A caterpillar green around the gills, part three

The wasp pupae did not look particularly remarkable, but inside a rapid transformation was taking place. In just one week, the wasps emerged as adults.

The newly emerged wasps gathering on the lid of the vial.

They were, of course, still just as small. Nevertheless, looking closely, it is possible to see that there were two types of wasps. While some of the wasps had typical antennae, the antennae of the other wasps were branched, giving the appearance of delicate antlers.

A view of the wasps from underneath.

The two types of wasps did not mean that the caterpillar host had been parasitized by two different species, however. The two types were males and females. As in some other insects (for example this moth and this mosquito), the more elaborate antennae belonged to the males.

The wasps likely belong to the tribe Eulophini in the family Eulophidae.

Finally, it was time for the wasps to go off in search of their next hosts -- though the one pictured above spent some time inspecting my hand before disappearing into the air.

A caterpillar green around the gills, part two

After emerging from their caterpillar host, the young wasps quickly lost their plump, bright green forms.

Day 1: The wasp larvae (right) emerge from the moth caterpillar (left).

Over the next two days, they first faded to a dull yellow...

Day 2: The wasp larvae begin to pupate.

...and then shriveled and blackened.

Day 3: The wasp larvae have become pupae.

However, the wasps were not sickening and dying -- they were progressing normally through their development from larvae to pupae. Meanwhile, the moth caterpillar that stood by, apparently healthy except for its inertia, had its own development frozen. To be continued...

A caterpillar green around the gills, part one

This Halloween, instead of featuring a seasonable insect or spider, I will share a spooky story of a "possessed" caterpillar.

Parasitoids may be among the smaller enemies that a caterpillar has, but they are also among the most insidious.  When a female parasitoid (generally a small wasp or fly) finds a suitable caterpillar, it lays its eggs on or even inside the caterpillar.  The parasitoid larvae then emerge from the eggs and proceed to feed on the caterpillar.  What becomes of the caterpillar once the parasitoid invasion is complete?  It may be mummified, vanish from inside a fuzzy shroud, or perhaps more strangely -- be left apparently unharmed.

A copper underwing (Amphipyra pyramidoides) caterpillar and recently emerged parasitoid wasp larvae.

The light green caterpillar shown above and below is surrounded by the darker green larvae of a parasitoid wasp.  The wasp larvae had recently finished feeding inside the caterpillar and had broken through the sides of the caterpillar to finish their development outside.

The slits that the wasp larvae emerged through are visible behind them.

Meanwhile, the caterpillar just sat there as if unperturbed by the litter of parasitoids.

However, the caterpillar was hardly passive.  When the parasitoid larvae were threatened by an approaching object, the caterpillar became surprisingly aggressive.

The parasitoids had left the caterpillar alive, but not at liberty.  Though the caterpillar was no longer needed as food, it could still be manipulated into serving as the parasitoids' protector.

To be continued... but in the meantime, you can explore some more: Parasitoid Increases Survival of Its Pupae by Inducing Hosts to Fight Predators

A stitch too late

The hydrangea leaftiers wrapped themselves in multiple layers of protection, but what did they need to be shielded against?  Another group of caterpillars that I encountered over the summer illustrated a potential danger.  These caterpillars were also busy tying leaves.

Woven together leaves.

However, as they built their shelters, they were exposed on the exterior of the leaves.

A caterpillar, probably of a tortricid moth (Tortricidae). 

One of the vulnerable caterpillars exhibited evidence of a recent attack: two parasitoid eggs attached to its body.

A caterpillar with two parasitoid eggs on it.

Even if this caterpillar escaped the attention of predators and hid itself within the leaves, it was probably the parasitoid larvae that benefited from the shelter in the end.

A taller tail

Wasps with "stingers" the size of hypodermic needles may sound like the stuff of nightmares, but they are quite real.

A giant ichneumon wasp (Megarhyssa nortoni quebecensis).

Happily, they are also quite harmless (at least to people).  Their needle-like "stingers" are used for laying eggs, not injecting venom.

A size comparison.

The ovipositors (literally, "egg placers") of giant ichneumons are so disproportionately long because of where their eggs need to go.  Giant ichneumons, just like their more modest relatives, are parasitoids of other insects.  The unusual challenge they face is that their hosts, the larvae of horntails (a.k.a. wood wasps), feed deep within wood.  To reach them, female giant ichneumons must pierce directly through the wood with their ovipositors.

The giant ichneumon searching for signs of larvae below.

However, first the wasps must complete another difficult task -- locating their hosts within the wood.  The wasp that I watched spent some time circling around and feeling the wood with its long antennae, but it appeared that there were no horntail larvae in reach.

Caterpillars on the grass, part four

By the time fungus-infected caterpillars crawl up to the tops of grass stems  (or to other elevated positions), they are almost certainly doomed.  Therefore, it might seem reasonable to assume that this 'height seeking' behavior is instigated by and for the benefit of the fungus.  Yet, there is another possibility.

Though it is too late for the dying caterpillars to save themselves, they may be acting to save their relatives.  Female moths and butterflies sometimes lay their eggs in clumps, with the consequence that sibling caterpillars develop in close proximity.  For these families, it would be advantageous if diseased individuals left the group to avoid infecting the others.  Furthermore, being stuck at the top of a grass stem may have significant drawbacks for the fungus if large herbivores or predators of the caterpillars are around.

Whether climbing up grasses was more beneficial for the caterpillars or the fungus, there were some caterpillars that avoided infection.  About the same time and in the same area that I found the sick, green caterpillar, I caught a much healthier version that had been crawling across the ground.

A healthy moth caterpillar.

I took the healthy caterpillar home to observe whether it too would fall victim to the (at the time) mysterious epidemic.  However, unlike the sick caterpillar, which was rapidly engulfed in fungus, the healthy caterpillar soon metamorphosed into a pupa...

A healthy moth pupa.

... and later emerged as a nondescript, grayish brown moth.

Caterpillars on the grass, part three

I took the sick caterpillars home, sealed within plastic bags to keep whatever might be inside the caterpillars from getting out into my apartment.  Within a few hours, my suspicions had been confirmed: the caterpillars were sprouting fungal fruiting bodies.  By the next morning, the caterpillars were completely covered in shrouds of fungus.

One of the sick caterpillars the next morning.

Once I had solved the central mystery of what was killing the caterpillars, it became possible to find explanations for the strange circumstances surrounding the caterpillars' deaths.

The first thing that had struck me as odd was that I found most of the dead caterpillars on the tops of grass stems.  Yet, the grasses -- unlike many nearby plants -- did not show any signs of being eaten by caterpillars.  Why were the caterpillars on the grasses?  The most likely answer is that the grasses were the tallest plants around.  Insects infected by some types of fungi exhibit "summit disease", in which they climb up to high points shortly before they die.  One hypothesis is that the insect host is being manipulated by the fungus into seeking out a spot that will maximize the transmission of the fungal spores to new hosts.

The second puzzling circumstance was that the caterpillars were firmly attached to the grass stems, despite sometimes being in awkward positions (such as the one pictured below).  Such attachment can be another result of manipulation by the fungus; however, in this case, it was more likely due to the fungus directly.  Fungal hyphae can grow through the insect and into the plant underneath, tightly anchoring the insect into a spot favorable for the transmission of fungal spores.

A dead caterpillar anchored to a plant stem.

The third unusual circumstance was that the only time I found dying caterpillars was in the evening after a rain storm.  Although possibly coincidental, these high humidity conditions are ideal for the production of spores and the infection of new hosts.  Indeed, some fungi have been shown to use the insects' own circadian rhythms to time the insects' deaths favorably (from the point of view of the fungi, of course).

Was the curious behavior of the caterpillars all for the benefit of the fungi?  To be continued...

Explore some more: BIZARRE INTERACTIONS AND ENDGAMES: Entomopathogenic Fungi and Their Arthropod Hosts

The vanishing act

The monarchs were not alone in facing danger in the garden this winter.  On the papaya, there were signs that Alope sphinx moth (Erinnyis alope) caterpillars had been chewing on the edges of the leaves.  However, the caterpillars themselves were nowhere to be seen.  These caterpillars can be well camouflaged against papaya leaf veins, but in this case the caterpillars were not simply disguised.  The caterpillars were gone, and in their place, something else was lined up along the leaf veins.

A ball of white fuzz along a papaya leaf vein.

On several of the papaya leaves, there were fuzzy white objects.  Although the objects were roughly cocoon shaped, they were obviously not the cocoons of the sphinx moths (which pupate on the ground).  Looking from another angle, I could tell that the white fuzz was hollow inside -- just as if it had been made around a caterpillar.

The hollow center of the white fuzz.

Indeed, it looked that way because it had been shaped around a caterpillar.  Parasitic wasp larvae had eaten the caterpillar and then spun their own cocoons within a fuzzy matrix around the quickly disappearing remains of their host.  In a previous year, we kept some of this white fuzz in a jar to find out what was inside; the result was a jar full of tiny black wasps!

Explore some more: Erinnyis alope life cycle

The fallen monarchs

Last winter, we found a monarch chrysalis that had fallen to the ground.  We brought it inside and several days later the story ended happily as the monarch successfully emerged and took flight.  This winter, falling was still a danger -- my mother found two chrysalises on the ground -- but there were also more serious threats lurking in the garden.

The remains of a caterpillar that had begun to form a chrysalis.

When I arrived in Florida and surveyed the garden, the only monarchs that I found were a caterpillar that had died while metamorphosing into a chrysalis (possibly due to disease or parasitism) and a chrysalis that did not look much healthier.

Something seems to have gone wrong for this monarch chrysalis.

The chrysalis was a dark brown color instead of bright green.  Although a healthy monarch chrysalis should turn dark shortly before the butterfly emerges (see here), something was wrong in this case -- the monarch's wing pattern was not visible.

A few days later, the chrysalis was still intact... but empty.

After a few days, the chrysalis was hollow with no obvious sign of what had happened to the butterfly that had been developing inside.  Meanwhile the chrysalises that my mother had rescued from the ground were also brown and hollow.  What had happened to all the monarchs? 

Pupae (left) from the flies that parasitized this monarch chrysalis (right).

Looking in the container below the rescued chrysalises, we found several pupae. These pupae belonged to flies -- flies that had parasitized the chrysalises and then emerged instead of the butterflies.  Unfortunately, since the container was not sealed, the adult flies had already escaped.

Winsome invaders, lose some invaders

Of the thousands of invasive Japanese beetles that I see each summer, a small number have white ovals stuck to them.  These white ovals, which are the eggs of the parasitic "winsome fly" (Istocheta aldrichi), are usually attached to a beetle's pronotum (just behind the head) or sometimes to its elytra (the hard coverings over the wings).  Although the eggs do not look like much, they mean that the beetle has only a few more days to live.

Mating Japanese beetles (Popillia japonica); these beetles are unlikely to have any offspring, however, since the female has several winsome fly (Istocheta aldrichi) eggs glued to her.

About a day after the eggs are laid, larvae hatch from them and bore into their beetle host.  After a few more days, the beetle dies, eaten from the inside by the fly larvae.  Like the Japanese beetles themselves, winsome flies were introduced into North America from Japan.  Unlike the Japanese beetles, the flies were introduced intentionally -- in the hope that they would restrict the growth of the Japanese beetle populations.  However, it has now been more than 90 years since the flies were first introduced, and the Japanese beetle remains a growing problem.

Explore Some More: Biological Control of Japanese Beetles

A cradle of roses

As the rose hips ripen here in Maine, they are acquiring both a pretty red blush and quite a few pockmarks.  What has been causing these small scars on the surfaces of the rose hips?

A ripening rose hip with several small, dark wounds.

In the past, I had often seen rose hip flies (Rhagoletis basiola) sitting on and nearby the rose hips.  These flies did not seem to be doing much, though, except sometimes rotating their wings in what may be a mating display.  However, over the last few days, I have caught a couple of the flies in the act --

A rose hip fly (Rhagoletis basiola) ovipositing into a rose hip.

 -- puncturing the rose hips with their ovipositors and laying their eggs inside.

Another rose hip fly (Rhagoletis basiola) ovipositing into a rose hip.

When I waited for one of the flies to finish laying and leave, I saw a fresh hole in the rose hip.  Checking back the next day, I found that the hole had scarred over to match the many other pockmarks on the rose hip.

Long live the queen butterfly

Although one encounter with a parasitoid wasp ended without incident, the queen caterpillars (Danaus gilippus) were not out of danger.  As I was looking over my pictures from the previous day, I noticed another wasp -- sitting on top of the largest of the queen caterpillars.

A queen caterpillar (Danaus gilippus) and a parasitoid wasp.

If you have trouble finding the wasp in the picture above, look between the 5th and 6th yellow stripes from the left, or just look at the close-up below.

A close-up of the parasitoid wasp on the queen caterpillar.

In the subsequent pictures that I took (which unfortunately are not focused on the wasp), the wasp's abdomen is curved down and the wasp appears to be ovipositing (laying eggs) into the caterpillar.  After inspecting this series of pictures, I decided to monitor the caterpillar closely for any sign that it was indeed parasitized.  However, the next morning, the caterpillar had disappeared from the milkweed.  By searching the surrounding area, I eventually located the caterpillar in a sheltered spot where it was beginning its transformation into a pupa.

The queen caterpillar preparing to pupate.

One day later, there was a very healthy-looking chrysalis where the caterpillar had been.

The chrysalis of the parasitized(?) queen caterpillar.

Over the next few days, the chrysalis continued to look as it should, without any dark discoloration to suggest that there were a couple hundred wasps developing inside instead of a butterfly.  I left Florida before I could be sure what the result would be, but I have been informed that in the end the wasp's attempt failed and it was a butterfly that emerged from the chrysalis.

This is a different queen butterfly (Danaus gilippus), since I didn't get to see the one that emerged from the chrysalis.

Royal parasite

Many plants protect themselves from herbivory with toxic chemicals.  However, some herbivores not only tolerate these compounds, but also actively sequester them to become distasteful themselves.  For example, caterpillars such as monarchs (Danaus plexippus) and queens (Danaus gilippus) prefer to feed on milkweeds, which contain toxic cardiac glycosides.  Nevertheless, this dangerous diet does not deter all the caterpillars' potential enemies.  One day when I went to check on the caterpillars, I found a parasitoid wasp roaming the milkweed plant.

A parasitoid wasp on a milkweed stem.

With its antennae twitching up and down, the wasp walked along the milkweed stem...

The wasp walking along a stem above a queen caterpillar.

...and gradually closed in on one of the queen caterpillars.

The wasp perched directly above the queen caterpillar.

When the wasp reached the end of the stem, it appeared poised to descend and parasitize the caterpillar.  Yet, anticlimactically, the wasp flew off and the caterpillar continued eating the milkweed in peace.

Saved by the camera

I was standing near the crabapple tree when a dark shape on one of the leaves caught my eye.  As I moved closer, I saw that there were actually two dark shapes -- a parasitoid wasp and a jumping spider. 

A jumping spider sneaking up on an ichneumon wasp.

The jumping spider was stalking the parasitoid wasp, which was preoccupied with laying an egg.  With the spider poised to strike, I thought the wasp had no chance to escape.

The jumping spider closes in on the ovipositing parasitoid wasp.

Mysteriously, though, this was as close as the spider got.  After looking at the wasp for a couple of seconds, the spider abruptly turned and moved back down the leaf.  Perhaps it was spooked by the camera, or perhaps the wasp was simply too large for the spider.  Meanwhile, the wasp continued laying its egg.  A couple of minutes later, it turned to face the site where it had been laying an egg or eggs, then spent some time apparently chewing.

The ichneumon wasp chewing nearby its oviposition site.

Once the wasp had flown off, I turned the leaf over to see what had been parasitized.  What I found was the mine of a tentiform leaf miner, with a hole where the wasp had been facing.

A tentiform leaf miner mine with a hole (on the left) where the wasp appeared to be chewing.

A tall tail

How do wasps get their eggs inside other insects? First, the female wasp must find its host insect. This task may not seem difficult when the host is large and out in the open. However, many wasps parasitize insects that live deep within plants. The hosts of the wasp featured in this video are burdock seedhead moth (Metzneria lappella) larvae.

* To see this video in high definition (1080p), you may need to (1) click "YouTube" to watch on the YouTube website and (2) change the settings at the bottom of the video screen.

To detect the moth larvae feeding within burdock flower heads, the wasp (Agathis malvacearum) uses its sensitive antennae. Once a host has been located, the wasp pierces through the flower head and into the larva with its long ovipositor (from Latin, the "egg placer"). Although the ovipositor resembles a giant stinger, it is used to inject an egg rather than a painful dose of venom.  In fact, the stingers of other wasp and bee species are modified ovipositors; thus, only the females are capable of stinging.

The egg snatchers

Summer is ending and there are fewer flowers blooming in the garden.  As a result, the foliage gets more of my attention.  It may not be changing color yet, but it is covered with insect and spider life.  Earlier this week, I noticed several clusters of small eggs on lamb's ear (Stachys byzantina) leaves and on grass.

I was curious to know what had laid all these eggs.  Although most of them had already hatched, I did not see any insects nearby nor any damage to the leaves from hungry young insects.  Therefore, when I found a cluster with about half the eggs still unhatched, I decided to keep the eggs in a jar and observe what emerged. 

The leaf and eggs in my "incubation chamber": a jam jar with a damp paper towel.

The next morning, I saw my first hatchling -- but it was not the offspring of whatever had laid the cluster of eggs.  Instead, it was a parasitoid wasp.  Some time ago, this wasp must have hatched from an egg laid inside one of the already small eggs visible in the picture below.  It then grew, consuming the insect that was developing in the surrounding host egg. 

A parasitoid wasp emerged from one of the eggs.

Two more days have passed and the first wasp has been joined by several more wasps.  Nearly all the eggs have hatched, but I am no closer to finding out what laid them!

The painted lady in distress

At the butterfly garden, monarchs weren't the only butterflies to find their favorite plants.  Painted lady butterflies (Vanessa cardui) had also been attracted to the garden and were busy drinking nectar from the many flowers.

Painted lady butterfly (Vanessa cardui) drinking nectar from a coneflower (Echinacea sp.).

Whereas monarchs specialize on milkweed, painted ladies prefer thistle (in fact, they are also known as 'thistle caterpillars').  Even when small, the caterpillars can be located easily due to the white silk 'tents' that they weave around themselves.  Once a caterpillar has eaten enough thistle, it forms a chrysalis and begins its metamorphosis into a butterfly.

Painted lady chrysalis (Vanessa cardui) hanging on a thistle, surrounded by silk webbing.

However, the tent does not protect the chrysalis from all enemies.  I found one chrysalis swaying in a gust of wind.  I waited until the wind died down so that I could get a better picture.  Surprisingly, even when the wind stopped, the chrysalis was still shaking violently.  Looking more closely, I saw that there was a small wasp sitting on it.

Painted lady chrysalis (Vanessa cardui) being parasitized by a chalcid wasp.

It was the touch of this wasp, a parasitoid of the painted lady, that was causing the chrysalis to shake.  If the wasp succeeded in laying its eggs despite the shaking, then in a few days it will be a new generation of wasps, not a butterfly, that emerges from this chrysalis.


Explore some more:
Charlotte Rhoades Park and Butterfly Garden

A galling development

The rose bushes in our garden appear to be going through a difficult age.  Each time I walk by, I notice more large red "pimples" swelling up from their leaves.

Wasp galls on rose leaves.

To my surprise, when I poked one of these "pimples", it popped right off the leaf.  Curious to know what, if anything, was inside the gall, I dissected it.

Wasp larva inside a rose gall.

Inside, I found the culprit.  A wasp larva (probably Diplolepis sp.) was growing inside the gall, feeding on the soft tissue of the walls.

The curse of the mummy

This weekend, to explore a bit further afield, I visited a public garden.  While the other visitors were admiring the densely packed flower beds and jotting down the names of plants, I was inspecting the undersides of leaves.  Leaves might not seem to have much to offer when compared to the brilliant colors of flowers and the fast-paced action of the insects that visit them.  However, the plainness of leaves disguises a world of quiet intrigue.

Often, the view from above provides a sign of the action underneath.  Chewed leaf edges are a clue that there may still be a hungry caterpillar below.

A furry caterpillar munches on a leaf.

Meanwhile, folded leaves can shelter a nest.

A female Misumena vatia guards her nest.

Even the leaves that look normal from above may hide a surprising secret.  As the people around me were busy identifying new plants to add to their own gardens, I discovered a mummy. 
 

A mummified caterpillar.

This caterpillar had been mummified by a parasite (likely a wasp).  The developing parasite would have fed on the caterpillar from inside before breaking out of the mummy through the hole that is visible at the top.