Monday, February 11, 2013

The story behind "Range and Variation of Oecetis parva".

Disclaimer: The views, opinions, and judgements expressed in this blog post are solely those of the author. They are not intended to represent the views or opinions of Clemson University, the Department of Energy, or Savannah River Ecology Lab. Nor are they meant to represent the opinions of the other authors of the "Oecetis parva" article. Just to  cover all bases and my rear.

An Island of Green from Space: Savannah River Nat'l Laboratory is just right of center, a circle of green forest surrounded by agriculture and suburban development. (from Google Maps)
During my last two years at Clemson University, I was employed as a research assistant in conjunction with the Savannah River Ecology Lab (SREL) at Savannah River National Laboratory (SRS) in Aiken, South Carolina. The SREL had received a grant from the parent organization, the Department of Energy, to repeat a thirty year old aquatic insect survey of Upper Three Runs Creek and it's tributaries.

Upper Three Runs Creek and Tributaries. The four sampling sites marked are the same as the previous study, all of them located downstream from a bridge crossing. (from Google Maps)
These stream systems, located in the northern part of SRS, have among the richest levels of aquatic insect diversity in the world, with at least 575 species recorded, including some species endemic only to this location. In comparison, tropical streams surveyed thus far have an average of 400 species. You could chalk this up to sampling completeness, but Upper Three Runs is still a gem of aquatic insect diversity in North America. These numbers come from a year long study conducted from September 1976 to August 1977 (Morse et al. 1980), where a team of aquatic insect taxonomists, including my master's adviser Dr. John Morse, collected black light samples at 4 locations along the stream corridors. These collections were repeated every two weeks for the entire survey year, ending up with 51 total light trap samples and a massive amount of material to sort and identify. Since the majority of aquatic insects are nocturnal, including caddisflies, mayflies, and stoneflies, a year long black light survey will pull in most of the aquatic insect diversity in an area. And if that wasn't enough, the researchers also took two benthic net samples at each of the four locations every two weeks. (You might notice the 51 samples don't add up to a complete sampling regime. Not every location was surveyed every two weeks, either due to failures of traps to work, not enough traps, or other issues. But at least one site was sampled for that entire year, and the rest for at least half all the collection dates.)

Site A, Upper Three Runs Creek, looking downstream. No rocks, but plenty of woody debris and aquatic plants.
The really interesting thing about Upper Three Runs Creek and it's tributaries, Tinker and Mill Creeks, is they don't really look like biodiversity hotspots. Most aquatic entomologists associate high diversity with mountain streams, or at least with rocky riffle areas. Upper Three Runs Creek is located in the sandhills and coastal plain region of South Carolina, a black water stream with high tannic acids. It flows through southern pine forest and swamp. It has no rocks. So, when entomologists first look at the creek, it's kind of disappointing. No rocks, just shifting sand and silt substrate.

Upstream, at Site B. Those rocks are part of the bridge stabilization structure and are not naturally occurring.
What they soon find out is that all the tremendous diversity is tied up to these little pockets of heavy woody debris and submerged aquatic plants. These microzones of the stream are absolutely coated with aquatic insects. And so, Upper Three Runs Creek is sort of obscure in it's diversity, unless you happen to stick your D-net in the right place. Or, if you set up a black light and sit back as the sun goes down.

In Fall of 2008, I had the opportunity to see for myself. My adviser, Dr. Morse, was contacted by Dr. J Vaun McArthur of Savannah River Ecology lab about a repeat of the 1978 survey. In particular, they were interested in adult caddisfly diversity. I had plenty of prior experience identifying the larvae, but almost none identifying the adults, so I knew this would be a particularly challenging project. In the previous survey and subsequent work, nearly ~160 species were found at these locations, some of which were new to science. We were also hoping to have a more complete sampling regime, with traps running at all four locations for the entire year. Since SRS is a high security government facility with high safety standards, we had to plan ahead for each of the collecting trips and could not stay with the traps overnight.

Rube Goldberg Setup at Site A. This was taken in March, thus the early spring plant growth. By May they were as tall as the umbrella.
As for the traps themselves, they were a makeshift contraption. A pvc pipe tripod suspends a black light over a plastic pan filled with ethyl alcohol. The light is hooked up to a deep cycle battery, and the whole unit is placed under a tied and staked down umbrella in case of rain. But despite looking like a Rube Goldberg machine, they worked quite well for our purposes.

Less Rube Goldberg: This trap was under a bridge so it didn't need an umbrella.

When I returned from a collecting trip, I would sort the caddisflies out the samples.

Insect Cometary: This was an average night of sampling. I don't like killing so many insects at once, but when doing faunistics this is often necessary. We sort out what we need and save the rest for future research. The only thing that gets tossed are the moths, which we can't do much about.
I also picked out a goodly portion of the other orders of aquatic insects for identification at some point down the line.

A Really Good Day: This was the best (worst?) sample I ever sorted, and this is only the caddisflies, some of which had already been removed.
 The caddisflies were often very dense in the samples. Some of the spring collections had thousands of individuals.

Oodles of Caddis: There are at least 7 genera in this shot, probably twice that number. Everything in view is less than 15 mm in length, most around 10.
Identification was slow at first. Like I said, I had no experience with adult Trichoptera before this assistantship, and I was doing species level identifications of both males and females. For the males, we had an atlas of genitalia, but for the females I was working from primary literature and guesswork.

Largest and Smallest: Hydatophylax argus, the largest caddisfly in North America, and Neotrichia falca, one of the smallest. Note: H. argus is not found in Upper Three Runs Creek.
Some caddisflies are tiny, as shown in this picture of Neotrichia falca (Family Hydroptilidae) next to the massive Hydtatophylax argus (from the Clemson Arthropod collection). I was careful to pick out the hydroptilids along with the much larger species of other families.

Despite the previous work, I was finding species not previously known from Upper Three Runs. But it wasn't until I saw these guys that I was stumped.

Males of the mystery caddis, now known to be Oecetis parva Banks. Individuals are ~5 mm.
These are tiny caddisflies, only 5-6 mm in length, but they aren't hydroptilids. When I keyed them out, I found they were in the family Leptoceridae, the long horned caddisflies. Called such because usually they have long antennae. As you can see, these didn't. My identification placed them in the genus Oecetis, but they weren't in genitalia atlas. Eventually I checked the literature for every species of Oecetis in North America. Through a roundabout way I finally found illustrations of the last species, Oecetis parva. Nathan Banks, who originally described O. parva in 1907, didn't include an illustration in his publication. It took a trip to the British Museum by the late Herbert Ross to remedy this situation. And in 1938, Ross published an illustration of the lectotype. The illustration matched my specimens.

Or...they sort of matched.

The first law of Biology is "variation exists". This is something every taxonomist must keep in mind during his or her work, or enter the folly of unnecessary junior synonyms. My specimens had the same general look, the same clasper shape, the same size and color, but there was something off about the tenth tergite. This part of male caddisfly genitalia is the last dorsal plate of the abdomen, often modified into various shapes. The shape of the male genitalia fits that of the female like a key in a lock, and it's thought this is one of the reasons there are so many species of insects.

Left lateral view of O. parva male genitalia. Between the pad with hairs near the top is a long finger projection, and under that a pair of mebraneous hooks. Insect reproductive parts are complicated.
The tenth tergite was different. It had a long, fingerlike extension between the cerci, visible both from lateral and dorsal view. And just below the finger, there were a pair of membranous hooks, visible from lateral view. Ross's illustration didn't show these distinctive structures. So I became excited. I thought I had a new species. For two months I waffled back and forth: it was a new species, it wasn't a new species, it was a new species, it wasn't a new species. As if I was picking petals off a flower.

There was also another issue with Oecetis parva. The only places this species was known from were 14 sites in Florida and the southern tip of Alabama. It was thought to be a far southeastern endemic, found only in forest pools. Aiken SC was two hundred miles outside its known range.

But as I sent for specimens from the Florida State Arthropod Collection, I soon found out my excitement was hubris. Variation exists, and there was variation in the Florida and Alabama specimens as well. Nothing quite as extreme, but intermediates between the reduced and elongate finger of the tenth tergite. Needless to say, I was a little crushed. This would have been my first species discovery.

There were still some interesting issues. Namely, why was Oecetis parva found so far outside of it's known range? And why was it found now, and not in the previous survey?  Talking to other southeastern Trichopterists, I learned that O. parva had been collected recently at two other new sites, one in Georgia, and another near Columbia, South Carolina. So Dr Morse, Dr. McArthur, and I decided to publish this new information. This included new illustrations, of the variation seen in males from South Carolina, and of the female genitalia, which had not been previously illustrated.

More genitalia. These are, however, much prettier, as this was after I learned how to use a vector image program. (Burington et al 2011)
 Around the same time we were finding Oecetis parva in our traps, the Center for Biological Diversity presented a petition to the US Fish and Wildlife Service, with 404 southeastern aquatic species they felt warranted listing under the Endangered Species Act. Several months later, USFWS released a slightly shorter list of 374 species which were slated for a 90 day finding, and Oecetis parva was on this list. Yes, this is the caddisfly I mentioned rather cryptically in a post way back in 2011. However, my publication may have had an effect on the listing process, because I don't believe O. parva is any longer being considered. Which would mean that I as a taxonomist publishing basic natural history research has somehow influence government policy. Regardless of your opinion about whether it should have been or should not have been listed, that is kind of cool.

Recently, I gave a presentation on my master's research, including a segment on Upper Three Runs Creek and it's diversity.  I was looking at my range map for Oecetis parva, and a little hypothesis started to form, and over a few days it got bigger and bigger, until I felt like I had to share it. So, please allow me a little speculation.

Range map of Oecetis parva. Gray dots are those localities known previously. Black dots are new records. Red dot indicates unpublished previously unknown locality. Modified from Burington et al 2011
On the map, the grey dots represent all the prior localities for O. parva. The black dots are new localities in our paper. The red dot indicates a new location I recently heard about, in northeast South Carolina. And the first thing to notice is, it really does seem O. parva is limited to the sandhils and coastal plains of the Southeast United States, and particularly to well protected pine forest habitat. I also have word that Cheumatopsyche richardsoni has been collected at that red dot location, a species that we thought was endemic to Upper Three Runs Creek.

So, back to the big question: Why Savannah River Site? Why the massive diversity at Upper Three Runs Creek? Savannah River Site is known locally as the "bomb shop", because it was used for weapons grade plutonium manufacture during World War II and the Cold War. During presentations about the original 1976 survey, some wise-cracker would get up and ask "Maybe it's the radiation?" And we laugh at that joke, except, we didn't really know why there was this high diversity just here, not in the surrounding stream systems.

But it now seems that there are few if any true site endemics. Nearly all the species of Upper Three Runs Creek have been found elsewhere, and some of them widely separated, like Cheumatopsyche richardsoni. This suggests an answer, and that is: Yes, Upper Three Runs Creek is a beautiful diverse gem, but it is not unique. The southern pine forests and their stream systems used to stretch in an unbroken chain across the entire sandhills and coastal plain region of the southeast US. This diversity was probably all over the place. When industrial agriculture arrived in the early 20th century, almost all these original forests were plowed into farm fields. And now, this original diversity only remains in a few well managed pockets with protected headwater streams. We could test whether this is isolation or recent dispersal by the methods of population genetics. Unfortunately, I don't have the resources to do this currently.

This also suggests a second idea. When aquatic entomologists and aquatic ecologists just look at blackwater streams like Upper Three Runs Creek, we expect them to be of low diversity. But the natural state of these streams is HIGH diversity, and it's only because of widespread agricultural impacts that we are inclined to think differently. We need to turn the idea of blackwater streams as species poor on it's head. There are species new to science still being found in these pockets, indicative of what was lost and what treasures still are left.

Afterword: This project is in no way finished. Identifications are ongoing, and the material left is huge. I am no longer directly associated with this project and I hope it will be completed. During a recent conversation with Dr. Morse, he told me he was working through a sample from May of our collecting year. So far, that single black light trap sample has yielded over 5000 individuals and 57 different species of caddisflies. I remember that night. That was a good night.

Burington, Z. L., Morse, J. C., & McArthur, J. V. (2011). Distribution and variation of Oecetis parva (Trichoptera: Leptoceridae). Entomological News, 122(1), 100–106. [ed.: unfortunately, this is not open access. Entomological News does not yet have this option, despite being one of the few publications which will publish these sorts of articles.]

Morse, J. C., Chapin, J. W., Herlong, D. D., & Harvey, R. S. (1980). Aquatic insects of upper Three Runs Creek, Savannah River plant, South Carolina. I. Orders other than Diptera. Journal of the Georgia Entomological Society, 15(1), 73-101. 

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