crops, corn.  When beet armyworm caterpillars  (Spodoptera exigua) start eating a live corn plant, it releases a chemical which attracts  parasitiod wasps of the species Cotesia marginiventris (the larvae of which utilize beet armyworm caterpillars as hosts). If however the corn is invaded by corn earworns (Helicoverpa zea) it will release a different chemical which attracts a different   wasp Microplitis croceipes.  As scientists look further into such relationships, they are discovering that most plants have a vast range of chemical tags which are appealing to specialized parasitoid wasps (and to sawflies).  Perhaps one of the reasons that various blights have been able to make such deep incursions in new ecosystems is the absence of plants’ terrifying little friends.

Cotesia marginiventris on a corn leaf

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