RM Lati Ju a b Fundación Talking Oceans, Carrera 16 #127-81, Bogotá, Colombia a r t i c l e i n f o Article history: Received 12 January 2016 Received in revised form 7 March 2016 Accepted 8 March 2016 Available online xxxx a b s t r a c t . . . . . . . . . . . . 152 . . . . . . . . . . . . 154 . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . Acknowledgements . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . 161 Appendix A. Supplementary material . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . 161 References . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . 161 ⇑ Corresponding author at: Carrera 16#127-81, Bogotá, Colombia. E-mail address: julianalop14@gmail.com (J. López-Angarita). Forest Ecology and Management 368 (2016) 151–162 Contents lists available at ScienceDirect6. Prospects for the mangroves of the ETP . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . 1602.2. Early pre-Columbian societies . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . 2.3. Conquistadores and the colony . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . 3. Change in mangrove extent. . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . 4. The state of mangrove protection in the ETP . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . 5. Environmental policy related to mangroves. . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . .http://dx.doi.org/10.1016/j.foreco.2016.03.020 0378-1127/ 2016 Elsevier B.V. All rights reserved.. . 155 . . 157 . . 160Contents 1. Introduction . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . 152 2. An historical timeline of mangrove decline . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . 152 2.1. Evolution of perceptions & attitudes towards mangroves . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . 152Keywords: Archaeozoology Protected area Conservation Management Eastern Tropical Pacific Historical ecologyFrom native pre-Columbian subsistence economies to the modern global economy, mangroves have played an important role providing goods and services to human societies for millennia. More than 90% of the world’s mangroves are located in developing countries, where rates of destruction are increas- ing rapidly and on large scales. In order to design effective conservation strategies, it is critical to under- stand the natural dynamics and anthropogenic drivers of these coastal wetland habitats. We use retrospective techniques to reconstruct mangrove forest history in the Eastern Tropical Pacific. We exam- ine available, present day estimates of mangrove area and evaluate the representation of mangroves in the protected area systems of Costa Rica, Panama, Colombia and Ecuador, evaluating existing policies regarding mangroves. Archaeozoological evidence shows that mangroves were exploited for many thou- sands of years by pre-Columbian societies. Post-conquest deforestation prevailed during the next 400 years. Since 1990, despite increasingly positive attitudes towards mangroves and their inclusion in protected areas and conservation policies, mangrove cover has continued to decline due to expanding human activities (agriculture, aquaculture, coastal development), even in the presence of laws prohibit- ing their removal. Here we provide an historical ecology baseline of mangroves in the Eastern Tropical Pacific, from which to view current trends and map future trajectories. Given the myriad negative con- sequences of mangrove loss recorded worldwide, and the strong ecological connectivity of the region, developing effective strategies for mangrove management at an appropriate scale will be paramount to protect coastal livelihoods and biodiversity.  2016 Elsevier B.V. All rights reserved.c Smithsonian Tropical Research Institute, Balboa, Ancón, Panamá City, Panamaliana López-Angarita , Callum M. Roberts , Alexander Tilley , Julie P. Hawkins , Richard G. Cooke Environment Department, University of York, York YO10 5DD, UKn American countries a,b,⇑ a b a ceview and synthesis angroves and people: Lessons from a history of use and abuse in four journal homepage: www.elsevier .com/locate / forecoForest Ecology and Management groves played a crucial role in the way of life for many coastal soci- y an1. Introduction Largely restricted to tropical and subtropical latitudes, man- groves are the only vascular flowering trees that can live in the confluence of land, freshwater, and ocean (Hogarth, 2007). This involves adapting to fluctuating environmental conditions such as changes in salinity, regular soil inundation, shifting sediments, and in-water low oxygen concentrations (Kathiresan and Bingham, 2001). As such, mangroves display a large set of morpho- logical and ecophysiological adaptations to help them survive in these dynamic habitats. Among these adaptations are (1) the exclusion of salt by roots, (2) rapid canopy growth, (3) viviparous embryos, (4) tidally dispersed propagules, (5) exposed roots that breathe above ground, (6) highly vascularized wood, (7) efficient nutrient retention, and (8) salt-excreting leaves (Alongi, 2002; Duke, 2011). Despite being considered a rare forest type because of their small global extent (less than 1% of tropical and subtropical forests worldwide), mangroves provide a wide range of ecosystem ser- vices and direct uses including coastal protection, fuel (charcoal, firewood), food (fruit, leaves, associated vertebrates and inverte- brates), and construction material (Hogarth, 2007). Even though the ecological importance of mangroves has come to be widely rec- ognized, reports of the Food and Agriculture Organization show a widespread decline of mangrove area, with losses over 20% of total global coverage (36,000 km2) between 1980 and 2005 alone (FAO, 2007a). It has been claimed that estimated rates of mangrove loss are three to five times greater than the overall loss rates calculated for other forests and coral reefs on a global scale (Valiela et al., 2001). In light of the current degradation rate of marine ecosys- tems, intensifying anthropogenic impacts, and climate change, protected areas emerge as an essential strategy for conservation. More than 90% of the world’s mangroves are located in developing countries, where rates of destruction are rapidly increasing (Duke et al., 2007). In order to design more effective conservation strategies, it is critical to understand long-term anthropogenic effects as well as the natural dynamics of this marine-coastal habitat in space and time. Study of forests’ past dynamics represents a fundamental insight (Dahdouh-Guebas and Koedam, 2008). Pre-Columbian soci- eties represent more than 95% of the history of mangrove/human interaction in the neotropics. Historical ecology techniques derived from social sciences, such as exploration of documentary archives and archaeological investigations, can provide valuable informa- tion and complement other direct survey methods (e.g. remote sensing) applied to understand current processes and map possible future trajectories (Dahdouh-Guebas and Koedam, 2008). The Eastern Tropical Pacific (ETP), is a distinct marine ecoregion encompassing continental shore between southern Baja California to northern Peru including oceanic island groups such as Cocos, Malpelo, and Galápagos oceanic islands (Spalding et al., 2007). However, within this broader region, the Pacific waters of Panama, Costa Rica, Colombia and Ecuador (Fig. 1) share particular conser- vation significance by containing a cluster of World Heritage Sites (Edgar et al., 2011). This area, termed in this study as the ETP, is an important biogeographical region in terms of marine resource pro- ductivity and biodiversity, supporting a range of rich fisheries and exhibiting many endemic species (Fiedler and Talley, 2006). In this paper we use retrospective techniques to reconstruct mangrove forest history in ETP countries, with the aim of understanding the historical reasons behind mangrove deforestation in the region. Additionally, we review available estimates of mangrove area from recent years and evaluate the representation of mangroves in the 152 J. López-Angarita et al. / Forest Ecologmarine protected areas of four countries, examining existing poli- cies regarding mangrove conservation. The historical timeline of ETP mangrove forests and their current protection status that weeties, and are closely linked with human culture. In India, the Solomon Islands and Kenya, mangroves have been regarded as sacred spaces where special rites take place, temples are erected, and trees worshipped (Kathiresan and Bingham, 2001). In LatinMangroves’ ability to thrive in salt water has attracted substan- tial scientific attention and academic curiosity, especially among botanists (Walters et al., 2008). However, since our understanding of the services provided by mangroves, as a coastal habitat has been scant and defective until recently, attitudes towards man- groves as an ecosystem have been ambivalent (Lugo and Snedaker, 1974). As far as we know, the first descriptions of mangroves by ancient literate observers were made in the year 325 BCE by Nearchus, the Greek Admiral of Alexander the Great’s fleet. In the ‘Chronicles of Nearchus’ he described mangroves in the Red Sea, the Persian Gulf, and the Indus Delta (Bowman, 1917). Twenty years later in 305 BCE Theophrastus, a pupil of Aristotle, also referred to mangroves in his ‘Enquiry into Plants’ (Schneider, 2011): ‘‘But there are plants in the sea, which they call ‘bay’ and ‘olive’ [. . .]. On the islands which get covered by the tide they say that great trees grow, as big as planes or the tallest poplars...” (Hort, 1916). On the American continent, the first Spanish chronicler to describe mangroves from a botanical standpoint was Gonzalo Fernández de Oviedo in his ‘General and Natural History of the Indies’ in 1531, placing emphasis on their usage by indigenous communities: ‘‘Mangrove is one of the best trees in these lands, and it is common in these islands (Greater Antilles) and in Tierra Firme (mostly the Isthmus of Panama). Its wood is one of the best ones around for building shelves, poles, posts for houses, fences, window frames, and doors and other small things. . .the bark of these mangroves is singularly good for tanning cow leather in a short time” (de Oviedo y Valdés 1535). Literature about mangroves between the 17th and 20th cen- turies focused mainly on describing mangrove morphology, habi- tat, distribution, species diversity, taxonomy, and systematics (Bowman, 1917). From around 1900 onwards, studies that high- lighted the ecological role of mangroves (mostly regarding their functions of sediment consolidation and shoreline maintenance) emerged to join earlier descriptive literature (Lugo and Snedaker, 1974). The second half of the 20th century signalled the first public initiatives for mangrove conservation following work that high- lighted their economic value for Florida fisheries due to their role in food web enrichment (Lugo and Snedaker, 1974). Thus, the his- tory of society’s perceptions towards mangrove systems has evolved only recently from being considered as a barren wasteland of unhealthy soils, to being complex ecosystems upon which humans depend. The following sections explore the decline of mangrove forests in the ETP region. 2.2. Early pre-Columbian societies As the 16th century quote from Oviedo (above) implies, man-present improves our understanding of the relationship dynamics between mangroves and humans, and provides a regional informa- tion baseline from which governments can build improved man- agement strategies. 2. An historical timeline of mangrove decline 2.1. Evolution of perceptions & attitudes towards mangroves d Management 368 (2016) 151–162America, the importance of these habitats to indigenous cultures is evident from zooarchaeological data, which supports cultural anthropological inferences about prehistoric subsistence and y anJ. López-Angarita et al. / Forest Ecologecology (Wake et al., 2013). Examples of regional mangrove resource exploitation by pre-Spanish peoples are numerous. When present, mangroves were intensively utilized for timber, charcoal, tannins, shell collection, and fishing (Prahl, 1989; Lacerda et al., 1993). Species that frequent mangroves often represent a large bio- mass accessible from the land, and can be readily harvested by fairly simple techniques (e.g. by hand, and with weirs and traps) (Cooke and Jiménez, 2004). This generated a steady source of ani- mal protein and enhanced human population growth, sedentism and ultimately societal complexity. Dating from the early Forma- tive Period (1800 BCE–200 CE), the coastal culture of Valdivia Fig. 1. The Eastern Tropical Pacific region encompasses the Pacific coasts of Panama, Cost the region according to Giri et al. (2011) is shown. (For interpretation of the references tod Management 368 (2016) 151–162 153(Ecuador) holds evidence not only of broad-based fish and marine molluscs capture from mangrove habitats and shallow intertidal waters, but of hunting for mangrove associated birds like grebes, ibises, ducks and coots (Stahl, 2003). In central Panama, aquatic resources and particularly fresh and preserved fish contributed substantially to the diet of pre-Columbian societies (Cooke et al., 2008). In the early indigenous communities’ transition from nomadic to sedentary living, resource rich habitats such as estuarine man- grove are thought to have played a fundamental role (Prahl, 1989; Lacerda et al., 1993; Raymond, 2008). The earliest and most a Rica, Colombia and Ecuador (red line, inset map). The distribution of mangroves in colour in this figure legend, the reader is referred to the web version of this article.). y ancomplete records of permanent settlements have been discovered in the small coastal valleys of south-western Ecuador (Raymond, 2008). Using carbon dating of fossilized Cucurbita fruit (squash and gourd), Piperno and Stothert (2003) were able to identify an early pattern of agriculture in coastal Ecuador that dates back to the Early Holocene (10–12,000 calendar years ago). Relevant early agricultural sites were located at the interface between marine coastal, fluvial and mainland habitats. Therefore, fertility and diversity of coastal low lands adjacent to mangroves might have provided a suitable place to hunter–gatherer communities in coastal Ecuador while they started cultivating edible plant vari- eties, on their way to establishing fairly sedentary occupations (Piperno and Stothert, 2003). Evidence of pre-Columbian use of mangrove-estuarine resources has been found throughout the ETP: Reitz and Masucci (2004) found that the main invertebrates in deposits of the Ecuadorian coastal settlements, Valdivia and Machalilla, are mangrove-associated molluscs such as the horn shell Cerithidea pulchra and the blood cockle Anadara tuberculosa. Between 700 BCE and 500 CE, the culture called ‘‘Tumaco/Tolita” situated between Buenaventura (Colombia) and Esmeraldas (Ecua- dor), harvested mangrove products, such as molluscs, fish, crabs, birds, and mammals (Villegas et al., 1994; Zuluaga and Romero, 2007). Pre-Columbian societies took advantage of the biologically diverse ichthyofauna of the ETP by exploiting a wide range of spe- cies, mostly marine inshore and euryhaline freshwater fish found in mangrove channels and low salinity shallow waters using tidal traps, weirs, and perhaps hook and line (Cooke and Jiménez, 2004). The importance of fish in the diet is evident in archaeolog- ical sites of the Coclé culture from the lowlands of central Panama, where the targeted fish taxa (e.g. catfish, sleepers, snook, toadfish and croakers), point towards a fishing strategy that focused on intertidal mudflats, mangrove forests and tidal rivers (Cooke and Ranere, 1999). However, not only coastal settlements benefited from the abundant fish resources: In one of the most populated zones in pre-Columbian Panama, the littoral and adjacent wooded savannahs of Parita Bay (a mangrove fringed estuarine system), marine fish bones have been recovered in sites located 13–60 km from the coast (Cooke and Jiménez, 2004). Cooke and Ranere (1999) found that 70% of the fish consumed between 1500 and 1800 years ago in a site 13 km away from the Parita Bay coast, were of marine origin. These included many that frequent man- groves, but also others that eschew this habitat and favour clearer water currents at the seaward edge of the turbid estuarine mixing zone. According to ethnoarchaeological data, it is suggested that fish was preserved to be exchanged with inland communities by salting and sun-drying (Carvajal-Contreras et al., 2008). The facility of sun-drying salted fish for local and regional consumption, and its subsequent distribution inland, is apparent at the Vampiros rock-shelters on an ephemeral ancient strand line in Parita Bay (Carvajal-Contreras et al., 2008). The above summary underlines the potential of archaeozoolog- ical research in Latin America to provide detailed data about how pre-Columbian societies interacted with the coastal habitats through time, in tandem with substantial diachronic geomorpho- logical changes that affect mangrove extent, accessibility and dis- tribution. Much information, however, remains to be uncovered in this field. This type of research is challenging given that: (1) the conservation of archaeological evidence is impaired by the instability and ephemerality of relevant coastal landforms in time and space (Clary et al., 1984; Cooke and Ranere, 1999); (2) the dif- ficulty of accurate identification of species, especially in speciose families and genera with heterogeneous life histories, and (3) the 154 J. López-Angarita et al. / Forest Ecologscarcity of qualified researchers in fish biology and archaeoichthy- ology in most countries (Cooke and Martin, 2010).2.3. Conquistadores and the colony The Spanish were the first to provide written accounts and descriptions of the mangroves of the American continent during their expeditions. Some coastal pre-Columbian societies used man- grove wood, apparently preferentially. In the early stages of the colonial period, however, the Spanish intensified the exploitation of mangrove wood by utilising it heavily for construction, espe- cially shipbuilding, because of its water resistant qualities, hard- ness, length, and girth (De Ulloa and Juan, 1826). Timber harvesting played an important role in construction and leather- work, while mangrove charcoal was used in sugar production. For these reasons, mangrove wood became part of the tax or ‘tri- bute’ that the indigenous communities had to pay the Spanish king (Plate 1) (De Ulloa and Juan, 1826; Prahl, 1989). During the 17th century, the Spanish were eager to broaden their naval domain and promoted the construction of shipyards in strategic cities of Ecuador, Costa Rica and Panama (Guayaquil, Nicoya, Ciudad de Panama) (Jordán Reyes, 2006). These demanded large quantities of wood, such as Tabebuia sensu lato, mangrove, and laurel (Cordia spp.). The Spanish monarchy claimed that the Guayaquil shipyard was the most important of the Pacific coast of the Americas because of the quality of its ships (De Ulloa and Juan, 1826). Between the 16th and mid-18th centuries, the demand for wood for the shipyard and for the construction of churches and buildings in Lima was so high, that mangrove poles exported from the Pacific of Colombia reached six thousand poles per year (Prahl, 1989). Mangrove wood from Ecuador (Esmeraldas and Guayaquil regions) was also exported to Perú to build coastal cities such as Lima, because of the lack of forests in this region (Patiño, 1990). Jorge Juan and Antonio de Ulloa mention the exploitation of mangrove wood in Ecuador in their book ‘Secret news of America’, published in 1747: ‘‘In these works [building and repairing] they employ great quan- tities of mangroves taken from Guayaquil annually by the King- . . .the loss of mangroves and workforce [on the repair of walls], rises to very considerable quantities” (De Ulloa and Juan, 1826). Translation by J. Lopez-Angarita The demand for mangrove wood was so high that the Spanish monarchy were forced to issue regulations for its exploitation, such as licences and permits required for cutting certain species, or in certain areas (Jordán Reyes, 2006). After gaining independence from the Spanish crown in the early 19th century, the young Republics were left without an understanding of the importance of managing their forestry resources, while facing political volatil- ity and instability (van Bottenburg, 1952). Mangrove wood exploitation became a very important industry on the Pacific coast of the continent, with its main hubs in Buenaventura (Colombia) and Guayaquil (Ecuador). Uncontrolled logging activity continued for many years without any replantation of trees (Cifuentes, 2002). Exploitation and commercialization reached industrial levels after 1948, when two businesses located in Buenaventura monop- olized tannin production for the next 30 years. By the 1960s they were producing approximately 3000 tons of mangrove wood per month, mostly red mangrove, Rhizophora mangle (Leal, 2000). By the 1970s mangrove wood exploitation in Colombia for tannin extraction and construction, had reached its peak, and subse- quently collapsed, for two reasons: (1) Prices in Colombia were undercut by the international tannin market, and (2) deforestation levels increased tannin manufacturing effort (Cifuentes, 2002). Large trunks were diverted to making power line poles and railway sleepers (Prahl, 1989). d Management 368 (2016) 151–162For more than 400 years, colonial and republican use of man- grove wood was governed only by profit maximisation, causing y anJ. López-Angarita et al. / Forest Ecologwidespread deforestation. It wasn’t until the 1990s that mangrove forests began to be considered as ecosystems, and managed as such (Lacerda et al., 1993). In Costa Rica, mangroves started to be impacted by coastal development in the early 1940s when the country’s population underwent a rapid rise and began to convert large areas of mangrove stands to agriculture, aquaculture, and wood extraction (FAO, 2007b). By 1982, Ecuador had the world’s largest area dedicated to shrimp production, and in only 30 years following the construction of the first shrimp ponds in 1969, 57% of Ecuador’s mangroves had been cleared for shrimp farming (Ocampo-Thomason, 2006). This was the result of the high interna- tional demand for shrimp and the economic incentives provided by the government (Martinez-Alier, 2001). Panama was one of the first countries in Latin America to estab- lish a commercial shrimp farming industry (Bolanos, 2012) and after shrimp aquaculture began in 1974, production grew rapidly with 8100 ha under production in 1998 (Suman, 2002). However, despite mangrove-lined channels being often eradicated, the most impacted habitat was that of high tidal flats or salt flats (albina in local Spanish) publicly owned and adjacent to mangroves in the central Pacific provinces of the country (Suman, 2002). Into the 1990s mangroves were still important assets in Costa Rica and Panama for tannins and charcoal production (Lacerda et al., 1993). Nowadays, mangrove clearance or other anthropogenic modifi- cation is related to aquaculture, agriculture and urban land uses. Timber extraction still causes degradation of remaining forests, although newer threats include solid waste disposal, pollution, ris- ing sea level and overfishing (Hogarth, 2007). Where mangroves are close to urban areas, their conversion to a constructed environ- ment (e.g. housing, ports, and industries) is widespread (Benfield et al., 2005). Other areas are transformed into arable and grazing land (Giri et al., 2008). However, the most important driver of Plate 1. ‘‘Indigenous exploitation by the Spanish conquerors”. A mural by Diego Rivera (1 quarter). Because of its high quality, large amount of mangrove wood was utilized as bud Management 368 (2016) 151–162 155mangrove loss is aquaculture, in particular extensive shrimp aqua- culture, which is often related to unsustainable practices involving the use of (1) fishmeal production from wild-caught fish, driving overfishing and associated bycatch to feed shrimp, and (2) fungi- cides, pesticides and antibiotics, which pollute ground water and damage soil leading to pond abandonment and prevention of recol- onization by mangroves (Páez-Osuna et al., 2003, 1998). 3. Change in mangrove extent Obtaining reliable estimates of long-term changes in the areal extent of mangroves is compromised by the lack of data and large variance of area estimates. Significant differences between each country’s estimates are apparent. These discrepancies in part reflect the difficulties in arriving at accurate estimates through mapping (Heumann, 2011; Kuenzer et al., 2011). By 1999 it was suggested that certain Latin American countries had lost up to 40% of their total mangrove area (Lacerda and Schaeffer-Novelli, 1999). However, precise estimates of mangrove deforestation are still lacking for the region due to the inherent difficulties in estab- lishing a baseline. Only since the late 1990s has satellite spatial imagery been used for systematically mapping natural resources at a global scale (the Enhanced Thematic Mapper Plus system of Landsat was launched in 1999) and recent advances in remote sensing technology have facilitated the availability of higher reso- lution estimates (Spalding et al., 2010). Even so, many present-day mangrove formations are narrow or patchy, and blend subtly with other habitats, making them hard to detect using satellite data imagery, and estimates prone to error (Manson et al., 2001). To determine the change of mangrove coverage in the ETP we collected published estimates of total mangrove forest area for Panama, Costa Rica, Colombia and Ecuador. We compiled all 929–1945) showing an indigenous workforce involved in wood extraction (top right ilding material. Mexico City – Palacio Nacional. Source: http://tinyurl.com/qdhx3j. estimates available in the literature, from the earliest to the latest, regardless of the detection method (FAO, 2007b,c; Giri et al., 2011; Guevara-Mancera et al., 1998; Lacerda et al., 1993; Prahl, 1989) (Table 1. Supplementary material). In some cases more than one annual estimate was reported (by different sources). Here we aver- aged the estimates and used the standard error as an indicator of or overestimated the real coverage, however, despite the variabil- ity of the data, there is a clear trend of mangrove area decline. From the rate-of-loss data (Table 1), it seems that Panama has experi- enced the greatest overall loss of mangrove cover in the region, fol- lowed by Colombia and Ecuador. Costa Rica shows the highest proportion of intact mangrove forest, but also has the smallest Table 1 The most recent and first available estimates of mangrove area, the percentage lost, and the mean annual rate of loss for the four countries of the Eastern Tropical Pacific. Country Mangrove area (ha) Percentage loss of mangrove area (ha) Annual rate of loss (ha y1) Annual percentage loss rate Most recent estimate (Giri et al., 2011) Earliest estimate (year) Panama 154,227 486,000 (1980)a 68.2 10,702 2.20 Ecuador 137,698 362,727 (1969)b 62.0 5358 1.48 Colombia 213,857 501,300 (1960)c,A 57.33 5636 1.12 Costa Rica 39,034 64,452 (1979)d,A 39.4 794 1.23 A The year of the earliest estimate provided corresponds with the most reliable estimate in relation to the data, hence this year of earliest estimates do not match those of Fig. 2. a,d FAO (2007b). b Ocampo-Thomason (2006). c Villalba (2005). 156 J. López-Angarita et al. / Forest Ecology and Management 368 (2016) 151–162precision for the different estimates. For our calculations, we used the dates of the dataset rather than the date of publication of the estimate, unless the dataset date was not specified. Including all the available figures of mangrove cover will likely increase the error margin of the estimation of trends, however, given the scar- city of historical mangrove area information we decided the possi- ble bias was justifiable. We estimated the change in mangrove area by country and the rate of mangrove loss by calculating the difference between the earliest and latest available estimates of mangrove area. We then divided the change in area by the number of years between the lat- est and earliest estimate (Table 1). We found high variability among published estimates of man- grove area with notable oscillations in time, and a high standard error for area measurements estimated in different sources for the same year (Fig. 2). From this we assume that the irregular results were due to the different techniques being used to conduct year-by-year area measurements since the precision and accuracy of remote sensors can vary significantly depending on methods and mapping objectives (Mumby et al., 1999). As our results repre- sent all existing estimates of the region, they should be interpreted with this in mind. Some values are likely to have underestimatedFig. 2. Change of mangrove area from 1960 to 2010 in the Eastern Tropical Pacific. The g Error bars are calculated using one standard error from the mean for years with more tmangrove area of the four countries. Neighbouring Panama and Costa Rica showed the greatest dif- ference in the magnitude of mangrove area loss. Costa Rica has a strong tourism sector and thanks to the high proportion of pro- tected areas (World Economic Forum, 2013) and national laws in favour of ecosystem conservation, has maintained a successful eco- tourism industry (Krüger, 2005). Therefore, total area of mangrove lost in Costa Rica is low compared to the other countries in the region, as legislation has proven effective in general (Jiménez, 2004). On the other hand, Panama has a growing infrastructure sector, with urban areas spreading rapidly into natural areas such as wetlands, despite protection policies in place (Kaufmann, 2012) (Box 1). The greatest proportion of mangrove destruction in Panama has occurred around Panama City where coastal wetlands have been heavily disturbed in the last two decades as the city grows and land is reclaimed from the sea (Kaufmann, 2012). Beach areas that are near small patches of mangroves, i.e. Punta Chame to San Carlos, have also suffered mangrove loss for tourism develop- ment. Many Panamanian environmental organizations, govern- ment and non-profits, are vociferous about the dangers of mangrove destruction, but political corruption too often inhibits protection and conservation action (Mate, 2005).raph was constructed using all available mangrove area estimates in the literature. han one independent estimate. Box 1 Panama City’s disputed treasure. - at in - te an - tio gr - in - tri th w im t (A us be so , 20 - ne - va 4. The state of mangrove protection in the ETP In Latin America and the Caribbean, Guarderas et al. (2008) found that, despite the increase through time in the number and area of Protected Areas only 1.5% of the coastal and shelf waters of the region are under some type of conservation protection (percentage of exclu- sive economic zone protected: Costa Rica = 0.45%, Panama = 1.18%, Colombia = 9.17%, Ecuador = 12%) (Table 2. Supplementary material). Since lack of protection can be extremely costly in terms of loss of ecosystem services (Tallis and Kareiva, 2005), there is a great need to include highly valuable coastal wetland habitats such as man- groves within protected schemes. Polidoro et al. (2010) found that the highest proportion of threatened mangrove species in the world occur in Costa Rica, Colombia and Panama, with 25–40% of mangrove Box 2 Mangrove diversity in the ETP. There are two major floral realms widely recognized in patterns of mangrove distribution: the Indo West Pacific (IWP) and the Atlantic East Pacific (AEP). The IWP com- prises 57% of the global mangrove area, is rich in species (62) and extends from East Africa eastwards to the Central Pacific; whereas the AEP that encompasses all of the Americas, West and Central Africa only hosts 12 species in 43% of the global mangrove area (Spalding et al., 2010). The major differences in floral composition of mangroves in tropical America started to develop after the closure of the Panama isthmus 3.5 million years ago, which separated the Pacific from the Atlantic. Afterwards very particular climatic processes (dry seasonal climate) that started in the Miocene eragaveshapetotheactualflorawhichhastwodistinctgroups ofmangroves: species restricted to seasonal dry climates, and species restricted to high precipitation climates (Jimenez, 1999). In Panama and Costa Rica there are marked dry and rainyseasons incertainareas,butprecipitationshowsastrong spatial pattern depending on topography. In zones with high terrestrial runoff, mangrove communities can be very exten- sive and diverse. Examples of this are the Golfo de Nicoya and the TA˚rraba-Sierpe delta in Costa Rica, and Golfo de Chiriquı´ andGolfodeSanMiguel inPanama.The largest areas of mangroves in western South America can be found in the humid coastline of the Colombian Pacific and the north of Ecuador (Esmeraldas region),whereasdryer areas in southern Ecuador have limited mangrove cover (Spalding et al., 2010). In the ETP, mangrove swamps are generally more abun- dant on the Pacific coastline as many estuaries, bays and rivers provide a suitable environment for development of 1 : re pa 2 3 C3 J. López-Angarita et al. / Forest Ecology and Management 368 (2016) 151–162 157mangrove destruction can continue, despite existent inter- national agreements and national laws protecting man- groves. Examples like this exist all over the ETP, where wetlands are bought for private use (agriculture, rice and oil palm) without public consultation or in complete defi- ance of their protected area status.3 Historical losses of mangrove cover will never be fully appreci ed (Alongi, 2002), but even the recent reported losses of coverage the ETP highlight the urgent need to strengthen information sys ms and obtain reliable figures on which to base future estimates d conservation measures. The best estimates rely on a combina n of remote sensing images, aerial photos, forest surveys, and ound-truthed maps, yet for remote and inaccessible areas achiev g a high accuracy is still very challenging (Manson et al., 2001). Mangrove losses can be very costly, especially for developing coun es, and are the result of our failure to link ecological processes with eir societal and economic benefits. The need to protect mangroves ith effective conservationmeasures is best advocated by the negative pacts recorded after human-caused perturbations to the habita longi, 2002). As valuation of mangrove services has proven to be a eful tool for proposing a more sustainable use of wetlands, we have en able to understandmore clearly how costly are the ecological and cial implications of mangrove loss (Naylor et al., 2000; Valiela et al. 01; Walters et al., 2008), and have discovered some of the promi nt economic benefits that may represent hope for the future conser tion of mangroves (Aburto-Oropeza et al., 2008; Rönnbäck, 1999). http://www.ancon.org/index.php?option=com_content&view=article&id=452made for re-establishment of the bay’s protection status. This pressurewas effective and onApril 2013, the Court lifted the former suspension of the protected area, emphasizing that the suspensioncontradictsPanamanian laws for thepro- tection of wetlands (Entrada No. 123–12). However, the con- stant conflict of interests competing for the bay’s land, create a continuous legal tug of war for the protected area.2 The case of Panama Bay is a clear example of howThe earliest mentions of Panama City are found in Spanish chronicles from the 16th century, which describe it as ‘‘sick” given its location on ‘‘a lagoonof foul smell”with rivers ‘‘filled with crocodiles”, where the Spanish conquerors used to feed on ‘‘the great quantity of clams” (de Cieza de LeÆn, 2005). Authors describe thewetlands of PanamaBaywith a negative connotationcommonuntil the lastdecadesof the20thcentury (D’Croz andKwiecinski, 1980). Thanks to awareness regarding the importanceof theecosystemservices thatmangrovespro- vide to the capital, PanamaBaywasdesignatedaRamsarwet- land site in 2003 and a protected area in 2009 (CREHO, 2010). In April 2012 the supreme Panamanian Court of Justice approved a ‘‘provisional suspension” of the resolution that created theprotectedarea, reducing the rates formangrove loggingpermits for commercial projects and illegal logging penalties.1 Later in May 2012 the Ministry of Development approved construction of exclusive residential areas inside the protected area. Several environmental protection organi- zations and citizens rejected the Court’s decision and criti- cized it heavily, while protests were held and demandschazo-total-a-nefasta-decision-de-la-corte-contra-area-protegida-bahia-de- nama&catid=102:notas-actuales-ancon&Itemid=225. http://www.aida-americas.org/es/refdocs/1843. http://www.aida-americas.org/es/project/el-humedal-bah%C3%AD-de-panam% %A1-mantiene-su-condici%C3%B3n-de-%C3%A1rea-protegida.extensive coverage, contrasting with the sandy, high-energy shoreline and narrow tidal amplitude of the Caribbean coast (Spaldinget al., 2010).Ahighnumberof tidal flatsand thesig- nificant freshwater input from upstream and precipitation allow mangrove trees of the Pacific coast to grow up to 50minheight,whileonly small andstunted treesnot exceed- ing 5m are found in the Caribbean (FAO, 2007a). Mangroves inLatinAmericaandparticularly in theETPhave relatively low plant diversity (Table 3), with only 11 species (Ya·ez-Arancibia and Lara DomO˜nguez, 1999). However, as an ecosystem they provide great structural complexity creating highly diverse environments that provide multiple ecosystem services. In the ETP the most common genera of mangroves are Rhizophora and Avicennia. These two genera are widely dis- tributed in the continent with the most widespread speciesbeing R. mangle and A. germinans (Lacerda et al., 1993). licie 989 2 can y anTable 2 A summary of the international conventions, regional agreements, and national laws, po Tropical Pacific. Policy description Costa Rica Panama International Level Ramsar Convention on Wetlands Approved in 1991 Approved in 1 Convention of Biological Diversity Ratified in 1992 Ratified in 199 Regional Level Central American agreement for the Central Ameri 158 J. López-Angarita et al. / Forest Ecologspecies classified as threatened under the IUCN Red List Categories of Critically Endangered, Endangered and Vulnerable (Box 2). Despite the high mangrove biomass found in the ETP (Hutchison et al., 2014), mangrove tree species diversity within the region is low relative to other regions (Box 2), making it partic- ularly vulnerable to species loss, and consequently, the effects on human livelihoods and ecosystem services are expected to be greater than in other regions with higher diversity (as systems with higher regional species richness are argued to be more stable) (Worm et al., 2006). Moreover, the ETP suffers from significant gaps in protected area coverage compared to other regions such Regional agreements involving mangroves protection of the environment (1989) the protection of t (1989) Marine Corridor of the Eastern Tropical Pacific (2004) Marine Corridor o Tropical Pacific (2 Central American policy for the Conservation and Rational Use of Wetlands (2002) Central American Conservation and Wetlands (2002) National Level Definition of wetland, land tenure laws 1992. Wetlands are public assets with multiple uses Mangroves are pu Policies and laws relating to mangroves. Exploitation and usage regulations. – 1940. Wastelands Law, mangrove wood extraction needs specific government approval – 1996. Forestry Law limits the exploitation and logging of mangroves – 1998. Biodiversity Law makes all wetlands protected areas, dedicated to the conservation and protection of biodiversity, soil, and water resources. All exploitation prohibited only research and recreation permitted – 1998. General la Environment. Man conservation prior ecosystem with hi and productivity – 2006. The loggin commercialization modification of an prohibited. Only a authority declares sustainable – 2006. Highly val such as mangrove conservation prior – 2008. All wetlan particularly mangr zones of managem National Environmental authority with jurisdiction over mangroves 1978. Ministry of the Environment and Energy National System of Conservation Areas (SINAC) 1998. National Au Environment (ANA 1994. National Sys Areas (SINAP) 2006. Panama Aut Aquatic Resources National research and conservation initiatives – 1993. National Strategy for Wetlands – 1999. National Wetland Programme – 2001. National Policy for Wetlands – 2004. Inventory water bodies with fishing and aquacu – 2010. Inventory and coastal wetlan Republic of Panam Management strategies 1998. All wetlands are protected areas Most Ramsar sites have management plans 2003. The Aquatic Authority issues sp guarantee the sust exploitation of mas and regulations related to mangrove habitats for each of the countries of the Eastern Colombia Ecuador Approved in 1997 Approved in 1991 Ratified in 1992 Ratified in 1992 agreement for Permanent Commission of Permanent Commission of the d Management 368 (2016) 151–162as the Caribbean, as well as little connectivity between existing protected areas (Guarderas et al., 2008). These are factors that highlight the need to focus on designation of a protected area net- work in the region, rather than single reserves established in isola- tion (Guarderas et al., 2008). To explore the characteristics and management strategies of the protected area system in the ETP, we consulted the literature and available information in government websites to create a list of those protected areas that include mangroves and are formally rec- ognized by each national authority. We conducted a review of the management plans of the protected areas identified and, given the he environment the South Pacific includes an action plan for the protection of the coastal areas of the region (1979) South Pacific includes an action plan for the protection of the coastal areas of the region (1952) f the Eastern 004) Marine Corridor of the Eastern Tropical Pacific (2004) Marine Corridor of the Eastern Tropical Pacific (2004) policy for the Rational Use of No regional agreement specifically on wetlands No regional agreement specifically on wetlands blic assets Mangroves are public assets Mangroves are public assets w for the groves are given ity as an gh biodiversity g, use, , and y mangrove are llowed if the activity as uable habitats s have ity d areas and oves are special ent – 1982. Commercialization of mangrove wood poles prohibited – 1995. Logging of certain mangrove species restricted or prohibited – 1996. Any activity that exploits mangrove or associated resources is required to have a special licence – 1998–2002. National Environmental Policy puts all coastal ecosystems under integrated marine and coastal management – 1996. Certificates for Forestry Incentives – 2000. National Policy of the Ocean and Coastal Spaces – 1994. Construction of new shrimp farms prohibited – 2004. Exploitation and logging of mangrove prohibited, for all but ancestral communities – 2004. Forestry Law, license needed to exploit mangroves – 2007. 1 nautical mile from the coastline declared as zone reserved for species reproduction (with specific regulation and uses) – 2008. Shrimp farms obliged to restore 10–30% of the areas illegally occupied – 2008. Conservation and management of fragile and threatened ecosystems such as mangroves regulated by the state thority for the M) tem of Protected hority for 1993. Ministry of the Environment, National Natural Parks of Colombia 2011. National Authority of Fishery Resources Ministry of the Environment of Ecuador 2008. National System of Protected Natural Areas of continental emphasis on lture of continental ds of the a – 1990. Mangroves of Colombia – 1990. Conservation, Management and Use of the Mangroves of Colombia – 2000. National Programme for Mangroves – 1984. Temporal and spatial study of mangroves, shrimp ponds and salinas. This study was updated in 1987, 1991, 1995, 1999, 2004, and 2007 1985. Inventory of mangroves in Continental Ecuador Resources ecial permits to ainable ngroves 1991. Afro-descendant and indigenous communities have authority to manage their traditionally occupied lands 2000. Agreements of sustainable use of the mangroves with ancestral users (a no-take area within a limited take area). To determine how well mangrove habitats are represented in these protected areas, we used data from Giri et al. (2011), representing the latest spatial information of global mangrove coverage available from the World Conservation Monitoring Centre (WCMC). Giri et al. (2011) used 1000 Landsat images, ground-truthed data, and published litera- ture to estimate the global distribution of mangroves. Mangrove area calculations were performed inside and outside protected areas using polygons in ArcGIS 10.2 (ESRI). We estimated the pro- portion of protected mangroves using maps of the protected areas obtained from Protected Planet (www.protectedplanet.net) the online interface of the World Database on Protected Areas, com- bined with national databases from government and non- governmental organisation databases. According to our sources, there are fifty-one protected areas in J. López-Angarita et al. / Forest Ecology and Management 368 (2016) 151–162 159multiple management categories found, we classified the protected areas following Guarderas et al. (2008) into: no-take protected areas, limited-take protected areas, and mixed-use protected areas Table 3 Mangrove species found in the Eastern Tropical Pacific. The IUCN column provides the sp Vulnerable, (LC) Least Concern. Species Common name IUCN Acrostichum aureum Helecho de playa LC Avicennia bicolor Mangle salado, negro, o prieto VU Avicennia germinans Mangle negro o iguanero LC Conocarpus erectus Mangle Jelí LC Laguncularia racemosa Mangle blanco LC Mora oleifera Mangle nato VU Pelliciera rhizophorae Mangle piñuelo VU Rhizophora mangle Mangle rojo LC Rhizophora racemosa Mangle rojo LC Rhizophora  harrisonii Mangle rojo – Tabebuia palustris Mangle marica VU Total Fig. 3. The number of protected areas including mangroves in the ETP by country and management category (no take, limited take and mixed use) (Upper panel). Total mangrove area by country in the ETP, and percentage included in protected areas (Lower panel).the ETP that include mangroves and these cover a wide range of management categories and schemes (Table 3. Supplementary material). Twenty-two occur in Costa Rica, 15 in Panama, 10 in Ecuador and 4 in Colombia (Fig. 3). Protection schemes range from national parks to wildlife refuges and ecological reserves managed by local communities. There are marked differences in the manage- ment approaches of each of the countries. Costa Rica and Panama have a higher proportion of no-take protected areas than Ecuador and Colombia. In Costa Rica coastal wetlands are all no-take areas (RAMSAR, n.d.) (Table 2), so any protected areas that allow use of non-wetland natural resources and have mangroves within their limits are classified as mixed-use protected areas. Mangrove repre- sentativeness results show that at a regional level 47% of the total mangroves of the region are included within protected areas. Costa Rica and Panama lead the region in mangrove protection, with 58.7% and 51.9% respectively, whereas Colombia, at 23.7%, has the lowest proportion of protected mangroves in the region. Among the key protected areas in the region, which conserve a high proportion of mangrove area are the Terraba–Sierpe Ramsar wetland in Costa Rica (Plate 2) with an extent of 30,000 ha, San- quianga National Park in Colombia with 80,000 ha, and the Ecolog- ical Reserve Manglares Cayapas Mataje in Ecuador with 51,300 ha. As a general trend across the ETP, there is poor documentation on the governance of protected areas and many still lack management plans. Additionally, the administrative structure of protected areas were originally designed for terrestrial areas, but recently govern- ments have increased the representation of marine areas and habi- tats in protected areas (Alvarado et al., 2012). Official agreements for marine conservation facilitate the implementation of participa- tory management schemes for protected areas (García, 2010), with the aim of generating economic alternatives for communities, such as ecotourism (TNC, 2011). Evidence of participatory management processes and schemes during the creation and administration of ecies conservation status according to the IUCN Red List of Threatened Species: (VU) Costa Rica Panama Colombia Ecuador X X X X X X X X X X X X X X X X X X X X X X X X X X X X X X X X X X X X X X X X 10 11 11 8 We reviewed all existing environmental policies related to waste lands in Latin America because governments failed to under- stand their ecological significance. Nor did they understand their mou y anmangroves at international and national levels, by searching the literature, soliciting legal documents from government offices, and consulting their websites (Table 2). We found that as recentlythe protected areas are limited, even though governments officially recognize their importance (Fundación Futuro Latinoamericano, 2011). 5. Environmental policy related to mangroves Plate 2. Mangroves of Costa Rica showing an aerial view of a mangrove fringed river (right panel). Photo (c) López-Angarita, J. 160 J. López-Angarita et al. / Forest Ecologas 30 years ago, wetlands and especially mangroves were consid- ered unproductive land by local governments. The ignorance of the value of mangroves in terms of provision of ecosystem services, or merely the attraction of short-term financial gains to be had from developing mangrove land, enhanced their destruction and clearance. Frequently governments and multinationals like the World Bank and the International Monetary Fund encouraged this attitude (FAO, 2007c; Ocampo-Thomason, 2006; Warne, 2011; Yañez-Arancibia and Lara Domínguez, 1999). This situation started to change in the 1990s as a result of increased global awareness of ecosystem services, and soon governments of the ETP joined inter- national movements towards more environmentally oriented poli- cies through international initiatives, such as The Ramsar Convention on Wetlands and the Convention on Biological Diver- sity (CBD). Regional agreements emerged later such as the Central Ameri- can Policy for the Conservation and Rational Use of Wetlands (2002), a common working agenda to strengthen the conservation and sustainable use of wetlands through regional cooperation and action. In South America, the Permanent Commission of the South Pacific created an action plan for the protection of coastal areas of the region (1981). Decades later, in 2004, the UNESCO declared the Marine Conservation Corridor of the Eastern Tropical Pacific (http://whc.unesco.org/en/seascape/) aiming to support the sus- tainable use of marine natural resources in the ETP, through the establishment of joint regional policy strategies that are supported by the community at large, international cooperation mechanisms and non-governmental sectors (www.cmarpacifico.org). The coun- tries in the ETP have different approaches to mangrove protectiongreat importance for local subsistence economies and, ironically, lucrative export resources such as shrimp. A shift in attitudespolicies ranging from full protection to managing them as crucial components for human livelihoods (summarised in Table 2). 6. Prospects for the mangroves of the ETP For a long time mangroves were considered tantamount to th in Golfito (left panel) and the mangrove forests of Terraba–Sierpe protected area d Management 368 (2016) 151–162began to appear in the 1990s in the face of increasing numbers of scientific investigations that demonstrated the utility of man- groves for human well being (Lacerda et al., 1993). Concomitantly, Latin American environmental policy underwent a transformation and approved many international agreements (e.g. CBD, Ramsar, CITES), which led to the modification of political constitutions. New environmental legislation was passed, and several conserva- tion and research initiatives started with the assistance of interna- tional agencies and NGOs (Columba, 2013; CREHO, 2010; Ministerio de Medio Ambiente, 2002; SINAC, 2010). Currently the appearance of much new legislation and of the proliferation of pro- tected areas, bear witness to the political will of Latin American countries to conserve their mangroves. However, coastal deforesta- tion persists in the region despite of the emplacement of protection mechanisms such as protected areas and national environmental policies (Box 1). Other noteworthy problems persist, such as the lack of resources for implementing new policies, weak institutional platforms, and the need for qualified personnel (López Angarita et al., 2014). In addition enforcement is often not effective (Alvarado et al., 2012; García, 2010; TNC, 2011). Even though the new legislation is laudable and often effective, it is imprudent to assume that illegal activities have ceased in mangroves. They have not. There are still illegal activities threatening mangroves in all nations, highlighting the need for institutional capacity to support legislation (FAO, 2007c). Natural resource management of interface habitats such as mangroves can be highly challenging given the multiple sectors with jurisdiction over them (e.g. fisheries, forestry, agriculture, urban development, transport), all with differing agendas and y anpositions on their use (Box 1). This translates into frequent con- flicts of interests between sectors, often disregarding mangrove conservation, a risky situation given the strong cohesion and asso- ciation of mangroves and local livelihoods. In coastal communities with strong ecological and social linkages conservation has a higher economic value than any form of destructive exploitation, such as logging or aquaculture. These linkages are bound to be stronger in highly connected regions such as the ETP, where non- destructive mangrove exploitation represents the main livelihood activity for many local communities. The ETP region needs to protect mangroves effectively, with tangible actions and accurate figures, by taking advantage of the existent regional agreements and commitments, homogenizing political barriers, and framing sustainable development objectives at a regional level. Acknowledgements This research was funded by fellowships (J. López Angarita) from the Colombian Department of Science and Technology (COL- CIENCIAS), the Schlumberger Foundation Faculty for the Future Programme, the World Wildlife Fund’s Russell E. Train Education for Nature program, the Smithsonian Tropical Research Institute, and Save our Seas Foundation. We thank Dr A. Altieri for insights on an early manuscript. This work is dedicated to the memory of the Colombian botanist and historian Santiago Díaz Piedrahita (1944–2014), who shared his extensive knowledge and passion about Spanish conquest chronicles and botany, and provided active insight to this research. 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