Ecosystem services provided by amphibians and reptiles in Neotropical ecosystems

Abstract

Human welfare depends directly or indirectly on the services provided by ecosystems. Amphibians and reptiles represent a high proportion of global species diversity and include species that are widely distributed throughout the world and play a variety of roles that benefit humans. The aim of this study was to identify and describe the ecosystem services provided by amphibians and reptiles in Neotropical ecosystems to evaluate the contribution of these highly diverse groups to human welfare. We conducted a literature review of articles and books from databases and university libraries and collected data from 106 studies. Amphibians and reptiles contributed directly and indirectly to the four types of ecosystem services: provisioning, regulating, cultural, and supporting. Most available studies reported the use of direct services from reptiles and indirect services from amphibians. Although eight ecosystem services were identified, most studies focused on reptiles as seed dispersers and protein sources. Biological pest control and bioturbation were the most widely studied services obtained from amphibians. Further research are necessary to understand the ecological functions involving amphibians and reptiles and their importance in the provision of key ecosystem services for human well-being.

Keywords:

• amphibians
• reptiles
• ecosystem services
• ecological functions
• human welfare

1. Introduction

Amphibians and reptiles represent a great diversity of species that are widely distributed across the globe and carry out a variety of functions in the Earth's ecosystems (Valencia-Aguilar et al. 2012). The two groups are similar in some respects; for example species from these two classes occupy close habitats, are ectotherms, and are similarly vulnerable to habitat degradation, disturbance, pollution of the environment, introduction of exotic species, etc. (Pough et al. 2004; Goldstein et al. 2005; Andrews et al. 2008). In Neotropical ecosystems, these groups play a key role in energy flow and nutrient cycling in both aquatic and terrestrial environments, in addition to helping control pest populations and potentially acting as pollinators and seed dispersers (Valencia et al. unpublished results).

Many organisms add value to human life, for example, plants and animals are used to produce medicine, food, clothing, and building materials, among other important resources. However, economic value is not the only reason to conserve biodiversity; all organisms, as components of ecosystems, contribute directly or indirectly to ecosystem functions and provide numerous services to humanity (Collins & Crump 2009).

According to the Millennium Ecosystem Assessment (MEA 2005), ecosystem services are the benefits obtained by human populations from ecosystems and are classified as follows: provisioning services (which directly meet human needs for food, fuel or building materials such as wood); regulating services (regulatory functions that are performed by ecosystems and generally allow for societies to have water and to rely on natural phenomena and weather patterns); cultural services (which are valued because of the well-being associated with recreational, spiritual or aesthetic experiences); and supporting services (which support other types of services and sustain ecosystems and biodiversity) (Martín-López et al. 2009; Haines-Young et al. 2010a; Nelson & Daily 2010).

Some authors have suggested a broader definition in which ecosystem services are considered to include any aspect or component of an ecosystem used directly or indirectly by people to improve their well-being. In this sense, ecosystem services include the structure of the ecosystem itself and the processes and functions of the ecosystem, due to the integration of these aspects, the essential human requirements for daily life can be met (De Groot et al. 2002; Díaz et al. 2006; Fisher et al. 2009; Martín-López et al. 2009; Haines-Young et al. 2010b). Based on this broader concept, two types of uses can be identified in general for humans: direct-use services, are those used or consumed directly by humans (i.e., provisioning and cultural services), and include food, crops, wood for fuel or construction, medicinal products, and hunting, in addition to recreational and cultural activities such as enjoying the outdoors, wildlife watching, water sports, and other spiritual or social utilities that do not require the production of goods (DeFries et al. 2005).

In contrast, indirect-use services, are those used or consumed indirectly by humans, though the positive externalities that ecosystem provide, supporting the production of others services, these include: regulating ecosystem services such as pollination, seed dispersal, climate regulation, carbon sequestration, and the control of pests and diseases, and also supports ecosystem services, these are necessary for the production of all direct services. For example, by influencing primary production and processes, such as water and nutrient cycling, biodiversity indirectly supports the production of food, fiber, and shelter (DeFries et al. 2005).

It is critical to understand both extent to which ecosystem services are important to human well-being, and the relationships between a group of individuals within a species, their ecological functions, and the ecosystem services they provide, because ecological degradation and simplification can lead to a decrease in the ecosystem services that are likely to have a negative impact on the human welfare (Luck et al. 2003; Raudsepp-Hearne et al. 2010). Therefore, the objective of this study was to identify and describe the ecosystem services provided by amphibians and reptiles in Neotropical ecosystems to understand their ecological roles and the importance of these groups to human welfare. This can also contribute to highlight the value of these groups and thus consider these services among motivations for their conservation.

2. Data sources

The data used in this analysis were compiled from the following sources: (1) bibliographic databases ISI WEB OF KNOWLEDGE, JSTOR, SCOPUS, and, in certain cases, Google Scholar, from which journal articles were downloaded; (2) book chapters; (3) information provided by national and international researchers; and (4) the Celsius bibliographic exchange platform of the Universidad del Valle, from which a number of papers were requested. Search queries were restricted to the following keywords: ecosystem services, amphibian, reptiles, frog, toad, caecilian, salamander, lizard, snake, caiman, turtle, and tortoise; and combinations of the words amphibians and reptiles with hunting, meat, trade, feeding, consumption, biological control, mosquito control, diet, predation, food habit, seed dispersal, seed ingestion, dispersers, frugivory, saurochory, pollination, foraging, and flower.

2.1. Data collection

Data regarding the ecosystem services that amphibians and reptiles provide were collected from publications, written in English, Spanish, and Portuguese, and from the past four decades (1970 to 2012) for the 32 countries located in the Neotropical zone. The resulting information was classified according to, the type of ecosystem service, the specific ecosystem service, and the use type (direct or indirect). This paper is divided in two main sections: the first addresses the quantity of data collected, and the second reviews the ecosystem services provided by amphibians and reptiles according to the previously described classification.

The classification proposed by the MEA (2005) was chosen, although other classifications of ecosystem services have been proposed (De Groot et al. 2002; Boyd & Banzhaf 2007; Fisher et al. 2009), because it is the best known and reported in the literature, it is easy to understand for stakeholders, and it is key to have dialog with policy-makers.

3. Results

The data query regarding ecosystem services provided by amphibians and reptiles generated 106 studies, of which 68% dealt with reptiles and 32% with amphibians. Eighty-three per cent of these studies were conducted in South America (71% focused on reptiles, 12% on amphibians), followed by Central America with 13% (9% for reptiles, 4% for amphibians) and the Caribbean with 4% (1% reptiles, 3% amphibians). Studies were found to address at least one of the evaluated groups (either amphibians or reptiles) in 53% of the countries in the Neotropics. However, only 12% of the countries had at least one study for both groups. Sixty-four per cent of the studies were conducted in the South American countries of Brazil, Argentina, and Venezuela, which together comprise only 9% of the countries in the Neotropics.

The data from studies dealing with amphibians or reptiles from the past four decades were categorized into the four types of ecosystem services, within eight services; supporting: nutrient cycling, bioturbation; regulating: biological control, seed dispersal; provisioning: protein sources (food source), raw materials and medicinal resources; and cultural: rituals. For the 1970s, only studies related to regulating and supporting services provided by caiman species in aquatic systems of the Brazilian Amazon and by anuran tadpoles in island aquatic systems were found. For the 1980s, studies were found examining the role of frogs and lizards in seed dispersal and the use of certain amphibian species and reptiles by rural and urban communities to obtain protein and raw materials. During the 1990s, studies similar to those of the previous decade and research on the contribution of tadpoles to nutrient cycling through bioturbation were conducted. In the last decade, the number of studies has continued to increase, and new studies have addressed the discovery of new medicines and the use of reptiles and amphibians in cultural practices and religious rituals (Figure 1).

Figure 1. Number of studies from the past four decades regarding ecosystem services provided by amphibians and reptiles in Neotropical ecosystems.

Four services of indirect use and four services of direct use were identified (Figure 2). For most of the studies (61%), the ecosystem services were categorized as provisioning services, with 53% focusing on documented use (food and commercial markets) of amphibians and reptiles in rural and urban communities.

Figure 2. Number of studies addressing Neotropical amphibians or reptiles, categorized by use value. A. Indirect-use services, necessary for the formation and renewal of natural resources. B. Direct-use services from which people directly obtain goods.

Ten per cent of the studies related to supporting services: 4% evaluated the role of frogs and caiman species in nutrient cycling and 6% examined how certain species of tadpoles (frogs) influence ecosystem functions through bioturbation. Twenty-seven per cent of the studies were categorized into regulating services: 20% identified lizard or turtle species as potential dispersal agents; and 7% assessed the importance of frog species in the biological control of herbivorous arthropods and human disease vectors (Figure 2A). Animals used for medicine were reported in approximately 8% of the studies (Figure 2B). Only 1% of the studies were related to cultural services, in which the animals were used for religious rites and ceremonies.

In total, 176 species of amphibians and reptiles were reported to potentially provide direct or indirect services to human societies. Of these species, 40 were amphibians belonging to 10 different families and one order. Amphibian species from the families Hylidae and Bufonidae were mentioned most frequently for supporting, regulating, provisioning, and cultural services, while species of the Leptodactylidae and Ranidae families were exclusively linked to supporting and provisioning services. For reptiles, 136 species belonging to three orders, two sub-orders and 30 families were described. The family Alligatoridae was mentioned in the studies related to supporting services; the families Iguanidae, Liolaemidae, Scincidae, Teiidae, Testudinidae, and Geoemydidae were linked to regulatory services; the families Alligatoridae, Teiidae, Boidae, Colubridae, Viperidae, Podocnemididae, Testudinidae, Cheloniidae, and Dermochelyidae were linked to provisioning services; and the families Testudinidae and Chelidae were mentioned as important for cultural services.

3.1. Direct-use services

3.1.1. Provisioning ecosystem services

3.1.1.1 3.1.1.1. Food sources

High production efficiency improves people's access to food, so efficient food production is one of the principal services provided by ecosystems (Laterra et al. 2011). Wildlife is an important food resource that provides animal protein to human populations (Aquino et al. 2007). Many species, from invertebrates, fish and amphibians to reptiles, birds, and mammals, have been and continue to be used to improve human well-being (Nasi et al. 2008). Within the amphibian and reptile groups, some species are important historical and current food sources for the inhabitants of rural areas in different parts of the world and are utilized to meet basic subsistence needs (Mittermeier et al. 1992; Thorbjarnarson et al. 2000). For example, the indigenous Chortí people of Honduras, similar to their pre-Hispanic predecessors, consume the anurans Lithobates berlandieri, L. maculatua, and L. vaillanti; the turtles Kinosternon scorpioides, Chelydra serpentina and Rhinoclemmys pulcherrima; the lizards Ctenosaura similis and Iguana iguana; and the snakes Boa constrictor and Crotalus durissus (Marineros 2007).

Until a few decades ago, the Miskito indigenous societies of Nicaragua relied heavily on meat, skin, shell, fat, and calipee (a gelatinous substance used as a basis for turtle soup) from the marine green turtle Chelonia mydas for their livelihoods. But due to the overexploitation of this turtle, however, turtle populations declined (Nietschmann 1974; Bräutigam & Eckert 2006). The capture of marine turtles (Lepidochelis olivacea, Caretta caretta, Dermochelys coriacea, etc.) for food and handicrafts manufacturing has declined due to regulations that have the Neotropical coastal countries for your protection. But still, it is evident catches and illegal traffic of these species, especially their eggs, in these countries (Bräutigam & Eckert 2006).

The mountain chicken Leptodactylus fallx is a large frog (snout-vent length of 135 mm), habitat of Montserrat and Dominica, West Indies, which is used as a food item and as its name derives from the fact that its meat taste like chicken (Malhotra et al. 2011). The island of Dominica formerly had an estimated annual harvest of 8000–36,000 animals (Fa et al. 2004).

The lizards Tupinambis rufescens and T. merianae, which are prized for their flavor, comprise 32% of the wild meat that some groups in Argentina, Bolivia, and Paraguay incorporate into their diets (Norman 1987; Bolkovic 1999; Cuellar 2000; Hill & Padwe 2000). The flesh of these lizards has nutritional value for humans and is considered as a high-quality food source because of its balanced fatty acid content and low cholesterol levels compared with beef, chicken, and some fish (including perch and rainbow trout). The meat of T. merianae contains relatively low cholesterol levels and could provide an interesting alternative for human consumption (Caldironi & Manes 2006). In addition, reptiles such as B. constrictor, Chelonoidis chilensis, C. denticulata, Chelonoidis spp., Podocnemis unifilis, Caiman yacare, Melanosuchus niger, and Lachesis muta are frequently consumed by people living in Argentina, Bolivia, and Paraguay (Bolkovic 1999; Arispe & Rumiz 2002; Tejada et al. 2006).

In the Amazon region of Colombia, Brazil, and Peru, wildlife has historically been and continues to be an important source of animal protein for rural communities and indigenous ethnic groups (Wetterberg et al. 1976; Aquino et al. 2007; Mancera & Reyes 2008). These groups extract more than 67,000 tons of wildlife meat from the region annually (Wetterberg et al. 1976; Gomez et al. 1994 in Mancera & Reyes 2008). Turtles and caimans are two of the most important sources of protein in rural and indigenous diets, with many people consuming Podocnemis expansa, P. lewyana, P. unifilis, Chelonoidis carbonaria, C. denticulata, Chelus fimbriatus, Chelydra serpentina, Kinosternon spurelli, K. scorpiodes, Rhinoclemmys melanosterna, R. nasuta, R. punctularia, Trachemys callirostris, Caiman crocodilus, Paleosuchus trigonatus, and M. niger. These species are important to rural communities because of their nutritional contribution (Milton et al. 1991; Fachín et al. 1996; Rubio 1996; Peres 2000; Remor et al. 2000; González 2003; Peres & Nascimento 2006; Aquino et al. 2007; Cuesta-Ríos et al. 2007; Racero-Casarrubia et al. 2008; De la Ossa et al. 2011).

Commercial hunting of caiman meat began in the 1970s, just as the hide trade declined. In Mamirauá, Brazil, where the alligator species M. niger and C. crocodilus were hunted for the sale of meat, kill levels reached 115,000 kg of fresh meat (approximately 5230 M. niger individuals and 2865 C. crocodilus individuals) in 1995. The dried meat was sold in the state of Pará, Brazil, and in Colombia, generating approximately $57,600 USD for local communities (Da Silveira & Thorbjarnarson 1999). Despite the market for meat, hunting alligators for hides was much more lucrative due to the high prices of hides and the lack of traditional consumption of alligator meat (because of the abundance of fish) (Da Silveira & Thorbjarnarson 1999).

In Manaus, Brazil, and in Venezuela, many species of wildlife, particularly P. expansa, P. unifilis, and P. vogli, are often consumed by local inhabitants in restaurants. Additionally, the trade in these species fuels the bushmeat markets in some regions of Brazil (Wetterberg et al. 1976). Exploitation of wildlife resources in Venezuela has caused a problem for the sustainability of these species. Despite the availability of other sources of protein in the region (such as fish), villagers have a strong tradition of turtle consumption due to the quality of turtle meat. Conservation programs have achieved little success in protecting the turtles in the region (Hernandez & Espin 2003).

In some rural areas of Mexico, animal protein from bushmeat is estimated to make up 70% of the human protein intake, representing an important supplement to local diets (Loa et al. 1998). For example, in the northern Yucatan, hunting is a common practice for farmers and is primarily aimed at meeting food needs. Iguanas (Ctenosaura spp.) and crocodiles (Crocodylus moreletii) are among the animals consumed (Ortega et al. 1999). For indigenous and mestizo communities in Chiapas, the hunting of wildlife is an important subsistence activity provisioning food for many people without sufficient funds to purchase meat every day. Dermatemys mawii, Trachemys scripta, C. moreletii, Ctenosaura similis, Iguana iguana, and B. constrictor could represent, in some cases, a valuable source of protein; these reptiles make up 1% of the total species hunted (Naranjo et al. 2004; Naranjo & Cuarón 2010; Naranjo 2012). Also, in Baja California peninsula, Pacific Mexico, the marine turtles has been harvested for food, this coupled with bycatch mortality was estimates to be as high as 35.000 turtles per year, representing a region with one of the highest known sea turtle mortality rates in the world (Senko et al. 2011).

3.1.1.2 3.1.1.2. Raw materials and trade

Many Latin American countries export amphibians and reptiles for trade in North America, Europe, and Asia (Thorbjarnarson 1991). For example, between 2002 and 2008, more than 1.48 billion live animals were imported into Texas to be sold as pets, including Dendrobates auratus, Dendrobates pumilio, Dendrobates tinctorius, T. merianae, B. constrictor, Epicrates cenchria, Lampropeltis triangulum, and C. Carbonaria. The market prices for these species ranged between $30 and $22,500 USD (Prestridge et al. 2011).

In Costa Rica and in Nicaragua, farmers use iguana (I. iguana) skin to make crafts, purses, wallets, shoes, and bags (Peters 1993). On the Pacific coast of Honduras, the L. olivacea egg trade has been a major economic activity locally and regionally for more than 40 years and serves as an alternative or supplementary income source. In El Salvador and in Honduras, almost 100% of the eggs from the clutches of these turtles have been collected and sold, amounting to $7680.30 USD in trade in one season (Lagueux 1997). Tortoises of the genus Kinosternon and Podocnemis have similarly been exploited in the Brazilian Amazon. Due to the overexploitation of these species for their meat and the industrial use of their eggs, in the early 1980s the use of these tortoises was reduced to small cottage industries for the production of home remedies and cosmetics (Alho 1985).

In Nicaragua, the pet trade (for exportation) of amphibian species belonging to the genus Agalychnis and Dendrobates and reptiles such as B. constrictor, L. triangulum, Basiliscus spp., and Scheloporus malachitus, generated more than $1.5 million USD in 1996 and represented 70% of the animals exported from the country (Jori 1998 cited by Chardonnet et al. 2002). Colombia, which has a high potential in trading wildlife goods and services due to high levels of native biodiversity (Mancera & Reyes 2008), received more than 50 million USD as income from wildlife exports between 1929 and 1969, with reptiles representing 36.73% of the total wildlife exports. In 1998, iguana and hicotea turtle eggs brought in revenues of $90 million and $5 billion USD, respectively (Baptiste et al. 2002 in Mancera & Reyes 2008).

The Neotropics contain 9 of the 22 species of crocodiles existing in the world, which have been exploited commercially for their hides and exported to Uruguay, the United States, Germany, France, Holland, England, Italy, and Japan. This trade began in the twentieth century in Argentina, Bolivia, Brazil, Colombia, Ecuador, French Guiana, Guyana, Paraguay, Peru, Suriname, Trinidad and Tobago, and Venezuela. The export of Crocodylus acutus, C. moreletii, C. intermedius, and M. niger (Pefaur 1996) shifted to the genus Caiman, reaching exports of approximately 11,649,655 hides (Colombia) and 300,000 hides (Bolivia) of C. crocodilus and C. yacare between 1950 and 1980 (Medem 1981, 1983). The spectacled caiman (C. crocodilus) and the black caiman (M. niger) are two of the Latin American crocodiles which are mostly exploited by the leather industry. From 1960 to 1980, an average of 7.5 million hides were exported to the United States, Europe, and Japan, of which the vast majority came from wild catches with only a small percentage from ‘ranching’ (Thorbjarnarson 1991; Da Silveira & Thorbjarnarson 1999; Ojasti & Dallmeier 2000).

In the last decade, more than 30 tons of hides and 28 tons of meat from C. yacare were exported from Bolivia to Germany, Belgium, Canada, China, Spain, the United States, France, Hong Kong, Italy, Japan, and Thailand, among other destinations. The C. yacare trade earned between $11 and $122 billion USD for Bolivia. This type of alligator meat is prized in many countries for its exotic flavor and its high protein (18.68%) but low calorie, cholesterol, and saturated fat (0.57%) contents. The high demand for C. yacare hides is related to their quality and the competitive export prices (Institito Boliviano de Comercio Exterior 2010). Other products derived from caimans can provide additional income sources: in Brazil and in Venezuela, the fat (used for soap) and the largest teeth (used to make ivory ornaments) of caimans were also exported (Medem 1983). The development of facilities to extract other products from caiman carcasses, such as bone meal from the skeleton and secretions from the paracloacal musk glands used in perfume production, could generate additional revenue (Thorbjarnarson 1991).

The decline of wild crocodile, caiman, and iguana populations due to their rapid exploitation, combined with the growing international demand for hides, led to the development of breeding farms for the export of hides and meat (Larriera et al. 2008; Mancera & Reyes 2008). This recent activity has gained prominence in the international trade for individual animals and products generated through captive breeding. The focus has been on the production of the hides and meat of babilla crocodiles (C. crocodilus and C. crocodilus fuscus), caimans (C. acutus, C. fuscus, C. latirostris, and C. yacare), iguanas (I. iguana), lizards (Tupinambis nigropunctatus, and T. teguixin), and boas (B. constrictor). These products are exported to the United States, Thailand, Singapore, Japan, Italy, France, China, and Mexico, among others, generating between $20 and $25 million USD annually (Palacios et al. 1999; Nassar-Montoya 2000; CGR 2005 cited by Rivera 2005; Mancera & Reyes 2008).

Lizards from the genus Tupinambis have traditionally been hunted by indigenous and rural communities for subsistence (Norman 1987; Fitzgerald et al. 1994). In the past decades, this resource provided an important source of income, and despite decline in demand, Tupinambis hunting remains one of the few economic alternatives for residents living within its range (Fitzgerald 1994b; Bolkovic & Ramadori 2006). The exploitation of these lizards is important at all levels of the economy in countries such as Argentina and Paraguay. Each year more than 1,900,000 hides from the species T. teguixin and T. rufescens are exported to the United States, Canada, Mexico, Hong Kong, Japan, and several European countries, generating over $20,000,000 USD for the export countries (Norman 1987; Fitzgerald et al. 1991; Fitzgerald 1994a, 1994b; Fitzgerald et al. 1994).

Despite the importance of Tupinambis as a renewable natural resource, the populations of this species have never been managed, rather being merely exploited by the international demand for hides (Fitzgerald 1994b; Fitzgerald et al. 1994). The hunting of these lizards in various locations (both traditional and new sites) has profound implications for the long-term stability of their populations and the tanning industry that depends on them. Despite high hunting rates, the Tupinambis populations have not yet disappeared because of their high density and the availability of their habitat. However, some studies indicate that these populations are becoming more vulnerable due to hunting pressure on the larger individuals (males and females), which are usually the breeders (Fitzgerald et al. 1991).

3.1.1.3 3.1.1.3. Medicinal resources

Amphibian skin is a morphological, physiological, and biochemically complex organ that meets a wide range of functions necessary for the survival of amphibians. The skin contains granular glands which synthesize a wide range of chemical compounds that protect against infection by bacteria, fungi, and predators. The number and diversity of compounds produced by the granular glands in amphibian skin is surprisingly high, and the compounds include biogenic amines, bufodienolides (bufogenines and bufotoxines), alkaloids, peptides, and proteins (Daly et al. 1987; Clarke 1996; Wells 2007). Given the respiratory and antimicrobial functions of amphibian skin, some of the molecules found in secretions could likely be useful in treating skin and respiratory infections (Clarke 1996). Some of these compounds have been isolated, identified, and characterized leading to the development of medicinal products for human and veterinary uses (Clarke 1996; Tyler et al. 2007).

The skin of the genus Phyllomedusa is a rich source of peptides with many potential uses including antimicrobial, neurological, and muscular. In recent decades, more than 200 peptides from more than 10 species of Phyllomedusa have been identified and are being used in the development of new drugs to fight nosocomial infections and infections that are resistant to multiple drugs (De Azevedo et al. 2010). The secretions from the skin of Phyllomedusa bicolor contain a variety of vasoactive peptides including high levels of phylloceruleina, phylloquinina, phyllomedusin and sauvagine, and small quantities of deltorphin (Daly et al. 1992). Reports on the discovery and isolation of alkaloid epibatidine, secreted by the frog Epipedobates tricolor, indicate that this alkaloid has significant analgesic activity and is 200–500 times more powerful than morphine and 200 times stronger than nicotine (Damaj et al. 1994 in Elguero et al. 1996). Despite the side effects of epibatidine at analgesic doses, several studies are evaluating a derivative of this alkaloid to determine its possible therapeutic application in such diseases as Parkinson's and Alzheimer's and in pain management (Elguero et al. 1996; Daly et al. 2006).

Many reptiles produce large quantities of strong poisons, primarily complex mixtures of peptides, proteins, and biomolecules that can produce various effects in humans. The study of these toxins has contributed to the development of pharmaceuticals, and many of the compounds isolated from these natural sources are now used to manufacture drugs for the treatment of human diseases (Mackessy 2010). Research has demonstrated the existence of antimicrobial properties in the venom of Neotropical snakes, particularly snakes from the genus Bothrops. Studies on Bothrops jararaca venom indicate that components of the venom, including LAAO (L-amino acid oxidase) and antithrombin proteins have important pharmacological and antimicrobial qualities (Batista et al. 2008; Ciscotto et al. 2009).

3.1.1.4 3.1.1.4. Traditional medicine and beliefs

In many cultures, particularly those with limited or no access to primary medical services, animals have been used as medicinal sources and are integral to healing practices (Alves et al. 2007, 2009). Reptiles are among the most utilized animal groups in traditional folk medicine, and their role in the prevention and cure of disease has been reported in various socio-cultural contexts worldwide (Alves & Santana 2008). For example, some indigenous groups in the Amazon associate P. expansa with cultural concepts of social formation, human settlements, marriage, agricultural production, fluvial landform ownership, fertility, and abundance (Von Hildebrand et al. 1997).

In Argentina, Brazil, Colombia, Mexico, Paraguay, and Venezuela, rural and some urban communities use more than 60 amphibian and reptile species for medicinal purposes. Medicinal products from the skin, meat, fat, eggs, shell, and rattles of reptiles such as Amphisbaena fuliginosa, Cnemidophorus ocellifer, T. merianae, T. nigropunctatus, I. iguana, B. constrictor, Corallus caninus, Eunectes murinus, Bothrops asper, C. durissus, L. muta, Porthidium nasutum, C. denticulata, C. mydas, K. scorpioides, P. expansa, Phrynops geoffroanus, C. yacare, and C. crocodilus, and the skin and fat of Rhinella jimi, Leptodactylus labyrinthicus, and Leptodactylus vastus are used and sold in rural markets for the treatment of diseases such as asthma, rheumatism, bleeding from wounds, arthritis, osteoporosis, tumors, cancer, inflammation, pterygium, epilepsy, erysipelas, allergies, measles, cellulite, acne, spots, scars, eczema, bruises, pain (tooth, back, throat, ears, kidneys, and bite aches), and hearing loss (Amaya 1984; Norman 1987; Silva & Strahl 1994; Vázquez et al. 2006; Cuesta-Ríos et al. 2007; Alves & Santana 2008; Alves et al. 2009; Silva et al. 2009). In addition to medicinal use, amulets containing animal parts, such as the teeth from caimans like C. latirostris, M. niger, and Paleosuchus palpebrosus, are used in spiritual treatments (Alves et al. 2007).

Indigenous tribes in the Brazilian Amazon have several uses for the skin secretions of the amphibians P. bicolor and P. tarsius. For example, the Ticunas used the secretions of these frogs for preparing ‘curare.’ The Wayãpi put secretions of P. bicolor in scarifications on their arms to improve their archery ability and reduce cramping. Additionally, tribes from the Paño linguistic group (Mayorunas, Marubos, Arnahuacas, and Matsés) mix the secretions of P. bicolor with saliva and rub them into burns in their arms and chest, causing discomfort and a period of deep apathy for two to three hours followed by a state of euphoria that is accompanied by a feeling of strength and greater acuteness of the senses, making them better hunters (Caramaschi & Cruz 2002). The use of secretions from P. bicolor has begun to spread to large cities in Brazil (Lima & Labate 2007). For example, in the state of Rondônia, people from various social classes and levels of education have received applications of the Kambo ‘frog vaccine’, which reportedly alleviates head and muscle aches and helps control diabetes, rheumatism, allergies, and gastritis (Bernarde & Santos 2009).

In recent years, a number of studies have been conducted to determine the effectiveness of substances used in popular medicine that are derived from reptiles in Brazil (Batista et al. 2008; Ciscotto et al. 2009; Ferreira et al. 2011; Santos et al. 2011). The body fat of the lizard T. merianae, which is widely used to treat infections, does not demonstrate significant antimicrobial activity against bacteria such as Escherichia coli and Staphylococcus aureus when used alone or in combination with antibiotics or UV-A irradiation (Ferreira et al. 2009). However, the use of this oil in the ear is effective for treating edema, and its use is supported by the pharmacological community because tests have revealed that the oil is capable of inhibiting edema by 42%. This effect is most likely associated with reduced levels of arachidonic acid and its metabolites, thereby reducing the production of pro-inflammatory mediators (Ferreira et al. 2010). In similar tests performed with oil extracted from the fat of B. Constrictor, the oil did not demonstrate direct antibacterial activity. However, combining the oil with antibiotics increased its effectiveness for the treatment of diseases caused by bacteria due to the synergistic activity of the antibiotics and the oil (Ferreira et al. 2011).

Decoctions from Ameiva ameiva, Tropidurus hispidus, and T. semitaeniatus are often used in traditional medicine to treat bacterial infections, including pharyngitis and tonsillitis. Researchers have tested these solutions (alone and in combination with antibiotics) to evaluate their antimicrobial effects against bacterial strains including E. coli, S. aureus, and Pseudomonas aureuginosa (Santos et al. 2011). These studies have found that the decoctions alone do not have a substantial effect on the growth of bacteria; however, when the solutions are combined with antibiotics they enhance the effect of the antibiotics through minimal inhibition of bacterial strains. A chemical test of the extracts revealed the presence of alkaloids, providing evidence of modulating action by the extracts. Based on these results, the extracts are a promising source of natural materials for use in the production of new antibiotic drugs (Santos et al. 2011, 2012).

3.1.2. Cultural ecosystem services

Cultural services are non-material benefits obtained through contact with the surrounding ecosystem. These services are determined by the human perception of their environment, which in turn is a product of their knowledge of the community to which they belong. Because people are strongly influenced by ecosystems, changes to the ecosystem could significantly impact the cultural identity, social stability, knowledge systems, religions, heritage values, social interactions, and recreational services (recreational use and artistic, spiritual, and intellectual fulfillment) of human societies (De Groot et al. 2005; TEEB 2010).

The cultural services provided by wildlife are determined by the cultural viewpoints of the contemporary and pre-Hispanic cultures present in a given country (Balvanera et al. 2009). Many rural and urban populations in the Neotropics use certain species of amphibians (mainly frogs) as good-luck charms because they symbolize fertility or represent the flowering process. This belief is attributed to the fact that these animals seemingly appear out of nowhere after heavy rains (Collins & Crump 2009). According to the inhabitants of Villavicencio, Colombia, rubbing ‘La piedra del amor’ (a frog carved on a rock) helps individuals to find couples or increase their fertility. Likewise, archaeologists in Valle del Cauca have found pottery with frog designs, which may have been used by indigenous communities during ceremonious rituals.

Throughout history, different cultures and religions have used animal species in rituals and sacrifices to obtain protection or ask for favors from a deity. Generally, the use of animals in rituals and sacrifices reflects the cultural and spiritual value of these species. The Afro-Brazilian religion of Candomblé includes a sacrificial ritual practice called orô in which more than 20 species of animals are used, including the toad Rhinella schneideri and the turtles P. geoffroanus and C. denticulata. The choice species depends on the preferences of the orishas (deities) to which they are offered. The toad is used to make offerings to the orisha Nana and the turtles are offered to the strong and powerful Shango (Neto et al. 2009). In addition, amphibians and reptiles have been a source of inspiration for folklore, arts, and corporate marketing campaigns. In Bogotá, Colombia, for example, a frog has been associated with the urban water services company for over a 100 years; this symbolizes water, humidity, and life.

On the other hand, the ecotourism conducted for observation of the marine turtle nesting (Turtle-watching tourism) has been famous in some Pacific beaches; as in the case of the Tortuguero Nationa Park, in Costa Rica, where a high influx of tourist during the times of nesting of marine turtle C. mydas (1300 tourist in July 1990; Jacobson & Figueroa Lopez 1994).

3.2. Indirect ecosystem services

3.2.1. Regulating ecosystem services

3.2.1.1 3.2.1.1. Disease control

Resistance to chemical insecticides by insects that act as disease vectors has created new problems in the fight against human disease. Such problems can be alleviated with integrated pest control measures that do not damage the environment. The implementation of new approaches, such as the use of biological controls, has helped to reduce environmental and economic costs (Jenkins 1964). However, integrated control strategies require detailed knowledge of the ecology of the disease vector organisms and their natural enemies.

In Argentina, Peltzer and Lajmanovich (2002) observed that the Lysapsus limellus frog feeds on flies and dragonflies associated with organic matter and standing water. The majority of the fly species that make up the diet of this frog belong to the family Ephydridae, which causes human diseases. Therefore, L. limellus can act as a biological control in the ephemeral pools in which it is found. Spielman and Sullivan (1974) and Rodriguez and Gonzalez (2000) observed that Osteopilus septentrionalis tadpoles consumed larvae of the mosquito Culex quinquefasciatus in both laboratory and field conditions. They found that the larvae of Culex pipiens quinquefasciatus were never abundant in places with tadpole populations, suggesting that the tadpoles were predators of these mosquito larvae and thus reduced the mosquito populations. When tadpoles of O. septentrionalis were introduced in regions containing C. p. quinquefasciatus larvae, mosquito populations declined. Their results suggest that tadpoles of O. septentrionalis may help to regulate the abundance of C. p. quinquefasciatus in some areas.

In Argentina and in Paraguay, caimans C. yacare and C. latirostris play an important role in controlling species populations as natural predators of aquatic mollusks such as snails, which are intermediate hosts for the trematode species Fasciola hepatica. Fasciola hepatica is a damaging endoparasite that infects the livers of cattle and sheep (Medem 1983). Similarly, in Bolivia, caimans prey on fish including palometas (piranhas) of the genus Serrasalmus, Pygocentrus, and Rooseveltiella, that attack livestock as they pass through the marshes, tearing at their udders, lips, and tongues (Medem 1983).

3.2.1.2 3.2.1.2. Control of agricultural pests

Pest management is important to protecting food supplies worldwide. Pests cause an estimated loss of nearly half of the commercial crop production each year because controls are inefficient and invasive pests often destroy entire harvests (Schwartz & Klassen 1980). The pests attack a wide variety of plants at all stages of their growth; therefore, a pest control agent must do more than occasionally consume the pest species. In order to have a positive effect on the agricultural resource, a biological control agent must negatively impact the entire pest population (Whelan et al. 2008).

In Argentina, 30 million tons of genetically modified soybeans are produced annually. Soybean crops are affected by a variety of insect pests and plant seedlings that cause various types of damages and crop losses (Hartmann et al. 1999 in Attademo, Peltzer et al. 2007). Research on the role of amphibian populations in pest control has demonstrated the importance of Rhinella arenarum, Leptodactylus latinasus, Leptodactylus chaquensis, and Physalaemus albonotatus in the biological control of certain arthropod species that damage soybean crops. In these studies, the arthropods, such as beetles, isopods, and members of the Orthoptera and Hymenoptera orders, that damage soybeans represent a significant portion of frog diets, specifically 78% (R. arenarum), 48% (L. chaquensis), 44% (L. latinasus), and 21% (P. albonotatus).

Increasing crop diversity in intensive agricultural systems could result in changes in habitat diversity that ultimately promotes the abundance and effectiveness the pests’ natural enemies (Altieri 1992 in Peltzer et al. 2005). Additionally, 11 arthropod groups harmful to soybean plants (Lepidopteros, Isopodos, and Formicidos) were found to be consumed by the anuran Physalaemus biligonigerus. These arthropods comprised 64.7% of the total prey categories for P. biligonigerus (Attademo, Peltzer et al. 2007). Of the 1963 food items consumed by 62 individuals of R. arenarum, 1439 were arthropods harmful to soybean plants, accounting for 73% of their diet. These studies suggest that frogs, natural enemies of many pests, could be used as effective biological controls to reduce pest damage to soybean crops. Maintaining these frog populations in agroecosystems could provide an effective biological control mechanism (Lajmanovich et al. 2003; Attademo et al. 2005; Peltzer et al. 2005; Attademo, Cejas et al. 2007; Attademo, Peltzer et al. 2007; Peltzer et al. 2010).

3.2.2. Dispersion and frugivory

Because the pulp of many fleshy fruits is an important food source for certain terrestrial turtles and herbivorous and omnivorous lizards, these reptiles are expected to act as seed dispersers (Valido & Olesen 2007). In recent decades, the number of studies on the role of reptiles in pollination and seed dispersal has increased (Galindo-Uribe & Hoyos-Hoyos 2007), and fruit consumption has been reported in over 200 species of reptiles. The studies have indicated that the role of these species as mutualistic double agents (dispersers and pollinators) has been underestimated and that pollination and seed dispersal by lizards is more common on islands (Olesen & Valido 2003). Some authors have suggested that in the Neotropics, the consumption and transport of reproductive items (flowers and fruits) by lizards and turtles may affect the reproduction of various plant species and the vegetation structure of the community (Traveset 1990; Guzmán & Stevenson 2008; Jerozolimski et al. 2009). These studies not only demonstrate the ecological importance of reptiles but also allow an examination of the potential economic role that these organisms could play by aiding the reproduction and spread of commercially interesting plants (Tables 1, 2).

Table 1. Species of trees and other plants in Neotropical ecosystems with seeds dispersed by amphibians and lizards and their human or agricultural uses

Group	Dispersal species	Dispersed species	Uses	Economic importance	Country	Reference
Amphibian	Xenohyla truncata	Anthurium harrisii	O		Brasil	Da Silva et al. (1989)
		Erythroxylum ovalifolium			Brasil	Fialho (1990)
Lizards	Cyclura	Coccoloba uvifera		x	Bahamas	Iverson (1985)
		Casasia clusiifolia	O
	Ctenosaura similis	Acacia farnesiana		x	Costa Rica	Traveset (1990)
		Ficus sp.
		Spondias purpurea		x
		Guazuma ulmifolia		x
		Simarouba glauca		x
		Nertera granadensis	O		Chile	Wilson et al. (1996)
	Liolaemus pictus	Relbunium hypocarpium	C
	Liolaemus bleii	Berberis empetrifolia	O, M, E		Chile	Celedón-Neghme et al. (2008)
	Phymaturus flagellifer	Calandrinia sp.			Chile	Celedón-Neghme et al. (2005)
		Berberis empetrifolia	O, M, E
		Rumex acetosella	E, M
	Tupinambis merianae	Solanum lycocarpum			Brasil	Castro and Galetti (2004)
		Eugenia uniflora		x
		Eugenia sp.
		Morus nigra		x
	Tropidurus torquatus	Melocactus violaceus	O		Brasil	Cortes-Figueira et al. (1994)
Note: O, ornamental; M, medical; C, crafts; E, edible.

Table 2. Species of trees and other plants in Neotropical ecosystems with seeds dispersed by tortoises and their human or agricultural uses

Dispersal species	Dispersed species	Uses	Economic importance	Country	Reference
Rhinoclemmys funerea	Dieffenbachia longispatha	E, W
	Ipomoea trifida	O
	Ficus glabrata	M
	Ficus sp.
	Cecropia sp.
	Solanum ochraceo- ferrugineum
	Spondias mombin			Costa Rica	Moll and Jansen (1995)
Rhinoclemmys annulata	Ficus sp.
	Philodendron sp.
	Jacaratia dolichaula	E
	Solanum siparanoides
	Faramea suerrensis
	Miconia affinis	SR
Chelonoidis carbonaria	Ficus sp.			Brasil	Strong and Fragoso (2006)
	Aechmea sp.	O
	Genipa americana		x
Chelonoidis chilensis	Ziziphus mistol		x	Argentina	Varela and Bucher (2002)
	Prosopis nigra		x
	Prosopis elata	W
	Prosopis torquata	W
	Celtis pallida		x
Chelonoidis denticulata	Spondias mombin
	Tetragastris altissima
	Jacaratia digitata	E
	Jacaratia spinosa	E
	Celtis sp.
	Brosimum lactescens	M
	Attalea maripa	E
	Pourouma guianensis	M
	Genipa americana		x
	Rollinia sp.
	Rauvolfia mirantha			Brasil, Perú	Strong and Fragoso (2006); Guzmán and Stevenson (2008); Jerozolimski et al. (2009)
	Cecropia membranacea	M
	Cecropia sciadophylla
	Loreya strigosa
	Miconia sp.
	Ficus insipida
	Ficus maxima
	Ficus sp.
	Helicostylis tomentosa	E
Chelonoidis nigra	Carica papaya	E	x	Ecuador	Sadeghayobi et al. (2011); Blake et al. (2012)
	Passiflora edulis		x
	Psidium galapageium	W	x
	Psidium guajava
	Hippomane mancinella	W	x
	Opuntia echios
Note: O, ornamental; W, wood; M, medical; C, crafts; E, edible; SR, soil retention.

3.2.3. Supporting ecosystem services

3.2.3.1 3.2.3.1. Nutrient cycling

The nutrient cycle describes the movement of elements within and between biotic and abiotic entities. Nutrients can be extracted from mineral and atmospheric sources or recycled from their organic to ionic forms. These nutrients are subsequently reabsorbed and returned to the atmosphere or soil (Lavelle et al. 2005). Organic materials (compounds of biological origin) are critical in determining the availability of nutrients for plants. The major nutrient stock in soils, sediments, and water is usually contained in organic compounds. Because absorption by plants requires the inorganic forms of nutrients almost exclusively, the processes that mediate the biological decomposition of organic matter are critical to nutrient availability (Parton et al. 1988 in Lavelle et al. 2005). The coqui frog (Eleutherodactylus coqui) increases the rate of nutrient cycling in terrestrial systems in Puerto Rico by increasing the availability of nutrients in the forest through deposition of wastes (feces, urine, and carcasses) and population movements. In addition, the coqui frog can increase the rate of post-disturbance forest succession during early succession, when both plant and frog densities are high. The absence of these frogs from the system can decrease the amount of K (potassium; by 5.7–6.6 kg/ha) and P (phosphorus; by 3.1–3.7 kg/ha) available for leaf litter decomposition, greatly impacting the rates of nutrient cycling because both nutrients are essential for the microbial activity and the growth of forest plants (Beard et al. 2002, 2003).

In Panama, Espadarana prosoblepon, Sachatamia albomaculata, Hyalinobatrachium colymbiphyllum, and Centrolene spp. tadpoles are important to nutrient cycling in aquatic ecosystems by stimulating the fungal activity in litter (Connelly et al. 2011) and may increase the concentration of nutrients in aquatic systems through their excretions. The absence of these species can alter the structure and functions of the system (Whiles et al. 2006). In a 2-year study in the Rio Maria, Panama, following the decline of populations of Lithobates warszewitschii, Hyloscirtus spp., and Colostethus spp. tadpoles, the substrate changed from a relatively clean, coarse sediment to a dense layer of organic soil composed mainly of senescent diatoms. The rate of nitrogen cycling and biological activity also decreased. The loss of tadpoles from this freshwater system caused dramatic changes to the ecosystem that were not offset by the activity of other species in the river (Whiles et al. 2013).

Food chains form a network of nutritional relations that are important to the energy flow in ecosystems (Govenar 2012); therefore, food chains provide an appropriate context for determining how organisms modify and regulate energy transfer (Polis 1994). Amphibians and reptiles are predators of a wide range of invertebrates and vertebrates. In many cases, these animals are generalists that prey on eggs, tadpoles, juveniles, adults (Wells 2007), and bodies in an advanced state of decomposition (Sazima & Strüssmann 1990; Mora 1999; DeVault & Krochmal 2002), thereby enhancing the flow of nutrients in the ecosystem through energy transfer in food chains (Lavelle et al. 2005). Frogs are often critical to the food webs of aquatic and terrestrial systems in which they can reach high densities and biomass and are important prey for many species (Schiesari et al. 2009). In addition, frogs can digest many materials (feathers, beaks, hair, or chitin), making them a high-quality nutrition source for other animals (Burton & Likens 1975; Bouchard & Bjorndal 2000; Wells 2007; Collins & Crump 2009).

4. Discussion

Although the data describing the importance of amphibians and reptiles to ecosystems and human societies in this study came from only half of the countries in the Neotropics, the research indicated that amphibians and reptiles provide many ecosystem services, some of which are vital to the functioning of the ecosystems and to the provision of other services.

These services have been affected by decline in the amphibian and reptile populations (Gibbons et al. 2000; Stuart et al. 2004; Reading et al. 2010), undoubtedly jeopardizing human well-being. Research efforts should identify, describe, and analyze the benefits that human societies gain (directly or indirectly) from amphibians and reptiles. In addition, the extent to which threats to these species could affect the provision of services should be assessed, especially in the highly diverse Neotropics. The services provided by amphibians and reptiles have rarely been considered among motivations for acting on their conservation status (Gratwicke et al. 2010). The development of conservation plans for species in these groups and their inclusion in endangered species categories could directly or indirectly help to protect the ecosystem services provided by these organisms.

Among the indirect services provided by these groups, nutrient cycling and seed dispersal form the basis for the provision of other services. The seed dispersal vital to plant propagation, in some systems, is primarily mediated by reptile species (lizards and turtles) (Olesen & Valido 2003; Jerozolimski et al. 2009; Zuël et al. 2012). These animals disperse plant seeds that are of ecological and economic importance to human society, and the plants that are important food sources for rural communities. While the role of reptiles in seed dispersal is evident, the importance of amphibians in seed dispersal processes is not yet known. Therefore, studies are needed to assess the potential ecological roles of amphibians, not only in seed dispersal but also in shaping the structure and composition of vegetation communities upon which human populations often rely for food, medicine, and raw materials.

Like seed dispersal, pollination is an important process in the reproduction of plants. Although research in Europe and Africa (mostly islands) (Pérez-Mellado et al. 2000; Hansen et al. 2007; Nelson 2010) has demonstrated the importance of some reptile species in the pollination of plants, studies exploring the role of amphibians and reptiles in pollination in the Neotropics are scarce. Except for two studies in Brazil in which the role of lizards as pollinators was examined, no studies have been published to address this topic. Further ecological and ethnological research could provide information regarding the feeding and foraging habits of different species, allowing for the identification of potential mutualistic interactions among species of amphibians, reptiles, and plants. Such information could also improve understanding of how the direct and indirect interactions among these organisms and others contribute to ecosystem services.

Redundancy is an important aspect of ecosystems in that many species can support the same ecosystem service, thereby increasing ecosystem resilience against disturbances (Luck et al. 2003). Studies in freshwater systems have not only demonstrated the importance of tadpole communities in nutrient cycling but have also indicated the potential ecological consequences of their loss. Such losses cannot be offset by ecological redundancy, even in biologically diverse regions such as the Neotropics (Whiles et al. 2006, 2013). Therefore, researchers must determine how the loss of species populations or an entire community could affect the generation or flow of support services such as nutrient cycling. Future studies similar to those of Whiles et al. (2006, 2013) should be carefully considered and replicated in other systems to determine the significance and value of amphibians and reptiles in ecosystem functioning and the provision of ecosystem services.

Although some authors indicate that the uncontrolled trade on particular species of amphibians and reptiles has had impact on their populations (Gibbons et al. 2000; Gratwicke et al. 2010; Reading et al. 2010), few of these studies have evaluated the impact of trade and traffic in the Neotropical countries where many human communities have historically used these groups their subsistence (Klemens & Thorbjarnarson 1995; Alves & Santana 2008).

Ethnobiological studies are necessary, in this sense researchers should work closely with the rural and urban communities inhabiting the Neotropical ecosystems not only to learn the traditional knowledge of these communities but also to determine the cultural value of different amphibian and reptile species because, as shown in this study, not all species are used for the same purpose. Certain species are used as food, others are used for medicinal purposes, and still others are offered as sacrifices to deities. Little is known about the cultural services provided by amphibians and reptiles to Neotropical societies. Such knowledge is important to understanding the consequences of the loss of these threatened species on the cultural and religious activities of traditional and ethnic groups. On the other hand, the potential role of these organism in the provision of ecosystem services related to food security, of some indigenous and non-indigenous communities is important, however, is essential to make progress in studies of the local population dynamics, to identify potential stocks offerings these services.

Acknowledgments

This review was made posible by the support of the Conservation Leadership Programme (CLP) and Conservación Internacional Colombia (CI). We thank Dr. Karen Beard, Dr. Paola M Peltzer, Dr. Vivian Páez, Dr. Brian Bock, Dr. Carlos Piña, Dr. Eduardo O. Pineda, Dr. Rômulo Alves, Dr. Matt Whiles, and Dr. Pablo R. Stevenson, for their assistance in providing information for this review.