1. Introduction
1.1 Long term monitoring
Modern amphibian declines and extinctions are incomparable to that of any other class over the
last few millennia (Stuart et al 2004). The global loss of amphibians demonstrates how the world
is changing, and how conservation practices must also adapt. Detailed information on amphibian
populations in decline is often not available (Gascon et al 2005). Therefore it is crucial that long
term monitoring of populations and areas with high species richness, such as the Amazon
rainforest, are monitored for the effects of decline. Long term monitoring of populations is an
effective technique in understanding the extent and cause of the widespread decline of amphibian
populations (Caughley and Gunn1996).
The Lago Preto Concession Area is situated on the Peruvian side of the Yavari River in the
region of Iquitos. It has a tremendous diversity of frogs and there is opportunity for ongoing
research. Therefore, it is an ideal location to monitor the effects of amphibian decline due to
climate change, chytridiomycosis and other impacts. This study examines anuran abundance and
diversity at the Lago Preto Concession Area and investigates ecological trends across different
habitat types. Data collected are compared with that of previous studies to get a more accurate
picture of species abundance and this baseline data can be used to help a long-term monitoring
project in the area.
1
1.2 Conservation status of Amphibians
Amphibians, which comprise frogs, salamanders and caecilians, all descend from an ancient
ancestry of organisms and form integral roles within the world’s ecosystems. Amphibians are
both predators and prey; they help control populations of insects that transmit diseases and feed
on crops, and the tadpoles of many frogs play a major role in aquatic ecosystems (Mendelson,
2006).
The most successful, widespread and numerous of amphibians are the anurans, but they are more
commonly known as frogs and toads. There are more than 5,500 species of anurans that live in
various habitats from mountain slopes to deserts and can be found on every continent excluding
the polar regions (Attenborough, 2008). The vast majority of species occurs in the Amazon
rainforest and the Montane forests of South America. At a single site in the upper Basin of the
Ecuadorian and Peruvian Amazon 81 species of frog have been found, which equals the total
number of species in the whole of North America (Duelman 1992). The Amazon Basin is the
most diverse and species rich place on the planet for frog fauna.
Over the past few decades scientists have observed a significant number of population declines
and extinctions, which suggests a general Global Amphibian Decline (GAD) is taking place
(Young 2001, Mendelson 2006 ). At present almost one-third of the worlds 5,743 described
amphibian species are threatened with extinction, at least 122 species are believed to have
already gone extinct since 1980, and 130 species have not been found in recent years and are
presumed extinct. The scope of these declines and extinctions is far greater than mammals and
2
birds over the last few millennia. Declines have spread geographically and the numbers of
species involved is still increasing. (Mendelson, 2006).
2. Reasons for decline.
2.1 Habitat loss, alteration and fragmentation.
At present the greatest danger to amphibians is habitat loss, which is impacting 90% of
threatened species (Beebee, 1996, Mendelson, 2006). Frogs need a variety of habitat types
throughout different stages in there life process. Many amphibians are habitat specific. Pearman
(1997) observed that species richness and diversity can vary in response to precipitation levels,
elevation, forest type and structure. As a consequence, if one part of the ecosystem is altered it
can seriously upset the behaviour and survival of a population, due to specific habitat
requirements needed for reproduction and population growth.
Amphibian diversity can be significantly altered in response to habitat alteration, as many
species are restricted to different habitat types due to complex life cycle, terrestrial and semi
aquatic breeding regimes, the predation of eggs and the necessity of keeping the skin moist.
Furthermore, many amphibians have specialised feeding behaviour; therefore they are
susceptible to changes in the abundance or composition of food sources, potentially leading to
geographical isolation or local extinction (Pearman, 1997).
During the 1990s, South America lost 4% of its total forest cover, due to the increasing
population and the demand for land for agriculture and housing. However, this figure does not
include the destruction of mature forests that are being replaced by secondary growth as loggers
3
selectively remove trees. (Young et al., 2004). Habitat fragmentation caused from habitat
destruction and alteration results in population isolation on small pockets of suitable habitat
surrounded by larger areas of unsuitable habitat. These small pockets are also known as
‘islands,’ and are often too small to sustain effective breeding populations (Kricher, 1997). Over
time, populations begin to lose genetic diversity, lacking the capability of responding to
environmental changes, such as climate change, and increasing the likelihood of extinction
(Frankham, 2005).
Unfortunately, habitat destruction is continuing at a fast pace. Estimates predict that South
America will reach 768 million inhabitants by 2050, resulting in a higher demand for resources
and intensifying the threat to amphibians in Latin America (Young et al, 2004).
2.2 Climate change
Habitat destruction, alteration and fragmentation are thought to be the main reasons for the
current high rates of extinction within amphibians (Beebee, 1996, Mendelson, 2006). However, a
large proportion of species that are extinct or critically endangered are species that have declined
in seemingly undisturbed environments (Pound, 2006). The causes for decline have remained
unclear, partly because of the complexity of amphibian life cycles and biology (Alford and
Richards, 1999). Although disease is thought to be a major cause, its relationship to
environmental change is not well documented (Berger, et al. 1998; Blaustein and Kiesecker,
2002).
At present, evidence from several scientist ( Kiesecker, Blaustein, 2002; Pound, 2007) suggests
that climate change may be one of the causes. Pound et al (2007) found evidence that suggests
4
increased levels of UV-B exposure caused by climate change are increasing the probability of
frog embryos becoming infected by the fungus, Saprolegnia ferax. Reductions in water depth
due to altered precipitation patterns caused by climate changes expose embryos to damaging
UV-B radiation, increasing the chance of a lethal infection (Pound et al, 2007).
Over the past three decades, the averaged air and sea-surface temperatures of earth have
increased dramatically, due to anthropogenic factors (Parmesan and Yohe, 2003). The tropical
Pacific and Atlantic Ocean are vital in controlling climate and levels of precipitation over Central
and South American Tropics, where the vast majority of amphibians exist. Therefore natural
populations could be vulnerable where local climate is heavily influenced by the tropical Pacific
and Atlantic Ocean. In addition, intense warm episodes caused by El Niño have created extreme
climatic effects that have detrimentally affected biological communities, such as those which live
in the Amazon rainforest (Root et al, 2005).
Rising temperatures have also begun to affect changes in amphibian behaviour. Increases in
temperature are thought to be causing frogs to call and breed earlier in the year (Pound et al,
1999; Gibbs, 2001). Though no detrimental effects have been recorded due to changes in
breeding season, it is important that long term research is implemented and more knowledge is
gained.
2.3 Chytridiomycosis
During the 1990s, significant worldwide declines in amphibian populations became noticeable
with significant losses seen in Costa Rica, Australia’s east coast and western North America
(Mazzoni et al; 2003; Welldon et al; 2004). In 1999 the cause of this decline was identified as a
5
new species Batrachochytrium dendrobatidis (Bd), which infects amphibians and causes the
potentially fatal disease chytridiomycosis. The fungus excludes a lethal toxin or suffocates the
frogs by clogging skin pores (Halliday 2008). Since the findings, Bd has been linked with
amphibian population declines on every continent inhabited by amphibians, and is now seen as
one of the biggest threats to amphibian extinction worldwide (Weldon et al; 2004).
Museum specimen from the 1930s identify the disease as originating from South Africa. It is
thought the spread of the disease began with the commercial trade of the clawed frogs (Xenopus
laevis) (Berger et al, 1999). When Bd is introduced to a new site, it begins to spread through
water courses and amphibian-to-amphibian contact at a rapid rate. A widespread study across
Central America on the spread of Bd calculated the rate of progression at 28-100km/yr
(Amphibian Ark, 2008).
In moist, cool habitats were Bd thrives it is expected that 50% of amphibian species and 80% of
individuals can be expected to become extinct within a year (Lips, 2006). At present there is no
cure for wild species, although a small number of species seem capable of surviving with a Bd
infection. These infected species are expected to serve as reservoirs and carriers for future
outbreaks. Furthermore, many of the species resistant to Bd are recognised as invasive pest
species for example the marine toads, American bullfrogs and African clawed frogs (Amphibian
Ark, 2008).
Amphibians in captivity are also under threat from Bd and deaths in both private and zoo
collections have been reported during 2006 and 2007 in Australia, Europe, USA and Japan
(Berger 1998). At present there are several different treatments that have been used with varying
6
degrees of success, including anti-fungal drugs such as itraconazole. However, New Zealand
scientists have found what they believe to be a cure for the disease. A commonly used eye
ointment, Chloramphenicol, is thought to cure frogs when they are bathed in the solution,
although because of known side-effects in humans it is unlikely that it can be used in the wild
(Griggs, 2007). Therefore, if such findings are correct, zoos and private collectors will have
more options when trying to control an outbreak or rescue frogs from the wild. The bigger
challenge for researchers must be to find a cure that will work in the wild.
At present, chytridiomycosis has only been observed in a relatively low number of cases in Peru.
However, our understanding of the extent of the declines in Latin America, due to
chytridiomycosis is limited to a few well-documented studies, so further research is needed
(Young 2001).
2.4 Trade in amphibians
The harvesting of wild amphibians represents a significant threat to the survival of many species.
The global trade in amphibians for food, biomedicine, and the pet trade is thought to be affecting
around 36 threatened species, representing 3% of all amphibians identified (IUCN, 2006;
Young et al; 2004).
A large majority of amphibians in trade are distributed for frog meat, a practice that is common
in Europe, Canada and the United States. Initial reports in the 1990s identified that Europe
imported approximately 6,000 tonnes of frog legs, and America imported 10,000 tonnes of frog
7
meat (IUCN, 2006; Jensen et al; 2003). The vast majority of frog meat is harvested from the
wild, with the rest coming from farmed populations.
The use of amphibians for medicinal purpose is still being developing, so only represents a small
proportion of amphibians in trade. Asia and Chinese are the main consumers of amphibians for
medicinal use, where it is common for medicinal shops to sell organs, such as dried ovaries and
hallucinogenic skin (Schlaepfer, 2005). Research for medicinal use amongst frog species is on
the increase; as new breakthroughs in science have discovered that some species secrete peptides
that can provide vital biomedicines, including treatments for cancer and HIV. The collection of
peptides can cause substantial stress to individuals and could have harmful effects to wild
populations (IUCN, 2006).
Most amphibians in the pet trade are captive bred; however some species are not and are still
collected from the wild. At present, Peru exports 26 different frog species, all of which are on
Appendix 2 of CITES and are classified as Least Concern by IUCN (IUCN, 2006). All of the
species exported from Peru are within the genus Dendrobatidae and if not managed correctly
could pose a threat to members of this group in the near future (IUCN, 2006; Jensen et al, 2003).
2.5 Pollution and amphibians as indictors
Amphibians are very susceptible to pollutants within their environment (Mandelson 2006).
Amphibians have porous skin, allowing both air and water to pass through it, along with other
toxins. Contaminants within air and water are thought to have a strong impact on the many
amphibian populations by damaging immune systems and thus causing infertility, and
8
malformations. Contaminants can lead to unhealthy adults entering breeding population,
resulting in a more vulnerable population. It can then proceed to these environmental
contaminants causing local population declines and extinction. Amphibians are more vulnerable
than other species to environmental change because they live out their life in two different
habitats, on land and water. In addition, amphibians prey on invertebrates that are both
terrestrial and aquatic, therefore are vulnerable to a bioaccumulation of toxins, which can cause
death and reproductive abnormalities. In view of this amphibians are often referred to as
'environmental indicators', which is another way of saying they are like 'canaries in the coal
mine' (Halliday 2000). Amphibians might be warning us of unsafe environmental conditions
that could eventually seriously impact our health. There is still little research on the effects of
pesticide in amphibians, but early studies indicate that use of chemicals in farming can
negatively affect nearby amphibians which could explain population declines in areas that have
not experienced alteration in habitat (Young et al, 2004).
3. Amphibians Contribution to humanity
The skin of amphibians is more permeable than ours and allows liquids to pass through it fairly
easily; as a consequence they are susceptible to subtle changes in their environment (Mandelson
2006). Although this permeability allows them to live away from water bodies and exploit
different environmental niches, it also means they are at risk of absorbing toxins and chemicals
directly into their body (Attenborough, 2008).
To combat against viruses and microbes that may enter through their permeable membrane, they
have developed some unique biological characteristics to protect themselves. Frogs and other
9
amphibians secrete chemicals onto their skin. This complex mixture of bioactive peptides
provides a first line of defence against bacteria, fungi and viruses (Bradbury 2005). These
peptides have profoundly enhanced the lives of humans in numerous ways. They provide vital
biomedicines, such as compounds that are being refined for antibiotics, stimulants for heart
attack victims, and treatments for diseases including depression, stroke, seizures, Alzheimer’s,
and cancer. Furthermore, new research indicates that the Australian red-eyed treefrog (Litoria
chloris) gives us a compound capable of preventing HIV infection (Amphibian ark, 2008).
Although much of this research is in the early steps, it signifies the necessity of protecting
species not only for their importance to ecosystems and their intrinsic value, but for the benefit
of human life.
4. BIOLOGY
4.1 Biological features
Frogs and toads are classed as amphibians in the order of Anurans. They differ physically from
other amphibians, having a much shorter backbones and at most only nine vertebrae. No adults
have a true tail, revealed by the genus Anura meaning ‘without tail’ (Cogger et al, 1998). The
leg and arm bones of anurans are also different to that of other amphibians as both radius and
ulna, and the tibia and fibula, are fused together. Also, the anklebones of the hind legs are
significantly elongated compared to the front feet allowing them to jump, which is their primary
form of locomotion (Cogger et al, 1998). Toes are usually linked by a membrane, helping them
to drive forward when swimming in water. Teeth are absent in many species, reflecting the
adaptation to insectivorous feeding of most anurans. Feeding is also aided by a proportionally
large and unconnected tongue, which has great movement outside the mouth. Like all
10
amphibians, the skin of frogs is permeable to water and must be kept wet, thus most species live
in moist habitats were they can replenish their water supply (Rodriguez, 1994).
Most species only vary slightly between sexes. The identification is usually based upon the
presence of a vocal sack amongst males. Unlike other terrestrial species, anurans do not use
scent marks to confirm territories and signal for mates. The majority use sound produced when
air is pushed from the lungs over vocal cords, through the mouth into a vocal sack that swells
and vibrates (Rodriguez, 1994). Each species of frog has a different call that can only be
recognised by the other members of its species. Many species also have ear membranes that can
only resonate within their own vocal range therefore can not hear sounds that are equally loud to
humans (Attenborough, 2008).
The evolution of frogs from water to land has developed a unique way of detecting sound on
land. Frogs detect sound using a circular patch of skin called the tympanum, which is held taut
over a surrounding ring of cartilage just above the jaw, below the eye. Each is connected to a
capsule in the skull by a bone allowing the frogs to hear in air (Attenborough, 2008).
4.2 Reproduction
Most North American and European anuran reproduction follows a simple, annual three-step
process; first clumps or long strips of eggs are laid in water and then fertilised by the male which
grasps the female; secondly the eggs hatch into tadpoles which feed on algae. They then grow
legs and metamorphose into froglets; and finally the froglets move onto land where they eat
insects and grow into adults which return to water the following year to repeat the process.
However, there are many other species, mostly in the tropics, that follow different reproduction
processes. In Peru and other South and Central American countries many species breed
11
throughout the year and the females can produce several clutches per year (Rodriguez, 1994).
Many Hylidae species mate and live in the trees and place their eggs on plants over ponds and
slow moving streams. Once the eggs have hatched they drop into the water. Some
eleuthodactylid species lay their eggs on land without having an aquatic stage, whilst some
dendrobatydae species develop youngsters within a pouch on their body until they have become
froglets (Attenborough, 2008).
Regardless of our increasing knowledge about frog species and behaviour, there is still little
information that exists on many species, especially those of South America (Rodriguez, 1994).
5. Methods and Material
5.1 Study site
In this study I examine the diversity and abundance of anurans between three different habitat
types, varzea, terra-firme, and Agujal in a remote area of the Peruvian Amazon. The study was
conducted between the 25th May and the 11th June at the Lago Preto Concession Area (4°28’S,
71°46’W, ~90 m elev.). The Lago Preto Concession Area is part of the larger proposed Yavari
Reserved Zone, an area of over 1 million hectares that stretches from the Peru-Brazil border in
the east, to the Reserva Comunal Tamshiyacu-Tahuaya in the west. The Lago Preto Concession
Area is situated near to the mouth of the Yavari Miri River, on the Peruvian side of the Yavari
River (Pitman et al, 2003).
The climate is seasonal and typical of a humid lowland tropical forest. There is a high annual
precipitation averaging between 2000mm to 3000mm. December to March are often the wettest
12
months of the year with June, July and August being the driest. The annual mean temperature is
constant throughout the year at 24-26° (Bowler, 2006). However, during the first week of study
we experienced a climatic phenomenon, when winds coming north from the Antarctic produced
temperatures as low as 10° (Bodmer per communication, 2007).
The area between Ucayali and the Yavari River holds the most diverse tree communities in the
World (Vasquez-Martinez and Philips, 2000). The area is unique as it consists of three main
habitat types - varzea, terra firme and agujal, which are in close proximity to each other (Bowler,
2006).
Varzea forests are positioned on the fringes of the main rivers of the Amazon basin and total
around 300,000 km² (Ayres et al, 1999, Kvist and Nebal, 2001). Varzea forests are seasonally
inundated with white water and large quantities of sediment rich deposits, originating from the
Andes (Pires and Prince 1985; in Bowler 2006). The sediment rich deposits result in fertile soils
and are of considerable biological significance (Ayres et al, 1999). The undergrowth is modest
due to the frequent flooding and the vegetation that exists is adapted to survive partially
submerged (Whitmore, 1999). The annual flooding has also resulted in a high degree of
endemism amongst fauna and flora (Ayres et al, 1999).
Terra firme forests are those that are elevated and not seasonally flooded. They are positioned off
the floodplain and make up about 96% of the total Amazon forest (Richer, 1994), and are the
most extensive forests in the Yavari Valley (Kvist and Nebal, 2001). As terra firme forests are
not flooded, the soil quality is low and lacks the nutrition of varzea and aguajal forests. The
13
foliage ground cover is fairly dense and the average canopy height is between 25-30 m (Kricher,
1994).
Aguajal, or palm swamps, are permanently water logged due to the clay soils which retain water.
The forest assemblage is very dense with a canopy height of about 20 m and consists of thick
undergrowth. The Yavari Agujal is dominated by the palm fruit Mauritia flexuosa which makes
up about 25-60% of the floodplain (Pitman et al 2003). Aguajal in the Yavari is common on the
flood plains but also occurs in high areas of varzea forest that do not flood profoundly, but do not
dry out during periods of low precipitation (Bowler, 2006).
5.2 Data collection
Six transects of 500m were surveyed in three habitat types - varzea, terra firme and aguajal.
Transects were conducted night and day in varzea and terra firme, though this could not be
achieved in agujal due to difficult conditions. To compensate for this, each transect in aguajal
was conducted twice during the day. Transects were conducted during the period when
amphibians are most active (Rodríguez and Duellman 1994). Day transects were carried out
between approximately 7:00am-2pm and night transects took place between approximately
7:15pm-1am.
Two - three people conducted surveys during the day and night including a guide to direct
through the forest and assist in amphibian detection. To maximise anuran detection the length of
time spent on each 500m transect was relatively long and took between 1h 30min-4h. Visual
14
encounter surveys (VES) during the day were carried out using a probe to disturb leaf litter and
vegetation (Donnelly et al 2004). During the VES all possible microhabitats were searched,
including leaf litter, tree trunks, decayed logs, fallen palm leaves and bromeliads. Due to the
cryptic nature of anurans the disturbance of this vegetation using a probe was the most
systematic method of detection (Donnelly et al 2004). This was achieved by methodically
probing through the area directly in front of the observers, including up to approximately 3m on
either side of the trail. On occasion, some amphibians were observed beyond 3m, however as the
study aims to assess diversity, these specimens were included. To identify anurans during night
transects instead of probing through leaf litter, torches were used to catch the reflection of light
from the eyes of anurans.
Before each survey the following information was recorded: date, name of observer, place, area
searched, weather conditions, start time and finish, and habitat description. When individuals
were encountered information was recorded about species type and the time of capture.
Upon detection and capture of an individual each specimen was handled carefully and
morphological characteristics, such as webbing between fingers, iris and pupil colour, presence
of tympanium, were examined and photographed. This was followed by the recording of
morphometric measurements; snout to vent length (SVL) measured with a calliper to the nearest
0.1mm, sex (if possible), stage (juvenile, adult), distance along and from the transect, vegetation
type and microhabitat use, time recorded and species when possible.
When identification of an individual was not possible in the field, photographs and recorded
observation could be used and compared to the identification guide produced by Rodriguez et al.
15
(1994). To distinguish between species the following characteristics were observed: body size
and shape; iris colour and shape; number and length of toes and phalanges; presence and
patterning of dorsolateral, cranial, belly, ventricular, leg and feet markings and presence of
webbing.
5.3 Statistical analysis
I analysed data using Microsoft Excel and performed statsistical tests using SPSS 15.0 for W
indows. Analysis was based upon the use of the arithmetic mean, standard deviation of samples,
species richness, abundance across habitat type. Tests used were Shannon’s diversity index, and
analysis of variance (ANOVA).
16
6. Results
6.1 Inventory of anurans
Class
Order
Family
Scientific Name
Amphibia
Anura
Bufonidae
Bufo marinus
Bufo typhonius
Dendrophryniscus minutes
Colostethus marchesianus
Colostethus melanolaemus
Colostethus trilineatus
Dendrobates sp
Dendrobates uakari
Epipedobates femoralis
Epipedobates trivittatus
Allophyryne sp
Hyla boans
Hyla fasciata
Hyla geographica
Hyla lanciformis
Hlya parviceps
Hyla rhodopepla
Osteocephalus leprieurii
Osteocephalus planiceps
Osteocephalus taurinus
Scarthyla ostinodactyla
Scinax garbei
Scinax rubra
Scinax cruentomma
Andenomera sp. 1
Andenomera sp. 2
Andenomera hylaedactla
Eleutherodactylus altamazonicus
Eleutherodactylus buccinator
Eleutherodactylus croceoinguinis
Eleutherodactylus delius
Eleutherodactylus diadematus
Eleutherodactyus malkini
Eleutherodactylus martiae
Eleutherodactyus ockendeini
Eleutherodactylus peruvianus
Eleutherodatylus sp
Eleutherodactylus sulcatus
Eleutherodactylus variabilis
Eeutherodactylus Visarsi
Hemiphractus scutatus
Ischnocnema quixensis
Leptodactylus diodrs
Leptodactylus pentadactylus
Leptodactylus rhodanutus
Leptodactylus rhodomystax
Leptodactylus wagneri
Vanzolinius discodatactylus
Syncope antenori
Dendrobatidae
Hylidae
Leptodactylidae
Microhylidae
Table 1. Inventory of anurans 2003, 2006 and 2007
Number
of
Individuals
recorded in each year
2003
2006
2007
1
22
38
34
4
1
3
6
5
1
2
1
10
1
2
1
1
2
1
2
3
1
5
3
2
1
2
1
1
8
3
18
8
1
1
5
1
1
1
2
4
1
13
3
2
10
3
1
8
1
1
2
1
2
1
1
1
4
1
2
5
14
2
1
1
3
1
2
3
1
1
1
4
1
1
2
4
1
34
49
31
1
1
17
With reference to Table 1, a total 49 species have been collectively reordered in the years of
2003, 2006 and 2007 at the Largo Preto Concession Area. In 2003 a total of 142 individuals were
recorded representing 26 species and 4 anuran families. In 2006 the largest number of
individuals was recorded, with 158 individuals representing 24 species and 5 anuran families.
The fewest number of individuals were recorded in 2007 with a total of 132 individual captured.
However, in 2007 the number of species captures increased representing 33 species and 5 anuran
families. All individuals recorded were used in the survey results.
The anuran survey of 2007 added fourteen new species to the inventory list of the Lago Preto
Concession area. Of the species, one species was recorded in the Bufonidae family (Bufo
marinus), three species in the Dendrobatidae family, (Dendrodbates sp, Dendrobates uakari,
Epipedobates femoralis) two species in the Hylidea family, (Osteocephalus taurinus, Sinax
rubra) and eight species in the leptodactylidae family (Eleutherodactylus buccinators,
Eleutherodactylus diadematus, Eleutherodactylus malkini Eleutherodactylus sulcatus,
Eleutherodactylus visari Hemiphractus scutatus. Leptodactylus pentidactylus, Leptodactylus
rhodantutus).
Although fourteen species were added to the inventory, several species were not recorded that
had been in the previous years. The most noticeable of these species was Eleutherodactylus
peruvianus. In 2003 E. peruvianus was recorded fourteen times; this declined dramatically in
2006 to only two recordings, and in 2007 no E. peruvianus were recorded. Andenomera sp 1 also
declined in a similar pattern. In 2003 thirteen individuals were recorded followed by only three
in 2004 and two in 2007. There was only one species that significantly increased in the number
of recordings (Osteocephalius leprieurii). In 2003 Osteocephalius leprieuri had eight recordings
18
followed by a decrease in 2006 with three recording, and in 2007 it increased to eighteen
recordings. Finally two species were consistently the most abundant in all of the three surveys Bufo typhonius and Vanzolinius discodactylus.
6.2 Family Numbers
Most individuals captured in each year were in the leptodactylids family (Fig….). In 2003 a total
of 76 leptodactylids were recorded, followed by 87 leptodactylids in 2006 and 56 leptodactylids
in 2007. In the year of 2003 the second largest family was the hylids family with 38 individuals
followed by the bufonids family with 26 individuals. Though, in years of 2006 and 2007 the
Bufonids family was the second largest family to be recorded. In 2006 the Bufonids family
represented 39 individuals and in 2007 a total of 38 individuals were recorded. In 2003 the
Leptodactylids family and the Hylids family collectively represented 80.28% of total number of
individuals recorded. Whereas in 2006 it was the leptodactylids family and Bufonids family that
collectively represented 79.75 % of total number of individuals recorded. In 2007 this
percentage slightly decreased with the leptodactylids family and the bufonids family collectively
representing 71.21% of the total number of anurans recorded. In 2003 the bufonids family
represented 18.3% with 26 individuals recorded leaving 2 individuals in the family dendrobatids
representing 1.4%. No microhylids species were recorded in 2003. The dendrobatids family in
2006 represented 12.02% with 19 individuals recorded. This was followed by the hylids family
which had dropped significantly since 2003. In 2006 it represented only 7.59 % compared to
26.76% in 2003. Only one individual form the microhylids family was found in 2006
representing 0.63% of individuals recorded. Finally, in 2007 the percentage of hylids recorded
had increased with 26 individuals recorded representing 20% of the population. The
19
dendrobatids family represented 8% with 11 individuals recorded, leaving the family microhylids
with only 1 individual representing 0.8% of the individuals captured.
100
90
80
No. of Individuals
70
60
50
40
30
20
10
0
1
Bufonidae
2
Dendrobatydae
2003
3
Hylidae
2006
4
Leptodactylidae
5
Microhylidae
2007
Figure 1. A comparison of family numbers across three studies at Lago Preto (all species
pooled).
20
80
70
60
no.of Individuals
50
40
30
20
10
0
Varzea
Tirre firme
Agual
Habitat
2003
2006
2007
Figure 2. Origin of individuals collected all species pooled.
6.3 Origin of individuals
Anurans were collected in three different habitats – varzea, tirre firme and aguajal. There were
clear differences in the number of individuals recorded in each habitat. Figure 2 shows that over
the three years most individuals were found in the varzea habitat. This correlates with the data
found in 2006 and 2007, though in 2003 most individuals were recorded in terra firme. Over all,
21
aguajal produced the least number of individuals recorded. This is clearly seen in the years of
2007 and 2006; however in 2006 fewer individuals were recorded in terra firme than in aguajal.
6.4 Species Richness
In total 49 species have been collectively reordered in the years of 2003, 2006 and 2007. Terra
firme was the most species rich habitat over the three studies and in study year retrospectively.
All years combined there were 37 species in total recorded in terra firme. Varzea was the second
most species rich over the three studies and in each study retrospectively with 25 species in total.
Aguajal was the least species rich with only 12 species recorded over the three studies.
25
No. of Species
20
15
10
5
0
Vazea
terre firme
aguajal
Habitat
2003
2006
2007
Figure 3. Comparison of Species richness between habitats
22
7.2 Abundance of Species 2007
Results for the varzea habitat show that it was dominated by two species, Bufo typhonius and
Osteocephalusleprieurii. Bufo typhonius was the most abundant species within varzea followed
closely by Osteocephalus leprieurii. The third most abundant species was Vanzolinius
discodatactylus. The remainder of species have relatively low abundance within the varzea.
0.0035
0.003
Abundance (Individuals/km)
0.0025
0.002
0.0015
0.001
0.0005
ae
m
El
e
ut
h
op
hr
y
ni
sc
an
ol
el
en
dr
D
ol
os
te
t
hu
s.
M
m
hu
s.
C
us
er
us
od
m
ac
in
ty
ut
lu
es
s.
El
d
ia
eu
de
th
m
er
at
od
us
ac
El
ty
lu
eu
s.
th
Vi
er
sa
od
rs
ac
i
ty
us
.m
H
al
yl
ki
a.
ni
G
eo
gr
ap
hi
Le
ca
pt
H
od
yl
ac
a.
ty
bo
lu
an
s.
s
pe
nt
O
ad
st
eo
ac
ce
ty
lu
ph
s
al
O
us
st
.le
eo
pr
ce
ie
ph
ur
Va
al
ii
us
nz
.p
ol
la
in
ni
iu
ce
s.
ps
di
sc
od
at
ac
ty
lu
s
us
an
es
i
ar
ch
ty
p
C
ol
os
te
t
Bu
fo
.
p
G
er
a.
no
m
An
de
iu
ho
n
an
dm
a
s
0
Species
Figure 4. Abundance of individuals within varzea 2007
23
no
m
er
a.
G
p
B
a
uf
D
en
o. ndm
d
t
El
a
y
ro
eu
ba pho
th
ni
te
D
er
od end s. s us
p
ro
ac
ba eci
ty
El
es
te
eu lus
s.
th
a
El
u
eu ero ltam ak
a
El
eu the dac azo ri
ro
t
th
n
yl
d
ic
er
us
us
od act
ac ylu sul
El
c
s
at
.b
eu tylu
us
u
s
th
er . cr cci
na
od
oc
to
eo
Ep act
r
in
y
ip
gu
ed us.
i
o
n
o
c
is
H bate ken
em
de
s.
i
i
Is phr Fem ni
Le chn actu or
a
o
pt
s
od cne
sc lis
u
ac
m
ta
a.
tu
Le tylu
s. quix s
pt
pe
od
Le
nt ens
ac
a
i
pt
od tylu da s
ct
s.
ac
y
rh
ty
od lus
l
an
Le us.
r
h
ut
pt
u
od od
O
ac om s
st
ty
ys
eo
ta
ce lus
x
.w
O
ph
st
a
gn
eo alu
er
s.
c
le
Sc ep
pr i
ha
ar
i
e
lu
th
u
s.
yl
ta rii
a.
u
o
rin
Sc
st
u
i
in
ax nod s
ac
.C
ru
t
en yla
to
m
S
Va
Sy cina ma
nz
nc
x.
ol
r
in
iu ope ubr
s.
an a
di
sc
t
od eno
r
at
ac i
ty
lu
s
An
de
Abundance (Individuals/km)
(Figure 5). More species were identified within terra firme than in varzea and aguajal, though
like varzea, terra firme is dominated by Bufo typhonius. However, when both habitats are
compared, the abundance of Bufo typhonius is higher in Varzea than in terra firme. The second
most abundant species in terra firme was Eleutherodactyus ockendeini, but it was considerably
less abundant that Bufo typhonius. The remainder of species have relatively low species
abundance within terra firme.
0.0025
0.002
0.0015
0.001
0.0005
0
Species
Figure 5. Abundance of individuals within terra firme 2007
24
Only two species were recorded in Aguajal, Bufo marinus and Vanzolinius discodatactylus. The
most abundant species by far was Vanzoliniu discodatactylus. Bufo marinus had a low
abundance with only one individual identified (Figure 6).
0.0035
0.003
Abundance (Individuals/km)
0.0025
0.002
0.0015
0.001
0.0005
0
Bufo. marinus
Vanzolinius.discodatactylus
Species
Figure 6. Abundance of individuals within aguajal 2007.
25
6.6 Habitat diversity indices
The species diversity in each habitat is illustrated in figure 7 below. The Shannon Weiner results
show that the terra firme has the highest level of diversity. Following close behind is varzea,
then Aguajal, which has a comparatively very low level of diversity.
2.5
2
Diversity index
1.5
1
0.5
0
Varzea
Terrefirme
Aguajal
Habitats
Figure 7.Diversity of species within three different habitats 2007. (Shannon Weiner Index).
26
Habitats
Mean
N
Std. Deviation
varzea
1.9697
33
4.59949
Tirra firme
1.4848
33
2.50151
.5758
33
3.13279
1.3434
99
3.53456
Agaujal
Total
Table 2. The mean number of individuals within Varzea, Terra firme, and Agujal for 2007.
Table 2 confirms that varzea and terra firme have a significantly higher average number of
individuals than aguajal. Varzea has the highest average number of individuals followed by terra
firme and then aguajal.
Sum of
Squares
Mean
df
Square
F
Sig.
Between
6.092
1
6.092
Within Groups
59.908
97
.618
Total
66.000
98
9.864
.002
Groups
Table 3. ANOVA Results
27
The ANOVA table above shows that there is a significant difference in the species abundance of
anurans between the three major habitats. This can seen as the significance is above 0.05.
7. Discussion
7.1Family numbers
Most individuals were recorded in the leptodactylid family, which was somewhat expected due
to the survey techniques used, which favoured terrestrial species. Also, the leptodactylids are the
largest family of anurans within the tropics of South America. The second most abundant family
in the tropics of South America is hylids (Huyse 2005). However, very few species of this
family have been recorded at Lago Preto in comparison to what has been found in other areas of
the Iquitos region. Rodríguez and Duellman (1994) identified over fifty species of the hylid
family within the Iquitos region in comparison to only fourteen species that has been found at
Lago Preto. Although it needs to be taken into consideration that Rodríguez and Duellmans’
(1994) findings were over a much larger area, their findings still highlight the possibility of
finding more species within the hylid family at Lago Preto. The major reason for not recording
more species within this family is likely due to the bias of the survey methods. All three studies
concentrated on finding species that were found within the leaf litter, which reduced the chance
of recording arboreal Hylidae species.
The second most abundant family recorded at Lago Preto over the three studies was the
Bufonidae family. However, the Bufonidae family had relatively few species recorded with in its
family at Lego Preto. This family was significantly dominated by one species alone, Bufo
typhonius, with only two other species within this family being recorded, Bufo Marinus and
Dendrophyryniscos minutes. The domination of Bufo typhonius within this family at Lago Preto
28
could be explained by the breeding characteristics of this species. Bufo typhonius is an explosive
breeder (Wells, 1979) so, as all three studies have been conducted at approximately the same
time of year and most Bufo typhonius individuals recorded have been juveniles, it is likely that
the surveys have coincided with the end of the breeding season. Such findings of amphibian
distribution and activity have long been recorded to be influenced by abiotic and biotic factors
(Alonso et al, 2001).
Low numbers of microhylids and dendrobatids have been found at Lago Preto. This was
expected as both families are relatively small in number and in physical size making them
difficult to record.
7.2 Abundance of Anurans in Varzea, Terra firme and Aguajal.
In the studies from 2003, 2006 and 2007 on anuran abundance at the Lago Preto anurans were
found in all three major habitats. However, there were differences in the assemblages of the
species found in each habitat. The abundance research from 2003 and 2006 showed that the
abundance of species was greater in varzea and in terra firme than in aguajal. This was
confirmed again in the results of 2007 where the abundance of individuals were found to be
greatest in varzea. The cause for this in 2007 was the high numbers of Bufo typhonius and
Osteocephalus leprieurii within the varzea habitat. Nearly all recordings of the two species were
juveniles and as both of these species need water for breeding and the initial stages of their
lifecycle, varzea habitat is ideal (Rodríguez and Duellman 1994). Furthermore, as survey
methods were biased towards terrestrial species and Bufo typhonius is a terrestrial species it is no
coincidence that it was the most abundant species found.
29
Terra firme was the second most abundant habitat in 2007 and like varzea it was dominated by
Bufo typhonius. All other species within this habitat were evenly spread, all having relatively
low levels of abundance. The most abundant family within terra firme was the leptodactylids,
accounting for at least three quarters of the population of anurans.
When comparing the three studies form 2003, 2006 and 2007 all studies suggest that the aguajal
habitat produces the least amount of individuals. In 2007 this was clearly observed as very few
individuals were recorded. Another interesting note regarding species abundance is that aguajal
is the only habitat where Bufo typhonius was not the most abundant. Vanzolinius discodactylus
was the most abundant species and besides one recording of Bufo marinus it was the only species
recorded. Again like Bufo typhonius in the varzea habitat all recorded individuals of Vanzolinius
discodactylus were in the early stages of their life cycle. The underlying factor for the high level
of Vanzolinius discodactylus juveniles in aguajal are likely to be linked to high production of
fruits. The high production of fruit results in abundant numbers of insects, on which many of the
Vanzolinius discodactylus individuals were seen feeding on. Though the majority of the insects
are relatively small their high densities provide ample food for juvenile anurans. Furthermore,
the fact that the majority of insects feeding on the fruit are small is advantageous to juveniles,
which require large amounts of small prey (Thomson 2006).
An explanation for why so few individuals and species were recorded in aguajal is the difficulty
to manoeuvre through the habitat whilst conducting a survey. This is because of difficult
conditions caused by swampy ground and poor visibility due to thick foliage (Bowler 2006).
Contributing to the low levels of abundance and diversity of species in aguajal is the lack of data
30
for night transects. Only one night transect was possible during the survey of 2007 as conditions
were too difficult. This could have seriously affected the results as most anaran species are
nocturnal in habit (Rodriguez, 1994). However, it is possible that low levels of abundance and
diversity exist due to agujal being an unstable habitat, because of constant flooding, resulting in
less ecological niches, food and suitable microhabitats for species to live in (Pitman et al 2003).
7.3 Species richness and diversity
The surveys conducted in 2003, 2006 and 2007 all indicate that species richness is greatest in
terra firme followed by varzea and then aguajal. These findings correlate with previous studies
indicating that terra firme habitats should contain the highest proportion of species. This is due
to the increased diversification of vegetation, arthropods and floral species. The increase in
diversification of fauna and flora, combined with the stable environment that terra firme
provides, creates many more ecological niches allowing more species to live within one habitat
(Pitman et al, 2003).
Although the species inventory was increased by fourteen species in 2007, resulting in 47 species
in total recorded at Lago Preto, the level of species richness recorded is much less than in other
studies conducted in the Amazon Basin. At a single site in the upper basin of the Ecuadorian and
Peruvian Amazon 81 species of frog have been found (Duelman 1992). Evan closer to the study
site, in protected areas along the Rio Yavari Miri and the Rio Yavari, levels of anuran diversity
encountered by Perez et al (2007) were over 71 species in the same habitat types.
31
The lower level of species diversity recorded at Lago Preto could be due to several reasons. One
reason could be that the study began at the beginning of the dry season when amphibian activity
is not at its highest. Therefore amphibian diversity can be expected to be less than what would
be expected during the wet season (Young et al, 2004). Amphibian activity in the Neotropics is
seasonal with an increased productivity and reproduction during the early months of the rainy
season. This is believed to ensure maximum reproductive productivity, avoiding the possible
obliteration of tadpoles during the drier months (Alonso et al, 2001). As the studies of 2003,
2006 and 2007 were conducted during the start of the dry season, levels of anuran diversity can
not be expected to be at their highest.
Unusual weather conditions during the first week of the 2007 survey could also have affected
levels of anuran diversity. Temperatures as low as 10° coming north from the Antarctic were
produced by a climatic phenomenon that only occurs approximately every ten years. (Bodmer
per communication, 2007). Climatic changes during the beginning of the 2007 survey could
have been unfavourable for amphibian activity resulting in a decrease in observation (Pechmann
1991).
7.4 Trends in species abundance 2003, 2006 and 2007
When comparing the abundance of individual species in each study there have been some
noticeable trends. Throughout the studies Vanzolinius discdactylus have been the most abundant
species, though it seems that each species has a preference in habitat. Vanzolinius discdactylus
appears to prefer aguajal where it has been recorded in all three studies to be the most dominant.
32
While Bufo typhonius appears to be less restricted in the studies in 2006 and 2007 it was clearly
more abundant in varzea.
However, there is also evidence of declines in species abundance. In 2003 Eleutherodactylus
peruvianus was the most abundant species within terra firme. This declined dramatically in 2006
and then in 2007, no individuals were recorded in either habitat. A similar decline has occurred
in another leptodactylid, Adenomera sp.1. It too was recorded as one of the most abundant
species in 2003 and has since declined. There are a number of possible reasons for the declines,
including climate change, chytridiomycosis, or any of the other threats that amphibians face, but
none can be ascertained from this data alone. More research would be needed.
On the other hand, with each year of comparative data, there have been species added to the
inventory of Lago Preto, and in one case a species’ abundance appears to have increased
(Osteocephalus leprieurii).
8. Further research
Studies lasting more than two years are uncommon (Skelly et al 2003), but as amphibians are
globally declining, it is imperative that long term monitoring of anuran diversity and abundance
at Lago Preto continues, as it is a strong hold for many species. Long term monitoring has been
identified as the ideal way to collect and document changes in abundance and distribution of
species (Caughley and Gunn 1996). Historical data is a necessary step in understanding past
actions and detecting the effects of climate change, chytridiomycosis and other relevant impacts
and in formulating management strategies (Skelly 2003).
33
Long term monitoring for amphibians is even more important as presence and absence and
distribution can change from year to year. There are two possible explanations for fluctuations.
Year to year fluctuation in sampling could be a result of inadequate surveying and the cryptic
behaviour of anurans. Secondly, changes in distribution could reflect anuran behaviour. Anurans
are known to stop breeding during periods in which climate is unfavourable reducing their
abundance and then rebound when climate is favourable (Pechmann et al 1991; Skelly 2003).
Consequently, consistent long term monitoring of anuran populations such as that of
Eleutherodactylus peruvianus and Andenomera sp.1 is necessary to understand the true
fluctuation in abundance and distribution.
In addition to the continuation of the long term monitoring using the study methods of the three
previous studies, it is important that new study techniques are used to favour arboreal species,
primarily those within the Hylidae family, most of which are nocturnal and only descend to
breed around lakes, ponds and streams for breeding. A suggested solution to monitor arboreal
species would be to identify species through audio surveillance, as most species have their own
individual call (Donelley 2004). This could be combined with surveys of breeding grounds such
as lakes, ponds and slow flowing stream. A variety of survey method techniques has a better
chance of increasing the reliability of data collected for long term monitoring and future
management strategies.
34
9. Limitations
A few limitations existed during this study which may have influenced the results and amount of
data I was able to collect. The short time period for study (from 25th May to 11 June) affected the
amount of data that could be collected. The time of year in which the study and previous studies
have been conducted is likely to have affected the abundance and diversity of anurans recorded,
as all studies were conducted at the beginning of the dry season, when anuran activity is not at its
highest. In addition different structures of vegetation and ground conditions between habitats
created different levels of visibility, skewing the chance of recording an individual and the use of
semi-permanent trails is likely to have some impact on diversity. And finally, the bias of survey
methods towards terrestrial species is likely to have affected results.
10. Conclusions
Amphibian populations are affected by a number of different factors, from natural fluctuation
due to disease and climatic/breeding preferences, to anthropogenic factors such as climate
change, and habitat to destruction. Data collected in 2007 correlates with that of the previous
years and other research conducted on anuran abundance and diversity within the South
American Tropics. Anurans were found to be the most abundant in varzea whilst terra firme was
the most diverse, with aguajal appearing to be the least abundant and diverse. However, there
35
may be influential variables which have not been accounted for, such as the different levels of
visibility between habitats and the time of year at which all three studies have been conducted.
It is important to minimise the impact that amphibians face, not only for their intrinsic value and
for their importance within the ecosystem, but because they can be used as environmental
indicators of ecosystem health. The conclusions drawn from this study and those of previous
years can be useful in providing base line data for the long term monitoring of anurans at Lago
Preto. Although anurans at Lago Preto face relatively little amount of physical disturbance from
human activities due to habitat destruction, it is still important to monitor changes in abundance
and diversity, as it is still possible that numbers may be declining due to chytridiomycosis and
climate change. Therefore it is essential that consistent and long term monitoring continues at
Lago Preto.
36
11. List of References
Alford, R. A., Richards, S. J., (1999) Global amphibian declines: a problem in applied ecology.
Annul. Rev. Ecology Systems. 30, 133–165
Attenborough, (2008). Life in Cold Blood. BBC Books.
Amphibian Ark, (2008). Frightening statistics. Available at:
http://www.amphibianark.org/statistics.htm
Alonso A., Dallmeier F. and Campbell P. (2001). Urubamba: The Biodiversity of a
Peruvian Rainforest, SI/MAB Series #7. Smithsonian Institution, Washington, DC.
Ayer, J.M., Alves, A.R., Queiroz, H., marmontel, M., Moura, E., Magalhaes Lema, D., Aevedo,
A., Reis, M., Santos, P., SIlveiria, R Materson, D. (1999). Mamiraua: The conserrvation of
Biodiversity in an Amazonian Flooded Forest. In Vazea: Diversity, Development, and
Conservation of Amazonian’s Whitewater Floodplains, edited by Padoch, C., Ayres, J.M.,
Pinedo-Vasqez, M. Henderson, A. The New York Botanical Garden Press.
Blaustein, A. R. & Kiesecker, J. M. (2002) Complexity in conservation: lessons from the global
decline of amphibian populations. Ecology Letters. 5, 597–608
37
Berger, L. et al. (1998) Chytridiomycosis causes amphibian mortality associated with population
declines in the rain forests of Australia and Central America. Proc. Natl Acad. Sci. USA 95,
9031–9036
Berger, L., Speare, R., and ken,t A., (1999) Diagnosis of chytridiomycosis in amphibians by
histologic examination. Availalbe at;
http://www.jcu.edu.au/school/phtm/PHTM/frogs/histo/chhisto.htm. Accessed on 21/02/2008
Bodmer, R., (2007). Climatic phenomena; per communication.
Bradbury, J., (2005) Frog skin hope for HIV prevention. Drug Discovery Today; 10- 22, 15;
1489-1490
Bowler, M., (2006). The Ecology and Conservation of the Red Uakari Monkey on the Yavari
River. Dice, Thesis.
Caughley, G., and Gunn. A. (1996). Conservation biology in theory and practice. Blackell
science, Cambridge, Massachusetts.
Cogger H.G. and Zweifel R.G. (1998). Encyclopedia of Reptiles and Amphibians, 2nd edition.
Academic Press, San Diego.
38
Donelly, M.A., Chen, M.H., Watkins G.G. (2004). Sampling amphibians and reptiles in the
Iwokrama Forest ecosystem. Proceeding of the Academic of Natural Sciences of Philadelphia.
154: 55-69.
Frankham, R, Ballou, J.D., Briscoe, D.A., (2005) A Primer of Conservation Genetics. Cambridge
University Press.
Gascon, C. Collins, J.P, Moor, R.D, Church, D.R., McKay, J.E., and Mendelson J.R (2005)
Amphibian Conservation Action Plan. Prooceedings; IUCN/SSC Amphibian Conservation
Summit 2005.
Griggs, K., (2007). Frog killer fungus ‘breakthrough’. Available from;
http://news.bbc.co.uk/1/hi/sci/tech/7067613.stm
Halliday, T. (2000) Do frogs make good canaries? Biologist, London 47, 143-146.
IUCN, Conservation International, and Nature……?????. (2006). Global Amphibian Assessment
(www.globalamphibians.org). Accessed on: 03/01/2008
Tine, H. & Filip V. (2005) Long term monitoring Comparing Host and Parasite Phylogenies:
Gyrodactylus Flatworms Jumping from Goby to Goby. Systematic Biology, 54, 5, 710-718.
Kricher J., (1997) a Neotropical Companion; An introduction to the Animals, Plants, and
Ecosystems of the New World Tropics. Princeton University Press.
39
Kvist, L.P., and Nabel, G. 2001. A review of Peruvian Flood plain forests: ecosytems,
inhabitants and resource use. Forest Ecology and management 150; 2-26.
Lips, K.R., et al, (2006). From the cover: Emerging infectious disease ans the loss of biodiversity
in a Neotropical amphibian community. PNAS; 103; 2165-3170. Available from;
http;//www.pnas.org
Mazzoni R., Cunningham A.A., Daszak P., Apolo A., Perdomo E. and Speranza G. (2003).
Emerging Pathogen of Wild Amphibians in Frogs (Rana catesbeiana) Farmed for International
Trade. Emerging Infectious Diseases 9.
Mendelson, J.R, et al (2006). Confronting Amphibian Declines and Extinctions
Science; 313-5783, p. 48
Parmesan, C., Yohe, G. A., (2003). Globally coherent fingerprint of climate change impacts
across natural systems. Nature 421, 37–42
Pearman P.B. (1997). Correlates of Amphibian Diversity in an Altered Landscape of Amazonian
Ecuador. Conservation Biology 11: 1211-1225.
Pechmann, J.H.K., et al (1991) Declining amphibian populations: the problem of separating
human impacts from natural fluctuations. Science 253,892-895.
40
Pires, J. M and Prance, G.T. 1985. the vegetation types of the Brazilian Anazon. Amazonia G.T
Prance and T.E. Lovejoy, eds. Pergamon Press: New York. 109-145. Cited In: Bowler, M.,
(2006). The Ecology and Conservation of the Red Uakari Monkey on the Yavari River. Dice,
Thesis.
Pounds, J.A., (2006) Widespread amphibian extinctions from epidemic disease driven by global
warming. Nature 439, 161-167
Pound, J.A., Fogden, P.L and Cambell, J.H., (1999) Biological response to climate change on a
tropical mountain. Nature 398, 611-613
Rodríguez L.O. and Duellman W.E. (1994). Guide to the Frogs of the Iquitos Region,
Amazonian Peru. Natural History Museum, University of Kansas.
Root. L., MacMynowski, D. P., Mastrandrea, M. D. & Schneider, S. H., (2005) Human-modified
temperatures induce species changes: Joint attribution. Proc. Natl Acad. Sci. USA 102, 7465–
7469
Schlaepfer M.A., Hoover C. and Dodd C.K. (2005). Challenges in Evaluating the Impact of the
Trade in Amphibians and Reptiles on Wild Populations. BioScience 55
Skelly D.K, Yurewicz, K.L., Werner, E.E and Relyea, R.A. (2003). Estimating decline and
distribution change in amphibians. Conservation Biology, 17,3, 744-751.
41
Thomson, L. (2006). Amphibian Diversity at the Lago Preto Concession Area and anlysis of
habitat distribution. Dice practicle reseach project. 17 June-11 July.
Young, B.E, Lips, K.E, Reaser, J.K., Ibáñez, R., Salas, A.W., Cedeño, J.R., Coloma, L.A., Ron,
S., Marca, E., Meyer, J.R., Muñoz, A., Bolaños, F., Chaves, G., Romo, D., (2001). Population
Declines and Priorities for Amphibian Conservation in Latin America.
Conservation Biology 15, 5. 1213–1223.
Wells, K.D (1979). Reproductive Behavior and Male Mating Success in a Neotropical Toad,
Bufo typhonius. Biotropica, 11, 4. 301-307
Weldon C, du Preez LH, Hyatt AD, Muller R, Speare R, (2004) . Origin of the amphibian chytrid
fungus. Emerg Infect Dis. Available from: http://www.cdc.gov/ncidod/EID/vol10no12/030804.htm. Accessed on 29/12/07
Young B.E., Stuart S.N., Chanson J.S., Cox N.A. and Boucher T.M. (2004). Disappearing
Jewels: The Status of New World Amphibians. NatureServe, Arlington, Virginia.
42