The evolutionary canary in the coal mine*

*note -this post originally appeared on the Applied Ecologist's blog

Like canaries in coal mines, species can provide important information about deteriorating environmental conditions. A whole sub-discipline of environmental biomonitoring has emerged to provide the necessary tools to evaluate biological responses to changes in environmental conditions. While historically biomonitoring focused on contaminant concentrations in sentinel species –such as heavy metals in clams; modern biomonitoring uses information across multiple biological levels of organisation, from tissues, to organism behaviour, to the abundances and distributions of species. Since it is impossible to assess every aspect of an ecosystem’s response to pollution, scientists and practitioners still need to make decisions about which elements of an ecosystem should be monitored.

A coal miner with a canary –the classic sentinel species (url for photo: http://www.academia.dk/Blog/wp-content/uploads/CanaryInACoalMine_2.jpg)

In freshwater systems, diatoms are often the preferred organisms for monitoring since they have high diversity and diatom communities are structured strongly by local environmental conditions. Because of their long use in biomonitoring, freshwater biologists have sensitivity and indicator values for thousands of diatom species. Thus, in principle, you should be able to sample diatom communities in lakes and rivers of interest, and then assess the water quality based on the presence and abundance of different diatom species. While such proxies should always be validated and interpreted carefully (Stephens et al. 2015), there is a long and successful history of using diatoms for environmental monitoring.

Image of diatoms from a scanning electron microscope. (By Kostas Tsobanoglou - Own work, CC BY-SA 4.0, https://commons.wikimedia.org/w/index.php?curid=45315566)

The difficulty in practice is to identify diatom species, which requires expert training and can be time consuming. A number of researchers have pursued proxies and surrogates, for example using life form (e.g., diatom shape) or higher taxonomic groupings, instead of identifying species (Wunsam, Cattaneo & Bourassa 2002). In a recent article in the Journal of Applied Ecology, Francois Keck and colleagues (Keck et al. 2016) take this one step further, by using diatom evolutionary relationships as the biomonitoring tool.

Keck et al. employ novel statistical methods to create clusters of species based on their evolutionary relatedness from a phylogenetic tree and species’ sensitivity to pollution and show that these clusters, when delineated by short to moderate phylogenetic distances, do a good job of replicating species-level community pollution sensitivity indices.

This may seem like a onerous task, to assign diatoms to a correct position on a phylogenetic tree, but with the availability and now widespread use of DNA barcoding techniques, it is becoming easier to get genetic data for microscopic assemblages than to identify cells to species. This means that samples can be fit to the phylogenetic clusters without needing to shift through samples. Further, if species are observed, which have not been properly assessed for their sensitivity, they can be assigned an expected sensitivity value based on their relatedness to assessed species.

The phylogenetic tree and species’ sensitivities (Fig. 2 in Keck et al.).

While diatom evolutionary history may not have been strongly influenced by environmental pollutants in the past –because they are relatively recent stressors; it is clear from Keck et al.’s results that closely related species are similarly sensitive to pollution. Other fields of applied management have also begun to incorporate evolutionary history in the design and assessment of applied actions –for example, restoration (Hipp et al. 2015). Evolutionary history can provide important insights and management tools for dealing with the consequences of environmental change.

References

Hipp, A.L., Larkin, D.J., Barak, R.S., Bowles, M.L., Cadotte, M.W., Jacobi, S.K., Lonsdorf, E., Scharenbroch, B.C., Williams, E. & Weiher, E. (2015) Phylogeny in the Service of Ecological Restoration. American Journal of Botany, 102, 647-648.

Keck, F., Bouchez, A., Franc, A. & Rimet, F. (2016) Linking phylogenetic similarity and pollution sensitivity to develop ecological assessment methods: a test with river diatoms (microalgae). Journal of Applied Ecology.

Stephens, P.A., Pettorelli, N., Barlow, J., Whittingham, M.J. & Cadotte, M.W. (2015) Management by proxy? The use of indices in applied ecology. Journal of Applied Ecology, 52, 1-6.

Wunsam, S., Cattaneo, A. & Bourassa, N. (2002) Comparing diatom species, genera and size in biomonitoring: a case study from streams in the Laurentians (Quebec, Canada). Freshwater Biology, 47, 325-340.

The Toronto Salmon Run

Guest Post by Sara Bowman, currently enrolled in the Professional Masters of Environmental Science program at the University of Toronto-Scarborough

The Toronto Salmon Run

Toronto has been called a lot of things, but I think my favourite is “A City Within a Park”. Between High Park, the Rouge, and countless other parks based around our river systems, there are so many opportunities for people to connect with nature and forget they live in a city that is 2.6 million people strong. Despite my frequent excursions into the parks of Toronto, I still will often see something new that spurs a whole whack of questions and excitement about the area I call home.

Case in point: the salmon run! Cycling to work on October 13th I was lucky enough to witness my very first salmon run along the Don River, between Sheppard and Finch. You couldn’t help but notice the nearly 2 foot long fish struggling northward against the current, especially when a few individuals would have a violent encounter followed by swimming speedily away. I whipped out my cell phone and took as many videos and pictures as I could without being late to work. All throughout my shift questions started cycling through my head. Where in the river do the fish spawn? How many types of salmon are in Lake Ontario? Where did they come from? How are they faring from a conservation perspective? In no particular order, here are some answers I found to these questions!

Photo Credit: Tony Bock, The Toronto Star

First of all – I think my salmons were Chinook, which is the largest of the Pacific Salmons[1]. Chinook Salmon were intentionally introduced to Lake Ontario some time in the 1960s (Coho Salmon, another Pacific Salmon species, was introduced at around the same time), mainly for sport fishing, and as a bio-control for non-native fishes[1]. Their introduction was also important for essentially replacing the native Atlantic Salmon and Lake Trout, which were the top predators[1]. Atlantic Salmon were extirpated from Lake Ontario in the late 1800s due to fishing pressures, and today programs like Bring Back The Salmon are undertaking re-introduction efforts, and also habitat restoration and public outreach so that extirpation doesn’t just happen again[2].

Although thousands of individuals of Chinook are stocked in Lake Ontario every year, it is believed that natural reproduction occurs, and that they are well on their way to becoming naturalized[1]. In an ocean system, Chinook Salmon migrates up streams (the ones where they were born) from the Pacific Ocean to mate and lay eggs (spawn). Once they have spawned, they die, unlike the Atlantic Salmon which makes the trip back down to the Ocean after spawning[3]. The adult female will choose a site to make her “redd” (essentially a nest for the fish eggs) based on the water velocity and depth, and on the composition of the substrate, which should be gravel[3]. At first I was confused about how the fish managed to get so large in just a year, but it turns out that once they hatch after 3-5 months, they can spend up to 2 years in the streams where they undergo certain changes to prepare them for salt-water life[3]. Once they are back in the Pacific, they will stay there to feed and grow for up to six years[3]!

Lake Ontario is home to seven species of fish in the family Salmonidae, of which only 3 are native: the Atlantic Salmon, the Lake Trout, and the Brook Trout[1]. The Brown Trout, Chinook Salmon, Rainbow Trout, and Coho Salmon were all introduced[1].  My first thought, and this may be yours to, is how Atlantic Salmon could be considered native to Lake Ontario – after all “Atlantic” is in their name, and the distance between the Atlantic and Lake Ontario is pretty far, even for a determined migrating fish. So how did the fish get into our lakes? The Ice Age. The last one ended about 12,000 years ago, and Toronto was under about a kilometer or two of ice. When the glaciers retreated northward, basins were carved into the land and were filled with the melted water, and because of all the extra water from the ice, the St. Lawrence connection between the lake and the ocean was stronger[4]. Because the Atlantic Salmon had some freshwater adaptations for when it was spawning, it was able to naturalize to its new all freshwater environment[1].

National Oceanic and Atmospheric Association, 1999 

As the 2012 Fishes of Toronto report explains, as settlement around Lake Ontario and its streams increased in the 1800s and 1900s, the river temperatures increased, erosion increased, pollution from sewage increased, and physical structures blocking migration like dams were built. This would ultimately result in the local demise of the species from Lake Ontario.  Luckily, as I mentioned above, restoration efforts are under way to restore Atlantic Salmon populations. I wondered whether or not here might be some detrimental effects on any of the salmonid populations when or if Atlantic Salmon makes a come back, but a study in Ecology of Freshwater Fish from 2012 by Jessica Van Zwol and others found that a mix of Atlantic Salmon, Brown Trout and Rainbow Trout in stream breeding grounds did not significantly impact productivity[5]. Lake Trout is another native of Lake Ontario that suffered major population declines. In the 1970s some restoration efforts were began, but today the population has to be maintained by fish reared in a hatchery – the amount of natural reproduction occurring is not enough to prevent the species from extirpation[2].  

What can we do to ensure the future of these top open-water predators in Lake Ontario? For starters, we can be more conscious of what we are putting down our drains – it leads to the rivers and can pollute them. Be aware of proper chemical disposal. You can engage in tree planting programs along riverbanks to help prevent erosion. You can even help with salmon hatchery programs and habitat restoration to help give the populations a boost so that they can maintain their ecological roles, and be around for fishers to fish for generations to come.

Thanks for reading!!

References

1.Fishes of Toronto: A Guide to Their Remarkable World. City of Toronto, 2012. URL: 
https://www1.toronto.ca/City Of Toronto/Toronto Water/Files/pdf/F/Fishes of TO_PRINT_Feb23%5B1%5D.pdf
2. Lake Ontario Atlantic Salmon Restoration Program. Bring Back the Salmon Lake Ontario. 2013. URL:  http://www.bringbackthesalmon.ca/?page_id=12 
3. Chinook Salmon. NOAA Fisheries. Updated May 14, 2015. URL: http://www.nmfs.noaa.gov/pr/species/fish/chinook-salmon.html 
4. About Our Great Lakes: Background. National Oceanic and Atmospheric Administration. 
[U.S. Army Corps of Engineers and the Great Lakes Commission] Published 1999. URL: 
http://www.glerl.noaa.gov/pr/ourlakes/background.html 
5. Van Zwol, J., Neff, B., Wilson, C. 2012. The effect of competition among three salmonids on dominance and growth during the juvenile life stage. Ecology of Freshwater Fish. 21: 533-540. Accessed online: http://publish.uwo.ca/~bneff/papers/Van Zwol et al_Salmonid Dominance.pdf

Should we still be testing neutral theory? If so, how?

Siepielski, A.M. , Hung, K-L., Bein, E.E.B, McPeek, M.A. 2010. Experimental evidence for neutral community dynamics governing an insect assemblage. Ecology. 91. 847-857

For many ecologists, neutral theory was a (good/bad, you choose) idea that dominated ecology for the last decade but failed to provide the burden of empirical proof necessary for its acceptance. Even its creator Stephen Hubbell  recently suggested that the controversial hypothesis is no longer a plausible description of community structure, going as far to say that it is “good starting point”, a “valuable null model”, and a “useful baseline” (in Etienne et al 2011). 

But ideas, when they’re shared, are no longer the sole property of their creators. Other researchers continue to study neutral theory, and despite the apparent consensus that neutral theory is not an important explanation of community structure and dynamics, papers testing neutral theory continue to be published. This leads to an important question: do we still want to test for neutral dynamics? And if we do, how should we approach it, given what we have learned from the past decade of strawman arguments and using pattern-based evidence for processes (e.g. looking at species-area relationships and species abundance distributions)? What empirical evidence would provide strong support for the predictions of neutral theory?

Damselfly larvae
(http://www.uta.edu/biology/robinson/odonate_research.htm)

In “Experimental evidence for neutral community dynamics governing an insect assemblage”, Siepielski et al. (2010) attempt to provide a more rigorous test of neutral theory using two Enallagma (damselfly) larvae. Siepielski et al. focus on changes in demographic rates (growth, mortality) in response to changes in species relative and total abundances. In particular, they predicted that if niche differences drive coexistence, increasing a species’ relative abundance should drive lower growth rates and higher mortality, since that species is above its equilibrium; lowered relative abundances should result in higher growth rates and lowered mortality since the species is below its equilibrium density. As a result, species should return to their equilibrial abundances. Raising the total abundances but leaving the relative abundances untouched should have similar demographic responses across species and have no effect on the relative abundances. In contrast, neutral theory predicts that if all species are equal, their demographic rates depend on the density of the entire group (total abundance) and not on each individual species’ relative abundance. Therefore the response of demographic rates to changes in species relative abundances, while the total abundance is held constant, should provide support to either neutral or niche theory.

For two Enallagma sp. larvae Siepielski et al. used cages in the littoral zone of lakes, with cages receiving different treatments of relative abundance and/or total abundance manipulation. The result of these manipulations were that replicates with increased total abundances and constant relative abundances had lowered per-capita growth rates, while replicates with manipulated relative abundances and constant total abundances showed no change in demographic rates. Both species had similar mortality rates across the experimental treatments, although their growth rates differed slightly. From these results, Siepielski et al. concluded that these species are ecologically equivalent.

One of the reasons work (such as this) from Mark McPeek’s lab is interesting is because he is an outlier: someone whose work is deeply rooted in a natural system, and yet who also argues that ecological equivalency seems plausible, and attempts to support that argument. Regardless of whether the Enallagma species are in fact ecologically equivalent, this paper provides an example of how coexistence theory can be more rigorously tested than simply observing species co-ocurrences and concluding species coexistence. Further, it provides some interesting discussion about whether ecological equivalency is possible within functional groups, with niche differences occurring between functional groups (see Leibold and McPeek 2006, and from MacNaughton and Wolf 1970 for similar suggestions). Future work might focus on questions such as how to capture the effects of small niche differences, which, if balanced against very similar fitnesses could explain stable coexistence. In addition, it might be valuable to look at how resources fluctuate and how much overlap there is in resource requirements among species, when looking at how growth and mortality change with species densities.

With Adam Siepielski, Mark McPeek also published the paper “On the evidence for species coexistence: a critique of the coexistence program” about the apparently lowered standards for tests of niche-based species coexistence compared to those of neutral theory. What is certainly true is that experimental tests of coexistence theory are often less rigorous than necessary to support any coexistence theory, and should strive to take a more rigorous approach. If nothing else, this will allow criticism of particular theories to focus on the ideas themselves, rather than on how those ideas were tested.