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A Second Species of the Family Allophrynidae (Amphibia: Anura)
Abstract and Figures
We describe Allophryne resplendens, a new species from two localities in the Amazon rain-forest of Loreto, Peru, of the family Allophrynidae, which was monotypic until this discovery. The new species can be readily differentiated from Allophryne ruthveni on the basis of dorsal and ventral coloration both in life and in preservative, transverse processes of presacral II ori-ented anterolaterally (oriented laterally in A. ruthveni), 19 nucleotide autapomorphies for 761 base pairs (bp) of the mitochondrial gene 16S, and 16 for 923 bp of 12S. Maximum parsimony analysis of the mitochondrial gene 12S and a fragment of up to 1060 bp of 16S supports the new species as sister to A. ruthveni.
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... The genus Allophryne was proposed to accommodate the monotypic species Allophryne ruthveni Gaige, 1926 from Amazonian Guyana. Two other Allophryne species were described as recent as in the 2010s: A. resplendens Castroviejo-Fisher, Pérez-Peña, Padial &Guayasamin, 2012 andA. relicta Caramaschi, Orrico, Faivovich, Dias &Solé, 2013. ...
... The genus Allophryne was proposed to accommodate the monotypic species Allophryne ruthveni Gaige, 1926 from Amazonian Guyana. Two other Allophryne species were described as recent as in the 2010s: A. resplendens Castroviejo-Fisher, Pérez-Peña, Padial &Guayasamin, 2012 andA. relicta Caramaschi, Orrico, Faivovich, Dias &Solé, 2013. ...
... Individuals of Allophryne resplendens were identified in the field by its distinctive color pattern consisting of bright yellow blotches on a black background (Castroviejo-Fisher et al. 2012; Fig. 1). Along an 800 m trail, at least 30 calling males of A. resplendens were found in an explosive breeding event that lasted a couple of days in a flooded forest after heavy rains. ...
Snakebite envenoming is currently considered a neglected tropical disease, which affects over 5 million people worldwide, and causes almost 150 000 deaths every year, as well as severe injuries, amputations and other sequelae. Snakebite envenoming in children, although proportionally less frequent, is generally more severe, and represents an important challenge for pediatric medicine, since they often result in worse outcomes. In Brazil, given its ecological, geographic and socioeconomic characteristics, snakebites are considered an important health problem, presenting approximately 30 000 victims per year, approximately 15% of them in children. Even with low snakebite incidence, children tend to have higher snakebite severity and complications due to the small body mass and same venom volume inoculated in comparison to adults, even though, due to the lack of epidemiological information about pediatric snakebites and induced injuries, it is difficult to measure the treatment effectiveness, outcomes and quality of emergency medical services for snakebites in children. In this review, we report how Brazilian children are affected by snakebites, describing the characteristics of this affected population, clinical aspects, management, outcomes and main challenges.
... The genus Allophryne was proposed to accommodate the monotypic species Allophryne ruthveni Gaige, 1926 from Amazonian Guyana. Two other Allophryne species were described as recent as in the 2010s: A. resplendens Castroviejo-Fisher, Pérez-Peña, Padial &Guayasamin, 2012 andA. relicta Caramaschi, Orrico, Faivovich, Dias &Solé, 2013. ...
... The genus Allophryne was proposed to accommodate the monotypic species Allophryne ruthveni Gaige, 1926 from Amazonian Guyana. Two other Allophryne species were described as recent as in the 2010s: A. resplendens Castroviejo-Fisher, Pérez-Peña, Padial &Guayasamin, 2012 andA. relicta Caramaschi, Orrico, Faivovich, Dias &Solé, 2013. ...
... Individuals of Allophryne resplendens were identified in the field by its distinctive color pattern consisting of bright yellow blotches on a black background (Castroviejo-Fisher et al. 2012; Fig. 1). Along an 800 m trail, at least 30 calling males of A. resplendens were found in an explosive breeding event that lasted a couple of days in a flooded forest after heavy rains. ...
... bright and ornate coloration of this species (Castroviejo-Fisher et al., 2012). Its colour pattern is a notorious diagnostic feature that distinctive A. resplendens from the other species of its genus (Castroviejo-Fisher et al., 2012). ...
... bright and ornate coloration of this species (Castroviejo-Fisher et al., 2012). Its colour pattern is a notorious diagnostic feature that distinctive A. resplendens from the other species of its genus (Castroviejo-Fisher et al., 2012). Members of Family Allophrynidae are rare in sampling studies (Castroviejo-Fisher et al., 2012;Caramaschi et al., 2013), which prevent researchers to understand their range of occurrence and ecology. ...
... Its colour pattern is a notorious diagnostic feature that distinctive A. resplendens from the other species of its genus (Castroviejo-Fisher et al., 2012). Members of Family Allophrynidae are rare in sampling studies (Castroviejo-Fisher et al., 2012;Caramaschi et al., 2013), which prevent researchers to understand their range of occurrence and ecology. Herein we provide the second record of A. resplendens in Brazil, in the Alto Juruá Valley. ...
... Allophrynidae: This family contains a single genus, Allophryne, and until this year was monotypic (Castroviejo-Fisher et al. 2012). The species we encountered, A. ruthveni is distributed throughout the Guiana Shield (GS; LaMarca et al. 2010). ...
... Numerous individuals were observed/captured at Site 1 that displayed a divergent color pattern when compared to "typical" A. ruthveni. As the recently described species from eastern Peru, A. resplendens, is diagnosed from A. ruthveni primarily on dorsal color pattern and mitochondrial DNA sequence divergence (Castroviejo-Fisher et al. 2012), we initially hoped we had found a third species for the genus. However, preliminary genetic data (unpub. ...
A total of 149 ant species from 35 genera and 10 subfamilies have been identified from the collections made during the 2012 RAP survey of Southeastern Suriname. Additional work is ongoing to process and identify the remaining samples, which will undoubtedly raise the total number of species, possibly to over 200 species. The results indicate a healthy and diverse ant fauna reflective of pristine rainforest. Ants play important roles as predators, scavengers, and seed-dispersers in tropical forests. The ant data from Southeastern Suriname will add to a growing dataset on the ant ant fauna of the Guiana Shield, which is still poorly documented, to help identify areas of high diversity and endemism that are important to conserve within the region. Data on ants and other invertebrates are important since these groups may be able to illustrate differences between habitats within the Guiana Shield that larger animals with wide geographical ranges do not discern.
INTRODUCTION
With over 12,000 described species of ants in the world (see AntWeb), and their social lifestyle consisting of colonies ranging in size from just a few to millions of workers, ants are a dominant force in all terrestrial ecosystems, especially tropical rainforests. They are important members of the ecosystem, with high biomass and population size, and provide key ecological functions such as aerating and turning soil, dispersing plant seeds, consuming dead animals, and controlling pest insects. In addition to their ecological importance, ants have several features that make them especially useful for conservation planning, including: 1) they are dominant members of most terrestrial environments, 2) they are easily sampled in sufficiently high numbers for statistical analysis in short periods of time (Agosti et al. 2000), 3) they are sensitive to environmental change (Kaspari and Majer 2000), and 4) they are indicators of ecosystem health and of the presence of other organisms, due to their numerous symbioses with plants and animals (Alonso 2000).
Ants have been poorly surveyed in Suriname. After the 2005 RAP survey of the Lely and Nassau Mountains (Sosa Calvo 2007) and the 2010 RAP survey in the Kwamalasamutu region of SW Suriname (Alonso 2011), a conservative estimate of about 370 ant species had been recorded in Suriname. However, given the low effort of ant sampling in Suriname and the few localities sampled, there are likely many more ant species in the country.
METHODS
Ants were surveyed at RAP Site 1 (Upper Palumeu River), RAP Site 2 (Grensgebergte), and RAP Site 4 (Kasikasima). Ants were surveyed using hand search-collecting methods and the Winkler method (Agosti et al. 2000). In the search-collecting method, the ants nesting under stones, under or inside decayed wood and those foraging on ground, litter, tree trunk and plants were searched for and collected. This method was employed at all three camps around the camp and in the forest along the principal trails.
The second sifting method used was the Ants of the Leaf Litter (ALL) protocol (Agosti et al. 2000). Along each transect, a 1×1-m quadrat was set up every 10 m (for a total of 10 quadrats per transect). The leaf-litter, rotten twigs, and first layer of soil present in the quadrat were collected into a cloth sifter and shaken for about a minute. Within the sifter was a wire sieve of 1-cm² mesh size, which allowed small debris and invertebrates such as ants to fall through the mesh into the bottom of the sifting sack. The sifted leaf litter was then placed in a full-sized Winkler sack, which is a cotton bag into which four small mesh bags containing the leaf litter are placed. Due to their high level of activity, ants run out of the litter and the mesh bag and fall to the bottom of the sack into a collecting cup of 95% ethanol. The Winkler sacks were hung in the field lab for 48 hours.
A total of 10 Winkler Transects were sampled at the following sites:
• Upper Palumeu (RAP Site 1, approx. 270 m a.s.l.): Two 100 m winkler transects were sampled in the forest along the trail to Brazil, starting after the helipad. Leaf litter was dry and fairly thin. Two 100 m winkler transects were sampled in the forest up the hill behind the camp. 5 days collecting.
• Grensgebergte (RAP Site 2, approx. 800 m a.s.l.): One 100 m winkler transect was sampled in forest behind the RAP tent. Leaf litter was very wet due to heavy rain the night before and in the morning. One 100 m winkler transect was sampled in the forest at the top of the mountain above the rocky outcrops. Litter was wet and thick. These two transects were combined when hung in the Winkler sacs due to logistical difficulties when RAP Camp 1 flooded. 1 day collecting.
• Kasikasima (RAP Site 4, approx. 200 m a.s.l.): Two 100 m winkler transects were sampled along the trail by the river (towards the METS camp). Three 100 m winkler transects were sampled in forest along the trail between the RAP camp and the Kasikasima rock, most on the tops of hills on flat plateaus. 6 days collecting.
The ant specimens were preserved in 95% ethanol and sorted to morphospecies. Some specimens were identified to species level by L. Alonso and J. Sosa-Calvo using ant taxonomic literature and the ant collection at the National Museum of Natural History in Washington, D.C.
PRELIMINARY RESULTS
For this report, ants from six of the 10 winkler transects were sorted and identified to morphospecies. These included: 2 transects from RAP Site 1 (Upper Palumeu), 2 transects from RAP Site 2 (Grensgebergte), and 3 transects from RAP Site 4 (Kasikasima). Only a few of the hand collecting samples have been identified so far, with an emphasis on the ants collected from ant-plants.
A total of 149 ant morphospecies representing 35 genera and 10 subfamilies were identified from the sorted collections (see Appendix 7.1). Most of the species were from the Winkler transects since only a few of the hand collections have been sorted so far. Additional work is ongoing to process and identify the remaining samples, which will undoubtedly raise the total number of species, possibly to over 200 species. A total of 72 ant species were recorded from RAP Site 1, 25 species from RAP Site 2, and 92 species from RAP Site 4 (Appendix 7.1).
Genera typical of the region including many large ants that were commonly seen in the forest, including the arboreal species Daceton armigerum, Cephalotes spp., and Camponotus spp., the large-eyed terrestrial Gigantiops destructor, and several species of army ants. Many species of tiny leaf litter dwelling dacetines (Strumigenys, Octostrumd) were collected at all three sites, indicating good primary forest. Species of the genera Pheidole, Pachycondyla and Odontomachus were commonly observed and collected. Pheidole was the most speciose genus, which is typical for tropical rainforest.
Many ant-plants in the family Melastomataceae (Tococa sp.?) were found in the area, housing obligate ant mutualists in domatia at the base of leaves. Most of these plants contained Pheidole (possibly cf. minutula) or Crematogaster sp. 7. The ant-plant Hirtella duckei (Chrysobalanaceae) was collected at RAP Site 4 and housed Allomerus sp. (see page 26) Pseudomyrmex sp. was collected from Triplaris near the Kasikasima Camp (Site 4), and Azteca sp. was collected from Cecropia on top of the rock at RAP Site 2.
One or two species of fire ants, Solenopsis spp., were collected during the RAP survey. They may both be S. geminata, the tropical fire ant, which is native to the region. A light orange species was found under a log in the forest near RAP Camp 1 and in Palumeu village, and a darker species was common on open rocks on top of the Grensgebergte mountain (Site 2) at about 500 m. Further study is needed to determine the species.
DISCUSSION
Ants were abundant at the Southeastern Suriname RAP sites but did not seem as numerous or conspicuous as they were at the Werehpai RAP site during the Kwamalasamutu RAP survey (Alonso 2011). Much of the area surveyed was in seasonally flooded forest, which may partially explain the perceived lower abundance of ants and thin leaf litter in many areas. The forest between the RAP camp at RAP Site 1 (Upper Palumeu River) and the helipad became completely inundated on August 17. Ants and other organisms in the leaf litter are adapted to this environment and often must move when the floodwaters come. Atta sp. (leaf cutting ants) nests were observed only on higher terra firme ground.
Tropical lowland rainforests typically harbor a high diversity of ants. For example, Longino et al. (2002) found over 450 ant species in an area of approximately 1500 ha in Costa Rica, and LaPolla et al. (2007) reported 230 species from eight sites in Guyana. A RAP survey in Papua New Guinea (Lucky et al. 2011) reported 177 ant species from the low-land site (500 m). More studies of ant diversity throughout Suriname are needed to estimate the country's ant diversity, and thereby provide important baseline data for conservation and management of Suriname's biodiversity.
While in-depth analysis cannot be done until all the ant samples have been processed, these preliminary results indicate that Southeastern Suriname has high ant diversity. Data from winkler transects sampled at eight sites in Guyana (LaPolla et al. 2007) reveal comparable levels of ant species richness per transect. The winkler transects done in Guyana included 20 samples each while those from this RAP survey included 10 samples each. Thus two transects from this survey would roughly equal the sampling effort of one transect in Guyana. Table 7.1 shows the number of ant species recorded in each of the Winkler transects in this RAP survey and in Guyana at comparable elevations.
Table 7.1. Number of ant species recorded in per Winkler transects during this RAP survey of Southeastern Suriname (this RAP survey) and from Guyana (LaPolla et al. 2007).
Likewise, further analyses are needed to determine if there are differences between the ant species composition of the three RAP sites sampled in Southeastern Suriname, and also between Southeastern Suriname and other sites within the Guiana Shield. However, the preliminary morphospecies data for the six winkler transects sorted suggest that there may be some differences in species composition between the sites (see Appendix 7.1). Many of the leaf litter ant morphospecies identified so far (collected in Winkler transects) were found at only one of the RAP sampling sites. RAP Sites 1 and 3 were sampled for an equivalent amount of time (5 and 6 days respectively) so further comparisons can be made between the two sites.
Altitudinal differences in ant species richness and composition have been well documented in many tropical regions of the world with higher richness at lower elevations (Johnson and Ward 2002, Lessard et al. 2007). Thus it may be that the Grensgebergte site (RAP Site 2, 800 m) has lower ant richness than the two other sites. However, this difference is more likely due to the almost constant rainy conditions during sampling at that site and to the short duration of sampling there (1 day). The site was overcast with clouds during most of the survey. The winkler transect was collected during rain and thus the leaf litter was very wet and sticky. Furthermore, the leaf litter sample had to be taken to RAP Site 1 to be hung in the winkler sacks, but RAP Camp 1 flooded at that time and thus the sample was hung two days later, which likely affected the survival of the ants in the sample.
Ants play many critical roles in the functioning of the tropical terrestrial ecosystem, including dispersing seeds, tending mutualistic Homoptera, defending plants, preying on other invertebrates and small vertebrates, and modifying the soil by adding nutrients and aeration (Philpott et al. 2010). Another critical function provided by ants is that of scavenging (see page 27); ants are often the first animals to arrive upon a dead animal and start the decomposition process. Ants are particularly important to plants since they move soil along the soil profile through the formation of their mounds and tunnels, which directly and indirectly affects the energy flow, habitats, and resources for other organisms (Folgarait 1998). Thus ants are important to study and to include in conservation planning.
ANT SPECIES OF NOTE
Several ant species in Southeastern Suriname are common and conspicuous and have interesting life histories and behaviors. These ant species can thus serve to highlight the key roles that ants play in the ecosystem.
Gigantiops destructor —the Jumping Ant—is a large black ant common on the forest floor in the Werehpai area. These ants have extremely large eyes with which to see and avoid their predators and their prey. They move very quickly and actually jump around on the leaf litter, which is unusual for an ant. Despite its name—destructor—these ants are timid, so you have to sneak up on them carefully. They do not bite or sting but defend themselves by spraying formic acid from their gaster. These ants forage for small invertebrates in the leaf litter and are often found nesting near Paraponera clavata nests, possibly to benefit from the aggressive defense of the larger ants.
Daceton armigerum —the Canopy Ant—is a beautiful golden-colored ant that lives high in the canopy of trees. They have large heads with strong muscles that power their sharp mandibles. Their eyes are under their head so that they can see below them as they walk along branches in the tree-tops. Another key to their success in the canopy is that their claws are very clingy and can keep a tight hold on branches and tree trunks.
Cephalotes atratus —the Turtle Ant, or Gliding Ant, lives high up in the tree canopy. With its flattened body and large turtle-shaped head, it lives within rotting twigs and branches and blocks the entrance to its nest with its head. Living so high in the canopy, these ants face the threat of falling out of their tree into the terrestrial territories of other, more ferocious ants. Thus they have evolved a way to avoid falling to the forest floor. If they fall from their tree, these ants stretch out their bodies and legs to glide (Yanoviak 2005). They can detect the tree trunk by the relative brightness against the dark greenery and twist in the air to point their abdomen toward their host tree, making a safe landing back home.
Eciton burchellii —the Army Ant—has very large colonies with millions of workers that move through the forest in a swarm raid, capturing everything in their path. These ants do not have a permanent nest but have a “bivouac”—a temporary nest site consisting of a giant ball of ants, usually found under a rotting log or in the hollow of a tree. These ants sting and bite and are very aggressive, even to humans, so one needs to watch where they step around these ants. It is very interesting to watch an army ant swarm since many other creatures can be seen jumping and running to get out of the path of the ants, and some specialized antbirds follow the swarm to catch these invertebrates for their meal. The soldiers of E. burchellii have very long mandibles that are used to suture wounds by some indigenous peoples. In addition to their swarms for catching food, these ants are also often seen moving their colony to a new bivouac (which is necessary when they run out of food in an area), carrying their larvae and pupae slung under their bodies.
Odontomachus spp.—Trap-Jaw Ants—are large ants common on the forest floor (see page 27). These ants hold the world record for the fastest reflex in the animal kingdom. They forage by walking around with their mandibles (jaws) wide open. They have small trigger hairs between the mandibles that detect prey items (such as small invertebrates) and trigger the mandibles to snap shut very quickly to capture the prey. These ants often nest in the leaf litter trapped in small palm trees, in the terrestrial leaf litter, or in the soil. They are long, sleek, elegant ants, but have a nasty sting, so care must be taken to avoid touching them.
Paraponera clavata —the Bullet Ant or Congo Ant—is famous for its very powerful and painful sting. It is one of the world's largest ant species and is common in Neotropical lowland rainforests. These ants nest in the ground at the base of trees but forage up in the tree-tops on nectar and invertebrates. While they forage solitarily, they often have a relay of ants for passing large nectar droplets from the treetops to the nest, from one ant to another. These ants are one of the few ant species that make sound to communicate with one another. They can “stridulate” by rubbing their legs along their thorax to make a high-pitched squeaky sound.
Atta sp.—the Leaf-cutting Ant—is well known for its unique and fascinating agricultural lifestyle. Atta are fungus-growers—the workers cut pieces of leaves from a wide variety of trees to bring back to their nest where the leaves are chewed up by smaller workers and inserted into a large fungus garden, which the ants tend and cultivate. The ants do not feed on the leaves. Instead, they feed the fruiting bodies of the fungus to their larvae. Their nests are very large with many large underground chambers. It is fun to watch the workers cutting leaves and carrying them over their head back to the colony. Atta are parasitized by tiny phorid flies, which lay their eggs on the ants. When a fly larvae hatches, it burrows into an ant's head and develops inside, thereby killing the ant. Small Atta workers are often seen hitching a ride on the leaf carried by a larger worker- it is thought that these small ants serve to ward off attacking phorid flies.
Pseudomyrmex spp.—the Tree-dwelling Ants. Many species live in the rotting, hollow twigs and branches up in the trees. They often fall from the trees, landing on the top of tents and even on your shirt, especially after a wind blows through the forest. Some species are specialized, obligate inhabitants of ant-plants, which provide a hollow cavity and sometimes food bodies or nectar for the ants. In exchange, the ants protect the plant by capturing and eating herbivorous insects that may eat the plant. These ants have large eyes and very long, slender bodies (their body form is distinctive) and a painful sting, so it's best to take care when observing them.
CONSERVATION DISCUSSION AND RECOMMENDATIONS
The ant data from this RAP survey are part of an ongoing program of the “Ants of the Guiana Shield” led by Dr. Ted Schultz of the Smithsonian's National Museum of Natural History in Washington, D.C. and collaborators. These data will be combined with the winkler data collected by J. LaPolla and colleagues in Guyana (LaPolla et al. 2007), data from previous RAP surveys, and future surveys in the Guiana Shield to determine hotspots of ant diversity and endemism in the Guiana Shield to guide conservation priorities. The data will also be used to select indicator groups that can be used to more quickly assess the status of the ant community and the ecosystem.
Data on ants and other invertebrates are important since these groups may be able to illustrate differences between habitats within the Guiana Shield that larger animals with wide geographical ranges do not discern. This will aid in identifying important areas of the Guiana Shield for conservation. More data should be collected on ants and other invertebrates for the Guiana Shield in order to determine these patterns.
Like many tropical taxa, many ant species and populations face a range of threats. The most immediate and widespread threat comes from the loss, disturbance, or alteration of habitat. Fragmentation studies have revealed that ant species richness and genetic diversity can be affected even in large forest patches of 40 km² (Brühl et al. 2003, Bickel et al. 2006). Nomadic ant species such as army ants need large expanses of habitat to find enough food to feed their exceptionally large colonies (Gotwald 1995). Likewise, deforestation and forest fragmentation can cause local extinctions of the neotropical swarm-raiding army ant Eciton burchellii and other army ants (Boswell et al. 1998, Kumar and O'Donnell 2009).
Global climate change is likely already affecting the distribution of many ant species. For example, Colwell et al. (2008) predict that as many as 80% of the ant species of a lowland rainforest could decline or disappear from the lowlands due to upslope range shifts and lowland extinctions (biotic attrition) resulting from the increased temperature of climate change.
Solenopsis geminata is native to South American rainforests but can become a destructive pest when it spreads into disturbed areas or is introduced to other parts of the world. This species was present in disturbed areas in the villages and could become more widespread in the forest if it moves in along trails. This species often invades areas that have been disturbed so their absence is a good sign of a healthy ant fauna and ecosystem. It is recommended to survey and monitor the presence of this species on the trail to Kasikasima to avoid spread of this species by humans.
Given that ants are highly conspicuous and abundant in Southeastern Suriname they should be a key component of nature walks and eco-tourism visits in the region. Several ant species are large enough to attract the attention and admiration of tourists. These ant species have fascinating life histories and behaviors that give them “personalities” which tourists will find fascinating.
Many ant species require closed canopy forest to maintain the appropriate microclimate they need to survive. These species are found only at pristine sites. Preliminary indications of the ant fauna at all three sites indicate the presence of many forest species among the ant fauna. A full analysis of the ant species, once identified, will reveal whether any ant species are of conservation concern and also how some of the ant species can serve as indicators of the health of the ecosystem.
Southeastern Suriname is one of the last extensive pristine rainforests of the world, containing high and unique biodiversity. This region should be protected from fragmentation by development such as roads and hydropower projects. Likewise, mining and other extractive industries should also be prohibited in the region to avoid impacts on the forests, its species, and the freshwater resources of the region.
REFERENCES
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LuckyA. E.Sarnat L.E.Alonso 2011Ants of the Muller Range, Papua New Guinea. In RichardsS.J. GamuiB.G. Rapid Biological Assessments of the Nakanai Mountains and the upper Strickland Basin: surveying the biodiversity of Papua New Guinea's sublime karst environments. RAP Bulletin of Biological Assessment 60.Conservation InternationalArlington, VAGoogle Scholar
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PhilpottS.M. IPerfecto I.Armbrecht C.L.Parr 2010Ant diversity and function in disturbed and changing habitats. In L.LachC.L.ParrK.L.DDabbottAnt Ecology, Oxford University PressNew York, USAGoogle Scholar
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Sosa CalvoJ. 2007Ants of the leaf litter of two plateaus in Eastern Suriname. In AlonsoL.E. J.H.Mol A Rapid Biological Assessment of the Lely and Nassau Plateaus, Suriname (with additional information on the Brownsberg Plateau). RAP Bulletin of Biological Assessment 43. Conservation InternationalArlington, VA, USAGoogle Scholar
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Appendices
Appendix 7.1. Ants collected during the 2012 RAP survey of Southeastern Suriname. W=winker leaf litter transect, H=hand collecting
continued
continued
continued
... Allophrynidae: This family contains a single genus, Allophryne, and until this year was monotypic (Castroviejo-Fisher et al. 2012). The species we encountered, A. ruthveni is distributed throughout the Guiana Shield (GS; LaMarca et al. 2010). ...
We conducted a herpetofaunal inventory at four sites in Southeastern Suriname from March 8–28th 2012, and recorded 47 species of amphibians and 42 species of reptiles. These numbers are lower than other areas within the Guiana Shield that are better sampled (e.g. Iwokrama, Guyana; Nouragues, French Guiana), but are relatively high when compared with other sites sampled over the same time period (e.g., recent RAP surveys in Suriname). Seven (six frogs and one snake) of the total 89 species encountered could not be assigned to any nominal species. These unidentified taxa may represent novel species, yet require validating genetic and morphological data before formal diagnoses can be made. A number of records represent range expansions for taxa within the Guiana Shield (e.g. Rhinatrema bivitattum, Alopoglossus buckleyi). Additionally, a teiid lizard (Cercosaura argulus) is recorded for just the second time in Suriname. Encountering >80 total species (including 19 snake species) is evidence of a healthy, diverse and seemingly pristine forest ecosystem.
INTRODUCTION
Reptiles and amphibians form a prominent, speciose component of tropical forests and many aspects of their biology (e.g. small body size in concert with large population sizes, intermediate roles in food webs, strict micro-habitat requirements, etc.) contribute to their value as a focal group for biotic surveys. Amphibians are very good indicators of disturbance (Stuart et al. 2004) because they are sensitive to changes in microclimate, particularly as most possess a biphasic lifestyle (i.e. two distinct life stages, larval and adult) heavily dependent on high quality water resources. Amphibians are well suited for rapid assessments as they are often easy to sample; but when that is not the case, their species-specific diagnostic calls aid passive identification, particularly for hard to collect species (e.g. canopy dwellers; Marty and Gaucher 2000). Biotic surveys of amphibians in particular are imperative as widespread and poorly understood disease vectors (e.g. chytrid fungus and ranavirus) are causing worldwide declines, even in seemingly pristine areas (Lips 1998). Lizards are more diverse in primary forest, compared to secondary or modified forest (i.e. plantation; Gardner et al. 2007), suggesting they are also sensitive to changes in micro habitat. Presence of turtles and tortoises can also be a good indicator of hunting pressure as they are often targeted for subsistence hunting by local Amerindians (Peres 2001). Although one of the smallest South American countries, Suriname possesses a wide variety of amphibians (>100 species according to Señaris and MacCullough 2005; 107 species according to Ouboter and Jairam 2012) and reptiles (>170 species; Ávila Pires 2005). While very few of these species are endemic to Suriname itself, most are endemic to the larger Guiana Shield or the more inclusive Amazo-Guianan Subregion. The goal of this RAP survey in southern Suriname was to provide baseline information on the diversity and abundance of amphibians and reptiles for the areas in and around the Grensgebergte and Kasikasima Mountains. We sampled four sites incorporating both upland and lowland habitat, from seasonally flooded forest to human modified secondary forest to exposed granite outcrops. We also provide basic statistics comparing our findings with other RAP surveys in Suriname, as well as other well-studied regions in the Guianas (e.g. Iwokrama, Guyana; Nouragues, French Guiana). Finally, we discuss conservation recommendations for the region.
METHODS
Of the four main RAP study sites, herpetological collections were made in only three (Upper Palumeu River — Site 1 [9 days], Grensgebergte Mountains — Site 2 [2 days], and Kasikasima — Site 4 [6 days]; the unsampled site (Site 3) was visited only by the aquatic team while they were heading downriver between Sites 1 to 4). In addition, some species were encountered at the METS resort in Palumeu (Site 5 [1 day]), a subset of which was encountered at other sites.
In order to encounter as many species as possible, opportunistic encounters and captures were made primarily via active searching. We walked pre-established trails through forest, in forest clearings, and on stream banks. Surveys were conducted at various times of the day (although focusing on main activity periods at dusk and dawn) and early evening to mid-night. Passive frog call surveys were performed at night and if the calling male was suspected of being near the ground, efforts were made to locate it. Special attention was taken to search in a variety of habitats, particularly in streams/creeks and under logs/fallen bark — areas known to harbor rarely seen species or those with strict habitat requirements, as well as after inclement weather (i.e. heavy rains). We turned stones and logs, opened rotting logs, and raked litter to reveal hidden animals. At times, we deviated off of the main trail/transect to search adjacent habitat or features (e.g. fallen log, swampy pool) we deemed of interest or where animal activity was observed. Opportunistic surveys are effective for collecting as many species as possible in a short time period and sampling total species richness (Donnelly et al. 2004). Unfortunately, care was not taken to painstakingly record each individual of each species encountered, so only qualitative assessments of species relative abundance are provided (Appendix 9.1).
When possible and/or necessary, animals were caught either by hand, noose, net or rubber band, and preliminary identifications were made. Additionally, a portion of the total catch was euthanized (via subcutaneous injection of dilute Euthanaze®), fixed in 10% formalin solution, and then stored in 70% ethanol as museum voucher specimens (stored at the National Zoological Collection of Suriname, Anton de Kom, Universiteit van Suriname). These specimens were given unique field identification tags and many have representative life photographs (taken by S. Nielsen, P. Naskrecki and/or T. Larsen). R. Jairam later performed more rigorous, museum-based, morphological identification to verify species IDs. Samples of liver/muscle tissue for DNA analyses were extracted from voucher specimens (before formalin fixation) and stored in 95% ethanol (stored in the University of Mississippi frozen tissue collection).
We compared data on amphibian and reptile surveys from five sites in the Guiana Shield (Nouragues and Arataye, French Guiana — Born and Gaucher 2001; Petit Saut, French Guiana — Duellman 1997; Piste Ste. Elie, French Guiana — Born and Gaucher 2001; and Iwokrama, Guyana — Donnelly et al. 2005) originally assembled by Watling and Ngadino (2007), as well as three additional sites from two previous RAP surveys in Suriname (RAP 43, Watling and Ngadino 2007; RAP 63, Ouboter et al. 2011). Although undetected and/or undescribed species certainly exist throughout the Guiana Shield, the non-RAP surveys — which occurred over multiple seasons — are better sampled compared to RAP surveys (which generally span just a number of days), therefore, direct comparisons must be viewed with some uncertainty. Additionally, the geological complexity of the Guiana Shield makes comparisons of species communities/composition between high elevation inselbergs and low elevation seasonally flooded forests difficult, as different habitats support different species and different overall levels of species richness may be expected may provide counterintuitive arguments. Instead, we provide these data as a benchmark with which to compare this current study.
RESULTS AND DISCUSSION
We observed a total of 89 species of reptiles and amphibians during this survey (Table 9.1). While most of the species are confidently sorted to known species, seven (six frogs and one snake) of the total species encountered could not be assigned to any nominal species and 23 are listed as cf., meaning only informal identifications are possible without more comparative material and rigorous morphological and/or molecular examination. Appendix 9.1 lists the species we recorded and a qualitative measure of abundance for each species for the four collection localities. Upper Palumeu River (Site 1) provided the most diverse list of species (56 species, 63% of total — 30 amphibians and 26 reptiles; of which, 12 amphibians and 16 reptiles were only encountered at Site 1; see Table 9.2). This result may partially be explained by the amount of time spent collecting in that locality versus the other sites (8 days total versus the 2nd longest stay — 6 days [Site 4]), thus affording us greater opportunity to encounter a wider variety of species. However, some other subtle vegetation or habitat differences might also have played a role (e.g. presence of seasonally flooded lowland forest in Site 1). Grensgebergte Mountain (Site 2: 13 species, 15% of total species encountered; 6 amphibians and 7 reptiles, of which 1 amphibian and 3 reptiles were only encountered at Site 2) was by no means speciose, but provided two unique snake records: Dipsas copei and the only sighting of Bothrops atrox. Kasikasima (Site 4) was the second most diverse site (45 species, 51% of total —24 amphibians and 21 reptiles; of which, 6 amphibians and 10 reptiles were encountered only at Site 4). Palumeu (Site 5) was not particularly diverse (18 species, 20% of total —13 amphibians and 5 reptiles; of which 7 amphibians and 2 reptiles were encountered only at Site 5), although we suspect that the surrounding area could potentially harbor other species. As the expedition was not focused on this area, the species encountered were all observed/collected within one 24-hr. period (including one rainy night) before continuing on to Site 1.
Table 9.1. Herpetofaunal richness at 12 sites in the Guiana Shield, including data from the two previous RAP surveys to Nassau/Lely Mountains and Kwamalasamutu. In each column, data are presented as raw species number/percentage of total herpetofauna.
Table 9.2. Breakdown of reptile and amphibian species encountered at each locality and the site-specific percentage of the total species recorded, as well as how unique each site was for both taxonomic groups.
When the results for all localities are combined, our findings are comparable to those of RAP 63 of the Kwamalasamutu region of southwestern Suriname (Ouboter et al. 2011; see Table 9.1), which recorded 78 species of amphibians and reptiles (42 and 36, respectively), and is from a geographically close region. However, when each site is analyzed separately, our numbers are much more similar to those found by Watling and Ngadino (2007; RAP 43) in eastern Suriname, which also spent a similar amount of time sampling each of their two sites (-5 days). RAP 43 focused solely on areas of intermediate/high elevation, which harbored fewer (albeit more highland endemic) species. All recent RAP surveys, including the present study, generally recorded fewer species than other areas within the Guiana Shield (see Table 9.2), which can likely be explained by total days of search effort.
A number of species (24 of 89 total sp.) were recorded at the two sites that received the greater proportion of our search effort (Sites 1 & 4). Of the species that were recorded at just one site (45 spp.), most had congeneric relatives present at other sites, possibly/effectively filling similar ecological niche space (e.g. the snake Atractus torquatus was present only at Site 1 and A. flammigerus only at Site 4; however, one could argue that these two species occupy similar niches in the ecosystem). Albeit an extraneous assumption, there remains the possibility that given more search effort, other congeneric (and potentially ecologically similar) species could also be found (or that competitive niche exclusion restricts them to microhabitats that we failed to survey adequately). This pattern is also seen when comparing our results to the two other recent RAP surveys (RAPs 43 & 63); of the 89 species recorded in the present study, RAP 43 (49 spp. total) recorded 23 (26%) and RAP 63 (78 spp. total) recorded 44 (49%) of the same species (see Appendix 9.1 and Table 9.1). However, in both of these two related surveys, congeneric species (which have the potential to be ecologically similar) were collected (see species marked as “N*” in Appendix 9.1). Thus, at a higher taxonomic scale, our results are similar (see further description below). A number of species that were recorded by these previous RAPs were noticeably absent from our collection efforts (e.g. frogs such as the microhylid, Chiasmocleis shudikarensis, the ceratophryid, Ceratophrys cornuta, and the pipid, Pipa aspera), although these species are generally less likely to be sampled due to their cryptic, semi-fossorial, and/or fully aquatic lifestyles.
The ∼104 currently recognized amphibian species recognized in Suriname are representative of 38 genera in 13 families (Señaris and MacCullough 2005, Ouboter and Jairam 2012). Due to the “rapid,” abbreviated nature of RAP surveys, we were unlikely to encounter all the biodiversity a geographic area harbors (especially as some of Surinames -104 amphibian species are restricted to coastal lowlands or other areas/habitat we were unlikely to survey in southern Suriname; see Ouboter and Jairam 2012). During the course of this RAP, we recorded -47 species from 19 genera and 7 families (45%, 50%, and 54% of Suriname's currently recognized totals, respectively). Considering the aforementioned shortcomings of this type of survey, capturing roughly 50% of the known amphibian biodiversity of Suriname is a positive result. By comparison, RAP 43 (36 spp. from 13 genera and 5 families) and RAP 63 (42 spp. from 19 genera and 10 families) each recorded approximately 35% and -50–70% of the diversity, respectively.
Although we observed and/or collected a smaller percentage of the total reptile diversity of Suriname (-170 spp., 92 gen., 23 fam.), our results are roughly similar in pattern to those for amphibians outlined above. We collected 42 species from 37 genera and 17 families (25%, 40% and 74% of the Surinamese total, respectively). Similar to the above results, RAP 43 collected a smaller percentage of the total (17% of Suriname's total spp., 24% of gen., 48% of fam.), whereas RAP 63 had results similar to (albeit less than) the present study (21% of Suriname's total spp., 35% of gen., 65% of fam.). Why these results represent a larger proportion of the higher-level diversity than we recovered in amphibians is unknown, but could be representative of an underestimate of amphibian familial diversity.
Without further work, it is difficult to say whether we adequately surveyed the region in our limited time during this survey, but we did achieve comparable results to recent, previous RAP surveys. Although the number of‘new’ or rare species we collected was comparatively low (and really awaits thorough taxonomic revision of a number of groups) the real value of this region was the great diversity of herpetofauna seen and/or collected in a short time. We propose that these results suggest that southern Suriname is a local hotspot for herpetofaunal richness and if conserved in this pristine/ semi-pristine state, this region will remain a true preserve of biodiversity.
Below are brief accounts of some of the species/taxonomic groups we encountered that are of interest due to their conservation status, distribution, natural history or potential as a new species, etc.
Class Amphibia, Order Anura
Allophrynidae: This family contains a single genus, Allophryne, and until this year was monotypic (Castroviejo-Fisher et al. 2012). The species we encountered, A. ruthveni is distributed throughout the Guiana Shield (GS; LaMarca et al. 2010). Numerous individuals were ob served/captured at Site 1 that displayed a divergent color pattern when compared to “typical” A. ruthveni. As the recently described species from eastern Peru, A. resplendens, is diagnosed from A. ruthveni primarily on dorsal color pattern and mitochondrial DNA sequence divergence (Castroviejo-Fisher et al. 2012), we initially hoped we had found a third species for the genus. However, preliminary genetic data (unpub. 12S data) does not provide resounding evidence for elevating the Suriname population to a separate species. Further work is underway.
Dendrobatidae: We encountered two subfamilies within this super group of dart-poison frogs, Dendrobatinae and Aromobatinae. The latter contains >100 species in five genera, whereas Dendrobatinae contains 12 genera and >170 species. These frogs are terrestrial, largely diurnal, and display a unique reproductive mode exhibiting parental care.
Within Aromobatinae, we encountered four ‘species’ representative of two genera, Allobates and Anomaloglossus. Allobates femoralis is widely distributed across the Amazo-Guianan subregion (AGR; La Marca et al. 2010), whereas Allobates granti is distributed within a more limited area of the eastern GS (Kok 2008; Ouboter & Jairam 2012). Although neither species possessed particularly aberrant morphologies, Fouquet et al. (2012) has shown that there is considerable, geographically concordant genetic substructure across each species' respective range, potentially harboring complexes of cryptic species. As the taxonomie work is ongoing, it is difficult to accurately assess whether the populations sampled during this RAP survey are distinct from the larger Surinamese (or GS) groups delimited by Fouquet et al. (2012). Anomaloglossus baeobatrachus (IUCN Data Deficient) and Anomaloglossus sp. (see page 23) were abundant where they were found (Sites 1 and 4). Individuals of the latter found at the Kasikasima site possessed atypical (in comparison to A. baeobatrachus) dorsal color patterns (i.e. blotchy, not uniform). Similar to Allobates, Fouquet et al. (2012) has shown considerable, geographically concordant genetic divergence across these species' respective ranges, although it is currently unclear whether the Anomaloglossus “sp.” referenced in that paper is the same taxon we encountered on this RAP. Unfortunately, at present we have been unsuccessful at obtaining informative DNA sequence information to compare to that of Fouquet et al. (2012), although work is ongoing.
Within Dendrobatinae, we encountered two species representative of two genera. Of the two species of Amereega that occur in Suriname, we found just A. trivitatta (see page 29), which is widespread across the AGR, although absent from the eastern GS. Such a wide distribution could harbor cryptic species, as has been found in closely related species within the genus (see Brown and Twomey 2009). However, of the individuals we collected, there was no significant morphological divergence to suggest that scenario. We encountered this species in three of our four collection localities (all lowland), including the relatively altered forest surrounding Palumeu (Site 5), where they were quite common. We also encountered Dendrobates tinctorius (see page 29), which is found only within the GS, but is unique in possessing highly variable, geographically isolated color patterns. Although there is some taxonomie contention whether the different morphs should be treated as unique taxa, genetic data suggests the different color morphs (i.e. populations) are representative of within species variation only (Noonan and Gaucher 2006). This taxon was only observed at Sites 1 and 2 (including egg masses and tadpoles at Site 1), although two strikingly different color morphs were found at each locality. At the Grensgebergte Mtns. Site (2), L. Alonso and P. Naskrecki encountered a differently colored morphotype of D. tinctorius compared to the lowland coloration found near Site 1, although based solely on a partially out of focus photo voucher we believe it to represent the “common” color morph.
Bufonidae: This hyper-diverse, globally distributed family contains >35 genera with >500 described species, with a number of genera and species endemic to South America. Although only seven species were encountered on this RAP, they were by far the most abundant amphibians at each of the lowland sites (Sites 1, 4 and 5). The genus Amazophrynella was recently separated from Dendrophryniscus (Fouquet et al. 2012a), and of the two described and one undescribed species, one — A. minuta (see page 29) — has a broad AGR distribution that includes Suriname. Although the common name — tree toads — suggests an arboreal existence, we encountered numerous individuals at Sites 1 and 4 during the day hopping around in the leaf litter. Although we are fairly certain of their taxonomic placement based on morphology, evidence suggests this taxon is actually a species group (Coloma et al. 2010; Fouquet et al. 2012a). Further taxonomic work is required, albeit beyond the scope of this report.
Rhaebo guttatus also has a widespread pan Amazo-Guianan distribution (Azevedo-Ramos et al. 2010). This prodigious species is terrestrial and nocturnal, and was common where it occurred (Sites 1 and 4). As it requires undisturbed primary forest, this species was absent from disturbed, human-modified areas (Site 5), where it was instead replaced by the more ecologically tolerant cane toad, Rhinella marina (e.g. observed around human habitation and in a maintained airstrip). Members of the genus Rhinella are generally nocturnal, explosive breeders, and representative species were found at all four sampled sites during this RAP survey. Rhinella marina has a large native distribution spanning from central South to southern North America, but is considered an invasive species in numerous other countries, notably Australia and the US (Solís et al. 2009). We also encountered at least three other species in this genus, R. lescurei, R. margaritifera and R. martyi. Rhinella lescurei and R. martyi are described species of the R. margaritifer species group (Fouquet et al. 2007), which is broadly distributed in primary rainforest across northern South America (Solís et al. 2009). We encountered a fourth form, R. sp., that we believe could be an additional member of the R. margaritifera group. Unfortunately, many of the specimens we collected were juveniles, and the named species are quite similar morphologically, so accurate identification has proven difficult. Further work is required.
Centrolenidae: Members of this family are commonly called glass frogs, as their transparent venter makes visible their internal organs. They are nocturnal, colored in shades of neon green and are often found in overhanging vegetation along streams and rivers, although their coloration and behavior make them particularly difficult to locate. Suriname has at least five species of centrolenids (Ouboter and Jairam 2012). We collected just two specimens on this RAP survey, both tentatively identified as Hyalinobatrachium cf. taylori, which is widespread across the GS. Only one specimen was collected from each of the sites where they were present (Sites 1 and 4), although numerous males were heard calling at both places.
Hylidae: This mega-diverse family is composed of “true tree frogs and their allies” comprising 900+ species in 45+ genera that are distributed mainly in the New World (particularly South and Central America) as well as Australia. They are nocturnal, generally arboreal and display a variety of reproductive modes. There are -40 species known from Suriname (Ouboter and Jairam 2012), however, just 15 were encountered on this RAP, representative of six genera. We collected six species of Hypsiboas treefrogs, including a putatively undescribed taxon, H. sp. “chocolate” (see page 23) and four species of Scinax, including a putatively undescribed taxon (see page 23) that we believe could represent a Surinamese population of a novel species proposed by Fouquet et al. (2007). The genus Scinax is in great need of revision and specimens we collected could represent novel species, but further evidence is required to better understand genetic patterns and species boundaries. These species were not particularly common, but representative hylids were present at each site — although not all species were present at each site. A single specimen of the species Trachycephalus coriaceus and two Dendropsophus cf. brevifrons specimens were recorded (one via cell phone camera photo). The former species has an interesting disjunct distribution with populations present in the eastern GS and southwestern Amazonia, but absent from northeastern Amazonia. Frogs from the genus Osteocephalus representing two species (O. taurinus and O. leprieuri) were some of the most commonly encountered vertebrates at Site 1, yet only a single individual of the latter was found at any of the other sites (Site 4). Lastly, we also recorded the charismatic tiger leg monkey frog species, Phyllomedusa tomopterna (see page 29) from Site 1. This species requires pristine forest habitat and is distributed widely across the AGR (La Marca et al. 2004).
Leptodactylidae: Colloquially known as southern frogs, this group is composed of 190 species in 13 genera, all of which are restricted to the New World. This group of frogs is diverse in body size (e.g. 26mm SVL in Adenomera heyeri vs. 185mm in Leptodactylus pentadactylus) and in ecology (e.g. Lithodytes lineatus is often associated with ant nests, whereas Leptodactylus leptodactyloides prefers open areas like savannahs and forest edges). We found up to 12 different species (two currently identified to “sp.”) from three genera, -60% of Suriname's total leptodactylid diversity. Members of this family were observed at all four sites, with the greatest diversity of species from Sites 1 and 5 (i.e. Upper Palumeu and Palumeu). Most of the species we encountered are assignable to the genus Leptodactylus, although we also collected two forms we cannot yet accurately identify: Adenomera sp. and Leptodactylus sp.. With the exception of L. longirostris and L. myersi (which have a more restricted distribution in the GS), the species we encountered are all widely distributed across the AGR — and a few even extend into southern Central America. At site 2, L. myersi was the most abundant terrestrial vertebrate observed and it was quite easy to find juvenile frogs living in the moist spaces under nearly every granite exfoliation in the seeps on the exposed inselberg face.
Craugastoridae: This family contains the most speciose genus of vertebrates, Pristimantis, with over 400 species (-5 in Suriname) of direct-developing frogs (i.e. lacks a living larval stage). Their deviation from the reproductive strategy norm, liberating them from semi-/permanent water sources, may be one reason for their widespread distribution and successful speciation in a variety of habitats. One described species was encountered (Pristimantis chiastonotus), which is distributed throughout the eastern GS. This species is found in leaf litter, generally at low altitudes (<700m asl), and it has been suggested that they are able to cope with some degree of habitat disturbance (Gaucher and Rodrigues 2004). We also collected individuals not immediately identifiable to a named species (which we are calling Pristimantis sp.) (see page 23). We found Pristimantis species at all four collection localities, including disturbed habitat (i.e. Palumeu) and in the Grensgebergte Mtns. (roughly 750m asl).
Class Amphibia, Order Gymnophiona
Rhinatrematidae: This family of caecilians (a fossorial group of primitive, limbless amphibians) is composed of two species-poor genera endemic to South America. Only one species was encountered on the RAP, Rhinatrema bivitattum (see page 28), which appears to be distributed across the northern Guiana Shield, from Guyana to Brazil (Gaucher et al. 2004). It was previously only known from the Brownsberg region of Suriname (Nussbaum and Hoogmoed 1979) and thus our record represents a significant southern range extension. Our local guides collected a single specimen while clearing the area of vegetation for the tent camp at Site 1.
Class Reptilia, Order Squamata
Gekkota: This diverse lizard group has a near worldwide distribution as geckos are found on every continent but Antarctica. Representatives of three families (Sphaerodactylidae, Phyllodactylidae and Gekkonidae) were encountered during this RAP survey. All three families have representative species from the New and Old Worlds, as well as northern and southern hemispheres, although the history of occupation in the New World for sphaerodactylids and phyllodactylids is much older than for gekkonids. Gamble et al. (2011) found evidence to suggest that modern New World sphaerodactylids reached northern South America in the Cretaceous before the break-up of Gondwana (i.e. Gondwanan vicariance), and phyllodactylids arrived shortly thereafter (either via vicariance or dispersal), whereas geckos in the family Gekkonidae reached the New World much later (i.e. within the last 5–10 mil. yrs.) via long-distance, over-water dispersal. We only encountered one species of gekkonid on this RAP, Hemidactylus mabouia, which is native to Africa, although it can now be found throughout South and Central America and the Caribbean (via either natural or anthropogenic forces of dispersal). This species was common on the main building of the METS resort in Palumeu. The sphaerodactylid gecko species, Gonatodes humeralis, was also fairly common in primary forest and forest edges (Sites 1, 4 and 5) and is distributed widely across northern South America. Although neither was common, the two other sphaerodactylids encountered, G. annularis (see page 28) and the rather diminutive Pseudogonatodes guianensis, are restricted to moist microhabitats generally in lowland forest (although the former can be found at -800m on the Tafelberg; Ouboter pers. comm.). We consider encountering both of these species as a good indicator of forest health. Lastly, we encountered the phyllodactylid gecko Thecadactylus rapicauda, a prodigious species that reaches 125mm in snout-vent length. What was once considered one widely distributed taxon found throughout northern South America, Central America and the Lesser Antilles, this species has recently been split into three (T. solimoensis is restricted to the western Amazon and T. oskrobapreinorum from Sint Maarten). This species is sometimes commensal with man-made structures.
Lacertiformes: This morphologically and ecologically diverse group (sensu Townsend et al. 2004) is distributed throughout the Americas and includes three lizard families: Teiidae, Gymnothalmidae and Amphisbaenidae. Teiid and gymnothalmid lizards were the most commonly encountered reptiles at each site during this RAP. Species of lizards in these families are active hunters and were commonly encountered moving through the leaf litter (e.g. Alopoglossus, Arthrosaura, Leposoma), in streams/pools (e.g. Neusticurus) (see page 28), under logs (e.g. Gymnopthalmus), or moving in the open near tree falls and around camp (e.g. Ameiva, Kentropyx). The existence of Cercosaura argulus in Suriname was previously based on one record from Palumeu (Hoogmoed 1973) and the distribution map provided by the IUCN website does not confirm its presence in the country (Doan and Avila-Pires 2010). We here provide confirmation of its residence in southern Suriname. Additionally, our tentative taxonomic designation for Alopoglossus buckleyi would suggest a significant range extension for this taxon. There are morphological differences separating this taxon from the widespread A. angulatus (corroborative genetic data is also being gathered), however, this designation is still tentative and will require more comparative material for us to be confident. A single worm lizard putatively identified as Amphisbaena cf. vanzolinii (see page 28) was encountered during the second night at Site 4 moving through our recently constructed camp. This taxon — like most amphisbaenian species — is infrequently collected due to its fossorial habits but it appears to be patchily distributed across the western AGR.
Scincomorphs: Skinks are the second most diverse squamate group (behind Gekkota) and are also distributed nearly worldwide, although there are only -18 species in South America. We encountered a single species, Mabuya nigropunctata, at all forest sites — including high elevation — and were commonly observed basking or foraging around open canopy tree falls. Mabuya nigropunctata is widespread across Amazonia and can even be found in St. Vincent in the southern Caribbean. Miralies and Carranza (2010) recently published molecular evidence suggesting this taxon might be a complex of three largely allopatric lineages, although they did not suggest new names for the distinct lineages they recovered. We observed numerous individuals at Sites 1, 2 and 4, yet this wily taxon successfully evaded capture so we have no voucher or genetic material with which to compare to Miralles and Carranza (2010).
Serpentes: According to Ávila Pires (2005), Suriname possesses more than 100 snake species from 8 families. Although most of our records were of single individuals, we encountered 19 species from 6 different families. While this may seem like a paltry sum compared to the total, snakes in general are difficult to collect due to their cryptic biology, and some are restricted to specific habitat types/food sources (e.g. mangroves) that were not targeted or near the sampling sites of this study. By comparison, the two previous RAP surveys to Suriname, Lely/Nassau (RAP 43) and Kwamalasamutu (RAP 63) recorded just 6 and 17 snake species, respectively. The family Colubridae comprised the majority of the species we encountered (13 sp.), including the most commonly encountered species (i.e. the Blunthead Tree Snake (Imantodes cenchoa) and two species of ground snake (Atractus spp.), although still only a small fraction of Suriname's total colubrid diversity (>75 sp.). Colubridae is the largest snake family and includes about two-thirds of all described snake species (>300 genera, >1,900 species). Site 2 (Grensgebergte) provided the only records of Cope's Snail-eater, Dipsas copei, and the fer-de-lance, Bothrops atrox. There is some confusion regarding the type locality of the former (i.e. Suriname; see Kornacker 1999), although undoubtedly it is quite rare and is represented by only a handful of specimens collected in Suriname. The fer-de-lance on the other hand is often one of the more common snakes encountered in lowland tropical forests; yet we saw only one, and at >700 m. We posit that this is a result of undersampling rather than absence of the species from the lowland sites and if we had utilized pitfall trap arrays with funnel traps on this survey, we are confident we would have encountered more “common” terrestrial species, such as Bothrops spp.
Testudines: Although only a few individuals of two species were observed, we argue that presence of turtles and tortoises are positive signs of limited hunting pressure. Due to their ease of capture and convenient storage, humans have been subsistence hunting tortoises for millennia (Thorbjarnarson et al. 2000) and many cultures in South America continue this practice. A single individual of the flat-headed turtle, Platemys platycephala, was observed by R. Jairam at Site 1 foraging in partially flooded lowland forest. At least two different individuals of the yellow-footed tortoise, Chelonoidis denticulata, were encountered at the high elevation site 2, sitting in vegetation near slowly flowing seeps, while a third individual was also observed foraging in the lowlands between camp and Kasikasima mountain (Site 4). While by no means an extensive survey, the presence of these species is likely correlated to the seemingly pristine quality of the forests.
CONSERVATION RECOMMENDATIONS
Of the species we encountered, only a fraction has been assessed for the IUCN Red List of Threatened Species, and most are listed as Least Concern or Not Evaluated since they are widely distributed across either the greater Guiana Shield or some portion of Amazonia. Due to myriad factors (e.g. weather, collection technique, collector fatigue), it is likely that we failed to collect all representatives of the herpetofaunal community at each site. With repeated surveys, we expect that our species lists would increase. Given the amount of time available at each site, we found a community that appeared speciose and could be harboring a few putatively “new” species (e.g. Hypsiboas sp. “chocolate”). This survey also provided collection records that have contributed to geographic range extensions for species not previously known from Suriname (e.g. Cercosaura argulus and Alopoglossus buckleyi), as well as new records for particularly rarely encountered species (e.g. Dipsas copei, Rhinatrema bivittatum, Amphisbaena cf. vanzolinii). Observing little in the way of disturbance or man-made alterations, we suggest that these sites (with the possible exception of the altered forest near Palumeu) are healthy and productive, and are presumably acting as a corridor for gene flow through this region of the Guiana Shield. The presence of species that are rarely seen or were previously unrecorded in Suriname helps to substantiate that there is (or was) an historical connection between this and surrounding areas. Helicopter flights over the area confirm that the forest is widespread and contiguous, which is hopefully contributing to species/genetic admixture between protected areas. Future conservation/ landscape genetic work might confirm a connection between the forests surrounding our main study sites and adjacent protected areas, but we nonetheless advocate that maintaining the pristineness of this corridor should be a priority for healthy ecosystem function and to maintain natural gene flow throughout the Guiana Shield.
ACKNOWLEDGEMENTS
We would specifically like to thank Antoine Fouquet and Philippe Kok for assistance in identifying some of the more taxonomically confusing species. We also wish to thank the other members of the RAP team — both scientists and guides/members of the support team — that contributed to this study via opportunistic collections and/or photographic vouchers.
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Appendices
Appendix 9.1. Amphibians and reptiles recorded during the current RAP study. A qualitative assessment of species abundance for each site where the occurred is included (VC: very common, >10 individuals observed; C: common, l>x >10 individuals observed; UC: uncommon, only 1 observed/captured), as well as general geographic distribution (W: widespread; GS: Guiana Shield; AGR: Amazo-Guianan Subregion; E: exotic), IUCN threat status (LC: least concern; NE: not evaluated; DD: data deficient) and type of microhabitat in which the species was recorded. The last two columns indicate whether the same (Y or N) species were recorded by the two most recent RAP surveys in Suriname. In some cases, congeners (N* i.e. a close taxonomic relative) were recorded instead of the species we documented in the present study.
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... Amphibians generally have a low vagility and high philopatry, which are characteristics that promote differentiation and ultimately speciation (Wells 2012. In this sense, although most anuran species would be expected to have small geographic distributions with distantly separated populations having greater genetic differences, there are some cases of widely distributed species with low genetic distances, such as Dendropsophus nanus (Boulenger, 1889) (Fouquet et al. 2007), Allophryne ruthveni Gaige, 1926(Castroviejo-Fisher et al. 2012, and Adelphobates galactonotus (Steindachner, 1864) (Rojas et al. 2020). There are also cases of low genetic distances between distinct species, such as Pseudopaludicola jaredi Andrade, Magalhães, Nunes-de-Almeida, Veiga-Menoncello, Santana, Garda, Loebmann, Recco-Pimentel, underestimated. ...
Frogs of the family Centrolenidae are adapted to live at high altitudes, and so it is not surprising that their greatest diversity is in the Andes mountain range. Here we extend the known geographic distribution of Vitreorana ritae by more than 550 km towards southern Amazonia. The species was identified by morphological, acoustic and molecular characteristics (mitochondrial marker 16S rRNA). The records reported here are the first for the genus Vitreorana in the state of Mato Grosso, Brazil, as well as for the transition zone between the
Amazonia and Cerrado biomes. These records are consistent with the hypothesis that the low number of species of centrolenids reported in the lowlands of the Amazon region may be the result of limited sampling. Even though V. ritae is distributed throughout the Amazon, most of its diagnostic morphological characteristics are conserved. Thus, the great rivers of the Amazon Basin do not seem to act as geographical barriers for this species; however, due to the limited sample size, further acoustic and molecular studies are needed to confirm this hypothesis.
The eyes of frogs and toads (Anura) are among their most fascinating features. Although several pupil shapes have been described, the diversity, evolution, and functional role of the pupil in anurans have received little attention. Studying photographs of more than 3200 species, we surveyed pupil diversity, described their morphological variation, tested correlation with adult habits and diel activity, and discussed major evolutionary patterns considering iris anatomy and visual ecology. Our results indicated that the pupil in anurans is a highly plastic structure, with seven main pupil shapes that evolved at least 116 times during the history of the group. We found no significant correlation between pupil shape, adult habits, and diel activity, with the exception of the circular pupil and aquatic habits. The vertical pupil arose at least in the most recent common ancestor of batrachians, and this morphology is present in most early-diverging anuran clades. Subsequently, a horizontal pupil, a very uncommon shape in vertebrates, evolved in most neobatrachian frogs. This shape evolved into most other known pupil shapes, but it persisted in a large number of species with diverse life histories, habits and diel activity patterns, demonstrating a remarkable functional and ecological versatility.
Aim
The diversity of brood size across animal species exceeds the diversity of most other life‐history traits. In some environments, reproductive success increases with brood size, whereas in others it increases with smaller broods. The dominant hypothesis explaining such diversity predicts that selection on brood size varies along climatic gradients, creating latitudinal fecundity patterns. Another hypothesis predicts that diversity in fecundity arises among species adapted to different microhabitats within assemblages. A more recent hypothesis concerned with the consequences of these evolutionary processes in the era of anthropogenic environmental change predicts that low‐fecundity species might fail to recover from demographic collapses caused by rapid environmental alterations, making them more susceptible to extinctions. These hypotheses have been addressed predominantly in endotherms and only rarely in other taxa. Here, we address all three hypotheses in amphibians globally.
Location
Global.
Time period
Present.
Major taxa studied
Class Amphibia.
Methods
Using a dataset spanning 2,045 species from all three amphibian orders, we adopt multiple phylogenetic approaches to investigate the association between brood size and climatic, ecological and phenotypic predictors, and according to species conservation status.
Results
Brood size increases with latitude. This tendency is much stronger in frogs, where temperature seasonality is the dominant driver, whereas salamander fecundity increases towards regions with more constant rainfall. These relationships vary across continents but confirm seasonality as the key driver of fecundity. Ecologically, nesting sites predict brood size in frogs, but not in salamanders. Finally, we show that extinction risk increases consistently with decreasing fecundity across amphibians, whereas body size is a “by‐product” correlate of extinction, given its relationship with fecundity.
Main conclusions
Climatic seasonality and microhabitats are primary drivers of fecundity evolution. Our finding that low fecundity increases extinction risk reinforces the need to refocus extinction hypotheses based on a suggested role for body size.
Standardization and repeatability is at the heart of all scientific research, yet very little literature exists to standardize morphometric measurements within vertebrate groups. This is particularly true for amphibians. Our study attempts to rectify this lack of methodological standardization for the measurement of morphological characters in anurans through an extensive literature survey of 136 species descriptions representing 45 currently recognized families of frogs. The survey revealed 42 morphological measurements represented in five percent or more of the literature reviewed. All measurements are listed by most commonly used name, acronym, and most precise definition, and we provide statistics summarizing the variation in measurement use and description from the surveyed literature. Of these 42 measurements, a subset of 16 were found in the top 75% of all surveyed descriptions and identified as a focal set of recommended measurements in an effort to standardize the morphometric measurements that describe anuran species diversity. Illustrations of these 16 measurements are provided as a visual reference for standardizing their measurement.
The fourth edition of the textbook Herpetology covers the basic biology of amphibians and reptiles, with updates in nearly every conceptual area. Not only does it serve as a solid foundation for modern herpetology courses, but it is also relevant to courses in ecology, behavior, evolution, systematics, and morphology. Examples taken from amphibians and reptiles throughout the world make this book a useful herpetology textbook in several countries. Naturalists, amateur herpetologists, herpetoculturists, zoo professionals, and many others will find this book readable and full of relevant natural history and distributional information. Amphibians and reptiles have assumed a central role in research because of the diversity of ecological, physiological, morphological, behavioral, and evolutionary patterns they exhibit. This fully revised edition brings the latest research to the reader, ranging over topics in evolution, reproduction, behavior and more, allowing students and professionals to keep current with a quickly moving field.
A new species of rhinatrematid caecilian, Rhinatrema ron sp. nov., is described based on a single specimen from the state of Amazonas in Brazil. The new species differs from other Rhinatrema in several features, including its larger size, different colouration, and distinctively plicate oral mucosa.
A multiple sequence alignment program, MAFFT, has been developed. The CPU time is drastically reduced as compared with existing
methods. MAFFT includes two novel techniques. (i) Homo logous regions are rapidly identified by the fast Fourier transform
(FFT), in which an amino acid sequence is converted to a sequence composed of volume and polarity values of each amino acid
residue. (ii) We propose a simplified scoring system that performs well for reducing CPU time and increasing the accuracy
of alignments even for sequences having large insertions or extensions as well as distantly related sequences of similar length.
Two different heuristics, the progressive method (FFT‐NS‐2) and the iterative refinement method (FFT‐NS‐i), are implemented
in MAFFT. The performances of FFT‐NS‐2 and FFT‐NS‐i were compared with other methods by computer simulations and benchmark
tests; the CPU time of FFT‐NS‐2 is drastically reduced as compared with CLUSTALW with comparable accuracy. FFT‐NS‐i is over
100 times faster than T‐COFFEE, when the number of input sequences exceeds 60, without sacrificing the accuracy.
— We studied sequence variation in 16S rDNA in 204 individuals from 37 populations of the land snail Candidula unifasciata (Poiret 1801) across the core species range in France, Switzerland, and Germany. Phylogeographic, nested clade, and coalescence analyses were used to elucidate the species evolutionary history. The study revealed the presence of two major evolutionary lineages that evolved in separate refuges in southeast France as result of previous fragmentation during the Pleistocene. Applying a recent extension of the nested clade analysis (Templeton 2001), we inferred that range expansions along river valleys in independent corridors to the north led eventually to a secondary contact zone of the major clades around the Geneva Basin. There is evidence supporting the idea that the formation of the secondary contact zone and the colonization of Germany might be postglacial events. The phylogeographic history inferred for C. unifasciata differs from general biogeographic patterns of postglacial colonization previously identified for other taxa, and it might represent a common model for species with restricted dispersal.