Or – What do I do when field observations don’t match lab results. This is a philosophical debate that has plagued ecologists for decades and it brings up all sorts of issues – relevant scale, extrapolation, replication and pseudoreplication, variable control, realism, and the list can go on and on. How did I arrive at the crux of this debate? Cochlodinium polykrikoides. It is a harmful algal species, now a common annual occurrence in Long Island, NY, whose blooms are known to be ichtyotoxic, and more recently, to be potentially devastating to shellfish as well. Now I am not a harmful algae person by any stretch of the imagination, but many of my colleagues are, and I often find myself engaged in healthy debates with them over the utility of lab vs field experiments.
Why? Well there is a body of literature that suggests C. polykrikoides is harmful to a number of shellfish species. In fact, chronic exposure in the lab has led to high mortality and depressed growth rates of juvenile bivalves. Other studies demonstrate rapid mortality of bivalve larvae in lab exposures over periods as short as 24 hours. Lab experiments have proved especially useful in determining the mechanism of toxicity, and determining how dense blooms should be to have particularly devastating impacts. The Gobler lab at the School of Marine and Atmospheric Sciences at Stony Brook University is at the forefront of many of these studies.
Again, I am not a harmful algae person, so why do I care about this? Well, my study organism, the bay scallop, can be affected by these blooms. That, and the fact that millions of dollars have been invested to restore bay scallop populations in NY waters. The earliest research of these blooms out of New York (where they first appeared in 2002 and have recurred annually since 2004) indicated harm for bay scallops. Using 5-l plastic buckets and bloom water collected from the field, Gobler and others (2008) demonstrated up to 75% mortality of juvenile scallops (~11mm shell height) after 9 days of exposure. Additionally, this stud demonstrated a significant impact on scallop growth rates, being half in the bloom water as in controls – so even those scallops that survived were not doing well.
Other studies out of the lab have showed something even worse – up to 100% mortality of scallop larvae over relatively short time scales during the lab study. In well plates, Gobler and Tang utilized 10 ml of varying bloom densities of C. polykrikoides or a control consisting of T-Iso (Tahitian isochrysis) . In this study, with 20 larvae in each 10-ml well, the highest CP cell densities, >2000 per ml, caused rapid 100% mortality of bay scallops, within 10-24 hours. This is clearly problematic, as blooms occur when scallop larvae are expected to be in the water, so this has potential to be devastating to the restoration effort.
If we extrapolate based on these results, we would expect extremely low recruitment and abundance of bay scallops. In fact, the Gobler et al paper from 2008 says exactly that: “Our results demonstrate that the failure of this population to recover could be due, in part, to recent outbreaks of C. polykrikoides blooms in this system.” Wow. Has that for scaling up! What’s the problem here? Well, first and foremost, the statement is fundamentally false. Anyone who has been following this blog can attest to the fact that scallop populations are indeed recovering. The most recent literature shows over 13-fold increases in on bottom densities of scallops in restored basins – see Tettelbach and Smith, 2009. And a manuscript we are currently finishing shows even better results. Landings have been increasing as well, as demonstrated here:
In addition, as an unexpected natural experiment of sorts this summer, I was able to observe scallop recruitment in the presence of C. polykrikoides, which means the scallop larvae survived, remained competent, settled, grew, and survived all in the presence of this harmful algal blooms. This is preliminary data still, and remember, I was not looking for this relationship. In fact, I was simply interested in monitoring scallop recruitment in Shinnecock Bay, a south shore lagoon, with healthy eelgrass populations (and eelgrass is the preferred scallop habitat, although other habitats are also important). That was my goal. Being interested in all things, I thought it would be useful to have an idea of size fractionated chlorophyll analysis for each of my Shinnecock Bay study sites, to see what the differences might be across the bay. Additionally, I collected water that I fixed with Lugol’s so I could have an idea what the phytoplankton community looked like. As a part of this process, I was able to get CP cell densities at the same sites which I collected scallop recruits.
So what gives? Well, I think that its clear that lab experiments can’t be so easily extrapolated to the ecosystem level. And maybe, we shouldn’t even attempt to extrapolate these data to ecosystem scale processes. Lab experiments are good because they are extremely reproducible, can rapidly generate data, regulate all independent variables, and are lend toward easy replication. However, they have limitations in both spatial and temporal scale, realism and generality. So while larvae in 10 ml of high concentrations of CP all die within 24 hours in the lab, the likelihood that that kind of exposure happens in the field is extremely unlikely. Even the 5-l bucket experiments were unrealistic. The lab experiments failed to incorporate physical and biological characteristics of the system. Things such as larval availability, larval behavior, algal behavior, water column depth, variations in temperature, daylight, salinity, the community, etc, are all ignored in the lab experiments.
However, by its very nature, CP is difficult to study in the field. It is a spatially aggregating, chain forming species – so that over the spatial extent of the bloom you can experience cell densities that vary by orders of magnitude. It also undergoes diel vertical migration, so that it is at the surface during the day and the bottom at night (where exactly they go at the bottom is another story). It just can’t be controlled in the field and its spatial extent and bloom density is highly variable and unpredictable. So figuring out the problems with the lab exposures is not as simple as placing some scallops out in the field. So its a question that is not easily solved, which is probably why it is still being debated after decades.
In case you couldn’t tell, I am a field ecologist by trade, so I am obviously a little biased. But I do personally believe that lab experiments, while important, have limited utility in ecological studies without appropriately scaled field studies to corroborate the results. Many times, microcosm studies don’t. I am not as bullish on lab studies as Stephen Carpenter (1996) who suggests “an ecologist who isolates organisms in bottles may not be working on communities and ecosystems in any relevant sense.” I think that microcosms and lab experiments have their place – and that they provide valuable information for ecological studies, and I do employ them on a limited basis. It is just in my strong opinion that their value becomes limited without field testing the results.
Either way, it is certainly an interesting debate. Both sides have valid arguments – reproducibility, replication, control in lab experiments, the realism, relevant scales, and generality in field and natural experiments. The ideal combination of lab and field experiments depends on the questions asked and species studies. But it is clear that at times, the field observations don’t match what would be expected from lab experiments. This doesn’t mean either side is wrong, but illustrates the need to utilize both practices.
EDIT – This blog post is not intended to suggest harmful algae don’t have impacts in the field. There are plenty of examples from the field of harmful algae having impacts on fauna – including the recent sardine die-off in California. Rather, it is only to illustrate disconnects between field and lab observations.
Carpenter, S. (1996). Microcosm Experiments have Limited Relevance for Community and Ecosystem Ecology Ecology, 77 (3) DOI: 10.2307/2265490
Gobler, C., Berry, D., Anderson, O., Burson, A., Koch, F., Rodgers, B., Moore, L., Goleski, J., Allam, B., Bowser, P., Tang, Y., & Nuzzi, R. (2008). Characterization, dynamics, and ecological impacts of harmful Cochlodinium polykrikoides blooms on eastern Long Island, NY, USA Harmful Algae, 7 (3), 293-307 DOI: 10.1016/j.hal.2007.12.006
Tang, Y., & Gobler, C. (2009). Cochlodinium polykrikoides blooms and clonal isolates from the northwest Atlantic coast cause rapid mortality in larvae of multiple bivalve species Marine Biology, 156 (12), 2601-2611 DOI: 10.1007/s00227-009-1285-z
Tettelbach, S., & Smith, C. (2009). Bay Scallop Restoration in New York Ecological Restoration, 27 (1), 20-22 DOI: 10.3368/er.27.1.20