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!