Natural history collections in ecological research

Once I dreamed a dream of being an evolutionary biologist.  As I imagined it, I would hang out in a natural history museum, comparing fossils to one another, taking notes on the minute differences, and piecing together the history of life. It wasn’t until a job fair years ago, when I babbled to an evolutionary biologist about morphologies, collecting specimens, and, pretty much word for word, “working in a dusty basement full of drawers of fossils,” that I realized it was an unlikely future.  The scientist looked at me like I was nuts: “Um… that’s not really what I do.  I work with DNA and genomes.”  I pushed him further, but his answer was clear: The job I described did not exist anymore.

Why can't I just hang out and compare the varying shapes of animals in a basement lair? Image: Wikimedia Commons: Haeckel, Kunstformen der Natur (1904), plate 44: Ammonitida

But while the job does not exist (or is a rare find at best), the specimens do. There are still huge archives at museums stuffed with bones, skins, ad infinitum. I am fortunate to have a friend who works at the American Museum of Natural History in New York in the mammals department. When I visited Catherine back in October, she was spending most of her time with the bat specimens, ensuring that they were in proper order and condition.

She gave me a tour of the place and I was blown away: I had always dreamed of walking into a room, stacked ceiling to floor with hippo skulls, and there I was! Catherine showed me the cleaning rooms, where fresh skeletons are picked clean by flesh-eating beetles; slid open a case in which hung tiger skins, as if it were her coat closet; and, by far my favorite, the marine mammal room, with massive whale vertebrae lined up on shelves. It’s funny to imagine a whale complaining of back pain, but there was even a pair of calcified vertebrae among the bunch.

After walking through the maze of rooms and seeing this vast collection with my own eyes, I couldn’t help but wonder: What are these even used for anymore? Certainly, education, but the museum was already packed with skeletons and stuffed animals without this backup. Catherine told me that sometimes researchers try to extract DNA from specimens, but that purpose alone doesn’t seem to make the best use of this huge collection. If taxonomy is now prescribed by genomics, are these collections, compiled and curated over centuries, going to waste?

In the past couple months, I stumbled upon three papers describing three different ways that these collections can be used to study ECOLOGY! (O, be still, my heart!)  The first, in Marine Ecology, online on Feburary 16, 2011, argues for the use of natural history collections to inform us about past species assemblages of areas that haven’t been heavily studied — baseline data. The researchers used Saba Bank, a reef in the Caribbean Netherlands, as a case study, studying coral specimens collected by divers in 1972. In this older collection, there were five species of corals collected that are no longer found in Saba Bank, suggesting that this understudied reef may need greater protection.

This may seem like an obvious use – but the authors note that it’s relatively unexploited. This may be because of poor record keeping, or the difficulty of locating collections from a specific area that have been shipped off to another museum. Another problem is that, if earlier sampling methods weren’t written down, it’s hard to know how representative a collection is of the area. Divers, not scientists, collected the Saba Bank specimens, so they may not have been trying to take note of all the species there at the time. But finding five species that survived there previously but don’t now is very useful information, no matter the completeness of the collection.

Certain organisms can provide information about their growth through growth rings, which makes their presence in natural history collections useful for learning about environmental conditions. Robert Scott is remembered for failing to reach the South Pole before Roald Amundsen – and part of the reason he was so slow is that he was so busy collecting specimens and taking measurements for SCIENCE. During his 1901 and 1913 expeditions, Scott collected Cellarinella nutti, a bryozoan that develops growth rings. Because this species was collected throughout the twentieth century, scientists were able to date the rings based on collection date, and create a timeline of relative growth: did the bryozoans grow significantly more in one decade than another?

The scientists found no change in growth between 1890 and 1970, but a sharp increase since the 1990s, as they published in Current Biology on February 22, 2011. Based on studies in related species, they think that this growth acceleration is either related to (a) greater production of phytoplankton, the food chain base or (b) a switch in the dominant species of phytoplankton, which could alternatively be more nutritious, speeding their growth. If they’re correct, it means that these museum specimens provide evidence for a recent increase in carbon storage on the seafloor in the Antarctic.

A chicken infected with avian pox with lesions around its beak and eyes. Image: Wikimedia Commons: Roman Halouzka

Natural history specimens can also be useful for tracking the development of disease in an animal population. Avian pox is caused by a DNA virus (the aptly named Avipoxvirus) that causes lesions either externally, on feather-free areas, or internally, in the mouth, windpipe and lungs. Beyond the metabolically draining effects of the virus, the pox symptoms can cause trouble feeding, cleaning and breathing. The virus is carried by mosquitoes and has been linked to the extinction of Hawaiian bird species.

Avian pox has been identified recently in the Galapagos islands, affecting mockingbird, warbler, and finch species that are only found there. To figure out when the virus arrived to help trace the progression of the infection, scientists used natural history specimens. Digging through past collections, the researchers selected birds with lesions like those found on avian pox victims, and looked for viral DNA to confirm that these lesions were caused by the virus. Their research, published on January 13, 2011 in PLoS ONE, reports the earliest specimen with avian pox they found was infected in 1898, and that the infections generally followed the pattern of human colonization. This suggests that the virus has been spread not by mosquitoes moving between islands, but by chickens and other pox-carrying fowl brought by settlers.

These perhaps unexpected uses for natural history collections — to reconstruct species assemblages, extrapolate climatic or ecological variability reflecting growth, or trace a disease through a population — should force scientists to rethink their collection methods. Historically, these collections were created to answer a simple question: What species are out there? As a December 2010 paper in the American Journal of Botany notes (hat tip to Colin Schultz), this mindset often leads to (a) oversampling of rare species, as just one or two specimens can misrepresent their abundance proportionally and (b) undersampling of common species, since just a couple specimens will do.

But gathering fully representational collections is easier said than done. These are real people out in the field, digging in the dirt or seafloor and may not have the space or energy to haul back many examples of a single species. Plus, you can go too far in the other direction; there is also no need to destroy the ecosystem for the sake of fair sampling!

But it does make clear that the age of DNA and genomics does not exclude the need for sampling. To ensure that past collections remain useful as ecological tools, scientists need to keep sampling for the sake of future science.

Edit: Fabulous commenters leave links to relevant articles! They each get a gold star sticker

• Tracing the history of the parasite Wolbachia in butterflies using museum collections
• Utilizing museum specimens to map deep sea creatures
• Using bivalve fossils to study the latitudinal diversity gradient extending from the equator

>Barnes, D., Kuklinski, P., Jackson, J., Keel, G., Morley, S., & Winston, J. (2011). Scott’s collections help reveal accelerating marine life growth in Antarctica Current Biology, 21 (4) DOI: 10.1016/j.cub.2011.01.033

Hoeksema, B., van der Land, J., van der Meij, S., van Ofwegen, L., Reijnen, B., van Soest, R., & de Voogd, N. (2011). Unforeseen importance of historical collections as baselines to determine biotic change of coral reefs: the Saba Bank case Marine Ecology DOI: 10.1111/j.1439-0485.2011.00434.x

Parker, P., Buckles, E., Farrington, H., Petren, K., Whiteman, N., Ricklefs, R., Bollmer, J., & Jiménez-Uzcátegui, G. (2011). 110 Years of Avipoxvirus in the Galapagos Islands PLoS ONE, 6 (1) DOI: 10.1371/journal.pone.0015989

Steege, H., Haripersaud, P., Banki, O., & Schieving, F. (2010). A model of botanical collectors’ behavior in the field: Never the same species twice American Journal of Botany, 98 (1), 31-37 DOI: 10.3732/ajb.1000215

If you feed them, they will come: the effects of nitrogen fertilization on community composition in a salt marsh

Eutrophication has gained a pretty bad reputation considering that it is a natural process.  The word itself comes from the Greek “eutrophia” which means “healthy” and simply means the addition of nutrients into an ecosystem encouraging plant growth.  Of course, there’s good reason why eutrophication has such negative connotations these days.  Since the industrial revolution, the amount of fertilizing nutrients, particularly nitrogen and phosphorus, entering ecosystems from runoff has doubled.  Just like your mother told you, too much of a good thing can be bad: too much nitrogen cause unlimited plant, algal, or phytoplanktonic growth.  When these organisms die, their decomposition uses up an incredible amount of oxygen, creating areas where these is little (hypoxic) or no (anoxic) oxygen.  One of the most famous areas for this overgrowth leading to hypoxia from eutrophication is the Gulf of Mexico dead zone, which is 6000-7000 square miles!

Satellite image of the northern Gulf of Mexico/Mississippi Delta showing hypoxic coastal water (light blue). This color change is due to excessive nutrients being washed into the sea. Source: Jacques Descloitres, MODIS Land Rapid Response Team, NASA/GSFC, January 2003.

But this is not necessarily how the story always ends.  A little bit of fertilizer runoff can actually fertilize natural ecosystems.  This typically increases the growth of plants or other photosynthetic organisms, whose growth is normally limited by the scarcity of nitrogen and phosphorus.  When there are more plants, there is more energy available to herbivores and, in turn, omnivores and carnivores, altering the food web.

So – as you can guess – we are very interested in studying how these food webs are changed, and how the fertilizer runoff from human activities alters the structure of communities.  One effect frequently seen is that the increase in nutrients allows rarer plant species the opportunity to grow.  This increase in plant diversity leads to a greater diversity of herbivores, since herbivores that only feed on one type of plant are drawn in.  Thus this increase in diversity of species can ripple throughout the system.

One question that ecologists have been asking is how a pure plant biomass increase would effect the diversity of herbivores, omnivores and carnivores in an ecosystem.  That is – not an increase in plant diversity, but a simple increase in the amount of food available.  This is a harder question to study than you might think.  Most ecosystems are diverse to start, and the rarer species with greater nutrient requirements are always looking for a way to wiggle their way in to grow and reproduce.

Spartina alterniflora-dominated salt marsh at College Creek in James City County (Colonial National Historical Park). Photo: Irvine Wilson / © DCR Natural Heritage.

A recent study in Ecology features some beautiful experiments that do a great job addressing this question.  Gina Wimp and her crew studied a salt marsh on the coast of Tuckerton, NJ.  Salt marshes are usually a monoculture: they only have one species of plant growing, a grass called Spartina alterniflora.  Not only is it a monoculture, but just one plant!  This grass species has a rhizomal root system, which can spread its roots underneath the soil and shoot up new stalks where it can find the resources and space.  So in miles of salt marsh, you will often find a single organism.  Pretty amazing!

The researchers used this monoculture to their advantage to see whether the species composition of the community changed when there was simply MORE Spartina available as a food source.  The researchers marked off three types of plots in the salt marsh.  One was an unaltered control plot, and the other two had “low” and “high” nitrogen additions 5 times throughout the 2-month growing period.  The “high” level was the maximum amount of nitrogen you could add without killing the Spartina.  They samples the insect communities 4 times during the season, and also took measurements of the changes in plant biomass and grass height when they sampled these insects with a D-vac suction sampler.  (Yes, a vacuum for bugs.)

What did they find?  Well, to start off, they did find significantly greater growth of Spartina in the fertilized plots, and it remained a monoculture, confirming what we already thought we knew.  (Phew!)  In the fertilized plots, they found not only more insects living on the grass, but a greater diversity of species, as you can see in the figure below.  The asterisks above the sampling date show that there was a significant difference between each nitrogen treatment – that is, the different in number of insects was large and consistent enough that it was not due to chance.  AND! On top of that, the actual communities of insects were also significantly different.

 

Arthropod species diversity and abundance in plots of Spartina alternifora grown under 3 different nitrogen fertilization conditions (control, low and high). Both diversity and richness increased with greater fertilization. From Wimp et al. 2010 (Ecology)

In summary: the increase in the amount of plant biomass alone (through fertilization) not only increased the number of insects and the number of different species sequentially, but also the relative abundances of each of those species to one another.  WHOAA!

What does this mean really?  Most of the focus on overfertilization from runoff has been on these dead zones and areas of hypereutrophication that I discussed earlier.  But this study shows that, even when plant diversity is unaffected, the addition of nitrogen and phosphorus affects not only plant growth, but what species are living in an area and how many of each are around.  That is: we are changing entire ecological communities.

On one hand, this seems like a good thing.  When a little bit of fertilizer reaches ecosystems, there is an increase in production and an overall increase in biodiversity, which we generally agree is a good thing.  But the problem with changing the structure of a community and even altering its food web is the potentially for causing a fundamental change in an ecosystem itself.  Seems like a strange concept – but what if the increase in growth brings in an organisms that somehow disrupts the growth of Spartina in the first place?  Then, while we temporarily have a buzzing, diverse community of organisms, the initial community could be lost, decreasing overall biodiversity.

I’m not trying to scare you or be a fearmongerer: but these are the extreme questions we have to ask when contemplating how our actions are influencing the typically balanced communities of organisms that surround us.  This truly beautifully-designed study gives us the information that communities can change just from more food resources being available.  And we can use this information to help regulate agriculture and prevent vast ecological changes from occurring that could be detrimental to the organisms, and us, in the end.

Wimp, G., Murphy, S., Finke, D., Huberty, A., & Denno, R. (2010). Increased primary production shifts the structure and composition of a terrestrial arthropod community Ecology, 91 (11), 3303-3311 DOI: 10.1890/09-1291.1