Figure 1. Anolis gundlachi, Orocovis, Puerto Rico.
The agroecosystems that produce the life-sustaining stimulant we know as “coffee” have long been used as model systems to study complex ecological interactions and ecosystem services, with numerous studies revealing trophic interactions among coffee plants, pests, and pest-predators. Despite the high abundance and overlapping distribution of Anolis lizards, relatively few studies have addressed their functional role in agriculture. In our recent study titled, “Anolis Lizards as Biocontrol Agents in Mainland and Island Agroecosystems,” my colleagues and I explore the biocontrol potential of anoles against the world’s most devastating coffee pest, the coffee berry borer (Coleoptera: Hypothenemus hampei) in mainland and island settings.
My vision of agricultural landscapes as post-apocalyptic biodiversity deserts was trumped the minute I stepped foot onto a shade coffee farm in Orocovis, Puerto Rico. Far from the dystopian nightmare that I had envisioned, this diversified shade coffee farm bustled with the herpetological glory and natural complexity of a native forest (Fig. 1). Furthermore – and perhaps most importantly – the farmer complained not of issues with crop yield, pests, and disease.
As a plant, coffee occurs naturally in the forest understory and is cultivated traditionally among native shade trees as an understory crop. While pressures to increase production have led many farmers to transition to more intensive practices (i.e., the reduction of shade cover and application of agrochemicals to manage crop pests), these methods are becoming increasingly unsustainable and insufficient in light of emerging biological threats. In addition to climate change and the emerging coffee rust disease, the coffee berry borer poses a unique threat for dozens of coffee growing nations and nearly 20 million small-scale farmers who depend on coffee production as a primary commodity and means of subsistence. While the coffee berry borer (CBB) is capable of inducing 60-90% reductions in yields and persists unaffected by topical pesticides, our understanding of the predator-prey interactions that drive its top-down control and how these factors vary across management regimes and eco-geographic space has profound socio-economic and environmental implications for biological control.
Figure 2. Representative photographs of diversified shade coffee in Mexico (a), diversified shade coffee in Puerto Rico (b), intensive sun coffee in Mexico (c), and intensive sun coffee in Puerto Rico (d).
To assess the biocontrol capacity of anoles, we conducted experimental and field-based tests of how CBB populations respond to anole predation across mainland (Mexico) and island (Puerto Rico) coffee farms with parallel forms of land-use intensity. Anole functional response and infestation reduction potential were assessed by simulating pest outbreaks in the lab, while coffee farms were surveyed along complementary gradients of intensification. Organic, diversified shade coffee farms were representative of low-intensity production, and sun coffee monocultures that included the application of agrochemicals were representative of high intensification (Fig. 2).
Figure 3. Mean number of coffee berries infested by the coffee berry borer ( ± 1 SE) in the presence and absence of Anolis lizards in laboratory settings.
Our experimental results are the first to show that anoles are capable of both consuming the coffee berry borer in high quantities and significantly reducing infestations in laboratory settings (Fig. 3). In Mexico and Puerto Rico, individual anoles reduced CBB infestations by an average of 49% and 83%, respectively. Linear and nonlinear models were used to fit CBB consumption data to functional response curves, revealing a type III functional response to manipulations in CBB density for each region.
Results from our field surveys show Puerto Rican anole abundance to be negatively correlated with decreasing canopy cover, whereas anole abundance in Mexico correlated negatively with reduced coffee height (i.e., crops that had been pruned or reduced below 1.5 meters). In Puerto Rico, the greatest abundance of anoles was found at intermediate intensity values, with the negative trend in abundance being driven by a single farm with zero anoles. This farm, along with several similar plots in Mexico revealed the application of agrochemicals to have deleterious effects on anole abundance.
Figure 4. Anolis dollfusianus, Chiapas, Mexico
In Mexico, Anolis dollfusianus and A. sericeus were the only two anole species present on farms surveyed (Fig. 4 & 5), along with a single species of Ameiva and two unidentified species in the genus Mabuya. In Puerto Rico, anoles were the solitary lizard genus present on farms surveyed with an average abundance that was twelve times greater than that of Mexico. Patterns of species richness were congruent with previous studies, revealing Anolis cristatellus and A. stratulus to favor sun coffee and open canopy, while A. gundlachi and A. evermanni increase in abundance with increasing shade. Additionally, anole richness and abundance was greatest on farms with intermediate levels of canopy cover, suggesting that the impact of intensification is buffered by greater levels of functional diversity among Puerto Rican anoles.
Figure 5. Image of an adult Mexican anole, Anolis sericeus, perching in a coffee shrub in Chiapas, Mexico.
Figure 6. Rare photo of field pests antagonizing their biocontrol agent.
Among the many challenges encountered during this study, collecting habitat data in an actively curated ecosystem was most difficult. Due to the occasional maintenance of weeds and undesirable vegetation, several habitat features were ephemeral and could not be included in this study. Additionally, estimates of CBB infestation reduction would have been most robust for experiments conducted under field conditions, but the development of non-invasive enclosures that omit co-occurring CBB predators (i.e. ants and birds), and omit researcher pests (i.e. domestic chickens, Fig. 6) were not feasible within the timespan of this study.
The results of this study reveal that anoles are likely an important predatory component of coffee agroecosystems and contribute to the insurance of biological control in diversified farming systems. While mainland anole populations were sensitive to habitat disturbance, our results from Puerto Rico shed light on the role of pre-adaptive traits that promote community resilience to habitat disturbance. Additionally, the future conversion of natural spaces to intensive monocultures is predicted to isolate shade-adapted species to forested islands and contribute to pre-existing extinction pressures. Conservation initiatives such as Puerto Rico’s National Model Forest, an act of legislation protecting 20 interconnected natural areas across the island, are predicted to be critical steps in facilitating future sustainable development.
Entrance to Finca Guaragua, a diversified shade-coffee farm in Orocovis, Puerto Rico. The sign reads, “Agriculture is the backbone of a people/village.”
In light of the devastating impacts of hurricane Maria in Puerto Rico and the September earthquakes in Chiapas, future studies exploring the resilience of diversified agroecosystems, and the potential contribution of biodiversity to post-disaster agroecosystem resilience are especially important. Spiller et al.’s 2016 study showing that anole predation bolsters post-hurricane plant recovery on small islands in the Bahamas offers insight into the potentially unique role of anoles in post-disturbance crop recovery.
Coffee’s capacity to sustain global biodiversity and family livelihoods rest in our ability to find conservation approaches that allow farmers to use landscapes productively while also providing viable habitats for wildlife. Until then, the coffee berry borer will remain academia’s biggest competitor for the sacred, life-sustaining coffee bean.
Skip Lazell
Back in 1958 I first attained recognition for anole systematics by discovering spectacularly distinct subspecies of Anolts oculatus in different geographic ecozones of Dominica. My number one research site was a banana plantation at Woodford Hill owned and managed by Charles Winston (and Family), who was dedicated to managing agricultural land in harmony with natural ecosystems. It sure did work! Skip
Ivan Monagan
Thank you for your insight, Skip! I recall exploring a small banana plot adjacent to one of my shade-coffee sites in Mexico and being surprised by the apparent increase in abundance of anoles (and skinks). It would be interesting to see how that plays out on a larger scale. Are you aware of any collections made at the Winston farm/area in recent years? Thanks again.
Levi Gray
Very cool. We tend to get Anolis laeviventris regularly in the Soconusco, including in coffee plantations. Although I don’t think they were nearly as common as A. sericeus and A. dollfusianus. Occasionally we’d get A. serranoi if we were far enough SE on the slopes of the Sierra Madre del Sur de Chiapas.
One thing that stands out about those coffee plantations is that they are filled with what we sometimes refer to as “trash species”–species that tend to be really common in disturbed lowlands. If an anole species tolerates highly disturbed habitats, it seems to do well in shade-grown coffee plantations. Local anole species with more restrictive niche requirements tend to be absent. Based on my experience, you often need to find patches of actual forest to get Anolis matudai or A. petersii, both of which are common in the right habitat and still tolerate a fair amount of disturbance. In sum, mid-elevation shade-grown coffee plantations tend to resemble highly disturbed lowland anole communities.
There was a student (César Antonio Cruz-Parra) that did some work on the slope of Tacaná that got similar results looking at overall herp communities. He is now at UNICACH working in El Ocote last I checked.
James T. Stroud
Hey Levi, nice observations – those patterns are repeated in the herp communities of much of the oil palm plantations of SE Asia. Disturbance tolerant/forest gap/edge species seem to do pretty well in them.
Ivan Monagan
That’s an interesting observation, Levi– particularly your comment on anole communities in mid-elevation shade coffee resembling communities in highly disturbed lowlands. It was certainly surprising that we only found A. dollfusianus and A. sericeus despite certain sites being visually indistinguishable from adjacent forests. Thank you!
Levi Gray
It might be even more apparent in the anuran communities. I hardly ever see non-trash frogs in a shade grown coffee plantation down there, whereas other (sometimes highly) disturbed patches of forest can still yield a variety of species with more restricted niche requirements.