Shadiness in the global leaf economics spectrum

new borracho.cut4 copy.jpg

(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 


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.

OTS leftovers: Does leaf pH influence herbivory?

My research focuses on how species have adapted to environmental variation and how these adaptations influence species’ niche breadths and geographic distributions. Although IUntitled focus on tropical plants, and insect herbivores are a substantial biotic selection pressure, herbivory is not a topic I actively pursued until I participated in an OTS course last summer. On my OTS course I was able to investigate an array of topics from plant defense to plant-mediated tri-trophic interactions, all of which are documented in our 2015 OTS coursebookOf all the projects I participated in, the last project of the course remains my favorite because it has provoked new questions, some of which have informed my thesis research.

In this last project, my classmate and I were following-up a previous study in which we investigated the ability of leaf pH to predict herbivory in plants. Literature suggested that low pH values deter herbivores in the sub-arctic where ungulates, not insects, are the dominant herbivores. Consequently, the influence of leaf pH on herbivory in tropical to sub-tropical regions where insects are the dominant herbivores is unclear. In our first project, my classmate and I found no effect of leaf pH on standing herbivore damage in the 5 Piper species we measured. For our follow-up project we were interested in determining the sources of variation that may have influenced leaf pH, and thus, the results of our previous study. Ultimately, we decided to investigate diurnal and ontogenic changes in leaf pH for two Piper species. 


Figure 1: Ontogenic changes in leaf pH of P. multiplinervum & P. hispidum

Interestingly, our immature leaves exhibited the lowest pH values (Fig 1), and immature leaves have previously been shown to be the most palatable to insect herbivores. Compared to mature leaves, immature leaves tend to receive more insect herbivory because they are softer, are higher in nutrients, but also produce more chemical defense compounds. Therefore, leaf acidity may be correlated with leaf age and linked to chemical defenses that deter herbivores. If so, leaf pH could be an easily-measured trait used to understand the susceptibility of plants to insect herbivory.

In addition to ontogeny, leaves also exhibited diurnal changes in their chemistry (Fig 2). We found that both immature and mature leaves that were measured in the morning (~9am) had lower pHs than leaves measured in the the afternoon (~4pm). These diurnal fluctuations may have resulted from changes in carbonic acid and cytoplasmic proton gradients throughout the day. However, given the potential relationship of pH to chemical defenses, it is easy to speculate that some chemical defenses could fluctuate throughout the day in addition to ontogenic phase. 


Figure 2: Diurnal changes in leaf pH of P. multiplinervum & P. hispidum

Since our first study did not properly measure herbivore damage, the effect of pH on insect herbivory remains an unanswered question. The observations from our follow-up study indicate pH is probably correlated with ontogeny, which has been shown to influence the production of chemical defenses that deter herbivory. pH was also observed to fluctuate diurnally, and may indicate diurnal changes in herbivore deterrence.

What I think is exciting about these results is that if pH does influence herbivory, insects may feed upon leaves according to temporal differences in leaf chemistry. In turn, these short-term temporal feeding preferences could promote co-existence of insect species, which greatly outnumber plant species, and are likely to overlap in diet-breadth. There are many unanswered questions that this project has induced that warrant further investigation before any concrete conclusions can be made about the influence of pH on insect herbivory. 

My uncharacteristic foray into plant-insect interactions has led me to a new understanding of niche-breadth and coexistence theories through concepts such as the storage effect that incorporate temporal niche partitioning – a topic of great relevance to my thesis. Moreover, my newfound interest in herbivory highlights the benefit of stepping outside the territory of your own research in order to gain a better understanding of it. 

Now that I am in Florida, where Pipers are introduced and rare,  I’ve been
gathering information on the native species Psychotria nervosa to address some of the questions I developed while on my OTS course. I’m currently collecting and identifying insects that feed on P. nervosa, and have already quantified ontogenic changes in leaf nutrients. As my course-load dwindles and the resources at the International Center for Tropical Botany 
become available, I hope to dedicate more time to understanding how leaf chemistry influences insect herbivory in the sub-tropics as a side-project…so stay tuned.


Me (Tim Perez) happily collecting Piper cenocladum at La Selva Biological Station, Costa Rica.

Going Graduate?


The final semesters of an undergraduate education are an exciting time for many students as they are confronted with how to apply their education. Volunteering, interning, and jobs are usually the first things that come to mind for soon-to-be graduates, but members of FIU’s GLADES Club were curious about what it takes to pursue a graduate degree. This past Tuesday GLADES undergraduates organized a panel of current graduate
students and professors to discuss the processes of searching for and applying to graduate ecology programs. The panel included PhD students Belén Fadrique, Jeremy May, and Timothy Perez (me), while professors were represented by Drs John Kominoski, Ken Feeley, and Lidia Kos.  Below are some of the important items we discussed
that many people pursuing graduate school are unaware of:

  • Don’t pay for Grad School! Unlike undergraduate degrees you should not pay for graduate school. In most graduate programs, students are actually paid a modest salary – typically through scholarships, teaching assistantships, and research assistantships. However, tuition is typical for professional degrees like MDs, DDSs, etc., but not PhDs.
  • You DO NOT need a master’s degree to pursue a PhD. In fact, masters programs are becoming increasingly harder to find and fund. Anyways, sometimes research experience is as valuable as a master’s degree…
  • Get research experience! Good grades and great GRE scores are always helpful, but there is no substitute for doing actual science. Grad school is a lot of research, so get practice now! This will help you decide if you actually want to go to grad school too. You will also likely get practice writing and presenting research, which are valuable skills for graduate school. Shameless plug: Feeley lab now looking for undergraduate research assistants! Contact us for details!
  • Apply to the Advisor and the Program – not necessarily the school. When you apply to a graduate program, at least in ecology, you are really applying to work with the advisor. In other words, make sure you are familiar with and interested in a potential advisor’s research. It is just as important that you get along with your potential advisor – send your potential advisor emails, Skype, and make a visit to their lab if you can to see if it is a good fit. Of course, a supportive and collaborative department or program is also an important consideration.
  • Network. Like most professions, academia has its fair share of networking. By being interested in others’ research, talking to co-workers, forming collaborations – basically being a curious and gregarious person – you will increase gain a leg-up on competition via word-of-mouth opportunities.

Lastly, I offer my own two cents. I recommend recent graduates to thoroughly explore their interests before applying to grad school. Graduate school can be a lot fun, but it is also a lot of work, requires lots of dedication, and takes multiple years to complete. Before you decide to apply to a graduate program ask yourself if is really what you want. If you can’t imagine yourself doing anything else except graduate school, then get those applications ready!


OTS Course Blog

It is currently the last official week of my OTS Course, Tropical Biology: An Ecological Approach. During this course I have had the pleasure of sharing adventures with outstanding graduate students and scientists in some of Costa Rica’s most beautiful ecosystems. We are all sharing some our experiences on this blog (my post can be viewed here). Keep an eye out for when I post a link to our Course Book. This book will contain a collection of projects that students have completed individually, or with faculty, at the handful of sites we have visited.

It is hard to pick a favorite site, but Monteverde is in the top three. Judging by the smiles on everyone’s faces below, I think they would agree with me…

Students of OTS' Tropical Biology: An Ecological Approach,  Summer 2015

Students of OTS’ Tropical Biology: An Ecological Approach (Summer 2015), Monteverde Cloud Forest Reserve, Costa Rica.

FUN!ctional Traits: Stomata Density

Cananga odorata abaxial leaf surface @ 100x with stomata circled in red.

Cananga odorata abaxial leaf surface @ 100x with guard cells and stomata circled in red.

Stomata are the microscopic pores that facilitate the movement of gasses into and out of leaves. Carbon dioxide goes into the leaf, while oxygen and water vapor go out. The opening and closing of stomata (stoma=singular) are mediated by the guard cells, which can expand and contract depending on their turgor pressure. Turgid guard cells open the pores, flaccid cells close them. Stomata are key to evapotranspiration and water and solute transport from roots, to shoots, to leaves. Coupled with other plant functional traits, stomata can indicate how a plant is interacting and coping with its environment. In an upcoming project I will being quantifying stomatal density with other traits, among different species along an environmental gradient.

From reading the literature, it is apparent that changing one variable in a leaf, such as stomatal density, can have a cascade of effects on other traits and photosynthetic rates. However, I cannot think about stomata density without first considering Woodward’s 1987 paper, ‘Stomatal numbers are sensitive to increases in CO2 from pre-industrial levels.’ I really like this study because it used herbarium records dating back 200 years to show stomata densities have decreased over time. After growing plants in varying concentrations of carbon dioxide, Woodward was able to show that the decreases in stomata density of herbarium specimens likely resulted from increases in global CO2 concentration.

It is interesting to note that atmospheric CO2 concentrations were 340 µmol/mol at the time of Woodward’s study. We have just recently passed the grim 400 µmol/mol milestone, which is disconcerting in light of another observation Woodward made: Some plants did not change their stomatal density above ambient CO2 (340 µmol/mol) conditions. What does that mean for plant physiology?  Rico et al. 2013 suggest plants may shift towards lower water requirements and greater xylem fortification – in other words – plants become more drought tolerant…if they can.

While I’m reading up on that, I will leave you with a 400x close up of the more stomata (below). In both top and bottom pictures, I have circled some of the stomata. The guard cells look like two touching crescents. The guard cells are mostly closed, because the leaves are dead (ultra-flaccid), plus the cells have probably contracted some. The black cone shapes are hairs. These images are nail polish molds of the the abaxial (bottom side) of Cananga odorata. The green color is an after-effect.

Cananga odorata abaxial leaf surface @ 400x with two stomata circled in red.

Cananga odorata abaxial leaf surface @ 400x with two stomata circled in red.

Works Cited:

Rico, C., Pittermann, J., Polley, H. W., Aspinwall, M. J. and Fay, P. A. 2013. The effect of subambient to elevated atmospheric CO2 concentration on vascular function in Helianthus annuus: implications for plant response to climate change. New Phytologist 199: 956–965.

Woodward, F. I. 1987. Stomatal numbers are sensitive to increases in CO2 from pre-industrial levels. Nature 327:617–618.