Not Seeing the Grass for the Trees

I appreciate repetition.

My favorite class in high school was AP Chemistry, but I think I owe most of my AP success to the previous year's slog through regular Chemistry. By the time I took AP Chem, all the basics were finally settled in my mind and I could hit the higher-level concepts that I’d only whiffed at the year before.

The second time I ran a marathon I had so much more fun — and so much more left in the tank for that last, terrible 10K.

The second time I read a paper from a new-to-me sub-discipline, or with specific, sophisticated statistical methods, I get a similar boost of adrenaline and understanding. These déjà vu methods* are often serendipitous — it’s hard to consciously search for them — but they are so rewarding when I stumble into them. Déjà vu methods struck PLoS ONE this winter in the form of land cover change captured in Landsat images. The Landsat program has been capturing satellite images of Earth since the 1970s, and researchers can compare decades of Landsat images to tell a time-lapse story of changing land cover at a high resolution. Two great papers used this method to explore trends in forest cover on opposite sides of the globe: New England in the United States and the Western Ghats in India. 

As I read Thompson et al.’s ‘Forest loss in New England: A projection of recent trends’ I could imagine the last twenty years of land cover change in my mind’s eye before even glancing at the figures. I’ve lived in New England nearly my entire life; I went to grad school in one of the three case study sub-regions, and worked college summers in another. The third case study sub-region is a long stretch of coastal Maine that I drove through every field season on my way to Acadia National Park. I’ve collaborated on remote sensing work, but it’s not my wheelhouse, so reading Thompson’s paper allowed me to enter this world in a really intuitive way because the results and projections already felt familiar to me. 

And then I read ‘Not seeing the grass for the trees: Timber plantations and agriculture shrink tropical montane grassland by two-thirds over four decades in the Palani Hills, a Western Ghats Sky Island.’ Here, Dr. Arasumani and a team of academic and non-academic researchers used four decades of Landsat images to quantify patterns of land cover change in grasslands, forests, plantations and agriculture in a region of southern India called the Palani Hills. This is a landscape that I could not imagine — fortunately Arasumani’s team collaborated with photographer Prasenjeet Yadav who created an amazing 4-minute film. This video is a fantastic introduction to the ecosystem with beautiful footage of the shola grasslands and shola forests. ‘Not seeing the grass for the trees’ is a response to the local perception that timber plantations have replaced shola forests in the sky island of the Palani Hills. Local conservation policies center on restoring shola forest trees, with little focus on the shola grasslands. So, a group of scientists began using Landsat to challenge the current conservation view. As Dr. Milind Bunyan and Dr. Robin Vijayan write, 

“The popular discourse that timber plantations are invading shola forests runs deep and wide, but there are exceptions to this observation. In the state of Kerala for instance, there is growing appreciation that it is the grasslands that have been lost to plantations and not the forests. The state that holds a majority of this ecosystem both in original and modified states (viz. Tamil Nadu) however, largely believes that plantations have invaded forests (although there are individuals in the state forest department who now recognize the loss of grasslands).”

Coauthor Robert Stewart and his late wife Tanya Balcar had been working in the Palani Hills since the 1980s: their Vattakanal Conservation Trust focused on forest and grassland conservation and they were among the first to notice that the grasslands were disappearing. The story of how Tanya Balcar’s observations snowballed into this paper is a lovely peek behind the curtain of conservation research: the collaborations, the shoestring budget, the surprises, and the great food all ring true to my experiences working with NGOs and government agencies in New England. Bunyan and Vijayan gave me a long version to edit down, but I love the details too much.

“[Tanya and Robert] convinced some of us who were working on different projects in this landscape including Ian Lockwood, a two-generation resident of Palani Hills, and a friend of Tanya & Bob. Using his skills as a geographer, Ian conducted a preliminary GIS analysis, which revealed the dramatic changes that had occurred during his lifetime; he then published these results on his blog. This caught our attention when we realized that much of the change in the landscape had occurred very recently, and providentially within the period of LANDSAT imageries.Anil and Sunayana Choudhary from INTACH Kodaikanal (listed in the acknowledgements) were the people who really made the project happen. They generated INTACH funding for the project to conduct fieldwork, and to hire a technician to do the GIS and ground-truthing. As with most research projects however, we did not stick to the script and ended up hiring two technicians (one for the lab and the other for the field), despite uncertainties at the time on how we would support both of them. Of these, Danish Khan came with a tremendous wanderlust and was therefore, the natural choice for our field component, and Arasumani M., who graduated at top of his class, was the lab person conducting the GIS analyses.The only thread that binds all of us is a desire to work in the landscape, albeit on varied aspects, and understand and document the threats and changes in this landscape, which required a baseline that we could use for future studies. This was an extremely frugal study, and most of us contributed significant amounts of time (and in some instances, money) to the project in different ways. With different roles on the project, we found working together relatively easy and complementary. A lot of our work also involved working different physical locations (including putting these responses to your questions together), and used cloud-platforms like Google Docs. We’re also proud to say that our meetings were almost like large family gatherings, full of great food (supplied generously by the Choudharies), and travelling through the landscape.”

Through Landsat images and ground-truthing, this team found that shola grasslands — the dominant cover type forty years ago — had been invaded by agriculture and plantations. Agriculture and plantations overran shola grasslands with different spatial patterns of replacement and degradation: agriculture takes over in “large, compact, and spatially aggregated patches” while plantations puncture the landscape with small, irregular-shaped patches as invasive plantation species spread into the ecosystem. This analysis also found that only half of the existing grasslands are currently included in the Kodaikanal Wildlife Sanctuary; they identified eight additional grasslands along cliff edges or bordering abandoned agricultural areas to include in this sanctuary.

Finally, the authors conclude with four specific conservation recommendations: (1) identify and conserve core grasslands (2) check invasion in sparsely invaded grasslands (3) review indiscriminate removal of mature plantations (4) contain agriculture. I asked Bunyan and Vijayan how these recommendations have been received by the Kodaikanal Wildlife Sanctuary and the local communities. They write “In addition to our town hall meetings, we have had several interactions with forest department staff of the KWS to disseminate our conservation recommendations. We opine that the Forest Department is positive, and we hope to work with them to be able to achieve the goals stated in the paper. The publicity that this article has generated, which has been covered in the national media and now internationally, will go a long way in promoting these recommendations.” 

I wish good luck to them as they continue this important work! And thank you for enriching my winter with beautiful images of the shola grassland!

References:

Arasumani M, Khan D, Das A, Lockwood I, Stewart R, Kiran RA, et al. (2018) Not seeing the grass for the trees: Timber plantations and agriculture shrink tropical montane grassland by two-thirds over four decades in the Palani Hills, a Western Ghats Sky Island. PLoS ONE 13(1): e0190003. https://doi.org/10.1371/journal. pone.0190003 

Thompson JR, Plisinski JS, Olofsson P, Holden CE, Duveneck MJ (2017) Forest loss in New England: A projection of recent trends. PLoS ONE 12(12): e0189636. https://doi.org/10.1371/ journal.pone.0189636    

* To expand on déjà vu methods, I present the thylacine. Last November I read a preprint of a paper on thylacine extinction; I don’t actually know anything about thylacines, but my friend Kevin Burgio was a coauthor, I had studied abroad in Australia when I was in college, and I thought it sounded cool. This thylacine paper introduced me to Bayesian Extinction Estimators and less than a month later, my PhD advisor published ‘A statistical estimator for determining the limits of contemporary and historic phenology’ — a paper that repurposed Bayesian extinction estimators for historical and herbaria-based phenology data. Reading the thylacine paper serendipitously primed me to fully understand this methodological approach for my own field (plant phenology). I'm not the brightest crayon in the box, but if I just keep reading déjà vu methods, I'll make it to razzmatazz.

Flying Foxes and Lilford’s Wall Lizards: At Your (Seed Dispersal) Service

I'm Dr. Caitlin McDonough MacKenzie, a new PLOS Ecology Community Editor. Last summer I was a PLOS Ecology Reporting Fellow at the 2016 Ecological Society of America meeting and I'm excited to join the team year-round! My first post as a Community Editor has me reflecting on my field site in the "off season", #poopscience, and the under-appreciated role of seed dispersers in ecology and conservation. Two papers dig into the seed dispersal services provided by charismatic megafauna in island ecosystems, and in both cases it's not much of an exaggeration to say: 'Save the Seed Disperser, Save the World.' 

I study plant phenology, specifically leaf out and flowering, on an island in Maine. I leave my field site just as flowers are senescing and unripe fruits are developing, and return again in early spring to catch the last patches of snow before the first green shoots emerge. I hardly ever think about what my plants are doing from July through April, but of course the ecological processes in these months — fruiting, seed dispersal, germination — underlie a fundamental assumption of my fieldwork: that there will be new plants each year when I return. I depart Maine and the seeds are just developing in green fruits, I arrive and new green stems are popping out of the soil, but in between seed dispersal was quietly a crucial, and perhaps overlooked, part of this circle of life. 

Two recentpapers in PLOS One highlight the seed dispersal services of charismatic megafauna in different study systems with implications for island conservation and habitat restoration. Both studies focused on the relationship between an animal seed disperser and a plant that prefers to grow in open, sunny environments. In Sa Dragonera Natural Park, on an islet in the Mediterranean off the coast of Mallorca, Dr. Constanza Neghme and her coauthors studied Ephedra fragilis, an evergreen shrub that produces pseudo-flowers and pseudo cones. E. fragilis is an early successional shrub, colonizing new areas and establishing in open ground without a “nurse” (for example, another plant) to provide shade and minimize water loss. So, E. fragilis seeds need to get to these open areas, away from the shade of their parents. In fact, seeds that were not dispersed, and landed below the parent plant, did not survive in Neghme’s study.

Dr. Ryszard Oleksy and collaborators worked in three forests in varying states of fragmentation and degradation across Madagascar, with a focus on fig trees: Ficus polita, F. grevei and F. lutea. These are all pioneer species, able to survive in degraded areas, and as their root systems penetrate hard substrates, they can improve aeration and drainage of the soil, facilitating the establishment of other plants. Fruiting fig trees depend on frugivores (fruit-eating animals) for seed dispersal, but rapid deforestation in Madagascar has decimated native wildlife populations, dramatically reducing animal-mediated seed dispersal. Dr. Neghme’s E. fragilis and Dr. Oleksy Ficus have particularly charismatic seed dispersers: wall lizards and flying foxes. The Lilford’s wall lizards (Podarcis lilfordi) are “superabundant” on Dragonera islet; they are endemic to the Balearic islands, but now extinct on nearby Mallorca and Menorca. Neghme reports that they are the only known seed dispersers of E. fragilis on the islet. In Oleksy’s research, the Madagascan flying fox (Pteropus rufus) is studied as a potential long-distance fig seed disperser. Madagascan flying foxes are the largest bat species on Madagascar. These frugivores crush fruit in their mouths to devour the fruit juice and soft parts (often including seeds), then spit out the fibrous fruit coating, not unlike my two-year-old eating blackberries. I’m sure she would love to eat figs with flying foxes if given the chance.

Both of these studies depend heavily on #poopscience. The #poopscience hashtag is popular among a certain segment of ecologists on twitter, and though the authors were unfamiliar with this term when I contacted them, they were universally enthusiastic to talk about their experiences in #poopscience. Neghme told me: “ My first time with poop science was when I was doing my bachelor thesis with lizard in high mountain ecosystems, I was helping a post doc and he encourage me to do questions by my own, then I saw the lizard poops carrying seed, and after reading an article from lizards as pollinators and seed dispersers in island ecosystems I started the journey in to poop.” Dr. Gareth Jones, the corresponding author on Oleksy’s paper, said that he’s “been into #poopscience for ages, initially using microscopic analyses to analyse prey of insectivorous bats, more recently using DNA barcoding to identify insects in poop to species level.”

To know what a seed disperser is eating, and to test the germination success of what Oleksy euphemistically calls “bat-processed seeds”, scientists collect and pick through lizard and bat faeces. Both studies planted “undispersed” (read: collected from parent plant) and dispersed (read: found in poop) seeds and tracked seedling emergence and seedling survival in a range of microhabitats. For both E. fragilis and the Ficus species, the “processed” seeds won. Lizard-dispersed and bat-dispersed seeds were much more likely to germinate, emerge, and survive as seedlings than the undispersed (non-faecal) seeds. Logically, the next question is where are the lizards and bats taking these seeds? We know you proverbially should not poop where you eat, but how far apart are the eating and pooping places of these lizards and bats? Neghme estimated how much time the lizards spent in different microhabitats on the islet, assuming that the proportion of time spent in each place would determine the probability of seed dispersal to those microhabitats. She and her colleagues walked transects and recorded if the lizards they spotted were in open areas, under Ephedra, or under other plants. The lizards spent most of their time in open habitats, and, unsurprisingly, this is where Neghme found the most lizard poop.

In Madagascar, 11 bats were outfitted with GPS devices, which tracked their movements overnight. These GPS tracks were combined with information about the bats’ gut retention time from a captive bat experiment. Basically, captured bats were fed a known quantity of fig seeds on banana slices and then researchers recorded the length of time between feeding and pooping, while counting the fig seeds present in each pooping event. (Ecology research can be especially glamorous.) Oleksy’s team then modeled the “seed shadow” of the bats’ flights — which is a nice way of saying they created a map showing where the bats were most likely to have pooped on the landscape. These “probable poop maps” confirm that Madagascan flying foxes are important long distance seed dispersers, and they frequently disperse seeds in degraded habitats as they fly between forest fragments. I love that both Neghme and Oleksy created sophisticated stochastic models of seed dispersal, and then ground-truthed them by walking through their field sites* and saying, “Yes. This is where the poop is.”

The ecosystem services provided by the E. fragilis shrubs on Dragonera and the Ficus fig trees on Madagascar are so important to habitat restoration and conservation. These early-successional species colonize open and degraded areas, and facilitate the growth and success of other, less-hardy plant species. But without their seed dispersers, they cannot access these open habitats and their seeds languish in the shade of parent plants. The Madagascan flying fox is listed as ‘Vulnerable’ in the IUCN Red List; Lilford’s wall lizard is ‘Endangered’. These seed-dispersing animals can act as super-conservationists: naturally maintaining and regenerating habitat through their poop. Neghme explained to me that the lizards are threatened by introduced predators and habitat loss, both “usual[ly] happen in island ecosystems to build tourist resorts.” In Madagascar flying foxes are legally hunted, and Oleksy notes that the “best protection would be to ensure that no one is allowed to hunt between August and December. Also no hunting at the roosting trees…Education would be a key to ensure local communit[ies] understand the role and importan[ce] of the bats.” The parallels between the lizards and the bats, the open-grown shrubs on Dragonera and pioneering fig trees in degraded Madagascan forests, run through these papers from study design to conservation implications. These strong relationships between plants and their animal seed dispersers highlight the importance of conserving species interactions for biodiversity maintenance and ecosystem functioning. Or as twitter might say: #poopscience can inform conservation! 

References:

Neghme C, Santamar ́ıa L, Calviño-Cancela M (2017) Strong dependence of a pioneer shrub on seed dispersal services provided by an endemic endangered lizard in a Mediterranean island ecosystem. PLoS ONE 12(8): e0183072. https:// doi.org/10.1371/journal.pone.0183072

Oleksy R, Giuggioli L, McKetterick TJ, Racey PA, Jones G (2017) Flying foxes create extensive seed shadows and enhance germination success of pioneer plant species in deforested Madagascan landscapes. PLoS ONE 12(9): e0184023. https://doi.org/10.1371/journal. pone.0184023 

*Note that ground truthing was limited by violence in Oleksy’s study. He explains: “at the time of the study south of Madagascar was at war with local rebels. I was based at Berenty Reserve which was rather safe, however due to the war we were not allowed to leave the reserve. We would still capture bats beyond its boundaries accompanied by a guard and ground truth in nearby areas. However, the more distant places to which bats flew were too dangerous to visit…Fortunately, we got enough data to analyse the GPS.” 

Leveraging the Power of Biodiversity Specimen Data for Ecological Research

A guest post from PLOS Ecology Reporting Fellow, Caitlin McDonough, on research from the Ecological Society of America Scientific Meeting in Ft. Lauderdale, Florida, August 7-11, 2016.

Leveraging the Power of Biodiversity Specimen Data for Ecological Research at ESA 2016 While ecologists spend their graduate days troubleshooting code, writing manuscripts, and fighting with dataloggers, they often trace their roots back to a love of natural history--an acknowledgement of a childhood curiosity sparked by museums, camping trips, and backyard bug collections. This curiosity ties us ecologists to a long line of scientists, taxonomists, and collectors; we imagine that we could have sailed on the Beagle, or climbed Chimborazo, or that we would have happily canoed the wild Allagash River to botanize with Kate Furbish. On Wednesday morning, a group of 21st century ecologists presented a modern twist on these natural history dreams, with research in collaboration with these taxonomists, botanists, and collectors of the past. (A video of the session will be posted here.) 

iDigBio (Integrated Digitized Biocollections) organized this session, which brought together a diverse array of ecologists who have leveraged the power of biodiversity specimen data to approach 21st century problems in taxonomy, conservation biology, and climate change research. Each project relied on some form of biodiversity specimen data — from herbarium specimens to insect collections to marine collections — for applications ranging from restoration ecology to unraveling cryptic speciation, or creating species distribution models to tracking patterns in phenology. Recent efforts to digitize biological specimen data have sparked a renaissance in their use — pressed plants and pinned bees that once sat neglected in a dusty corner are now accessible to researchers thousands of miles away. In many cases, the 19th century collectors would likely recognize these research goals as they too were interested in species distributions,  recorded phenological events, and made observations about interactions between herbivores and plants. But, Thoreau did not geotag his field notes, and Linneaus might be surprised to find his herbarium specimen available as a jpeg. The importance of making biodiversity specimen data digitally accessible was clear from the start of the session.

Pamela Soltis noted that there are over 1,600 natural history collections in the U.S. with somewhere between one and two billion specimens. But iDigBio estimates that only 10% of biodiversity specimens are digitized. Throughout the session, presenters noted both the benefits of accessing the digitized data and the challenges of working with taxa and trophic levels that were underrepresented in the digital specimen world. Katja Seltmann lamented the lack of digitized parisitoids collections, and called out a bias towards plants and pollinators. Joan Meiners, who uses digital natural history collection specimens to investigate native bee conservation, showed a graphic of the low proportion of digitized bee specimens at major U.S. insect collections. The next speaker, Francois Michonneau, topped both of their complaints with an example of a historic sea cucumber collection that had been preserved in pieces, the equivalent of an ornithologist placing a beak and talons in a glass bottle and calling it a bird collection.  It is clear that the biodiversity specimens that are digitized are inspiring new research. Emily Meineke shared the origin story of her herbaria research: her project began in her kitchen. While flipping through old specimen data online during a procrastination jag, she noticed herbivory damage captured in one of Linnaeus’ specimens. With a little more digging, she found evidence of herbivory in many specimens — leaf mines, chewing damage, and galls — as well as actual insects preserved in the old leaves. Another example of unintentional data captured in herbarium specimens is Amanda Gallinat’s fruit phenology study. She found over 3,000 specimens comprising 55 species in seven major New England herbaria that contained mature fruit pressed among the plant material. Just as Meineke realized that herbaria offer unprecedented opportunities to understand what factors drive herbivory rates across large spatial and temporal scales, Gallinat was able to assess patterns in fruiting across native and invasive species at a regional scale from the 19th century to the present. Meineke has begun surveying for herbivory damage in the Harvard University Herbarium collection, but she is also working to make this a citizen science project called Bite Marks in the Zooniverse. Soon everyone will have the opportunity to look at herbivory damage while procrastinating in their kitchens! 

In addition to the diverse research that has emerged from digitized biological specimens, this session provided some practical advice for all ecologists. Pamela Soltis presented Charlotte Germain-Aubrey’s project “Using museum data for species distribution modeling: The case of plants in Florida” and provided a thoughtful behind-the-scenes look at the building of a maximum entropy model. She deliberately explored the process behind decisions about climate data (e.g. average climate vs. climate data from the year of collection for each specimen), the area in which the model trains, smoothing response curves, and the number of background points. François Michonneau closed his talk with a great overview of his best practices for instituting data quality checks in R code workflow. While these skills are typically missing from our training, he stressed the importance of building a culture of documentation and replication, recommending courses from datacarpentry.org. Katelin Pearson showed that the collector community — a group that is regularly in the field, well-trained to recognize patterns and norms, and communicate with other experts — currently lacks the protocols and the semantics to document outliers in a consistent, meaningful way. This community has great potential to detect outliers in phenology, distribution, ecology, behavior, morphology, but at the present there is no direct feed between the collectors and ecologists who are tracking changes or outliers.

Finally, Libby Ellwood closed the session with an overview of iDigBio’s citizen science projects to engage the public in the work of digitizing the many, many biological specimens that are not yet a part of the digital record. 

Caitlin McDonough MacKenzie is a PhD candidate in the Primack Lab in the Biology Department at Boston University. She spends her field seasons in Acadia National Park, Maine studying leaf out and flowering phenology and patterns of historical species loss across plant communities. Her field methods include three ridge transects that are conveniently located adjacent to beautiful running trails and carriage roads. Away from Acadia’s granite ridges, she’s interested in underutilized sources of historical ecology data including herbarium specimens, field notebooks, photographs, and old floras; the potential for citizen science in phenology research; and the intersection of science and policy.  (Follow Caitlin on Twitter @CaitlinInMaine)