Reclaiming contaminated land through manipulating biodiversity

Contents of this post originally appeared on the Applied Ecologist, but with expanded thoughts here.

Five years ago I spent my sabbatical in China and worked closely with a lab in Guangzhou. While there, I built meaningful collaborations and friendships that have continued to advance the science I'm involved with. While in China, I accompanied my friend, Jin-tian Li to a biodiversity field experiment on contaminated post-mining lands in Hunan province, and our discussions led to the just-published paper (please e-mail me if you want a copy) in the Journal of Applied Ecology, first-authored by a former PhD student in my lab, Pu Jia.

Why do we care about degraded lands?

According to the IPBES report on land degradation, the degradation of productive lands and intact habitats is a major threat to sustainability, biodiversity and ecosystem functioning globally, which reduces the resiliency of ecological and economic systems. In many emerging economy countries, environmentally harmful practices that result in contamination render lands and habitats seriously degraded. In many circumstances, the restoration of contaminated habitats to original conditions is not an option because the capacity for these habitats to harbor intact native ecosystems is greatly compromised. In these cases, we need management options that allow us to reclaim contaminated and degraded lands (Nathanail & Bardos 2005), and preferably ones that increase biodiversity and ecosystem function (Rohr et al. 2016).

The potential role of biodiversity in reclaiming contaminated lands

While the ecological literature on the linkages between biodiversity and ecosystem function is vast and rich (e.g., Tilman, Isbell & Cowles 2014), the application of this field of research to reclaiming contaminated lands has been strangely depauperate, and so there’s little guidance on whether we should be planting diverse plant assemblages on contaminated lands, or if we ought to simply plant the most productive species or those that provide efficient phyto-removal of contaminants. This question is of fundamental importance to places like China, where rapid development and industrialization through the 1970s-1990s resulted in severe contamination of lands near mining and mineral processing facilities (Li et al. 2019), and now with China’s commitment to improving it’s environmental health, biodiversity research has the ability to impact policy and management at a national scale.

Our paper

We evaluated whether more diverse plantings increased reclamation and ecosystem functioning of a mine wasteland in Hunan Province, China, which had been severely contaminated with cadmium and zinc over decades. We sowed plots with 1-16 species and these were selected from the herbaceous species that grew around contaminated sites in the region, and more diverse assemblages produced more biomass and were more stable over time. Further, there was less heavy metal contamination of leaf tissues in the more diverse plantings, which reduces the impact on herbivores.

Importantly though, plant diversity spurred plant-soil feedbacks (PSFs) that appeared to drive the increased ecosystem functioning. Higher plant diversity supported higher soil bacterial and fungal diversity. Importantly, higher plant diversity was accompanied with more soil cellulolytic bacteria that exude enzymes that degrade cellulose and so drive decomposition and nutrient cycling, which are essential components of a functioning ecosystem. 




Furthermore, the multi-species assemblages also performed better because these high diversity treatments harboured fewer soil fungal pathogens (and by extension more beneficial soil fungi). This appeared to be driven by the fact that high plant diversity supported a greater diversity of soil chitinolytic bacteria that produce anti-fungal enzymes that degrade the chitin in cell walls of soil-borne plant-pathogenic fungi.

In the search for efficient ways to reclaim contaminated lands, sowing high-diversity plant assemblages appear to be an effective tool. The key for reclamation is to ensure that soil processes like decomposition and nutrient cycling are able to support a self-sustaining ecosystem, and higher plant diversity can ensure this. The next steps will be to field test this in real reclamation projects and to see this research work its way into best practices.

Li, T., Liu, Y., Lin, S., Liu, Y. & Xie, Y. (2019) Soil pollution management in China: a brief introduction. Sustainability, 11, 556.

Nathanail, C.P. & Bardos, R.P. (2005) Reclamation of contaminated land. John Wiley & Sons.

Rohr, J.R., Farag, A.M., Cadotte, M.W., Clements, W.H., Smith, J.R., Ulrich, C.P. & Woods, R. (2016) Transforming ecosystems: when, where, and how to restore contaminated sites. Integrated Environmental Assessment and Management, 12, 273-283.

Tilman, D., Isbell, F. & Cowles, J.M. (2014) Biodiversity and ecosystem functioning. Annual Review of Ecology, Evolution and Systematics, 45, 471-493.

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Moving on up to the regional scale

Like the blind men and the elephant, perspective drives understanding in ecology. The temporal and spatial scale of analysis (let alone the system and species you focus on) has major implications for your conclusions. Most ecologists recognize this fact, but consider only particular systems, scales or contexts due to practical limitations (funding, reasonable experimental time frames, studentship lengths). 

Ecologists have long known that regional processes affect local communities and that local processes affect regional patterns. Entire subfields like landscape ecology, metapopulations, metacommunities, and biogeography (species area relationships) highlight these spatial dependencies. But high-profile ecological research into biodiversity and ecosystem functioning ('BEF') primarily considers only local communities. Recently though, the literature has started to fill this gap and asking what BEF relationships look like at larger spatial scales, and how well local BEF relationships predict those at larger spatial scales.

'Traditional' BEF experiments were done at relatively small spatial scales (often only a few meters^2). Positive BEF relationships were commonly observed, but often were quite saturating – that is, only a few species were necessary to optimize the function of interest. If the impact of biodiversity saturates with only a few species, it would seem that surprisingly few species are necessary to maintain functioning. True, studies that considered multiple ecosystem functions are more likely to conclude that additional diversity is required for optimal functioning (e.g. Zavaleta et al. 2010). But a simplistic evaluation of the facts that a) ecosystem functioning rapidly saturates with diversity, and b) locally, diversity may not be generally decreasing (Vellend et al. 2017), could lead to overly confident conclusions about the dangers of biodiversity loss. Research on BEF relationships, as they transition from local to larger spatial scales, is increasingly suggesting that our understanding is incomplete, and that BEF relationships can grow stronger at large spatial scales.

A number of recent papers have explored this question, and in considering the essential role of spatial scale. Predictions about how BEF relationships will change with spatial scale vary. On one hand, in most systems there are only a few dominant species and these species may disproportionately contribute to ecosystem functions, regardless of the spatial scale. On the other hand, species-area relationships tend to increase rapidly at small scales, as community composition turns over. If that is the case, then different species may make important contributions in different places. Winifree et al. (2018) contrasted these predictions for three crop species that rely on natural bee pollinators (cranberries, blueberries, and watermelons). They censused pollinators at 48 sites, over a total extent of ~3700 km^2. Though at local scales very few bee species were required to reach pollination goals, the same goals at larger spatial scales required nearly an order of magnitude more bee species. These results in particular appeared to be driven by species turnover among sites--perhaps due to underlying environmental heterogeneity.

From Winifree et al. "Cumulative number of bee species required to maintain thresholds of 25% (orange), 50% (black), and 75% (purple) of the mean observed level of pollination, at each of n sites (16). Horizontal dashed lines indicate the total number of bee species observed in each study. Error bars represent 1 SD over all possible starting sites for expanding the spatial extent. For all three crops combined, each x-axis increment represents the addition of one site per crop".

Another mechanism for increased BEF at larger scales is insurance effects. The presence of greater diversity can interact with spatial and temporal environmental variation to increase or stabilize ecosystem functioning. Greater diversity should maximize the differential responses of species to changing conditions, and so buffer variation in ecosystem functioning. Such effects, when they occur through time are temporal insurance, and when they occur via dispersal among sites, spatial insurance. Wilcox et al. (2018) considered the role of synchrony and asynchrony among populations, communities, and metacommunities to ask whether local asynchrony affected stability (see Figure below for a nice conceptual explanation). Across hundreds of plant data sets, they found that asynchrony of populations did enhance stability. However, the degree to which it affected stability varied from very weak to very important (e.g. by 1% to 300%). Maximizing species or population differences at local scales apparently can have implications for dynamics, and so potentially stability of functioning, at much larger scales.

From Wilcox et al. "Conceptual figure showing how stability and synchrony at various spatial scales within a metacommunity combine to determine the stability of ecosystem function (here, productivity). In (a), high synchrony of species within and among local communities results in low stability at the scale of the metacommunity. In (b), species remain synchronised within local communities, but the two communities exhibit asynchronous dynamics due to low population synchrony among local patches. This results in relatively high gamma stability. Lastly, in (c), species exhibit asynchronous dynamics within local communities through time, and species-level dynamics are similar across communities (i.e. high population synchrony). This results in relatively high gamma stability. Blue boxes on the right outline stability components and mechanisms, and the hierarchical level at which they operate. Adapted from Mellin et al. (2014)."

Finally, Isbell et al. (2018) describe ways in which ecosystem functioning and other contributions of nature to humanity are scale-dependent, laying out the most useful paths for future work (see figure below).

From Isbell et al. 2018.

These papers make nearly identical points worth reiterating here: 1) we have done far too little work beyond the smallest spatial scales (~3 m^2) and so lack necessary knowledge of the impacts of losing of biodiversity, and 2) policy decisions and conservation activities are occurring at much larger scales – at the scale of the park, the state, or the nation. Bridging this gap is essential if we are to make any reasonable arguments as to why ecosystem function figure into  large-scale conservation activities.

References:
Sustaining multiple ecosystem functions in grassland communities requires higher biodiversity. Erika S. Zavaleta, Jae R. Pasari, Kristin B. Hulvey, G. David Tilman. Proceedings of the National Academy of Sciences Jan 2010, 107 (4) 1443-1446; DOI: 10.1073/pnas.0906829107. 

Plant biodiversity change across scales during the Anthropocene. Vellend, Mark, et al. Annual review of plant biology 68 (2017): 563-586.

Species turnover promotes the importance of bee diversity for crop pollination at regional scales. RACHAEL WINFREE, JAMES R. REILLY, IGNASI BARTOMEUS, DANIEL P. CARIVEAU, NEAL M. WILLIAMS, JASON GIBBS. SCIENCE16 FEB 2018 : 791-793

Asynchrony among local communities stabilises ecosystem function of metacommunities. Kevin R. Wilcox, et al. Ecology Letters. Volume 20, Issue 12, Pages 1534–1545.

Isbell, Forest, et al. "Linking the influence and dependence of people on biodiversity across scales." Nature 546.7656 (2017): 65.

Progress on biodiversity-ecosystem function requires looking back

Williams, L. J., et al. 2017. Spatial complementarity in tree crowns explains overyielding in species mixtures. - Nature Ecology & Evolution 1: 0063.

It seems at times that the focus on whether biodiversity has a positive relationship with ecosystem functioning has been a bit limiting. Questions about the BEF relationships are important, of course, since they support arguments for protecting biodiversity and suggests a cost of failing to do so. But as a hypothesis ('higher diversity is associated with higher functioning'), they can be rather one-dimensional. It's easy to think of situations in which other types of BEF relationships (neutral, negative) exist. So is it enough to ask if positive BEF relationships exist?

It’s nice then that there is increasingly a focus on identifying mechanisms behind BEF relationships, using both theory and empirical research. A new paper along these lines is “Spatial complementarity in tree crowns explains overyielding in species mixtures” from Laura Williams et al. (2017). "Overyielding" is the phenomenon in which greater total biomass is produced in a mixture of species compared to the expectation based on their biomass production in monoculture. Overyielding would suggest a benefit in maintaining polycultures, rather than having monocultures, and is a common response variable in BEF studies.

This study focused on the production of stem biomass in monocultures vs. polycultures of forest trees. Experimental communities of young tree species were planted with orthogonal gradients of species richness and functional richness, allowing the effects of species number and trait diversity to be disentangled. Complementarity in tree canopy structure in these communities may be an important predictor of overyielding in stem biomass. Complementarity among tree crowns (that is, the extent to which they fit together spatially without overlapping, see Fig below) should reflect the ability of a set of species to maximize the efficiency of light usage as it hits the canopy. Such variation in crown canopy shapes among species could lead to a positive effect of having multiple species present in a community. 

Example of crown complementarity.
From Williams et al. 2017.

To test this, the authors estimated crown architecture for each species using traits that reflect crown shape and size. These measures were used to predict the spatial complementarity expected with different combinations of tree species. In addition, a single integrative trait – maximum growth rate – was measured for each species. The authors hypothesized that the variation in growth rate of species in a community would be associated with variation in crown heights and so also a good predictor of overyielding.

They found that crown complementarity occurred in nearly all of the experimental polycultures and on average was 29% greater in mixtures than monocultures. Controlling for the number of species, communities with greater variation in growth rate did in fact have greater crown complementarity, as predicted. Further, higher levels of crown complementarity were strongly associated (R2~0.6) with stem biomass overyielding.

Fig 2&3 from Williams et al (2017). For experimental communities:
a) the relationship between crown complementarity and variation in growth rate.
b) the relationship between crown complementarity and stem biomass overyielding.

These results provide a clear potential mechanism for a positive effect of biodiversity (particularly trait-based variation) in similar forests. (As they state, "We posit that crown complementarity is an important mechanism that may contribute to diversity-enhanced productivity in forests"). Given the importance of the sun as a limiting resource in forests, the finding that mixing species that combining shade intolerant and shade tolerant strategies are more productive (the authors note that "growth rate aligns with shade tolerance and traits indicative of a tree’s resource strategy") is not necessarily surprising. It fits within existing forestry models and practices for mixed stands. This is a reminder that we already understand many of the basic components of positive (and neutral and negative) diversity-functioning relationships. The good news is that ecology has accumulated a large body of literature on the components of overyielding (limiting resources, niche partitioning, evolution of alternate adaptive strategies, constraints on these, the strength of competition, etc). From the literature, we can identify the strongest mechanisms of niche partitioning and identify the contexts in which these are likely to be relevant. For example, sun in forests and canopy complementarity, or water limitation in grasslands and so root complementarity might be a good focal trait. 

When is the same trait not the same?

Different clades and traits yield similar grassland functional responses. 2016. Elisabeth J. Forrestel, Michael J. Donoghue,  Erika J. Edwards,  Walter Jetz,  Justin C. O. du Toite, and Melinda D. Smith. vol. 114 no. 4, 705–710, doi: 10.1073/pnas.1612909114

A potential benefit of trait-centric approaches is that they may provide a path to generality in community ecology. Functional traits affect growth, reproduction, and survival, and so--indirectly--should determine an organism's fitness; differences in functional traits may delineate niche differences. Since fitness is dependent on the environment, it is generally predicted that there should be strong and consistent trait–environment relationships. Species with drought-tolerant traits will be most dominant in low precipitation regions, etc, etc. Since productivity should also relate to fitness, there should be strong and consistent trait–ecosystem functioning relationships.

There are also quite general descriptions of species traits, and the life histories they imbue (e.g. the leaf economic spectrum), implying again that traits can yield general predictions about an organism's ecology. Still, as McIntyre et al. (1999) pointed out, "A significant advance in functional trait analysis could be achieved if individual studies provide explicit descriptions of their evolutionary and ecological context from a global perspective."

A new(ish) paper does a good job of illustrating this need. In Forrestel et al. the authors compare functional trait values across two different grassland systems, which share very similar environmental gradients and grass families present but entirely different geological and evolutionary histories. The North American and South African grasslands share similar growing season temperatures and the same precipitation gradient, hopefully allowing comparison between regions. They differ in grass species richness (62 grass species in SA and 35 in NA) and species identity (no overlapping species), but contain the same major lineages (Figure below).

From Forrestel et a. Phylogenetic turnover for major lineages along a
precipitation gradient differed between the 2 regions.

Mean annual precipitation (MAP) is well-established as an important selective factor and many studies show relationships between community trait values and MAP. The authors measured a long list of relevant traits, and also determined the above ground net primary productivity (ANPP) for sites in each grassland. When they calculated the community weighted mean value (CWM) of traits along the precipitation gradient, for 6 of the 11 traits measured region was a significant covariate (figure below). The context (region) determined the response of those traits to precipitation.

From Forrestel et al.

Further, different sets of traits were the best predictors of ANPP in NA versus SA. In SA, specific leaf area and stomatal pore index were the best predictors of ANPP, while in NA height and leaf area were. The upside was that for both regions, models of ANPP explained reasonable amounts of variation (48% for SA, 60% for NA).

It's an important message: plant traits matter, but how they matter is not necessarily straightforward or general without further context. The authors note, "Instead, even within a single grass clade, there are multiple evolutionary trajectories that can lead to alternative functional syndromes under a given precipitation regime" 

The pessimistic and optimistic view of BEF experiments?

The question of the value of biodiversity-ecosystem function (BEF) experiments—their results, their relevancy—has become a heated one in the literature. An extended argument over the last few years has debated the assumption that local biodiversity is in fact in decline (e.g. Vellend et al. 2013; Dornelas et al. 2014; Gonazalez et al. 2016). If biodiversity isn't disappearing from local communities, the logical conclusion would be that experiments focussed on the local impacts of biodiversity loss are less relevant.

Two papers in the Journal of Vegetation Science (Wardle 2016 and Eisenhauer et al. 2016) continue this discussion regarding the value of BEF experiments for understanding biodiversity loss in natural ecosystems. From reading both papers, it seems as though broadly speaking, the authors agree on several key points: that results from biodiversity-ecosystem functioning experiments don’t always match observations about species loss and functioning in nature, and that nature is much more complex, context-dependent, and multidimensional than typical BEF experimental systems. (The question of whether local biodiversity is declining may be more contested between them). 

Biodiversity and ecosystem experiments typically involve randomly assembled plant communities containing either the full complement of species, or subsets containing different numbers of species. Communities containing lower numbers are meant to provide information about the loss of species diversity a system. Functions (often including, but not limited to, primary productivity or biomass) are eventually measured and analysed in relation to treatment diversity. Although some striking results have come out of these types of studies (e.g. Tilman and Downing 1996), they can vary a fair amount in their findings (Cardinale et al. 2012).

David Wardle’s argument is that BEF experiments differ a good deal from natural systems: in natural systems, BEF relationships can take different forms and explain relatively little variation, and so extrapolating from existing experiments seems uninformative. In nature, changes in diversity are driven by ecological processes (invasion, extinction) and experiments involving randomly assembled communities and randomly lost species do nothing to simulate these processes. Wardle seems to feel that the popularity of typical BEF experiments has come at the cost of more realistic experimental designs. This is something of a zero-sum argument, (although in some funding climates that may be true...). But it is true that big BEF experiments tend to be costly and take time and labour, meaning that there is an impetus to publish as much as possible from each one. Given BEF experiments have changed drastically in design once already, in response to criticisms about their inability to disentangle complementarity vs. portfolio effects, it seems they are not inflexible about design though.

Eisenhauer et al. agree in principle that current experiments frequently lack a realistic design, but suggest that there are plenty of other types of studies (looking at functional diversity or phylogenetic diversity, for example, or using random loss of species) being published as well. For them too, there is value in having multiple similar experiments: this allows metaanalysis and comparison aggregation, and will help to tease apart the important mechanisms eventually. Further, realism is difficult to obtain in the absence of a baseline for a “natural, untouched, complete system” from which to remove species.

The point that Eisenhauer et al. and Wardle appear to agree on most strongly is that real systems are complex, multi-dimensional and context-dependent. Making the leap from a BEF experiment with 20 plant species to the real world is inevitably difficult. Wardle sees this is a massive limitation, Eisenhauer et al. sees it as a strength. Inconsistencies between experiments and nature are information that highlight when context matters. By having controlled experiments in which you vary context (such as by manipulating both nutrient level and species richness), you can begin to identify mechanisms.

Perhaps this is the greatest problem with past BEF work, is that there is a tendency to oversimplify the interpretation of results – to conclude that ‘loss of diversity is bad’ but with less attention to ‘why’, 'where', or 'when’. The best way to do this depends on your view of how science should progress. 

Wardle, D. A. (2016), Do experiments exploring plant diversity–ecosystem functioning relationships inform how biodiversity loss impacts natural ecosystems?. Journal of Vegetation Science, 27: 646–653. doi: 10.1111/jvs.12399

Eisenhauer, N., Barnes, A. D., Cesarz, S., Craven, D., Ferlian, O., Gottschall, F., Hines, J., Sendek, A., Siebert, J., Thakur, M. P., Türke, M. (2016), Biodiversity–ecosystem function experiments reveal the mechanisms underlying the consequences of biodiversity change in real world ecosystems. Journal of Vegetation Science. doi: 10.1111/jvs.12435

Additional References:
Vellend, Mark, et al. "Global meta-analysis reveals no net change in local-scale plant biodiversity over time." Proceedings of the National Academy of Sciences 110.48 (2013): 19456-19459.

Dornelas, Maria, et al. "Assemblage time series reveal biodiversity change but not systematic loss." Science 344.6181 (2014): 296-299.

Gonzalez, Andrew, et al. "Estimating local biodiversity change: a critique of papers claiming no net loss of local diversity." Ecology (2016).

Tilman, David, and John A. Downing. "Biodiversity and stability in grasslands." Ecosystem Management. Springer New York, 1996. 3-7.

Cardinale, Bradley J., et al. "Biodiversity loss and its impact on humanity."Nature 486.7401 (2012): 59-67.

#ESA100 Have system -need science! The opportunities for green roof ecology

 Green roofs are now a mainstay of urban green infrastructure and a tool to promote sustainable urban development. A number of municipalities, including Toronto-where I live, now have bylaws or policies requiring green roofs on certain types of infrastructure. The rationale for these requirements is that green roofs provide direct energy savings, reduce albedo, reduce storm water runoff, and support other ecosystem functions and provide wildlife habitat. But it is these last two –the ecological benefits, though often touted, lack clear evidence. I attended an organized oral session on green roof biodiversity organized by Whittinghill, Starry and MacIvor, and it was clear from the presentations that people were excited by the opportunities for ecological research. More importantly, they made the case that we know so little about these systems, and research is desperately needed to guide policy –we simply need more ecologists working on this problem.

Chicago City Hall green roof, adapted from Wikipedia (CC-BY-SA 3.0)

I would argue strongly that urban systems, like green roofs, are understudied and that these systems are the very places that ecological concepts and theories can have relevance. My medical colleagues study human physiology or microbiology in order to cure sick people –their science has direct application to improving the world and human well being, and ecologists have the same opportunity. Like a sick patient, urban systems are where our science can have the greatest impact and can provide the most benefit. Urban systems are under direct management and provide ample opportunity to manipulate ecological patterns and processes in order to test theory and manage societal benefits.

Time to study cities!

Exploring the intersection of conservation, ecology and human well-being

I've seen a number of articles recently that explore in different way the intersection of environment and ecology, conservation and human societies. In particular, Frontiers in Ecology and Evolution (the free ESA journal you are gifted as a member) has dedicated an entire issue to the question of climate impacts on humans and ecosystems, and the papers cover important topics relating to changing climate and its effects on biodiversity, ecosystem integrity and human societies. Economic predictions suggest costs from fires, drought, and rising sea levels: whether protecting ecosystems will preserve their function and so mediate these costs to humans and other organisms is explored in depth. Of course, scholarly papers can be impersonal, but another article about the struggles of Inuit in the north to adapt (or not) to changing ecosystems provides a smaller, more human look at climate, development, and cultural change. Another study predicts that for some cultures, climate change (and the resulting difficulties growing food, maintaining livelihoods, obtaining water and human health risks) may be too much for them to withstand.

Finally, a long-form story by Paul Voosen in The Chronicle of Higher Education asks "Who is conservation for?". While not a novel question, through interviews with Gretchen Daily and Michael Soule, Voosen does a thorough job of illuminating conservation biology in the context of real-world limitations and realities, historical precedents, ongoing tensions between new and old approaches to conservation, and economic development. In the end it asks what motivates conservation: do we conserve purely for the sake of biodiversity alone, for economic and functional benefits, for aesthetic reasons, for charismatic and at-risk species? As Voosen subtly hints in the article, if leading conservation biologists can't agree on the answer, will it ever be possible to be effective?

Slightly unrelated, but there is a great short film online about the life of Alfred Russel Wallace, the less celebrated co-discoverer of natural selection.

Biodiversity and ecosystem functioning: now with more spatial scales, more functions, and more measures of diversity.

Jae R. Pasari, Taal Levi, Erika S. Zavaleta, and David Tilman. 2013. Several scales of biodiversity affect ecosystem multifunctionality. PNAS. 110:25

Responses:
1) Karel Mokany, Hugh M. Burley, and Dean R. Paini. β 2013. Diversity contributes to ecosystem processes more than by simply summing the parts. PNAS. 110:43.
2) Jae R. Pasari, Taal Levi, Erika S. Zavaleta. 2013. Reply to Mokany et al: Comprehensive measures of biodiversity are critical to investigations of ecosystem multifunctionality. PNAS. 110:43.

One of the big topics in ecology in recent years is ecosystem services and functioning. In particular, the question has been how diversity (in its many forms, including species, intraspecific, phylogenetic, or functional) relates to ecosystem function (often, but not always, measured in terms of productivity). Most often, this is framed as a question about how (alpha) diversity at the local scale affects one or two functional responses. Because diversity can be measured at multiple scales (local, regional or landscape, etc), because how we measure diversity is scale-dependent (i.e. alpha, beta, and gamma diversity), and because a functional ecosystem relies on many different services, the obvious next step is to think of biodiversity and ecosystem functioning in a framework that incorporates multiple spatial scales, multiple functions, and multiple measures of diversity.

A new paper in PNAS takes advantage of David Tilman’s long running Cedar Creek biodiversity experiment to explore how multiple functions in a landscape relates to local and regional diversity, and beta-diversity. In Pasari et al. (2013), the authors use five years of data collected for 168 9x9 m plots in the Cedar Creek experiment. These plots contained 1, 2, 4, 8, or 16 perennial plant species, and had measurements for 8 ecosystem functions (invasion resistance, aboveground NPP, belowground biomass, nitrogen retention, insect richness and abundance, and change in soil C and plant N). The authors simulated combinations of these plots to create 50,000 landscapes composed of 24 local plots. Multi-functionality in this case was the (scaled) mean of each of the 8 functions minus their standard deviation, for the landscape. The authors then asked whether the average alpha-diversity of the local plots, the beta-diversity between plots, and the gamma-diversity of the landscape were important predictors of this multi-functionality.

Not surprisingly, when considering the different functional responses individually, the average alpha-diversity of plots in a landscape was the most important determinant. Past research has shown that as local diversity increases, niches may be filled, or functional redundancy may increase, and so ecosystem functioning tends to increase. When considering all 8 ecosystem functions using a single measure though, beta- and gamma-diversity also appeared to be important, although alpha diversity remains the dominant predictor (figure below). It should be noted though that the total explained variance in functionality was always low. Increasing either alpha- or gamma-diversity increased multi-functionality, while the effect of beta-diversity on ecosystem functioning was not linear. “[O]nly experimental landscapes with low β diversity were capable of achieving very high multi-functionality, whereas high β-diverse experimental landscapes more consistently achieved moderate multi-functionality”. One important conclusion suggested by these results, then, is that even at larger scales the most important determinant of ecosystem function is how local communities are assembling, since this determines local diversity.

These results are an important update to the current state of biodiversity ecosystem function research, and add to the large body of research that says that all types of diversity are important insurance for functioning natural systems. It is difficult from this study to get a clear picture of how important each type of diversity is, and when alpha, beta, and gamma diversity might be more or less important. This is in part because despite the upsides of having multiple years of tightly controlled data from the Cedar Creek data, experimental communities artificially combined into landscapes lack realism. For example, beta-diversity captures turnover between communities that may result from spatial dynamics (environmental heterogeneity, dispersal, biotic interactions). All of these characteristics may be very important for functioning at the landscape scale. The response from Mokany et al. expresses some of these concerns, noting that artificially creating landscapes like this may omit important spatial and temporal connections found in real systems.

In addition, and this is a more technical concern about how alpha, beta, and gamma diversity are defined, I’m not clear on what the implications of using all three measures as explanatory variables in the same model may be. Mostly because under the strictest definitions of diversity, these three terms should be dependent on each other – changes in alpha and beta diversity necessarily alter gamma diversity. The authors didn’t use this definition in their study, but to understand the mechanisms that relate diversity and functionality, it may be more informative to take this inter-relationship into account.

Despite any caveats, I think that a role for beta-diversity in ecosystem functioning will be shown in further work, and perhaps its role will prove to be much greater than these initial results show. As we expand our understanding of the scales at which diversity matters, unfortunately this will no doubt highlight the limitations in our conservation focuses even more.

Can intraspecific differences lead to ecosystem differences?

Sara Lindsay Jackrel and J. Timothy Wootton. 2013. Local adaptation of stream communities to intraspecific variation in a terrestrial ecosystem subsidy. Ecology. Online early.

It’s funny how complex outcomes can arise from simple realizations. For example, it is plausible that when there are differences among individuals of a species (like when local populations are adapted to the local environment), these could implications for function on the ecosystem scale. But while there is increasing evidence for the importance of intraspecific variation for ecological interactions within communities, the question of how intraspecific diversity scales up to ecosystem functioning is still ambiguous.

Sara Jackrel and Timothy Wootton explore this question in “Local adaptation of stream communities to intraspecific variation in a terrestrial ecosystem subsidy”. The basis for their study was simple: local adaptation is common, and populations/genotypes/ecotypes tend to be best adapted to the particular conditions of their locale. For example, “spatial variation in prey and predators can lead to a geographic mosaic of co-evolutionary interactions”. Further, these localized interactions can affect the greater ecosystem, if individuals or materials move between ecosystem boundaries.

In particular, the authors note that there is evidence that tree species composition riverside can alter the composition of the local aquatic community. This occurs via leaf litter fluxes into the river: the type and amount of leaf litter that falls into streams varies, and so the type of macroinvertebrates in the recipient stream also varies in response. These macroinvertebrates break down the leaf litter via shredding, collecting, and filtering, playing an important role in nutrient cycles. Leaf litter is carried from a given tree by wind or water and may decompose near or far away, creating a connection between ecosystems. The question then is whether macroinvertebrate compositional shifts will occur in response to intraspecific differences in leaf (i.e. trees), and what the implications might be for ecosystem functions such as leaf decomposition. To explore this question, Jackrel and Wootton performed reciprocal transplants of leaf litter material between eight sites along rivers in the Olympic Peninsula of Washington.

All eight of these sites were early successional forests dominated by red alder. The authors collected fresh leaves from alder trees, bagging leaves from each tree separately. These bags of leaves were either placed in the river adjacent to the trees they were taken from, or in a more distant site. Non-adjacent sites were either in the same river as the home site, or in different river all together. Leaf packs were weighed before and after spending 17-18 days in the river. This would allow comparison of how decomposition rates vary between home and away sites, and between home and away rivers.

Their results suggested a few interesting things. First, the identity of a tree affects the rate of decomposition of its leaves: individual alder trees’ leaves were highly variable in the rate of decomposition. Second, the combined identities of trees at a site seem to have affected the composition of the decomposer community at the home river site: put leaves from that site in another river with a new community of decomposers, and the decomposition rate drops significantly. In general, leaves decomposed significantly more rapidly when in their home river, regardless of whether at the home site or elsewhere along the river. But if they put leaves upstream from the home site, but in the same river, the rate of decomposition also dropped. Upstream decomposer communities were apparently much worse at breaking down leaves from novel communities of alders. However, if you put the leaves in sites downstream from home, the decomposition rates are not significantly different than in the home site. This is likely because of the directional movement of a river, such that downstream locations receive leaf litter from all upstream sites, and so downstream decomposer communities experience a greater variety of leaf litter than upstream sites. This might lead to upstream sites being more closely adapted to the individual trees in their neighbourhood than downstream sites, which receive inputs from a wide variety of trees. These results suggest that individual differences in trees at different spatial locations can matter, both locally, across trophic levels, and even across ecosystems.

Admittedly there is not a lot you can infer about the mechanisms at play from this preliminary experiment. One interesting follow up would be to measure compositional differences in aquatic macroinvertebrates at very fine scales in correspondence with differences in trees. Another important question is whether these communities differ via phenotypic plasticity, adaptation to local sites, or species sorting. But this paper does hint at one way in differences among individuals can shape local ecosystems and even structure distant ecosystems (e.g. downstream decomposer communities) through fluxes across boundaries. And that is a rather complicated implication from a logical and simple starting point.

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.

Evidence for the evolutionary diversity-productivity relationship at several scales

Cadotte, M. W. 2013. Experimental evidence that evolutionarily diverse assemblages result in higher productivity. Proceedings of the National Academy of Sciences.

John J. Stachowicz, Stephanie J. Kamel, A. Randall Hughes, and Richard K. Grosberg. Genetic Relatedness Influences Plant Biomass Accumulation in Eelgrass (Zostera marina). The American Naturalist, Vol. 181, No. 5 (May 2013), pp. 715-724

Ecology is increasingly recognizing the value of non-species based measures of diversity in relation to ecosystem services, community diversity and invasibility, and conservation activities. One result is that we are seeing increasingly strong and interesting experimental evidence for the importance of genetic diversity in understanding populations, species, and communities are structured. Two recent papers are good examples of how our understanding is progressing.

For example, we are now at the point where research has clearly demonstrated the relationship between ecosystem functioning and evolutionary history, and now well-designed experiments can begin to explore the mechanisms that underlie the ecosystem functioning-evolutionary diversity link. The oft-demonstrated correlation between evolutionary diversity and productivity is explained based on the assumption that ecological similarity and evolutionary relatedness are connected. Diverse communities are often thought to have lower niche overlap (i.e. higher complemenarity), but these experiments often rely on highly distinct species (such as a grass and a N-fixer), which could over-emphasize the importance of this relationship. In Cadotte (2013), independent manipulations of phylogenetic diversity and species richness allow the author to explore separately the role of complementarity and selection effects (the increased likelihood that a highly productive species will be present as species richness increases).

The experiment involved old field plots, planted with between 1 and 4 species chosen from a pool of 17 possible species; evolutionary diversity (high, medium, or low) and species richness are manipulated to include all possible combinations. The study found found a much stronger relationship between phylogenetic diversity (PD) and biomass production then between species richness and biomass production, but this isn't especially novel. What is interesting is that it could also identify how selection effects and complementarity were driving this response. High levels of complementarity were associated with high levels of PD: polyculture plots with high complementarity values were much more likely to show transgressive overyielding. Plots with close relatives had a negative or negligible complementarity effect (negative suggesting competitive or other inhibitory interactions). There was also evidence for a selection effect, which was best captured by an abundance-weighted measure of evolutionary diversity (IAC), which measured the abundance of closely related species in a plot. Together, PD and IAC explain 60% of the variation in biomass production.

From Cadotte (2013).

The second study asks the exact same question – what is the relationship between biomass production and genetic diversity - but within populations. Stachowicz et al. (2013) looked at genetic relatedness among individuals in monocultures of the eelgrass Zostera marina and its relationship to productivity. Variation within a species has many of the same implications as variation within a community – high intraspecific variation might increase complementarity and diverse assemblages might also contain more productive genotypes leading to a selection effect. On the other hand, it is possible that closely related, locally adapted genotypes might be most productive despite their low genotypic variation. 

Similar to most community-level experiments, Stachowicz et al. found that looking at past experimental data suggested there was a strong relationship between genetic relatedness and biomass/density in eelgrass beds. Taxa (i.e. the number of genotypes) tended to be a poorer predictor of productivity. However, the relationship was in the opposite direction usually seen – increasing relatedness predicted higher biomass. This is difficult to explain, since it goes against the expected direction of complementarity or selection effects. Possibly cooperative/facilitative relationships are important in eelgrass monocultures. Data obtained from field surveys (rather than experimental data) suggested an alternative: possibly these studies didn’t cover a large enough range of relatedness. This field data covered a much larger range of relatedness values, and showed a unimodal relationship (below), indicating that the productivity-relatedness relationship had an optimum, where highly related or highly diverse assemblages were less productive. Although further work needs to be done, this is an intriguing possibility.

From Stachowicz et al. (2013). Grey dots represent range of relatedness values from experimental data only, compared to range covered by field survey.

At some scales, ecologists are now refining what we know about popular research questions, while at others we are just scratching the surface. Stachowicz et al. suggest that as we scale up or down our expectations should differ -  “the slope and direction of the relationship between genetic differentiation and ecological functioning might depend on the genetic scale under consideration”.

(Disclaimer - obviously Marc Cadotte was my PhD supervisor until very recently. But I think it's a nice paper, regardless, and worth a post :) )