The second success: Why flea beetles and Heliconius have the same number of species.

Root feeding larva of Monomacra violacea

After discovering the larval stages of all four genera of flea beetle, I realized that the beetles could be divided into two groups of five based on their larval feeding behavior: root/stem feeders in the genera Monomacra and Parchicola, and leaf feeders in Ptocadica, Disonycha and Pedilia (Pedilia larvae also eat stem tissue but not roots).  Then, remembering which beetles shared which plants, I realized that most plants hosted one species from each group, but not more than one.  This suggested that perhaps there were five distinct sets of Passiflora host plant, each supporting a different pair of flea beetles.  This in turn raised the question: do these same sets of plants support unique sets of Heliconius butterflies?  other insects?  The answer turned out to be yes!

Leaf feeding larva of Red Ptocadica

Solitary feeding generalist larva of Heliconius cydno

To answer this I turned to my research done in the 1970's and 80's, in which I measured and analyzed the host plant relationships of Heliconius.  There, I treated the butterflies as belonging to two species groups (group I and group II), each of which laid eggs on two main groups of Passiflora vines.  The vines themselves fell into three subgenera now called Astrophaea, Decaloba and Passiflora (why did they have to name one subgenus Passiflora?  It makes it wordy to always have to distinguish the genus from the subgenus).  Group I uses Decaloba , with one species specializing solely on Astrophaea.  Group II uses mainly subgenus Passiflora, but some species occasionally lay eggs on Decaloba and Astrophaea.  A complicated picture, but if you step back there is a simple pattern: Astrophaea with 1 species of Heliconius, Decaloba with 4 species and subgenus Passiflora with 5 species.  Within Decaloba and subgenus Passiflora there were some "generalist" species that would lay eggs on more than one Passiflora species, and some monophagous species specialized on one species only.

Group feeding H. doris larvae only eat Passiflora ambigua

After remembering this relationship, I looked up references on the genus Josia, an orange and black moth that feeds on Passiflora costaricensis at La Selva.  I got lucky and found an incredible  opus by James. S. Miller, a complete modern revision of the tribe of moths including Josia, called the Dioptinae.   According to his work, the 150+ species of Josia relatives included several genera specializing on the same three subgroups on Passiflora.  Getta feeds on subgenus Astrophaea, Josia feeds on Decaloba, and Lyces feeds on subgenus Passiflora.  Miller suggests that these genera may have co-evolved with Passiflora as it diversified over the past 40 million years.

Josia frigida feeds on Passiflora costaricensis at La Selva

Like Heliconius and Josiini, the flea beetles also specialize on the three subgenera.  Only one species (the Blue Monomacra violacea) feeds on more than one subgenus, and that only in the adult stage.  The others are all specialized to feed on one subgenus or another.  Thus, although we don't yet understand the precise reasons, it is clear that most Passiflora-feeding herbivores diversify and specialize on the three principal Passiflora subgenera.  A second finding from my original research on Passiflora and Heliconius is that different species, plant and butterfly, are found in different habitats within and adjacent to the forest.  For example, P. pittieri, the only member of subgenus Astrophaea, is only found within the forest, but the other two subgenera have members adapted to either forest or second growth environments.  As a result there are five sets of Passiflora species, as can be seen in the chart below.  Just what the flea beetle larval feeding data suggested!

One more observation completes the picture.  The Heliconius species may be divided into two types that probably don't compete with each other, generalists that fed on more than one Passiflora species, and monophagous species that normally only use one host plant. They don't compete strongly because the generalist species usually lay eggs singly on small isolated plants of more than one species.  The monophages on the other hand lay clusters of eggs on larger plants, and only on one species.   With these groupings in the chart above it becomes obvious why there are the same number of flea beetles as Heliconius: there are two sets of five host plant groupings for each type of herbivore!  The number does not add up to 20, because two Heliconius and 2 flea beetles are very rare and I don't have enough information to fit them in the chart.  Perhaps they are stragglers from other habitats in which they are more common.  Even with this complication, the chart shows clearly why the number of species in each community is about 8-10 species.

Interestingly, the community structure is not a function of chemical diversification in cyanogenic glycosides, which was one of my first hypotheses when I began the study.  Chemistry is obviously important in defining the three subgenera, although we don't understand its role, and it is also almost certainly important in the life histories of the monophagous species, but the overall role suggests that herbivore communities "deal" effectively with whatever cyanogens the plants throw at them.  Of course you may see in the chart three Passiflora species not widely used by either flea beetles or Heliconius at La Selva - they may have some effective chemical defense.  But the take home message is that the communities are determined by a combination of host plant taxonomy, habitat specialization, and larval feeding syndromes.  The second message is that the two communities are basically "full" or "saturated" with species.  This may be seen by the fact that each "box" in the chart has only one species, meaning that there is no "room" for two species to share the same "box."  This may be the reason that the same species are found now as were found in 1975 when I began the study.  Apparently these are relatively stable communities!

Success! Twice Over!

Blue Flea Beetle on leaf.  Hard to photograph - too reflective!

This shorter stay at La Selva is coming to an end, but it has been a good four-month stay. The effort to propagate cuttings of Passiflora lobata resulted two months later in 6 small but healthy potted plants with about 10 leaves each.   I was able to put these in cages with several Blue flea beetles, and, after a few weeks, got some eggs and larvae.  This was crucial, since the Blue Flea Beetle, with scientific name Monomacra violacea, is one of the most common flea beetles at La Selva.  It is also the most tolerant and can be found feeding on nearly every species of Passifora except two.  In past field seasons I found the larvae of the other genera, but Monomacra eluded me.

Monomacra species are obviously related to the three species of yellow Parchicola.  Both genera have a similar trim, elongated shape and both have a flattened rectangular depression on the posterior end of the pronotum, the "shield" immediately behind the head.  In 2013-14 I found eggs and larvae of two of the Parchicola species, and I expected the Blue beetles to be similar.  What I found was indeed some amount of similarity, but also some differences.

Like Parchicola "yellow-legged" (there is no official species name in this case), M. violacea cylindrical eggs are laid near the base of the plant.  Unlike Parchicola, the eggs are attached at the end (see photo).  The eggs hatch after an unknown number of days, and the slender, tiny larva emerges.  The larva is quite mobile, looping tail to head like a tiny inchworm.  The six thoracic legs are sturdy, grabbing the substrate easily.  The anal clasper is also relatively large and is surrounded by a ring of bristles. Each segment of the thorax and abdomen has two rows of pigmented flaps, like deflated balloons.  This pattern also contrasts with Parchicola, which have only one row of flaps.  Also, the larva is white rather than yellowish.  Otherwise, the young larvae of the two genera are similar.

Newly hatched M. violacea larva.

Newly hatched larvae have a transparent, unpigmented head capsule, bearing two large bulbous antennae capable of retracting into tubes on the head.  The legs and anal ring are also initially transparent, but after one day they melanize and darken.  The head capsule in particular become shiny black. The larvae loop along the rootlets of the host plant, feeding occasionally by chewing on root hairs and root tissue.  Typical feeding damage includes small pits eaten out of the pithy part of the root.  The central fibrous core of the rootlet is not eaten.

Third instar larva, almost fully grown and ready to pupate.

Above I was describing the first instar M. violacea larvae.  I have not yet seen the second instars, but the third instars are, of course, much bigger and fatter in relation to their body length.  The biggest change is that the pigmented flaps are replaced by tiny transparent spheres in the larger larvae.  They look like droplets of liquid but they are in fact cuticular, dry not wet.  The root environment where the larvae live has many predators such as centipedes, roundworms and isopods, and I can easily imagine the spheres are filled with some chemical deterrent.  But this just a guess at this time.

I forgot to explain the title of the blog: Success Twice Over! "  The eggs and larvae described here are one success.  The other has been my effort to make sense of the parallel species diversity of the flea beetles and the Heliconius butterflies.  More on that in the next blog.

Larval feeding damage to rootlet of P. lobata

Back to La Selva - in the rainy season!

Cement path at La Selva

Finally, after a full year, I am back at La Selva, working on the Flea Beetle Project!  During the past year Kim and I fulfilled a promise we made to ourselves to live for a full year on our Palomar property.  This turned out to be very successful and comfortable for us, to the point where it was hard to leave!  In fact Kim stayed an extra month to complete her job at Mother's Kitchen restaurant; she will join me in early September.

During the year we installed a broadband internet uplink, enabling me to update the flea beetle web site  (as well as allowing us to shop  and watch utube and netflix).   Also during the year I created a draft project summary, which may be found on the web page:

Red Ptocadica flea beetle on Passiflora lobata leaf.

http://johnterahsmiley.com/heliconius-passiflora-flea%20beetle/FB%20summary%202014/summary%202014.html .  To me this summary is very exciting, portraying a wide-angle picture of this tiny, complex, colorful world.  Writing the summary has also prompted me to focus on some of project's shortcomings, two of which I hope to correct on the present trip.  One is my lack of natural history observations during the June through August rainy season.  Another is that I still have not found the juvenile stages of one of the most common flea beetles, in genus Monomacra.

The present trip has begun ideally for correcting the first   problem - I arrived to La Selva August 5 after an unusually intense rainy season.  Any observations I can make over the next few weeks will tell a great deal about rainy season effects on the beetles.  Thus far, after a few days of observing,  I can say that many of the flea beetles are actively reproducing, as indicated by aggregations of 5-15 beetles of the same species on a plant, including mating pairs.  These include two species of Parchicola, Monomacra violacea, red Pedilia, and red Ptocadica.  The only common species I haven't yet found is yellow-tibia Parchicola.  This suggests (with the possible exception of yellow-tibia Parchicola) that life goes on as usual for the beetles during an intense rainy season.  This is in contrast to the Heliconius butterflies, whose numbers and activity seem greatly suppressed.  Perhaps another important difference between the flea beetles and the butterflies?

Red Pedilia larva after moulting to 2nd instar

As for the second problem, I need to grow a set of potted Passiflora vines for caging with Monomacra violacea flea beetles.  To do this I need to make Passiflora cuttings and root them, which takes a few weeks.   Once ready, I will catch the flea beetles and put them in the cage.  Then, over time, I will check the cages for eggs and larvae.  I predict great similarity to Parchicola, which is thought to be closely related to Monomacra, but we will find out.  In any case, it's great to be back!

Eggs of Red Pedilia on Passiflora pittieri