Studying Frankenstein: what can we learn from novel ecosystems?

There's been some discussion going around ecolog about an article telling the ecological story of Ascension Island. I should note that the original article is not a great example of science writing; it tries to create conflict that doesn’t exist and lacks a reasonable understanding of ecological theory. There are a couple linked chapters/publications about Ascension Island that make better additions to the story though (1, 2).

Ascension Island is one of those tiny islands first visited by Europeans in the 1600s. Like many young, small, isolated islands (1200 mi to the next nearest island), it was highly depauperate (~25-30 species of plants). Like many such islands, once humans became regular visitors, new species began to make their to way Ascension. The Brits and their love of cultivating and homogenizing particularly altered the island, and they systematically introduced species calculated to provide ecosystem services, aesthetic value, and food.

As a result, Ascension Island changed strikingly – once an island with lowland deserts and a rocky, barren mountainside, the mountain is today known as Green Mountain. The originally depauperate mountain is now lush with three different vegetation zones, a large variety of plants including “banana, ginger, juniper, raspberry, coffee, ferns, fig trees, Cape Yews, and Norfolk Island pines”, and a complex cloud forest. The original article presents this as some inexplicable outcome, but frankly it seems in keeping with existing ecological ideas. Under island biogeography, if you decrease the distance from an island to the mainland (including via human-aided dispersal), diversity should increase. Given the massive number of species that were introduced, and the coddling they received to aid their establishment, heightened diversity is hardly a surprise. And though the original article suggests that shared evolutionary history is necessary for complex ecosystems, coevolution is hardly a requirement for a functioning ecosystem to develop. Species may be able to coexist despite lacking a shared history--niches may not be filled as tightly as in a long-established, coevolved community, but invasive species research in general should have taught us that novel species combinations can easily occur. Secondly, many of the introduced species on the island are from the same part of the world and likely do share evolutionary history.

The mountain before and after. From Catling & Stroud.

from Hobbs et al. 2006

I hadn't given much thought before to the concept of “novel ecosystems” and it has received little attention from the ecological literature (excepting the odd papers, and much more attention from a conservation and management angle). Ascension is a particularly striking example of how human modification leads to ecosystems which are entirely different from anything that has ever been present on the planet. Novel ecosystems have been defined in a number of ways. Generally, they are synthetic ecosystems that include conditions and combinations of organisms never before in existence, and do not depend on human maintenance to persist (as agriculture fields would). Novel ecosystems may be considered to be the outcome of abandonment of human managed systems or else the degradation of existing systems through human activities and invasion (figure). Of course there are incredibly few ecosystems that aren’t affected in some way by human activities (especially in this age of intentional and unintentional human-mediated species introductions), but it is the truly unique ones that are particularly interesting.

There are at least two ways to approach novel ecosystems. One approach is parallel with invasive species and conservation research, and in fact these research areas overlap a fair amount. This is the way in which most research on novel ecosystems seems to be framed. Novel ecosystems carry many of the same issues about making value judgments as invasive species research, and issues of management and whether novel ecosystems can or should be returned to their original state dominate. For example, the conflict between maintaining alpha (island) and gamma (global) diversity exists on Ascension Island– modern, invaded Ascension Island provides greater diversity and ecosystem functioning (erosion control, food, temperature moderation, habitat) than the original barren landscape. But the original endemic species, not surprisingly, have gone extinct or are increasingly at risk.

But focusing solely on these difficult value-laden questions seems to have been at the cost of exploring the value of novel ecosystems as a study system. The most interesting examples of novel ecosystems are not simply modified or invaded ecosystems, but ecosystems that truly never existed before. Like post-shale dump landscapes in Scotland, where the refuse from mining is now host to unique grasslands that act as refugia for locally rare species; or the San Francisco Bay, which now is utterly unrecognizable compared to historical descriptions due to heavy invasion; or urban ecosystems with their unique habitats and issues; or even the habitat and connectivity created by stone fences which now occur on most continents. The questions here aren't always about invasion and management, but instead focus on what the new community looks like. How do novel communities assemble, what processes dominate (mass effects, environmental filtering, competition, predation, etc, etc)? How does ecosystem function relate to the community that assembles? Most BEF research after all, is focused on more traditional ecosystems. What leads to stability in a novel ecosystem, or are they stable at all? They can function is an example of highly unfortunate but also highly informative ‘natural’ experiments for ecologists. But at the moment, if you search for "novel ecosystems" on Google Scholar, the title words are "management", "conservation", "restoration" or "invasion". Actually, there probably are ecologists doing work on novel ecosystems from a purely ecological perspective, but this work gets grouped with  disturbance, invasion, and urban ecology: it just remains to consider them in a more unified fashion. If the conversation remains focused only on the conservation issues (as the discussion on ecolog seemed to shift to rapidly), it just seems like we're limiting ourselves a little.

The species we’ve neglected

Species in last 3 months' papers in Ecology Letters.
"Multiple species" tended to be meta-analyses.

Browse the abstracts of a high profile ecological journal (for example, Ecology Letters, right) and one pattern you’ll notice is that high impact, hypothesis-driven ecology usually involves a small pool of focal species. Plants, for example, dominate any discussion of community ecology and have since Clements’ and Gleason’s arguments. It is not that hard to see why – plants don’t move, for one, live in speciose groups, and often complete a full lifecycle in a matter of months. They are also the lowest trophic level and so pesky multiple trophic level interactions can be omitted.

Other groups of species also show up frequently. Insects are popular for some studies of herbivory (again, it is easy to estimate damage to species that can’t move), mutualisms, and predation. Butterflies and birds, being pretty and easy to count, make a nice model for species populations and climate change studies. And while it is easy to sound critical of this kind of system-based myopia, it exists for perfectly good reasons. Immobile plants, after all, are a major source of experimental knowledge upon which much of modern ecology relies. They are easy to work with and manipulate, and their responses are relatively easy to measure (phenology, fitness, biomass, herbivory). Further, once an experimental system is established, using that system becomes increasingly attractive. You have a growing literature to base decisions on, to put your results into context, and against which to prove the novelty or importance of your work. In contrast, if you do your work on the rare bunny-toed sloth-monkey, the novelty of the system may overwhelm the generality of the work. And so the short-term limitation is that established systems allow immediate in-depth studies, while novel systems, though necessary to broaden ecological knowledge, may (initially) relatively be shallow in their returns.

Establishing a new system may be a time-consuming activity with the possibility of failure. But these under-utilized species have something new to tell ecology. This is not to say that the popular systems of species have nothing to tell us anymore – not at all, given all the complexities of ecological dynamics – but they bias the story. The ecological processes at play are not likely much different between novel systems and traditional ones. But the same processes interact in different ways and differ in importance across systems, and so we may have unrealistic expectations about the importance of, say, competition, if we only focus on 1 or 2 systems. To follow Vellend’s (2011) framework, the processes of selection, drift, speciation, and dispersal are part of any ecological system. What differs is their importance, and their importance differs for reasons related to the ecological context and evolutionary history a species experiences. This is the reason that comparing Mark McPeek’s work on neutrality in damselflies with Jonathan Losos’ findings about adaptive radiation in anoles is so interesting. No one questions that adaptive radiations may drive one set of species and neutrality another, the real question is what about their contexts produces to this result. Unfortunately, if our current set of focal species is small, we are limited in our ability to make such informative comparisons.

Many of the limitations on species have been methodological: popular systems tend to involve amenable species. Other species may be very small, very mobile, very difficult to identify, or highly specialized in their habitats. This creates difficulties. But when we overcome them, the results are often revolutionary. For example, consider the current burst of interest in belowground interactions, once their incredible importance to plant community interactions became clear (e.g. Klironomos 2002, Nature). Further, techniques are continually improving in ways which make new systems tenable.

So we should continue to focus on a few well-understood systems, attempting to perfect our understanding and predictive abilities. There is much value in understanding a system as completely as possible. But on the other hand, we can limit ourselves by focusing too much. It seems like one of the big areas for growth in modern ecology is simply to expand into novel ecological systems.

(**It's probably too general and a bit unfair to refer to all plants and all insects as though they are monolithic groups, since they are each large and varied (which is part of the reason they've been useful thus far). And some of their great representation may in fact relate to the number of species available to study. But I do think the general point about the problem of focusing too much holds.**)

Everything you wanted to know about peer review (but no one mentions)

Since the British Ecological Society has published an introduction to reviewing successfully, here’s a short list of additional, less noted, observations about the reviewing process.

For example, excitement for reviewing is proportional to the number of reviews you have done

• When you are first asked, reviewing feels like a great honour. It is one of the first signs that some group larger than your lab or department recognizes your existence. You will spend an unreasonable amount of time perfecting your review.

This plot would not survive peer review.

• The novelty will wear off, and your enthusiasm upon receiving a review request will decline, usually in relation to your increasing workload. 

• Sadly, the urgent need to complete a review may also wane. You will probably submit the first review early, but after that… 

Despite declines in enthusiasm, review quality usually increases with the number of reviews you have done. Practice and experience make a difference. It is also a confidence boost to see your suggestions actually instituted and valued by the authors or editors.

Manuscripts fall broadly into only a few categories. They might be deeply flawed and unpublishable, and therefore easy to review; or they might be uniformly excellent and therefore easy to review. But these are the least common types you will experience. Most manuscripts have both strengths and weaknesses and fall somewhere on the spectrum between “accept” and “reject”. These are the papers that take the most time, since you must weigh the flaws against the strengths, agonize over what changes to suggest, what suggestions might get them around the biggest issues, and what recommendation to give the editor. It’s also easy to fall into Monday morning quarterbacking and make impractical suggestions - why didn’t you design your experiment like this? Why didn’t you measure that? While these points might be reasonable and relevant, but it is important to be clear as to what is within the scope of a revision and what is a bigger picture problem.

Reviewing is of course an important service to ecology. It can also makes a number of subtle contributions to your own professional development. Once the novelty of someone caring about your opinion has worn off, the best part of reviewing may be things you don’t expect.

• For example, one of the best parts of reviewing a paper in the same area as your research is seeing what literature the authors cite and how they cite them– some real gems you've missed can show up. 

• Reviewing a paper that falls so exactly in your body of knowledge that you feel completely qualified is a great feeling. It’s nice to be reminded that you have (mostly) mastered a topic you care about.

• When you are asked to review a paper that combines some topic or method you are well-versed in with ideas or systems or methodologies you are not familiar with, it can be truly eye opening. The funnest papers to review are the ones where you think “I never thought of that!”.

• Reviewing can give you the clarity to recognize the weaknesses in your own work.

Quotes that stick. #INT13

I'm back in Toronto now, and here are some quotes from talks that have really stuck with me. INTECOL was a great meeting, it was very interesting to hear about all the research from around the world. I hope all the attendees had a great time.

Sandra Diaz: “We just don't know enough to understand how functional diversity links to environmental change and ecosystem services.”

Erika Edwards: “big phylogeny, big trait data set analyses leave me feeling a little empty”

Erika Edwards: “carbon economy is part of the whole organism, not single traits.”

Joel Cohen: “Mathematics is like sex, you can talk about it but you shouldn't do it in public.”

Enrique Chaneton, Describing what happen during a study looking at the effects of grazing on ecosystem decomposition rates: “A volcano erupted during the study and sometimes shit happens, ….. the volcano killed many of the cattle.”

Carsten Meyer, Talking about global data availability in large databases: “Countries that under report are large emerging economies (china, India, Brazil, Russia) which could finance these efforts but for some reason do not.”

Ove Hoegh-Guldberg, ‘To get change we need to reach more than the brain, but the human heart”

INTECOL & the future of community ecology for infectious diseases – August 21st 2013 - #INT13

This year's conference has a strong focus on infectious disease which included today's symposium Community ecology for infectious diseases organized by Joanne Lello.

Throughout the symposium a great deal of interesting questions related to host-parasite interactions being addressed with a diverse set of methods ranging from the mathematical biology of Andy Dobson, to the experimental C. elegans / pathogenic bacteria systems of Olivier Restif and Gregg Hurst, the wild rodent systems of Heike Lutermann, Andy Fenton, and Owen Petchey, and the next generation molecular techniques employed by Serge Morand.

However, it was Robert Poulin the keynote speaker who set the theme of the symposium to which many of the speakers kept returning: What are the future directions of parasite community ecology? Dr. Poulin began the session with an overview of the recent trends in parasite ecology over the last few decades and Lawton's view that community ecology is a mess (Oikos 1999 – 84: 177-192). The initial research done on host-parasite interactions was centred within the one host – one parasite framework, often dealing solely with the effect of the parasite on its host. This was then expanded to the one host – multi-parasite level, often investigating drivers of parasite species richness among hosts via comparative analyses and occasionally extending to parasite-parasite interactions though the use of null models. Although the data were available beforehand, only recently has the field moved into the domain of multi-host – multi-parasite interactions, now focusing on questions of infection dilution, meta-analyses of parasite richness, and describing the networks of interactions within these communities.

Looking ahead into the future of this discipline, Poulin suggested that researchers should expand beyond simple topological networks of associations to include the strength of interactions, potentially via energy flow, and the use of network analyses on smaller scales using individual hosts. Serge Morand also highlighted the need to develop and incorporate parasite phylogenies into these multi-host - multi-parasite communities. His talk highlighted recent advances in next generation sqeuenceing and how these techniques can be applied to parasite communities. One obvious advantage is that through molecular phylogenetics researchers will be able to define and quantify a higher degree of parasite diversity, but additionally molecular markers can be used to uncover unexpected host diversity or identify species that may be difficult to distinguish through traditional taxonomic keys. Morand continued to press the application of new techniques in immunogenetics and the integration of methods in molecular epidemiology with the theory of transmission and community ecology.

Finally Andy Dobson posited that in addition to pressing forward with our research into infectious disease, it is imperative that contemporary researchers revist the “best hits” of the past and address important issues that have fallen to the wayside. Primarily Dobson pointed out that mathematically, aggregation and virulence of parasites have been shown as important factors for determining parasite co-existence. However, the concept of aggregation is often left out of contemporary discussions although it will be important to determine natural forms of the aggregation distribution and also to attempt to make the link between immunity and aggregation of parasites in a multi-host – multi-parasite community.

Whether incorporating novel molecular and statistical techniques, exploring previously unstudied model systems, or revisiting the context of contemporary research, it is clear that community ecology and infectious disease has a promising future and that it has progressed greatly from the mess Lawton made it out to be in 1999.

INTECOL day 2: Plenaries to rock you. #INT13

Today I had a number of journal related obligations (for the Journal of Applied Ecology -which is celebrating its 50th anniversary here at the conference) and I had time to attend just a few talks. I saw some great talks -especially by Tad Fukami on evolutionary priority effects, but I decided to only post my (inadequate) notes about two of the plenary talks today. They were great talks, and both of them really expanded my perception of human-caused effects on natural systems, in very different types of habitats. 

Ove Hoegh-Guldberg. Corals reefs and global climate change. Coral reefs occupy less that one percent of ocean area but one in four fish caught come from reefs, supporting 400 million people. In the Caribbean coral cover has drastically declined from 80 percent cover to about 10 percent. This has happened elsewhere too, Asia and Australia. In Australia, where coral reefs are well protected and financed, they are still declining. Human development, pollution from agriculture and over harvesting are the common local causes, but global warming and ocean acidification are major global changes. Marine systems are greatly warming, more than land, but very few studies in marine systems. Increases in sea temperature can result in mass coral bleaching and death of corals. Major bleaching events over the past two decades, killing significant proportions of coral. Even though temperature is the best predictor of bleaching, mortality is more variable and other factors may help corals recovery, and these other factors are what managers can influence. In the coming decades, warming temperatures will mean common widespread bleaching events, with some areas becoming too warm for corals. Based on large mesocosms that track local ocean temperature and co2 concentrations. With warming, the mesocosm reefs change into algal dominated systems, with fewer other types of species (e.g., sea cucumbers). Two scenarios to deal with climate change -mitigate or adapt. We need to mitigate within twenty years, reduce co2 emissions. To get change we need reach more than the brain, but the human heart. Partnered with Google to have street view for reefs (this is completely awesome -check it out here). This initiative is both science (mapping reefs) and important outreach, letting people experience diving. One billion people have visited with almost two million people 'dived' in the first week.

Nancy Grimm. Water systems in urban habitats. Populations around the world are moving to cities, and projections have over 650 cities with over a million people by 2025. Creates multiple stressors in urban ecosystems, and there is a new need to build knowledge capacity. Large proportions of people already live in urban areas with limited water supply, quality and delivery capacity. Eighty percent of the population lives in areas under threat of water scarcity, but some people have access to technological solutions that minimize this (e.g., arid USA). For others, ecological knowledge may help reduce this threat. Areas around the world are experiencing more heavy rainfall and flooding. The way municipalities deal with storm water is building hard channels and surfaces, but building ecological systems can better handle water and pollution. In the arid southwest, there are opportunities to retain storm water in semi-natural systems. Provides ecosystem services and denitrification.

Sorry for the brevity of the talk summaries -I'm working on a very full schedule!