Shadiness in the global leaf economics spectrum

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(Above is an image assembled in the Inkscape and GIMP programs — it shows the silhouette of an unidentified Piper sp. from Peru superimposed with a map generated in R. Below are some thoughts that Ken and I had on a 2016 Nature Plants paper  entitled, “Global plant traits estimates biased due to plasticity in the shade,” by Keenan and Niinemets.)

Much of the variance observed in the functional niche-space of plants can be explained by light. Despite the long-established and well-studied roles of light in plant ecology, Keenan and Niinemets1 highlight potential biases in studies of the global spectrum of leaf form and function that may arise through neglect of standardized light measurements. To correct for these biases, the authors advocate several important modifications in the procedures for sampling and reporting leaf functional data. Below, we expand upon some of these recommendations and highlight other sources of error in estimates of the leaf economics spectrum. 
We agree with Keenan and Niinemets (1) that studies investigating functional plant ecology should report some level of light exposure associated with trait data. While photon-flux density or canopy density estimates (e.g., from hemispherical photography) is ideal, these measurements may be prohibitive at times due to cost and/or feasibility (e.g. it can be extremely difficult to take measurements over mature canopy trees). However, crown illumination indices (CIIs) require no special equipment and are reasonably correlated with estimates of light exposure derived from hemispherical photography (2). Future meta-analyses amalgamating CII and trait data would inevitably suffer from inter-observer error, and additional error would be introduced through different methods of CII estimation (namely the number illumination categories[3]).  Therefore, we propose that ecologists use the 7 categorical light classes used by Clark and Clark (4) as the standard for quantifying light exposure when more sophisticated quantifications are unavailable.  
Standard protocol for measurements of leaf traits generally calls for sampling of fully sun-exposed leaves.  Sampling sun leaves from tall canopies can be difficult and the failure to properly sample fully-exposed canopy leaves has potentially introduced considerable error in estimates of leaf form and function, particularly for tropical forests (1). Canopy sampling techniques have traditionally relied on shotguns, which often require hard-to-obtain ammunition and permits. Until terrestrial laser technology and radiative transfer modeling become more accessible, some sampling constraints may be removed through the use of low-tech methods. Although infrequently reported in the literature, slingshots are commonly used in arboriculture for canopy-ascension and provide a less-invasive and more precise method for sampling canopies compared to shotguns.  More specifically, slingshots can be used to position weighted lines over small branches with fully sun-exposed leaves, which can then be harvested with the aid of serrated wires or modified chainsaw chains. Since slingshots can reliably reach heights up to approximately 50m, they are suitable for sampling all but the very tallest forest canopies.  
Standard sampling protocol also calls for recently matured leaves. As leaves age, they can undergo marked changes in traits such as leaf mass area and photosynthetic rate (5). It is also common for old leaves to develop epiphylls, which influence host leaf physiology through light preemption (6) and nutrient leaching (7). However, without previous information regarding phenology, determining which leaves are newly matured is inherently subjective. Assuming that studies have accurately sampled leaves with the same relative development, measurements of leaf traits are still likely to misrepresent the majority of leaves in a given canopy because newly matured leaves may be proportionally rare compared to all leaves in the canopy.  
When scaled up from individuals, unrepresentative measurements in leaf traits due to shading and age may result in gross stoichiometric miscalculations at the global level. For now, the implications of Keenan and Niinemets’ findings suggest that studies based on the reported global spectrum of leaf form and function may require some re-evaluation. We propose that increased use of CIIs, improved sampling techniques, and more detailed study of the within-canopy and age-related trait variation are effective ways to correct the observed bias in the leaf economics spectrum.  

1.Keenan, T. F. & Niinemets, Ü. Nat. Plants 16201, 1020–1029 (2016). 
2.Keeling, H. C. & Phillips, O. L.. For. Ecol. Manage. 242, 431–437 (2007). 
3.Jennings, S. B., Brown, N. D. & Sheil, D.  Forestry 72, 59–73 (1999). 
4.Clark, D. A. & Clark, D. B. Ecol. Monogr. 62, 315–344 (1992). 
5.Kitajima, K., Mulkey, S. S. Am. J. Bot. 89, 1925–1932 (2002). 
6.Anthony, P. A., Holtum, J. A. M. & Jackes, B. R. Funct. Ecol. 16, 808–816 (2002). 
7.Wanek, W. & Pörtl, K. New Phytol. 166, 577–588 (2005). 

Cross-posted on 

Truths and Answers about the Amazon

Andrew Boryga has recently posted a news article about some of the upwithclimate work on the University of Miami webpage. A link to the news article is HERE and a copy f the article, in its entirety is pasted below.


Truths and Answers about the Amazon

The Amazon rainforest in South America plays a vital role in regulating Earth’s climate and is home to thousands of species of wildlife. But much of what is currently known about the Amazon is based on about 1,000 plots of land each the size of a football field. That may sound like a lot, but not if you consider the Amazon covers over 2 million square miles or about two-thirds the size of the continental U.S.

“You have the biggest rain forest in the world, and we’ve only studied 1,000 football fields of it,” said Dr. Kenneth Feeley, the Smathers Chair in Tropical Trees at the University of Miami College of Arts and Sciences, who studies the ecology of tropical forests.

In a recent paper, “Ancient human disturbances may be skewing our understanding of Amazonian forests,” published in the journal Proceedings of the National Academy of Sciences, Feeley argues that not only have researchers just scratched the surface of analyzing the Amazon, but the plots of land that we do analyze may have biases that are not accounted for.

Namely, almost all of the plots are in areas with relatively “easy” access (for example, close to waterways or population centers) and have likely been impacted by humans for centuries.

According to Feeley, native inhabitants of Amazonia actively transformed and modified the forests along the Amazon River and its tributaries before their populations collapsed around the arrival of Europeans in 1492 AD. Given the long lifespan of Amazonian trees, many of the forests that biologists are studying today may still be recovering from human disturbances, potentially skewing interpretations of their growth and our understanding of how the Amazon is responding to climate change.

Meanwhile, Feeley said the scientific community at large has spent less time studying the more remote parts of the Amazon that are harder to get to and hence less likely to have been impacted by ancient human activities. That doesn’t mean scholars and scientists should throw away all the research that’s been done, he says, but they should take the potential impacts of ancient humans into consideration and be careful about drawing conclusions based on current datasets.

For example, Feeley said, it is hypothesized that, with increasing carbon dioxide in the atmosphere, tropical forests are able to grow faster and take up more of that CO2, thereby buffering the climate from our increasing carbon emissions. However, Feeley said, the research to support that claim is largely attributed to measuring a relatively small sample of trees that may have been disturbed by humans 500 years ago.

“How do we know those forests aren’t just recovering from that original disturbance?” he asked. “How do we know whether or not the rest of the Amazon is actually suffering under climate change and growing slower? Until we are confident in the answers to these questions, we shouldn’t count on the Amazon to protect us against our increasing greenhouse gas emissions.”

Despite the large uncertainties, scientists and policy makers are continuing to make big judgments about the entire Amazon based off a relatively small and potentially compromised sample. With the publication of his paper, Feeley hopes to get funding that would help him and his colleagues investigate more diverse samples of land throughout the Amazon.

He isn’t under the illusion that researchers will ever be able to assess the entirety of the Amazon but believes that, with help, scientists like him can do a more accurate job and gain better insight into the workings of the Amazon.

“If you think of a phone survey where people call you to ask questions, they’re taking a small but systematic sample from all over the country and extrapolating out to the population,” he said. “That’s analogous to what we need to do. A more systematic or targeted sampling approach just might help us discover truths and answers about the Amazon and the Earth that we might’ve missed so far.”

Feeley’s research collaborators include Crystal McMichael from the Institute for Biodiversity and Ecosystem Dynamics at the University of Amsterdam, Frazer Matthews-Bird from the Department of Biological Sciences at Florida Institute of Technology, and William Farfan-Rios from the Department of Biology at Wake Forest University.

By Andrew Boryga


AHI are skewing understanding of amazon

test of 360 image

We are starting to explore the use of 360degree spherical images for showing off the cool places around the world where we work. This is just a test to see if we can successfully embed one of these images in the blog. This image is of the walkway on University of Miami’s Coral Gables campus…

Gas exchange analysis in fossil leaves and climate change

Next month, experts in climate reconstruction will meet to create a consensus record of atmospheric CO2 over the past 66 million years.  Stomata will play an important role in the coming meeting when paleoclimatologists reconcile their calculation using leaf gas exchange in fossil leaves with other sources1.

It was Woodward in 1987 who first observed that a significant inverse relationship existed between plant stomatal density (number of stomata per mm2) and atmospheric CO2 concentration. Using herbarium specimens, he demonstrated that the stomatal densities and ratio in 8 temperate woody specimens collected 200 years ago were significantly higher than those of the same plant species today2.

In 2014, Franks et al.3 applied the same idea of counting stomata to fossil leaves and integrated their counts with the available models for leaf gas exchange. Another important parameter used in common leaf gas exchange analysis is the internal CO2 content. In fossil leaves, this concentration can be obtained using the isotopic signal of δ13C to discriminate between leaf and atmospheric carbon. A worrisome finding from this method is that the Earth’s climate could be more sensitive to CO2 concentrations than previously thought.



Conceptual idea for the analysis of leaf gas exchange in fossil leaves (taken from Franks et al. 2014)


Understanding the sensitivity of climate to carbon dioxide concentrations is a key point in the discussions of climate change. Scientists are trying to come up with better methods, with less uncertainty, which can help arrive at more accurate conclusions about our past climate. Hopefully, the stomata in fossil leaves can help in this effort. Another promised result from the meeting is an open source paleo-pCO2 database.

Thanks to the people in the plant bio journal club for pointing out this news.

  1. Hand, E. Fossil leaves bear witness to ancient carbon dioxide levels. Science 355, 14–15 (2017).
  2. Woodward, F. I. Stomatal numbers are sensitive to increases in CO2 from pre-industrial levels. Nature 327, 617–618 (1987).
  3. Franks, P. J. et al. New constraints on atmospheric CO2 concentration for the Phanerozoic. Geophys. Res. Lett. 41, 4685–4694 (2014).

Desperately lacking tropical data

A version of this post has also been published as an online comment in PLoS Biology

In his recent meta-analysis, “Climate-Related Local Extinctions Are Already Widespread among Plant and Animal Species“, Wiens looked at changes in species ranges and local extinctions driven by climate change.

Wiens claims to have broad taxonomic and geographic coverage of studies.  Unfortunately, this is not the case. In fact, from the true tropics (i.e., excluding studies from the Santa Catalina Mountains of Arizona, USA, the Appalachian Mountains of north Georgia, USA, and the high eastern Himalayas that Wiens categorizes as “tropical” for the purposes of his analyses), only 5 studies representing a total of just 341 species (35% of species, 18% of studies) are included.  All but one of these tropical studies (of 55 Andean bird species) are from oceanic islands (Borneo [insects], New Guinea [birds], Madagascar [amphibians], and Hawaii [plants]).  All tropical plants are represented by just 4 grasses in Hawaii.

The lack of data from the tropics is not Wiens’ fault but rather reflects a true underlying disparity in the state of knowledge about different systems of the world. Simply put, we know much more about the effects of climate change in North America and Europe than we do the effects of climate change in the tropics.  That said, Wiens needs to be more forthright in acknowledging this disparity.  Furthermore, given this extreme lack of data, it is clearly premature to conclude that “there were significant effects of climatic region overall, with extinction more common in tropical regions” and that “this pattern of more frequent tropical extinction arose from a much lower frequency of extinctions for temperate plants”. Four grasses from Hawaii tell us next to nothing about how the thousands of tropical plants are responding to climate change.  Or even if we lump the tropics and subtropics together as does Wiens, 4 grasses from Hawaii, 27 mountain desert plants from Arizona and 124 high-elevation Himalayan plant species (all with ranges restricted to elevations >3500 m asl) provide little information about how the thousands of other tropical and subtropical plants are responding to climate change.  The tropical data void is real and it is troublesome (Feeley et al. 2016a,b).  But before we can begin to address this lack of data it needs to be acknowledged and recognized for the problem that it is.


Wiens JJ. 2016. Climate-Related Local Extinctions Are Already Widespread among Plant and Animal Species. PLOS Biology 14(12): e2001104. doi: 10.1371/journal.pbio.2001104

Feeley KJ, Stroud JT, and Perez TM. 2016. Most “global” reviews of species’ responses to climate change aren’t truly global. Diversity and Distributions. In Press.

Feeley KJ, Silman M, and Duque A. 2016. Where are the tropical plants? A call for better inclusion of tropical plants in studies investigating and predicting the impacts of climate change. Frontiers of Biogeography. 7(4). fb_27602.

Protected areas will not protect the Amazon against climate change

Ken Feeley and Miles Silman have published a new article in the journal Diversity and Distributions entitled “Disappearing climates will limit the efficacy of Amazonian protected areas“.  This article discusses how protected areas, while a powerful tool against traditional threats such as hunting and deforestation, will fail to protect many parts of the Amazon against rising temperatures.  In other words, “protected areas are not a panacea and the current reserve system alone may be insufficient to conserve biodiversity in the face of rapidly rising temperatures. Migration, whether through explicit corridors or through landscapes of working forests managed to facilitate species movement, will be paramount in determining the future of Amazonia”.

A discussion of this article is featured in Mongabay


Disappearing climates will limit the efficacy of Amazonian protected areas

ABSTRACT: Amazonian forests support high biodiversity and provide valuable ecosystem services. Unfortunately, these forests are under extreme pressure from land use change and other anthropogenic disturbances. A recent study combined data from an Amazon-wide network of forest inventory plots with spatially explicit deforestation models to predict that by 2050, 36% or 57% of species will be ‘globally threatened’, as defined by IUCN Red List criteria, due to deforestation under Increased-Governance or Business-As-Usual scenarios, respectively. It was also predicted that the number of threatened species will drop by 29–44% if no deforestation occurs within protected areas. However, even the best-protected areas of the Amazon may still be susceptible to the effects of climate change and rising temperatures. To illustrate the potential dangers of climate change for Amazonian parks, we calculated the percentage of land area within all officially designated protected areas of tropical South America that will or will not have future temperature analogs under various scenarios of temperature change and park connectivity. We show that depending on the rate of warming and degree of connectivity, about 19–67% of protected areas will not have any temperature analogs in the near future (2050s). These results help to emphasize that protected areas are not immune to the effects of climate change and that large portions of Amazonian protected areas include ‘disappearing climates’. In the face of these disappearing climates, the biggest determinant of many species’ extinction risks may be their ability to migrate through non-protected habitats.


Figure 1

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Figure 1. Portions of officially designated protected areas of tropical South America that will (black) or will not (grey) have climate analogs under mean annual temperatures predicted for the 2050s according to the National Center for Atmospheric Research’s Community Climate System Model 4 (NCAR CCSM4) under Representative Concentration Pathways (RCPs) 2.6 (left hand panels, a and c) and 8.5 (right hand panels, b and d). Climate analogs are defined as having the same mean annual temperature ± 0.5 °C. In the top row (panels a and b), the search for climate analogs was extended to all connected or immediately adjacent (at ~5 km resolution) protected areas. In the bottom row (panels c and d), the search for climate analogs was restricted to within the same protected area. The percentage of protected area without future climate analogs under each scenario is indicated within each panel.

Feeley Lab Goes to ESA


The Ecological Society of America recently held their 101st annual meeting in Fort Lauderdale, just north of Miami. Needless to say,  the meeting’s location resulted in a strong contingent of ecologists from FIU and the Feeley Lab. Past and present lab members who showcased research included (in timchronological order):

PhD candidate Timothy Perez who presented a poster on the patterns of community assembly in the genus Piper along an elevational gradient in Peru.


PhD candidate James Stroud gave two talks – the first was on the use of citizen science to conduct lizard surveys, while the second explored how unique competitive evolutionary histories may influence priority effects and the assemblage of novel anole communities.

Paulo Olivas, a past Feeley Lab post-doc and now a research associate at FIU, presented a talk entitled “Differential growth and physiological responses to water level and soil type in two dominant Everglades macrophyes, Cladium jamaicense and Muhlenbergia capilaris”.

Ken Feeley presented a synthesis of research 20160811_143130
he has conducted with collaborators in Peru, Costa Rica, and Colombia that has investigated the up-slope shift in the distributions of tropical montane tree species in response to climate change.



Evan Rehm, a former Feeley Lab PhD student, presented research from his current post-doctoral position at Colorado State University, where he is working with collaborators to investigate how the loss of native avifauna can have cascading effects on the forest community. Evan’s talk discussed how to determine the seed dispersal services of avian frugivores to guide rewilding efforts on tropical islands.

Follow the links for each respective presenter to learn more about their research.

The global conservation status of many widespread and rare tropical tree species remains uncertain

Below is a copy of recent commentary that I published in Frontiers of Ecology and Evolution based on the article by ter Steege et al on “Estimating the global conservation status of more than 15,000 Amazonian tree species“.

Amazonian forests provide ecosystem services that are critical at the planetary scale. Unfortunately, human land use threatens to drive many rainforest species to extinction. In a recent study, ter Steege et al. (2015) provide valuable insight into the threats that current and future deforestation potentially pose for Amazonian tree species. In any such large-scale analysis dealing with thousands of poorly-known species, there are clearly going to be many assumptions and possible sources of uncertainty. Here, I highlight two major assumptions used by ter Steege et al. (2015) to simplify their analyses—namely in the handling of widespread species and rare species. These assumptions have the potential to strongly influence predictions of how many and which species are at risk of being lost to deforestation over the coming decades.

Some tree species are likely to be endemic to the lowland Amazon; however, there are also certain to be many species that have ranges extending to higher elevations, different ecoregions, or even different continents. While ter Steege et al. perfunctorily acknowledge (in their online Supplemental Material) the potential problems caused by widespread tree species with geographic ranges extending beyond the defined Amazonian study area, they make no attempt to quantify how pervasive of a problem this may be or to account for it in any of their analyses. Rather, ter Steege et al. assume that rates and patterns of deforestation outside the Amazon mirror those occurring inside the Amazon. This goes against the core proposition of the study that spatial patterns of species’ distributions, population densities, and the rates of deforestation, all combine in determining the degree to which species are threatened by habitat loss.

To get a sense of how many species may have ranges extending beyond the Amazon, I mapped the locations where Amazonian tree species are known to occur based on their herbarium collections records. More specifically, I downloaded all georeferenced occurrence records available through the Global Biodiversity Information Facility (GBIF; for the nearly 5000 Amazonian tree species occurring in the Amazon Tree Diversity Network’s (ATDN; forest plots and queried how many of these “common” species have recorded occurrences outside of the Amazon. I found that the vast majority (81%) of species have ≥1 occurrence outside the defined study region, one-fourth of the species have ≥50% of their occurrences outside the study region, and one-tenth of species have >90% of their occurrences outside the study region. Even if these extra-Amazonian populations are in some cases cryptic species, it is clear that many, if not most, Amazonian tree species are not actually endemic to the Amazon. For at least these widespread species, the data and methods employed by ter Steege et al. (2015) are insufficient to accurately estimate their true “global conservation status.”

In the case of rare species, there are believed to be ~11,000 Amazonian tree species (i.e., ~2/3 of total Amazon tree diversity) that are too rare to occur in any of the ATDN’s networked inventory plots (ter Steege et al., 2013). ter Steege et al. (2013, 2015) estimated the population sizes of these rare species based on an extrapolation of a rank-abundance curve created for the common species that do occur in their plots. ter Steege et al. (2015) then estimated the range sizes for rare species by assuming a fixed relationship between population size and range size. This methods explicitly disregards the different ways that species can be rare (i.e., the classic “7 forms of rarity”;Rabinowitz, 1981) by assuming that all rare species have small geographic ranges and that no rare species have large, low-density ranges. It is difficult to test this assumption due to the inherent relationship between a species’ density and its detection probability. However, it is easy to imagine that there may exist widespread species that occur at such low densities that they are effectively “invisible” to current census techniques—especially considering that the ATDN’s plots include < 0.8 million of the nearly 400 billion trees that they estimate to be growing in the Amazon (i.e., a sampling intensity of 0.0002%; ter Steege et al., 2013, 2015). In some cases, the ATDN may get “lucky” and a widespread low-density species will occur as a singlet or small number of individuals within one of their plots. According to the methods of ter Steege et al. (2015), however, the ranges of all species occurring in only a single plot, regardless of the number of individuals, are truncated to an arbitrarily set area (e.g., < 444 km from the plot where it occurs). A clear priority for future research in tropical forests is to understand the true nature of rarity.

The handling of rare and widespread species by ter Steege et al. likely adds large uncertainties to the predicted global extinction risks of many individual species. However, it is still possible that the cumulative result, that between about 30 and 60% of Amazonian tree species are threatened with extinction due to deforestation, is valid. The same two concerns about widespread and rare species were raised in a response to a previous study by Hubbell et al. (2008) that estimated the extinction risks posed by Amazonian deforestation (Feeley and Silman, 2008). A subsequent analyses byFeeley and Silman (2009) was then attempted with the explicit goal of at least partially bypassing these assumptions through the use of occurrence records, habitat maps and estimates of deforestation rates outside the Amazon (at the same time introducing other assumptions and possible sources of errors). Feeley and Silman (2009) predicted that Amazonian plant species will lose an average of 17 or 30% percent of their ranges by 2050 under Increased-Governance or Business-As-Usual models of deforestation—estimates that are strikingly similar to the new loss rates predicted by ter Steege et al. (ter Steege et al. predict that the population sizes of common Amazonian tree species will decrease by an average of 11 or 35%). In other words, while the data, methods, assumptions, and limitations differed greatly between studies, the final predictions were accordant. If nothing else, these studies all indicate that very high numbers of Amazonian species are already, or soon will be, threatened by deforestation. Add in the largely-unexplored effects of other human disturbances such as climate change, fire, forest degradation and defaunation (Peres et al., 2010), and it is clear that no matter what the underlying assumptions, the Amazon’s future is very dire indeed.

Evan Rehm, a former graduate student with FIU Department of Biology and ICTB (currently a postdoc at Colorado State University), and Dr. Kenneth Feeley have published a new article in the open-access journal Frontiers of Biogeography.  The article is entitled “Many species risk mountaintop extinctions long before they reach the top“.  In their article, Rehm and Feeley discuss the importance of ecotones, such as the alpline treeline, in setting current and future species’ distributions.  They highlight the fact that many species’ range boudaries are set by ecotones and that these ecotones may not shift concurrently with climate change – potentially resulting in rapid range compressions and elevated extinction risks.


Fall 2016 in Colombia

Ken Feeley has been awarded a Fulbright Research Fellowship.  With the support of the Fulbright Fellowship, Ken will spend the Fall 2016 semester on a sabbatical leave at the National University of Colombia in Medellin working on a collaborative study with Dr. Alvaro Duque. Ken’s research will build off of previous work that he and Alvaro conducted looking at climate-driven changes in the composition of Andean forests (published in the Proceedings of the National Academy of Sciences:  Ken and Alvaro will now look at how the observed changes in composition relate to species’ functional traits and climatic tolerances.