Biological control of pest species has come under a lot of criticism in recent years. Employed by governments and private businesses since the late 1800's, the practice was largely unregulated until the 1980's, and regulation remains varied and complicated among different countries, and different states within the U.S.

Classical biological control specifically refers to the importation of an alien species to control pests that are usually aliens themselves. Traditionally, it has been employed in agricultural systems, in which the alien pest arrived in its new location accidentally. More recently, classical biocontrol has been undertaken to control pests in natural systems, which in the case of plants, were usually intentionally introduced through horticulture trade of botanical gardens. It is currently viewed by many ecologists as a critical tool in the battle against invasive alien species, which are growing into an ever larger economic and ecological problem.

The recent criticism of biocontrol has focused on the likelihood of "non-target" attacks, which occur when the introduced agent feeds on unintended prey or plant species, including natives. This is an especially important problem in areas with many endemic species - in the U.S., the states most affected are Hawai`i, California, and Florida because of their high native species diversity. The concern about non-target attacks is excessive, in the opinion of most biocontrol practitioners, including Messing and Wright (2006), who describe a scenario in which the peril to Hawai`i's agriculture and ecosystems is being increased by a bureaucracy that will not allow alien biocontrol agents to be imported, even to combat serious economic and ecological pests in Hawai`i that are contributing to the destruction of native ecosystems.

Certainly their concern for the native species of Hawaii is not misplaced. Invasive alien plants such as thorny blackberry crowd out natives and are less likely to be eaten by foraging alien herbivores such as pigs and goats. Generalist insects such as the two-spotted leafhopper consume hundreds of native plant species which have no natural defenses against the aliens feeding on them. So it does seem unreasonable that Hawai`i is so stingy with its species importation permits, when researchers do their best to show that their biological control agents will not feed on any native species. (I know both of the authors personally, and can verify that they are stringent in their criteria for potential non-target interactions.)

The problem with Messing and Wright's paper is the same problem with most discussions debating the use of biological control in the scientific literature, at conferences, and in online discussions. While we are focusing much energy and attention on predicting non-target interactions, which in many biocontrol programs has thus been adequately addressed, there is almost no discussion about doing a better job of predicting whether or not the introduced agent will actually be effective once introduced.

Messing and Wright themselves toss out that only 16% of effective biological control programs have been effective at controlling the target, and yet later in the paper complain about their inability to introduce agents, which is based on the assumption that the introduced agents will actually work. The high probability that (based on current practices) they will not work is never addressed in their paper. Twice the number of effective biocontrol agents, or around 33% actually establish -- probably an underestimate, since follow-up generally does not extend for years, and those that are not actively controlling the target could be missed early in monitoring -- and rarely has any follow-up been done to understand their role in the native ecosystems. If they are not attacking non-targets, and they are not controlling the pest, how are they interacting with native species?

It is true, as Messing and Wright point out, that in the current modern age of regulation, non-target effects have greatly decreased. But it is also true that even in the case where a known specialist was introduced, there can be indirect food web effects discovered when people have taken the trouble to look, which they rarely do. In one case (Willis and Memmott 2005), a native parasitoid attacking an specialist insect herbivore introduced to control an alien weed increased greatly in numbers and thus made native herbivores much more susceptible to attack, upsetting the food web in the system.

Effective biological control programs are indeed cost-effective, but a lot of money is spent for many years on the assessment of a single agent, and are we getting our money's worth if only 1 in 6 actually work? A whole new science may need to be developed to further our ability to predict the effectiveness of biological control agents. Those who are generally against biocontrol find the balance of effective agents vs. the risk of non-target effects, which while getting lower, will never be zero, to be unacceptable. What if biological programs could predict effectiveness 50% of the time? That would alter the equation, and make these programs more palatable to many ecologists such as myself.

How can something as notoriously unpredictable as species interactions be better assessed before release? One method which would give researchers much better data about the role of species in both native and alien habitats is the construction of quantitative food webs. Normally when biocontrol workers go the country of the target pest's origin, they observe only the two-species interactions between the target species an its natural predators or herbivores. This provides no predictive value because plants and animals do not interact in 2- or 3-species bubbles, they interact complexly both directly and indirectly with many species. Why don't we construct food webs of biocontrol agents in their native habitat and figure out why they seem to be effective there? We can also do retrospective studies on established biocontrol agents that are ineffective and use food webs in both the new and native habitats to try and understand why.

Of course, ecological research is conducted at the whim of funding agencies, largely NSF in the U.S. Politics and inertia often determine what is funded more than science does. Perhaps someday, however, people will realize that for both economic and political reasons, research into the prediction of the effectiveness of biocontrol agents makes clear economic, ecological, and political sense. We do need biocontrol as an option for saving some ecosystems. But we particularly need biocontrol that works.


References

Messing, R.H. and Wright, M.G., 2006. Biological control of invasive species: solution or pollution? Frontiers in Ecology and Evolution 4:132-140.

Willis, A.J. and Memmott, J. 2005. The potential for indirect effects between a weed, one of its biocontrol agents and native herbivores: A food web approach. Biological Control 35:299-306.

Labels: ecology, Hawaii, invasive species, USDA

Eupithecia is a large, worldwide genus of inchworms (moths in the family Geometridae). The Eupithecia in Hawaii are unique because of the particular ecological niche they fill - they are predators, while nearly all other known caterpillars are plant feeders only.

Here is the abstract of the original paper describing carnivorous Eupithecia (Montgomery, S. L., 1983. Carnivorous caterpillars: the behavior, biogeography and conservation of Eupithecia (Lepidoptera: Geometridae) in the Hawaiian Islands. GeoJournal 7:549-556.):

A completely new feeding pattern has been found among caterpillars native to Hawaii: certain geometrid larvae (commonly called inchworms) consume no leaves or other plant matter. Instead, they perch inconspicuously along leaf edges and stems to seize insects that touch their posterior body section. By bending the front of their body backwards in a very rapid strike, the caterpillars opportunistically capture their prey with elongated, spiny legs and 900 larvae and eggs of these moths have been collected from native forests of all the main islands and reared in the laboratory. All are species of Eupithecia, a worldwide group of over 1000 members that had been reported to feed only on plant matter such as flowers, leaves or seeds. At least 6 of Hawaii's described Eupithecia species are raptorially carnivorous, only 2 are known to feed predominantly on plant material, especially Metrosideros flowers. A diet including protein-rich flower pollen and a defensive behavior of snapping may have preadapted Hawaii's ancestral Eupithecia for a shift to predation. Severe barriers to dispersal of mantids and other continental insect predators into Hawaii resulted in an environment favoring behavioral and consequent morphological adaptations that produced these singular insects, which can be commonly called the grappling inchworms.

When insects colonized the remote Hawaiian Islands over millions of years, the results were remarkable because the chances of them getting there were so slim. This meant that a species that managed to be blown out over vast distances of ocean and land on one of the islands faced little competition or predation pressure. They then diversified into ecological niches that would not have been possible for their mainland relatives. Because there were fewer predators in the islands than the mainland from which the colonizing Eupithecia originated, there was wide-open opportunity in predation and Eupithecia had the right biological tools to grab it, despite its evolutionary history as an eater of plant parts. Interestingly, people collected these caterpillars for years without recognizing them as predators, because it was assumed that all caterpillars must be plant feeders. The story is that they always died in the lab until a fly inadvertantly got into a rearing cage, and the caterpillar was observed eating it. In the clarity of hindsight, it is interesting that it did not occur to people that these were predators, because they have quite distinct morphology and behavior. They have raptorial claws adapted for grabbing struggling prey, and long thin appendages on the tip of their abdomens which probably work somewhat like the trigger hairs in venus fly-traps. They are sit-and-wait predators, disguising their long bodies along the edge of a leaf -- behavior that makes no sense for an herbivore caterpillar which must move around a lot to feed on the plant. When an insect touches the Eupithecia while crawling up a leaf edge, it whips its head around and captures it.

Nearly all the 22 known Hawaiian species of Eupithecia behave as described in the paper. Interestingly, some are host plant specific, even though they do not eat the plant, because they look so much like that particular plant and it gives them a great advantage in disguise. Some are even specific to the part of the plant on which they rest. One Eupithecia is specific to the green, living fronds of the native Hawaiian fern known as uluhe, and it is the perfect green to match their color. Another dark brown species is always found on the mats of dead fronds underlying the green, living part of the plant.

One exception to the sit-and-wait behavior of most Hawaiian Eupithecia is the species E. monticolans (above), which appears to behave much more like a plant-feeding inchworm. It does not have the raptorial claws or the trigger hairs on the abdomen, and does not sit along leaf edges as its congeners do. When I first collected it, its food was not known, but assumed to be flowers on the `ohi`a tree (as mentioned in the above abstract). I suspected this was not necessarily the case because I collected many from trees that were not in flower. I was not successful in rearing E. monticolans caterpillars for over a year, until I inadvertantly provided one with leaves that were loaded with galls made by small insects related to aphids, in the family Psyllidae. Within a day the leaves looked like swiss cheese, with all the galls eaten out of the leaves. From then on, I always provided this species with leaves covered with galls and I never again had problems rearing them to adulthood. So while E. monticolans was thought to be a "missing link" from pollen-eating to predatory behavior, they are in fact predators, but without the morphology to make a quick strike, they must rely on eating sessile insects that cannot escape or defend themselves from a slow-moving caterpillar.

Almost no parasitoids have been reared from Eupithecia caterpillars. It certainly seems likely that Eupithecia may be rarely parasitized because it is difficult for a parasitic wasp to sneak up on it and lay an egg without being caught. Here is a brief video showing lightning-fast E. orichloris capturing a parasitic wasp (and releasing it - apparently they are not very tasty).



Listen to the jazz tune "Inchworm" here...

Labels: cool bugs, ecology, Hawaii, insects

One of the most species-rich families of plants in Hawai`i is the Rubiaceae, or coffee family. Several of these will be apparent as you walk along the boardwalk in the Alaka`i Swamp. While 22 species of the rubiaceous genus Hedyotis are listed in the Manual of the Flowering Plants of Hawai`i (Wagner et al. 1999, Bishop Museum, Honolulu), one species, Hedyotis terminalis (manono), has dozens of subspecies and varieties listed. The Manual says that this species "is probably the most polymorphic species among Haaiian flowering plants except perhaps Metrosideros polymorpha" [ohi`a, described in Part 1].

You can say that again. As I began my research project, I brought specimens of most of the plants to the botanists at the National Tropical Botanical Garden in Lawa`i for identification. After a few months I had learned the local species well enough, but in the process I believe I brought specimens of H. terminalis to one botanist at least four times. It got to be a bit embarrassing, but eventually I got a feel for the gestalt of this species.

Which brings me back to the end of Part 1, in which I suggested that the word 'species' itself may be inadequate to describe the current state of Hawaiian plants along the evolutionary continuum. The Manual admits there is no easy way to classify either H. terminalis or M. polymorpha into multiple species. Similar problems exist in some insect groups. Those doing DNA analysis of island endemics usually find similar genetic variation within a species to that between related species, which means it is nearly impossible to find genetic markers to distinguish species. Only by doing an analysis of multiple genes and seeing where an individual insect falls out on a plot of other known insects is it possible to identify it genetically. As I did with some plants, I had similar problems recognizing with certainty one moth species, Scotorythra rara, the most common one in the swamp. Once again, with the help from an expert in that genus, I understood the range of variation in that species enough to recognize it on site.

But given these difficulties, how do we know these moths or plants are all in the same species? Morphology is certainly useful, and in many insects, genitalia structure is key for separating species. But is it definitive? I'm not sure. For most Hawaiian insects, some major information is missing - their ecology and behavior. Entomologists in the islands work almost entirely with dead specimens, knowing little about how they live their lives. Among the hundreds of insects I reared and called S. rara, there were not only dozens of food plants, but multiple morphologies of the larvae (which are inchworms). When I first began rearing the insects, I assumed all these would be different species. And no one has a clue about their mating behavior, which is theoretically crucial to the actual definition of a species - if two individuals can interbreed and produce fertile offspring, they are usually (but not always, especially in plants!) considered the same species.

There is another genus of moths that positively exploded in its radiation in Hawai`i, called Hyposmocoma. There are over 300 described species of Hyposmocoma, and many in description limbo. I would not be surprised if there are actually over a thousand (as there are of a more studied fly genus in Hawai`i, Drosophila). Unfortunately, these are tiny moths, and even less is known about their life histories than about Scotorythra. An eminent entomologist I worked with on occasion at the British Museum of Natural History had tried to work on the taxonomy of the group, and had simply given up. Many specimens he studied with similar genitalia had different wing morphology, and vice versa. The larvae are case bearers, meaning they hang out in a little silken bag, and for some species the structure of the case seemed to be distinctive. But for most, it is apparently not.

Why are species so hard to separate in Hawai`i? Evolution is a continuous process, that has no endpoint. But because the Hawaiian Islands are so recent in geological time, and it is so rare for any living thing to arrive there on its own over vast expanses of ocean, I believe we are still witnessing the messy sorting out of niche-filling. The traits of different species drift and become more distinct from each other through several processes, including physical separation (via geological events, for example) and assortative mating (in which more similar individuals mate and reproduce). In Hawai`i, we have to ask, who knows what a species is? because we have not found a way to actually watch how individuals from all of these different groups interact with each other, and the environment. Speciation is not an instantaneous process, and in Hawai`i, along the boardwalk of the Alaka`i Swamp, we are watching it happen.

The plants and insects of the swamp are finding their way. Unfortunately, the evolutionary process can no longer stay on its natural course in Hawai`i, because of the habitat destruction and thousands of alien species that are invading the natural areas like the swamp and creating selection pressures that would not have been there without humans. I feel fortunate to live during the time that I do, that I had a chance to see a glimmer of what Hawai`i was really like. Of course, I don't know an ecologist there who doesn't wish we could go back in time a couple hundred years before Europeans came, or even a couple thousand years before humans were there at all. We have to be content with the few slivers of the real Hawai`i that are left, and do our best to protect them, although the future looks bleak. When I am in the Alaka`i Swamp, I forget about the continuing destruction below me. As I peer through the mist, all I think about is the wonder of evolution.

For more about the moths and plants of the Alaka`i Swamp, click here.

Labels: environment, evolution, Hawaii, invasive species

The Alaka`i Swamp on the island of Kaua`i is not easy to get to. It used to be you could drive any rental car to the head of the Pihea trail and from there be quickly on your way into the swamp, but more often than not now the last mile or so of the road is closed due to potholes and persistent underfunding of the Hawai`i state parks system.

But in any case, the hike in is quicker from the Alaka`i Trail head. The 3-mile drive there, though, is not for the faint of heart these days. I was lucky; I began my research there in 1998, in the midst of a 4-5 year dry spell during which the road had just been graded; this may happen only every decade or so, probably whenever a bit of money can be freed up to do the work. By my last summer in the swamp in 2002, it was wet again, and the choice in many places was between trenching through foot-deep ruts or skating along the slick edges, while gunning the engine to get uphill, and beyond a steep drop-off to the deep canyon below.

From the trail head it is about a half mile until the beginning of the boardwalk. The boardwalk, built around 15 years ago, is a huge boon to hikers and researchers alike, and has helped protect a fragile ecosystem from constant erosion and trampling. The plants along this first part of the trail, including alien eucalyptus, fire trees, and the beginning thickets of strawberry guavas, are likely foreshadowing the future of the swamp; each time you return you notice the aliens have encroached a bit farther in. It's not just plants; it was a shock for me to discover ants in the swamp in 2002, never having before seen them in all the long days I worked there. (There are no native Hawaiian ants, but 40+ alien species have arrived on the islands, mostly via the horticulture trade.)

Finally, as you leave the edge of the boardwalk behind and march deeper into the Alaka`i Swamp, most of the alien plants melt away, and you are transported into a wonderland of island biogeography. Islands tend to have unique native flora and fauna, with many endemic species (occurring nowhere else). The farther the island from a continental land mass, from which species have naturally invaded over the millenia, the fewer the number of common ancestors that the island's species have. In taxonomic terms, this means you can end up with hundreds or even thousands of species within a single genus, as the descendents of a single common ancestor -- the seed washing up from the ocean, blown on the wind or stuck to a bird; the gravid female moth or ballooning spider blown off course for a thousand miles -- diversify rapidly (in geological time) to fill a whole new land of empty ecological niches. At the same time, whole taxonomic families of plants, insects, and birds do not exist in the islands, because serendipity did not bring them here.

This results in the unique jungle you pass through along the boardwalk, with one of the richest native plant assemblages remaining in the islands. The invaders are working their way in, though. To a local ecologist, the tangles of thorny blackberry plants and the sweet August aromas of kahili ginger blooms jar the senses, and turn the stomach. These don't belong here. They come from places distant enough that they could not have arrived by any method other than active human husbandry. But the blackberry is reaching farther and farther from the trails, its thorny branches and leaves standing out. No Hawaiian natives have thorns, including a native blackberry that supposedly occurs in the swamp, but that I have never seen in the wild. No native herbivorous mammals means no need for thorns; the imported pigs and deer here find the native plants quite succulent, and eschew the aliens with their defenses in place.

The ginger starts in a thick clump and spreads from there, quickly dominating light gaps before the slower native plants can gain a foothold. Despite the ecological damage this plant is doing, several species species of ginger are still sold as ornamentals. Apparently the profits of the horticulturists are more precious to Hawai`i's government than an ecosystem being slowly wiped forever off the face of the earth.

But these are the only two plants to gain a strong foothold in the swamp so far. Why? Is it because of the conditions here, which at times are decidedly untropical? On a winter day, the temperature can range from freezing to over seventy degrees farenheit; in summer the highs are much higher, the sun scorching at this altitude when the clouds have dissipated. The rainfall here is upwards of twenty feet a year. Rather than a true swamp, it is really a cloud forest, with most water provided in a constant dripping of condensation off the leaves, as opposed to torrential downpours.

Ohi`a, the dominant native plant, thrives under these conditions. It also thrives along the new lava flows of the kona coast of the Big Island, where barely a plant has yet gained traction, fresh water is only an occasional visitor, and the hard black lava radiates hundred-degree heat back on the trees from below. But you might suspect that a mutual transplant experiment would not work. The coastal Big Island ohi`a and the high-altitude Kaua`i ohi`a are two of dozens of subspecies of this plant classified within a mere three species, and they have clearly adapted to local conditions. But Hawaiian plants do not lend themselves easily to human-imposed Linnaean classification. The word "species" itself is completely inadequate to describe the multitudinous forms of life that occur in the world only on these islands.


To be continued...

Labels: environment, evolution, Hawaii, invasive species