Thanksgiving Reading List

Last November, Binghamton Unversity-SUNY’s WHRW station shared this message as part of their program ‘Broadcasting World Literature’: “Today, since it’s Thanksgiving week, I thought it would be good to start off with a reading or just do a reading of a native scholar’s take on giving thanks.” Daimys Garcia explains before she begins reading from Robin Wall Kimmerer’s Brading Sweetgrass,“It’s important to remember that Thanksgiving has history that’s rooted in genocide, colonization, and oppression of native peoples on this land so I thought it’d be great to read a piece by a native scholar who is thinking about thanksgiving not as the holiday but in the act of giving thanks.”

Garcia’s reading of the chapter ‘Allegiance to Gratitude’ is so beautiful — I cannot recommend listening to this episode of 'Broadcasting World Literature' enough. I echo Garcia’s sentiments that in Thanksgiving week, and Native American Heritage Month, we remember the history of this landscape, the indigenous people who were here and live here still, and the food that we’ve done our best to re-brand as thoroughly Americanized. 

Whether your preparations for Thanksgiving break involve long lists of ingredients for baking marathons, hamstring stretches for turkey trots, or stacks of lab reports for grade-a-thons, somehow we have arrived in late November. I pulled together a list of on-theme academic papers to keep your cocktail hour anecdotes accurate and your sidebars over the side dishes peer-reviewed.

Here is a totally non-thorough, mostly-ecological literature review of turkeys (and the extinct poultry you might expect on a more or less accurate Thanksgiving spread), cranberries, sweet potatoes, and…ptarmigan. But — before you dig into this feast of a reading list, remember Rule 7: Respect working hours, public holidays, and vacations. This is from the recent PLoS Computational Biology paper, Ten simple rules towards healthier research labs. “Working rules commonly in place in labs around the world often mean that academics work all day long, on weekends, and even during holidays,” the author, Dr. Fernando Maestre, writes. “The stress associated with this excessive work without a life outside the lab is one of the main reasons behind the increase in mental problems in academia, particularly among early career researchers and young PIs.”

You, my friend, are ahead of the game. Relaxing with a little blog reading before Thanksgiving and making excellent life choices. Well done! 

First, Americans check out turkeys on Wikipedia in November in alarming numbers. Dr. John Mittermeier and coauthors report that “pageviews for wild turkey Meleagris gallopavo show a seasonal peak in the spring and a sharp peak during the Thanksgiving holiday in the US.” This idea — that Americans are reading up on Thanksgiving turkeys year after year — was part of the inspiration behind Mittermeier’s PLOS Biology paper A season for all things: Phenological imprints in Wikipedia usage and their relevance to conservation.

If you aren’t convinced of the cultural relevance of turkeys, or question how much Americans love to look up turkeys on the internet, consider the fact that a recent PNAS paper, Characterizing the cultural niches of North American birds, had to treat google searches of turkeys as an outlier. In the Methods, they report, “After assembling estimates of relative interest for all 622 species, we normalized values so that bald eagle, the second most popular search topic, was assigned a value of 100, and all other taxa were assigned values proportionally. Wild turkey was the focus of more interest than bald eagle, but we considered the species an outlier (i.e., it received more than an order of magnitude more searches than bald eagle) and did not include it in our core analyses.” 

This turkey obsession is interesting in part because it begs the question, what are we learning from Wikipedia? I recently found this tidbit on the Wikipedia page for heath hens (Tympanuchus cupido cupido) “Heath hens were extremely common in their habitat during Colonial times, but being a gallinaceous bird, they were hunted by settlers extensively for food. In fact, many have speculated that the Pilgrims' first Thanksgiving dinner featured heath hens and not wild turkey.” Here’s the deal though: heath hens were about two pounds. The last population of heath hens lived (& died) on Martha’s Vineyard. I as wrote last month, I have a long-buried ecological connection to Cape Cod and its offshore islands, so while most college kids bring the emotional baggage of Pysch 101 to the Thanksgiving table, I was the know-it-all who threw down random historical ecological nuggets such as, it is unlikely that heath hens or their grassland habitats were as common in early colonial Massachusetts as some historical sources would have you believe. The story that servants refused to eat them multiple times a week is probably apocryphal. You see, I had read Interpreting and conserving the openland habitats of coastal New England: insights from landscape history in Forest Ecology and Management and — this was likely more influential since I was legitimately bad at reading papers until late in grad school — taken a seminar with the author Dr. David Foster. The paleoecological evidence does not support extensive openland vegetation in coastal New England until after European arrival. The landscape was mostly forest, and according to the preeminent expert on heath hens (here Foster and Motzkin throw in a wonderful citation from a 1928 Memoirs of the Boston Society of Natural History, definitely going in my #ToReadPile), the birds actually preferred, “open sandy woods and scrub oak barrens rather than grassland.” I love roping my family into this kind of argument and I am a lot of fun at parties. 

But back to turkeys — I found two more great turkey papers when I searched through my records in Papers (my reference software of choice). I was a bit confused when the results included a 1943 paper in The Condor titled, “Birds Observed between Point Barrow and Herschel Island on the Arctic Coast of Alaska.” It turns out that the author, Dr. Joseph S. Dixon, was comparing male ptarmigans to turkeys: “Ptarmigan were a most important food item after a winter of fresh meat starvation. By May 13, 1914, at Humphrey Point, the males were in full breeding plumage. They cackled and strutted about like diminutive turkey gobblers. From far and near their calls were heard over the snowy plain between the sea coast and the foothills.” 

If you want to go on a fascinating deep dive into the history of turkey husbandry before European settlers arrived to kick off a genocide, barely survive a winter, and two hundred years later get a national holiday declared during the Civil War, I recommend Dr. Erin Kennedy Thornton’s 2012 PLoS ONE paper Earliest Mexican Turkeys (Meleagris gallopavo) in the Maya Region: Implications for Pre-Hispanic Animal Trade and the Timing of Turkey Domestication. Thornton and her coauthors leverage archaeological, zooarchaeological, and ancient DNA evidence to confirm that Mayans in present-day Guatamala were raising domesticated turkeys. These turkey remains were discovered well south of the natural geographic range of the Mexican turkey, Meleagris gallopavo, which is the wild progenitor of what we know today the turkey on the Wikipedia page we check out every November — indicating that northern Mesoamerica and Maya cultural regions were engaged in animal trade as early as 300 BC–AD 100. They write, “prior information on Preclassic exchange comes primarily from non-perishable goods such as obsidian and ceramics so the non-local turkeys at El Mirador also expand our understanding of the types of goods that were exchanged long distances during this early period of Maya history.” Traveling long distances for turkey dinner is not a new idea. Mayan culture was holding it down well before the Spanish arrived and they didn’t even need to refer to a Wikipedia page each fall to get it done. 

If you are looking for a paper to pair with your ancient turkeys, consider Historical collections reveal patterns of diffusion of sweet potato in Oceania obscured by modern plant movements and recombination. In this 2013 PNAS paper, Dr. Caroline Roullier and her coauthors assessed genetic diversity in modern and herbarium samples of sweet potato (Ipomoea batatas) and confirmed that well before Columbus' time, Polynesian and South American peoples were sharing sweet potatoes. I love the subsection, “Did Genes and Names Disperse Together?” and the idea that linguistics is a kind of sleeper science — that names can keep information even while recombined genotypes and colonialism obscure the data. This is another powerful story of culture and food enduring; the spread on our dinner table for a celebration of settler colonialism can also be a story of resistance and resilience. 

Don’t forget the cranberry sauce! It’s mountain cranberry actually, since I’m an alpine ecologist. Mountain cranberry, Vaccinium vitis-idaea, is the berry behind the beloved Ikea treat, lingonberry preserves. According to a 2017 study in Biological Conservation by McDonough MacKenzie et al. (yes, that's me), volunteers struggle to identify mountain cranberry in a citizen science project recording flowering phenology above treeline. If you want to brush up on your plant ID skills before you hit the dinner table this year, check out the supplementary materials from Lessons from Citizen Science: Assessing volunteer-collected plant phenology data with Mountain Watch — it’s a page of photos of alpine plant species and their look-alikes. Honestly, if you have a laminator lying around this could be a really beautiful Thanksgiving placemat*. Do you think google scholar counts placemats towards your h-index? 

One last Thanksgiving resource. If you are struggling with how to talk to your family about climate change, Katharine Hayhoe has a webinar for you. Seriously, let's talk about climate change. This is tougher than checking out the wikipedia page for turkeys, but definitely a more meaningful discussion than the twenty-two-year-old at the table trying to school you about a heath hen you have never heard of and never claimed to be at the first thanksgiving anyway. Man, I am so much fun at parties. 

References:

Dixon, J. S. (1943). Birds Observed between Point Barrow and Herschel Island on the Arctic Coast of Alaska. The Condor, 45(2), 49–57. http://doi.org/10.2307/1364377

Foster, D. R., & Motzkin, G. (2003). Interpreting and conserving the openland habitats of coastal New England: insights from landscape history. Forest Ecology and Management, 185(1-2), 127–150. http://doi.org/10.1016/S0378-1127(03)00251-2

Garcia, Daimys, "Episode 9: Rethinking Thanksgiving: A Reading of "Allegiance to Gratitude" by Robin Wall Kimmerer" (2018). Broadcasting World Literature. https://orb.binghamton.edu/broadcasting_world_literature/9

Maestre, F. T. (2019). Ten simple rules towards healthier research labs. PLOS Computational Biology, 15(4), e1006914–8. http://doi.org/10.1371/journal.pcbi.1006914

McDonough MacKenzie, Caitlin, Georgia Murray, Richard Primack, and Doug Weihrauch. 2017. Lessons from Citizen Science: Assessing volunteer-collected plant phenology data with Mountain Watch. Biological Conservation, 208, 121-126. http://dx.doi.org/10.1016/j.biocon.2016.07.027

Mittermeier, J. C., Roll, U., Matthews, T. J., & Grenyer, R. (2019). A season for all things: Phenological imprints in Wikipedia usage and their relevance to conservation. PLOS Biology, 17(3), e3000146–12. http://doi.org/10.1371/journal.pbio.3000146

Roullier, C., Benoit, L., the, D. M. P. O., 2013. Historical collections reveal patterns of diffusion of sweet potato in Oceania obscured by modern plant movements and recombination. PNAS. http://doi.org/10.5061/dryad.77148

Schuetz, J. G., & Johnston, A. (2019). Characterizing the cultural niches of North American birds. PNAS, 205, 201820670–6. http://doi.org/10.1073/pnas.1820670116

Thornton, E. K., Emery, K. F., Steadman, D. W., Speller, C., Matheny, R., & Yang, D. (2012). Earliest Mexican Turkeys (Meleagris gallopavo) in the Maya Region: Implications for Pre-Hispanic Animal Trade and the Timing of Turkey Domestication. PloS One, 7(8), e42630–8. http://doi.org/10.1371/journal.pone.0042630 

*In putting together this post, I found an error in my supplementary materials! If you can find this mistake on your placemat, send me an email and I'll reward you with a Plant Love Stories sticker!

Looking for Human-Nature Connections in Seasonal Wikipedia Searches

Recently, I was wrapping up some revisions on a phenology paper and to comply with the journal’s style for taxonomy, I needed to know the authority on a species of white violets that a Maine hunting guide had noted in his diaries in the mid-twentieth century. Obviously, I turned to Wikipedia.

Ecologists who study phenology (or anything!) use Wikipedia all the time, but Dr. John C. Mittermeier and his coauthors take this practice to a whole new level in their paper A season for all things: Phenological imprints in Wikipedia usage and their relevance to conservation. This study, published in PLoS Biology earlier this month, uses Wikipedia page views to trace when humans show seasonal interest in the natural world. For over 30,000 species in 245 languages —which amassed 2.33 billion pageviews between July 2015 and June 2018 — they found some strong seasonal signals linking how and when people interact with plants and animals online.

“The idea for this study happened somewhat by chance to be honest,” Dr. Mittermeier confides. “I was collecting Wikipedia pageview data on different animals as part of another study (hopefully this should be published soon!) and on a whim I decided to plot a time-series of daily views to see what it looked like.” As an ornithologist, he was drawn to migratory bird data and his whimsical time-series plot for migratory bird page views peaked near its ecological migration season. This was the prototype for a figure in the PLoS Biology paper. Mittermeier says, “this [plot] made me curious as what other plants and animals might show seasonality in their views and how widespread these patterns might be in general.”

While searching for migratory birds on Wikipedia seems categorically different from actual birding, Mittermeier and his colleagues found strong correlations between these two activities. They compared trends in Wikipedia page views to eBird records. In this analysis, eBird frequency records are like “outdoor pageviews” of bird species. “It was easy to match the eBird taxonomy to the taxonomy used by Wikipedia,” Mittermeier says, “and the way in which seasonal abundance information was structured in eBird is very accessible.”

Birders, like Wikipedia users, are surprisingly great at generating big data. Just under half of the bird species in the dataset had page view patterns correlated with seasonal eBird records. But, for species that occurred in more than one of the four language/countries (Italy, Germany, Sweden, and the U.S.), just over a third showed a significant positive relationship between eBird frequency and pageviews across multiple languages. All of the countries in this analysis are in the northern hemisphere and experiencing basically the same seasons, so I asked Mittermeier if this result indicated that some birds are more "seasonally famous" in one location? He agreed that “some species do seem to be more “seasonally famous” than others, meaning that certain species may be viewed more as seasonal indicators. This could be a result of the behavior of the species (i.e. something about their seasonality is particularly visible and obvious), some sort of cultural context (maybe the species featured in a well known book or fairy tale and had a seasonal association there, for example), or some sort of combination of both of these. Comparing how seasonal indicator species are similar or different across languages would be a great way to gain insight into what leads to a species acquiring this significance. I think this is a fascinating question and one that would be very interesting to explore further.” 

But, the paper is not limited to birds, and human interest in animal and plant Wikipedia pages is not always aligned with ecological events. Figure 2 shows a spike in shark species page views that aligns with Shark Week. There are cultural drivers to the phenology of when humans search out certain species on Wikipedia. Mittermeier shares that, “The Wild Turkey was actually the first page that I looked at in relation to cultural events. Turkeys have such a powerful association with the Thanksgiving holiday in the United States I was curious as to whether this would impact people’s online searches (it does as we show in the figure!)” When the turkey hunch worked out, Mittermeier started brainstorming other cultural or marketing events associated with plants or animals that could impact online interest. “This was right around the time that Shark Week was going on over the summer and that’s why I decided to check if that had an impact on pageviews for Great Whites.”  

While the eBird community is full of self-proclaimed bird nerds, and eBird datahas been used inpeer-reviewed papers for over a decade, the programming around Shark Week has a decidedly different relationship to science and natural history. Dr. David Shiffman, a Liber Ero Postdoctoral Fellow in Conservation Biology at Simon Fraser University, studying how information related to sharks is spread on the internet, notes, “Shark Week has a well documented problematic relationship with the truth, spreading nonsense to its massive audience that I and other scientists have to spend years correcting.” I asked him what he thought about the Wikipedia-Shark Week connection that Mittermeier and coauthors uncovered. He says, “the temporary spike in public interest in sharks that Shark Week causes is something that the marine biology community takes advantage of to spread actual facts. This paper provides further evidence that scientists wishing to engage in public outreach about their area of expertise need to know their audience, and know that there are times of year when people are more likely to be receptive to learning about that topic!” Indeed, these seasonal patterns in interest — whether for migratory birds, Thanksgiving turkeys, or sharks — can be leveraged by conservation practitioners to affect policy and outreach.

Research into the public attitudes about species, including how they rise and fall seasonally, is important. Mittermeier and his coauthors write: “Seasonal changes in human interest in plants and animals can have an important role in conservation in at least three ways: (a) by identifying species for which phenology forms a component of their “value,” (b) by helping to reveal differences or similarities in how species are valued across cultural groups, and (c) by providing temporal awareness to help maximize the effectiveness of conservation marketing campaigns.” I’ve experienced this myself in a small way: when I publish papers on spring wildflowers in the dead of winter, the press releases don’t get much traction. 

And finally, I had to address the paradox of scholarly work based on Wikipedia. I’ve TA-ed intro Biology labs and scrawled “not peer-reviewed” next to many Wikipedia-base citations in lab reports. Mittermeier laughed with me, “My mother used to teach junior high school and was always telling her students not to cite Wikipedia and now here I am using it as the source for my research.” 

Reference:

Mittermeier JC, Roll U, Matthews TJ, Grenyer R (2019) A season for all things: Phenological imprints in Wikipedia usage and their relevance to conservation. PLoS Biol 17(3): e3000146. https://doi.org/10.1371/journal.pbio.3000146 

Bumble and Bumble: what’s black and yellow and maybe more than one species?

During the dark afternoons of December in New England, I like to scroll through my old field photos and think of all the green, growing things I’ve measured in beautiful places during those long-ago long-lit seasons. Yesterday I flipped through a couple field photos from a friend — “Photos of younger Jon! :)” he wrote in the email — and the same sunny feelings flooded in.

As a master’s student*, Dr. Jon Koch and his insect net chased bumble bees all over the western United States. He was studying bumble bee decline, but hit weird hurdle: a messy species boundary between two bumble bees. Taxonomists and field guides were torn on whether Bombus fervidus was or was not Bombus californicus. These two “species” in the Bombus fervidus species complex were nearly morphologically identical, except for their color patterns: B. fervidus is noted as usually mostly yellow with a little black, while B. californicus sports mostly black with some yellow in variable detail. They were maybe different species, maybe hybridizing, or maybe the same thing with different color morphs. As Jon explained to me, “If we don’t know what the species are, how will we manage them? Bumble bees are differentially sensitive to land use change, disease, etc. The bumble bees in the Bombus fervidus species complex are found to be impacted by one disease, Nosema bombi, but perhaps differently. Therefore, it is important to recognize what the species boundaries are because estimates of infection prevalence might be not be done correctly due to the inability to tell the species apart.” 

Jon wanted to bring some clarity to the species complex by providing some new molecular evidence with broader taxa sampling. His new PLoS ONE paper, “Phylogeny and population genetic analyses reveals cryptic speciation in the Bombus fervidus species complex (Hymenoptera: Apidae)” delivers on the broader taxa sampling — 320 specimens from 53 sites — but the clarity is a bit of a cliff hanger. During the fieldwork, Jon and his coauthors keyed out identifications for their bees based on the setal color, and also took a tarsal clipping from the mid-leg for DNA extraction and microsatellite genotyping. When they compared field identification to the genotypes, they had an ID rate of just under 94%. Jon and I agree that that’s a pretty good record for fieldwork with cryptic species** but he adds, “it’s also cool to think that 6.2% of the time we were wrong! These bees are great at fooling us.” 

The bees that were fooling Jon were B. fervidus dressed as B californicus and vice versa. In Pinnacles and Yosemite National Parks there were ten mostly black bees (the typical B. californicus look) that turned out to belong to the genetic cluster that usually wears mostly yellow. The rest of the bees with black setal coloration belonged to another clade based on genotype, though this clade also included some bees in yellow. I asked Jon, “What is going on with the bee costume parties in Pinnacles and Yosemite?” His wild speculation is that little black dress is the dominant phenotype for bees in these parks, and the typically-yellow-genotype wears black here because everyone else is doing it: “bumble bees are notorious for converging on a local phenotype, which can even make it very hard to tell distantly related species apart.” However, in the sites where both genetic clusters of the B. fervidus species complex overlap, they usually do not look alike, so they aren’t mimicking each other. 

Ultimately, Jon’s team determined that the species complex comprised two lineages, but that both lineages exhibit the yellow and black phenotypes depending on geography. So while the B. fervidus species complex is not a single species, B. fervidus and B. californicus are not NOT conspecifics. Jon explains, “those names [B. fervidus and B. californicus] might not even be valid! The holotype of B. californicus happens to be where the genotype assigned to the “B. fervidus” was collected in the Sierra Nevada.” In short, the original bee that taxonomists knew as B. californicus may actually be genetically on the B. fervidus side of the lineage, and eventually one or both names might need to be thrown out.

This “it’s complicated” conclusion might be depressing news for someone who dedicated so much time and energy towards disentangling the species complex, but Jon closes his email to me with a happy emoji “nature has so many surprises, and science is an ongoing process :)” In the meantime, this paper points out that even if we don’t have the right names in place, we know enough to recommend that managers use Jon’s non-lethal method of clipping a bit of mid-leg for genotyping, and monitor the two clades of the B. fervidus complex separately. This is a great reminder for all of us in conservation research: we need to keep the ongoing process in perspective, while also delivering our findings, however not-quite-as-clear-as-we-hoped or maybe-unnamed as they may be, to our partners in management and policy. 

References:Koch JB, Rodriguez J, Pitts JP, Strange JP (2018) Phylogeny and population genetic analyses reveals cryptic speciation in the Bombus fervidus species complex (Hymenoptera: Apidae). PLoS ONE 13(11): e0207080. 

*Now, old Jon and old Caitlin are David H. Smith postdoctoral fellows together :)

**see McDonough MacKenzie et al. 2017 — When I was a master’s student working with volunteer-collected data I would have killed for a 93.8% identification rate. One my species, Labrador tea, was correctly identified 27.3% of the time. This is not a cryptic species; it doesn't sometimes dress up as Diapensia. 

Summer Reading (Part 1)

We’re rushing out of the dog days of summer and into the start of a new semester — or in my case the start of parental leave, which is a little bit like embarking on a new semester at an unknown campus and while I completed the newborn syllabus three years ago, I have this sinking feeling that I don’t even know which classes I’m enrolled in yet. Regardless, I’m reflecting on my summer reading.

Over June, July, and August, I was all in on #365papers and I have a top ten list of scientific papers from these long summer days of slow reading. Because my “semester” might start at any moment, I’m breaking this post into two parts. First up: my favorite hot-off-the-press summer reads on mountains and phenology.

On Mountains

Think globally & way into the past…

1. Iglesias, V., Whitlock, C., Krause, T.R., Baker, R.G., 2018. Past vegetation dynamics in the Yellowstone region highlight the vulnerability of mountain systems to climate change. Journal of Biogeography 45, 1768–1780. doi:10.1111/jbi.13364

Fifteen pollen records covering 16,000 years and the 80,000 km2 mountainous Greater Yellowstone Ecosystem create an incredible review of elevational patterns of vegetation change in an iconic mountainous region. In this paper, Dr. Virginia Iglesias lays out the challenges of quanitifying pollen-vegetation relationships in mountain regions (aka what I didn’t know when I proposed my postdoc research) and then pulls in a staggering amount of modern and fossil pollen data to recreate the history of Yellowstone’s dominant conifers. These are stories of both stability and rapid change through past climatic changes with conservation implications for managers facing anthropogenic climate change. My favorite line: “The current vegetation distribution is, at best, a short and rather anomalous baseline for evaluating ecological responses to future climate change.” 

2. Elsen, P.R., Monahan, W.B., Merenlender, A.M., 2018. Global patterns of protection of elevational gradients in mountain ranges. PNAS 115, 6004–6009. doi:10.1073/pnas.1720141115

This study has it all: mountain biodiversity love, protected area planning, big data analysis, and beautifully designed maps of “elevational protection” across the globe. Full disclosure: Dr. Paul Elsen is a fellow Smith Fellow and I also got to see this paper as a speed talk at the North American Congress for Conservation Biology in July. The bottom line is this: when you zoom out, most of the world’s mountain ranges are narrowly protected — we need conservation across elevation gradients to effectively protect species under climate change. 

On Phenology 

Wherever you get your phenology data (maybe from TV?) scientists are asking some really interesting questions about community composition, temporal dynamics, and the implications of climate change on interspecific relationships…

3. Carter, S.K., Saenz, D., Rudolf, V.H.W., 2018. Shifts in phenological distributions reshape interaction potential in natural communities. Ecology Letters 30, 133–9. doi:10.1111/ele.13081

Amphibian breeding phenology is not the kind of phenology that I study — I don’t install recorders at ponds to capture EPs of overnight breeding calls, I don’t log hours listening to the audio to identify twelve different amphibian species and record the number of individuals per species calling during each recording session, and I certainly have not done this tirelessly for fifteen years. But I’m so glad that Dr. Shannon Carter and her colleagues did because their ingenuous analysis of changes in the timing of calling between pairs of amphibian species has huge implications for how we — plant phenology people included! — study phenological mismatch. The overlap (or "phenological distributions") of amphibian breeding calls has shifted in weird and non-uniform ways, and metrics like ‘first day of calling’ or ‘median call date’ don’t capture these changes well. This is just a great analysis of a grinder ball dataset (8 ponds in Northeast Texas, monitored consistently over 15 years) which opens up a window to these big questions — How do we monitor phenology? What information do we need to know that temporal mismatch is occurring?

4. De Frenne, P., Van Langenhove, L., Van Driessche, A., Bertrand, C., Verheyen, K., Vangansbeke, P., 2018. Using archived television video footage to quantify phenology responses to climate change. Methods Ecol Evol 149, 1791–9. doi:10.1111/2041-210X.13024

Dr. Pieter De Frenne and his coauthors have received tons of press coverage (best sub-headline: "ignore the lycra—look at the flowers") for this incredibly photogenic work. They basically watched 200 hours of TV (old coverage of the Tour of Flanders), justified this as “research” by grabbing screen shots of 46 shrubs and trees from along the cycling course, and found surprisingly strong advances in the timing of spring leaf out and flowering in these plants over the years. This is, on one level, the opposite of Carter et al listening to frog calls for fifteen years — the phenology monitoring here is opportunistic and there is only a single metric each year (what was happening on the day they filmed the Tour). But as De Frenne points out at the end of the paper: “Probably the most promising way forward for phenology research is to better integrate all types of phenology data…observational time series, experimental manipulations of climate, herbarium records, historical surveys of vegetation, historical maps, repeat photographs and other, yet unexploited, sources such as television video footage from broadcast archives.” 

5. Winkler, D.E., Butz, R.J., Germino, M.J., Reinhardt, K., Kueppers, L.M., 2018. Snowmelt Timing Regulates Community Composition, Phenology, and Physiological Performance of Alpine Plants. Front. Plant Sci. 9, 631–13. doi:10.3389/fpls.2018.01140 

Dr. Daniel Winkler, PLoS ESA Reporting Fellow 2016, tweeted out his new paper in July and he had me at “community composition, phenology, and physiological performance of alpine plants.” My “alpine-ish” communities include true alpine on Katahdin, but also Cadillac Mountain in Acadia, which is a whopping 1,530’ and more accurately described as ‘Northern Appalachian-Acadian Rocky Heath Outcrop’ by NatureServe. I’m definitely interested in the differences between alpine-restricted species and wide-ranging species. Winkler’s team recorded species diversity, flowering phenology, and physiological measurements including gas exchange, net CO2 assimilation, and stomatal conductance across plots along an elevation and aspect gradient in the Colorado Rockies. Two results jumped out at me: the alpine-specialists displayed less flexible flowering phenologies than the wide-ranging species, but there were not strong differences between these groups in physiology. This is the kind of paper that inspires mad grant writing — I'm interested but skeptical, will this hold up in my pet region/ecosystem/study system? I want to replicate this kind of research in the Northeast — and across a gradient of sites where phenology is tied to snowmelt (true alpine areas of Katahdin and the Presidential range), and where the two are (I think) decoupled (Cadillac Mountain). Winkler and I wrote a blog post together in 2016, I think I can convince him to collaborate on a larger scale — and get him to New England! 

Bonus “Reads”

Recent podcast episodes tangentially related to recent blogging

• This American Life covers The Feather Thief. My review of the book.

• Outside/In reports on underrepresentation in outdoor gear (aka 'shrink it and pink it' does not make women happy shoppers, especially when we can't find our sizes, preferred styles, or performance level). This touches on some of the same themes — inclusion & diversity in the outdoors — as my response to “Have Ecologists Lost Their Senses? Walking and Reflection as Ecological Method”

Hidden in Plain Sight: the Secret Tree Diversity of Cultural National Parks in the East

Last summer, my daughter received All Aboard! National Parks, a whimsical board book that devotes full-page spreads of colorful, kid-friendly illustrations to nine National Parks along a fictional railroad route. The National Parks skew western — Olympic, Yosemite, Yellowstone, Grand Canyon — with Acadia and Great Smoky Mountains representing the entire eastern half of the U.S. But, the book is a skewed representation of the National Park System in another way too: it only showcases the large, iconic, and “wild” national parks. Where are the National Battlefields, the National Recreation Areas, the National Scenic Rivers, and the National Historic Sites?

A recent paper from Forest Ecology and Management has me thinking that the cultural parks of the east that fall under the National Park Service umbrella deserve their own board book!

In the eastern United States, our National Parks dot the landscape as constellations of historic battlefields, homes of important historical figures, and wild islands of nature scattered across an eastern seaboard of cities, development, and fragmentation. But, it turns out that these small, cultural protected areas are harboring incredible tree species diversity. Dr. Kathryn Miller and colleagues from the National Park Service and University of Maine published “Eastern National Parks protect greater tree species diversity than unprotected matrix forests” after comparing tree species diversity measured in National Park Service Inventory & Monitoring plots to the species diversity recorded in nearby US Forest Service Forest Inventory and Analysis plots. Miller considered five metrics of diversity in each plot — number of individuals, tree species richness (how many species were in each plot?), Shannon evenness (are the species in the plot relatively as abundant as each other or are some super common and others very rare?), McNaughton Dominance (what is the relative abundance of the two most abundant species?), and Percent Rare N/S (what percent of species in a plot have fewer individuals than the average species abundance in that plot?).

The title of Miller's paper is a spoiler alert — the parks were more diverse than the matrix (non-park) forests — with park forests comprising higher species richness and a more even, less dominated distribution of abundance across species. She found this pattern of higher species diversity across the majority of the parks in the study, but it was most consistent in the lower latitude parks. Over a decade of publicly available data from the National Park Service’s Inventory & Monitoring plots and the Forest Service Forest Inventory and Analysis plots allowed Miller and her team to explore tree species diversity across 39 eastern National Parks, each containing between 4 (Sagamore Hill National Historic Site) and 171 (Acadia National Park) forest plots. Before Dr. Miller began her PhD at UMaine, she led field crews that collected some of the data in the National Park Service Inventory and Monitoring Program. Miller told me, “My field experience sampling and hiking around eastern forests has definitely helped me frame the types of research questions to ask, and interpret whether the results are meaningful. When I started this study, I suspected that at least some of our parks, particularly the larger ones (e.g. Delaware Water Gap National Recreation Area, New River Gorge National River), would have greater tree diversity. I was surprised, however, to find out that many of our cultural parks, which tend to be smaller and haven't been protected as long, also have greater stand-level tree diversity than matrix forests.”

Miller’s results are both expected and unexpected. First, there’s a general understanding among ecologists that eastern US forests today are smaller, younger, and more homogenous than they were before centuries of European settlement, land clearing, and timber harvesting. And, we know on a basic level that forests in US National Parks are largely protected from development and harvesting. So, it shouldn’t be shocking to find that forests managed by an agency that is dedicated to promoting ecological integrity and natural disturbance regimes are full of lots of species — not just the early successional ones. But, on the other hand, we often don’t imagine Minute Man Historical National Park — a battlefield replete with actors in Revolutionary War costumes — as bastion of biodiversity. Or, in the case of All Aboard! National Parks, we don’t imagine these cultural parks as national parks at all. So how did Miller land on this question — what made her interested in comparing the tree species diversity in parks and unprotected forests in the east? She muses that “this research question in particular was a follow-up to [our 2016 Ecosphere paper] "National parks in the eastern United States harbor important older forest structure compared with matrix forests" which compared metrics of forest structure in eastern national parks with surrounding matrix forests.” In that study, she found that “parks, regardless of park designation (e.g. National Park, National Recreation Area, or National Historical Park), had consistently older forest structure than matrix forests.” Were these older forests also more diverse? The same forest plot databases could answer that question as well! 

I asked Miller if her research changed her view of the ecological value of cultural national parks. “For me, the results of this study were very encouraging, and confirmed that our efforts to monitor and keep even the smallest parks' forests healthy are worthwhile. I am hopeful that the results of these studies are empowering to the resource managers in our cultural parks, and lead to stronger emphasis and additional resources for maintaining healthy forests in these parks. Ultimately our research also makes a strong case for the importance of protected areas in preserving forest biodiversity, even small urban parks.”

This research seems relevant to managers outside of National Parks as well — and Miller hopes that private landowners, state parks, and NGOs take note. She recognizes that resilience to global change is a big contemporary concern for many land managers. “In forests, tree diversity and structural complexity are important components of resilience, and our results demonstrate the positive influence that protection, particularly protection from logging, can have on forest resilience. In addition, park managers often receive pressure from well-meaning members of the public, and even other park staff to "clean up" forests after natural disturbances. In fact, this was typical management practice in the early days of national parks before we knew better.” She tied together her species diversity and forest structure research and reflected that, “coarse woody debris, dead and dying trees, and blow-downs all contribute to the overall diversity of a forest, and our research has shown that protected forests have more of these features than unprotected forests. Hopefully our research can help inform and support managers' decisions not to clean up after disturbances unless there is a concern about human safety (e.g. hazard trees).” Miller and I both work in Acadia — the kind of classic wild National Park that appears in our imaginations and children’s books as an iconic protected landscape. But as Miller points out, “Interestingly, Acadia National Park did not come out as being more diverse than surrounding matrix forests, particularly because the park has more extensive late successional forests that are largely dominated by red spruce.” She explains, “this isn't necessarily a bad thing, but it does suggest that the forests in Acadia may be more vulnerable to stressors than matrix forests, particularly stressors that could impact red spruce. While this isn't the greatest news, this is important information for park managers to know.”

Like many folks in the greater Boston area, I drive hours to Acadia and feel like I am stepping into a wilder, more biodiverse ecosystem when I lace up my hiking boots at the trailhead to Cadillac Mountain. But, there are pockets of protected tree species diversity hidden in plain sight across the eastern US. Miller’s research makes me rethink my summer road tripping plans — perhaps I should seek out some of those old, diverse forests in National Recreation Areas and Historical Parks, maybe some are actually accessible by railroad... I'm going all in on my research for the All Aboard! Cultural National Parks of the East board book pitch! 

References:Miller, K.M., McGill, B.J., Mitchell, B.R., Comiskey, J., Dieffenbach, F.W., Matthews, E.R., Perles, S.J., Schmit, J.P. and Weed, A.S., 2018. Eastern national parks protect greater tree species diversity than unprotected matrix forests. Forest Ecology and Management, 414, pp.74-84.

Miller, K.M., Dieffenbach, F.W., Campbell, J.P., Cass, W.B., Comiskey, J.A., Matthews, E.R., McGill, B.J., Mitchell, B.R., Perles, S.J., Sanders, S. and Schmit, J.P., 2016. National parks in the eastern United States harbor important older forest structure compared with matrix forests. Ecosphere, 7(7).  

National Parks are for the Birds

Happy National Parks week!While I tend to plan trips around plants — Thuja plicata in Olympic National Park, Lathyrus japonicas at Cape Cod National Seashore — I understand the draw of non-botanical Park residents: the iconic bison in Yellowstone, the wolves and moose of Isle Royale, the bald eagles cruising the coast of Acadia. 

Birds are among the most beloved park wildlife, and people — regular visitors, rangers and researchers alike — have been studying birds in National Parks for decades. Bird watchers are among the most consistent and prolific citizen scientists and their observations from National Parks to backyards comprise some of the largest and oldest community-based science research in the country. The most famous datasets of this kind are the Christmas Bird Count and the Breeding Bird Survey. These two datasets — covering a huge spatial area, a long species list, and over three decades of observations — allowed the National Park Service and the National Audubon Society to project bird responses to climate change across the National Park System.

Imagine you are standing in a National Park (I always imagine I am standing in Acadia). Take a moment to identify the avifauna — aka the birds — in this park. Now, zoom into the future, sometimes between 2041 and 2070. What birds are in your National Park now? Has your species list changed? Grown? Shrunk? Park managers, researchers, and bird watchers would all love to know the results from this time traveling exercise. Now, thanks to Dr. Joanna Wu and colleagues, we have these projections available! In a recent PLoS ONE paper, Wu and coauthors use the Christmas Bird Count and Breeding Bird Survey to model climate suitability for over 500 bird species. Then, they zoom into the future and look around at the projected climatic changes in 274 National Park. From this perspective in the future, they write a new species list for each park: which birds are disappearing, and which new colonizers are expected to move in. They find that most parks are likely to become more bird-y — potential colonizations will exceed extirpations, especially in the winter. 

The models of summer and winter distributions were trained on two big, old citizen science projects — the Breeding Bird Survey and the Christmas Bird Count. I asked Wu if it was coincidence that this research was grounded in community-based science, since both Audubon and the National Park Service depend on the general public for support. She writes, “these data sets were the only ones done with survey rigor at a large enough of a spatial scale to allow us to map out bird occupancy across the entire North America. It was certainly meaningful for Audubon as the compilers of the Christmas Bird Count data to rely on our community science products in a scientific study.” This shared enthusiasm between Audubon and the community of birders is reflected in the beautiful website that presents Wu's findings to the public: you can watch species turnover, click on specific parks, and look at national trends.And it’s not just that birds are charismatic fauna with huge fan bases that are obsessed with making lists (I’m looking at you, birdwatchers). Wu notes, “birds are important ecological indicators because they travel much larger distances on an annual basis (as a whole) than plants or mammals, and may thus be able to track climate better than other taxa.” So, when Wu and her colleagues project changes in bird communities at the National Parks, they are looking at the frontline of ecological changes under anthropogenic climate change.

“Though plants and mammals are shifting too, birds are indicators as they’re likely to respond first and more drastically. Of course this leads to a potential mismatch in resource availability as plants, insects, etc. respond at a different rate to climate change, leading to unforeseeable consequences.” 

Finally, I asked Wu what we can do if we live and/or work outside of a National Park. Unfortunately, Acadia is not actually home, and I wanted to know how my actual backyard fit into the bigger picture here. “Our research does show that birds are going to be on the move and the corridors between parks are important to support this change. State parks, wildlife sanctuaries, and even back yards are going to be increasingly important places for birds moving to new areas in light of climate change. One of the things we can do is planting native plants to provide resources for birds as they face unprecedented change to the climates and habitats they evolved in in the coming decades.” 

Enjoy National Park Week! Happy birding! 

Reference:

Wu JX, Wilsey CB, Taylor L, Schuurman GW (2018) Projected avifaunal responses to climate change across the U.S. National Park System. PLoS ONE 13(3): e0190557. https://doi. org/10.1371/journal.pone.0190557

Biodiversity Patterns in Melanesian Coral Reef Fish: New Research with Old Naturalists

Old naturalists are my jam. I dedicated my PhD dissertation to a 19th century botanist who had spent her childhood following Thoreau around the Concord woods. I have a soft spot for research that draws on the work of older ecologists, for data that was handwritten before the advent of ballpoint pens, for 21st century papers based on museum natural history collections. This nostalgia is well-timed: museum collections are increasingly digitized and freely available online, and the Biodiversity Heritage Library is doing the same for scientific literature on biodiversity.

Just as my kind of fieldwork no longer requires taking the steamship to downeast Maine and a buckboard on wild roads between logging communities, my scholarship is not dependent on scouring the library stacks for a particular volume or traveling to the archives of a natural history collection to comb through specimens for just the right sample. In the 21st century it is significantly easier to be an armchair laptop historical ecologist. Easier, but not easy.

“Natural history and collections seem to be a bit of a hard sell when it comes to the ecological literature, which surprised me,” says Dr. Kathryn L. Amatangelo. She and Dr. Joshua Drew just published a PLOS ONE paper using coral reef fish data from museum collections records, peer reviewed literature including fish check lists, and biological inventories. The biodiversity pattern they were attempting to analyze and understand — that reef fish diversity in the Indo-West Pacific decreases along a longitudinal gradient from species-rich Papua New Guinea to species-poor American Samoa — was described in 1906.

Amatangelo laments, “It seems almost passé to look at old collections and think about how and why long-dead historians collected their data. When you try to combine that with statistics and scientific analyses people seem to get a little squirrely.”

Drew and Amatangelo’s paper “Community Assembly of Coral Reef Fishes Along the Melanesian Biodiversity Gradient” applies modern ecological theory and big data statistical tools to observations recorded by David Starr Jordan, a Victorian-era ichthyologist who was both the founding president of Stanford University and a suspect in the possible murder of Jane Stanford. If that legacy is not problematic enough, he was also into eugenics.

Thanks to the efforts of Biodiversity Heritage Library (BHL), we can read Jordan’s 1906 paper “On a Collection of Fishes from Fiji” where he notes the diminishing diversity of fish as you travel across Melanesia. Drew remarks, “historical ecologists are always looking for old species lists, and it was super cool to find that he worked in my study system in Fiji.” Drew describes a Jordan as “an ichthyological hero of mine, a complex and not unproblematic figure”: Jordan’s writing on ichthyological biogeography and community change, his system for organizing ichthyological collections and his service on the US Fish Commission, a precursor of NOAA, provide a foundation for the kind of work that Drew and Amatangelo so beautifully execute here.

In the pursuit of quantitatively describing this biodiversity gradient, Drew and Amatangelo compiled presence/absence records for 396 fish species in five taxa across 7 countries. As Drew describes it, this dataset was created from “a massive literature search from collections-based and peer-review based lists that were then double-checked with FishBase.” They looked for agreement across all three datasets (collections, literature, and FishBase), which gave them more confidence in the data since it was not susceptible to the biases present in only one dataset. Amatangelo is a community ecologist with a plant background, she partnered with Josh Drew through a twitter connection, bringing statistical savvy to these new-to-her taxa and ecosystems. I asked her what it was like to work with unfamiliar study species in this project. “One downside was that things that were intuitive to Josh, such as why some traits are important, was a bit of a mystery to me. That could also be considered a positive, though, because it meant that Josh had to be able to explain WHY they were important, which helped in writing the paper.”

The paper’s ultimate goal was to illuminate the processes behind the reef fish biodiversity pattern to inform conservation efforts. Drew acknowledges that their conclusions are not ground-shattering — the biodiversity gradient was described 110 years ago, and likely broadly known before then in local communities. “But it’s nice to put a p-value on it,” he says. “Natural history and traditional ecological knowledge are not always recognized because they don’t come with a p-value, so here we did that. We probably could have told you the same result before, but this adds weight to the management recommendations.” Those management recommendations include collaborations across Melanesia to more efficiently share resources and partition the region into functional biodiversity groups.

Through the power of twitter, digitization, and online collections two modern ecologists were able to build on a paper from 1906 and study Melanesian coral reef fish diversity from their laptop screens in the United States. So much of this data would be instantly recognizable to Jordan, but so little of the actual process of collaborating, compiling and analyzing data, and writing a paper has remained constant since 1906.

Drew reflects on this revolution in his recent correspondence to Nature Ecology and Evolution: “Digitization of museum collections holds the potential to enhance researcher diversity.” He and coauthors write that “the advent of digitization (open access to images and specimen data) now makes a wealth of biodiversity information broadly available…Digitization allows access to museum holdings to those for whom collections have typically been out of reach.” The concentration of collections in the Global North is a reflection of our discipline’s role in the history of exploration and colonialism. Untangling this broader context of past research is perhaps the most impressive, thoughtful work that a historical ecologist could pursue.

In two papers this fall Drew has managed to both uphold the ichthyological legacy of Jordan, and articulately argue that the museum collections Jordan once organized in his spare time from being abhorrently racist, could be, in digital form, a force for increasing diversity in science. 

References:

Drew, Joshua A., and Kathryn L. Amatangelo. "Community assembly of coral reef fishes along the Melanesian biodiversity gradient." PloS one 12, no. 10 (2017): e0186123.

Drew, Joshua A., Corrie S. Moreau, and Melanie L. J. Stiassny. "Digitization of museum collections holds the potential to enhance researcher diversity." Nature Ecology & Evolution (2017):10.1038/s41559-017-0401-6

A Little Light Reading

As the leaves fall this October and the canopies bare their skeletal limbs, there’s suddenly more light filtering across the riverside trails in Maine and I’m wearing sunglasses on runs where I used to be totally engulfed in the shade. It’s hot toddy season, pumpkin spice season, submit-your-GRFP season. When the weather finally chills we’ll get into ugly sweater season, rush-to-take-family-photos-for-a-holiday-cards season, and grading-endless-finals season. Culturally, we humans divide the year into more than just autumn-winter-spring-fall. A recent PLOS ONE paper makes the case that understory plants probably do this too.

Janice Hudson and her coauthors explored the seasonal dynamics of sunlight in a temperate deciduous forest and the ecology of the common shade-tolerant shrub, spicebush. They were inspired, in part, by a relatively obscure 1977 Ecological Monographs paper* with the unassuming title “The Distribution of Solar Radiation within a Deciduous Forest,” in which the authors, Boyd A. Hutchison and Detlef R. Matt, outline the concept of phenoseasons.  

Get ready to update your calendars — the seven phenoseasons for life under a forest canopy are: winter leafless, spring leafless, spring leafing, summer leafing, summer fully-leafed, autumnal fully-leafed, autumnal partially-leafed. I only wish that Hutchison and Matt had dined with Tolkien. Imagine the invitation: “Let’s meet for second breakfast to celebrate the end of spring leafless.” [Insert ent joke here.] Hudson was interested in how changes in light availability affected understory plants like spicebush. As Hudson explains “broadly, this study was an attempt to better understand the pre-existing conditions of the forest…[are] light conditions...a controlling factor in the distribution and presence of plant species?” The phenoseason construct hasn’t taken off in ecology and the annual cycle of subcanopy light exposure is not well understood. Hudson and her coauthors stumbled on Hutchinson and Matt while working on a literature review, but the idea of phenoseasons — now update-able with a high-tech piece of equipment called line quantum sensors — seemed ecologically intriguing. Hudson’s background is in eco-hydrology and the link between seasonal changes in light and phenology had immediate implications for her. She wanted to know “how understory plants acclimate…[and] plant contributions to nutrient and water cycling during individual phenoseasons, and yet, the literature on the subject of phenoseasons is scant.”

Hudson’s team combined a year of intense field measurements with experimentally manipulated light conditions in growth chambers to explore light intensity through the phenoseasons. At Fair Hill Natural Resource Management Area in Maryland, Hudson and her team carried a light sensor through the forest of American beech and yellow poplar trees to measure light conditions above, within, and under the spicebush canopy, compiling over 4,500 measurements in a year across 26 sites (25 in the forest, one open area just outside the forest for comparison). 

When Hudson talks about light, she talks about photosynthetically active radiation (PAR) and, for this study, subcanopy photosynthetic photon flux density (PPFD), which is a measure of PAR. Unsurprisingly, the highest PPFD values under the beech and poplar canopy occur in spring leafing — the days are growing longer, the northern hemisphere is tilted toward the Sun, the trees are still mostly bare. During summer leafing, the subcanopy PPFD values drop, and continue to decrease into summer and autumnal fully-leafed, before a slight bump for the autumnal partially-leafed phenoseason. In a nod to Hutchison and Matt, Hudson recreates their 1977 figure mapping the contours of PPFD through the year at different canopy levels with her own data. It’s the scientific equivalent of siblings re-staging family photos as adults.

But what does it mean to be a spicebush living in the light environment depicted in these figures? In general, Hudson found that there’s almost 10 times more subcanopy light available during the leafless seasons than the leafing and leafed seasons. During the leafing and leafed seasons there are high-energy sun flecks and hot spots — think of a sun-dappled forest floor — which contribute to the variability of light measurements throughout the phenoseasons. But, mostly the understory species must make proverbial hay (read: Germinate! Flower! Leaf out! Photosynthesize like crazy!) while the sun shines in the short leafing seasons. Even in the leafless seasons, the open site received much more PPFD than the subcanopy: the woody surfaces of the trees were intercepting plenty of winter and early spring light.

The spicebush plants in the field and in the growth chambers grew best under the highest PPFD conditions found in the Maryland woods. This is the light niche. In the growth chambers, plants that received higher PPFD conditions were actually less healthy, produced fewer leaves and less biomass. Hudson wrote a beautiful explanation of this when we emailed and I have to let this paragraph speak for itself:

We know that all organisms have an ecological sweet spot, but very rarely are all conditions ideal. Canopy species are "less limited" in the sense that they may experience some shading by neighbors but are primarily subject to changes in light due to latitude, season, and sky conditions. This "light intensity niche" is especially important for shade-adapted and shade-loving plant species when you consider spectral filtration (one way that plants "communicate" with each other and adapt growth direction and strategy) and temporal sequences of incident radiation at both long and short time scales (the timing and amount of light availability is crucial for physiological and biochemical processes for these species). It puts a sort of "ceiling" on the amount of light that is useful for the understory plant, whereas for canopy species there really isn't such a thing as too much light – their growth is primarily limited by the lower boundaries of light availability.

 Finally, this study’s implications for climate change research are quite interesting. In the decades while the ‘phenoseasons’ concept was languishing, research in phenology has taken off: the timing of seasonal events like leaf out and flowering are almost universally creeping earlier in response to warming temperatures. This advancing spring phenology has been definitively tracked in temperate deciduous forests like Hudson’s study site. As the climate changes, leafing phenoseasons may bite into the leafless phenoseasons. The density of the canopy may change as the species composition, size, and height of canopy trees changes. As Hudson wrote, these are the pre-existing conditions in the forest from the perspective of an understory species. We often think about species migrations and no-analog communities when we talk about the ecological effects of climate change: now I think I’ll imagine the reshuffling of the pre-existing conditions, and the interactions between biotic and abiotic factors that create the “ecological sweet spots” that we study. And now, as we enter the autumn leafless, I’ll soak up the sun on my unseasonably warm October runs. 

*This paper’s obscurity is not helped by the fact that the google scholar pdf link takes you to a 627-page annual report hot off the mimeograph with old-timey typer-writer kerning; Hutchison and Matt’s paper is buried in this report (just scroll to page 327), though much easier to find via JSTOR.

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) 

Common Gardens For All Your Climate Change Needs

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

Experimental gardens are an old-school methodology. In perhaps the best known example in the 1930s and 1940s Clausen, Keck, and Hiesey transplanted Potentilla glandulosa across their range in the Sierras to explore the roles of environment and genetics played in determining growth form. Clausen, Keck, and Hiesey’s classic methodology of reciprocal transplanting has a contemporary application in climate change studies, whereby researchers relocate a plant (or seed) from its home and current climate to a transplant garden and new (and perhaps future) climate. Seven decades later, the Ecological Society of America’s 2016 Annual Meeting features experimental gardens that include species ranging from alpine forbs to douglas fir trees to a dune-loving annual—collected along latitudinal, elevation, and habitat gradients. 

Nicole Rafferty opened the Climate Change: Ranges & Phenology I session presenting her research on patterns of bumblebee visitation at the Rocky Mountain Biological Laboratory. As a part of this project, she installed a reciprocal transplant experiment with seeds from three elevations planted at 12 plots per elevation site. She wanted to test how alpine plant-pollinator relationships might change as plant communities experience new microclimates (for example, if a species is transplanted to a warmer site at a lower elevation). Unfortunately, the first year of this study coincided with a dry summer and low germination rates — as a result, in 2016 she switched to seedlings. In her 2015 seed study, the glacier lily seeds from mid-elevation had the lowest success in the transplants, suggesting that mid-elevation might be a barrier to plant migrations upslope for this species.  

Range shifts and phenological are also on the minds of researchers at the U.S. Forest Service. This time with an applied focus aimed at aiding land managers who will likely need to develop strategies to make Forest Service lands more resilient to climate change impacts. Sheel Bansal at the U.S. Forest Service’s Pacific Northwest Research Station and colleagues carried out a large-scale common garden study aptly named the Douglas-fire Seed-Source Movement trial. Their experiment used seeds from 60 sources throughout the species range in Washington, Oregon, and California and grew trees from each of the sources in 9 climatically-divergent field sites and also used artificial freeze experiments to test the impacts of changing environmental queues on Douglas fir cold hardiness and associated genetic linkages. They found strong differences in cold hardiness, with minimum winter temperatures and fall frosts as major predictors of cold hardiness based on seed source. Their results have important implications for the ability of species to shift their ranges by tracking climate envelopes, and further extend to land management efforts to maintain healthy forests experiencing future climates.

In the Great Lakes region, Elizabeth LaRue from the Emery Lab at the University of Colorado Boulder used a common garden to explore dispersal traits in American sea rocket (Cakile edentula var. lacustris). She knew that dispersal traits like pericarp, or seed wall, thickness and wet mass varied across the Cakile edentula range, but it was unclear if the variability was caused by environmental or genetic differences. Collecting seeds from across the range, and growing them together in a common garden isolated the role of genetic differences and revealed lower dispersal traits at the range edges. This data was used to inform species distribution models with different scenarios for starting dispersal genetics for Cakile edentula under climate change.

Kennedy Rubert-Nason in the Department of Entomology at the University of Wisconsin-Madison and his colleagues looked at the role of vernal freezes in determining aspen phenology and growth. They planted 6 aspen genotypes into common gardens at varying temperatures and examined a number of biological responses.  The number of days it took aspen to break bud accelerated in trees that experienced freeze-damage. Freeze-damaged trees were also stunted in their second year of growth when they experienced a freeze event during their first year. Defense compounds were also dramatically impacted, potentially indicating the negative effects of freeze events and the associated ability of the trees to defend against herbivores during their most vulnerable life stage. Their study nicely highlights the importance of the timing of environmental queues in dictating species susceptibility to a changing climate. 

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) 

Daniel Winkler is a PhD candidate at the University of California, Irvine and a recent National Park Service Young Leader in Climate Change. Daniel is a plant ecophysiologist interested in invasive species, evolutionary ecology, and climate change impacts on native communities in “extreme” environments. His field sites include much of the desert southwest, alpine regions of Colorado, the subalpine forests of Baja California, and the tundra of northern Japan. All of Daniel’s research focuses on climate change impacts on native systems, with an emphasis on parks and protected areas. You can follow him on Twitter @DanielEWinkler, his research on Facebook at www.facebook.com/GeoMustard/, or find more information on his website at www.winklerde.com.