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 recent papers 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.”