North-Western Journal of Zoology
Vol. 2, No. 1, 2006, pp.47-58
The effects of acid rain on anurans
and the possibilities of protection in Hungary,
focusing on the challenges of forest management
Zsuzsanna ANTAL1, Pasi PUTTONEN2
1
University of Debrecen Faculty of Agriculture,
Department of Nature Conservation Zoology and Game Management,
Böszörményi street 138., Debrecen 4032, Hungary, e-mail: [email protected]
2
The Finnish Forest Research Institute, Metla, Unioninkatu 40 A, 00170 Helsinki, Finland
Abstract. Twelve predominantly sylvan anuran species presently occur in Hungary (Table 1).
Unfortunately their numbers are decreasing. To stop, or at least decelerate this process, there is a
need to get acquainted with the dangers that prey upon them. Acid rain is one of these
contingencies. Acid rain can harm anurans both directly and indirectly. Direct effects are very
serious, but indirect effects are long lasting due to loss and damage of forests as very important
habitats. In assessment of ecology, anurans among other biotic elements are also participants of
the Earth’s ecosystem, while in assessment of biodiversity these species are also needed to
conserve the natural façade of Earth for the further generations. Thus protection of these animals
is one step in achieving aims of nature conservation. Forest management practices together with
modern nature conservation methods can benefit anuran protection in Hungary.
1. Introduction
According
to
Hartel
(2001)
amphibian,
and
therefore
anuran
extinctions, are attributed to several
causes including; climate change, habitat
loss and fragmentation, introduced
species (especially fish), biocides, UV-B
radiation and disease. Green (1999) states
that acid precipitation is also among the
causes. As a result amphibian extinctions
proceed very quickly, while our
knowledge in this field enlarges rather
more slowly, due to the fact that the
zoological literature on amphibians is not
very voluminous (Mazál 1997). We still
lack articles that examine the effects of
acid rain on anurans. In spite of meagre
research on the relationship between
anurans and acid rain, this article aims to
examine a current situation in protection
of anuran habitats in Hungary. We focus
on the complex effect of acidification,
through the loss of quality of forest
habitats, because we argue that role of
forest management in protection of
anurans and their habitats have been
neglected.
2. Life history and ecology of pond
breeding amphibians
Some 360-370 million years ago,
amphibians were the first vertebrates that
ascended from the water. Then, on the
brink of the Devonian and Carboniferous
periods during the Palaeozoic era, only
plants and invertebrates inhabited the
land. Since this geologic time, amphibians
Zs. Antal, P. Puttonen
48
have inhabited the Earth (Clarke 1993). In
the course of time they survived glacial
periods and outlived the extinct dinosaurs.
The
evolutionary
and
scientific
significance of amphibians lies in the very
fact that they are the existing link between
the Palaeozoic era and the present day.
Whilst amphibians have formed an
existing class for more than 350 million
years, the number of species and
populations is decreasing noticeably. The
reasons for the decrease are partly
imbedded in their unique anatomy and
lifestyle, while the biggest problem is the
loss and fragmentation of their habitats
(Kosik 2004a).
Table 1. The taxonomic classification of anuran species in Hungary (Kiss 2003)
Preferred habitat
Order: Anura
Family
Discoglossidae
Pelobatidae
Species
Bombina bombina
Bombina variegata
Pelobates fuscus
Bufo bufo
Bufonidae
Bufo viridis
Hylidae
Ranidae
Hyla arborea
Rana temporaria
Rana arvalis wolterstorffi
Rana dalmatina
Rana ridibunda
Rana lessonae
Rana esculenta
Because of their complex life cycle,
pond breeding amphibians require both
aquatic and terrestrial habitats to complete
their life histories (Green 1999). Water is
absolutely necessary for the reproduction
of anurans as after mating the females lay
their eggs into ponds or small puddles.
This is the first step of metamorphosis,
during which the eggs turn into juvenile
anurans that can leave the water and live
an amphibious lifestyle (Kiss 2003).
However, most species do not move far
from the water and all return in the
breeding season.
lowlands and hilly country; near to water
mainly rainy mountainous district; near to water
lowlands and hilly country; areas with loose sandy soil
everywhere in Hungary ; except reproduction period
distant from water;
mainly lowlands; except reproduction period distant from
water
rushes and forests; near to water
hilly country; moist forests and meadows
lowlands; swampy areas
lowland and mountain forests
lowlands; near to water
lowlands; near to water
lowlands, hilly country and mountainous district; near to
water
Therefore any disturbance, in either
their aquatic or overland habitats, will
affect the pond breeding amphibians’ year
round life. Moreover, the loss of
connectivity between these habitats has
the same result, through increasing the
mortality during mass migrations and/or
juvenile dispersal. Besides their complex
habitat requirements, the unique anatomy
and physiology of anurans exposes them
to many endangering environmental
factors. The skin of amphibians lacks
epidermal structures, such as scales or
feathers that are typical with other
The effects of acid rain on anurans and the possibilities of protection in Hungary…
vertebrates (Hartel 2001). The cuticle is
thin and rich in glandules, but there is no
insulative horn layer on the outer surface
of their skin. The glutinous excretion of
the glandules can provide a defensive
function against predators for certain
species, but their main function is to keep
the skin wet. This function is essential to
prevent desiccation of the animals. As the
lung of amphibians is considerably
underdeveloped, 60 percent of their
respiration is through their skin and the
dissolved oxygen in the water can partly
diffuse via the skin. Damage to the
insulator horn layer is life threatening
(Mazál 1997). As a result, the special skin
anatomy of amphibians is susceptible to
toxic substrates And damage by
ultraviolet radiation (Blaustein &
Kiesecker 2002). Both toxic substrates
and ultraviolet radiation are very
dangerous and potentially lethal to the
ova. The ova of amphibians do not have a
protective shell the membrane of the ova
is permeable just like the skin of the fullgrown animals (Kosik 2004a).
Amphibians are affected by habitat
degradation in two ways; on one hand
because of the complex life cycle and thus
the complex habitat demand, and on the
other hand, because of their specialised
anatomy.
Besides the mentioned ecological role
there are several other reasons for the
protection of anurans. One of these
reasons is that being predators as adults,
they play an important role in the
regulation of invertebrate populations in
the ecosystem. In the course of feeding
anurans consume a large amount of
invertebrates. Among these prey animals
there are species considered as pests in
agriculture, horticulture and forestry. By
49
regulating these invertebrate populations
anurans have a direct economical role.
Some anuran species serve as food for
humans whilst the excretions of some
species skin glandules are used by
medical science. Amphibians are still
widely used as model organisms for
research (Kiss 2003).
3. Effects of acid rain on anurans
There are numerous causes for the
declines in anuran populations and the
first step to stop these, or at least slow
them down is to recognise these causes.
Acid rain is one of these harmful
environmental factors (Räsänen et al.
2002, Glos et al. 2003. Beebee & Griffiths
2005).
Acidity is a natural characteristic of
rain, but since the beginning of the
industrial revolution the acid concentrate
in precipitation has increased. As widely
reported, acid rain has harmful effects on
both the living and the non-living
environment (ApSimon et al. 1997, Baum
2001, Moore 1994, Ormódi 1999, The
Swedish NGO Secretariat on Acid Rain
2005).
The harmful effects of acid rain on
anurans are both direct and indirect (Fig.
1). Indirect effects are mainly the
destructive impacts of acid rain on forests
that finally lead to damage or loss of some
critical terrestrial habitats.
3.1. Direct effects of acid rain on
anurans
As eggs and larvae, anurans live a
fully aquatic lifestyle and during the
larval stages they are most affected by
water acidity. This development stage
Zs. Antal, P. Puttonen
50
often occurs during the period of the
highest water acidity, following snowmelt
in the spring (Baum 2001). According to
Pahkala et al. (2001) the survival
probability of anuran larvae and
hatchlings are reduced by low pH (5.0),
the embryonic mortality can increase in
acidic water.
The case is all the same with anuran
ova. Just like the skin of the full-grown
animals, the ova lack defensive husk and
permeable for water (Kosik 2004a). Water
with toxic substrates can penetrate the
skin and the ova membrane, and can
damage the animals physiology. Toxic
substrates can cause reproductive
abnormalities and in more serious cases, a
combined effect of toxic substrates and
parasites can lead to deformations in the
number of limbs (Kiesecker 2002). These
deformations can affect the genetic
makeup of the species permanently and
can become hereditary.
Figure 1. Direct and indirect effects of acid rain on anurans.
All indirect effects should be taken into consideration as the consequence
of forest damage on anurans.
3.2. Indirect effects of acid rain and
anurans
Whilst the effects of low pH in surface
waters is significant during the larval
stages (Pahkala et al. 2002), in case of
adult anurans the indirect effect of
acidification of terrestrial habitats is more
important. The effects of acid deposition
can apply either directly or indirectly on
the trees. Direct damage mechanism
typically involves a progressive loss of
foliage with discoloration (yellowing or
browning) of the remaining leaves. In
some instances, there is evidence of death
or distortion of roots. Deterioration may
eventually result in death of the trees
(Packham et al. 1992). Besides direct
damage, forests suffer a large number of
different stresses such as drought, frosts,
insect
attack,
disease
and
soil
deficiencies, all of which can affect tree
health and appearance. Acid deposition
The effects of acid rain on anurans and the possibilities of protection in Hungary…
can make a tree more susceptible to these
stresses or be a primary cause of the
stress. Branches and stems can suffer
fungal, insect and mammal attack as well
as direct foliage damage such as that of
wind and storms. Increased evaporation is
also an acid deposition related stress to
branches and stems. Root effects are on
mycorrhizal fungi, water and nutrient
uptake (ApSimon et al. 1997).
Potentially the most serious effect is
the destruction of forests. However,
restoring the damage caused by acid rain
is not an easy job (Moore 1994). As most
anurans in Hungary use forested areas as
terrestrial habitats, the destruction of trees
can lead to deterioration and narrowing of
popular habitats.
3.3. Consequences of forest damage to
anurans
3.3.1. Increased warming - changes in
the quality of microhabitats
As a consequence of foliage loss due
to acid rain, more radiation will reach the
forest floor. Increased amounts of sunlight
can lead to an increased surface
temperature, and thus to a higher water
vapour pressure deficit. Consequently,
the evaporation of the surface waters can
increase (Varga 2005). This can lead to
the drying out of small ponds and wet
surfaces in the area. Small puddles as well
as bigger water bodies are important
reproduction sites for anurans as they use
these surface waters to lay their ova
(O’Shea & Halliday 2001). As an
amplifying factor, wind speeds within
forests can increase and thus maintain a
higher evaporation demand. As the
surface waters evaporate, nutrient
availability increases that can result in
51
eutrophication that can change vegetation
composition (Loch 1999). The main
impact of the appearance of sylvan
stagnant water bodies is the loss of the
reproduction sites and the essential
aquatic habitats for anurans.
It is also possible that because of
warmer temperatures and the increased
evaporation the sensitive outer layer of
anurans can desiccate more easily. As
forests lose their canopy and plants lose
their foliage, shaded hiding places are
reduced. The distances to the nearest
water body grows so anurans need to
consume more resources for movement
and moving exposes them further to many
other threats. Movement during the
reproductive periods reduces the fitness of
anurans that can result in reproductive
disturbance and decreased number of
descendants (Bihari 2002).
3.3.2. Balks in the food chain
During the larval stages, anuran larvae
consume algae and other aquatic vegetal
substrates. They also consume mud,
seaweeds and numerous small animals
like worms and little crawfish. Therefore,
shrinkage of sylvan waters endangers the
food
source
of
juveniles.
The
characteristic food composition for adults
is mainly composed of insects and other
arthropods, snails and worms. Fortunately
in most anurans species full-grown
animals can consume every kind of prey
animal within a particular size range and
can, therefore, tolerate an alteration in the
potential food composition (Soós w.y.).
However due to the altered circumstances
the composition of the superior predator
species can also suffer changes. Superior
predators that are uncommon in a certain
52
area can arrive and potentially negatively
affect anuran populations.
As anurans are in the middle of the
sylvan food chain as primary predators,
changes in their number affects the other
levels as well (Moser & Pálmai 1992).
With the decrease of anurans, number of
pests can increase, while changes in the
number of the higher level predators can
also occur.
3.3.3. Increased ultraviolet radiation
input
The interaction between acidification
and ultraviolet radiation may be highly
population specific these stressors can act
in a synergistic fashion (Räsänen, K
2002).
The ultraviolet radiation reaching the
earth’s atmosphere has been classified in
three categories of wavelengths; UV-A
(320--400 nm), UV-B (280--320 nm) and
UV-C (less than 280 nm). UV-A is
beneficial to the earth’s environment and
living organisms whilst UV-C is absorbed
by the earth’s atmosphere. UV-B is
proven to have harmful effects on both
plants and animals (Breuer 1993).
According to Pahkala et al. (2001)
UV-B is likely to have negative effects on
the development of anuran embryos,
either in terms of survival or early growth
performance. However, the reaction of the
differs between anuran species. Unlike
many other studies (Anzalone et al. 1998,
Blaustein et al. 1998, Corn 1998, Lizana
& Pedraza 1998). Pahkala et al. (2001)
showed that neither UV-B treatment nor
UV-B in combination of low pH had a
significant effect on moor frog (Rana.
arvalis)
embryos.
One
possible
explanation for this discrepancy could be
the observation that activity of the
Zs. Antal, P. Puttonen
photolyase enzyme (involved in the
removal of UV-B radiation-induced
DNA-damaging photoproducts from
cells) is known to differ between the
different species (Pahkala et al. 2001).
Several studies (Blaustein et al. 1994,
1996, 1999, Van de Mortel et al. 1998)
have found that species with high
photolyase activity are more resistant to
UV-B radiation than species with low
photolyase activity. The more resistant
species include several ranids, and it is
possible that R. arvalis also belongs to
this resistant group of species.
Notwithstanding the fact that some
anuran species are more resistant to UV-B
radiation than others, UV-B radiation has
harmful effects on anurans. It has been
proven that ultraviolet radiation possesses
mutagenic features (Berend et al. 1999).
Besides all mentioned effects, UV-B
radiation can degrade the immune system.
Organisms that are injured or are under
stress, are more easily affected (Kosik
2004a).
3.3.4. Difficulties in winter survival
Several methods of winter survival are
known within vertebrates including;
winter migration to areas with more
favourable conditions, quiescence and
suspended animation. Amphibians, as
poikilothermic animals, apply the method
of suspended animation. Suspended
animation is common not only among
amphibians but among other animals
including some mammal species (Kosik
2004b). How amphibians and thus
anurans act during this process, is again a
unique feature.
Amphibians burrow into the ground
for the winter. Whilst some species
choose the mud layer of aquatic habitats,
The effects of acid rain on anurans and the possibilities of protection in Hungary…
most of them prefer terrestrial habitats for
wintering. With the temperature decline,
the amphibian’s body temperature
decreases to a point a few degrees above
freezing. To prevent the body from
freezing, amphibians need to hide into
deeper layers of the soil, where the
environmental temperature is above zero
during the whole winter season. The
average digging depth of anurans is only
3 cm, but there are reports on 20--30,
even 40 cm digging depths (Mazál 1997).
After choosing a wintering place, the
body temperature of the wintering animal
oscillates; it cools down then rises to the
normal level several times. Finally, the
body temperature decreases to 2--4 °C,
the heartbeat declines to 10 %, and
oxygen utilisation declines to only 2 % of
the normal. These alterations bring about
hibernation, and the procedure of the
suspended animation of the animal starts
(Kosik 2004b).
As prebventing the body t from
freezing throughout the winter is crucial
for the anurans hibernating in terrestrial
habitats, they prefer soil of the deciduous
forests rather than of conifers. The reason
of this preference is twofold. First, there
is the significant thermal effect of dead
fallen leaves that are larger than that of
coniferous needles. Second, anurans
require neutral or mildly alkaline soil
conditions for the wintering as the skin
glandules produce an alkaline mucus to
keep the outer layer of the body moist.
Under acid conditions, such as in the soil
of coniferous forests, functioning of the
skin glandules can be impaired result in
decreased mucus excretion (Mazál 1997).
Reduced leaf litter on forest floors, as
a result of acid rain, has two
consequences: reduced thermal cover and
53
diminished temperatures on the forest
floor. The increased acidity of the soils is
a problem itself for anurans, since pH has
been shown to play a significant role in
influencing the spatial structuring of
herpetofauna (Chambers et al. 2006). Soil
acidity has a negative impact on the
distribution of terrestrial amphibians
(Wyman & Hawksley-Lescault 1987). If
the normal functioning of the skin
glandules is impeded, the winter survival
of anurans could become uncertain
(Mazál 1997). However, the pH tolerance
of anuran species may vary (Pahkala et al.
2001).
4. Changes in Hungarian forest
structure
4.1.
Ecosystem
sensitivity
to
acidification in Hungary
The sensitivity to acid deposition
varies largely between different areas
(The Swedish NGO Secretariat on Acid
Rain 2005). Problems arise, sooner or
later, in situations where acid deposition
exceeds the buffering capacity of the soil.
Exceedance is a variable that describes
the difference between the mean annual
acid deposition and critical load (The
Green Lane, the official World Wide Web
site of Environment Canada 2002).
Critical load is an estimate of how much
pollution an ecosystem can tolerate.
Critical loads are classified into 6
categories according to the sensitivity of
the different areas. Categories are given in
acid equivalents per hectare per year.
Sensitive ecosystems possess 200 or less
acid equivalents per hectare per year,
while least sensitive ecosystems can
54
tolerate more than 1500 (The Swedish
NGO Secretariat on Acid Rain 2005).
Fig. 2 shows the ecosystem sensitivity
for acidification in Hungary. Hungary has
a medium sensitivity for acidification.
The most sensitive areas are located at the
Zs. Antal, P. Puttonen
northern part of the country while the
biggest part of the country is less
sensitive. Importantly however, the
largest part of the forested areas is in the
more sensitive regions for acid deposition
in Hungary.
Figure 2. Ecosystem sensitivity to
acidification in Hungary. Data are given in acid
equivalents per hectare per year according to
the critical loads. By the classification of
critical loads Hungary has a medium sensitivity
for acidification. The most sensitive areas are
located at the northern part of the country and
however the largest part of the country is less
sensitive. Forested areas are mostly in the more
sensitive regions for acid deposition in
Hungary.
4.2. The rate of forested area and the
trend of the changing figures in Hungary
About 20 %, 17 750 km2, of the total
area Hungary of is forested (93 030 km2;
Központi Statisztikai Hivatal 2003). The
reasons for this low rate are not only
inadequate forest management methods or
nature conservation, but are rooted in
complex causes such as accession of
cultivated agricultural areas at the
expense of forests and demand for timber
and destructive effects of the wars in the
course of history (Solymos et al. 2001.)
Changes ofthe forested area in Hungary
are shown on Fig. 3.
Protection of sylvan fauna and flora
would require improvement of forest
health and also increase in forested area in
Hungary to provide needed habitats.
Fortunately the forested area has
increased by 120 km2 since 1990
(Központi Statisztikai Hivatal 1994), by
The effects of acid rain on anurans and the possibilities of protection in Hungary…
reforestation and afforestation, however
re- and afforestation are primarily
concerned with economic benefits and
less with ecological aspects. Forest
55
plantations are dominated by exotic tree
species (Németh & Némethné-Katona
1997).
Figure 3. Changes in the forested area of Hungary from historic times to the present day
(Solymos et al. 2001). In the course of history the rate of forested area decreased for different
reasons. From the middle of the last century there is an increase. However re- and afforestation is
primarily aimed at economic benefits, thus natural forests have been replaced by exotic tree
species in forest plantations.
5. Conclusions and
recommendations
According to Puky (2000), there are
several endangering factors for anurans
worldwide, the lack of knowledge seems
to be the most important of all harmful
affects. Information deficiency is greater
in Hungary than the European average,
thus the effective protection of the
different anuran species is very difficult
even in nature conservation areas. One
solution for this problem would be to
carry out base surveys to collect raw data
and also to conduct nature conservation
research, like monitoring surveys,
according to current requirements.
However, there are only a few
available field studies on the effects of
acid rain on anurans and moreover, the
evaluation of the status of aquatic and
terrestrial habitats is also lacking. In
contrast there are published experimental
data regarding the negative effects of acid
rain on some anuran species. Acid rain
can cause harms to amphibians both
directly and indirectly. Forests serve as
habitat for several anuran species where
these animals feed, reproduce, hide and
over-winter. A link between anuran
Zs. Antal, P. Puttonen
56
protection and the overall aims of nature
conservation are evident. According to
FAO State of the world’s forests (2003),
sustainable use of forests is an essential
part of conservation, and vice versa.
Equitable distribution of the benefits is
necessary to achieve both. It follows that
the conservation of biological diversity is
an integral component of sustainable
forest management.
In setting up a comprehensive forest
management system, the establishment of
adequate criteria and indicators to guide
management practices is a basic
requirement. It would be advisable to
work out a broad monitoring system that
should focus on the observation of the
effects of management acts on the state of
all sylvan ecosystems of Hungary.
The natural and near-natural forests,
that provide habitats for the anuran
species in Hungary, are essential and
therefore, an increased protection of these
woods is needed.
Restoration of habitats that already
have started to degrade and consequently
decline, and those that are threatened is
required (Camargo et al. 2002, George &
Zack 2001, Huxel. & Hastings 1999).
Reforestation and afforestation are
important for ensuring a more extensive
protection of anuran species in Hungary.
However reforestation and afforestation
should be carried out using tree species
that would develop the characteristics and
structures of natural woody associations.
Exotic species should be avoided and
used only after thorough deliberation to
achieve benefits without causing harms to
the environment.
Because of negative effects of habitat
losses and fragmentation on the landscape
level forest ecosystems, conservation and
restoration of large, continuous forest
habitats is needed. Rebuilding of the
connectivity between already fragmented
habitats by reforestation is an important
start. The protection of forest edges
against structural damage, damage by fire
and colonisation of exotic species are
further
methods
for
decreasing
fragmentation. The protection of forest
edges is possible by diversifying and
promoting less intensive types of land
use, managing the use of fire, minimising
the application of toxic chemicals and
controlling the introduction of plant
species from outside the forest area (FAO
State of the world’s forests 2003).
Whilst realising that in a long-term,
sustainable forest management is able to
produce timber and marketable nontimber forest products with an economical
value,
launching
natural
forest
management,
that
considers
the
maintenance of biodiversity as important
as the earliest possible financial benefit,
would serve as the basis for anuran
protection in Hungary.
Acknowledgements.
We would like to express our thanks to Prof. Dr.
Károly Mészáros head of the Institute of Forest
Assets Management at the University of West
Hungary, Faculty of Forestry; for submitting the
study “State and possibility of afforestation”, and
giving his consent to use the graph included in the
4.2 part of the study. We would also like to thank
János Antal for creating the figures that are included
in this article and Tibor Hartel for reviewing the
article.
References
Anzalone, C. R., Kats, L. B. and Gordon, M. (1998):
Effects of solar UV-B radiation on embryonic
development in Hyla cadaverina, Hyla regilla,
The effects of acid rain on anurans and the possibilities of protection in Hungary…
and Taricha torosa. Conservation Biology 12:
646-653.
ApSimon, H., Pearce, D. and Özdemiroglu, E. (eds.)
(1997): Acid rain in Europe Counting the cost.Earthscan Publications Ltd., London.
Baum, E. (2001): Unfinished business: Why the acid
rain
problem
is
not
solved.
http://cta.policy.net/relatives/18480.pdf.Accessed: 28.05.2006
Beebee, T. J. C. and Griffiths, R. A. (2005): The
amphibian decline crisis: a watershed for
conservation biology? Biological Conservation
125: 271-285.
Berend, M. (1999): Spontán és indukált mutációk.In: Berend, M., Gömöry, A., Kiss, J., Müllner E.
& Tóth, G., Biológia III.: 589-591. Akadémiai
Kiadó, Budapest.
Bihari, Z. (2002): Etológia. Debreceni Egyetem
Agrártudományi
Centrum
Mezőgazdaságtudományi Kar, Debrecen.
Blaustein, A.R., Hoffman, P.D., Hokit, D.G.,
Kiesecker, J.M., Walls, S.C. and Hays, J.B.
(1994): UV repair and resistance to solar UV-B
in amphibian eggs: a link to population
declines? Proceedings of the National Academy
of Sciences, USA 92: 1791-1795.
Blaustein A. R., Hoffman, P. D., Kiesecker, J. M.
and Hays, J.B. (1996): DNA repair activity and
resistance to solar UV-B radiation in eggs of the
red-legged anuran Rana aurora. Conservation
Biology 10: 1398-1402.
Blaustein, A. R., Kiesecker, J. M., Chivers, D. P.,
Hokit, D. G., Marco, A., Belden, L. K. and
Hatch, A. (1998): Effects of ultraviolet radiation
on amphibians: field experiments. American
Zoologist 38: 799-812.
Blaustein, A. R., Hays, J. B., Hoffman, P. D.,
Chivers, D. P., Kiesecker, J. M., Leonard, W.
P., Marco, A., Olson, D. H., Reaser, J. K. and
Anthony, R.G. (1999): DNA repair and
resistance to UV-B radiation in western spotted
anurans. Ecological Applications 9: 1100-1105.
Blaustein, A. R. and Kiesecker, J. M. (2002):
Complexity in conservation: lessons from the
global decline of amphibian populations.
Ecology letters 5: 597-608.
Breuer, H. (1993): SH atlasz Fizika. Springer
Hungarica Kiadó Kft., Budapest.
Camargo, J. L. C., Ferraz, I. D. K. and Imakawa, A.
M. (2002): Rehabilitation of degraded areas of
Central Amazonia using direct sowing of forest
tree seeds. Restoration Ecology 10 (4): 636-644.
57
Chambers, J., Wilson, J.C. and Williamson, A.
(2006): Soil pH influences embryonic survival
in
Pseudophryne
bibronii
(Anura:
Myobatrachidae). Austral Ecology 31: 68-75.
Clarke, B. (1993): A kétéltűek törzsfejlődése és
rendszerezése. In: Veress, I. (ed.), Guiness
Enciklopédia Az élőhely: 78. Pannon
Könyvkiadó, Budapest.
Corn, P. S. (1998): Effects of ultraviolet radiation on
Boreal toads in Colorado. Ecological
Applications 8: 18-26.
Food and Agricultural Organization of the United
Nations (2003): How sustainable use of forests
can contribute to conserving biological
diversity. In: FAO 2003. State of the world’s
forests: 8-95. FAO, Rome.
George, T. L. and Zack, S. (2001): Spatial and
temporal considerations in restoring habitat for
wildlife. Restoration Ecology 9 (3): 27-279.
Glos, J., Grafe, U., Rödel M-O. and Linsenmair K.
E. (2003): Geographic variation in pH tolerance
of two populations of the European common
frog, Rana temporaria. Copeia 3: 650-656.
Green, D. M. (1999): How do amphibians go
extinct? Proc. Biology and Management of
Species and Habitats at Risk, Kamloops, B. C.,
15-19 Feb. 1999.
Hartel, T. (2001): A kétéltűek pusztulása: pár újabb
hipotézis összegzése. ACTA Hargitensia 8: 121126.
Huxel, G. R. and Hastings, A. (1999): Habitat loss,
fragmentation, and restoration. Restoration
Ecology 7.3: 30-315.
Kiesecker, J. M. (2002): Synergism between
trematode infection and pesticide exposure: A
link to amphibian limb deformities in nature?
Proceedings of the National Academy of
Sciences 99: 9900-9904.
Kiss, I. (2003): Kétéltűek (Amphibia). In: Bakonyi,
G. (ed.), Állattan: 409-424. Mezőgazda Kiadó,
Budapest.
Kosik, I. (ed.) (2004a): A kétéltűek egyetlen élete.
Sulinet.http://www.sulinet.hu/tart/ncikk/jd/0/11
866/keteltuek.htm. Accessed: 28.05.2006
Kosik, I. (ed.) (2004b): Hibernáció. Sulinet.
http://www.sulinet.hu/tart/ncikk/aa/0/5238/start.
htm. Accessed: 28.05.2006
Lizana, M. and Pedraza, E. M. (1998): The effects of
UV-B radiation on toad mortality in
mountainous
areas
of
central
Spain.
Conservation Biology 12: 703-707.
58
Loch, J. (1999): Agrokémia. Debreceni Egyetem
Agrártudományi
Centrum
Mezőgazdaságtudományi Kar, Debrecen.
Mazál, I. (1997): Kétéltűek (Amphibia) és hüllők
(Reptilia) vonulás- és telelésvizsgálata a Fertőtó partján. Technical College Thesis. Roth
Gyula Erdészeti és Faipari Szakközépiskola,
Sopron.
Moore, P. (1994): Környezetszennyezés: a savas
eső. In: Pécsi, T. (ed.), Az élővilág atlasza: 164165. Geoholding Rt. SKO Lap- és Könyvkiadó,
Szlovákia.
Moser, M. and Pálmai, Gy. (1992): A környezetvédelem alapjai. Nemzeti Tankönyvkiadó,
Budapest.
Németh, I. and Némethné Katona, J. (1997): Zöld
kalandra fel! Környezetvédelemről túrázóknak –
túristaságról környezetvédőknek I. Havasi
Rózsa Kft., Budapest.
Ormódi, B.: (1999). A fenyők védelme – Savas eső,
haldokló fák. Démász Híradó. 23.12.
http://www.demasz.hu/hirado/html/199912/sava
seso.shtml. Accessed: 28.05.2006
O’Shea, M. and Halliday, T. (2001): Határozó
kézikönyvek Hüllők és kétéltűek.-Panamex Kft.,
Budapest.
Packham, J. R., Harding, D. J. L., Hilton, G. M. and
Stuttard, A. (1992): Functional ecology of
woodlands and forests. Chapman & Hall,
London.
Pahkala, M., Laurila, A., Björn, L. O. and Merilä, J.
(2001): Effects of ultraviolet-B radiation and pH
on early development of the moor anuran Rana
arvalis. Journal of Applied Ecology 38: 628636.
Pahkala, M., Räsänen, K., Laurila, A., Johanson, U.,
Björn, L. O. and Merilä, J. (2002): Lethal and
sublethal effects of UV-B/pH synergism on
common frog embryos. Conservation biology
16 (4): 1063-1073.
Puky, M. (2000): A kétéltűek védelme
Magyarországon. In: Faragó, S. (ed.), Gerinces
állatfajok
védelme:
143-158.
NyugatMagyarországi Egyetem Erdőmérnöki Kar,
Sopron.
Räsänen, K. (2002): Evolutionary implications of
acidification: a frog’s eye view. Acta
Universitatis
Upsaliensis,
Comprehensive
Zs. Antal, P. Puttonen
Summaries of Uppsala Dissertations from the
Faculty of Science and Technology 764.
Uppsala. 32 pp.
Räsänen, K., Laurila, A. and Merilä, J. (2002):
Carry-over effects of embryonic acid conditions
on development and growth of Rana temporaria
tadpoles. Freshwater biology 47: 19-30.
Solymos, R., Mátyás, Cs., Mészáros, K., Faragó, S.,
Holdamf, Gy., Csóka, P., Gémesi, J. and
Telegdi, P. (2001): Az erdőtelepítés helyzete és
lehetőségei. Nyugat-Magyarországi Egyetem,
Erdőmérnöki Kar Erdővagyon-Gazdálkodási
Intézet. Sopron. 11-12.
Soós, L. (ed.) (w.y.): Brehm Az állatok világa 12.
Hüllők és kétéltűek. Gutenberg Könyvkiadóvállalat, Budapest.
The Green Lane. The official World Wide Web site
of Environment Canada (2002): Adequacy of
existing programmes. http://www.ec.gc.ca/
acidrain/acidr/acidr_s3_e.htm. Accessed: 28.05.
2006
The Swedish NGO Secretariat on Acid Rain (2005):
Acidification.
http://www.acidrain.org/pages/
acidEutrophications/sub3_1.asp. Accessed: 28.
05.2006
Van de Mortel, T., Butterman, W., Hoffman, P. D.,
Hays, J. B. and Blaustein, A.R. (1998): A
comparison of photolyase activity in three
Australian tree anurans. Oecologia 115: 366369.
Varga, B. (2005): A Balaton és a Keszthelyi-öböl
párolgásés
egyszerű
vízmérleg
meghatározásának meteorológiai vonatkozásai.
University
thesis.
Veszprémi
Egyetem
Georgikon
Mezőgazdaságtudományi
Kar,
Keszthely.
Wyman, R. L. and Hawskley-Lescault, D. S. (1987):
Soil acidity affects distribution, behaviour, and
physiology of the salamander Plethodon
cinereus. Ecology 68 (6): 1819-1827.
Submitted: 23 May 2006 / Accepted: 17 June 2006
Corresponding Editor: T. Hartel
English Language Editor: A.P. Pernetta