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2014

Monteverde: Ecology and Conservation of a Tropical Cloud Forest - 2014 Updated Chapters

Nalini M. Nadkarni

Nathaniel T. Wheelwright

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Recommended Citation Nadkarni, Nalini M. and Wheelwright, Nathaniel T.(editors), "Monteverde: Ecology and Conservation of a Tropical Cloud Forest - 2014 Updated Chapters" (2014). Bowdoin Scholars' Bookshelf. Book 4. http://digitalcommons.bowdoin.edu/scholars-bookshelf/5

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1 Introduction — Update 2014

Nalini M. Nadkarni & Nathaniel T. Wheelwright

In the last three decades, Monteverde, Costa attractions to attract ecotourism as an economic Rica has emerged as a critical venue for research driver, and good infrastructure to support it; and in tropical montane biology. Over 350 scientific a rare degree of civic awareness and community articles and 10 scholarly books have been engagement (Nadkarni et al. 2013). generated. In terms of conservation and training For example, the presence of a strong young biologists, Monteverde is considered one scientific understanding of the negative effects of the premier tropical cloud forest sites in the of deforestation on soil erosion, water quality, world. and biodiversity prompted the early conservation This rich research, conservation, and movement. This helped raise awareness about education legacy exists even though the research the presence of remarkable species such as the infrastructure has been extremely limited, Resplendent Quetzal and Golden Toad and the relative to many other major tropical field threats they faced from fragmented landscapes, stations. Research has mostly been conducted by introduced species, and changing climates. The single investigators, often with little or no presence of such charismatic species, living in extramural support, and there have been few such charismatic habitats, attracted student large-scale, long-term, multi-institutional groups and tourists to the area. This led to an projects. income flow that could support continued Synergistic interactions between several preservation and additions to cloud forest distinctive features of Monteverde appear to preserve areas, which expanded opportunities explain the high research productivity in the face for scientific research. The sense of civic of limited research support: a long-time awareness and spirituality of this Quaker- emphasis on watershed protection and originated community fostered a sense of conservation; a commitment to education, from personal responsibility to carry out actions to bilingual local grade schools to graduate field benefit people, wildlife, and plants. courses offered by the Organization for Tropical Studies and other groups; outstanding natural

Because montane forests comprise a much translation of this translation. We had two main smaller land area and have a lower economic objectives. The first objective was to educate, value than lowland forests, they have tended to inspire and engage as many people as possible in attract fewer scientists and less funding and the effort to protect tropical cloud forests. When research infrastructure. Monteverde provides an we were in graduate school, the standard model example – and potentially a model – for of conservation was this: acquire a lot of land, scientists in other montane cloud forests and put a big fence around it, and keep people out. other tropical ecosystem types that do not attract That approach has been discredited over the large funding and yet still can produce excellent years, and now everyone realizes the importance science (Nadkarni et al. 2013). of having people "buy in" on conservation It has been 14 years since Monteverde: projects. Our second objective was to attempt to Ecology and Conservation of a Tropical Cloud shift the culture of scientists who conduct Forest was first published (Nadkarni and research in developing countries, then return Wheelwright 2000). Given the many new home to publish their work in English in research projects that have appeared in the scholarly journals. "Education" literally means interim, we felt it was time to update the book. "leading outward" — in this case, taking More importantly, the book's cost and the fact information about tropical biology and that it was published only in English effectively conservation that is currently sequestered in put the book out of reach for many readers in expensive books in privileged libraries and Latin America. Clearly, it is time to translate the making it freely available on the web to anyone book into Spanish, particularly in light of who speaks Spanish. accelerating rates of biodiversity loss — Within six weeks of initiating a Kickstarter "defaunation" — and the paucity of conservation campaign monitoring studies in the neotropics (Fig. 1; (www.kickstarter.com/projects/768016193/rainf Dirzo et al. 2014). In addition to translating the orest-conservation-making-science-available-i) original book, we requested representatives of in December, 2014, we received contributions the Monteverde research, conservation, and from 185 individuals from all walks of life and education communities to write an actualización from all over the world—Costa Rica, of course, for each chapter. The actualizaciones are not but also New Zealand, France, Canada, the meant to describe in detail everything that has Netherlands, Spain, Switzerland, Mexico and transpired in each field since the original book other countries, which has made the translation, was published, but rather to inform the reader of updating and publication of this book possible. significant advances and relevant literature on We hope that readers will find it a useful that topic. resource for understanding and protecting In the spirit of Monteverde research, tropical cloud forests not just in Monteverde but education, and education, we drew upon grass- throughout Latin America. roots support — rather than applying to traditional funding sources — to fund the

Fig. 1. Locations of all sources of invertebrate abundance time series data. The size of the circle is relative to the number of species studied in a given location. Note the paucity of studies in Latin America and the tropics in general (figure from Supplementary Material in Dirzo et al. 2014).

Literature Cited Nadkarni, N.M., and N.T. Wheelwright (eds.). 2000. Dirzo,R., H.S. Young, M. Galetti, G. Ceballos, N.J.B. Monteverde: Ecology and Conservation of a Isaac, and B. Collen. 2014. Defaunation in the Tropical Cloud Forest. Oxford University Press. Anthropocene. Science 345: 401-6. 573 pp. (also available online at digitalcommons.bowdoin.edu). Nadkarni, N., K. Sheldon and S. Gotsch. 2013. The perfect storm: educational, conservation, and community synergisms for tropical ecology research in Monteverde, Costa Rica. Symposium: Association for Tropical Biology and Conservation, San José, Costa Rica.

2 Physical Environment — Update 2014

Kenneth L. Clark, Robert O. Lawton & Paul R. Butler

The original chapter on the “Physical briefly review selected studies at the end of each Environment” had two goals: 1) review what is section. known about the climate and weather, geology, geologic history, geomorphology, soils, and Climate and Hydrology of Monteverde hydrology of Monteverde, and 2) identify areas We still lack complete information on climate where our knowledge is incomplete and further and hydrologic cycling for Monteverde, investigations will be fruitful. Since its especially long-term data on changes in wind- publication, our overall understanding of driven cloud and precipitation inputs, tropical montane regions has benefitted from evapotranspiration, and stream flow. However, global-scale comparative data. Recent recent studies are closing these information quantitative information on how variation in the gaps. Our understanding of hydrologic cycling physical environment interacts with biotic in Monteverde has benefitted from a more processes at the population, community and complete understanding of the biophysical ecosystem scales are beginning to be addressed. controls of cloud formation and persistence, and Here, I summarize some of the recent research recent measurements of cloud water and wind- on: a) climate and hydrology of Monteverde; b) driven precipitation inputs across the Caribbean recent information on geology and and Pacific slopes (Lawton et al., 2001, 2010, geomorphology, including more accurate ages Frumau et al. 2011, Hager and Dohrenbusch for recent volcanism, the large granodiorite 2011, Schmid et al. 2011). Estimates of pluton in the Monteverde area, and a refinement evapotranspiration and stream outputs have been of the tectonic interpretation of the region; c) refined using isotopic analyses of inputs, carbon, nutrients and enzymes in soils; d) the outputs, and isotopic signatures in tree rings impacts of deforestation on soil carbon and (Anchukaitis et al. 2008, Guswa et al. 2007, nutrients, and e) comparisons between terrestrial Rhoades et al. 2010, Sanchez-Murillo et al. and arboreal soils in the Monteverde area. I 2013). In addition, comparative information on hydrology in tropical montane cloud forests

(TMCF) has been advanced by recent syntheses However, limitations to our understanding of (Bruijnzeel et al. 2010, Jarvis and Mulligan these processes still exist (Nair et al. 2003, Ray 2011). Some of these investigations have been et al. 2006, 2009, 2010). driven by the realization that TMCF are Variability in cloud immersion and wind- especially susceptible to climate change (Pounds driven precipitation have been linked to a et al. 1999, 2006). Recent climate change model number of changes in Monteverde, e.g., simulations indicate that mean dry season decreases in populations of anoline lizards and surface air temperatures along the Pacific slope anurans (Pounds et al. 1999), potential of Costa Rica will increase 3.8 °C by 2100, in interactions with pathogens (Pounds et al. 2006), concert with increased variability in surface air and increased drought stress in plants temperatures and a projected decrease in dry (Anchukaitis et al. 2008, Goldsmith et al. 2013). season precipitation of approx. 14% (Karmalkar Experimental transplants of upper cloud forest et al. 2011). epiphyte mats to tree canopies at slightly lower Information from remote sensing applications elevations that experience longer dry season and simulation models have more accurately conditions suggest that vascular epiphytes are documented the biophysical controls over cloud vulnerable to the drier environments predicted base heights and the incidence of cloud for the bioregion due to climate change immersion during the dry season in Monteverde (Nadkarni and Solano 2002). (Lawton et al. 2001, 2010, Nair et al. 2008). The inputs of cloud water and wind-driven Conversion of Caribbean lowland forest to precipitation to forest canopies have been further pasture and agricultural lands has resulted in investigated since the work of Clark et al. greater surface air temperatures and sensible (1998a,b, 2005). Eddy covariance data and cloud heat flux, and lower latent heat flux and water impactors were used to estimate evapotranspiration rates. Reduced hydrologic inputs to Santa Elena Cloud Forest evapotranspiration over pastures raises the cloud Reserve in Monteverde (Schmid et al. 2011). condensation level in comparison to that over They reported cloud water deposition rates of forest, and decreases the moisture content in air 1.2 ± 0.1 mm day-1, within the range of estimates parcels during the dry season. Satellite imagery from other TMCF sites (reviewed in Bruijnzeel indicates that deforested areas of Costa Rica's et al. 2010). Cloud water measured directly Caribbean lowlands remain relatively cloud-free, averaged 5% of precipitation during the dry while forested regions have well-developed dry season, while use of a canopy hydrology model season cumulus cloud fields (Lawton et al. 2001, based on the use of δ18O isotope content as a Nair et al. 2008, Welch et al. 2008). Changes in tracer for cloud water deposition (see below) surface energy balance in the Caribbean represented 9% of dry season precipitation. lowlands have resulted in an increase in cloud Schmid et al. (2011) noted that δ18O was a base height, a decrease in cloud immersion reliable tracer for cloud water deposition, but (Lawton et al. 2001; Nair et al. 2003), and a also acknowledged the difficulties in separating reduction in the number of consecutive days cloud water vs. precipitation during events with precipitation during the dry season in characterized by a significant amount of wind- Monteverde (Pounds et al. 1999, 2006, Lawton driven horizontal precipitation. High collection et al. 2010). Regional atmospheric model efficiencies for different cloud water collector simulations have further linked changes in designs corroborated the investigations of surface energy balance to the incidence and Schmid et al. (2011), including those used in height of cloud immersion over the continental previous research efforts in Monteverde (Clark divide in the Monteverde region. Overall, these et al. 1998a,b, Frumau et al. 2011). results suggest that land use change in lowland Cloud and wind-driven precipitation inputs in forests can have large impacts on the climate of the MVCFR were monitored at seven climate adjacent mountains, although larger, global scale stations that measured rainfall, horizontal phenomena such as the El Niño-Southern precipitation, throughfall, temperature and soil Oscillation also contribute to variability in moisture along a 2.5 km transect across the climate in TMCF (e.g., Anchukaitis et al. 2010). Atlantic (windward) slope and the Pacific

(leeward) slopes (Hager and Dohrenbusch ground into a channel slowly over time, rather 2011). Annual precipitation ranged from 3690 than direct runoff; see Clark et al. 2000) sources mm on the leeward slope (similar to the amount during the dry season. They reported that dry measured by Clark et al. (1998a) of 4077 mm, season precipitation contributed from 0% to but above the long term average measured by J. 31% of baseflow for streams in the Monteverde Campbell lower in the community of 2519 mm) area, with the highest proportions occurring for to 6390 mm on the windward slope. Horizontal Río San Luis (31%) with headwaters along the precipitation was 3560 mm at the ridge, where it Brillante Gap. The contribution of dry-season exceeded rainfall during the dry season, precipitation to stream baseflow peaked near the compared to 330 mm and 28 mm at the lowest end of the transitional for most streams, whereas windward and leeward plots, respectively. For the water in the Río San Luis remained enriched comparison, Clark et al. (1998b) estimated 886 throughout the transition and dry seasons. mm of wind-driven cloud water and Additional analyses of δ2H in precipitation allow precipitation at a leeward forest site in the for an estimate of recycling of precipitation MVCFR. Throughfall amounts remained below between forests and the atmosphere before rainfall on the lower slopes, but exceeded deposition (Sanchez-Murillo et al. 2013). Air rainfall amounts on the ridge because of the mass trajectory analyses for Monteverde further additional wind-driven precipitation (Hager and indicated the input of “recycled” precipitation Dohrenbusch 2011). Forest census from the Caribbean lowlands. measurements made along their transect further The effects of cloud deposition on vascular confirmed that strong hydrologic and plant water status and epiphytes have been topographic gradients correspond to differences further investigated. Goldsmith et al. (2013) in soil conditions and the occurrence of used satellite and ground-based observations to distinctive forest types across the continental study cloud and leaf wetting patterns in pre- divide in Monteverde (Hager and Dohrenbusch montane and montane forests in Monteverde, 2011) . and evaluated the importance of direct uptake of Additional information on precipitation water accumulated on leaf surfaces to plant inputs and hydrologic cycling has been water status during the dry season. Although the facilitated by an analysis of the isotopic capacity for foliar water uptake differed composition of precipitation throughout Costa significantly between plants in montane and Rica (Rhoades et al. 2006, 2010, Sanchez- premontane forest plant communities, as well as Murillo et al. 2013; method reviewed in Scholl among species within a forest type, leaf wetting et al. 2011). Precipitation samples collected events resulted in foliar water uptake in all from 2003 to 2005 had seasonal signals in δ18O species studied. They concluded that foliar and δ2H that were more negative (indicating that water uptake is common in Monteverde, and relatively higher concentrations of heavier 18O improves plant water status during the dry and 2H isotopes occurred compared to the more season. Isotopic analyses of δ18O in tree rings of abundant lighter 16O and 1H isotopes of oxygen dominant species has allowed an estimate of and hydrogen) during the dry and transitional seasonality of the sources of water used and of seasons than during the wet season. In addition, water stress of trees in Monteverde (Anchukaitis cloud water has distinct δ18O and δ2H signals et al. 2008). Futher, δ18O analyses in main compared to rainfall (Schmid et al. 2011). stems of Pouteria sp. have been linked to long- Attenuated signals of these heavy isotopes term climate variability in the Monteverde propagate through forests to streamflow, and (Anchukaitis et al. 2010). provide a tracer for estimating cloud water and The role of epiphytic vegetation in stand wind-driven precipitation inputs to watersheds hydrology has been further quantified by Kohler during the dry and transitional seasons. For et al. (2007) and simulated by Clark et al. example, Guswa et al. (2007) used δ18O data in (2005). Epiphyte assemblages exposed to cloud precipitation and streamflow to partition water wetted up asymptotically, and began to baseflow (i.e., the portion of streamflow that is generate throughfall well below their water derived from the seepage of water from the storage capacity at saturation (323 ± 106 % dry

weight; Tobon et al. 2010). Evaporation Aguacate group during this time, and is overlain following cloud water events followed a by younger andesite lava of the Pleistocene logarithmic decay pattern. Tobon et al. (2010) Monteverde Formation along its northeastern noted that uptake and evaporation of cloud water boundary. was highly dynamic. These research efforts Recent tectonic interpretations and more further confirm the linkage of bryophytes and refined estimates for the rates and direction of vascular epiphytes to microclimatic conditions movement for Cocos plate subduction beneath in Monteverde, and suggest that they will likely the Caribbean plate occur in the literature. be some of the first organisms affected by MacMillan et al. (2004) present the plate changes in climate and wind-driven cloud and tectonic history for the southern Central precipitation amounts. American volcanic arc since the mid-Miocene. Geophysical, geochemical, and petrographic Geology of Monteverde studies have contributed to a better I summarize recent information on the understanding of regional geologic history geology of Monteverde, including more accurate (Derring et al., 2012, Hayes et al. 2013). Using paleomagnetic analyses of recent volcanic flows, isotope geochemistry and seismic velocity further research on the large granodiorite pluton analyses, Hoernle et al. (2008) indicated flow in in the Monteverde area, and an overall the mantle wedge beneath Costa Rica and refinement of the tectonic interpretation of the Nicaragua is trench-parallel rather than trench- region. These new dates better constrain the normal as in classical plate subduction models, magmatic and structural history of Costa Rica. and that parallel flow needs to be taken into Volcanic activity has occurred over a broad area account in models evaluating thermal and known as the Central American volcanic arc for chemical structure and melt generation in at least the past 24 Ma. Cromwell et al. (2013) subduction zones. They also noted that the conducted a comprehensive field and age isotopic signature in volcanic rocks in Costa determinations using paleomagnetic and Rica is consistent with seamounts along the 40Ar/39Ar analyses to date lava flows in Costa Galapagos hotspot track on the subducting Rica. They determined that modern composite Cocos plate, rather than from the mantle wedge volcanoes (those active today include Rincón de or eroded volcanic fore-arc material. This la Vieja, Arenal, Platanar, Poás, Barva, isotopic signature decreases continuously from Miravalles, Irazú, and Turrialba) have mainly central Costa Rica to northwestern Nicaragua. been built during two recent peaks in volcanism They estimated minimum northwestward flow dating (0.4–0.6 and <0.1 Ma), and are rates of 63–190 mm yr-1, comparable to the superimposed on older volcanic formations. magnitude of subducting Cocos plate motion (85 Igneous rocks in Costa Rica older than about mm yr-1). 8 Ma have chemical compositions typical of ocean island basalts and intra-oceanic arcs. In Soils of Monteverde contrast, younger igneous deposits contain The variability of soil nitrogen fixation abundant silicic rocks, which are significantly activity, microbial biomass, fungal and bacterial enriched in SiO2, alkalis, and light rare-earth abundance and diversity, and the abundance of elements, and are geochemically similar to the key functional genes for lignin degradation and average upper continental crust (Deering et al. bacterial N- fixation in forests on the Caribbean 2012, Hayes et al. 2013 ). Žacek et al. (2011) and Pacific slopes of Monteverde have been provided an account of the gabbro to correlated with soil moisture (Eaton et al. 2012). granodiorite Guacimal pluton in the Cordillera Investigation of the properties of soils in and de Tilarán. Plutons are exposed in all three near the Santa Elena Forest Reserve indicated major ranges (Talamanca, Central, and Tilarán that pastures created by forest clearing of the ranges) and were emplaced from approximately cloud forest contained 20% less carbon at 0 to 17 to 3.5 Ma, and mainly from 7–10 Ma during 30 cm depth than mature forest soils, and that 30 an apparent gap in volcanism. The Guacimal year old secondary forest contained intermediate pluton intruded into mafic volcanic rocks of the amounts of soil carbon, while no trend occurred

for soil nitrogen (Tanner et al. 2014). Soil CO2 interactions of climate change and land use flux followed the same trend as soil carbon; change in the Caribbean lowlands affect cloud mature forest soils exhibit slightly higher CO2 formation and dry season precipitation in flux, but greater spatial variability, and Monteverde? How closely coupled is the secondary forest soils have a higher flux than maintenance of biodiversity to changes in pasture soils. They suggested that differences in climatic and micro-climatic variables? Will soil CO2 flux between sites were due to changes in climate and precipitation drive differences in root respiration, controlled by the further local extinctions, and how could size and abundance of plant roots in the extinctions lead to changes in community-level subsurface. Comparing canopy and terrestrial interactions and ecosystem functioning? soils in the MVCFR, Nadkarni et al. (2002) Addressing these questions will involve the reported that the carbon content of canopy integration of field observations with simulation organic matter was significantly higher than studies, based on the abundant research terrestrial soil, but similar for phosphorus and conducted previously in Monteverde and other calcium. Canopy humus had very low pH TMCFs. compared to terrestrial soils. Terrestrial soil had Geological interpretation of Monteverde and a tenfold greater amount of extractable cations, Costa Rica is continuing to evolve. Regional but the C/N ratios and cation exchange capacity simulation studies of the plate boundaries of canopy humus and the upper soil horizon did incorporating rates and direction of movement not differ significantly. of tectonic plates derived from isotopic studies, a more realistic treatment of mantle convection Suggestions for Future Research processes, and mechanisms of incorporation of We are beginning to understand some of the basaltic oceanic material vs. more andesitic complex relationships between climate, continental plate material will further these microclimate, the distribution of species and research efforts. Increased use of sesmic ecosystem functioning at Monteverde. These sounding studies could help resolve some of recent data lead to key questions that should be these questions. addressed in future research efforts. How will

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Sánchez-Murillo, R., G. Esquivel-Hernández, K. Welsh, E. S. Brooks, J. Boll, R. Alfaro-Solís, and J. Valdés- González. 2013. Spatial and temporal variation of stable isotopes in precipitation across Costa Rica: An analysis of historic GNIP records. Open Journal of Modern Hydrology 3:226.

3 Plants and Vegetation — Update 2014

Emily Hollenbeck

The Monteverde area is home to a large and bromeliad species Werauhia werkleana unique flora, thanks to the topography of the (previously identified as Vreisia werkleana; W. mountains and the rare cloud forest that sits atop Haber, pers. comm.; Hammel et al eds, 2000) them. The original chapter in this book (Haber, (Rowe & Pringle 2005). The reproductive traits 2000) contains a thorough description of the of several species have also been studied in diversity and ecology of Monteverde’s flora. depth. Pitcairnia brittoniana is hummingbird- Here, I review a selection of recent research on pollinated (Bush & Guilbeau 2009), while plants and vegetation from the Monteverde area. Werauhia gladioliflora in the upper San Luis The abundance of epiphytes, plants that grow valley is pollinated by bats; W. gladioliflora perched on other plants, is one of the most flowers in the rainy season, with fruit maturation distinctive and striking aspects of cloud forest and seed dispersal occurring during the dry vegetation. Monteverde has remained an season (Cascante-Marín et al 2005). Both important location for research on epiphytes and species, however, were shown to be capable of canopy biology, led by the efforts of Nalini successful self-pollination, implying that these Nadkarni, who first ascended the canopy in 1980 plants are flexible in their reproductive strategies and began describing the rich flora found high and can continue reproducing independently of above the forest floor. Recent research has pollinator abundance (Cascante-Marín et al illuminated more details about the ecology and 2005, Bush & Guilbeau 2009). From a life history of the once-mysterious epiphytes, as community standpoint, the composition of well as their important interactions with the bromeliad species differs between primary and environment. secondary forest (Cascante-Marín et al 2006), A particularly characteristic family of but this was not explained by variation in seed epiphytes, the bromeliads (Bromeliaceae), has establishment success between species received substantial research attention in (Cascante-Marín et al 2008). Further studies on Monteverde recently. Evidence for arbuscular- population and community ecology of mycorrhizal fungal associations was found in the bromeliads are listed at the end.

Monteverde’s epiphyte flora interacts greatly climate, in order to understand the effects that with both climate and nutrient cycles (Nadkarni these impending changes will have on the 1986, Nadkarni and Matelson 1991, Hietz et al epiphytic flora and the biotic and abiotic 1999), and these relationships are becoming processes they affect. even better understood. For example, epiphytic Of course, the unique climatic conditions in plants seem to absorb and retain a substantial Monteverde have affected more than just the “air proportion of their nitrogen from atmospheric plants.” Various species of cloud forest trees inputs, such that the nitrogen cycle of arboreal perform foliar uptake, an unusual trait by which plant communities is relatively independent plants absorb water through their leaves, in from that of the trees and terrestrial soil (Hietz et reverse of the canonical water transpiration al 2002, Clark et al 2005). In addition to W. pathway. Finding this syndrome is perhaps not werkleana, associated mycorrhizal fungi were entirely surprising in the cloud forest; indeed, found in species from the families Araceae, tree species found just below the cloud base in Clusiaceae, and Ericaceae, with first records in Monteverde showed more limited capacity for Cavendishia melastomoides, Disterigma foliar uptake, implicating it as an important humboldtii, and Gaultheria erecta. Mycorrhizas adaptation to the specific mist-shrouded were not found in epiphytes from the common conditions that define cloud forest (Goldsmith et genus Peperomia (family Piperaceae) (Rains et al 2013). al 2003). These fungi, known mostly from Comparative studies between different forest association with ground-dwelling plants, aid types are becoming increasingly common, and nutrient and water absorption. ever more relevant. To understand the ongoing Epiphyte communities contribute hugely to and future impacts of global change on the water and nutrient cycling, overall biomass forests of Monteverde and elsewhere, it is (Nadkarni 1984, Nadkarni et al 2004), and crucial to know how different environmental species diversity of Monteverde’s forests (Haber conditions affect species and communities. 2000), but this valuable flora may be particularly Plants form the base of all ecosystems, and sensitive to ongoing environmental changes, usually interact more directly with the abiotic especially in climate. Recolonization of environment than do animals; thus, epiphytes proceeded extremely slowly after understanding their responses to environmental branches were experimentally stripped, change is paramount. suggesting that it is difficult and slow for canopy Currently, ample area is being left for forest communities to recover after unnatural regeneration, prompting deserved interest in the disturbance (Nadkarni 2000). Additional dynamics of these young secondary forests, how evidence implies that cloud forest epiphytes they differ from and interact with old growth depend on the frequent cloud immersion for habitats, and the advantages and disadvantages survival, presumably because they receive water of secondary forest for biodiversity and nutrients from the enveloping mist. When conservation. In Monteverde, the differences epiphytes in intact canopy mats were between primary and secondary forests have transplanted from the cloud forest at 1480m to been measured in several ways. For example, trees only 70-140m lower in elevation, but canopy-held biomass in old growth forests below the base height of the clouds, they around Monteverde has been variously measured suffered significant decreases in size and season- to be 15 times (Köhler et al 2007) and 50 times dependent mortality (Nadkarni and Solano (Nadkarni et al 2004) greater than in nearby 2002). Models of climate change predict that secondary forests, as well as offering different cloud height will rise in the coming decades nutrient balances (Nadkarni et al 2004) and (Still et al 1999), which would have serious significantly greater water storage capacity in implications for a cloud forest such as the primary forest (Köhler et al 2007). Monteverde, which resides at the top of its local Similarly, comparing plant species across elevation gradient. Ongoing research in the different climatic zones is moving from an Monteverde area is further exploring the interesting description of community turnover to relationship between epiphyte ecology and an urgent need to understand where, why, and

how plants are limited, enabled, or controlled by only 10% of seeds were dispersed into this climate. Monteverde is an excellent place to “high-quality” zone; over 70% of seeds ended study the biotic effects of variations in climate, up within 10m of a conspecific adult, where they because the unique topography of the area yields suffer higher mortality from predation and a wide range of temperature, precipitation, fungal infection (Wenny 2000b), consistent with seasonality, and other conditions, encompassing the Janzen-Connell hypothesis (Janzen 1970, six Holdridge life zones in a relatively small Connell 1971). There is evidence that different area (Haber 2000; Bolaños et al 2005). An species of birds create different seed shadows analysis of tree species composition and through dispersal. Bellbirds tended to deposit turnover across two 300m elevational transects over half of Ocotea endresiana seeds >25m in Monteverde revealed that species turnover from the parent tree, and more often in gaps, corresponds with gradients in climatic whereas other species of birds only dispersed conditions (precipitation, temperature, and soil), 6% of seeds so far away, and less than 3% in suggesting that many species respond strongly to gaps (Wenny 2000a). Two trees in the the diverse microclimates created by complex Meliaceae family, Guarea glabra and G. topography and sharp elevational relief, which kunthiana, are also bird dispersed, but the yields the high beta diversity found in the area secondary dispersal caused by rodents hoarding (Häger 2010). The discovery of foliar water the seeds may actually be another important uptake by Goldsmith et al (2013) emphasized component of their dispersal syndrome. The that the ability to absorb water from the clouds rodents tended to bring the seeds to microsites was stronger in tree species native to the cloud more beneficial for germination success, due to forest compared to other species found at only increased distance from conspecifics as well as slightly lower elevations, below the cloud base. ecological characteristics such as lower leaf Forthcoming elevational gradient analyses in litter and vegetation density (Wenny 1999). Monteverde include epiphyte species’ From a community standpoint, seed rain was distributions and microbial characteristics of compared between canopy branches and ground both terrestrial and arboreal soil. soil in Monteverde. The canopy seed rain was Population studies of the Lauraceae tree dominated by epiphytic species, while seeds Ocotea ternera have deepened our found on the ground were most commonly from understanding of this important species, which large trees, indicating successful adaptation of serves as a primary food source for many cloud directed dispersal for both groups. The majority forest birds. A long-term study with 20 years of of all seeds was dispersed by birds (Sheldon and measurements on a natural population of O. Nadkarni 2013). Within seed banks of pioneer ternera, a species with sexually dimorphic species, seeds that have greater chemical individuals, revealed that female trees suffer a defenses tend to persist for longer in the soil cost of reproduction, observed via reduced (Veldman 2007). lifetime growth and lower photosynthetic Due to the unique and incredibly diverse capacity in the year following reproduction. composition of Monteverde’s flora, new species Females also had overall slower growth rates and taxonomic revisions are constantly and photosynthetic capacity than males augmenting what is known. Recent newly (Wheelwright and Logan 2004), but larger leaf described species include, but are far from size, possibly to make up for their lower limited to, Dioscorea natalia (Dioscoreaceae) photosynthetic capacity (Wheelwright et al (Hammel 2000), Eugenia haberi (Myrtaceae) 2012). (Barrie 2006), and Mucuna monticola Seed dispersal is another crucial aspect of (Leguminosae-Papilionoideae-Phaseoleae) plant reproduction, and this life history feature (Moura et al 2012). For the most updated plant has been examined in depth in several species taxonomy, readers should consult the Manual de and communities in Monteverde. Seed survival Plantas de Costa Rica (Hammel et al, 2010) or in the bird-dispersed tree Beilschmiedia pendula the TROPICOS database at (Lauraceae) was found to be optimal in the zone http://www.tropicos.org. between 10-20m from the tree crown, although

In addition to the above discussed studies, population of Didymopanax pittieri, a here I provide a list of other papers published tree of wind-exposed lower montane since 2000 on plant topics from the Monteverde rain forest. Plant Ecology, 210:125–135 area.  Moran, R. C., K. Klimas, & M. Carlsen.  Cascante-Marín, A., M. de Jong, E. D. 2003. Low-trunk epiphytic ferns on tree Borg, J. C. B. Oostermeijer, J. H. D. ferns versus angiosperms in Costa Rica. Wolf, J. C. M. den Nijs. 2006a. Biotropica, 35:48–56. Reproductive strategies and colonizing  Muchhala, N. 2003. Exploring the ability of two sympatric epiphytic boundary between pollination bromeliads in a tropical premontane syndromes: Bats and hummingbirds as area. International Journal of Plant pollinators of Burmeistera cyclostigmata Sciences 167:1187-1195. and B . tenuiflora (Campanulaceae).  Cascante-Marín, A., N. von Meijenfeldt, Oecologia, 134:373–380. H. M. H. de Leeuw, J. H. D. Wolf, J. G.  Murray, K.G., and J. Mauricio Garcia- B. Oostermeijer, J. C. M. den Nijs. C. 2002. Contributions of seed 2008b. Dispersal limitation in epiphytic dispersal and demography to bromeliad communities in a Costa Rican recruitment limitation in a Costa Rican fragmented montane landscape. Journal cloud forest. Pp. 323-338, in: Levey, D. of Tropical Ecology 25:63-73. J., W. R. Silva, and M. Galetti.  Cascante-Marín A., N. von Meijenfeldt, (eds) Seed dispersal and frugivory: H. M. H. de Leeuw, J. H. D. Wolf, J. G. Ecology, evolution, and B. Oostermeijer, J. C. M. den Nijs. conservation. CABI Publishing, 2009. Dispersal limitation in epiphytic Wallingford, UK. bromeliad communities in a Costa Rican  Nadkarni, N. M., D. Schaefer, T. J. fragmented montane landscape. Journal Matelson, & R. Solano. 2002. of Tropical Ecology 25:63-73. Comparison of arboreal and terrestrial  Harvey, C. A. 2000. Windbreaks soil characteristics in a lower montane enhance seed dispersal into agricultural forest, Monteverde, Costa Rica. landscapes in Monteverde, Costa Rica. Pedobiologia, 46:24–33. Ecological Applications, 10:155-173.  Papes, M., A. T. Peterson, & G. V. N.  Harvey, C. A. 2000. Colonization of Powell. 2012. Vegetation dynamics and agricultural windbreaks by forest trees : avian seasonal migration: clues from Effects of connectivity and remnant remotely sensed vegetation indices and trees. Ecological Applications, 10:1762– ecological niche modelling. Journal of 1773. Biogeography, 39:652–664.  Kohlmann, B., D. Roderus, O. Elle, X.  Piper, J. 2006. Colonization of tubu Soto, & R. Russo. 2010. Biodiversity (Montanoa guatemalensis, Asteraceae) conservation in Costa Rica : a windbreaks by woody species. correspondence analysis between Biotropica, 38:122–126 identified biodiversity hotspots (  Stone, J. L., E. E. Wilson, & A. S. Araceae , Arecaceae , Bromeliaceae , Kwak. 2010. Embryonic inbreeding and Scarabaeinae ) and conservation depression varies among populations priority life zones. Revista Mexicana de and by mating system in Witheringia Biodiversidad, 2:511–559. solanacea (Solanaceae). American  Krings, A. 2000. Floristics and ecology Journal of Botany, 97:1328–33. of Mesoamerican montane climber  Waring, B. 2008. Light exposure affects communities: Monteverde, Costa Rica. secondary compound diversity in lichen Selbyana, 21:156–164. communities in Monteverde, Costa  Lawton, R. M. & R. O. Lawton. 2010. Rica. Pennscience, 6:11–13. Complex spacial structure in a

 Yanoviak, S. P., H. Walker, & N. M. Nadkarni. 2003. Arthropod assemblages in vegetative vs humic portions of epiphyte mats in a neotropical cloud forest. Pedobiologia, 48:51–58.  Yanoviak, S. P., N. M. Nadkarni, R. Solano. 2007. Arthropod assemblages in epiphyte mats of Costa Rican cloud forests. Biotropica, 39:202–210.

4 Insects and Spiders — Update 2014

Paul Hanson

In the last 15 years there have been a number here, there is still much to learned about the of publications on the insects of cloud forests, arthropods of cloud forests. and it is impossible to include all of them in this update. In particular, it has not been possible to Small insect orders compile all the taxonomic publications that For dragonflies and damselflies (Odonata) include species occurring in Monteverde, a there is a very useful website that provides keys compilation that would be useful since and descriptions of the families, as well as identification is the principal impediment to photos of all the species known from studying insects. Nonetheless, I have attempted Monteverde (Haber 2014). to mention the most important taxonomic For the order Orthoptera there are two publications (of an order, family or subfamily) general publications, one on katydids as well as some examples of specific (Tettigoniidae: subfamily Conocephalinae) investigations. (Naskrecki 2000) and another on grasshoppers As in Hanson (2000), this update is organized (suborder Caelifera) (Rowell 2013), which by taxonomic group. Nonetheless, some provide valuable resources for future research on publications deal with distinct groups and these groups of insects. therefore do not fit this organization, for example the studies of arthropods associated True bugs, spittlebugs, leafhoppers, with epiphytes (Yanoviak et al. 2004, 2006). treehoppers, etc. (order Hemiptera) Before commencing with the individual groups, The vast majority of true bugs (suborder two general comments should be made. First, the Heteroptera) are predatory or phytophagous, but estimations of species numbers in each order are species in the subfamily Triatominae too low, but updated estimations are not (Reduviidae) suck blood from vertebrates. In attempted here. Second, it is important to Costa Rica, one species, Triatoma dimidiata, is emphasize that despite the advances reported the vector of Chagas disease. One of the few studies of this species in the wild was carried out

in Monteverde (Salas Peña 2010), where it was Butterflies and moths (order Lepidoptera) found principally on trunks of live trees, although it was more abundant in residential For butterflies (superfamily Papilionoidea) areas. there is a website providing a list of species With respect to the suborder known from Monteverde, with more detailed Auchenorrhyncha, the principal publication in information and photos of the glasswing recent years is one on treehoppers butterflies (Nymphalidae: Ithomiini) (Haber (Membracidae), which includes a guide for 2001). identification, photos of all the genera, and In Hanson (2000) there is a summary of the summaries of their biology (Godoy et al. 2006). biology of Manataria maculata (Nymphalidae- This book should greatly facilitate future studies Satyrinae; now classified as a subspecies of M. of these gaudy insects. A publication on the hercyna), which lays eggs on bamboo in the spittlebugs (Cercopidae) associated with Pacific lowlands (Murillo & Nishida 2003), but pastures (Thompson & León-González 2005) spends most of the year in reproductive diapause will assist in identifying Monteverde species at higher altitudes, including Monteverde. This associated with grasses. is an unusual butterfly in that it is crepuscular Recently, a study was carried out in and uses different communal roosts—protected Monteverde which examined the responses of sites near the ground during the day and in the six species of Auchenorrhyncha to a model of a canopy at night, probably to avoid birds during redstart (Myioborus, Parulidae), a bird species the day and mice during the night (Hedelin & that hunts insects by first frightening and then Rydell 2007). Its Vogel’s organ, situated at the pursuing them. Two Membracidae (with base of the front wing, detects ultrasounds of structural defenses) were the most sensitive, insectivorous bats, allowing this butterfly to whereas two Cixiidae (defended by camouflage) respond with evasive flight (Rydel et al. 2003). were the last to flee; two Cercopidae (with Although Vogel’s organ is found in the majority aposematic coloration) showed an intermediate of Satyrinae, this is the first case where response (Galatowitsch & Mumme 2004). sensitivity to ultrasound has been demonstrated (other Satyrinae probably use this organ to Beetles (order Coleoptera) detect the sounds associated with birds in flight). Some general works that include aids for As mentioned in Hanson (2000), the only identification and summaries of biology are Satyrinae in Monteverde with transparent wings available for Staphylinidae (Navarette-Heredia is Cithaerius pireta (cited as C. menander). et al. 2002), Scarabaeidae-Dynastinae (Ratcliffe Recently, the larval host plant of this species has 2003), Scarabaeidae-Cetoniinae (Solís 2004), been discovered, Philodendron herbaceum Chrysomelidae-Cassidinae (Chaboo 2007) and (Araceae) (Murillo-Hiller 2009). Chrysomelidae-Chrysomelinae (Flowers 2004). Most families of Lepidoptera are One of the largest families of beetles is microlepidopterans, but their biology is Curculionidae, which includes the phytophagous relatively poorly known. The larvae of many weevils. Two groups that are found in species are leaf miners or leaf rollers. The larvae Monteverde and which have been the subjects of of a few species induce galls on plants; for research in recent years are members of the example, an undescribed species of Momphidae subfamily Baridinae associated with Piperaceae produces quite large stem galls on Conostegia (Prena 2010) and those in the tribe Derelomini oerstediana (Melastomataceae). (now known as Acalyptini; subfamily Curculioninae). Various members of the latter Flies (order Diptera) group are pollinators of palms, but some species Of all the principal insect orders, the have changed host plants and can be pollinators inventory of flies is the most advanced, both in of Cyclanthaceae and Anthurium (Araceae) Costa Rica as a whole and in cloud forests in (Franz 2006). particular. The two volumes by Brown et al. (2009, 2010) provide keys for the identification of fly genera and summaries of our knowledge

of each genus. This valuable work opens doors attached to its abdomen (Blanco & Barboza for future research on flies. 2005). Many of the specialists who collaborated in the production of the two volumes mentioned Wasps, ants and bees (order above are currently carrying out an inventory of Hymenoptera) the flies found in a cloud forest at Zurquí de There are two books in Spanish on the Moravia (Zurqui All-Diptera Biodiversity Hymenoptera of the Neotropical region, one that Inventory, ZADBI 2014). Although this cloud emphasizes identification (Fernández & Sharkey forest is located in a different mountain range, 2006) and the other with detailed summaries of the results of this project will be very applicable the biology of the order (Hanson & Gauld 2006). to the Monteverde cloud forest. When the results Although these books cover the entire region, of the Zurqui project become available we they provide a good introduction for studies of should have a significantly better understanding Monteverde hymenopterans. of the fly fauna of Costa Rican cloud forests. The vast majority of hymenopterans are The biology of fly larvae is extremely parasitoids of other insects, but in recent years diverse. This order includes the most species- several species have been discovered that have rich family of gall-inducers, Cecidomyiidae made an evolutionary transition to phytophagy. (Hanson & Gómez-Laurito 2005). Although For example, in Monteverde the larvae of there is a large diversity of plant galls in Eurytoma werauhia (Eurytomidae) feed on the Monteverde, there are very few studies of these floral buds of Werauhia gladioliflora insects. In large part this is due to the fact that (Bromeliaceae) (Gates & Cascante-Marín 2004). Cecidomyiidae is probably the largest family of In the Central Valley of Costa Rica the larvae of insects and at the same time probably harbors Allorhogas conostegia (Braconidae) induce galls the greatest proportion of undescribed species in the fruits of Conostegia xalapensis (more than 99%). Other phytophagous fly larvae (Melastomataceae), but it is possible that in include leaf miners, for example, two species of Monteverde another (undescribed) species of the Agromyzidae on Bocconia frutescens same genus produces these galls (Chavarría et (Papaveraceae) (Boucher & Nishida 2014). al. 2009a). This deserves more research, and if The larvae of other flies are predators, one of this hypothesis is correct, it could represent an the best studied families being Syrphidae. The interesting case of speciation. literature gives the impression that nearly all The wasps that are best known to the general predatory syrphid larvae feed on aphids and public are the eusocial wasps which construct other Sternorrhyncha (Hemiptera) on plants. paper (carton) nests (Vespidae, subfamily Nonetheless, the biology of predatory syrphids is Polistinae). The best studied species in probably much more diverse in the Neotropics. Monteverde is Polybia aequatorialis (O'Donnell For example, Ocyptamus luctuosus, a species et al. 2004, Jones et al. 2009), which is the only found in Monteverde, is a predator in the water species of Polistinae that occurs at very high that accumulates in epiphytic bromeliads elevations (more than 3000 m), where they have (Rotheray et al. 2000). Ocyptamus is one of the enormous colonies (Chavarría et al. 2009b). most diverse genera of Syrphidae and the Ants (Formicidae) continue to be one of the evidence suggests that it is not a monophyletic best studied hymenopteran families in group (Mengual et al. 2012). Monteverde. Some research deals with the entire Some adult flies are pollinators of certain ant fauna. For example, utilizing canopy plants. An unusual example from Monteverde is fogging, fewer species were found in secondary the fungus gnat, Bradysia floribunda (Sciaridae), forest than in primary forest, but the number of which pollinates Lepanthes glicensteinii species in pasture trees was similar to that in (Orchidaceae) via a mechanism known as primary forest (Schonberg et al. 2004). A study pseudocopulation. This orchid attracts and dupes of leaf litter ants showed that the complex of the male fungus gnats, which confuse the flower species was not very affected by the formation for a female gnat and then copulate with it, in of forest clearings (Patrick et al. 2012). Other the process receiving a pollinarium that becomes studies deal with particular groups of ants and in

recent years army ants (Ecitoninae, now placed Spiders (order Araneae) in Dorylinae) have received considerable A recent study of the arboreal spiders in attention, especially with respect to the effects of Monteverde found no differences in the altitude/temperature and forest fragmentation on abundance or number of species in primary the ants (O'Donnell & Kumar 2006, Kumar & versus secondary forest. Nonetheless, in both O'Donnell 2009, Soare et al. 2014), and the birds forest types vertical differences were observed, that accompany these ants (Kumar & O'Donnell with greater abundance and a greater number of 2007). species on tree trunks (from zero to two meters above the ground) than in the canopy (Yanoviak et al. 2003).

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Jones, T. A., N. A. Donlan, and S. O’Donnell. 2009. in the genus Ocyptamus (Diptera, Syrphidae). Growth and pruning of mushroom body Kenyon Studia Dipterologica 7:385–398. cell dendrites during worker behavioral Rowell, C. H. F. 2013. The Grasshoppers (Caelifera) of development in the paper wasp, Polybia Costa Rica and Panama. The Orthopterists' aequatorialis (Hymenoptera: Vespidae). Society: Publications on Orthopteran Diversity. Neurobiology of Learning & Memory 92:485– 611 pp. 495. Rydell, J., S. Kaerma, and H. Hedelin. 2003. Evasive Kumar, A., and S. O’Donnell. 2007. Fragmentation and response to ultrasound by the crepuscular elevation effects on bird–army ant interactions in butterfly Manataria maculata. neotropical montane forest of Costa Rica. Journal Naturwissenschaften 90:80–83. of Tropical Ecology 23:581–590. Salas Peña, R. 2010. Ecología del chinche bebesangra Kumar, A., and S. O'Donnell. 2009. Elevation and forest Triatoma dimidiata (Reduviidae: Triatominae) en clearing effects on foraging differ between ambientes domésticos y silvestres de surface and subterranean army ants (Formicidae: Monteverde, Costa Rica. Tesis de M.Sc., Escuela Ecitoninae). Journal of Animal Ecology 78:91– de Biología, Universidad de Costa Rica. 97. Schonberg, L. A., J. T. Longino, N. M. Nadkarni, S. P. Mengual, X., G. Ståhls, and S. Rojo. 2012. Is the mega- Yanoviak, and J. C. Gering. 2004. Arboreal ant diverse genus Ocyptamus (Diptera, Syrphidae) species richness in primary forest, secondary monophyletic? Evidence from molecular forest, and pasture habitats of a tropical montane characters including the secondary structure of landscape. Biotropica 36:402–409. 28S rRNA. Molecular Phylogenetics and Soare, T. W., A. Kumar, K. A. Naish, and S. O’Donnell. Evolution 62:191–205. 2014. Genetic evidence for landscape effects on Murillo, L. R., and K. Nishida. 2003. Life history of dispersal in the army ant Eciton burchellii. Manataria maculata (Lepidoptera: Satyrinae) Molecular Ecology 23:96–109. from Costa Rica. Revista de Biología Tropical Solís, A. 2004. Escarabajos Fruteros de Costa Rica. Fruit 51:463–470. Beetles of Costa Rica. Instituto Nacional de Murillo-Hiller, L. R. 2009. Early stages and natural history Biodiversidad, Santo Domingo de Heredia, Costa of Cithaerias p. pireta (Satyrinae) from Costa Rica. 238 pp. Rica Journal of the Lepidopterists' Society Thompson, V., and R. León-González. 2005. La 63:169–172. identificación y distribución de los salivazos de la Naskrecki, P. 2000. Katydids of Costa Rica. Vol. 1. caña de azúcar y los pastos (Homoptera: Systematics and Bioacoustics of the Cone-Head Cercopidae) en Costa Rica. Manejo Integrado de Katydids. Academy of Natural Sciences, Plagas y Agroecología (Costa Rica) 75:43–51. Philadelphia. 164 pp. + cd Yanoviak, S. P., G. Kragh, and N. M. Nadkarni. 2003. Navarette-Heredia, J. L., A. F. Newton, M. K. Thayer, J. S. Spider assemblages in Costa Rican cloud forests: Ashe, and D. S. Chandler. 2002. Guía Ilustrada Effects of forest level and forest age. Studies on para los Géneros de Staphylinidae (Coleoptera) Neotropical Fauna and Environment 38:145–154. de México. La Universidad de Guadalajara y Yanoviak, S. P., H. Walker, and N. M. Nadkarni. 2004. CONABIO, México. 401 pp. Arthropod assemblages in vegetative vs humic O’Donnell, S., and A. Kumar. 2006. Microclimatic factors portions of epiphyte mats in a neotropical cloud associated with elevational changes in army ant forest. Pedobiologia 48:51–58. density in tropical montane forest. Ecological Yanoviak, S. P., N. M. Nadkarni, and S. J. Rodrigo. 2006. Entomology 31:491–498. Arthropod assemblages in epiphyte mats of Costa O’Donnell, S., N. A. Donlan, and T. A. Jones. 2004. Rican cloud forests. Biotropica 36:202–210. Mushroom body structural change is associated ZADBI (Zurqui All-Diptera Biodiversity Inventory). with division of labor in eusocial wasp workers http://phorid.net/zadbi/ Consulted May 22, 2014. (Polybia aequatorialis, Hymenoptera: Vespidae). Neuroscience Letters 356:159–162. Patrick, M., D. Fowler, R. R. Dunn, and N. J. Sanders. 2012. Effects of treefall gap disturbances on ant assemblages in a tropical montane cloud forest. Biotropica 44:472–478. Prena, J. 2010. The Middle American species of Peridinetus Schönherr (Coleoptera: Curculionidae: Baridinae). Zootaxa 2507:1–36. Ratcliffe, B. C. 2003. The Dynastine scarab beetles of Costa Rica and Panama (Coleoptera: Scarabaeidae: Dynastinae). Bulletin of the University of Nebraska State Museum 16:1–506. Rotheray, G. E., M. Zumbado, E. G. Hancock, and F. C. Thompson. 2000. Remarkable aquatic predators

6 Birds — Update 2014

Bruce E. Young

Although the pace of research on birds in following summarizes the major findings of the Monteverde may have slowed during the 14 27 publications that encompass this new years since the last synopsis (Young and research. McDonald 2000), researchers continue to make important contributions to tropical avian biology Elevational Gradients, Migration, and and other scientific disciplines. Elevational Conservation gradients and migrations of birds along them New research has shed light on the still inspire research in Monteverde, where field remarkable biotic turnovers associated with study at varying elevations is facilitated by the elevational gradients that characterize steep topography and easy access. These Monteverde and many tropical mountain slopes. gradients are also useful for studying biotic A new statistical analysis revealed that the beta responses to climate change, a growing threat to diversity (the increase in species richness across biodiversity, especially in the tropics (Colwell et habitats) of birds on the Pacific slope of al. 2008). Ornithologists completed two new Monteverde is twice as high as that at the same autecological studies and finished two long-term elevations on temperate mountains (Jankowski studies initiated in the 20th century, continuing a et al. 2009). Moisture gradients, rather than long and valuable tradition in Monteverde. Other elevation per se, best explained the rapid species scientists tackled new research topics in bird- turnover. The Caribbean slope of Monteverde, army ant interactions and behavior. Finally, with a less dramatic moisture gradient, has careful observation continues to extend our substantially lower beta diversity than that of the knowledge of natural history, such of the first Pacific slope, where a rain shadow accentuates nest description for Silvery-fronted Tapaculo moisture differences. One mechanism leading to (Scytalopus argentifrons; Young and Zuchowski narrow ranges of Monteverde birds appears to be 2003) and an observation of a Slaty-backed behavior. A series of song playback experiments Nightingale Thrush (Catharus frantzii ) foraging demonstrated that congeneric species that on a frog (Acosta and Morún 2014). The replace each other along elevational gradients

show interspecific territorial behavior toward four-part migration that spans 200 km (Powell one other (Jankowski et al. 2010). and Bjork 2004). Radio-collared individuals How does abundance correlate with range migrated from Monteverde to the Caribbean size in birds occupying Monteverde’s different lowlands of northwestern Costa Rica and elevational zones? An extensive analysis using southeastern Nicaragua during the period of both mist-net and point count data revealed that September to December, then flew to species occupying fewer sites also tend to be southeastern Costa Rica where they remained less abundant in those sites than those occupying until March. Then they migrated to their more sites (Jankowsli and Rabenold 2007). At a breeding area at 1000-1800 m on the Caribbean broader scale, species with larger range sizes slope of Monteverde. Finally, in June and July, occupied more habitat zones in Monteverde than the birds migrated back across the continental those with smaller range sizes. Species endemic divide to mid-elevation Pacific slopes in to Costa Rica and western Panama tended to Monteverde, where they remained until occur at the highest elevations and have lower September. The migrations of bellbirds and abundance. These results highlight the umbrellabirds highlight pressing conservation conservation challenges posed by this and other needs. Although the breeding areas of both are endemic highland avifaunas: most species are well protected in Monteverde, each spends relatively rare at both geographical and local significant periods of time in unprotected scales. habitats. Umbrellabirds descend to the lowest Seasonal migration across elevational elevation where intact forest remains on the gradients continues to attract scientific attention. Caribbean slope of Monteverde. Loss of lowland A study of eight large frugivorous bird species, habitat may be a limitation for the Monteverde including guans, trogons, toucans, and cotingas, population as this species is known to occur at confirmed the results of earlier studies on much lower elevations elsewhere in Costa Rica seasonal movements (Chaves-Campos 2004). where lowland forests persist. Bellbirds are also The birds generally nest at higher elevations and vulnerable because they spend at least half of move to lower elevations when not breeding, their annual cycle on unprotected lands. although some individuals remain at high elevations year round. This pattern may be Climate Change partially explained by seasonal changes in fruit Ongoing climate change threatens species abundance and precipitation, but additional and ecosystems worldwide. Sensitivity of factors may also be involved. A separate study Monteverde habitats to climate and dramatic of vegetation seasonality did not detect a link climate differences over small spatial scales between vegetation changes and the migration of combine to make the area ideal for studying the one of the species that Chaves-Campos studied, effects of climate change on natural systems. the Bare-necked Umbrellabird (Cephalopterus Careful monitoring of the breeding birds in a glabricollis; Papes et al. 2012) small study plot near the entrance of the Radio-tracking of two of these large, migrant Monteverde Cloud Forest Preserve revealed that frugivores, the Bare-necked Umbrellabird and lower elevation species were colonizing and that Three-wattled Bellbird (Procnias higher elevation species were declining (Pounds tricarunculatus), revealed more details about the et al. 1999). Annual colonizations were closely annual movements of the two species. These tied to the annual number of precipitation-free species are important from a conservation days, which result from increasing temperatures standpoint because both are categorized as that raise cloud-bank levels. threatened on the IUCN Red List of Threatened A subsequent study modeled the effects of Species. The Bare-necked Umbrellabird appears future climates on the community of montane to make a straightforward migration between birds. Using data on current population sizes, breeding areas at 800-1400 m, and lower fine spatial-scale models predicted the decline of elevations (600-800 m) during the nonbreeding nearly half of 77 species currently occurring in season (Chaves-Campos et al. 2003). The the higher elevation forests of Monteverde bellbird, on the other hand, makes a spectacular during the next 100 years (Gasner et al. 2010).

More sobering was the finding that seven of the Rosa National Park, 115 km away in the Pacific eight species predicted to become extirpated in lowlands (McDonald 2003). Although gene flow the region already have small ranges restricted to appears to be greater up from Santa Rosa to Costa Rican and western Panamanian highlands. Monteverde than in the reverse direction, the intense sexual selection on this lek-breeding Birds and Army Ants species appears to be insufficient to create A new area of study for Monteverde is the significant genetic isolation to lead to speciation. interaction between birds and army ants. The Brown Jays are known for their cooperative bird-army ant relationship is well known in breeding system in which multiple females and tropical lowland forests, where several specialist males contribute to the rearing of young. Use of species forage on insects and other invertebrates multi-locus DNA fingerprinting has shown that as they flee advancing army ant foraging raids. virtually all chicks in a nest are the offspring of Recent observations in Monteverde reveal that a a single primary female breeder that is able to surprising diversity of montane birds also follow suppress breeding by other females in her group army ants when they swarm. During two months (Williams 2004). Males have much less skewed of opportunistic observations at 1200-1650 m breeding success, with multiple paternity elevation, researchers identified 41 bird species occurring in 33-40% of nests, and extra-group attending army ant raids (Kumar and O’Donnell paternity occurring in at least 20% of nests. 2007). Neither the diversity nor the abundance Group size is important in determining the of ant-following birds was influenced by breeding success of a group. Larger groups are elevation, but both factors were affected by better able to defend territories with isolated forest patch size. More bird species and more nesting trees, which are key to preventing nest individuals followed army ants in continuous predation, the leading cause of nest failure forest than in small forest fragments. More (Williams and Hale 2006). Increased nesting extensive observations showed that resident success and post-fledging survival were also species are more likely to follow raids than long- correlated with group size. The benefit to non- distance migrants, and eight resident species reproductive helpers in a group appears to be regularly visit army ant bivouacs to determine access to future breeding opportunities. when raids begin (O’Donnell et al. 2010). Observation of marked individuals showed that Although no montane species rely on army ants breeding females and their social mates maintain as extensively as some lowland specialists, their bond across years and have higher nest attending army ant raids is an important foraging attendance and nestling feeding rates than activity for several montane bird species. helpers (Williams and Hale 2007). Compared to other New World jays, however, social mates Autecological Studies invested relatively less in nesting activities, A major contribution of ornithological suggesting that mate guarding may not be an research in Monteverde has been a series of effective strategy (Williams and Hale 2008). autecological studies that provide detailed The Slate-throated Redstart is a common aspects of the life cycle and behavior or montane resident in all but the highest elevation forests in tropical birds (Young and McDonald 2000). Monteverde, calling attention to itself with its Over the last 14 years, new results became constantly flashing white outer tail feathers. A available from two of those studies, on Brown set of ingenious experiments and observations Jays (Cyanocorax morio) and Long-tailed confirmed a hypothesis that the adaptive value Manakins (Chiroxiphia linearis), while of this plumage coloration is to startle researchers initiated studies of two additional invertebrate prey during flush-pursuit foraging. species, the Black-Breasted Wood-Quail Individuals that had their white outer tail (Odontophorus leucolaemus) and Slate-throated feathers experimentally blackened foraged with Redstart (Myioborus miniatus). In an epilogue to only one-third the success of controls in which a long-term study of Long-tailed Manakins, a inner, black tail feathers where colored with a genetic study found little differentiation between black marker (Mumme 2002). Further tail- manakins in Monteverde and those in Santa coloring experiments that mimicked the natural

variation in the extent of white tail feathers in year) song development period also strengthens geographic subspecies of the Slate-throated the argument that bellbirds learn their songs, as Redstart ranging from Mexico to Bolivia does the fact that adults continually relearn suggested that white tail feathers are adaptive for songs (Kroodsma et al. 2013). increasing foraging success, but the extent of white is constrained by regional habitat Landscape Ecology characteristics (Mumme et al. 2006). One novel study developed land-cover Breeding in the Slate-throated Redstart is models of bird use of habitats in forest typical for Monteverde birds, spanning the late fragments in Coto Brus, in southern Costa Rica, dry and early wet seasons from late May to early and then tested the models’ ability to predict June during a five-year observation period bird diversity and abundance in Monteverde (Mumme 2010). Females incubate clutches that habitats at similar elevations and life zones, 230 average 2.9 eggs, but both parents feed young. km away (Lindell et al. 2006). The results were Fledging occurred at an average age of 11 days, mixed. Coto Brus models for canopy and parents subsequently provisioned fledglings insectivores, understory insectivores and non- for an additional four weeks. Nesting success insectivores, and edge non-insectivores were was 40%, with predation the cause of 85% of successful for characterizing abundance of nest failures (Mumme 2010). Monteverde birds in these habitats. However, Black-Breasted Wood-Quail live year-round Coto Brus models for open-country birds did not in coveys of an average of four individuals predict abundances of open-country birds in (range 2-9) at similar densities (about one covey Monteverde. None of the predictions for species per 3.3 ha) in both fragmented and intact forest richness developed from the Coto Brus data set (Hale 2006). This species also breeds at the dry- were more accurate than null models at wet season transition. Larger coveys produce predicting species richness in Monteverde more offspring than small coveys, hinting that communities. These findings indicate that land the species may have a cooperative breeding cover models are best extrapolated over the system (Hale 2006). Sampling of 50 individuals region where parameters are measured. from Monteverde revealed nine polymorphic On a finer spatial scale, one observer asked microsatellite loci, providing useful markers for what influenced bird visits to Sapium future genetic studies of this and other glandulosum trees isolated in pastures. Fifty-two Odontophorus species (Hale and Hughes 2003). bird species visited focal trees, preferentially visiting larger, more isolated trees with higher Behavior epiphyte loads (Sheldon and Nadkarni 2013). Several lines of evidence now indicate that Although epiphyte loads helped attract birds, Three-wattled Bellbirds learn their songs, most foraging activity was focused on the host making this species the first sub-oscine tree itself. Visitation was not affected by the passerine known to learn songs (Saranathan et distance of trees from forest edges, suggesting al. 2007, Kroodsma et al. 2013). Song learning that Monteverde pastures are small relative to has previously been documented only in distances birds are willing to travel for foraging hummingbirds, parrots, and oscine passerines. opportunities. First, variation in mitochondrial DNA sequences and nuclear microsatellite loci does not Conclusions correspond with the three vocal dialects of the Study of Monteverde’s avifauna continues to species, which occur in Nicaragua, Monteverde, provide new perspectives on tropical birds. and Talamanca in southern Costa Rica Although the area will continue to provide ready (Saranathan et al. 2007). In addition, access to protected study sites, the future is Monteverde birds appear to be bilingual, using uncertain for some members of the bird the Talamanca as well as Monteverde dialects; a community. Climate change threatens to reduce captive male raised in isolation developed the diversity of endemic species, and the abnormal songs that more closely resembled shortage of protected habitats outside of birds that occurred nearby. The lengthy (six Monteverde may compromise the persistence of

some regional migrant species. Colonization by (Dornelas et al. 2014). The new body of research lowland species may serve to maintain species from Monteverde extends the outsized role that richness, consistent with observations of the region’s avifauna has played in shaping our assemblages in which species richness remains understanding of tropical avian biology. despite declining temporal beta-diversity

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landscape in Monteverde, Costa Rica. Journal of Williams, D. A. and A. M. Hale. 2008. Investment in Tropical Ecology 29:459–462. nesting activities and patterns of extra- and Williams, D. A. 2004. Female control of reproductive skew within-group genetic paternity in a cooperatively in cooperatively breeding brown jays breeding bird. Condor 110:13–23. (Cyanocorax morio). Behavioral Ecology and Young, B. E. and W. Zuchowski. 2003. First description of Sociobiology 55:370-380. the nest of the Silvery-fronted Tapaculo, Williams, D. A. and A. M. Hale. 2006. Helper effects on Scytalopus argentifrons. Wilson Bulletin 115:91- offspring production in cooperatively breeding 93. Brown Jays (Cyanocorax morio). Auk 123:847. Young, B. E. and D. B. McDonald. 2000. Birds. In Williams, D. A. and A. M. Hale. 2007. Female-biased Monteverde: Ecology and Conservation of a helping in a cooperatively breeding bird: Female Tropical Rainforest, N. M. Nadkarni and N. T. benefits or male costs? Ethology, 113:534–542. Wheelwright (eds). Oxford University Press, New York, pp. 179-222.

77

Mammals — 2000–2017

Robert M. Timm Richard K. LaVal

Mammalogists currently recognize We are fortunate that a number of nearly 6,400 species of Recent mammals biologists have worked at Monteverde worldwide and the number of new species beginning in the 1960s and considerable being recognized has increased dramatically information and voucher material are in recent decades. It is estimated that available for study. We now know that at perhaps as many as 7,500 species might least 90 of mammals occur in the greater occur when additional studies are Monteverde area. However, one of the completed. This increase in the number of outcomes of these studies is that a number of mammal species known is a result of name changes are proposed each year. exciting new discoveries in the field, as well These better reflect relationships between as additional study of scientific specimens species; however, a bewildering array of housed in museums. Using new techniques, new names often makes it difficult to including genetic data, as well as traditional understand what is happening when authors morphological studies, scientists are refer to an animal for which more than one undertaking taxonomic revisions that scientific name exists, sometimes significantly increase our understanding of surrounded by controversy. A scientific the diversity of mammals and the name associated with a species is a relationships among species. hypothesis. Eventually, usage of these new 2

names in scientific publications will lead to comparisons should be made for each zone their acceptance (or refinement, in some and not the entire list as representative of cases). Meanwhile, it is up to researchers to Monteverde. Comparisons are best made make the sometimes difficult decisions as to with specific habitats (life zones) within the whether to use the new names in our greater Monteverde area. publications. Herein, our decisions are LaVal’s (in press) extensive use of based on the current literature, our Anabat detection systems has added a experience with these species both in the number of species of bats new to the various field and in study of museum specimens, life zones that were not detected via standard and the best information currently available mist nets. This has been especially true for to us. Many of the name changes we the emballonurid and molossid bats. provide below to the list of mammals of Life zones are generally agreed to be Monteverde appear in specialized systematic biologically defined areas in which there is revisions; to assist researchers interested in notable similarity between the flora and Monteverde mammals, we provide the new fauna throughout the zone. These are often name as well as a footnote to the older defined by the species of birds and plants name. that occur there because these are easily At present, only one species of mammal, observed and that has been especially true at a newly described small-eared shrew, is Monteverde. On mountain slopes, upper apparently endemic to Monteverde. A and lower elevational limits can help to single specimen of shrew found in the define the zones, but it is generally agreed Reserve in 1973 was described recently as now that any boundaries between two Cryptotis monteverdensis; extensive efforts adjacent zones are poorly defined and to obtain additional specimens have proven flexible over time. When climate change futile to date (Woodman and Timm 2017). leads to warmer (or cooler or drier) A species of harvest mouse of the genus conditions, these elevational limits may Reithrodontomys found in the cloud forest move up or down the mountain as organisms also represents an undescribed species (see attempt to remain within the temperature below). Additionally, intriguing and humidity limits to which they are observations suggest that one or more adapted. Thus, a bat for example originally unrecognized species of rodents might be restricted to Zone 1 in Monteverde, might found in the cloud forest (LaVal, pers. obs.). move up to Zone 2 under warming Researchers who wish to make conditions (see LaVal 2004). In our 2000 comparisons between regions, habitats, or list of distributions of mammals in the elevations should use this English version or Monteverde region, we listed southern the Spanish updated version (LaVal and cotton rats as rare in zones 1 and 2. Today, Timm 2014; Apéndice 11) of our species cotton rats are abundant in those zones in lists of Monteverde mammals because a disturbed habitats. The rain shadow on the significant number of changes have been Pacific slope, heavily disturbed grassy areas, made since 2000. These changes are due in and climate change have seemly created part to a more refined understanding of abundant habitat for this grassland species at distributions and systematic relationships of Monteverde as well as elsewhere on Costa the mammals, but also to improved ability to Rica’s Pacific slopes. At Monteverde, detect species and distributional changes due plants and birds were originally used to to climatic change. Because six life zones define the life zones, whereas most species are represented in the updated species lists, of mammals were distributed across two or 3

more life zones (see Timm and LaVal book in 2000. The first in this series, 2000a, b, c). Apéndice 10 (Timm and LaVal 2014), is a Owing to our ever-increasing knowledge Spanish translation of the original Appendix of Monteverde mammals and the long-term 10 from the Monteverde book. The second work that has been done there, interesting (LaVal and Timm 2014) is a Spanish changes in distributional and ecological updated version of that original listing of patterns are being discovered. Distributions Monteverde mammals and their distributions of mammals across the elevational zones and abundance. Herein, we update the clearly are changing. LaVal documented distributions of mammals in the six life that vampire bats moved up into the zones represented in the greater Monteverde Monteverde area in the 1990s and cotton rats region, add species newly discovered in the moved up and became abundant in the past region, and provide literature updates. In decade. LaVal noted that cotton rats first these updated versions, we provide brief started appearing in zone 2 in the early comments explaining taxonomic changes 2000s, whereas they were previously known that have occurred since the original listing only from zone 1. An intriguing example of was published in 2000 provided as footnotes a truly sympatric distribution is the to the original appendix. In the References discovery of the two species of mouse below, we include the 25 publications that opossums—Marmosa mexicana and M. have appeared based on the study of zeledoni—in LaVal’s home. The mammals at Monteverde since our 2000 observations were made years apart so the overview, as well as references that we cite two similarly appearing species may not be in preparation of these updated versions. temporally sympatric, but the dry forest Keys to the bats of Costa Rica based species (M. mexicana) and the wet forest extensively on our experience at Monteverde species (M. zeledoni) are now documented were provided in English (Timm and LaVal from a single residence in Monteverde. 1998) and Spanish (Timm et al. 1999). A Three similarly-sized species of small-eared very useful and beautifully illustrated key to shrews are known from the Reserve with the rodents of Costa Rica was provided by Cryptotis nigrescens widespread and Villalobos-Chaves et al. (2016). common throughout the area, whereas C. On a positive note, two factors favor a merriami and C. monteverdensis are known bright future for Monteverde mammals: 1) only in the reserve and are both rare. An immense area of contiguous pristine Considerable differences in the forearm habitat and regenerating forest, around bones of the three similarly-appearing 50,000 hectares, has been preserved and is shrews were documented by Woodman and relatively well-protected in the Monteverde Timm (2017), and they speculated that the area; 2) Most, although not all, Monteverde differences reflected more ambulatory above mammals have distributional and ecological ground versus more semi-fossorial foraging. ranges that cover several life zones and thus This chapter was undertaken along with are less threatened by climate change than two companion chapters (apéndices 10, 11) many birds and herps that may be restricted to update the research and findings in the to one or two life zones. field of mammalogy that have taken place since the publication of the Monteverde

4

Table 1. Mammal distributions and abundances in the Monteverde region—2017.

Richard K. LaVal and Robert M. Timm

Scientific Name Common Name Abundance 1 Life Zone 2 ______

Didelphimorpha Marsupials

Didelphidae American Opossums

Caluromys derbianus Woolly Opossum uncommon 1, 2, 3

Chironectes minimus Water Opossum uncertain 1

Didelphis marsupialis Common Opossum abundant 1, 2, 3, 4, 5, 6

Marmosa mexicana Mexican Mouse Opossum uncommon 1

Marmosa zeledoni Mouse Opossum common 2, 3, 5, 6

Metachirus nudicaudatus Brown Four-eyed Opossum rare 6

Micoureus alstoni Alston’s Opossum uncommon 2, 3, 6

Philander opossum Gray Four-eyed Opossum uncommon 1, 2, 3, 5, 6

Eulipotyphla Shrews

Soricidae Shrews

Cryptotis merriami Merriam’s Small-eared Shrew rare 3

Cryptotis nigrescens Blackish Small-eared Shrew common 2, 3, 4, 5, 6

Cryptotis monteverdensis 3 Monteverde Small-eared Shrew rare 3

Chiroptera Bats

Emballonuridae Sac-winged Bats

Balantiopteryx plicata Gray Sac-winged Bat uncommon 1, 2

Cormura brevirostris Wagner’s Sac-winged Bat rare 6 5

Cyttarops alecto Short-eared Bat rare 3

Diclidurus albus Northern Ghost Bat rare 2, 4, 6

Peropteryx kappleri Greater Dog-like Bat uncommon 2, 6

Peropteryx macrotis Lesser Dog-like Bat rare 2

Rhynchonycteris naso Proboscis Bat rare 2

Saccopteryx bilineata Greater White-lined Bat common 1, 6

Mormoopidae Mustached Bats

Pteronotus davyi Lesser Naked-backed Bat uncommon 2, 5

Pteronotus gymnonotus Big Naked-backed Bat uncommon 1, 2, 3, 4, 5, 6

Pteronotus mesoamericanus 4 Mesoamerican Mustached Bat uncommon 1, 2, 3, 4, 5, 6

Pteronotus personatus Lesser Mustached Bat uncommon 5

Phyllostomidae American Leaf-nosed Bats

Phyllostominae Gleaning Bats

Glyphonycteris sylvestris Tri-colored Big-eared Bat rare 2

Lonchorhina aurita Sword-nosed Bat uncommon 5, 6

Lophostoma brasiliense Pigmy Round-eared Bat rare 1, 6

Micronycteris hirsuta Hairy Big-eared Bat rare 2, 6

Micronycteris microtis Little Big-eared Bat uncommon 1, 2, 3, 4, 6

Micronycteris minuta Tiny Big-eared Bat rare 6

Micronycteris schmidtorum Schmidt’s Big-eared Bat uncertain 5, 6

Mimon cozumelae Cozumel Spear-nosed Bat rare 2

Phylloderma stenops Northern Spear-nosed Bat rare 6

Phyllostomus discolor Pale Spear-nosed Bat common 1, 2

Phyllostomus hastatus Greater Spear-nosed Bat rare 5, 6

Tonatia saurophila Stripe-headed Bat rare 6 6

Trachops cirrhosus Frog.eating Bat uncommon 1, 2, 3, 4, 5, 6,

Vampyrum spectrum False Vampire Bat rare 1, 2, 3, 4, 6

Glossophaginae Pollen- and Nectar-feeding Bats

Anoura cultrata Handley’s Tailless Bat uncommon 2, 3, 4, 5, 6

Anoura geoffroyi Geoffroy’s Tailless Bat common 1, 2, 3, 4, 5, 6

Choeroniscus godmani Godman’s Long-nosed Bat rare 1, 2, 3, 4

Glossophaga commissarisi Commissaris’ Long-tongued Bat common 1, 2, 3, 4

Glossophaga soricina Pallas’ Long-tongued Bat common 1, 2, 3, 6

Hylonycteris underwoodi Underwood’s Long-tongued Bat common 2, 3, 4, 5

Lonchophyllinae Long-tongued Bats

Lonchophylla robusta Panama Long-tongued Bat rare 2, 3, 4, 5, 6

Carolliinae Short-tailed Bats

Carollia castanea Allen’s Short-tailed Bat uncommon 1, 2, 5, 6

Carollia perspicillata Short-tailed Fruit Bat uncommon 1, 2, 3, 5, 6

Carollia sowelli 5 Silky Short-tailed Bat common 1, 2, 3, 4, 5, 6

Carollia subrufa Gray Short-tailed Bat rare 1

Stenoderminae Fruit-eating Bats

Artibeus intermedius Davis’ Fruit Bat uncommon 1, 2

Artibeus jamaicensis Jamaican Fruit Bat common 1, 2, 3, 4, 5, 6

Artibeus lituratus Big Fruit Bat common 1, 2, 3, 4, 6

Dermanura azteca Highland Fruit-eating Bat rare 2, 6

Dermanura phaeota Pygmy Fruit-eating Bat uncommon 4, 5, 6

Dermanura tolteca Toltec Fruit-eating Bat abundant 1, 2, 3, 4, 5, 6

Dermanura watsoni Thomas’ Fruit-eating Bat uncommon 2, 4, 6

Centurio senex Wrinkle-faced Bat rare 1, 2, 3 7

Chiroderma salvini Salvin’s White-lined Bat rare 2

Chiroderma villosum Shaggy-haired Bat rare 2

Ectophylla alba Caribbean White Bat rare 6

Enchisthenes hartii Velvety Fruit-eating Bat rare 1, 2, 3, 4

Platyrrhinus helleri Heller’s Broad-nosed Bat uncommon 1, 2, 5

Platyrrhinus vittatus Greater Broad-nosed Bat common 1, 2, 3, 4, 5, 6

Sturnira hondurensis 6 Highland Yellow-shouldered Bat abundant 1, 2, 3, 4, 5, 6

Sturnira mordax Talamancan Bat uncommon 2, 3, 4, 5, 6

Sturnira parvidens 7 Little Yellow-shouldered Bat uncommon 1, 2

Vampyressa thyone Little Yellow-eared Bat rare 2, 3, 5, 6

Vampyrodes major Great Stripe-faced Bat rare 2, 5

Desmodontinae Vampire Bats

Desmodus rotundus Common Vampire Bat uncommon 1, 2, 3, 5, 6

Diphylla ecaudata Hairy-legged Vampire Bat rare 2

Natalidae Funnel-eared Bats

Natalus lanatus 8 Highland Funnel-eared Bat rare 2

Thyropteridae Disk-winged Bats

Thyroptera tricolor Spix’s Disk-winged Bat common 2, 3, 4, 6

Vespertilionidae Vespertilionid Bats

Bauerus dubiaquercus Doubtful Oak Bat rare 2, 3, 5

Dasypterus ega Southern Yellow Bat common 2, 4, 6

Dasypterus intermedius Northern Yellow Bat rare 2, 6

Eptesicus brasiliensis Brazilian brown Bat common 2, 3, 4, 5, 6

Eptesicus furinalis Argentine Brown Bat uncommon 1, 6

Eptesicus fuscus Big Brown Bat uncommon 2, 3, 4 8

Lasiurus castaneus Tacarcuna Bat rare 4, 5

Lasiurus frantzii Central American Red Bat common 2, 3, 4, 5, 6

Myotis albescens Silver-haired Myotis uncommon 6

Myotis elegans Elegant Myotis uncommon 6

Myotis nigricans Black Myotis common 1, 2, 3, 4, 6

Myotis oxyotus Montane Myotis uncommon 2, 3, 4

Myotis pilosatibialis 9 Hairy-legged Myotis abundant 1, 2, 3, 4, 5, 6

Myotis riparius Riparian Myotis uncommon 1, 2, 6

Rhogeessa io 10 Rainforest Yellow Bat uncommon 6

Molossidae Free-tailed Bats

Eumops auripendulus Shaw’s Mastiff Bat uncommon 1, 2, 4, 6

Molossus molossus Little Mastiff Bat common 1, 2, 6

Molossus rufus Black Mastiff Bat uncommon 1, 2, 5

Molossus sinaloae Sinaloan Mastiff Bat common 1, 2, 6

Nyctinomops laticaudatus Broad-eared Bat uncertain 2

Promops centralis Big Crested Mastiff Bat rare 2, 6

Tadarida brasiliensis Brazilian Free-tailed Bat uncommon 1, 2, 6

Primates Primates

Atelidae Howler and Spider Monkeys

Alouatta palliata Mantled Howler Monkey common 1, 2, 3, 4, 5, 6

Ateles geoffroyi Black-handed Spider Monkey uncommon 2, 3, 4, 5, 6

Cebidae Capuchin Monkeys

Cebus capucinus 11 White-faced Capuchin common 1, 2, 3, 4, 5

9

Cingulata Armadillos

Dasypodidae Armadillos

Cabassous centralis Northern Naked-tailed Armadillo rare 2, 3, 4, 6

Dasypus novemcinctus Nine-banded Armadillo abundant 1, 2, 3, 4, 5, 6

Pilosa Anteaters and Sloths

Bradypodidae Three-toed Sloths

Bradypus variegatus Brown-throated Three-toed Sloth rare 1

Megalonychidae Two-toed Sloths

Choloepus hoffmanni Hoffmann’s Two-toed Sloth common 1, 2, 3, 4, 5, 6

Cylopedidae Silky Anteater

Cyclopes didactylus Silky Anteater uncertain 2, 6

Myrmecophagidae Anteaters

Myrmecophaga tridactyla Giant Anteater originally here, but 1 now extirpated

Tamandua mexicana Northern Tamandua uncommon 1, 2, 3, 5, 6

Lagomorpha Rabbits

Leporidae Rabbits and Hares

Sylvilagus floridanus Cottontail Rabbit uncommon 1, 2, 3

Sylvilagus gabbi 12 Forest Rabbit rare 2, 3

Rodentia Rodents

Geomyidae Pocket Gophers

Orthogeomys cherriei Cherrie’s Pocket Gopher common 2, 3, 6

Sciuridae Squirrels

10

Microsciurus alfari Alfaro’s Pygmy Squirrel common 2, 3, 4, 5, 6

Sciurus granatensis Neotropical Red Squirrel common 1, 2, 3, 4, 5, 6

Sciurus variegatoides Variegated Squirrel abundant 1, 2, 3, 6

Heteromyidae Pocket Mice

Heteromys desmarestianus Desmarest’s Spiny Pocket Mouse common 5, 6

Heteromys nubicolens 13 Cloud-dwelling Spiny Pocket Mouse common 1, 2, 3, 4

Cricetidae Long-tailed Rats and Mice

Handleyomys alfaroi Alfaro’s Rice Rat uncommon 2, 3, 5

Melanomys chrysomelas 14 Dusky Rice Rat uncommon 5, 6

Nephelomys devius 15 Tome’s Rice Rat common 2, 3, 4, 5

Nyctomys sumichrasti Sumichrast’s Vesper Rat uncommon 1, 2, 3, 5, 6

Oligoryzomys fulvescens Pygmy Rice Mouse rare 2, 3, 5

Oligoryzomys vegetus Pygmy Rice Mouse rare 2, 3, 4

Ototylomys phyllotis Big-eared Climbing Rat rare 1, 2

Peromyscus nudipes 16 Naked-footed Mouse abundant 1, 2, 3, 4, 5

Reithrodontomys brevirostris Chiriquí Harvest Mouse common 1, 2, 3, 4, 5, 6

Reithrodontomys creper Chiriquí Harvest Mouse uncommon 4

Reithrodontomys sp.17 Harvest Mouse rare 4

Rheomys raptor Goldman’s Water Mouse rare 3, 4, 5

Scotinomys teguina Alston’s Brown Mouse common 2, 3, 4, 5, 6

Sigmodon hirsutus Southern Cotton Rat common 1, 2

Transandinomys bolivaris 18 Long-whiskered Rice Rat rare 6

Tanyuromys aphrastus 19 Long-tailed Montane Rat rare 4, 5

Tylomys watsoni Watson’s Climbing Rat common 2, 3, 4, 5, 6

11

Erethizontidae Porcupines

Coendou mexicanus Prehensile-tailed Porcupine common 1, 2, 3, 4, 5, 6

Cuniculidae Pacas

Cuniculus paca Paca uncommon 1, 2, 3, 4, 5, 6

Dasyproctidae Agoutis

Dasyprocta punctata Agouti common 1, 2, 3, 4, 5, 6

Carnivora Carnivores

Canidae Coyotes, Foxes, and Dogs

Canis latrans Coyote uncommon 1, 2

Urocyon cinereoargenteus Gray Fox common 1, 2, 3, 5

Mephitidae Skunks

Conepatus semistriatus Striped Hog-nosed Skunk uncommon 1, 2, 3, 4, 6

Spilogale angustifrons Southern Spotted Skunk rare 2

Mustelidae Weasels and Otters

Eira barbara Tayra common 1, 2, 3, 4, 5

Galictis vittata Grison rare 2, 3, 5, 6

Lontra longicaudis Southern River Otter rare 1, 2, 3, 4, 5, 6

Mustela frenata Long-tailed Weasel uncommon 1, 2, 3, 4, 5, 6

Procyonidae Raccoons and allies

Bassaricyon gabbii Olingo common 1, 2, 3, 5, 6

Bassariscus sumichrasti Central American Cacomistle uncertain 3

Nasua narica White-nosed Coati abundant 1, 2, 3, 4, 5, 6

Potos flavus Kinkajou common 1, 2, 3, 4, 5, 6

Procyon lotor Raccoon common 1, 2, 3, 5, 6

12

Felidae Cats

Leopardus pardalis Ocelot uncommon 1, 2, 3, 4, 5, 6

Leopardus tigrinus Little Spotted Cat uncertain 1, 3, 4, 6

Leopardus wiedii Margay uncommon 2, 3, 4, 5, 6

Panthera onca Jaguar rare 3, 4, 5, 6

Puma concolor Puma, Mountain Lion, Cougar uncommon 1, 2, 3, 4, 5, 6

Puma yagouaroundi Jaguarundi uncommon 1, 2, 3, 4, 5, 6

Artiodactyla Deer and Peccaries

Tayassuidae Peccaries

Tayassu pecari White-lipped Peccary originally widespread, but now extirpated

Pecari tajacu Collared Peccary common 2, 3, 4, 5, 6

Cervidae Deer

Mazama temama 20 Central American Brocket Deer uncommon 1, 2, 3, 4, 5, 6

Odocoileus virginianus White-tailed Deer uncommon 1, 2

Perissodactyla Tapirs and Horses

Tapiridae Tapirs

Tapirus bairdii Baird’s Tapir uncommon 3, 4, 5, 6

Species introduced into the area by humans

Mus musculus House Mouse common 1, 2, 6

Rattus rattus Black, Roof Rat uncommon 1, 2, 6

1 Abundance categories: abundant = often observed and/or captured in appropriate habitats; common = frequently observed in appropriate habitats; uncommon = only occasionally observed in appropriate habitats; rare = very few records for Monteverde; extirpated = previously known from the area, but no longer in the region due to overhunting and habitat destruction; uncertain = of unknown abundance. 13

2 Life Zone: These correspond to the 6 Holdridge life zones in Monteverde area. Brief descriptions and elevational ranges of each zone are found in Table 1 below. 3 A species new to science described by N. Woodman and R. M. Timm. 4 Name recently changed from P. parnellii. 5 Name recently changed from C. brevicauda. 6 Name recently changed from S. lilium. 7 Name recently changed from S. ludovici. 8 Recently recorded from Costa Rica for the first time. 9 Name recently changed from M. keaysi. 10 This genus is currently being revised and the authors state that this is probably an undescribed species. For now we provisionally use the name R. io to provide consistency with the published literature. 11 Some anthropologist suggest the name for the Central American capuchins should be C. imitator. 12 Name recently changed from S. brasiliensis. 13 A species recently described from Monteverde by Anderson and Timm (2006). 14 The correct name for the species of Melanomys at Monteverde may be M. chrysomelas. It is likely that at least two species of Melanomys occur in Costa Rica. 15 Name recently changed from Oryzomys albigularis. 16 Bradley et al. (2016) suggested that the Peromyscus at Monteverde should be considered as conspecific with those of Nicaragua and as such P. nicaraguae. Reed treats all Peromyscus in Costa Rica, Nicaragua, and adjacent countries as belonging to the widespread species P. mexicanus. We suspect that eventually two or perhaps three species of Peromyscus will ultimately be recognized in Costa Rica and continue to treat the species at Monteverde as P. nudipes until the systematic relationships among these species are better understood. 17 A new species being described by R. M. Timm and M Soley. 18 Name recently changed from Oryzomys bolivaris. 19 Name recently changed from Oryzomys aphrastus. 20 Name recently changed from Mazama americana.

Table 2. Characteristics of the Holdridge life zones in the Monteverde area and Life Zone code numbers associated with mammal distributions. Life zones are arranged in sequence along a transect across the mountains from the Pacific to the Atlantic slope.

Elevation Annual Dry Season Canopy Life Life Zone (m) Rainfall Duration Height Zone (range in mm) (months) (m) ______Premontane Moist Forest 700–1300 2000–2500 5.5 ca. 25 1

Premontane Wet Forest 1300–1500 2500–3500 5 30–40 2

Lower Montane Wet Forest 1500–1650 3000–5000 3 25–35 3

Lower Montane Rain Forest 1650–1850 5000–8000 2 20–30 4

Premontane Rain Forest 700–1600 4000–7000 1 30–40 5

Tropical Wet Forest 500–700 3500–4500 1 30–50 6

Modified from Haber (2000).

14

sucking louse from a Central References American swimming mouse. Anderson, R. P. and R. M. Timm. 2006. A Journal of Parasitology new montane species of spiny 87:1409–1413. [pdf: pocket mouse (Rodentia: https://kuscholarworks.ku.edu/h Heteromyidae: Heteromys) from andle/1808/4494] northwestern Costa Rica. Gardner, A. L., and M. D. Carleton. 2009. American Museum Novitates A new species of 3509:1–38. [pdf: Reithrodontomys, subgenus http://hdl.handle.net/1808/4468] Aporodon (Cricetidae: Andrews, B. M., and F. A. Chinchilla. Neotominae), from the 2015. First capture of Cyttarops highlands of Costa Rica, with alecto in the Costa Rican cloud comments on Costa Rican and forest. Letters to the Editor, Bat Panamanian Reithrodontomys. Research News 56:19–20. In Systematic mammalogy: Baird, A. B., J. K. Braun, M. A. Mares, J. contributions in honor of Guy C. Morales, J. C. Patton, C. Q. G. Musser, Voss, R. S. and M. Tran, and J. W. Bickham. 2015. D. Carleton (eds.). Bulletin of Molecular systematic revision of the American Museum of tree bats (Lasiurini): doubling Natural History 331:157–181. the native mammals of the Haber, W. A. 2000. Plants and vegetation. Hawaiian Islands. Journal of In Monteverde: Ecology and Mammalogy 96(6):1255–1274. conservation of a tropical cloud Bradley, R. D., M. Nuñez-Tabares, T. J. forest, Nadkarni, N. M. and N. Soniat, S. Kerr, R. W. T. Wheelwright (eds.). Oxford Raymond, and N. Ordóñez- University Press, New York, pp. Garza. 2016. Molecular 39–94. systematics and phylogeny of Holdridge, L. R. 1967. Life Zone Ecology. Peromyscus nudipes Revised edition. Tropical (Cricetidae: Neotominae). Pp. Science Center, San José, Costa 201–213, In Contributions in Rica. natural history: A memorial LaVal, R. K. 2004. Impact of global volume in honor of Clyde Jones. warming and locally changing Manning, R. W., J. R. Goetze, climate on tropical cloud forest and F. D. Yancey, II (eds.). bats. Journal of Mammalogy Special Publications of the 85:237–244. Museum, Texas Tech LaVal, R. K., R. O. Lawton, and R. M. University, 65:1–273. Timm. (in press). The effect of Chinchilla, F. A. 2009. Seed predation by environmental variables on mammals in forest fragments in nightly activity patterns of Monteverde, Costa Rica. insectivorous bats monitored Revista de Biología Tropical over ten years in a tropical 57:865–877. premontane forest, Costa Rica. Durden, L. A. and R. M. Timm. 2001. KU ScholarWorks. Hoplopleura janzeni n. sp. LaVal, R. K. and B. Rodríguez-H. 2002. (Phthiraptera: Anoplura), a new Murciélagos de Costa Rica/Bats. 15

Editorial INBio, San José, Costa Journal of Wildlife Diseases Rica, 320 pp. 49:1014–1018. LaVal, R. K. and R. M. Timm. 2014. Muchhala, N. 2003. Exploring the Mamíferos de Monteverde— boundary between pollination 2014. Apéndice 11, In syndromes: Bats and Monteverde: Ecología y hummingbirds as pollinators of conservación de un Burmeistera cyclostigmata and bosquenuboso tropical, B. tenuiflora (Campanulaceae). Wheelwright, N. T., and N. M. Oecologia 134:373–380. Nadkarni (eds.). Bowdoin Pine, R. H., R. M. Timm, and M. Weksler. Scholars’ Bookshelf Book 3. 2012. A newly recognized [http://digitalcommons.bowdoin clade of trans-Andean .edu/scholars-bookshelf/3] Oryzomyini (Rodentia: McCain, C. M. 2004. The mid-domain Cricetidae), with description of effect applied to elevational a new genus. Journal of gradients: species richness of Mammalogy 93:851–870. [pdf: small mammals in Costa Rica. http://hdl.handle.net/1808/9974] Journal of Biogeography 31:19– Reid, F. A. 2009. A field guide to the 31. mammals of Central America & McCain, C. M. 2006. Do elevational range Southeast Mexico. 2nd Edition. size, abundance, and body size Oxford University Press, New patterns mirror those York, 334 pp. documented for geographic Rodríguez-Herrera, B., R. Medellín, and R. ranges? A case study using M. Timm. 2007. Murciélagos Costa Rican rodents. Neotropicales que acampan en Evolutionary Ecology Research hojas: Neotropical tent-roosting 8:435–454. Bats. Instituto Nacional de McCain, C. M., R. M. Timm, and M. Biodiversidad (INBio), Santo Weksler. 2007. Redescription Domingo de Heredia, Costa of the enigmatic long-tailed rat Rica, 178 pp. Sigmodontomys aphrastus http://hdl.handle.net/1808/13705 (Cricetidae: Sigmodontinae) Rodríguez-Herrera, B., J. D. Ramírez- with comments on taxonomy Fernández, D. Villalobos- and natural history. Proceedings Chaves, and R. Sánchez. 2014. of the Biological Society of Actualización de la lista de Washington 120:117–136. [pdf: especies de mamíferos vivientes https://kuscholarworks.ku.edu/h de Costa Rica. Mastozoología andle/1808/4462] Neotropical 21:275–289. Mehrkens, L. R., L. A. Shender, M. J. Romero, A. and R. M. Timm. 2013. Yabsley, B. C. Shock, F. A. Reproductive strategies and Chinchilla, J. Suarez, and K. V. natural history of the arboreal, K. Gilardi. 2013. White-nosed Neotropical vesper mouse, coatis (Nasua narica) are a Nyctomys sumichrasti. potential reservoir of Mammalia 77(4):363–370. Trypanosoma cruzi and other [http://hdl.handle.net/1808/1244 potentially zoonotic pathogens 1] in Monteverde, Costa Rica. 16

Rossi, R. V., R. S. Voss, and D. P. Lunde. Costa Rica) 52:1–32. [pdf: 2010. A revision of the http://hdl.handle.net/1808/4521] didelphid marsupial genus Timm, R. M., R. H. Pine, and J. D. Hanson. Marmosa. Part 1, The species in in press. A new species of Tate’s ‘mexicana’ and ‘mitis’ Tanyuromys Pine, Timm, and sections and other closely Weksler (Rodentia: Cricetidae: related forms. Bulletin of the Oryzomyini) from Ecuador, American Museum of Natural with comments on relationships History 334:1–83. within the Oryzomyini. Journal Timm, R. M. and R. K. LaVal. 2000a. of Mammalogy. Mammals. In Monteverde: Timm, R. M. and C. Vriesendorp. 2003. Ecology and conservation of a Observations on feeding tropical cloud forest, Nadkarni, behavior in the vesper mouse, N. M. and N. T. Wheelwright Nyctomys sumichrasti. (eds.). Oxford University Press, Zeitschrift für Säugetierkunde New York, pp. 223–244. 68:126–128. [pdf: Timm, R. M. and R. K. LaVal. 2000b. http://hdl.handle.net/1808/4482] Observations on Monteverde’s Wenny, D. G. 1999. Two-stage dispersal of mammals. In Monteverde: Guarea glabra and G. kunthiana Ecology and conservation of a (Meliaceae) in Monteverde, tropical cloud forest, Nadkarni, Costa Rica. Journal of Tropical N. M. and N. T. Wheelwright Ecology 15:481–496. (eds.). Oxford University Press, Villalobos-Chaves, D. and C. W. Dick. New York, pp. 235–236. 2014. Rediscovery of the rare Timm, R. M. and R. K. LaVal. 2000c. Tacarcunan bat Lasiurus Appendix 10. Mammals of castaneus (Chiroptera: Monteverde. In Monteverde: Vespertilionidae) in Costa Rica. Ecology and conservation of a Ecotropica 20:83–86. tropical cloud forest, Nadkarni, Villalobos-Chaves, D., J. D. Ramírez- N. M. and N. T. Wheelwright Fernádez, E. Chacón-Madrigal, (eds.). Oxford University Press, W. Pineda-Lizano, and B. New York, pp. 553–560. Rodríguez-Herrera. 2016. Timm, R. M. and R. K LaVal. 2014. Clave para la identification de Mamíferos de Monteverde— los roedores de Costa Rica. 2014: Apéndice 10, Pp. 843– Escuela de Biología, 852, In Monteverde: Ecología y Universidad de Costa Rica, conservación de un bosque Ciudad Universiaria Rodrigo nuboso tropical, Wheelwright, Facio, Costa Rica. N. T. and N. M. Nadkarni (eds.). Wainwright, M. 2002. The natural history Bowdoin Scholars’ Bookshelf. of Costa Rican mammals. Zona Book 3. Tropical, S.A., 383 pp. http://hdl.handle.net/1808/20667 Woodman, N. and R. M. Timm. 2017. A Timm, R. M., R. K. LaVal, and B. new species of small-eared Rodríguez-Herrera. 1999 shrew in the Cryptotis thomasi [2000]. Clave de campo para species group from Costa Rica los murciélagos de Costa Rica. (Eulipotyphla: Soricidae). Brenesia (Museo Nacional de Mammal Research, 62:89–101. 17

http://hdl.handle.net/1808/23211

January 2018

Robert M. Timm Richard K. LaVal University of Kansas The Bat Jungle Lawrence, Kansas USA Monteverde, Costa Rica

8 Plant-Animal Interactions — Update 2014

K. Greg Murray & Judith L. Bronstein

Plant-pollinator Interactions pollination syndromes. He found that both birds The suites of morphological, phenological, and bats visited flowers of both plant species, and behavioral characteristics of plants and but that only bats effectively pollinated both. pollinators that comprise “pollination Hummingbirds effectively pollinated B. syndromes” remain useful for predicting the tenuiflora, but because the reproductive parts of players in pollination mutualisms. For example, B. cyclostigmata extend further from the red tubular flowers are likely to be visited by nectaries, birds can access nectar without hummingbirds, and short-tongued bees are more contacting the anthers and stigma. This work likely to visit flowers with a more open nicely demonstrates the need for caution in morphology that doesn’t restrict their access to assuming too much about the identity of nectar and pollen. However, the frequent pollinators merely on the basis of floral finding that floral visitors aren’t restricted just to morphology and timing of nectar secretion. those usually associated with a particular Muchhala suggests that these species of syndrome has increasingly led to criticism of the Burmeistera demonstrate generalization for utility of the syndrome idea itself (e.g., Ollerton pollination by both bats and hummingbirds. 2009, but see Rosas-Guerrero 2014), as has the Work at Monteverde since 2000 has added realization that many animals feed at flowers detailed information on the basic reproductive usually associated with different types of biology of local plants as well. {Cascante- pollinators. {Muchhala, 2003, Exploring the Marin, 2005, Reproductive biology of the boundary between pollination syndromes: bats epiphytic brorneliad Werauhia gladioliflora in a and hummingbirds as pollinators of Burmeistera premontane tropical forest}, for example, cyclostigmata and B-tenuiflora studied the flowering phenology and breeding (Campanulaceae)} work with Burmeistera system of the bat-pollinated bromeliad Werauhia tenuiflora and B. cyclostigmata at Monteverde (formerly Vriesia) gladiolifolia, and {Bush, demonstrates some of the ambiguity of 2009, Early autonomous selfing in the

hummingbird-pollinated epiphyte Pitcairnia rates and appear to be more pollen-limited than brittoniana (Bromeliaceae)} elucidated the those at lower elevations (e.g., San Luis) or breeding system of the hummingbird-pollinated those further south in Costa Rica (i.e., Las bromeliad Pitcairnia brittoniana. Both species Cruces and Las Alturas; {Stone, 2008, Pollinator were capable of self-pollination, and both fruit- abundance and pollen limitation of a and seed set were equivalent in plants limited to solanaceous shrub at premontane and lower self-pollination as in those available to montane sites}. However, when {Stone, 2014, pollinators. Self-pollination is common among Transmission advantage favors selfing allele in epiphytes, which may suffer unpredictable experimental populations of self-incompatible visitation due to their isolation and limited floral Witheringia solanacea (Solanaceae)} created displays {Bush, 1995, Breeding systems of experimental gardens with both genotypes and epiphytes in a tropical montane wet forest}, but allowed them to be pollinated naturally, SC and Bush and Guilbeau found that pollen loads SI plants had roughly equivalent fruit- and seed deposited by hummingbirds were also sufficient set but less than 10% of SC seeds resulted from to ensure nearly full seed set in P. brittoniana. self-fertilization. They concluded that embryonic As they noted for P. brittoniana, it seems likely inbreeding depression was still substantial in SC that many epiphytes cross-pollinate when plants, but suggested that these genotypes will pollinators are available, but self-pollinate when continue to spread because the transmission they are scarce. advantage of selfing through male function Another contribution from Monteverde is effectively outweighs even severe inbreeding Judy Stone’s work with colleagues on depression. pollination ecology and breeding system evolution in Witheringia solanacea. Self- Plant-Frugivore Interactions compatibility has evolved independently many Much of the work on plant-frugivore times, but the conditions that favor it remain interactions in Monteverde since the book’s somewhat controversial because theory predicts publication has focused on the post-dispersal that they must outweigh the costs of self- fates of seeds. To a large degree this emphasis fertilization (primarily lowered fitness via the mirrors that in the field of plant-frugivore production of offspring with two copies of interactions in general. It is motivated by the deleterious alleles). Most investigations of the understanding that the evolutionary evolution of self-compatibility rely on consequences of seed dispersal for plants comparisons of different but closely related (including coevolution with frugivores) are species, but {Stone, 2006, Variation in the self- mediated by the effects of dispersal on seed fate incompatibility response within and among and plant demography. Some of Wenny’s work populations of the tropical shrub Witheringia on dispersal of large-seeded species also deals solanacea (Solanaceae)} found populations of explicitly with dispersal per se, however. W. solanacea with both self-incompatible (SI) Wenny (1999) showed that seeds of and self-compatible (SC) genotypes at Beilschmiedia pendula, one of the largest seeds Monteverde and Varablanca. SI genotypes of dispersed by birds at Monteverde, are rarely W. solanacea suffered nearly complete deposited more than 10 m beyond the crowns of embryonic lethality when experimentally self- fruiting trees, but that seeds dispersed even short pollinated ({Stone, 2010, Embryonic inbreeding distances from the parent suffer less predation depression varies among populations and by (from rodents and beetle larvae) than those mating system in Witheringia solanacea deposited directly beneath the crown. His work (Solanaceae)}, but SC genotypes did not, and demonstrates that dispersal is indeed beneficial Stone et al. concluded that deleterious alleles for B. pendula, and that the effect occurs on had already been largely purged from the SC quite a small spatial scale. In contrast, seeds of genotypes. Such purging is most likely to occur Ocotea endresiana suffered nearly complete when plants are severely pollen-limited, and W. removal by predators regardless of dispersal solanacea populations near the MCFP did distance from the parent tree {Wenny, 2000, indeed have lower pollinator (bee) visitation Seed dispersal of a high quality fruit by

specialized frugivores: High quality dispersal?}. Although secondary dispersers increased median Most birds moved seeds less than 25 m, but distances only slightly, they did have a profound male Three-wattled Bellbirds (Procnias effect on seed fate by burying seeds 1-3 cm deep tricarunculata) often deposited them beneath in the soil. Buried seeds were far more likely to courtship display perches, many of which survive than those that remained on the soil overhang treefall gaps. Wenny’s experiments surface, which were killed mostly by rodents failed to show any difference in gap vs. and insects (G. glabra) or by Collared Peccaries understory seed removal rates, but seedlings in (G. kunthiana). Wenny’s work on seed fate at gaps grew more rapidly and suffered less Monteverde also included comparisons among mortality from pathogenic fungi than did those ten additional species with different seed sizes, in understory. Thus, male Bellbirds provide a and although highly variable within size good example of directed dispersal (sensu Howe categories, seed survival tended to be higher for and Smallwood 1982), and may be the largest seeds. Because these seeds continued disproportionately important for recruitment of to suffer rodent attack after germination, O. endresiana. Determining the strength of the however, the relationship between seed size and effect relative to that of other dispersers will seedling recruitment was complex. {Wenny, require more detailed study, however. 2005, Post-dispersal seed fate of some cloud Another example of directed dispersal at forest tree species in Costa Rica} estimated that Monteverde is provided by {Sheldon, 2013, five species of small rodents were responsible Spatial and Temporal Variation of Seed Rain in for about 70% of seed predation. Insect the Canopy and on the Ground of a Tropical infestation was also common in some species, Cloud Forest} study, which compared the “seed but mostly occurred before dispersal. Secondary rain” deposited on the forest floor with that movement of seeds (by rodents) for short deposited in the forest canopy in part of the distances was common, but only Guarea was MCFP. Their study employed seed traps, with commonly cached and often buried; most seed those in the canopy estimating seeds that are movement thus resulted in predation. deposited and that accumulate in epiphyte mats Given the importance of mammalian seed and the soil associated with them. Despite broad predators as mediators of plant population overlap, the species composition of the seed rain dynamics, how forest fragmentation and was statistically distinct in each habitat: epiphyte distributional changes driven by climate change seeds dominated in the canopy, while those of will affect mammal populations is of great large trees were most common on the forest importance in montane habitats like those in floor, suggesting that dispersers do move Monteverde {Gibson, 2013, Near-Complete epiphyte seeds to especially appropriate Extinction of Native Small Mammal Fauna 25 establishment sites more often than would be Years After Forest Fragmentation;Meserve, expected by chance. Seeds dispersed by birds 2011, Global climate change and small mammal (rather than by mammals or wind) dominated in populations in north-central Chile;Sheldon, both habitats and over all seasons, highlighting 2011, Climate change and community the importance of animal dispersers – especially disassembly: impacts of warming on tropical birds – in maintaining the ecological integrity of and temperate montane community structure}. the Monteverde forest. {Chinchilla, 2009, Seed predation by mammals {Wenny, 1999, Two-stage dispersal of in forest fragments in Monteverde`, Costa Rica} Guarea glabra and G-kunthiana (Meliaceae) in compared mammalian seed predator populations Monteverde`, Costa Rica} studied the effects of and seed removal rates in a large tract of primary (by birds and non-flying mammals) and continuous forest (including the MCFR) and in secondary (by scatter hoarding rodents, e.g., two nearby forest fragments of 350 and 20 ha. agoutis) dispersal on survival and germination in As expected, the fragments were missing some two species of Guarea. Seeds were moved up to of the larger species of seed predators (e.g., 65 m beyond parent tree crowns by primary peccaries and pacas), but experienced seed dispersers, but median distances were within 15 removal rates that were only marginally lower m for both G. glabra and G. kunthiana. than those in intact forest. Chinchilla attributed

much of the compensatory predation in the experiments were consistent with the fragments to the higher abundance of the comparisons between seed bank and annual seed specialist seed predator Heteromys rain densities outlined above: seeds of the same desmarestianus there, compared to intact forest, species with high seed bank : annual seed rain where it was uncommon. ratios also survived well in the field since 1993 Murray and Garcia-C. (2002) reported on a (Murray and Garcia-C 2002). {Veldman, 2007, long-term study of the roles played by seed Chemical defense and the persistence of pioneer dispersal and seed survival in facilitating plant seeds in the soil of a tropical cloud forest} coexistence of a large guild of pioneer plant investigated the chemical basis for the patterns species that depend upon a limited resource: of mortality among six of the pioneer species in space in recently formed treefall gaps. They Murray and Garcia-C’s (2002) study (P. found that the top 10 cm of Monteverde soils rivinoides, C. polyphlebia, G. poasana, U. elata, contains 3000 to 6500 viable but dormant B. frutescens, and Witheringia meiantha), and pioneer seeds per square meter - seeds that found that seed extracts from species that germinate rapidly in response to gap formation. survive for long periods in the soil were indeed And because species richness is high even on more toxic to arthropods and fungi in the very small spatial scales (ca. 20-25 species per laboratory. The responsible chemicals in B. 625 cm2 sample), both intra- and interspecific frutescens were identified as three related competition for space in recent treefall gaps is alkaloids, all of which were much more intense. Murray and Garcia-C’s work showed concentrated in seeds than in leaf tissue. P. that spatial heterogeneity of the soil “seed bank” rivinoides and G. poasana contain chemicals was extremely high, however, so that toxic to fungi as well, but they remain as yet competitively inferior pioneer species were unidentified (Veldman et al. 2007, K. G. likely sometimes to germinate in gaps without Murray, unpublished data). Chemical defense any superior competitors nearby. This of pioneer plant seeds is thus clearly important, phenomenon, termed “recruitment limitation,” and much work remains to be done. can facilitate coexistence by reducing the {Nadkarni, 2009, Canopy Seed Banks as intensity of competition on ecologically relevant Time Capsules of Biodiversity in Pasture- spatial scales. Part of the spatial patchiness in Remnant Tree Crowns} found that the soils and the seed bank resulted from patchiness in the epiphyte mats that accumulate in tree canopies seed rain, but site-to-site differences in density also accumulate seed banks, just as do soils on and species composition were also magnified by the forest floor. Moreover, they surveyed such survival probabilities in the soil that varied by seed banks in the canopies of remnant pasture species. trees to determine whether such seed banks Despite the fact that the life histories of most might augment other effects that render remnant pioneers include a soil seed bank, Murray and trees effective “regeneration foci.” They found Garcia-C. found a wide range in the ability of that these seed banks contained dense and seeds to survive for long periods in the soil. diverse assemblages of seeds, including many Some, like Phytolacca rivinoides, Bocconia woody species characteristic of primary forest, frutescens, and Guettarda poasana, maintain and concluded that pasture canopy seed banks soil seed banks with densities several orders of could function as “time capsules” of forest magnitude higher than the annual seed rain, biodiversity that could speed forest regeneration suggesting that seeds survive in Monteverde’s recovery on pastures. Nadkarni and Haber also soil for tens to hundreds of years. In contrast, compared the seed banks in remnant tree other species of pioneers, like Cecropia canopies with those in primary forest tree polyphlebia and Urera elata, maintain soil seed canopies and in soils from the forest floor. Seed banks with only a year’s worth of seed rain, densities and species richness in forest floor suggesting high mortality rates. Only Hampea soils, but those from pasture and primary forest appendiculata and Piper umbellatum among the tree canopies did not differ from one another 23 species studied in detail did not maintain a Earlier work on plant-frugivore interactions seed bank at all. Results of replicated field at Monteverde demonstrated that some of the

most important fruit-eating birds migrated of the Tilaran Mountains`, Costa Rica} studied altitudinally, and suggested that these the occurrence of Bare-necked Umbrella birds at movements were driven by seasonal patterns in different elevations in the Monteverde-Arenal- fruit availability at different elevations. Since San Ramon region of the Cordillera de Tilaran, the publication of Nadkarni and Wheelwright and found that their movements over an (2000), these patterns have been further elevation range from 400-1400 m correlated to investigated by Chaves-Campos et al. (2003), seasonal patterns in fruit availability. And as Chaves-Campos (2004), Powell and Bjork with Bellbirds, elevations used for breeding (2004), and Papes et al. (2012). {Powell, 2004, were fairly well-protected, while those used Habitat linkages and the conservation of tropical outside the breeding season were not. Like Biodiversity as indicated by seasonal migrations {Powell, 2004, Habitat linkages and the of three-wattled bellbirds} elucidated the conservation of tropical Biodiversity as migratory patterns of Three-wattled Bellbirds in indicated by seasonal migrations of three- detail using radiotelemetry, and found that birds wattled bellbirds}, Chaves-Campos concluded breeding on the Atlantic slope of the Cordillera that the inadequacy of protected lands used de Tilaran crossed over to highly fragmented during the non-breeding season constituted a forest on the Pacific slope just 5-15 km away significant threat to the species in the region. after the breeding season. In September and {Chaves-Campos, 2004, Elevational October, they migrate to the lowlands of movements of large frugivorous birds and northeastern Costa Rica and southeastern temporal variation in abundance of fruits along Nicaragua, and in November and December they an elevational gradient} studied changes in the migrate to southwestern Costa Rica, where they abundances of large fruit-eating birds between remain until returning in March to the Atlantic 400 and 1400 meters elevation in the Cordillera slope near Monteverde to breed. Powell and de Tilaran in relation to the availability of fruits, Bjork suggested that the birds are following the and found mixed evidence that the migratory availability of their primary food sources (fruits movements of these birds are driven in large part in the family Lauraceae) as the fruiting seasons by fruit availability. Although small sample of species in different parts of the bellbird’s sizes and high variation among replicates made range wax and wane, rather than following an statistical comparisons difficult, Chaves-Campos invariant migratory route. Whatever the reason, suggested that migratory movements of these the four areas used over the annual cycle were birds were driven by fruit availability in the non- separated by as much as 280 km, and much of breeding season, but not during the breeding the land in three of the four areas (lowlands of season. northeastern and southwestern Costa Rica, and Most recently, {Papeş, 2012, - Vegetation middle elevations on the Pacific slope of Costa dynamics and avian seasonal migration: clues Rica near Monteverde) is highly fragmented and from remotely sensed vegetation indices and poorly protected. Powell and Bjork concluded ecological niche modelling} investigated the that the bellbird population (and hence the possibility of explaining bellbird movements on forests in which they perform important seed the basis of remote sensing data that could serve dispersal services) are thus vulnerable, despite as a proxy for forest canopy characteristics. adequate protection of the forests used during They generated ecological niche models based the breeding season. In part as a result of their on several remotely sensed vegetation indices work, the Costa Rican government and several that reflect seasonal changes in canopy structure private-sector organizations are cooperating to and productivity, but these did not explain create the Bellbird Biological Corridor, which seasonal bellbird movements in the Monteverde will protect a migratory corridor on the Pacific region reliably. Rather, these models suggested slope by promoting habitat restoration and that much of the Atlantic slope is suitable for protection, largely on privately held lands. breeding, but that factors other than vegetation Similarly, {Chaves-Campos, 2003, seasonality, e.g., lower rates of nest predation at Altitudinal movements and conservation of bare- middle elevations, may attract bellbirds to necked Umbrellabird Cephalopterus glabricollis middle elevations for breeding.

Animal-mediated seed dispersal and cattle pasture trees at Monteverde was demonstrated pasture regeneration directly by {Sheldon, 2013, The use of pasture Since Groom’s (2000) study of woody plant trees by birds in a tropical montane landscape in regeneration in abandoned pastures, much of the Monteverde`, Costa Rica}, who documented work on seed dispersal at Monteverde has over 900 visits by 52 species in 20 different concerned the role that such dispersal by animals families to just one common pasture tree species plays in pasture regeneration. Cattle production (Sapium glandulosum). They also found that the now occupies over 27% of rural land area in size of the tree, its degree of isolation from other Latin America ({Murgueitio, 2011, Native trees trees, and the size of its epiphyte load increased and shrubs for the productive rehabilitation of bird visitation. Surprisingly, Murray et al. (2008) tropical cattle ranching lands}, yet the ultimate found that wind-dispersed remnant trees were fate of most pasture lands is abandonment or just as effective as recruitment foci for animal- conversion to some other use, often via dispersed colonists as were trees that themselves regeneration to forest. Much of the work on produced fleshy fruits sought by animals, pasture regeneration concerns the physical and presumably because seed dispersers are also biological barriers that limit the rate and attracted to the elevated perch sites, cover, and constrain the trajectory of regeneration (e.g., perhaps insect food resources that such trees {Holl, 2000, Tropical Montane Forest provide. Restoration in Costa Rica: Overcoming Barriers Murray and colleagues also tracked the to Dispersal and Establishment}, and since progress of regeneration to determine how the limited seed availability is one of the more spatial and compositional patterns of regrowth obvious factors, many have concentratd on the that were initiated by seed dispersers changed roles that seed dispersing animals play in over time. As has been found elsewhere (e.g., transporting seeds from surrounding forest into {Schlawin, 2008, 'Nucleating’ succession in pastures. recovering neotropical wet forests: The legacy {Murray, 2008, The roles of disperser of remnant trees}, the concentration of pasture behavior and physical habitat structure in colonists beneath remnant trees formed regeneration of post-agricultural fields} reported “recruitment foci” or “nucleation sites” for on a long-term study of regeneration in two forest plant species. Subsequent censuses of the pastures near the MCFP, and found that nearly same and similar plots 14 and 30 years post- all early colonization by woody plants with abandonment showed that the initial strong animal-dispersed seeds was beneath the crowns effect of remnant trees on the density and of bordering trees and “forest remnant” trees that species richness of regeneration became weaker were left standing in the pasture when it was over time – by 30 years post-abandonment, both created. In contrast, wind-dispersed species density and species richness of pasture colonists colonized areas without overhanging vegetation was just as high in parts of the original pasture just as frequently as areas beneath remnant trees. that had lacked overhanging tree crowns as in Concentration of early colonists beneath areas beneath remnant trees. The reason, of remnant trees or planted “tree islands” has been course, was that as the pasture colonists grew found in many other studies as well (e.g., and formed expanding islands of regenerating {Sandor, 2014, Remnant Trees Affect Species forest centered on the original remnant trees, the Composition but Not Structure of Tropical colonists themselves served as perch sites for Second-Growth Forest} and references cited animals carrying seeds and the land area without therein; {Zahawi, 2006, Tropical forest overhanging tree crowns decreased to zero. restoration: Tree islands as recruitment foci in The work of {Harvey, 2000, degraded lands of Honduras} – a pattern that COLONIZATION OF AGRICULTURAL results in part from the attraction of forest birds WINDBREAKS BY FOREST TREES: to habitats with greater structural complexity EFFECTS OF CONNECTIVITY AND and in part to the tendency of birds to defecate REMNANT TREES;Harvey, 2000, and regurgitate seeds while perched rather than WINDBREAKS ENHANCE SEED in flight. The attraction of birds to isolated DISPERSAL INTO AGRICULTURAL

LANDSCAPES IN MONTEVERDE`, COSTA diverse assemblages of seeds, including many RICA} in planted windbreaks between active woody species characteristic of primary forest pastures in the Monteverde region also and concluded that pasture canopy seed banks demonstrates the importance of animal seed could function as “time capsules” of forest dispersers in forest regeneration in agricultural biodiversity that could speed forest regeneration landscapes. As was the case for remnant trees, on abandoned pastures. the seed rain of woody species beneath Clearly, both remnant trees and windbreaks windbreaks was orders of magnitude more dense facilitate forest regeneration in agricultural and far more diverse than in pasture just 5 landscapes at Monteverde and elsewhere, largely meters away (Harvey 2000a). Bird-dispersed because of the interaction of their physical species predominated, but pastures received structure with the behavior of dispersers – almost as many bat-dispersed seeds as especially birds. These patterns highlight both windbreaks, perhaps because bats defecate in the importance of maintaining healthy disperser flight as well as when perched. Harvey (2000b) populations as well as managing landscape also studied colonization of windbreaks and features such as pasture size and composition, so adjacent pastures by surveying seedlings of as to maintain the interactions that facilitate forest plants recruited into them, and in many forest regeneration. ways her findings parallel those of Harvey (2000a): forest plants readily recruited into Fig biology windbreaks, especially those forest plants Figs remain a subject of fascination to dispersed by birds. Moreover, both density and biologists, especially those who work in the diversity of colonists was significantly higher in tropics. Our understanding of figs’ complex windbreaks connected to adjacent forest patches interactions with other species has been than in those not so connected. reviewed most recently by Herre et al. 2008, but Neither Harvey (2000a,b), Murray et al. new information continues to accumulate at a (2008), nor Sheldon and Nadkarni (2013b) rapid pace. Yet, in spite of growing worldwide found any correlation between seed input, recruit interest in figs, no publications have appeared density or bird visitation with distance to the over the past fifteen years describing research nearest forest edge, perhaps because the pastures carried out at Monteverde. Ficus pertusa, which typical of the region are relatively small – rarely has attracted the great majority of attention in more than a few hundreds of meters across. Monteverde, has been studied a little more Neither did {Aide, 1996, Forest recovery in elsewhere in Costa Rica as well as in Mexico abandoned cattle pastures along an elevational and Brazil, mostly in the context of its flowering gradient in northeastern Puerto Rico}) in Puerto phenology and seed dispersal. Ficus yoponensis Rico, where pastures are also relatively small. remains a species of great interest to researchers In regions like Amazonia, however, where at Barro Colorado, Panama, where it is pastures can be kilometers across, distance consumed heavily by bats that act as highly effects may be common. {DaSilva, 1996, Plant effective seed dispersers (Heer et al. 2010). succession`, landscape management`, and the Ficus tuerckheimii, F. crassiuscula, and F. ecology of frugivorous birds in abandoned velutina remain little-studied from the Amazonian pastures}), for example, found that pollination and seed dispersal perspective. even tanagers that frequent the forest/pasture It is particularly unfortunate that F. boundary rarely travel more than 150 meters into tuerckheimii has not attracted more attention, pasture. because it offers one of the clearest exceptions Nadkarni and Haber (2009) elucidated to a major piece of conventional wisdom about another way in which remnant pasture trees may figs: that every one of the >750 fig species has a act as effective regeneration foci and thereby unique pollinator. As Ramirez (1970) first facilitate forest regeneration on abandoned showed and several unpublished undergraduate pastures: via the seed banks that accumulate in course projects in Monteverde have followed up soils and epiphyte mats in the canopies of on, F. tuerckheimii has two pollinators (not “no” remnant pasture trees. They found dense and as the original text of this chapter erroneously

states), often cohabiting a single fig appear regularly (e.g., Herre et al. 2008, Jandér inflorescence. They are easily distinguished by et al. 2012). color: Pegoscapus carlosi is black and P. mariae Work has accelerated in recent years yellow. New molecular data that allow fig wasps documenting seed dispersal and the dominant that appear identical to the human eye to be role fig fruits play in the diets of tropical discriminated have made it clear that F. vertebrates. A comprehensive review of fig tuerckheimii may not be that unusual in hosting consumers worldwide is now available multiple pollinators (Marussich and Machado (Shanahan et al. 2001), as is a detailed 2007). Conversely, certain pairs of fig species investigation of how fig fruit characteristics are now known to share a single pollinator (Moe have evolved in suites or “syndromes” et al. 2011). Overturning a related assumption - (Lomascolo et al. 2010). Intriguing geographical that figs and fig wasps must usually speciate differences within individual fig species together, given that there are hundreds of mostly continue to appear and still remain to be one-to-one interactions - reconstruction of explored. For example, new work finds F. evolutionary relationships using molecular data pertusa seeds to be abundant in bat droppings in reveals a much messier picture (Machado et al. Brazil (Teixiera et al. 2009), suggesting a 2005, Lopez-Vaamonde et al. 2009). However, primary role for bats as seed dispersers there. how speciation occurs and how associations This is consistent with observations from between particular pairs of fig and pollinator Panama, but distinctly different from species arise remain unresolved (Cook et al. Monteverde, where bats reject the red-ripe fruits. 2010). Ecologists increasingly identify figs as The most surprising change in our ecological keystone resources for fruit consumers. The understanding of the fig pollination mutualism is health of fig populations worldwide is, however, that developing fig wasps do not, as was threatened by habitat loss, habitat fragmentation, believed for over a century, consume fig seeds. and selective harvest for wood (e.g., Felton et al. Rather, before laying an egg, a female fig wasp 2013). Furthermore, invasive frugivores deplete deposits a secretion that transforms an ovule into fruits essential to the well-being of native a gall; her offspring feeds upon sterile tissue vertebrates, while at the same time failing to (Jousselin and Kjellberg 2001, Martinson et al. disperse fig seeds in a germinable condition 2013). This leads to the obvious question of why (Staddon et al. 2010). There is a pressing need to these wasps transfer pollen at all, given that their treat figs as key targets for tropical conservation. offspring don’t eat seeds! There is some They may also hold promising roles for forest evidence that in seedless figs, wasp larvae restoration. develop very poorly (Jousselin et al. 2003). These and earlier studies at Monteverde Thus, regardless of their diet, active pollination highlight both the complexity of the interactions by the mother does appear to increase the among mutualists and their role in the success of her offspring. Even though fig wasp maintenance of whole ecological communities. larvae don’t consume seeds, each one still As important, they demonstrate how important it develops within an ovule that would otherwise is to base conservation planning on sound produce a seed. It remains unresolved why fig knowledge about the natural history of the wasps don’t lay eggs in every ovule, which organisms involved. Going forward, we hope would appear to benefit fig wasps in the short that biologists will continue to be drawn to run but which could lead to the demise of fig Monteverde both for the opportunity to reproduction and the extinction of both partners understand the natural world better and to satisfy in the long run. New ideas for how this uneasy their own need to preserve a particularly worthy relationship can persist over evolutionary time corner of it.

Literature Cited

9 Ecosystem Ecology and Forest Dynamics — Update 2014

Kenneth Clark

The original chapter on the “Ecosystem of carbon and nutrient content between Ecology and Forest Dynamics” summarized terrestrial and epiphytic vegetation; d) the research on four areas of ecosystem ecology. processing of atmospheric deposition of nitrogen The authors: a) described forest structure, and other nutrients by epiphyte-laden canopies; composition, and dynamics of two primary and e) carbon, nutrient and enzymes in soils, and forest stands, a windward elfin woodland and a the impacts of deforestation on soil carbon and leeward cloud forest; b) reviewed research nutrients. I then suggest future research efforts that focused on ecological roles of directions that will help fill some of the gaps in canopy biota in forest nutrient cycles; c) ecosystem level information at Monteverde. compared ecosystem-level data collected at Monteverde to other tropical montane forests; A. Forest Structure and Biomass. Recent and d) identified areas where our knowledge is data on forest structure and biomass have been incomplete and further investigations were published since the original chapter (Nadkarni et warranted. Since its publication, our overall al. 2004, Hagel and Dohrenbusch 2011, Kohler understanding of ecosystem ecology in tropical et al. 2007). Forest census measurements made montane regions has benefitted greatly from at seven stands along a 2.5 km transect across global-scale syntheses (Bruijnzeel et al. 2010, the Atlantic (windward) and Pacific (leeward) Giambelluca and Gerold 2011, Dalling et al. slopes indicated maximum canopy heights 2015). Here, I summarize some of the recent ranged from 6 to 20 m, number of stems from research on; a) forest structure and biomass in 1160 to 3280 ha-1, and basal area from 33 to 99 Monteverde, including new mass estimates for m2 ha-1 (Hager and Dohrenbusch 2011). epiphytes and hemi-epiphytes; b) linkages Estimated aboveground biomass ranged from 84 between climate, hydrology and forest structure t ha-1 in the wettest, most wind-exposed site, to and functioning; c) more complete comparisons 431 t ha-1 in a lower elevation stand (assuming a

wood density of 0.56 g cm-3; Nadkarni et al. Unfortunately, few stands have been censused at 2000). In a 4-ha leeward cloud forest stand, regular and long enough intervals to estimate canopy height was 18-25 m and stem density tree and understory production, although gap was 2062 individuals ha-1, with large (>30 cm dynamics measurements in the windward cloud DBH), medium (10-30 cm DBH) and small (2- forest described in Nadkarni et al. (2000), and 10 cm DBH) stems totaling 159, 396, and 1507, tree turnover measurements in the intensively respectively (Nadkarni et al. 2000). Stand studied leeward cloud forest stand described in biomass was 490 t ha-1, with approx. 95% of this Nadkarni et al. (2000, 2004) come close. In the in stem and branch wood (Nadkarni et al. 2004). later stand, trees in a 4-ha plot have been Aboveground biomass in a secondary forest measured and tagged, and tree increments have dominated by Conostegia oerstediana was 152 t been measured, but results have not been ha-1 (Nadkarni et al. 2004). reported yet (G. Goldsmith, pers. comm.). Other Recent research efforts have also processes have not been measured at any study quantified epiphyte mass in a number of forests site with sufficient resolution to calculate a in Monteverde, with estimates from primary complete forest carbon budget. forests ranging between 16 and 39 t ha-1. One limitation to estimate net primary Nadkarni et al. (2004) reported an epiphyte mass production in tropical montane cloud forests is value of 33.1 t ha-1 for an intensively-studied that although canopy height and diameter at leeward cloud forest. Approximately 60% of the breast height (dbh; 1.37 meters) measurements epiphyte mass was dead organic matter (DOM; are relatively straightforward, allometric 20.7 t ha-1), and mass of epiphytic bryophytes, equations to calculate biomass, and with roots, stems and foliage was 4.1, 5.2, 2.1 and 0.7 repeated measurements, biomass increment, for t ha-1, respectively (Nadkarni et al. 2004). The cloud forest trees are rare in the literature. In sum of bryophytes and epiphyte foliage in the addition, unlike many tree species in temperate canopy represented 67 % of the sum of canopy forests, tree ages cannot be estimated reliably and understory foliage. Values of 26 and 32 t ha- from tree cores and counts of annual rings for 1 for epiphyte mass, and 6 and 7 t ha-1 for hemi- many tropical tree species. A potential alternate epiphytes and lianas were reported for two method for estimating stem production is to use stands at 1200 and 1450 m elevation, annual growth increments estimated from of respectively (Hager and Dohrenbusch 2011). δ18O isotope signals in tree stems. Seasonal DOM averaged 23.6% and 26.4% of epiphyte isotopic signals of δ18O occur in tree stems of mass in these two stands. Epiphyte mass in dominant species in Monteverde, and this has primary forest near San Gerardo was estimated allowed an estimate of seasonality of the sources to be 16.2 t ha-1 (Kohler et al. 2007), with of water used (Anchukaitis et al. 2008). This epiphytic bryophytes, vascular epiphytes, and technique could be extended to estimate annual DOM estimated at 11.5, 3.9 and 2.1 t ha-1, growth increments from tree cores. respectively. Epiphyte mass, primarily epiphytic bryophytes, was much lower in a secondary B. Linkage of forest structure and forest stand dominated by Conostegia ecosystem processes to abiotic factors. Recent oerstediana, totaling only 0.2 t ha-1 (Nadkarni et studies have further linked patterns of cloud, al. 2004). wind-driven precipitation and soil water content Many of the pools and fluxes needed to across the Monteverde area to forest structure, calculate productivity of terrestrial and epiphytic epiphyte abundance and plant water status, and vegetation have been measured at Monteverde. soil microbial biomass and functioning. Hager For example, litterfall and epiphyte litterfall and Dohrenbusch (2011) measured rainfall, (Nadkarni et al. 1992a,b, 1995), litter horizontal precipitation, throughfall, temperature decomposition (Gholz et al. 2000, Cusack et al. and soil moisture at seven forest stands along the 2009, Currie et al. 2010), production and same 2.5 km transect across the Atlantic slope decomposition of epiphytic bryophytes (Clark et and the Pacific slopes that they measured forest al. 1998a), and colonization of branches by structure. Patterns of forest structure and epiphytes (Nadkarni 2000, et al. 2002). biomass along their transect corresponded to the

strong hydrologic and topographic gradients, soil. Hietz et al. (2002) indicated that canopy and to differences in soil moisture conditions DOM is derived primarily from epiphytes, with across the continental divide in Monteverde. only minor inputs from host tree litter matter. Nadkarni and Solano (2002) used experimental They concluded that the epiphyte N cycle transplants of upper cloud forest epiphyte mats appears to be largely detached from the tree-soil to tree canopies at slightly lower elevations that cycle. However, Matson et al. (2014) reported experience longer dry season conditions, that rates of N cycling in canopy DOM were demonstrating the importance of cloud and sensitive to slight changes in forest floor nutrient wind-driven precipitation to vascular epiphytes availability in an Andean tropical montane during the dry season. Similarly, Heitz et al. forest, indicating a greater coupling between (2002) reported that epiphytes on small branches epiphytic and terrestrial N cycling. Their results also had less negative δ13C values, indicating indicated that canopy DOM was a significant N more frequent water stress occurred, compared source for epiphytes, and N mineralized in to vascular epiphytes rooted in canopy DOM or canopy DOM contributed up to 23% of total terrestrial vegetation. Variability in microbial (canopy + forest floor) mineral N production in biomass, fungal and bacterial abundance and tropical montane forests. Cardelús and Mack diversity, and the abundance of key functional (2010) reported comparisons of epiphytic genes for lignin degradation and bacterial N- vegetation along an elevational transect on fixation, as well as soil nitrogen fixation activity, Volcan Barva. They reported that epiphytes have been linked to patterns of soil moisture in rooted in canopy DOM had higher N forest stands along the Caribbean and Pacific concentrations than “atmospheric” epiphytes, slopes of Monteverde (Eaton et al. 2012). while P content did not vary among groups. They also reported higher variability in foliar C. Comparisons of nutrient content of δ15N values, with no differences between terrestrial and epiphytic vegetation. More epiphytes rooted in canopy DOM and complete nutrient analyses of terrestrial and atmospheric epiphytes. Their data indicated epiphytic vegetation have been reported in the significant correlations between P literature (Heitz et al. 2002, Nadkarni et al. concentrations of ferns and orchids and host tree 2004, Cardelús and Mack 2010). Although foliage, supporting the results of Matson et al. epiphytic bryophytes and vascular epiphyte (2014). Nadkarni et al. (2002) reported that the foliage were lower in nitrogen (N) and carbon content of canopy DOM was phosphorus (P) content than tree foliage in the significantly higher than terrestrial soil, but intensively-studied leeward cloud forest stand similar for phosphorus and calcium. Canopy (1.4, 1.4 and 2.3 % N, and 0.08, 0.09 and 0.10 % humus had very low pH compared to terrestrial P, respectively), N and P mass in bryophytes and soils. Terrestrial soil had a tenfold greater epiphytic foliage represented 45 and 61 % of the amount of extractable cations, but the C/N ratios mass in canopy foliage (Nadkarni et al. 2004). and cation exchange capacity of canopy humus The natural abundance of 15N in epiphyte and the upper soil horizon did not differ bryophytes more closely matched those in significantly. precipitation compared to host tree foliage, indicating that atmospherically deposited N was D. Processing of atmospheric deposition of retained by epiphytes (Heitz et al. 2002). They nitrogen and other nutrients by epiphyte- also reported that vascular epiphytes on small laden canopies. Our understanding of nutrient branches without canopy soil had lower N foliar inputs via atmospheric deposition has benefitted concentrations and δ15N signals than those from recent measurements of cloud water and rooted in canopy DOM, suggesting that wind-driven precipitation at Monteverde epiphytes on smaller branches also retained a (Frumau et al. 2011, Hager and Dohrenbusch greater proportion of N directly from cloud 2011, Schmid et al. 2011), in addition to water and precipitation. Overall, epiphytes had isotopic analyses of precipitation and streamflow lower δ15N values than host tree foliage, and (Rhodes et al. 2010; see Chapter 2). Eddy canopy DOM had lower values than terrestrial covariance data and cloud water impactors were

used to estimate hydrologic inputs to Santa cup” in their canopy hydrology model (see Elena Cloud Forest Reserve in Monteverde below). Tobon et al. (2010) noted that uptake (Schmid et al. 2011), and they reported cloud and evaporation of cloud water was highly water deposition rates of 1.2 ± 0.1 mm day-1. dynamic, leading to relatively long residence Cloud water measured directly averaged 5% of times of ions in cloud water and mist in precipitation during the dry season, while use of epiphytic bryophyte mats, facilitating nutrient a canopy hydrology model based on δ18O retention. isotope content as a tracer indicated that cloud A canopy model was developed and water deposition represented 9% of precipitation evaluated to estimate inorganic nitrogen (N) during the same period (see Chapter 2). Because retention from atmospheric deposition by cloud water is approximately 19, 24 and 8 times canopy components in a leeward cloud forest - + enriched in NO3 , NH4 and H+ compared to (Clark et al. 2005). They first estimated net precipitation, deposition represents a significant retention of inorganic N by samples of epiphytic input of these and other ions to forest canopies bryophytes, epiphyte assemblages, vascular in Monteverde (Clark et al. 1998a,b, 2005). epiphyte foliage, and host tree foliage that were The effects of cloud deposition on vascular exposed to cloud water and precipitation plant water status and epiphytes have been solutions. Leaching experiments indicated that - investigated recently. Using satellite and NO3 was strongly retained by epiphytic ground-based observations to study cloud and bryophytes, but not by vascular plant foliage. + leaf wetting patterns in pre-montane and Net retention of NH4 by epiphytic bryophytes montane forests in Monteverde, Goldsmith et al. and epiphyte assemblages was somewhat lower, + (2013) evaluated the importance of direct uptake and reflected the internal cycling of NH4 in of water accumulated on leaf surfaces to plant DOM (Clark et al., 2005). Results were then water status during the dry season. The capacity scaled up to the ecosystem level using a multi- for foliar water uptake differed significantly layered model of the canopy derived from between plants in montane and premontane measurements of forest structure and epiphyte forest plant communities, as well as among mass in Nadkarni et al. (2004). Their model was species within a forest type. However, leaf driven with hourly meteorological and event- wetting events resulted in foliar water uptake in based atmospheric deposition data, and model all species studied. Although Clark et al. (2005) predictions were evaluated against measured little inorganic N retention from tree measurements of throughfall collected at the site foliage characterized by relatively thick, waxy (Clark et al. 1998b). Model predictions were cuticles, other leaf types were not investigated. similar to field measurements for both event- Goldsmith et al. (2013) and more recently based and annual hydrologic and inorganic N Gotsch et al. (2015) investigating vascular fluxes in throughfall. Simulation of individual epiphytes and hemi-epiphytes concluded that events indicated that epiphytic bryophytes and foliar water uptake is common in Monteverde, epiphyte assemblages retained 33 to 67% of the and improves plant water status during the dry inorganic N deposited in cloud water and season. It is possible that cloud water and precipitation. On an annual basis, the model canopy throughfall also result in available predicted that epiphytic components retained 3.4 nutrients for some vascular plants. kg N ha yr-1, approx. 50% of the inorganic N in The role of epiphytic vegetation in stand atmospheric deposition (6.8 kg N ha yr-1). Thus, hydrology and nutrient retention from epiphytic bryophytes play a major role in N atmospheric deposition has been further retention and cycling in the canopy by quantified by Kohler et al. (2007) and simulated transforming highly mobile inorganic N (ca. - by Clark et al. (2005). Epiphyte assemblages 50% of atmospheric deposition is NO3 ) to less + exposed to cloud water wetted up mobile (exchangeable NH4 ) and recalcitrant asymptotically, and began to generate forms in biomass and remaining litter and throughfall well below their water storage canopy humus. capacity at saturation (Tobon et al. 2010). Clark Overall, these studies provide a much better et al. (2005) modeled this process as a “leaky understanding of the role of epiphytes in N and

P cycling in tropical montane forests. N retention and cycling by epiphyte bryophytes Suggestions for Future Research and canopy DOM can provide an important source of N for forest ecosystems. In the A developing technology that could be useful canopy, N cycling in DOM is a significant N to scaling up from plot measurements is the use source for vascular epiphytes, although the of light detection and ranging (LiDAR) systems. activity of canopy roots remains to be Although the digital elevation model (DEM) of determined (e.g., Hertel et al. 2011). Canopy the forest floor would be challenging to DOM could be important in overall stand N accurately generate in some areas of cycling where N cycling rates in soil on the Monteverde, this technique has estimated forest floor is relatively low (e.g., due to biomass and canopy structure in other tropical waterlogging) and the mass of canopy DOM is forest ecosystems (e.g., Clark et al., 2011, Asner relatively large. These research efforts further et al. 2012, Vaughn et al. 2013). confirm the linkage of bryophytes and vascular A second fruitful area of investigation would epiphytes to microclimatic conditions in be the use of eddy covariance to measure net Monteverde, and suggest that they will likely be CO2 exchange (NEEc) and forest productivity. some of the first organisms affected by changes Although eddy covariance have been used to in climate and wind-driven cloud and estimate CW deposition in the Santa Elena cloud precipitation amounts. forest (Schmid et al. 2011), this technique has not been used to estimate long-term net CO2 E) Carbon, nutrients, and enzymes in soils. exchange in Monteverde. One limitation to this The variability of soil nitrogen fixation activity, approach in the complex terrain, although some microbial biomass, fungal and bacterial locations in the lower MV community would be abundance and diversity, and the abundance of appropriate. Even discontinuous NEEc data key functional genes for lignin degradation and could be integrated with various forest bacterial N- fixation in forests on the Caribbean productivity models such as PnetCN (Thornton and Pacific slopes of Monteverde have been et al. 2002) or ED2 (Medvigy et al. 2013) to correlated with soil moisture (Eaton et al. 2012). estimate net primary productivity of forests in Investigation of soil properties in and near the Monteverde. Some satellite datasets (such as the Santa Elena Forest Reserve indicated that MODIS NPP algorithms) may be difficult to pastures created by forest clearing of the cloud apply to Monteverde because of cloudiness. forest contained 20% less carbon at 0 to 30 cm However, CO2 exchange and florescence data depth than mature forest soils, and that 30 year collected from the recently launched NASA old secondary forest contained intermediate Orbiting Carbon Observatory 2 satellite may amounts of soil carbon, whereas no trend for soil provide useful information for remote areas such nitrogen occurred (Tanner et al. 2014). Soil as Monteverde. CO2 flux followed the same trend as soil carbon; Finally, the impact of reduced cloud water mature forest soils exhibit slightly higher CO2 deposition during the dry season may affect flux, but greater spatial variability, and canopy N cycling. The global trend has been secondary forest soils have a higher flux than towards enhanced N deposition due to vehicle pasture soils. They suggested that differences in emissions, fertilizer use and agriculture soil CO2 flux between sites were due to practices, leading to greater NH3 and NOx differences in root respiration, controlled by the emission and ultimately higher rates of N size and abundance of plant roots in the deposition. However, if the mechanism of subsurface. delivery to epiphyte laden canopies change, little is known about canopy processing of dry deposition in Monteverde, or how this may impact both non-vascular and vascular epiphytes.

References

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10 Conservation in the Monteverde zone: contributions of conservation organizations — Update 2014

Leslie J. Burlingame

The Monteverde conservation organizations 10.1 Socio-Economic Developments in the documented in 2000 have matured and evolved, Monteverde Zone joined by additional organizations that A. General Developments developed in new niches. Their primary focus Population in the Monteverde zone has has moved beyond talking about sustainability to increased in the last 15 years to about 6000; at practicing it, though there is not yet consensus least 150,000 tourists visit each year on how to define sustainability and what (www.monteverdefund.org). This rapid growth measures to take (Gora 2013). put pressure on local institutions and resources More publications and theses/dissertations and increased socio-economic problems. Years related to the chapter topic are now available, of effort led to the emergence of a local district but most sources are still "gray literature," government in 2003; it works with national and though much has been posted on the Internet. I local organizations to confront environmental have carried out interviews in annual two-week problems, especially those related to water and visits to Monteverde, with frequent follow-up e- solid waste (Ewing 2007). The Santa Elena mail contacts. Updates to essays that were at the office of the Instituto Costarricence de end of the chapter are included in the text below Acueductos y Alcantarillado, AyA (Costa Rican as (essay). Institute of Water and Drainage), joins with local organizations to protect springs, treat drinking water, and clean and monitor streams

2 and rivers, but there is not enough clean water in to transfer land ownership to the farmers of La the dry season and treatment of gray and black Bella but to place certain "forested areas ... in water remains inadequate. In 2010, ecological easements in the name of the conservation organizations joined the local Asociación Finca La Bella with the University government to create a commission (COMIRES) of Georgia as the partner organization to develop plans to deal with the area's solid responsible for assuring that these areas are waste to comply with a nation-wide 2010 law being conserved in forest" (K. VanDusen and Q. (Ley No. 8839). The local government now Newcomer, pers. comm., Cresson 2013). runs regular garbage pick-ups, has built a El Buen Amigo (essay) was a second recycling collection center, involves volunteers experimental coop located in San Luis (update in monthly recycling pick-ups, and has started by E. Vargas): building mini-recycling receptacles around the "…Around 2004 the remaining five region (M. Díaz, pers. comm.). families stopped individually managing the dairy The Coope Santa Elena (Coope), which operation of the farm. ... They sold the 10+ ha of dominated so many aspects of life in pastureland that had been bought through the Monteverde from the 1970s to the 1990s, faced work and effort of the ... members of the group bankruptcy in 2001. It closed or sold its credit and other support (MCL). ... With the sale union, grocery store, hardware, and agricultural income, the families were able to buy or supply store; private businesses replaced these construct another home in San Luis entities (Guindon 2001, McCandless 2008). (two families moved to another community). Two Coope-affiliated organizations survived in The original farm (131 ha) was not sold; it altered form: Comité de Artesanías Santa Elena- continued to be a property under the care of one Monteverde (CASEM) and Finca La Bella. The of the Leitón brothers and his family. I still see coffee coop producing Cafe Monteverde is in the many reasons to think that this project had a process of closing or being transferred to a positive impact on the lives of the participants. different organization in 2014 (Q. Newcomer When I talk with the young people, now adults, and G. Vargas, pers. comm.). that were the small children during the BA farm CASEM (essay), like La Campesinita years I can clearly see how they were proud of (essay), has empowered women and opened themselves and empowered to pursue different educational and economic opportunities for them or new life projects." since the 1980s (Stocker 2013). It became a B. Growth of Tourism completely independent cooperative in 2001 Tourism has grown rapidly in Costa Rica (Cooperativa de Comercialización de Artesanías since the 1990s. In 2013, the government's de Santa Elena de Monteverde or Costa Rican Tourism Institute (ICT), which has CASEMCOOP R.L.). They currently have more been promoting tourism aggressively, reported a than 85 members producing handmade crafts. In record 2.4 million international arrivals 2010, they added a restaurant that serves (Madrigal 2014). Many of these arrivals were "typical" Costa Rican food. They face two main tourists who headed to the beaches and non- challenges: recruiting younger members and sustainable mega-developments primarily owned competing with more than a half dozen other art by foreign investors, but many visited more and craft stores that have grown up, many run by sustainable smaller scale ecotourism venues with former CASEM members (P. Jiménez, pers. local owners in less accessible places such as comm.). Monteverde (Honey 2008). Guide books and Finca La Bella's (essay) trusteeship was on-line sources continue to cite Monteverde as a "transferred to the Institute in 2003 when there must-visit location; Monteverde and Santa Elena was concern that the bank might take it when rank number 1 of 25 "Top Experiences" in Costa [the Coope] ... could not pay their debt" (K. Rica in Lonely Planet (2012). No accurate data VanDusen, pers. comm.). In 2013, on the number of visitors each year exist, but representatives from La Bella, MVI, the San estimates range from 150,000 to 250,000. When Luis Development Association, and the the road to Monteverde is paved in 2016, there Monteverde Monthly [Quaker] Meeting agreed will certainly be more visitors, though they may

3 not stay as long. Tourism has become sostenible.co.cr); the two largest Monteverde Monteverde's primary source of income, Reserves (MCFP and CER) and some replacing the agricultural sector (the iconic sustainable farms and schools fly the Bandera Cheese Factory was sold in 2013 to a large Azul. Mexican company). The Center for Responsible Travel (CREST) Facilities for tourism have expanded, stresses another international approach to ethical especially those linked to adventure tourism, tourism, which encourages tourists to support including numerous canopy tours with zip lines, sustainable environmental, economic, and social hanging bridges, "sky trams," "Tarzan" swings, development of the area they visit. CREST and and bungee jumps. One hotel owner estimated MVI sponsored an International Travelers' that about half of his guests booked both an Philanthropy Conference in 2011, which led to a adventure tour and a visit to a reserve, with a 3-year pilot project (funded by the Inter- quarter each on just one type of tour (P. Belmar, American Foundation) that became the pers. comm.). independent non-profit Monteverde Community There are more than 20 larger hotels and Fund (MCF, Fondo Comunitario Monteverde, many smaller types of lodging, including inns, FCM) in 2013 (Wilkins 2011; pensions, cabins, and even one small hotel with www.monteverdefund.org): rooms built up in trees. Restaurants, cafes, art "The Monteverde Community Fund ... is and craft shops, and souvenir stores have dedicated to mobilizing resources that bolster proliferated. Many new educational exhibits the work of our engaged citizenry and have developed, including the Bat Jungle, the community organizations around themes of Ranario (Frog Pond), Butterfly Gardens (essay), sustainability. Among its varied fundraising Serpentario (Serpentarium), hummingbird strategies is the Monteverde Traveler’s gardens, and orchid gardens. Several private Philanthropy Program, which seeks to more farms offer tours, and almost everyone runs a effectively capture resources from the influential night tour. Chocolate, sugar cane (the tourism sector and equitably channel them into Trapiche), and coffee tours include tastes and priority initiatives identified by the community. the option to buy these goods (R. LaVal, pers. MCF currently provides small grants for projects comm.). related to environmental conservation, social ICT developed a Certification for Sustainable and cultural development, as well as sustainable Tourism (CST) in 1997; hotels have to meet economic practices. Other service offerings extensive criteria in four different categories to include training and technical assistance with receive ratings project proposal development and facilitating (www.visitcostarica.com/ict/paginas/sostenibilid spaces where residents, businesses and non- ad, Honey 2008). One hotel in Monteverde now profit organizations can benefit from peer has the highest rating. Its owner said "Our hotel exchanges. The organization ... operates as an was always developed in a sustainable independent entity with 2 staff members, way...CST was a way to show the world what approximately 30 associates and a growing we did in a way that could be measured... Our network of local and national business guests do very much appreciate the fact that we collaborators" (J. Welch, pers. comm.). run an eco operation" (P. Belmar pers. comm., Although tourism has brought many benefits www.hotelbelmar.net, agrees with Gora 2013). to the Monteverde area, it also has negative Several other rated hotels emphasize their strong effects (Chamberlain essay) beyond the obvious sustainability philosophy and practices (H. water and waste issues. Social and health Smith, pers. comm.). Some tour agencies problems include poorer nutrition and obesity highlight CST certified facilities. ICT (junk food replacing home grown food), drug developed a separate certification system, the use, and thefts. Although natural history guiding Blue Flag (Bandera Azul) for beach has provided many well-paying jobs and communities, nature reserves, and ecologically financial opportunities, economic inequality has managed land (Honey 2008; increased; many jobs are in the low-paying www.visitcostarica.com/ict, www.turismo- service sector, and the cost of living has

4 increased (R. LaVal, pers. comm.). Land prices regarding climate change" have skyrocketed, and adequate near-by housing (bosqueternosa.wordpress.com). They have is unaffordable for most. Tourism has become a funded projects for local conservation sort of monocrop vulnerable to environmental organizations and schools, and Santa Elena's and economic changes. The worldwide AyA. They made grants for biodigestors for recession that started in 2008 had serious wastewater treatment on some San Luis farms, negative impacts as tourism and international for reforestation of springs and riparian buffer donations dropped. Effects rippled through the zones (CRCF), and for research on bird Monteverde economy; several businesses went populations in cloud forests and biological bankrupt (P. Belmar and R. LaVal, pers. corridors (Bosqueterno poster 2014). comm.). A hotel owner stated: "For the moment, the market is keeping new 10.3 The Monteverde Cloud Forest development at bay, but if we were to Preserve (MCFP) experience another boom, the risk of The MCFP remains the most visited private overdevelopment is high" (P. Belmar, pers. reserve in the area, welcoming almost 70,000 comm.). There is still no zoning (H. Smith, visitors per year to its cloud forests (TSC 2006). pers. comm.). However, numerous groups are It has 40 employees and creates about 600 jobs aware of these problems and are trying to do directly and indirectly in the area something to solve them (Honey 2008, Koens et (www.reservamonteverde.com). The Preserve's al. 2009, Burlingame 2013, Stocker 2013). size is 4025 ha, less than previously because of the 2007 settlement of the dispute with the 10.2 The Quakers and Bosqueterno, SA Monteverde Conservation League (MCL) (BESA) involving land purchased in the initial Peñas In 2001, Quakers in Monteverde and other Blancas campaign (1986-1989). MCL kept the community members celebrated the 50th 5300 ha from its campaign, and some horse- anniversary of the Quaker's arrival in trading of land parcels smoothed out the border Monteverde. They published an illustrated between the CER and the MCFP (B. Law, pers. collection of original documents and essays on comm.). life in Monteverde over the 50 years, including The Management Plan of 2005 reaffirmed material on the history of many of the land use zoning: 97% of the Preserve has organizations discussed in this chapter (Guindon absolute protection; 1% is zoned for special use; 2001). and 2% is for public use in the "Triangle," (13 K BESA, the organization that they established of trails for tourists). In the last 15 years, in 1974 to protect 554 ha of their watershed, several new trails have been built and most continues to be managed by BESA's Board and existing ones have been widened and re- protected by the Monteverde Cloud Forest hardened. A hanging bridge was added; viewing Preserve (MCFP), owned by the Tropical platforms at La Ventana, the waterfall, and Science Center (TSC) in San José. In 2006, restaurant and signs, bridges, benches, and trail negotiations with TSC produced a new rental edges were rebuilt with recycled plastic boards. agreement for use of Bosqueterno's trails (by Visitation reached a high of 80,270 in 2008 and ever more visitors) and for leases on declined afterwards (with the global recession), telecommunication towers on its Cerro Amigo. then increased to 67,950 in 2013 These funds, plus new income from Costa Rica's (www.reservamonteverde.com; R.W. Carlson Environmental Service Payments, allowed and C. Hernández, pers. comm.). Most BESA to start a small grants program in 2008 to buildings have been remodeled with a focus on support "projects having to do with protection of sustainable construction and practice, most springs, including reforestation; education notably the Casona's "rustic" lodge that can focused on water quality and river ecology; sleep 43 and the restaurant, which were certified prevention, elimination, or treatment of in 2009 by the CST Program. The Reserve's contaminated waters; general education web page features a tab for "Sustainability" that regarding freshwater conservation; education lists the practices the Preserve has instituted.

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MCFP also received (2012) the ecological Blue shows more individual researchers investigating Flag award for the protection of natural areas the effects of climate change on various including water and waste management (M. organisms. Alan Pounds was hired as "Resident Díaz, pers. comm.). Scientist" in 1999 to study climate change in the The Environmental Education Program Reserve. Canopy researcher Sybil Gotsch (EEP) has two staff members who work with 1- (Franklin and Marshall College) began a study 6th grade students and teachers in 12 local of the vulnerability of epiphyte communities to schools; students also visit the Preserve. EEP changes in climate by examining the has broadened its focus on the Preserve's forest ecophysiological responses of selected common to deal with global climate change, endangered epiphytes to water loss (S. Gotsch, pers. comm.). animal species, and water and waste (Blum Costa Rican researcher L. Moreno continued her 2012). The Preserve continues to work with 17-year investigation on the effect of climate students from all Costa Rican high schools that change on the abundance and composition of have ecotourism programs and universities with bird species in the MCFP (Y. Mendez, pers. biology and applied science programs (M. Díaz, comm.). pers. comm.). EEP's important role in the The Preserve has also established its own Comisión de Educadores Ambientales de projects in cooperation with Costa Rican Monteverde (CEAM) is discussed in section Universities and Instituto Nacional de 10.8. Biodiversidad (INBio). In 2007, they There have been significant developments in established "Permanent Monitoring Plots" (1 ha MCFP's support for scientific research and its each) in seven locations. This work built on applications. The new Alexander Skutch previous projects by B. Haber, who "established Laboratory opened in 1999 as the Monteverde long-term phenology plots around the book went to press. The 200 m2 building has community, with a few trees marked in the two labs, offices, and a classroom. Some basic reserve." Starting in 1987, N. Nadkarni "was the lab equipment is provided, but researchers are first to put in hectare plots that have been expected to bring most of their own equipment. continually re-measured every 5 years, with The Research Program has a Director and two marked and measured trees (about 2500 in 5 ha, assistants; its goal is to “generate information 4 in the primary forest, 1 in the secondary forest and technical and scientific knowledge that will within the Research Area of the Reserve" (N. help make management decisions relevant to the Nadkarni, pers. comm.) In 2010, MCFP set up protected resources in the area..." a network of meteorological stations, and they (www.reservamonteverde.com/research.html). began an Amphibian Monitoring project under The 2009 Plan Estratégico de Investigación the direction of A. Pounds. contains data from 1979 - 2009 showing that The idea of a corridor to connect the 20% of the studies were done by Costa Rican conserved areas in Monteverde to the Gulf of researchers and students. Chapter 1 of Nicoya had been discussed for years. TSC had Monteverde: Ecology and Conservation of a taken the lead with the purchase of the largest Tropical Cloud Forest had shown a decline in remaining forest patch on the Pacific side, a 240 the number of researchers as tourism increased; ha farm subsequently called the San Luis however, there was a jump in the number of Biological Reserve, and developed a MCFP projects in 2000 and 2001, followed by a Management Plan (Méndez 2009). MCFP has decline until 2006, increasing to a high point in played an important role in planning the new 2009, when there were 31 studies; a subsequent Bellbird Biological Corridor (BBC) (Section document shows the 2009 level continuing and 10.6. D.) even increasing in 2012 (Programa investigación, RBNBM, CCT 2014). The 10.4 The Monteverde Conservation subject matter of studies from 1979-2009 was League and the Children's Eternal Rainforest on: plants (41%), arthropods (21%), birds (MCL/CER) (18%), and the remaining 20% on other animals. By 2014, MCL's CER grew to 22,600 The Register of Research projects for 2013 ha, the largest private reserve in Costa Rica.

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MCL has continued to pursue its mission "to to produce surveys of CER's borders that can be conserve, preserve, and rehabilitate tropical used in legal defenses of those borders and in ecosystems and their biodiversity" through pursuit of legal titles (MCL Annual Reports, forest protection, environmental education, Burlingame 2013). reforestation, sustainable development and eco- Major improvements to CER's infrastructure tourism, and scientific research. MCL has been have been made over the last 15 years with recognized nationally and internationally for its attention to environmental sustainability. Trails successful conservation efforts, most recently and signage, road and Internet access have been including the Costa Rican Blue Flag award improved. The two biological stations (San (Bandera Azul) for protected natural areas. CER Gerardo and Poco Sol) are powered by has been supported for many years by sister renewable energy and have gray water treatment organizations in Sweden, the United States, the plants; the Poco Sol station was completely United Kingdom, Japan, and Germany rebuilt by 2010. The offices of the MCL on the (acmcr.org, Burlingame 2013). Monteverde and Atlantic sides of CER and The League’s financial difficulties in the structures at Bajo del Tigre have all been 1990s made additional land purchases a low remodeled. The Bajo del Tigre sector is the only priority until 2002, when Rachel Crandell, a part of CER that is easily accessible from the teacher, founded the MCLUS in Missouri. In Monteverde area; it receives 75% of the visits to consultation with MCL's leadership, in 2004 CER (MCL Annual Report 2013). Night walks Crandell launched a new Land Purchase and started at Bajo Tigre in 2003 have become a Protection Campaign, using 50% of each significant source of funds for MCL. A native donation for Land Purchase, 40% for protection plant greenhouse was constructed in 2005, and a (which includes the operation of MCL and labeled demonstration garden was replanted MCLUS), and 10% for endowment. MCL around the Visitors' Center. In 2012, an established a prioritized list of properties to buy, observation platform overlooking a regenerated focusing on filling out the borders of CER to forest, a meeting/picnic area, and gray water natural boundaries and blocking points of easy treatment system were added; the following entrance, buying land to connect pieces of CER, year, a state-of-the-art classroom was built and buying inholdings. In a return to the (MCL Annual Reports, B. Law and W. original vision for the MCL, they also wanted to Zuchowski, pers. comm.). extend CER on the Pacific slope to help create a Although MCL's economic difficulties ended corridor for altitudinally migrating animals. the Environmental Education (EE) Program in MCL sister organizations in the U.K. and 1995, most of MCL's personnel continue Germany and others also contributed to the land involvement with some EE activities, including purchases. After Crandell's death in 2009, U.S. leadership roles in community recycling and supporters continued MCLUS, renamed Friends roadside and stream clean-up. In 2007, of Children's Eternal Rainforest (FCER) in 2012 MCLUS/FCER increased funding for EE. Local (MCLUS/FCER Annual Reports at children visit Bajo del Tigre for EE activities, friendsoftherainforest.org). with transportation funded since 2010 by BESA, Following the 2007 Peñas agreement and the Finca Steller Education Center on the between MCL and TSC, MCL had an additional Atlantic side of CER. In 2012, a five-year grant 5300 ha to protect in CER. Squatters are no provided for an environmental educator to work longer a problem, but MCL's forest guards face with schools on the Atlantic side of CER on serious challenges from illegal poaching, such topics as recycling, biodiversity, animal logging, capture of live animals, and removal of welfare and abuse, water resources and the plants. Guards monitor endangered species; importance of wetlands (www.friendsofthe there was great excitement in 2013 when rainforest.org/annual-report-2012). motion-sensing cameras photographed a jaguar The League's tree nurseries have produced and tapirs. MCL personnel also help 1.6 million trees (B. Law, pers. comm.). Most researchers. The important Land Ordering of these were planted in MCL's windbreak Project, which began in 2006, uses GIS and GPS project and persist, as do others planted under

7 special projects. Finca Steller has a small native offset payments for forest protection and tree nursery that produces a few thousand native reforestation, but first they have to get legal title tree species per year. The Fundación to all the land in CER, which will require a Conservacionista Costarricense (FCC) is raising special legislative bill. The League's case was native tree species on the Pacific slope that MCL helped by its successful 25th Anniversary, in has used for reforestation of degraded recognition of which the Costa Rican postal pastureland. Zuchowski's ProNativa service issued four commemorative stamps on organization promoting the use of native plants National Parks Day, August 24, 2011 that began with the greenhouse and (Burlingame 2013). demonstration project at Bajo Tigre has expanded (Burlingame 2013). 10.5 Santa Elena Cloud Forest Reserve MCL's financial deficit, incurred when the (SECFR) Debt-for-Nature-Swaps and grants ran out in the SECFR is achieving its goals to share "the mid-1990s and contributions were still benefits of tourism and using them as a tool for earmarked for land purchase, was at its worst in [sustainable] development where entrance fees 2001. Gradually, the MCL's finances began to are employed for the protection and improve. The most important new source of management of the Reserve and to provide a income was payment for environmental services better quality of education in the Colegio [Sta. (ESP) by the government program FONAFIFO Elena high school] and some schools of the (Fondo Nacional de Financiamiento Forestal) zone" (Y.M. Arias, pers. comm.). Since 2009, and two private hydroelectric companies. MVI's there have been about 30,000 visitors per year, Annual Reports document the dramatic increase more than double the highest number in the in the areas of CER included in ESP and an 1990s. These visitors provide indirect economic equally dramatic increase in income for the benefits to tourism businesses in the community MCL, going from no income in 1996 to an and employment as Reserve staff and guides average of 62% of MCL's operation's income most of whom are graduates of the Colegio, thus from 2009 to 2011 (MCL Annual Report 2013). fulfilling another goal of SECFR (W. Bello, Other income is from fees for entry to trails, pers. comm.). There are new programs in mainly at Bajo del Tigre; unrestricted donations environmental education, reforestation, and for operations; the sale of merchandise in MCL species monitoring. facilities; and net income from the biological The road to the 310 ha Reserve is now stations. Donations for specific projects, improved, thanks to adventure tourism sites just including land purchase, are an important source below. In 2012, the Visitor's Center was rebuilt; of income. Another source of funds is interest it and a new half k of hardened trail are on investment, including a growing endowment handicapped accessible, making the SECFR the fund; Rachel Crandell had made MCL the first in the area to meet the requirements of Law beneficiary of her substantial life insurance 7600 for equal access. An orchid garden whose policy. plants were rescued from the forest floor, a small Unfortunately, in 2012, the Costa Rican medicinal plant garden, and other native plants government changed its policies on ESP, attract butterflies and hummingbirds. The 12 k deciding to help small landholders with 50 ha or of the four original trails and their signage have less. MCL and several other conservation been improved. If the weather is clear, organizations in Monteverde saw their incomes spectacular views of Arenal Volcano and Lake, drop dramatically as land under ESP phased out. the Gulf of Nicoya, and the Lake of Nicaragua By 2013, inflation and increased expenses await those who scale the new 12 m high metal (including legal costs) had raised the estimated observation tower on the Youth Challenge trail amount needed to run the organization to a half (reservasantaelena.org). million dollars per year (MCL Annual Report SECFR's environmental education 2013). MCL is exploring ways to increase the coordinator worked closely with the Colegio number of visitors to CER from the 2013 level students and teachers in the Ecological Tourism of 7000 and find new funding, especially carbon degree program. Blum (2012) stressed the

8 broader definition of EE, including as Palo Verde and Lomas Barbudal previously environmental ethics and values, used by part of ACT or the Tempisque Conservation SECFR and the national high school curriculum Area). Arenal National Park was put in a new compared to MCFP's more biological approach 11th conservation area, Huetar Norte (ACAHN). to EE. However, Blum's research was Although all of SECFR is in ACAT, whose conducted in 2003 just as EE approaches in the main office is in Tileran, parts of CER are now two organizations started to converge. Both in three Conservation Areas (Y. Rodríguez, pers. include more attention to water and waste comm., acarenaltempisque.org). problems in the area, endangered species, and SECFR is a member of other environmental global climate change. The Commission on groups in the area such as COMIRES, CEAM, Environmental Education of Monteverde and the Bellbird Biological Corridor. They also (CEAM; see 10.8 below) began in 2003 under have special international agreements with the leadership of the heads of EE at SECFR and Rocky Mountain National Park in Colorado: a MCFP. Also in 2003, SECFR started working 2012 one through ACAT for exchange visits of with 5 primary schools around the Reserve in department heads, and an exchange of students ways similar to MCFP, providing programs at in 2014 from SECFR and the Park to study the schools, workshops for teachers, and scientific monitoring (Y.M. Arias, pers. comm.). engaging students and teachers in activities. SECFR’s EE program also works with the 10.6 New Conservation Organizations: Grupo Amigos del Ambiente (Friends of the A. Costa Rican Conservation Foundation Environment), a group of Colegio students that (CRCF) that formed in 2011. The group, which had In 2002, local residents, including biologists, grown to 32 volunteer students by 2012, set up a established the CRCF to protect, connect, and recycling program in the Colegio and at SECFR restore "tropical habitats with a special emphasis and became involved in fieldwork with on the deforested Pacific slope of Costa Rica ... researchers from four Costa Rican universities [in] areas critical for the survival of the Three- monitoring amphibians, birds, and water and air wattled Bellbird (Procnias tricarunculata)" quality (Y.M. Arias, pers. comm.). They also (fccmonteverde.org). CRCF grew out of George monitor mammals with 8 donated motion Powell's 1990s discovery that the endangered detecting cameras and post photos of pumas and Bellbirds rely on the wild avocado fruit trees ocelots on their website that grow in Pacific slope forests, during their (reservasantaelena.org/proyectos [and] post-reproductive period. Although the breeding /Boletines). The group joins visitors and other grounds of the Bellbird and Resplendent Quetzal students in a reforestation project in areas are well protected on the Caribbean slope of bordering the Reserve using donated tree Monteverde, the decline in Bellbird numbers seedlings; since 2011, about 5000 trees have after 1998 was traced to habitat loss in the been planted per year (Y.M. Arias, pers. Pacific Rain Shadow Forest. comm.). CRCF planned to create a 7 k biological The Administrative Board of the Colegio corridor to link the protected Monteverde continues to manage SECFR and has signed new Reserve Complex with a lower protected zone, leases every 5 years with ACAT-MINAE (Area Cuenca Abangares, creating the Bosque para de Conservación Arenal-Tempisque or Arenal- Siempre (The Forest Forever). They developed Tempisque Conservation Area and the strategies to create the corridor: land purchases, Ministerio del Ambiente y Energía or Ministry conservation easements, cooperation with of the Environment and Energy). The landowners, and pasture restoration. As of Conservation Area (one of 10 administrative 2014, CRCF owns four wildlife reserves and has divisions of the country) had been called ACA two other privately owned areas under (Area de Conservación Arenal) and included conservation easements, providing successful Arenal National Park. In 2007, the Conservation protection to 77.5 ha (D. Hamilton, pers. Area was reorganized to include territory down comm.). Working with farmers and other to the Tempisque River (adding protected areas landowners, conservation organizations,

9 students, and volunteers, they reforested CRCF from volunteers and one half-time employee. properties and many others. Their main tree She created demonstration gardens with signage nursery is at La Calandria, a private reserve and around these organizations and at the Biological biological station in Los Llanos. Research Station, Monteverde Centro, local businesses, projects include experiments with seedling and private yards. At CFS, she helped establish propagation, survival, and growth rates, and the gardens featuring specific plants to attract bats, most effective and cost-efficient restoration birds, butterflies and bees. In 2007, she practices (fccmonteverde.org, monteverde- developed an illustrated Electronic Field Guide institute- to Native Ornamental Plants of Monteverde blog.org/environmental/2013/9/18/poster...). (http://efg.cs.umb.edu/efg2/TypePage.jsp) with CRCF has produced and distributed 173,000 free the Electronic Field Guide Project at U. Mass. native tree seedlings of 93 species (D. Hamilton, Boston. These activities led to the formation of pers. comm.). a ProNativas Network in 2008 with workshops, CRCF continues its annual Bellbird census. conferences, and a website (pronativas.com, W. Since 2009, the decline appears to have slowed; Zuchowski, pers. comm.). the numbers of bellbirds have held steady (D. C. Curi-Cancha Reserve (Curi-Cancha) Hamilton, pers. comm.). Many other birds The 83 ha Curi-Cancha opened in 2011 on depend on the corridor, including neotropical property owned by the Lowther family, which migrants, such as scarlet tanagers, rose breasted they purchased in 1970 from Hubert grosbeaks, wood thrushes, Baltimore orioles, Mendenhall, one of the original Quaker settlers. and several migrant warblers. The U.S. Fish and It forms a corridor linking BESA on the north Wildlife Services' Neotropical Migratory Bird and east down to land owned by MVI and CRCF Conservation Program has provided several and has a "mix of virgin forest, secondary grants to the CRCF. BESA and FCER (see growth of varying ages and some pasture" (J. above), along with the British Embassy, GEF Lowther, pers. comm.). CRCF has planted from the UN Small Grants Program, and several many native trees bearing fruits favored by U.S. zoos also supported CRCF with grants. bellbirds and quetzals. Curi-Cancha is legally Many donations and work efforts have come recognized as a Refugio de Vida Silvestre through a student organization, The Change the Privado by MINAE and aims to be an World Kids (a US non-profit), and researchers, "economically and environmentally sustainable interns, and students (fccmonteverde.org). The business" (reservacuricancha.com, J. Lowther, CRCF has recently joined other conservation pers. comm.). It has become popular with organizations in the creation of two larger guides and tourists because it is less crowded projects, the Bellbird Biological Corridor and than MCFP (limit of 50 visitors per day), has the Monteverde-Arenal Bioregion Initiative (see more open areas for animal viewing, and a lower D and E). admission cost. In 2013, 10,000 people visited B. ProNativas-Monteverde (ProNativas) the reserve, providing economic benefits for Reforestation with native rather than fast- more than 25 guides and for taxi drivers (M. growing introduced tree species had gradually Ramírez, pers. comm.). become accepted as the norm, but it took a new D. Bellbird Biological Corridor (BBC) organization to convince people in Monteverde The Three-wattled Bellbird Biological of the many environmental advantages of Corridor (66,000 ha) aims to connect the planting native ornamental plants and the Monteverde Reserve Complex through four environmental threats from invasive exotic watersheds and 11 life zones down the Pacific plants. Willow Zuchowski, author of Tropical slope to the Gulf of Nicoya. In 2008, building Plants of Costa Rica, founded the non-profit on earlier corridor proposals to protect such organization ProNativas in 2004 with the altitudinal migrants as the Bellbird and the support of local conservation organizations and Quetzal, a local Council formed to make the outside funding. She had to collect seeds and corridor a reality. The seven founding members cuttings, have greenhouses built (at MCL, CFS, of the BBC were: the Arenal-Tempisque and MVI), and then plant gardens with help Conservation Area (ACAT-MINAE), CRCF,

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MCFP, MCL, MVI, SECFR, and UGACR). In Tropical Ecology Research in Monteverde, 2009, these groups agreed to pay for a part-time Costa Rica," the session included presentations Co-ordinator for the Project. With funding from by six Monteverdans with different institutional the GEF-Small Grants Program of the United perspectives (ATBC Online Web program for S- Nations, they elaborated and are implementing a 11, 25 June 2013). They examined the special Strategic Plan with a mission to reestablish and interactions in Monteverde of "conservation, maintain: biological connectivity, conservation education, ecotourism, civic awareness, and of natural resources, and the well being of local spirituality" that made Monteverde such a communities (Corredor Biológica Pájaro productive location for scientific research even Campana, Plan Estratégico 2011-2016). though it had no major biological research By 2014, the Project created maps using station (N. Nadkarni, pers. comm., see Nadkarni satellite images and GIS of the physical, and Wheelwright 2000). How could biological, and land-use features of the proposed Monteverde's success be improved and how corridor. They monitored bird populations, could it serve as a model for nearby and other documented water abundance and quality, and tropical areas? produced thousands of trees for reforestation. MABI drew 55 participants including BBC members are requesting funding for native representatives from all the organizations tree reforestation around existing springs. They discussed in this update and more from the meet and facilitate workshops with civic and larger bioregion and beyond such as MINAE- community organizations in the corridor to SINAC; AyA Santa Elena; the Universities of educate them about the BBC and learn about Georgia, Texas A&M, Brown, California, their concerns. By 2013, 26 organizations were Stanford, Utah, and Vermont in the States and affiliated with the BBC (Welch 2007, cbpc.org, the Universidad Nacional in Costa Rica; The N. Vargas and R. Guindon, pers. comm.). School for Field Studies; FCER; Conservation E. Monteverde-Arenal Bioregion Initiative International and the Nature Conservancy (MABI) (iniciativamonteverdearenal.blogspot.com/2014/ MABI, the newest cooperative conservation, 02/instituciones-invitadas-invited.html). The research, education, and sustainable conference began with poster presentations by development project, was launched at a Feb. the different organizations so that everyone 2014 conference at the Monteverde Institute. P. knew the focus, priorities, and activities of the Raven, in his welcoming remarks, framed the other organizations. Emphasis was on forging focus of the conference: "How can the talents "communication links between existing groups" and activities of the many organizations who (N. Nadkarni, pers. comm.). have permanent facilities in this region or visit it Participants worked to develop a common repeatedly become a conceptual entity with vision. Further discussion and planning took more facilities, educational opportunities, more place in committees: Education, Conservation, extensive conserved and restored areas, an Research, Maps, Communication, and Funding. enhanced contribution to sustainable tourism, The leaders of each committee constituted a and lasting value...[that is] fully integrated with Coordinating Committee. The Conference blog the welfare of all the people who inhabit the outlines the challenges, possible solutions, and region"? committee proposals (iniciativamonteverdearenal.blogspot.com/2014/ (iniciativamonteverdearenal.blogspot.com/2014. 02/welcoming-remarks-peter). 02....). The Research Committee is developing a The Initiative grew out of a symposium website where scientists will be able to post organized by N. Nadkarni at the joint 50th research projects and data sets. A key next step anniversary meeting of the Association for is finding funding to hire a part-time Tropical Biology and Conservation (ATBC) and coordinator; a follow-up conference is planned the Organization for Tropical Studies (OTS) for 2015 (N. Nadkarni, pers. comm.). held in San José, Costa Rica in June 2013. Entitled, "The Perfect Storm: Educational, Conservation, and Community Synergisms for

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10.7 Environmental Education and program, "Globalization, Development, and Sustainability at the University/College Level Environment," began in 2009 as a joint venture Primarily for Students from North America between Mount Holyoke and Goucher Colleges. Costa Rica has become the leading Latin The Living Routes Program: Tropical Ecology, American study abroad destination (Dyer 2014, Development, and Social Justice (2011-2013), Institute of International Education 2014). focused on the impact of national and Monteverde has been a magnet for international policies on local sustainability, college/university courses, starting with the OTS conservation and social justice. MVI also graduate Fundamentals course in 1971 collaborates with partner institutions to offer (Burlingame 2002). The Monteverde Institute customized services (F. Lindau, pers. comm., has offered programs for international students Burlingame 2013). since 1987; in the last 15 years, three other By 2009, MVI's campus occupied 24 ha; two institutions have established centers in the area. years later, MVI and CRCF began joint A. The Monteverde Institute (MVI) management of the newly created 14 ha Dwight MVI has built on its mission of "education and Rachel Crandell Memorial Reserve adjacent for a sustainable future," providing a broad to MVI's campus (D. Hamilton, pers. comm.). range of courses supported through many This Reserve completes a corridor in the 62,000 institutional partnerships. It puts sustainability ha of privately protected forest reserves known and conservation into practice on its campus and as the Monteverde Reserve Complex. through its courses and community interactions. A new wing was added to the main building MVI has encouraged students, researchers, in 2002 to house the John and Doris Campbell interns, and volunteers to develop applied Library. Behind it is a small classroom building, research projects that generate information and constructed in 2002 by the Fox Maple School of options to help local communities deal with Traditional Building (Maine) using non-native pressing issues. In addition, MVI has brought trees. Construction of a new outside timber- substantial educational, cultural, and economic framed, multi-functional, glass-enclosed benefits to local communities (Burlingame 2013, classroom in 2012 was a collaborative project MVI Annual Reports, monteverde-institute.org). among local artisans, volunteers, and MVI By the end of 2013, MVI had provided nearly courses (Burlingame 2013, monteverde- 480 courses (long and short) for about 8900 institute.org/facilities-at-mvi). Sustainable students; there are now about 25 courses each construction has been joined by sustainable year (F. Lindau, pers. comm.). Tropical Biology practice at MVI, as detailed on MVI's web site. and Conservation, the University of California MVI has worked with homestay host families to Education Abroad Program (UCEAP) given two help them improve energy efficiency in their semesters per year since 1987, has consistently homes, and to promote recycling and had the largest number of students. In the composting. continuing long course, "Sustainable Futures" In 2013, students and volunteers developed (SF), upper level undergraduate and graduate demonstration organic "Carbon Gardens" around students in architecture, landscape architecture the new classroom, including a vegetable and and planning, engage in “service learning” to herb garden, a keyhole garden, rain gardens (to develop their knowledge and skills by working use rain runoff from the Fox Maple roof), a (gratis) on planning and designing projects that greenhouse for raising native plants, and a native help local communities and institutions. tree nursery producing saplings for reforestation. Projects have ranged from designs for specific Native plants and tree saplings are planted on facilities (including those of MVI) to large scale MVI's campus and donated to local people for “scenario planning," development plotting and their use. Volunteers tagged trees behind the tracking in the area, and scenarios for the future. main MVI building to establish an arboretum. In 2001, a partnership with the University of The gardens will also be used for experiments South Florida produced an annual course on with sustainable agricultural techniques and will "Globalization and Community Health." A provide educational opportunities and nutritional semester-long interdisciplinary place-based information for MVI students, staff, and local

12 communities (D. Hamilton, pers. comm.; MVI has provided direct financial benefits monteverde-institute-blog.org). for staff, teachers, taxi drivers, cooks, guides, From the beginning, MVI was interested in and for families offering homestays for MVI fostering, facilitating, and applying research in students, as well as owners and employees of the region. Research done by international tourism establishments and other businesses. In students and faculty working with MVI staff and 2010, MVI paid out more than $350,000 to resource people from the area continues to be community service providers (Wilkins 2011). made available to other researchers and the These payments, in turn, flow back into the community through presentations of research community, as does money spent by MVI's findings and the collection of research papers in international faculty, students, and researchers. the library; many are now digitized. In 2008, Some in the community have received MVI began its Integrated Water Resources individualized financial benefits such as Program, which builds on concerns over use of scholarships to attend MVI courses or aid (for water resources and public health. The program MVI employees) to continue their education. also carries out education and community MVI developed serious financial problems by outreach, particularly through its Adopt-a- 2005 as its financial debt burden grew (from the Stream Program that supervises monthly stream construction of its new building and library monitoring data collection and annual reports by addition and from land acquisition) while students from the three high schools. "The income from courses decreased. Beginning in Impact of Economic Change on Food Habits and 2006, MVI's Director, working closely with the Nutritional Health in Monteverde, Costa Rica: Board, instituted drastic reductions in expenses Mixing Agriculture and Tourism," began in through major personnel cuts, sale or divestment 2008 with funding from the National Science of some properties, and expanded efforts to Foundation and collaboration from the increase income and find new partnerships for University of South Florida. Data indicated that offering courses on a regular basis. The leaner, as families increased their involvement in more focused MVI paid off its debts by 2008 tourism, food insecurity and health problems and successfully began expansion of its financial increased. In 2012, MVI decided to promote base (more courses and students) and extension better nutrition through demonstration gardens of its community outreach. The Director and to encourage more physical exercise with a reactivated the U.S. non-profit Alliance for the "Monteverde in Motion" program (Burlingame Monteverde Institute (AMVI) in 2009. 2013). B. Council on International Educational MVI has used proceeds from its international exchange (CIEE) courses to support programs that enhance CIEE is a U.S. based non-profit organization education, well being, and sustainable that has provided international exchanges in development and culturally enriching activities many countries since 1947 (ciee.org). In Costa in Monteverde and surrounding communities Rica, CIEE is based in Monteverde, where it (monteverde-institute.org/current-projects for started offering a summer Tropical Ecology and link to PDF: Community Initiatives and Conservation Program with MVI in 1989. Alan Programs 2013). They collaborated with the Masters became the Director in 1993 and local district council to make safe walkways oversaw expansion into semester programs in along the main road a reality. In 2012, MVI 1996. MVI provided Spanish language reached out to a new group, local 12-15 year instruction until 1999, when CIEE became a olds, with a camp experience. Counselors aged freestanding program. In 2007, CIEE added 16-20 and adult volunteers from seven area Sustainability and the Environment, with Karen communities helped the younger kids have fun, Masters as Director. CIEE then moved to its engage in community service, and "develop own Study Center in Cerro Plano where there healthy and educational links between are classrooms, meeting areas, a library, and Monteverde's youth and its community computer facilities with eco-friendly members.” It is now an annual event construction and native plant landscaping; (monteverde-institute.org/summer-camp). students live with homestay families. The

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Ecology Program has courses and lives at the Over the next ten years, UGACR built Biological Station (ciee.org/study-abroad/costa- campus facilities with an emphasis on rica/monteverde/sustainability-environment). sustainability. Climate is controlled in: a wet lab Both Programs take extensive field trips on the furnished with basic equipment, an insect Pacific and Altlantic slopes (A. and K. Masters, collection, GIS lab, and herbarium, which pers. comm.). includes William Haber's donation of his The Tropical Ecology and Conservation extensive herbarium. Indoor and open-air Program is designed for biology majors, with classrooms are equipped with the state of the art courses in biology, conservation, and Spanish, electronic equipment. There are three weather and one that explores the historical impact of stations, one of which posts real time data on the humans on tropical ecosystems, including website; fiber optics and WiFi connect campus indigenous cultures, European settlement, sites to the Internet. Four bungalows house ranchers and farmers, ecotourists, and students; faculty, researchers, and interns have conservationists (A. Masters, pers. comm.; their own residences. The sustainable capacity is course details and reports on the website). The 60 people per night (Q. Newcomer, pers. full texts of all research papers since 2004 are comm.). The cafeteria, a computer lab, library, available in MVI's library digital collection; and offices are located in the student union. A each one has an abstract in English and Spanish recreation center, fields and courts for various and the collection is key-word searchable (M. sports, and 3 k of trails provide activity options. Leitón, pers. comm.; monteverde- UGA landscape architecture students designed a institute.org/mv-digital-collections-Tropical 1.5 ha botanical garden, which includes Ecology). medicinal plants and an arboretum. UGA rebuilt The Sustainability Program includes courses the 12-room Ecolodge San Luis, and in 2012, in conservation biology, policy, natural history, was awarded 4 leaves under ICT's Certification Spanish, and sustainability (K. Masters, pers. for Sustainable Tourism (CST). (UGA comm.). Students have completed internship Sustainability Report 2010 & 2013, Q. projects ranging from construction of a Newcomer and A. Cruz, pers. comm.). biodigestor and composting toilet for a coffee UGACR began tracking goals and farm to designing native plant gardens and improvements in campus sustainability in 2010 greenhouses. They built artificial wetlands to (dar.uga.edu/costa_rica). The campus has an treat gray water, created a website and produced organic farm that produces 15% of food GIS maps of reforestation plots for CRCF, and consumption. Livestock waste is processed by a worked with Hydroponics of Monteverde on biodigestor, set up as a demonstration project for "alternative, renewable fertilizers" (K. Masters, local farmers. In 2013, a large biodigestor was pers. comm.). built on campus to process all human waste; it C. University of Georgia, Costa Rica produces methane to power the kitchen stove, (UGACR) and 97% of the water used is returned clean to In 2001, the University of Georgia the forest (A. Cruz, pers. comm.). A native tree Foundation purchased the 63 ha Ecolodge San nursery (started by CRCF and taken over by Luis and Biological Station in San Luis to UGACR) produces 4000-5000 seedlings of 50 develop a satellite campus for UGA. The species of native trees to donate for reforestation property, which adjoins both the MCFP and projects each year. Over 30,000 trees have been CER, is 60% forest, 30% sustainable farm, and planted on San Luis farms and lower elevations, 10% built space (Q. Newcomer, pers. comm.). some by students seeking to decrease their UGACR's Mission "is to advance our carbon footprint incurred by their travel to the understanding, through instruction, research and Campus. outreach, of the interconnected nature of human (dar.uga.edu/costa_rica/index.php/site/sustainabi and environmental systems, particularly the lity_initiatives, Q. Newcomer and L. Ramírez, concepts of socio-cultural, ecological, and pers. comm.). economic sustainability" UGACR runs about 25 UGA programs (dar.uga.edu/costa_rica). (semester and short-term) per year, representing

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40 disciplines and 11 Colleges with about 250- (soltiscentercostarica.tamu.edu/content/mission- 275 students and 75 faculty and teaching vision-and-objectives). assistants. Programs include Tropical Biology, The land and facilities of the new center were Landscape Architecture, Tropical Reforestation donated to the TAMU System by Bill and Service-Learning, Veterinary Medicine, Wanda Soltis. Bill Soltis, a TAMU graduate, Sustainability of Tropical Agro-Ecosystems, had traveled to Costa Rica on business and Environmental Anthropology, Latin American started buying forested land next to CER to and Caribbean Studies, and Theater and Film preserve it. He donated 16 ha that had been (dar.uga.edu/costa_rica). About 40-45 short deforested for a farm and reforested it for the programs (average 5 days) for institutions other campus, provided a 100 year free lease for ca. than UGA, including OTS, bring ca. 1200 100 ha of primary and secondary forest that he students and faculty a year. More than 700 and partners own on the border of CER (E. tourists are staying an average of 4 days at the Gonzalez, per. comm.), and underwrote Ecolodge in 2013-2014; they eat in the cafeteria construction costs for the Center, using designs and participate in campus activities. (Q. by TAMU architecture students. An academic Newcomer, pers. comm., building has a wet and dry lab, 3 classrooms, dar.uga.edu/costa_rica). UGACR actively library, computer facilities and WiFi, offices, promotes research on campus and in the area, and cafeteria, with 8 dormitories that sleep up to offering information on facilities, logistical 56. All of the facilities are handicap accessible support, institutional partnerships, and research (soltiscentercostarica.tamu.edu). sites; research project are listed at The Center hosts courses run by TAMU dar.uga.edu/costa_rica. faculty focused on Environmental Design, Water Community involvement and outreach are Management, Field Studies in Tropical Biology, part of UGACR's mission. They purchase 25% and Geography Mapping. They also facilitate of their food and many services from local service-learning programs; in 2010, TAMU's providers. UGACR joined MVI to raise funds chapter of Engineers Without Borders built a for 12 small-farm sized biodigestors in the San computer lab at the School of San Juan de Peñas Luis community; their students and other Blancas. Students from TAMU's College of volunteers provided installation labor and aid to Education established an English as a Second San Luis schools (UGACR Strategic Plan 2013, Language Program for local children and Q. Newcomer, pers. comm.). UGACR is an donated English books to the school active partner in the BBC; they conduct water (soltiscentercostarica.tamu.edu). Non-TAMU quality research at 5 sites on each of the 3 rivers schools and organizations, such as OTS, have in the corridor and have contributed to GIS maps brought courses, workshops, and tour groups to of the corridor (A. Cruz, pers. comm.). the Center (soltiscentercostarica.tamu.edu). D. Texas A&M-Soltis Center (TAMU- Since 2007, geographers and other Soltis) researchers have been mapping and establishing Texas A&M opened its 117 ha Soltis Center benchmarks in the 100 ha of forest, gathering for Research and Education in 2009. It is baseline data on biota, making species lists, and located in San Isidro de Peñas Blancas, San collecting data at a meteorological station that Ramon, adjacent to the eastern border of CER posts real time on-line information (soltiscentercostarica.tamu.edu). TAMU-Soltis (soltiscentercostarica.tamu.edu). Monteverde seeks to: “train succeeding generations of Texas scientists have contributed to baseline research; A&M students with the aid of experiential, field- D. Hamilton and R. LaVal have collected based learning; catalyze and facilitate critical vertebrates, and B. Haber has collected insects and innovative research in the biological, for his Electronic Field Guide Project (D. physical, and social sciences; [and] serve as a Hamilton, pers. comm.). Most of the current major international location for research and researchers come from TAMU. The Director education in sustainability issues and wise encourages more researchers to use the site, as stewardship of natural resources" the site provides a unique and rich setting for

15 research and education activities (E. Gonzalez, The school is committed to Quaker values, pers. comm.). including "Stewardship: The school promotes an appreciation of and connection to the natural 10.8 Environmental Education in the world. By increasing our awareness of our Public and Private Schools interdependence with all life on earth, we strive A. EE in Schools of the Monteverde Area- to use water, land, and other resources mindfully Overview and wisely. Our resolve is enhanced by the EE in local primary and secondary schools natural beauty and biodiversity that surrounds include more attention to water and waste issues, us" (mfsschool.org/about-us). Students go on climate change, endangered species, and field trips to local reserves and educational sustainable living (Blum 2012). Primary nature exhibits. They carry out an independent schools (grades 1-6) supported by the project in their last year; e.g., following a stream government include two in Santa Elena and from its origin to the sea, investigating the local Cerro Plano and ca. 20 other in surrounding recycling program. High school students have towns. The Colegio Técnico Professional de organized recycling at the school. Santa Elena offers specialized programs or C. Cloud Forest School (CFS) majors in agriculture, ecological tourism, and The CFS, established in 1991, has 200 food services in addition to traditional academic students and is the only school in the area subjects (See Section 10.5). Their web page dedicated to "learning the language of a states: "The protection of nature and its sustainable future" through environmental resources are our principal objective in teaching" education and on-campus land stewardship. [colegiosanta elena.org; author's translation]. (cloudforestschool.org, Burlingame 2013). CFS There are also 3 private bilingual schools in the acquired its 46 ha campus through a loan from area: Monteverde Friends School (MFS), The the U.S.-based Nature Conservancy, to establish Cloud Forest School (CFS), and the Adventist legal precedents for conservation easements in School that are now accredited by the Ministerio Costa Rica. The easement put the farm (72% de Educación Pública (MEP: Ministry of Public forested) under strict protection. "Green Education). All area schools have basic Building" standards for new buildings were curricula, including Environmental Education, developed in 2003 and used that year in shaped by MEP. Teachers in the primary construction of the Gazebo or Kiosco (with schools still lack sufficient training and Monteverde's first solar panel) and all resources for EE and depend upon the EE subsequent construction (Burlingame 2013). Programs at the two cloud forest reserves (Blum Once CFS owned the land, they hired a 2012). CEAM (see below) helps coordinate EE steward to monitor land-use plans and work with activities. the EE Coordinator, staff, and volunteers to A new initiative in sustainable development integrate the curriculum with stewardship involving Colegio majors comes from a activities. By 2013, more than 14,000 native Monteverde Community Fund grant to the trees had been planted (M. Brenes, pers. Colegio in 2014 to help build a biodigestor to comm.). Volunteers have constructed and process animal waste from the agricultural maintained trails and mapped all the program, which will keep the waste out of reforestation areas (CFS Rainbow Spring 2014). regional streams and produce methane gas for An organic vegetable garden and farm, worm cooking in the Food Services Program composting facilities, 2 greenhouses, and native (monteverdefund.org/mcf-newsletter-January - plant gardens featuring a medicinal plant garden 2014). Students from the 3 high schools are and thematic gardens to attract bats, butterflies, involved in the Adopt-a-Stream program offered bees, hummingbirds, and birds provide by MVI for monthly monitoring of the health of additional EE resources. local streams. Environmental Education has always had a B. Monteverde Friends School (MFS) central role in CFS's curriculum. Recently, the MFS had 115 students in pre-K through 12th EE Coordinator introduced grade level themes grade in 2013-2014 (C. Evans, pers. comm.). based on the National Education for

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Sustainability, K-12 Student Learning Standards more than 40 active organizations in its network (L. Grenholm, pers. comm.; (ceammonteverde.weebly.com/integrantes.html). s3.amazonaws.com/usp_site_uploads/resources/ 123/USP_EFS_standards_V3_10_09.pdf). This 10.9 Conclusion: Lessons from is part of a "spiraling curriculum [that] allows Monteverde and Topics for Future Research for an interdisciplinary approach to learning A. Recommendations for Future Work about the environment, society, and economy for Environmental organizations and CFS students beginning at the age of 3" (CFS conservation activities are rich areas for Rainbow Fall 2013). Land stewardship is an historical analysis and documentation. Many of integral part of EE, and students care for their the organizations discussed in this Update are own campus daily; they have established a more than 20 years old; their early records are campus-wide recycling program. They also take deteriorating in quality. This history should be field trips to local reserves and educational preserved in digital form, preferably in a central nature exhibits. location. It would be ideal to have a single CFS is enrolled in the ICT Blue Flag electronic database with up-to-date-records and Program (L. Grenholm, pers. comm.). In 2013, live web-site links for all these organizations. CFS formed a new alliance with UNION AyA Santa Elena and ACAT based in Tileran VARSAN S.A., owner of a local sustainable have become important players in conservation, farm, to offer students opportunities for EE, and sustainable development; they are both internships, hands-on farm activities, and involved in MABI. The developments of these educational tours. The business is committed and emerging regional organizations (e.g., BBC "to offer young people a career alternative to and MABI) should be followed. EE programs tourism" (CFS Rainbow Spring 2013, G. started at MCL in 1986, at MCFP in 1992, and Vargas, pers. comm.). at CFS in the early 1990s. Those early students D. CEAM are now adults; the impacts of EE on their lives The Commission on Environmental should be assessed. Education of Monteverde (Comisión de Recommendations for special projects are: a) Educación Ambiental de Monteverde; CEAM) is a history of the Finca La Bella community; b) a cooperative group of environmental educators analysis of the evolution of issues and players formed in 2003 by the MCFP, SECFR, CER, related to water in the Monteverde area; c) ACAT, the local government, and local office of sustainable and organic agricultural experiments AyA (ceamonteverde.weebly.com). They in the zone; d) the developments of personal coordinate environmental activities, raise local networks linking conservation organizations and environmental consciousness, and contribute to their impact on building a base for consensus sustainability. From 2005-2009, they sponsored decision-making. an annual prize contest for ecological stories by There are many topics to explore in the students from 14 schools. The 15 best stories growth of Monteverde area tourism, beginning from all these years were published in 2014 with with an accurate estimate of the number of funding from the local government and BESA tourists in Monteverde to assess environmental (M. Díaz, pers. comm.). impacts, including water and waste. This is also CEAM, under the leadership of M. Díaz from critical to understand the impact of paving the MCFP and Y.M. Arias of SECFR, organized a road up the mountain. A study on the growth of 3-year training program for those concerned the area’s adventure tourism industry, and the with environmental issues and education. effects of the commission system, will show the Funded by ACAT and the US Fish and Wildlife sector's economic contribution to the Zone. Service, workshops involved 103 people from How sustainable are tourism businesses, and conservation organizations, local government, how do they define, value, measure, and and agencies in the region (Menacho 2010). implement sustainability? The answers to these ACAT's CREA (Comisión Regional de questions will come from carefully designed Educación Ambiental or Regional social science surveys and questionnaires, which Environmental Education Commission) has brings up another issue. MABI is in the process

17 of setting up a database of researchers and C. Successes of Conservation research in the sciences; social scientists should Organizations be included in this. Finally, this Update has 1. A traditional measure of conservation shown that large changes have occurred in the success is the amount of forest that has been last 15 years; there needs to be a mechanism to acquired. By 2014, BESA, MCFP, CER, add current information to this online Update at SECFR, Curi-Cancha, and CRCF had acquired least every five years. 27,650 ha; these reserves are part of the Arenal- B. Failures or Problems of Conservation Monteverde Protected Zone of 70,000 ha. Most Organizations of them are included in ACAT's 395,046 ha "There are multiple visions and practices of which have some measure of protection. environmentalism operating in a scene of 2. Local residents are employed by the complicated regional social, economic, political, reserves as unarmed guards; they try to build and ecological change" (Vivanco 2006). good relations with people living around the Conservation organizations have not made reserves while protecting wildlife and plants sufficient efforts to understand the differing from poachers. visions and practices. "The fact that many 3. The practice of linking forest patches to residents see the now-protected forests as off- protected areas via corridors has expanded limits to their recreation and use reinforces the beyond buying land. CRCF has been authority of the environmental organizations that establishing a corridor linking two protected police those lands, but fuels quiet talk by some areas, and BBC is establishing a corridor from people of future land invasions" (Vivanco 2006). the continental divide in Monteverde to the Gulf Another anthropologist discusses conflicts of Nicoya that includes people living in the area. between the values of conservationists and more 4. Reforestation in rural and more settled urban Costa Ricans in Sta Elena and Cerro Plano areas has continued through the efforts of many with their development associations and their organizations and projects. understanding of sustainability in more social 5. Environmental Education is part of the and economic terms (Blum 2012). Some Costa curriculum for primary and high schools. Ricans have resented a lack of access to Numerous groups have provided EE for local scientific research information generated in schools and for the broader community. For Monteverde but available only in English and in example, in June 2014, CEAM, the University locally inaccessible specialized journals (Blum of Costa Rica (UCR), and the National 2012). University of Costa Rica (UNA) organized an Some think that the rapid development of all-day Water Fair (Feria del Agua) in Sta Elena. tourism, especially adventure tourism, is Almost all the conservation organizations destroying what was special about Monteverde. discussed in this update had multiple Crowds of tourists in MCFP and other tourist representatives with tables full of literature, destinations, billboards, and heavier traffic are posters, and small give-aways. Water was the associated problems. In addition, tourists and central focus of lectures, workshops, the population increase they caused have demonstrations, and lots of fun educational strained water supplies, increased amounts of activities for children, who packed the place. waste, and burdened infrastructure. Other forms of EE have expanded in the Financial stability remains a persistent institutions for foreign university students, in problem for many of the conservation guided tours of reserves, and in educational organizations in Monteverde. Problems were businesses with animals and orchids. magnified with the global economic downturn 6. Organizations have continued to emerge: a by 2009; for Monteverde, this involved local government, a cooperative group to solve decreases in tourism and international donations. garbage and recycling problems (COMIRES), a Organizations are aware that they need to Community Fund, the CRCF, ProNativas, the develop endowments and more stable sources of BBC, and MABI. Volunteers serving on funding. committees and on each other’s Boards link these organizations to each other and to

18 continuing organizations. Monteverde's submit copies of their articles or opt for open conservation organizations occupy different access to their publications (L. Kutner, pers. niches and do not compete with each other. comm.). The successes of conservation organizations D. The Monteverde Zone and its in these areas have been possible because of the Conservation Organizations as Models following factors (Burlingame 2000): Simply copying Monteverde and its 1. Resident and visiting scientists provided conservation organizations and applying these basic and applied knowledge that led to the activities elsewhere is problematic because of formation and growth of conservation the unique elements in Monteverde and in Costa organizations and their programs. Rica. However, some of the conservation and 2. Economic prosperity and a diversified educational organizations can serve as models. economy supported the development of Monteverde's successes with ecotourism as a conservation organizations and made an way to support conservation organizations and educated middle class a reality. Since 2000, the development of ecotourism businesses can tourism has surpassed agriculture as the main serve as a model for certain locations. economic driver. The Monteverde-Arenal Bioregion Initiative, 3. Successive immigrants brought new launched in 2014, proposes to extend the perspectives, skills and knowledge, starting with synergisms of the Monteverde area that have the Costa Rican settlers, followed by the contributed to its successes in research, Quakers, then the biologists, the tourists and conservation, and education to the larger business people, civic leaders, educators, and bioregion around it. artists to create what the 2013 session at the E. "Human Voices Around the Forest" ATBC called "The Perfect Storm: Educational, E. Vargas' update to his (essay), "Human Conservation, and Community Synergisms for Voices Around the Forest" offers a concluding Tropical Ecology Research in Monteverde, vision of promises and challenges to Costa Rica." conservation successes: 4. Monteverde's conservation organizations “As neighbors living around the protected and the people who support them have been able areas, we enjoy the beauty of landscape, the to change as conservation thinking evolved from pureness of water and air, the peace of the bird’s a focus on preserving particular endangered songs; but it also implies a responsibility: to care species to concern about threats to biodiversity for this natural richness, as the source of life and to today's more general challenge of climate admiration for all creatures, among them, human change and need for ways to implement beings. For this purpose, it is essential that our sustainable development. They learned how to short and medium term actions be framed by an tap into outside sources of funding and steer integral, long-term vision. benefits of tourism to conservation and "The conservation organizations and the sustainable development ends. The government highlight the extension of protected organizations have shown resiliency and forest as proof of conservation success in resourcefulness; their success has been possible Monteverde and Costa Rica. However, we do because of dedicated, hard-working, and creative not know if in a few decades, these people. organizations will have the capacity and the 5. Information access has been improving. necessary resources to ensure the protection of Having the Monteverde book and Updates such a large area. Will they be able to do it available on the Internet in English and Spanish without the participation and support of the with free access will be a major contribution. people living around these forest reserves? The proposed online MABI database will also be What will be the future pressures on these areas? important. MVI's library has been building a Other actor’s voices are being heard, from the digital collection and has created an electronic inhabitants of nearby communities (e.g. list of MCFP's library holdings. MVI has an Guacimal, Chachagua) defending their water offprint collection, but they are missing many sources for human consumption from the agro- articles; researchers need to be encouraged to industry and tourism developments pushing for

19 water concessions. Furthermore, public and CFSF: Cloud Forest School Foundation private hydroenergy companies are creating CIEE: Council on International Educational more pressures as they construct dams on Exchange various rivers whose main water sources are in COMIRES: Comité de manejo integral de the Monteverde Reserve Complex. residuos sólidos [Solid Waste Management "These cases offer an idea of the big Committee] challenges for the conservation organizations, CRCF: Costa Rican Conservation Foundation governments, educational institutions, CST: Certification for Sustainable Tourism community leaders, farmers and enterprises of [from ICT] the region. Enduring sustainability will depend EE: Environmental Education on the will among all organizations and actors ESP: Environmental Service Payments involved to maintain and improve the FCER: Friends of the Children's Eternal collaborative work relationships that have Rainforest [previously MCLUS] distinguished our communities." ICT: Instituto Costarricense de Turismo [Costa Rican Tourism Board] MABI: Monteverde-Arenal Bioregion Key to Acronyms Initiative MCF: Monteverde Community Fund ACAT: Area de conservación Arenal- MCFP: Monteverde Cloud Forest Preserve Tempisque [Arenal-Tempisque Conservation MCL: Monteverde Conservation League Area; previously ACA] MEP: Ministerio de Educación Pública ATBC: Association for Tropical Biology and [Ministry of Public Education] Conservation MFS: Monteverde Friends School AyA: Acueductos y Alcantarillados [Costa MINAE: Ministerio del ambiente y energía Rican Water and Drainage Institute] [Ministry of the Environment and Energy] BBC: Bellbird Biological Corridor MVI: Monteverde Institute BESA: Bosqueterno, S.A. [Eternal Forest, OTS: Organization for Tropical Studies Inc.] SECFR: Santa Elena Cloud Forest Reserve CASEM: Cooperativa de Artesanías de Santa SINAC: Sistema nacional de areas de Elena-Monteverde [Crafts Cooperative of conservación [National System of Santa Elena and Monteverde] Conservation Areas] CEAM: Comisión de educación ambiental de TAMU-Soltis: Texas A&M University Soltis Monteverde [Commission on Environmental Center for Research and Education Education of Monteverde] TSC: Tropical Science Center CER: Children's Eternal Rainforest UGACR: University of Georgia, San Luis [previously BEN in English] Costa Rica CFS: Cloud Forest School [previously CEC in English]

Sources

Acknowledgments: This Update was made possible by very generous help from many individuals who provided essential oral and documentary information and/or detailed helpful feedback on drafts. I especially thank: Yaxine Maria Arias, Pedro Belmar, Wendy Brenes, Bob Carlson, Mercedes Díaz, Carol Evans, Ashley Gora, Eugenio Gonzalez, Laura Grenholm, Debra Hamilton, Patricia Jiménez, Richard LaVal, Bob Law, Fran Lindau, Julia Lowther, Alan Masters, Karen Masters, Yoryineth Méndez, Nalini Nadkarni, Quint Newcomer, Alan Pounds, John Trostle, Sue Trostle, Katy VanDusen, Eugenio Vargas, Justin Welch, Jannelle Wilkins, and Willow Zuchowski.

NOTE: Most of the sources for this Update are “gray literature,” unpublished computer generated reports, newsletters, and documents available from the organizations that produced them. Also, most all of the organizations discussed in this

20

Update have websites with extensive information and Facebook pages; most of these are not listed below since they are easy to find and subject to change.

Association for Tropical Biology and Conservation Costa Rican Tourism Institute (ICT). 2014. (ATBC). 2013. The Perfect Storm: Educational, www.visitcostarica.com/ict/paginas/ Conservation, and Community Synergisms for sostenibilidad. Tropical Ecology Research in Monteverde, Cresson, O. 2013. Blossoming and Building at Finca La Costa Rica. Bella. Quaker Earthcare Witness. 26(2.). atbc.confex.com/.../2013/webprogram/.../ www.quakerearthcare.org/article/blossoming- ATBC-OTS-2013_Progra...S-11 (June 25). and-building-finca-la-bella. Blum, N. 2012. Education, Community Engagement and Dyer, Z. 2014. Costa Rica remains most popular Latin Sustainable Development. Negotiating American study abroad destination. Environmental Knowledge in Monteverde, Costa ticotimes.net/2014/05/23/costa-rica-remains-most Rica. Springer, London, UK. popular ... Bosqueterno S.A. 2010. Bosqueterno, SA. Escofet,. G. 1998. One million visitors by 1999? The Tico http://bosqueternosa.wordpress.com. Times, San José, Costa Rica, 2 October. _____. 2014. Bosqueterno [poster by K. Johnson, R. _____. 1998. Tourism boom shows slump over. The Tico Guindon, J. Welch for the Monteverde-Arenal Times, San José, Costa Rica, 19 June. Initiative Conference]. BESA, Monteverde, Ewing, T. 2007. Community development and capacity Costa Rica. building: A case study of Monteverde, Costa Burlingame, L. 2000. “Conservation in the Monteverde Rica. Sociology-Dissertations. Paper 6. Zone: Contributions of Conservation http://surface syr.edu/soc_etd/6. Organizations.” Pages 351-388 in N. Nadkarni Friends of the Children's Eternal Rainforest (FCER) and N. Wheelwright, editors. Monteverde: [previously called Monteverde Conservation Ecology and Conservation of a Tropical Cloud League US (MCLUS)]. 2003 to date. Annual Forest. Oxford University Press, New York, USA Report. www. friendsoftherainforest.org. _____. 2002. Evolution of the Organization for Tropical Gora, A. 2013. Sustainable tourism norm transfer and the Studies. Revista de Biología Tropical 50(2): 439- case of Monteverde, Costa Rica. Senior Thesis. 472. Lake Forest College Publications. _____. 2015. History of the Monteverde Institute. http://publications.lakeforest.edu/seniortheses/7/ Lancaster, Pennsylvania, USA. [Lake Forest, Illinois, USA]. _____. 2013. A Short history of the Cloud Forest School Guindon, L., M. Moss, M. Rockwell, J. and S. Trostle (CFS) in Monteverde, Costa Rica. Lancaster, (eds.). 2001. Monteverde Jubilee Family Album. Pennsylvania, US. R.B. Sibaja, Monteverde, Costa Rica. _____. 2013. Short history of the Monteverde Conservation Haber, W., W. Zuchowski, and E. Bello. 2000. An League and the Children's Eternal Rainforest. introduction to cloud forest trees: Monteverde, Lancaster, Pennsylvania, USA. Costa Rica (2nd ed.). Mountain Gem Centro Cientifico Tropical (photos by B. Cole). 2006. Publications, Monteverde de Puntarenas, Costa Reserva Bosque Nuboso Monteverde. CCT, San Rica. José, Costa Rica. Honey, M. 2008. Ecotourism and sustainable development. Chornook, K. and W. Guindon. 2007. Walking with Wolf: (2nd. ed). Island Press, Washington, D.C., USA. reflections on a Life spent protecting the Costa Institute of International Education. 2014. Open Doors Rican wilderness. Wandering Words Press, Data. U.S. Study Abroad: Leading Destinations. Hamilton, Ontario, Canada. iie.org/Research-and-Publications/Open- Cloud Forest School Foundation (CFSF). 1997- date. Doors/Data/US-Study-Abroad/Leading- Rainbow [newsletter] CFSF, Sewanee, Destinations/2010-12. Tennessee, USA. cloudforestschool.org since Koens, J., C Dieperink, M. Miranda. 2009. Ecotourism as a Fall 2011. development strategy: experiences from Costa Cloud Forest School (CFS/CEC). 1992 to date. Board Rica. Environment, Development, and reports to the General Assembly. CFS, Sustainability 11(6) 1225-1237. Monteverde, Costa Rica. link.springer.com/article/10.1007/s10668-009- _____. 1995 to date. Director’s Reports to Board and to 9214-3. Assembly. CFS, Monteverde, Costa Rica. Law, B., R. LaVal, and W. Zuchowski. 1998. Bajo del Comisión de educación ambiental Monteverde (CEAM), Tigre guide. Monteverde Conservation League, editors. 2014. Cuentos ecológicos de Monteverde, Costa Rica. Monteverde. CEAM, Monteverde, Costa Rica. Lonely Planet, N. Cavalieri, A. Skolnick, W. Yanagihara. Corredor Biológica Pájaro Campana. 2011. Plan estratégico 2012. Lonely Planet: Discover Costa Rica (2nd. 2011-2016. www.cbpc. ed). Lonely Planet Publications Pty Ltd., n.p. Costa Rican Conservation Foundation. 2012-date. Madrigal, A. 2014. Tourist Flocked to Costa Rica in www.fccmontverde.org. Record Numbers in 2013. The Tico Times. www.ticotimes.net/2014/01/17/tourists-flocked....

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McCandless, S. 2008. Partial Power, Partial Knowledge: Vivanco, L. 2006. Green encounters: shaping and Accounting for the Dis-Integration of a Costa contesting environmentalism in rural Costa Rica. Rican Cooperative. Society and Natural Berghahn Books, New York, USA. Resources, 21 310- 323. Welch, J. 2007. Monteverde-Nicoya Biological Corridor: academia.edu/386148/Partial_Power_Partial_Kn Biophysical Analysis, Socio-Economic owledge ... Description and Project Cost Summary. Menacho, R.M. 2010. Programa de capacitación UGACR, Monteverde, Costa Rica. interinstitucional para la comisión de educación Wilkins, J. 2011. Educational and volunteer tourism in ambiental y educadores de Monteverde. Monteverde, Costa Rica. from Proceedings of 3rd Biocenosis 23(1):14-21. International Travelers' Philanthropy Conference. Méndez, Y. 2009. Plan de manejo de la Reserva biológica Travelersphilanthropy.org San Luis, Monteverde, Costa Rica. Proyecto final Zuchowski, W. 2004-2009. ProNativas Year End Report. ... por el titulo de Máster en Liderazgo y Gerencia Monteverde, Costa Rica. Ambiental otorgado por la Universidad para _____. 2007. Electronic Field Guide to Native Ornamental Cooperación Internacional (UCI). UCI, San José, Plants of Monteverde, Costa Rica. EFG Project, Costa Rica. U. Mass. Boston, USA. Monteverde Conservation League (MCL) 1987-date. (efg.cs.umb.edu/efg2/TypePage.jsp). Annual Report/Informe anual. MCL. _____. 2007. Tropical Plants of Costa Rica: A Guide to Monteverde, Costa Rica. acmcr.org since 2008. Native and Exotic Flora. Distribuidores Zona _____. Bulletin. 2009-date. MCL. www: acmcr.org. Tropical, S.A., Miami, Florida, USA. Monteverde Friends School (MFS). 2014. Profile 2013- _____. [2011]. The ProNativas Network. pronativas.org. 2014. MFS, Monteverde, Costa Rica. Monteverde Institute (MVI). 1993-date. Actas. MVI, Monteverde, Costa Rica. _____. 1987-date. Annual Report/Informe anual. MVI, Monteverde, Costa Rica. _____. 1987-date. Executive Director's report to General Assembly MVI, Monteverde, Costa Rica. Nadkarni, N. and N. Wheelwright, editors. 2000. Monteverde: Ecology and Conservation of a Tropical Cloud Forest. Oxford University Press, New York. Reserva Biológica Bosque Nuboso de Monteverde (RBBNB). 2005. Plan de manejo de RBBNM. www.reservamonteverde.com/documentos. _____. 2008. Plan program educación ambiental. www.reservamonteverde.com/documentos. _____. 2009. Plan estratégico de investigación 2010-2020. www.reservamonteverde.com/documentos. _____. 2014. Programa investigación RBBNM. Centro Cientifico Tropical, San José, Costa Rica. Stocker, K. 2013. Tourism and Cultural Change in Costa Rica. Lexington Books, Lanham, UK. University of Georgia Costa Rica (UGACR). 2010, 2011- 12. Sustainability Report dar.uga.edu/costa_rica/index.php/site/ sustainability_initiatives. _____. 2014. Sustainability Report. static.externalaffairs.uga.edu/costarica/UGACR_ Sustainability_Report_ 2013.pdf. _____. 2013. Strategic Plan 2011-2012. dar.uga.edu. _____. [2014]. Research Opportunities at UGA Costa Rica. UGACR, Monteverde, Costa Rica. U.S. Partnership for Education for Sustainable Development. 2009. National Education for Sustainability K-12 Student Learning Standards. Version 3. s3.amazonaws.com/usp_site_uploads/resources/1 23/USP_EFS_standards_V3_10_09.pdf.

11 Agriculture in Monteverde, Moving Toward Sustainability — Update 2014

Joseph D. Stuckey, Fabricio Camacho C., Guillermo Vargas L., Sarah A. Stuckey, and José Vargas L.

1. Introduction (generally) drier, and in recent years, weather The agricultural systems and sustainability events (rain, drought, and wind) have become issues described in the late 1990s remain more severe and their timing less predictable.2 relevant 15 years later. However, because land Monteverde’s production and consumption use patterns respond to dynamic social and patterns are increasingly dependent on global economic conditions, change is taking place on markets, prices, and international regulations. the margins of Monteverde’s land use economy. Small but growing numbers of landowners are This 2014 Addendum to Chapter 11, implementing more ecologically, socially, and “Agriculture in Monteverde, Moving Toward economically sustainable practices. Dairy Sustainability” outlines the direction of these changes, and identifies key global and local 2 Trade winds are a hallmark of dry season; they trends that appear to drive this change. We produce generally drier conditions on the Pacific comment on: economic trends (J. Stuckey), slope and wetter conditions near the continental climate change (F. Camacho), dairy (J. Stuckey), divide. As cloud water is intercepted at the peaks, the coffee (G. Vargas), and integrated farms (F. winds flow down the Pacific slope drying out the Camacho). Table 11.1 presents a list of people landscape, and preventing Pacific moisture – the interviewed. 1 source of the region’s heavy rains – from ascending. 2. Summary Shifts in trade wind patterns, whether linked to ocean Climate in the Monteverde bioregion is temperature cycles, changes in the jet stream or other changing, and Monteverde’s economy is phenomena, can produce dramatic local effects. When trade winds occur in rainy season, as has becoming increasingly integrated with global happened with some frequency in recent years and commerce. The climate is becoming warmer and notably in 2013 and 2014, we see extreme local variations: more moisture on the Atlantic slope; and on the Pacific slope, wetter highlands and more 1 Each of the authors is a long-term Monteverde drought in the lowlands. Generally we see more days resident. Where possible, the information reported in of drought, but more intense rainy days, where in a this addendum is based on peer-reviewed literature. very short amount of time it may rain most of the However, most of the observations about the local water of the month, as happened in May 2014 (F. economy are based on interviews with local farmers Camacho and J. Stuckey, pers. comm.). and community leaders.

farmers have adopted some new technologies; integrated farms and gardens provide produce their economic future remains uncertain as they for local markets. Several farmers have linked face global competition, rising land prices, and their farming activities to eco-tourism; some demographic shifts. Coffee production patterns coffee farmers are marketing farm-branded may shift as climate warms; many small products directly to clients. producers have developed synergies with eco- and educational tourism as a survival strategy. 3.1 Demographic Trends A population estimate based on extrapolation 3. Economic Trends of potable water connections administered by Two key forces are shaping the Monteverde local community water associations, region’s economy.3 First, international free trade (Acueductos y Alcantarillados, popularly known agreements are opening Costa Rica to global as AyA) indicates that Monteverde and competition, which puts small producers and surrounding communities comprise on the order businesses at a disadvantage relative to large of 5,000 to 8,000 inhabitants, not including scale, capital intensive ones. Second, the local “floating” tourist populations (V. Molina, pers. grafting of a tourist economy into an agrarian comm.) See Table 11.2. economy has created population growth, with The area has experienced immigration of accompanying pressures and opportunities that people from diverse socio-economic and cultural influence land use. Monteverde’s tourist backgrounds. Youth are increasingly mobile. economy grew at a phenomenal, although The area is undergoing cultural blending, which undocumented, rate until the 2008 global is associated with the value of English as an economic downturn. As the population and tax economic language, the effect of local private base have grown, infrastructure and access to schools, and educational tourism. public services have expanded. This, and The social and economic effervescence increased use of digital and other technologies, surrounding land use decisions contributes to has increased quality of life, in the sense that five trends: producers and consumers have more choices 1) Tourism has created economic opportunities than before.4 The use of cell phones, internet that drive increased population through banking, and credit and debit cards is prevalent. immigration and retention of local youth Three banks, three milk processors, two who stay in the area. This increases supermarket chains, and several national food urbanization pressure, which drives up land and beverage distributors operate in the area. prices first in communities closest to urban With the exception of eggs, most of the food and centers, and then, more gradually, in fresh produce consumed locally comes from outlying communities. outside the area. 2) Squeezed by the economics of global trade, Countering this increased commercialism, some farmers have ceased commercial some Monteverde residents seek to produce and farming, while others are increasing the consume food that is grown with scale of their businesses, adopting new environmentally and socially sustainable technologies or market niches to remain practices. A small but growing number of economically viable. 3) Youth increasingly pursue secondary and 3 We use the term “Monteverde” as defined in university education, which increases their Chapter 1, section 1.1, and in Chapter 11, p. 390 of mobility. Although some leave the area, the the 2000 publication. growing economy has provided jobs or 4 The area’s growing commercial activity has business opportunities that attract others to contributed to changing lifestyles. As a simple stay. function of access to services and opportunities, 4) Youth are leaving the farms. Older farmers quality of life has generally (but not uniformly) may remain tied to the land by culture or by increased. It would be interesting to study perceived necessity, or may sell their land. This raises changes in quality of life if “quality of life” were to be measured by other indicators, for example a central question: in the future, who will “happiness”. own the land, and how they will use it? Land

subdivision for residential or commercial 3.3 Tourism purposes is occurring in some communities, Commercial tourism in Monteverde has whereas in some cases, new landowners generated substantial wealth and jobs, and has develop integrated, diversified farming created important local synergies for economic systems. opportunity. Some land-owners have abandoned 5) The wealth generated during tourism’s farming to establish tourist businesses; others boom years has led to changes in the have integrated some tourism activities into their lifestyles of many residents and in the values farms. But tourism has not been a stable of voluntary cooperation for the common economic model: it is vulnerable to world good. This change is evident in the growth events, and to boom-bust cycles. Monteverde’s of consumerism, which, with the advent of tourism is characterized by seasonal fluctuations lean years in the economy has led to in visitation rates, and by intense competition unsustainable debt levels for many entities, among local businesses. This results in the and can lead to more social problems, in payment of high commissions to booking addition to the existing cases of agents, which drives up prices and reduces bankruptcies, foreclosures and Monteverde’s competitiveness as a destination. unemployment. Financial institutions have Availability of jobs in the tourist sector tends to facilitated this trend through their lending reduce the number of people available for farm policies, and by aggressively popularizing work. the use of credit cards. Educational tourism seems to be a stabilizing feature of Monteverde’s tourism, and a growing 3.2 Commercial Trends market segment. Several universities have Local farm production costs are closely tied campus facilities, staff, and/or programs to international petroleum and basic grains operating in the area (see Chapter 10’s prices, but due to the particular dynamics of addendum for more details on Costa Rica’s small economy, input prices tend to “Environmental Education and Sustainability rise quickly and fall slowly in response to at the University/College Level Primarily for international price fluctuations. Dramatic Students from North America”. Beyond fluctuations in international dairy prices have providing jobs and markets for farm products destabilized production and marketing plans university people and programs have shared (González 2008, Montero 2013, J. Vargas, pers. information and provided assistance that comm.). influence local attitudes and practices linked to Implementation of free trade agreements, land use. principally with the United States and the European Union will end protective tariffs on 3.4 Institutional Evolution imported dairy and other goods, and obligate Monteverde’s first District Municipal Costa Rican producers and exporters to conform government was elected in 2002. It and to rigorous international standards. The Costa subsequent administrations failed to adopt land Rican government has increased its enforcement use planning, but did increase the amount of of environmental and sanitary regulations. Trade revenue for local development. National agreements have paved the way for transnational institutions continue to expand services, tax companies to buy local businesses that decide to collection, and enforcement of health, sell rather than compete. Since the early 2000s, environmental, and other regulations. having tied Costa Rica’s economic aspirations to By 2014, the Ministry of Agriculture (MAG) international commerce, government plays three roles for Monteverde agricultural administrations have relied on information producers. Nationally, it monitors compliance technology and tourism as economic with international trade standards, e.g., by centerpieces, and have not articulated strong certifying that herds are brucellosis-free, and agricultural development and food security issuing the Veterinary Operating Certificate policies. (Vargas 2009, and J. Monge, pers. (CVO), which is required to commercialize farm comm.). products (J. Monge and J. Álvarez, pers.

comm.). Monteverde’s local MAG officials help dynamics. These variations are expressed farmer organizations gain access to government through the emergence of new disease vectors funds for special projects, and offer technical that have appeared to contribute to the extinction assistance in dairy, coffee, horticulture, of species such as the golden toad (Incilius aquaculture, and agro tourism. MAG’s periglenes) and the harlequin frog (Atelopus sp., assistance responds to demand rather than to Pounds et al. 2006), and through the decline of national planning priorities, and is constrained other amphibians and the presence of invasive by a limited budget (J. Álvarez and J. Martín, species representative of warmer lowland pers. comm.). climates in the cloud forest. SENARA (Servicio Nacional de Aguas One would expect that just as changes have Subterráneas, Riego, y Avenamiento – the occurred in the dynamics of natural ecosystems government agency that supervises subterranean in Monteverde, changes would also have water, irrigation, and drainage) and MAG occurred in the production patterns of promote agricultural irrigation schemes in agricultural processes. However, no specific several communities in the Monteverde region. analyses of the impact of climate variability on MAG and INEC, Costa Rica’s National Institute local production exist, so it is imperative for Statistics and Census, are conducting a document this information. national agricultural census, which may signal Global and regional projections indicate that increased government commitment to develop a change in the main climatic variables is national agricultural sector plan (Martín 2014). imminent even under the most drastic scenarios Locally, the Monteverde Milk Producers’ for mitigation and reduction of emissions of Association (APLM) has gradually expanded carbon dioxide and other greenhouse gases sale of farm supplies and technical assistance (IPCC 2007, 2013, Anderson et al. 2008), provision. Productores de Monteverde, S.A., the therefore it may be concluded that Costa Rica’s cheese plant that was founded by the Quakers in climate will be subjected to dry and rainy 1953, supported the National Milk Producers extremes (IMN 2008). Locally, when comparing Chamber’s efforts to influence national dairy the average rainfall between 1961 and 1990 with policies and free trade agreement negotiations. the average projected under the A2 scenario In 2013, Productores de Monteverde S.A. was (according to the IPCC nomenclature) between sold to the Mexican transnational conglomerate 2071 and 2100 for the mountainous region of the Sigma Foods, and continues to operate locally. Tilarán mountain chain, that variable will After decades of having been the only company decrease by 17% (IMN 2008). Maximum buying milk in the area, it now competes for temperature will rise an average of 6.39 ° C local milk with Dos Pinos, Costa Rica’s large while the minimum temperature will also suffer dairy cooperative, and Coopeleche, a regional an increase of 2.88 ° C (IMN 2008). dairy cooperative that sells its milk to Florida This new climate scenario may be perceived Farm and Ice, a transnational beverage as a threat or an opportunity for agricultural company. In 2013, CoopeSanta Elena failed, and production in the Monteverde area, as the future in 2014 Coopeldos struggles to survive. distribution of the climatic conditions of the 4. Agricultural Production in the Face of region can reduce or increase the productive Climate Change in Monteverde capacity of the currently installed systems. For By Fabricio Camacho C. example, coffee production in the region is shifting towards higher altitude areas such as 4.1 Trends Cañitas and Las Nubes. This could represent a Critical signs of climate change in the better business opportunity for producers in Monteverde area are trends toward an increasing these communities but also could mean direct number of dry days, and the gradual increase in competition or displacement for producers in minimum temperatures (Pounds et al. 2006) and lower areas such as San Luis, where plantations of precipitation in the highlands (IMN 2008). might be more prone to disease and to receiving These and other non-documented trends have lower market prices because of lower quality caused important changes in ecosystem coffee.

change, which would differentiate Monteverde’s 4.2 Adapting to Climate Change economy, may be a selling point for tourism. It The future success of Monteverde’s would generate important links in the local agricultural production will depend on the production chain that might be organized capacity and speed of local producers to adapt to through the creation of an entity that coordinates new climatic conditions. For example, coffee logistics so that producers can connect directly producers in warmer areas could incorporate with consumers. In any case, it is important to agroforestry techniques, combining production begin adapting agricultural activity to a model of of shade grown coffee interspersed with food clean and sustainable production that is closely crops and high value forest trees that allow linked to the market and that guarantees the producers to generate food for the household and sound management of natural resources, ensure a more resilient system that could ensuring a balanced development of production compensate for the lower yield of coffee. Some systems that meets but does not exceed the producers in San Luis have established carrying capacity of the land and the needs and agroforestry systems for shade grown coffee, aspirations of producers and consumers.5 although these are motivated by cultural and economic reasons, rather than as a climate 5. Dairy change adaption. However, these systems are By Joseph Stuckey more natural, less dependent on external inputs, and resemble traditional plantations and home 5.1 Economic Trends gardens, which make them more attractive to Dairy farmers are being squeezed by rising rural tourism and better adapted to climate costs. They face the threat of stagnant or falling change. milk prices as protective tariffs on dairy imports Other important factors that influence the are eliminated, even as the amount of capital level of success of future agricultural production needed to stay in business rises. These trends include: 1) the level of producer innovation to favor large producers over small ones. acquire technology that allows them to be competitive without exceeding the land’s 5.1.1 Climate Change carrying capacity; 2) access to information and Between 1999-2014, water production of 14 technical support from government and private springs supplying the Santa Elena Acueductos y organizations to help producers develop Alcantarillados (AyA) potable water system balanced systems; and 3) the ability to develop fluctuated in 2-3 year cycles that seem new market opportunities that recognize the real responsive to the El Niño and La Niña warming value of local production. and cooling events, which produce drier and Demand for food by Monteverde’s tourism wetter conditions locally (A. Sandí: unpubl. sector, and by the local population, represent two opportunities to capitalize agriculture. Except for a few small distributors of foods such as eggs, chicken meat, and vegetables, Monteverde currently has no direct, robust 5 “Clean” production refers to a world- wide connection linking agricultural producers, movement for “cleaner production” based on residents, and tourists, so the majority of its producing services and goods in an environmentally foodstuffs come from other regions, even though responsible way, by mitigating and minimizing the area has adequate conditions to produce negative impacts such as water pollution and GHC fresh food that could be absorbed by the local emissions. One definition for cleaner production: market. “Manufacturing process minimizing waste and Monteverde has the potential to increase local applying continuous prevention practices. These produce consumption, but this will require a method[s] include (1) raw materials and energy conservation, (2) toxic inputs elimination or cultural change by households and commercial reduction, and (3) toxic outputs reduction or consumers (supermarkets, grocery stores, hotels elimination” (http://thelawdictionary.org/cleaner- and restaurants) to consume local products. This production/).

data, Santa Elena AyA, pers. comm.).6 Although years, starting in 2016. Falling tariffs will affect most do not keep weather records, farmers milk prices to farmers. To comply with comment that in drier years, higher elevation international norms, farmers are also required to clouds reduce the beneficial effect of dry season invest in new technology and management mist, making dry seasons more intense and practices. slowing pasture growth for upland farms that normally receive this precipitation. However, in 5.1.4 Land Ownership Succession the drier years (e.g., 2013), farmers report that The trend of youth leaving the farm is an increased number of dry sunny days in rainy especially significant for dairying because: a) season favor pasture growth. The drier years are more people in Monteverde directly or indirectly associated with strong, un-seasonal, easterly depend upon dairying than on other types of winds. When such winds occur in rainy season, farming, and b) the success of dairy farms they prevent the Pacific moisture that normally depends on the quality of daily management, produces heavy rains from reaching which is more difficult to achieve when Monteverde, and exert chilling and mechanical delegated to hired labor. effects that slow pasture growth. In recent years, rainfall has tended to be concentrated in fewer, 5.2 Farm Production Trends but larger events, so that although total annual By 2014, the number of small farms rainfall may decline only modestly, more water producing milk had declined significantly. In the runs off, causing increased erosion and aquifer 1990s 17 farms in San Luis sold milk to the depletion. (F. Donato and J. Monge, pers. dairy plant; by 2014, only four remained (J. comm.). Fuentes, pers. comm.). Factors that contributed to this trend include: requirements to install on- 5.1.2 Dependence on Supplemental Feed farm refrigeration and other technologies, rising Grains production and transportation costs, rising land Farmers and local agricultural professionals values, opportunities for on-farm diversification report that the amount of supplemental feed or for off-farm employment, and demographic grain being used to produce a kilo of milk may shifts. During the same period, herds on some of have increased in recent years. Although we the more specialized farms grew in an effort to found no local studies to test this perception, if become more efficient. true, it would suggest that the profitability of In both lowland and highland dairies, all dairy farming may have declined, both because farms use refrigeration equipment and nearly all it is more expensive to produce milk using use milking machines. About 95% of the milk is imported feed grains than using farm-grown transported in tank trucks. Many farms have forages, and because the cost of grain has risen installed concrete cow paths to reduce erosion. relative to the price of milk (Montero 2008 and Many farmers have improved their barns and Vargas 2009). pasture irrigation systems in response to waste regulations. Nearly a dozen farmers use bio digesters and/or earthworm composting systems 5.1.3 Impact of Free Trade Agreements to process animal waste. Electric fences are Costa Rica’s milk prices have exceeded increasingly used to manage grazing. Farmers world milk prices in recent years (Montero use motorized backpack sprayers to apply 2013), and its dairy industry has been protected herbicides, pesticides, and foliar fertilizer; weed- by tariffs amounting to 65% of the value of eaters have mostly supplanted the machete for imported dairy products. The Central American cutting weeds. Some use harvesting machines to Free Trade Agreement (CAFTA) requires cut forage. Larger farmers keep computerized elimination of dairy import tariffs over nine financial and reproductive health records. (J. Monge and A. Murillo, pers. comm.).

6 Santa Elena draws water from 26 springs, and new sources are constantly being sought; long term production data only exist for the 14 older springs.

5.3 Highland Dairy Production Trends Between the late 1990s and 2014, average 6. Coffee in the Local Economy highland milk production increased by 60% to By Guillermo Vargas L. about 16 kg per cow per day. Over the same period, the amount of land in production As with other agricultural products and declined, while stocking rates increased slightly. processes, the region’s coffee economy is Jerseys became the predominant highland breed, changing. With the disintegration of CoopeSanta significant because Jersey milk contains more Elena and the proliferation of brands and solids than other breeds, and the milk price is marketing channels for Monteverde’s coffee, linked to milk solids content. These trends seem there are no data available to quantify coffee to result from increased use of supplemental production in 2014, but an outline of the history feed grains, supplemental forage feeding in dry and current patterns of coffee production can season, and genetic improvement through provide insights on its future. artificial insemination (J. Monge and A. Murillo, pers. comm.). 6.1 Before 1950 The families who settled in the Monteverde 5.4 Lowland Dual Purpose Dairy-beef region in the first quarter of the twentieth Production Trends century came mostly from the western part of Over the same period, lowland milk Costa Rica’s Central Valley. These families production increased about 142%, rising from brought with them the culture of coffee ca. 4.5 kg to 10.9 kg per cow per day, an production and consumption. increase associated with fundamental changes In the 1940s, several families in San Luis and that were made in the production system: Los Cerros produced enough coffee to sell part planting improved grass varieties; increased of the harvest in Las Juntas, and to the roaster cross breeding of beef breeds with higher Café La Moderna in Puntarenas. Coffee berries production, heat resistant dairy breeds; increased were dried on farms and then peeled by hand in use of feed grain supplements; transition from a wooden pestle. Transportation by horse to Las once-a-day to twice-a day-milking; expanded Juntas, and by oxcart and boat to Puntarenas, use of parasite controls; increased use of electric was slow and arduous. Coffee was not a viable fences; and on some farms, installation of economic option for local residents until the irrigation systems to improve pasture growth. By early 1950s, when one of the settlers, Ramón 2014, lowland farmers had not adopted the Brenes, commercially developed the cultivation practice of applying fertilizer to pastures (J. and processing of coffee on his own farm. The Monge and A. Murillo, pers. comm.). abundant water and better sun in the lower part of San Luis created the opportunity to set up a 5.5 Efficiency mill at the confluence of the San Luis and Increased production per cow per day in both Guacimal rivers. highland and lowland areas is associated with better management and increased use of various 6.2 From 1950 Through the Mid ‘80s energy inputs. However, it seems probable that From 1950 to 1980, coffee became the main the per-cow production average rose, in part, economy of small communities of San Luis and because the number of the smallest farms Los Cerros, and during harvest, generated declined at the same time that the remaining employment for residents of Santa Elena, Cerro farms were becoming more specialized. Further Plano and Guacimal. The coffee was partially study is needed to know whether the increased processed (wet processing) in San Luis, and then average per-cow production resulted in a net transported to the Central Valley for drying and increase of milk coming from these communities classification before being exported. The to the dairy plant and to assess the relative producers had no direct involvement in or profitability and environmental sustainability of control of those stages. At that time, growers lowland and highland dairy production systems achieved good yields because the soils sustained on the Pacific slope.

much of their original fertility. However, the 6.4 Proliferation of Local Coffee Companies price received for their labors did not correspond and Weakening of the Cooperative Economy to the export value of the beans, due to With the cooperative’s weakening, and the ignorance of small farmers of their legal rights, rapid growth of tourism, some farmers moved and the existence of multiple intermediaries. into tourism, as employees, entrepreneurs, or by The development of Monteverde’s dairy diversifying their farms to appeal to tourists. For economy presented an opportunity for economic example, agro-tourism has created economic diversification, giving farmers the possibility of opportunities for several Monteverde families, obtaining steady incomes and selling to a local and has become the third most popular attraction company in which they could participate as co- for visitors (after eco and adventure tourism). owners. Another opportunity presented itself at An estimated 20,000 tourists each year the early 1970s, when Coopeldos R.L., a participate in tours of coffee, sugar cane, cocoa regional coffee cooperative serving producers, and other farms developing more sustainable was founded. However, poor roads limited the agro-ecological practice (Holland 2010; G. ability of San Luis producers to take advantage Vargas, pers. comm.). of this cooperative marketing opportunity. Private coffee processing and roasting initiatives began in the early 2000s. By 2014, 6.3 Cooperativization of Coffee (1985-2000) there were 12 local coffee brands in the In the early 1980’s, the main coffee producer Monteverde. Micro-processing and roasting and owner of the coffee processing plant in San plants proliferated along with the brands. Café Luis shifted from coffee to beef cattle Florencia, one of several small family-farm production. When the San Luis coffee initiated brands, illustrates this tendency (see processing plant stopped operating regularly, Table 11.7). farmers chose to take their coffee to Coopeldos R.L. or to the Nicoya Peninsula to 6.5 Looking to the Future Coopepilangosta R.L., but both options incurred In 2014, the coffee economy is diverse: high transport costs. In response, in 1988 dozens of brands from outside the area compete CoopeSanta Elena R.L. started processing and with Monteverde’s own brands. Some local marketing coffee, having leased the San Luis entrepreneurs are seeking strategies for joint processing plant. marketing of the region’s coffee. There is During the 1990s coffee production and general support for collectively promoting marketing in Monteverde expanded Monteverde as a region that produces high significantly. CoopeSanta Elena managed to sell quality coffee. For example, in 2012 producers about half of its members’ harvest to Montana co-sponsored a Regional Coffee Fair. However, Coffee Traders, in Montana USA, at prices local entrepreneurs who have successfully superior to international prices. Based on an developed niche markets have a strong incentive agreement with Productores de Monteverde, to strengthen their own brands, rather than to S.A. the co-op created "Monteverde Coffee", a subsume them under a collective identity. brand sold regionally as "Coffee Produced in In a region apt for both coffee production and Harmony with Nature". It also received "Fair tourism, one producer reflected on the past and Trade" certification, which allowed Monteverde future. "Our region has a special combination of Coffee to be sold at higher prices in international opportunities for producing, processing, and markets. With a ready market and good prices, marketing coffee. Our product is known for its the area’s production increased. However, the high quality, and for sustainable environmental cooperative later faced economic problems and and social practices; however we face marketing weakened. This caused a loss of confidence by constraints related to scale and capital. What can farmers, a slight decline in the area’s coffee we learn from our previous successes and production, and encouraged the search for failures?" alternative marketing channels.

7. Examples of Entrepreneurship and Cabinas Capulín and Farm, between Santa Sustainable Farming in Monteverde Elena and Las Nubes, is a project that produces By Fabricio Camacho C. food (mainly vegetables) with low environmental impact, for home consumption Thanks to the leadership and vision of and for sale to the community. The project organizations and community members in the provides lodging to visitors and the opportunity Monteverde area, as well as favorable climate, to participate in farm activities. Other models soil and market conditions, several agricultural have been developed which also demonstrate, projects have integrated the concept of for tourists, artisan food production mainly for sustainable production in farming operations. family consumption and local sales, e.g., the Here, we summarize progress being made with Brenes Family Model Farm (La Cruz), Finca La integrated farms, agro-ecotourism, local Bella (San Luis) and Finca el Trapiche production and consumption, and farmers’ (Cañitas). These farms do not provide lodging, markets. but charge visitors a fee that helps offset the farm’s operating costs. The products of the 7.1 Integrated Farms Brenes Family Farm are sold at the Farmers Integrated farms respect the carrying capacity Market in Santa Elena. of the land and incorporate management practices that minimize the negative impacts of 7.3 Production for Home Consumption and agriculture, while maximizing the use of Local Market available resources without degrading them to Although not necessarily motivated by the generate direct and indirect benefits for farmers objective of low impact farming, the and for the environment and society in a Monteverde area is beginning to develop a sustainable manner over time (MAG 2008, Farm-to-Table movement led by some hotels Navarro 2012). See Table 11.8 for a more and restaurants to produce, on their own land or technical summary of the concept of integrated in partnership with local farmers, some of the farms, and Table 11.9 for a map of several food for their own operations. The two most integrated farms in the Montverde region. consolidated examples of this model are the (INSERT: Table 11.8, Integrated Farms Hotel Belmar and the Restaurant and Pizzeria Technical Summary Johnny. Meanwhile, the Monteverde INSERT: Table 11.9, Integrated Farms in Hydroponic Garden, located at Cabinas Los Monteverde, 2014 Pinos in Cerro Plano, produces vegetables and spices for area restaurants and hotels and for 7.2 Agro-ecotourism direct sale to the public at the garden or at the Although agro-ecotourism has been more Monteverde Farmers Market. predominant on coffee plantations in the Another interesting process is the use of Monteverde area (e.g., Café Monteverde, Café traditional home gardens, small semi-urban San Luis, Café La Bella Tica, Café Don Juan), gardens, and livestock propagation systems for other farms have also taken advantage of home consumption, which produce vegetables, tourism to diversify their productive activities. fruits and root crops, eggs, poultry, and pork. They often offer guided farm tours, and This type of production requires little space, educational activities linked to the region’s uses local inputs, and increases family food natural history and culture; some offer lodging security. Some families sell their surplus and entertainment for visitors. production, or exchange it with neighbors, The Terra Viva and Rancho Makena projects, helping the domestic economy and reducing in the San Bosco-Las Nubes area, are dairy dependence on external food markets. farms that have incorporated farm production Finally, the production of eggs for local and environmental impact mitigation processes consumption is significant in Monteverde. This with ecotourism. Both dairies offer lodging in production process has evolved around small cabins, and opportunities for tourists to engage family businesses that produce enough to meet in farm activities. the needs of the local market, a minimum of

5000 eggs per day (C. Santamaría, pers. “households” dependent upon dairy or Comm.). The eggs are distributed directly to coffee farms, as opposed to “viable farms?” local businesses and the Monteverde Farmers 4. How have educational opportunities Market. expanded options for youth? What are current trends related to youth education, 7.4 The Monteverde Farmers Market employment, and mobility? For example: In 2014, the Monteverde Farmers Market how many youth pursue higher education or celebrated its sixth anniversary. This weekly technical studies? How many are event provides a venue for local producers and graduating? How many drop out to work producers elsewhere in the country, to sell their locally or in other regions? How many products to local consumers. It also functions as return to live, work or share their knowledge an opportunity to strengthen and enrich the locally? How many have graduated, but cultural ties of friendship and unity among the work in other parts of the country? How residents of the community. The mix of many have studied abroad? How many producers, consumers, and visitors, as well as receive scholarships or support from local the generational diversity, is an example of the organizations, businesses, or private cultural richness that characterizes the individuals for primary, secondary, or Monteverde area. university education? Such a study could involve participation by the students 8. Topics for Future Research themselves, with support of local A fundamental challenge that applies to all organizations. farms is to develop a management culture involving record keeping and analysis. Other 8.3 Dairy pressing questions meriting quantitative and What can be done to reduce supplemental qualitative study include the following. feed grain use, and to increase production of quality forages? This should be linked to 8.1 Climate Change technical assistance on soil fertility 1. What impacts has climate change had on management. Artificial insemination programs agricultural production in the area? might consider the use of sires that have been 2. What are possible scenarios for the impact bred to maximize milk production in high of climate change on future agricultural forage/low supplemental grain ration contexts. production? Further study could also be done to measure the 3. What adaptation mechanisms can area relative profitability and environmental farmers undertake? sustainability of lowland and highland dairy production systems on the Pacific slope. 8.2 Economy 1. How are demographic, economic, and social 8.4 Coffee trends affecting land use options? What 1. What climate change adaptation measures outcomes are desired? What policies, are available for local coffee farmers? For incentives, and institutional arrangements example: coffee varieties with greater are needed to move toward the desired resistance to Coffee Rust (Hemilieia outcomes? vastatrix) and “Ojo de Gallo” (Mycenia 2. What role does indebtedness play in citricolor); alternatives for natural control of household livelihoods and land use fungus and insects (Coffee Borer Beetle, decisions? Hypothenemus hampei). 3. To what degree does the economic viability 2. What opportunities exist for the of dairy and coffee farms depend upon development of an umbrella brand for all the specialized versus diversified income local coffee that meets certain quality sources? How might the results of this standards? analysis change if the unit of analysis were

8.5 Integrated Farms Momentum is growing, in part because tourism What is the current and potential demand for, provides opportunities for local farmers to and capacity to produce local food? With this diversify, develop market niches, and to gain information it would be useful to design a plan increased access to information. to activate farm production. The study should Climate change as well as globalization and consider aspects such as funding opportunities dependence on external markets represent (development banks, the Monteverde unprecedented challenges for agricultural Community Fund, microcredits), stratification producers in the Monteverde area. However, in and production coordination, farm product Monteverde, there exists capacity and leadership collection systems, storage, distribution, to meet these challenges with courage, marketing, online ordering platform, technical intelligence, unity, and hard work. The mystique assistance, local production of inputs, linkages, of agriculture, and love for the land have not financial analysis, ecosystem services, carbon been eroded and are still alive in people who neutrality, and rural tourism, among others. have learned to work hand in hand with nature. The great challenge that remains in the short 9. Conclusions term is to transmit knowledge to new Land use in Monteverde is dynamic. The generations so that they will be motivated to original chapter, written in the late 1990s, return to the farms and make the job of feeding focused on agricultural production, stating that society a way of life that gives them an “(a)n agrarian society requires healthy land and opportunity for employment and personal adequate incomes for farmers”. In the fulfillment. It is imperative to work with the intervening years, we have seen rapid local market – households as well as hotels and development of tourism, coupled with restaurants – to develop strategic alliances so biodiversity conservation and various that it can absorb local food production as a environmental and educational programs. distinguishing feature of the economy and Tourism immediately affects the communities tourism. closest to the forest preserves, but its ripples influence job opportunities, immigration 10. Tables and Figures patterns, land prices, access to information, and cultural diversity throughout the region. 10.1 Table 11.1 People Interviewed Interaction between the area’s three economic The trends identified in this addendum are pillars – tourism, dairy and coffee – has created based on interviews with professionals working trends that shape opportunities and influence for farm support organizations, including the land use decisions. In short, moving the cheese plant, the Monteverde milk producers’ economy towards more sustainable land use association, the local office of the Ministry of goes beyond farming: larger social, economic, Agriculture, and the AyA, plus farmers, and and demographic trends shape the opportunities others. to which farmers respond. Farmers walk a fine line between profit and loss. Sustainable technologies take capital, and increased managerial effort and labor. We do not observe a trend toward increased managerial capacity of most farmers despite the promotional efforts of various institutions, but we do increasingly see cases of engaged, innovative, committed people who are developing more sustainable production systems. This trend is promising. It is a gradual process that requires cultural change, especially when the cost and the "work" of making the change is "now", and the benefits are long term, diffuse, or uncertain.

Resident Community Activities Francisco Donato Director, Monteverde Milk Producer’s Association (APLM) Ronald Briceño Agronomist, APLM Jose Aníbal Murillo M. Cattle Producer Relations Analyst, Productores de Monteverde, S.A. Juan José Monge M. Veterinarian, Farm Affairs Manager, Productores de Monteverde, S.A. Javier Marín Agronomist, MAG, Santa Elena Aníbal Álvarez M. Agronomist, MAG, Director of the Santa Elena office José Luis Vargas L. Business consultant, former General Manager, Productores de Monteverde, S.A. Manuel Torres O. Forestry Engineer, Monteverde resident Claudia Rocha M. Community Outreach Program Coordinator, Monteverde Institute Juan Ramón Fuentes R. Dairy herdsman and longtime resident of San Luis and Monteverde Victorino Molina R. President, AyA Santa Elena7 Aura Sandí S. Administrator, AyA Santa Elena Virgilio Brenes President, AyA San Luis Fray González N. Treasurer, AyA La Guaria Marvin Ramírez Administrator, AyA Monteverde José Vargas G. Coffee producer in the Monteverde area prior to 1960 Eugenio Vargas L. Co-owner, Vargas Leitón Family Farm, San Luis Guillermo Vargas L. Forestry Engineer, co-owner of Varsan, S.A. Farm, Cañitas Fabricio Camacho Forestry Engineer, General Manager, University of Georgia San Luis C. campus Joseph Stuckey Dairy farmer, economic and community development specialist Sarah Stuckey Co-owner, Costa Rica Study Tours, S.A., Monteverde Oldemar Salazar Owner, organic coffee farm, San Luis

7 Community Water and Drainage Administrative Association, (Asociación Administradora de los Sistemas de Acueducto y Alcantarillado Comunal, ASADA, also known as AyA).

10.2 Table 11.2 Indicative Population Monteverde and Surrounding Areas Indicative Population – Monteverde and Surrounding Areas

Community AyA Est. Population Connections Cabeceras 234 936 Cebadilla (estimate) 15 60 Guacimal, Fernández, Santa Rosa, & Sardinal 270 1,080 La Cruz (estimate) 15 60 La Guaria 42 168 Las Nubes 36 144 Los Tornos (estimate) 25 100 Monteverde 94 376 San Luis 80 320 Santa Elena, Cerro Plano, Lindora, los Cerros, Cañitas 1,400 5,600 Turín 22 88 Total 2,233 8,932

Notes: 1) Local AyA leaders estimate 4 people per connection. However, some connections serve no households; others serve multiple households; some households are served by non-AyA sources. For example San Luis reports 80 connections, but a 2012 community census identifies 103 households with a population of ~400-420 people. 2) Sardinal is not usually considered to be part of the Monteverde region. Source: V. Molina, V. Brenes, and other ASADA leaders (pers. comm.).

10.3 Table 11.3 The “Homestay” Industry Elena, Cerro Plano, Monteverde, Cañitas, Los Educational tourism, which has been Llanos, San Luis, and La Cruz (Claudia Rocha, operating in Monteverde since the late 1980s, pers. comm.). Hosting homestay students is a has been a vehicle for cultural integration. An popular strategy to augment household income, evidence of this is the “homestay” industry in but often, personal relationships resulting from which local families are paid to host visiting homestays open doors of opportunity for both students in their homes. For example, in June nationals and visitors, including occasional 2014, the Monteverde Institute, one of the larger marriages, as well as opportunities for travel and organizations that organize homestays, lists 176 education. active homestay families in their database. These are distributed among the communities of Santa

10.5 Table 11.5 Dairy Production Indicators

This replicates information from the 2000 for the update was compiled by: Juan José chapter to give a comparative snapshot of a Monge, José Aníbal Murillo, Francisco Donato, typical upland dairy farm in 2014. Information Ronald Briceño, Javier Marín, and Joseph Stuckey.

Indicator 1990s 2014 Herd size 16 cows, 67% of herd in 16 cows, 80% of herd in production production Cow breeds In order of importance: Holstein, In order of importance: Jersey, Jersey, Brown Swiss, Guernsey Holstein, Brown Swiss, Guernsey Feed Rotational grazing on Star Grass Rotational grazing continues, but pasture; 0.5-2.5 kg/day grain; with greater dependency on use of Elephant or King Grass; salt, supplemental grain; some silage minerals, urea, molasses bales, hay, and cut feed in dry season, as well as salt, minerals, urea, and molasses. Stocking rate 1.8 cows/ha 2 cows/ha Milking Twice per day Same Farm size 18 ha total, 14 ha in pasture 10 ha total, 8 ha in pasture (CATIE 1983) Milk 10 kg per cow per day 16 kilos per cow per day production Pasture Manual fertilization and liming, Same management herbicides (CATIE 1983, Stuckey 1989) Fertility Artificial insemination; birth rate Artificial insemination; no data on 58%; calf mortality rate 8% (CATIE calving and mortality rates. 1983) Mechanization In 1995, 60% of farmers used In 2014, almost 100% use milking milking machines (up from less than machines; all have refrigeration, and 5% in1979). Some farms had electric hot water tanks; 95% transport milk fencing and/or a tractor. No farms using bulk tank trucks. The use of had refrigeration (cold water was motorized backpack sprayers and used to cool milk) “weed eaters” is common. Labor Mostly family labor supplemented Family labor remains important, by part-time hired help. but the amount of contracted labor is increasing; tendency for youth to study and leave the farms. Family size 4.5 dependents per farm 3 dependents per farm.

10.6 Table 11.6. Highland/lowland Dairy Indicators, 2013-2014

Data from Farms that Deliver Milk to Productores de Monteverde, S.A. (May 2013 through April 2014) Indicator Highland Lowland No. of producers 107 32 Gross milk received at 27,271.79 kg. 5,238.6 kg. the cheese plant, daily average Farm production, 254.87 kg. 136.96 kg. daily average, kg No. milking cows 16 15 per farm, average Production, kg per 15.9 kg. 10.9 kg. cow per day, average Area, ha per farm, 10 ha 30 ha average Cattle breeds Jersey, Holstein and crosses Brown Swiss, Simmental, between the two Gir, and crosses of these with Brahman Artificial 50% of producers use AI No AI, use natural mounting insemination Refrigerated bulk 95,0% 100% tank Pasture fertilization Yes. Soils are acidifying, No. pH<~5.5; require lime, magnesium; high in iron/aluminum; limited phosphate availability. Forages African Star grass predominates Improved pastures: Brachiaria (Cynodon nlemfuensis), King brizantha, guinea/mombasa grass Grass/maralfalfa (Pennisetum sp), (Panicum máximum), sugar cane sugar cane, imperial (Axonopus maralfalfa, natural grass. spp.), mulberry (Morus spp), and natural grass. In dry season some use cut feed and hay: transvala (digitaría decumbes), and rice straw. Supplemental grain No data. 1-2 kg (kg per cow per day) Farm labor (Full 2 people per farm 3 people per farm time equivalent – FTE) Family labor (FTE) About 70% of the farms rely on About 80% of the farms use family labor. ~10% milk with hired family labor. labor. Most contract occasional labor to build fences and clean pastures. Source: Juan José Monge and José Aníbal Murillo Méndez

10.7 Table 11.7 The Café Florencia Case

Café Florencia is a coffee brand originating on a farm owned by the Vargas Leitón family in San Luis. It has been certified organic since 2009 by Eco-LOGICA, an organic products certifier, through a Costa Rican producers association called Organic Agriculture Movement of the Central Pacific (MAOPAC).

Approximately 25% of the crop is consumed by the Vargas Leitón family (“a rather large clan!”). The excess is marketed to:

 International student groups and professors that visit the farm as part of their educational programs,  The Monteverde Institute,  One of the local hotels, as part of its Certification for Sustainable Tourism program (CST)8,  A small group of clients in Portland Maine, members of a Community Support Agriculture (CSA) group,  Other contacts in San José.

8 A program of the Costa Rican Institute of Tourism (ICT), http://www.turismo-sostenible.co.cr/index.php?lang=es.

10.8 Table 11.8 Integrated Farms Technical Summary By Fabricio Camacho C.

The technical principles underlying the income, learning, innovation, mystique, management of integrated farms are: 1) belonging, identity and culture as a result of increased productivity, 2) increased ground assimilation of, and immersion in, the cover and water protection, 3) increased water environment experienced by people who are infiltration into the soil profile and decreased involved in the production process (Palomino runoff, 4) the proper management of soil fertility 2004, Navarro 2012). and maintenance of organic matter, 5) It is also estimated that integrated farms are neutralization and / or abatement of suitable models to combat the aftermath of the contamination and 6) the efficient use of energy Green Revolution as the management system (MAG 2008). helps to mitigate carbon emissions, to adapt to On integrated farms, every aspect is planned climate change, and to achieve food security, and linked together blending traditional which impact positively on poverty reduction, production methods with modern technologies promoting more equitable rural development and that enhance the natural productivity of the land a better quality of life in rural communities through a system that operates on planning and (UNDP SINAC 2013, INTA 2012, Gomez 2011, efficient use of space, resources (water, soil, Palomino 2004). biomass, waste) and energy available to generate fresh, clean, varied and healthy food, and to constantly boost agricultural employment,

10.9 Table 11.9 Integrated Farms in Monteverde, 2014

Organic Waste Value Educational Farm Name Products Market Fertilizer Management added Activities Production Foods University Pigs On-campus Compost Tube bio Cheese Students of Georgia, Cow milk consumption Earthworm digester Sour Local San Luis (1) Garden compost cream residents produce Bio-foliar Fruit fertilizer

La Vegetables Household Compost Tube bio Dried beef Students Querencia, and other consumption Bio-foliar digester Beverages Local San Luis (2) garden Local market fertilizer residents produce sales Cow milk Pigs Sheep Olivier Chickens Household Compost Tube bio Chicken NA Garro and Eggs consumption Chicken digester and pork Family, Pigs Local market manure processed San Luis sales Bio-foliar in pieces fertilizer Rancho de Tilapia Household Chicken Tube bio Tilapia NA Lelo, Pigs consumption manure digester and pork San Luis (3) Chickens Sale in own Bio-foliar sold in Eggs restaurant fertilizer restaurant Vegetables Local market Coffee sales Finca Coffee Household Compost NA Farm Students Florencia, Garden consumption branded San Luis produce Local and coffee Fruit international Certified Sugar market sales organic cane farm(5) Gregory Coffee Household Compost NA Farm Tourism Paradise Medicinal consumption Bio-foliar branded Café, San plants Local and fertilizer coffee Luis (4) international Certified market sales organic farm(5) biodynami c La Bella Coffee Household Compost Tube bio Farm Students Tica, San Pigs consumption Bio-foliar digester branded Tourism Luis (4) Fruit Local and fertilizer coffee Vegetables international Certified market sales organic farm (5) Café San Coffee Household Compost Tube bio Farm Students

Organic Waste Value Educational Farm Name Products Market Fertilizer Management added Activities Production Foods Luis, San Fruit consumption digester branded Tourism Luis (4) Vegetables Local and coffee international market sales Benito Goat milk Household Compost NA Goat NA Guindon, Cow milk consumption cheese Monteverde Sheep Local market Marmalad Vegetables sales es Fruit Garden produce Life Goat milk Household Compost Tube bio Farm Students Monteverde, Coffee consumption Earthworm digester branded Local Cañitas (3) Eggs Local market compost coffee residents Garden sales Bio-foliar Goat produce fertilizer cheese Fruit

(1) Functions as an integrated demonstration from other local producers to process and sell and experimental farm; engages in technology under their own specific brand. transfer including, for example, the installation (5) Internationally certified as organic coffee of biodigesters in neighboring farms in the through Movimiento de Monteverde area. To date, 15 biodigesters have Agricultura Orgánica del Pacífico Central been installed. (MAOPAC) (Central Pacific Organic (2) Functions as a membership model in Agriculture Movement), in affiliation with which clients pay for farm products in advance Certificadora de Productos Orgánicos y and periodically receive harvested products. Sostenibles Eco-LOGICA, (Eco-LOGIC (3) Has been awarded the Ecological Blue Organic Products Certifier) http://www.eco- Flag. logica.com/. (4) Processes coffee on site. In the case of La Bella Tica and Café San Luis, they buy coffee

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12 Conservation Biology — Update 2014

Nathaniel T. Wheelwright

In the 14 years since Monteverde: Ecology The first step in protecting biodiversity is and Conservation of a Tropical Cloud Forest conducting thorough inventories of species. In was published (Nadkarni and Wheelwright this regard, Monteverde has been a leader 2000), vast tracts of land have been newly among neotropical sites. Documentation of the protected in the Monteverde-Arenal Bioregion, region's stunning biological diversity continues thanks to the work of the Monteverde to be expanded by the observations of visiting Conservation League, Costa Rican and biologists and ecotourists, as well as local international conservation groups, and numerous farmers and citizen scientists (e.g., Rowe and generous donors. The Children's Eternal Pringle 2005, Yanoviak et al. 2003a). A team Rainforest is now the largest private reserve in from the Monteverde Cloud Forest Reserve, led Costa Rica, with an area of 22,500 ha, more than by Yoryineth Méndez, has been conducting twice the size of the Monteverde Cloud Forest regular censuses of frogs and toads from the Reserve (see Chapter 10 Update by Peñas Blancas Valley to the Reserve to the San Burlingame). A new generation of young Luis Valley. Preliminary results indicate scientists and policy makers, many of them recovery of species that had been missing for students on courses offered by the Organization more than a decade. Another team, led by Mark for Tropical Studies, the Council on Wainwright, documented the recovery of the International Educational Exchange, and the Green-eyed Frog (Lithobates vibicaria). University of California Education Abroad However, there remains much to do in Program, has visited Monteverde's forests. Monteverde with regard to several key areas of Building upon what was known about the conservation biology highlighted by region's flora and fauna a decade and a half ago, Wheelwright (2000). As of 2014, no one has yet they and others have worked with local published a study of the impact on cloud forest organizations to connect knowledge to plant or animal communities of invasive species conservation action. or native lowland species that have expanded their range upslope (e.g., Keel-billed Toucan,

Ramphastos sulfuratus; Bronzed Cowbird, Understanding the causes and consequences Molothrus aeneus). We still can only guess of rarity is also crucial for protecting which plants or animals in Monteverde are biodiversity. Jankowski and Rabenold (2007) keystone species (species whose loss would found that endemic species in neotropical have disproportionate negative effects on montane rainforests such as Monteverde tend to biodiversity; Ficus tuerkheimii and Acnistus be locally rare: there is a positive correlation arborescens, trees whose fruits are eaten by between distribution and abundance at several numerous bird species, are good candidates), spatial scales. There is also a correlation and the population genetic structure and between regions of high species richness and demographics are known for virtually no high endemism, at least for taxa such as Monteverde species (although see Soare et al. bromeliads, palms, aroids and scarab beetles, 2014). Gathering such information is critical according to Kohlmann et al. (2010), who single because it will help us prioritize conservation out premontane wet forests in the Cordillera de efforts and effect management plans that target Tilarán as among the most important particularly vulnerable or ecologically important conservation priority areas in Costa Rica populations. because of their biological diversity and Monteverde's arthropods have been well- uniqueness. catalogued (Yanoviak et al. 2003b, 2007; The main focus of conservation biology at Schonberg et al. 2004, Hanson 2014) but Monteverde since 2000 has been on the role of knowledge of most herbivorous insect species' landscape features in preserving biodiversity, host plants is lacking (see Hanson 2014). Soil particularly connectedness between habitats at fauna—bacteria, protists, fungi—remain a different spatial scales. Since the late 1970's, not mystery, although Nadkarni and colleagues only has the size of protected areas in the (Nadkarni et al. 2002, Rains et al. 2003) Monteverde-Arenal Bioregion (MAB) been continue to make progress understanding the greatly expanded, but forest regeneration has biology of soils in cloud forest canopies. also occurred throughout the region, thanks in Monitoring species that are easy to count and are large part to ecotourism, changes in local ecologically (or economically) important or that attitudes, and abandonment of pastures and indicate the health of Monteverde's communities coffee parcels (see Chapter 11 Update by and ecosystems ("indicator species") is essential. Stuckey et al.). As a direct result, population Populations of vocal animals such as frogs, declines in numerous species have been insects, mammals and birds can be monitored reversed. For example, there was little or no using new technologies such as real-time change in the number of bats (individuals and bioacoustics monitoring (Aide et al. 2013). species) captured per unit time per net length Three-wattled Bellbirds (Procnias over a 27-year period (LaVal 2004). Twenty- tricarunculata) and Resplendent Quetzals four new bat species, most of them from the (Pharomachrus moccino) are two obvious lowlands, colonized the area over the same time, species to begin with. For monitoring plant presumably in response to warming climates and responses to environmental changes, much could a 19% increase in forest area between 1973 and be learned by recording the annual timing and 1998 (based on aerial photographs; LaVal 2004). magnitude of flowering and fruiting of a Agricultural windbreaks, increasingly planted in taxonomically diverse set of common, easily open pastures throughout the zone, have had recognized tree species (Wheelwright 1986); numerous beneficial effects for biodiversity. For transects could be set up along readily accessible one thing, they provide habitat for forest tree roads in Monteverde with observations made by species and facilitate forest regeneration within "citizen scientists" and entered into on-going agricultural areas: 91 tree species representing phenological databases (c.f. U.S. National primary and secondary forests occur in Phenology Network). These studies need to be Monteverde windbreaks, with tree seedling designed and implemented quickly, with the densities highest in windbreaks connected to goal of pursuing them over the long-term. forest patches (Harvey 2000a). Dispersal of the seeds of trees and shrubs was greater in

windbreaks planted on dairy farms than in essentially, from the Continental Divide to sea nearby pastures, with 199 species recorded in level—and across international boundaries. seed traps during a single year; the presence of Climate change has surged to the fore as the remnant forest trees in pastures increased the central concern in conservation biology. Making number of tree species (Harvey 2000b). One headlines in the popular press in ways that encouraging discovery is that, in addition to tropical deforestation and the extinction crisis attracting seed dispersers, relict pasture trees can never succeeded in doing, fears about climate serve as "regeneration foci"—increasing change have awoken the public to take action to ecological connectedness on a temporal scale— mitigate the worst effects of global warming on by ameliorating soil microclimates and crop production, rising sea levels, disease supporting diverse canopy seed banks in their outbreaks, etc. It was apparent in 2000 that decomposing epiphyte masses (Nadkarni and Monteverde had already begun to feel the effects Haber 2009). of climate change. In future decades, the flora O'Donnell and colleagues have studied the and fauna of cloud forests throughout Latin effect of forest fragmentation in Monteverde on America will suffer from climate changes more army ants (Formicidae: Ecitoninae) and the birds than those of lowland habitats. Montane that facultatively take advantage of them to flush landscapes support distinctly high beta diversity insect prey. In one study, they found that, (the accumulation of increasing diversity as one compared to forest fragments, continuous forest moves between sites; Jankowski et al. 2009). supported greater bird species richness, larger Moreover, refuges to escape the rises in flocks and great total body mass of birds temperature and alterations in rainfall and attending army ant swarms (Kumar and seasonality that are already upon us are limited O'Donnell 2007). In another study, on mountaintops, and they diminish even further microsatellites were used to reconstruct as species are forced upslope. At least half of the genotypes and determine population genetic 77 cloud forest bird species included in the structure and found "isolation by landscape modeling study of Gasner et al. (2010) are resistance": forest clearing impedes dispersal predicted to decline in the next century, with and gene flow between colonies of the keystone eight species restricted to Central America ant species Eciton burchellii (Soare et al. 2014). projected to become locally extinct. Species that The increase in road-building and traffic in are particularly threatened include the Mountain Monteverde over the last several decades is Robin (Turdus plebejus)—one of the likely to have created new barriers to gene flow commonest and most important seed dispersers for numerous species (including, surprisingly, in the 1980s— and Collared Redstart certain understory bird species: Develey and (Myioborus torquatus), a familiar and unwary Stouffer 2001). Dust from traffic, as well as denizen of the cloud forest known as "amigo del noise and light pollution, are other unstudied hombre." Gasner et al. (2010) recommend factors that could negatively affect species near improving protection of cloud forests in larger developed areas in Monteverde. mountain ranges, such as the Cordillera Central For more mobile species, such as birds that and Talamanca, as a way of safeguarding migrate altitudinally, the importance of habitat threatened species from the Cordillera de connectedness is evident at much larger scales. Tilarán. Epiphytes will be negatively affected as In the last 14 years, radio transmitters and other well by shifts in microclimate, as demonstrated tracking devices have revealed details of the by greenhouse studies and experiments by altitudinal migrations of species such as Bare- Nadkarni and Solano (2002). Epiphytes that necked Umbrellabirds (Cephalopterus were transplanted along with their arboreal soil glabricollis) and Three-wattled Bellbirds from upper cloud forests to lower elevation trees (Chaves-Campos et al. 2003, Powell and Bjork exposed to less cloud water had higher leaf 2004, Papeş et al. 2012). These studies confirm mortality, lower leaf production, and shorter the importance of safeguarding natural habitats lives. The death of epiphytes resulted in radical within parks, reserves, and protected private changes in the composition of canopy lands across a broad altitudinal range— communities (Nadkarni and Solano 2002).

Still, some biologists, myself included, (Incilius [Bufo] periglenes) in Monteverde. wonder whether today's focus on climate change Using stable isotope measurements of tree cores has diverted attention from urgent and long- to reconstruct a century of hydroclimatology in standing—but still unsolved—threats to Monteverde, Anchukaitis and Evans (2010) biodiversity (Tingley et al. 2013). It is critical found annual variation in dry season moisture for Costa Rican decision-makers—in fact, associated with El Niño Southern Oscillation people interested in protecting cloud forests (ENSO) events and argue that the extinction was worldwide—to understand that species are likely due to a severe drought caused by the declining right now in Monteverde and 1986-1987 El Niño, rather than a long-term elsewhere primarily not so much because of trend in global warming. Research by Cheng et climate change but because of familiar factors al. (2011) implicates an "epidemic wave" of the such as habitat fragmentation, environmental chytrid fungal pathogen Batrachochytrium contaminants, and introduced species. Armed dendrobatidis (Bd), which moved south through with a better understanding of the present causes Central America and apparently reached of rarity and extinction, conservationists, Monteverde by 1987, with disastrous teachers, taxpayers, and voters can be make consequences for the Golden Toad. It is worth more informed decisions about where to invest noting, however, that Richards-Hrdlicka (2013) scarce resources for protecting biodiversity. For failed to find Bd in preserved Golden Toad example, Ocotea monteverdensis, a tree species specimens. Pounds et al. (2006) envision an in the Lauraceae restricted to premontane wet interaction between global warming and Bd, forest on the Pacific slope of the Cordillera de with warming climates creating the conditions Tilarán between 1200 and 1450 m, has recently for Bd outbreaks in the highlands of Costa Rica. been red-listed by the International Union for the There is much to be optimistic about in terms Conservation of Nature as "critically of conservation in Monteverde (Wheelwright endangered." Why? Because of "habitat loss and 2007). Forest regeneration, habitat degradation as forest areas have been cleared for connectedness, population rebounds of certain agriculture and housing, business and tourist high profile species (e.g., danta, Tapirus developments" (Joslin et al. 2013). (Note that bairdii), increasing awareness of other this formerly common species was called environmental issues, engagement of concerned Nectandra hypoglauca in earlier publications citizens—all of these are promising signs. We [e.g., Wheelwright et al. 1984, Mazer and hope that the next generation of Latin American Wheelwright 1993].) Although there is almost researchers will find in this book specific ideas certainly more forest cover today in Monteverde for their own research projects, and inspiration than 35 years ago (LaVal 2004; F. Joyce, pers. to advance and apply what we know about comm.), the main point is that many species are conservation biology to protect biodiversity in in decline quite independent of climate change. the cloud forests of Monteverde and throughout Debate continues about whether altered Latin America. climate caused the demise of the Golden Toad

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