Interacting Stressors in Anuran Ecology
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8/6/2019 Interacting Stressors in Anuran Ecology
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Stressors in Anuran ecology
Due to the large differences between the different ordersof amphibians such as niche differences, trophic level andhabitat differences at certain stages in the life cycle, lifehistory differences etc., this review will focus upon the
largest and most diverse order of amphibians, theanurans. The global amphibian decline is not a single event
with a single cause. Rather it is a number of declining populations with a number of individual factors orstressors caused by an accumulated deterioration inhabitat quality[9]. Therefore, in order to understanddecline at the global scale, it is necessary to study anuransat the individual or population levels and it is at theindividual level that the majority of research to date hasfocused. Anuran fitness is ultimately measured by survivalof individuals. In particular, the majority of studies havefocused upon tadpole survival. This is because tadpolesare limited in their potential to avoid ecological stressorsdue to the relatively restricted, homogeneous nature of their environment. In contrast, the adult phase of theanurans is specialised for dispersal, as well asreproduction[10] and so has a greater ability to avoidunfavourable environmental conditions. It is the lack of dispersal ability of the tadpoles that increases their
vulnerability to environmental stressors, thus making thetadpoles the focus for the majority of research.
Additionally, because tadpoles are confined to specificenvironments, i.e. water bodies, they are easier to locateand study compared with the adults.
There are three main categories for the stressorsimportant in anuran ecology; environmental, chemical and
biological. In the following paragraphs the stressors ineach category will be presented. The categorising of stressors here is for organisational purposes only and notintended to represent differences in level of threat orenvironmental ubiquity. Furthermore, many stressorscould be argued as belonging to multiple categories; forexample, nitrogen pollution may be either chemical (as itis here) due to its use in fertilisers, or biological wastefrom manure. Again, it is the stressor itself which isimportant, not how it has been categorised.
Environmental stressors
Environmental stressors primarily relate to climate changeand global warming. The effects of global climate changeare found across all environments, and freshwater is nodifferent. The two key aspects of climate change as they relate to anuran ecology are temperature, and rainfall.
Temperature changes affect anuran larvae in severaldifferent ways. Firstly, the emergence from hibernation of adults, and subsequent breeding, is correlated withtemperature in some species such as the Natterjack toad,Epidalea calamita , (Beebee, 1995 in [11])but not all [12].
When this phonological change does occur, it may havelimited effect on direct factors such as predation becausemany predators, like odonates for example, also alter
phenology in response to warming[13]. However, inaddition to potential earlier spawning, increased watertemperatures have been shown to increase the rate of
development of tadpoles[14] due to an increase inmetabolic rate ([15]; Rome et al. 1992 in [16]). Thecombined result of earlier spawning, and fasterdevelopment is an earlier emergence from the aquaticstage of the anuran life history and into the adult phase.
This earlier emergence in turn allows for more growth of
the post-metamorphic individuals and therefore allowsindividuals to reach a greater size prior to hibernation,thus increasing probability of surviving their first
winter[14].However, despite warmer springs on average, the
young of earlier spawning anurans will be exposed tomore individual days where the ground temperature dropsbelow 1.5°C, a condition which is positively correlated
with tadpole mortality[14]. Additionally, these studies have been conducted using
temperate species where spring warming is an importantindicator to breed. For many species of tropicalamphibians, the temperature of their natural environmentdoes not fluctuate a great deal around the average and sothese species are less likely to alter phenology in responseto global warming and may well be adversely affected by the divergence from their optimal temperature ranges. Nostudies as of yet, have quantified any significant differencein individual survival probability or of population growthrate as a result of global warming.
The Intergovernmental Panel on Climate Change(IPCC) predicts a change to the global rainfall regime
which can have multiple different affects for amphibiansaround the world. In temperate regions where annualrainfall is increasing, the result is to effectively decrease
water temperatures[14], causing the associated slowerdevelopment, reduced survival etc. Other areas of the
world such as central United States will experience areduction in annual rainfall and an increase in droughtevents[17]. This reduction is likely to result in a lower
water level for breeding ponds and a reduction inhydroperiod for ephemeral ponds used by many species.Reduced hydroperiod poses a great potential threat foramphibians. If the breeding pond dries before thetadpoles metamorphose, larvae desiccate and die[18].Studies have shown that amphibians show a degree of plasticity in timing of metamorphosis, and will increaserate of development in response to pond drying [10, 19].
The reduction in development time produces smallermetamorphosed individuals than those with „normal‟
development times. The smaller individuals have theassociated reduction in survival probability commonacross amphibians[10]. Interestingly, the earliermetamorphic individuals are even smaller than would beexpected purely by reduced development time, suggesting an additional cost to this phenotypic plasticity[19].
The second affect of reduced rainfall; lower waterlevels, has two different implications. Firstly, thedecreased water volume will increase the density of tadpoles, thus decreasing food availability and increasing density dependent effects and reducing overallpopulations. The second effect is in increasing exposureto harmful ultraviolet B radiation (UV-B).
UV-B radiation is another environmental stressor inanuran larval development. UV-B is filtered by plants and
water, therefore in shallow ponds or particularly in
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nutrient poor shallow mountain streams which do notsupport much plant growth; eggs and tadpoles can beexposed to rather high levels of UV-B radiation.Exposure to ambient UV radiation has been shown toresult in embryo malformations leading to direct mortality of the embryo, or latent mortality caused by reduced
competitive ability of the deformed tadpoles or adults[20]. The tadpoles and adults of many species do exhibit UV avoidance behaviour[21] which is why embryos areespecially susceptible; but in very shallow waters it is oftennot possible for tadpoles to avoid the harmful radiation.In addition to developmental deformities, UV exposurealters the metabolic rate of tadpoles potentially reducing developmental and survival rates [22], cf. [23]. As hasalready been seen, reduction in rate of developmentincreases risk of desiccation in a drying pool, especially
where the breeding pool is already shallow water, as wellas increasing the likelihood of exposure to other stressors.
Chemical stressors
Many chemical contaminants in freshwater habitats are asa result of intensive farming practices. Primarily, theseconsist of organic phosphorous and nitrogen fromfertilisers, or chemical agents such as herbicides andpesticides.
Phosphate contamination does not have any directimpact on survival, growth or development of tadpoles[24]. One impact phosphate pollution does have,is promoting algal blooms leading to eutrophication, theeffects of which are described later under the „biologicalstressors‟ section. Nitrates, in contrast are highly toxic tomany species of amphibian [25], 25] resulting in reduced
survival, weight loss, slower development anddevelopmental abnormalities. Nitrates also affect otherorganisms in the ecological system including theinvertebrate prey of adult frogs, or predatory fish.Evidence suggests that adults of these species are, ingeneral, less susceptible than many amphibians[26],however, eggs and young may be much more sensitive tonitrogen pollution[27]. Therefore over time thepopulation effects on the different species may balanceout, resulting in whole community losses.
Herbicides and pesticides can be very detrimental toamphibian populations. Two in particular have beenidentified as causes for population declines; the herbicide
atrazine, and the insecticide malathion. Atrazine is themost commonly used herbicide, and second mostcommonly used pesticide in the world[28],[29]. Thischemical stressor rarely has direct lethal effects onamphibians, but the latent effects may be just asdangerous for anuran individuals as any direct mortality.In a recent qualitative meta-analysis, Rohr and McCoy (2010) identified several consistent effects of atrazine onamphibian individuals including reduced size atmetamorphosis, reduced antipredator behaviours,increased susceptibility to disease and infection throughreduced immune function, and altered gonadaldevelopment and function[29]. Additionally, other studies
have shown ecologically relevant doses of atrazine toreduce male testosterone levels equivalent to those of females and produced demasculinized, hermaphroditic
males[28]. Amphibians are especially prone to the effectof atrazine during the larval stage; unfortunately breeding usually coincides with the spring application of thisherbicide, making it a serious potential[28].
Malathion is also linked to developmentalmalformations in amphibians, but in this case it is
primarily in the form of limb deformities. Studies haveshown an increase in malformations by 10% whenembryos have been exposed to malathion[30]. Themalformations both reduce competitive ability of thefrogs, but all increase predation risk. As well as the directeffects, the malathion exposure causes a latentsusceptibility to infection by parasitic Echinostoma trematodes, this is likely due to a poorly developedimmune system[31].
Biological stressors
Biological stressors in this system are far more diverse.Predator presence, parasites and eutrophication are themain biological influences in anuran survival, and all areclosely linked with each other.
As previously mentioned, agricultural runoff causing alarge input of organic phosphates into ponds and streamsetc. promotes algal growth, resulting in algal blooms. Thiseutrophication has several effects summarised in Box 1.
The effects of eutrophication have various impacts uponanuran ecology. Firstly, tadpoles are hypoxic tolerant,adapting their behaviour to compensate for low oxygenenvironments[32], whereas predatory fish are less capableof acclimating to the low oxygen environment[2]. Theincreased periphyton biomass in eutrophic conditionsboth provides more food for the tadpoles, but also for the
snails. This results in a community shift toward larger,more competitive Planorbella snail species. ThesePlanorbella snails are the first intermediate hosts for aparasitic trematode, Ribeiroia sp.[33]. The impact of thisincrease in parasite presence is discussed in more detailbelow.
One study[34] has shown reduced survival, growth,development and immunocompetence of Scinax nasicus tadpoles after only 7 days exposure to ponds showing eutrophication. However, the primary negative agent inthis study was likely to be the presence of pesticides in thesystem. Unfortunately, the experimental design in thiscase did not allow for the disambiguation of the results.
Being specialised for growth, tadpoles are highly efficient at converting periphyton to body mass, thusmaking anuran tadpoles an important prey source formany predatory species in the freshwater ecosystem. Fish,dragonfly larvae, other amphibians such as newts,salamander larvae or even larger tadpoles, are allimportant predators and as such complex predatoravoidance behaviours have evolved in many species.
Using chemical, visual and/or physical cues of predator presence[35] tadpoles will mediate their activity and position in the pond in response: For example,avoiding open water when fish chemical cues are present[35]. Reducing activity to avoid predation also means
reducing feeding rates, thus there is a close trade-off between growth rate and predation risk[36], [37].
Additional consideration occurs in hypoxic conditions.
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Normally tadpoles will come to the surface to breath fromthe air if dissolved oxygen is low, however if predatory salamanders were present then tadpoles reduced this
behaviour because under hypoxic conditions, salamandersmust also remain near the surface. As a result, individualsurvival increased under hypoxia due to the behaviouralplasticity of anuran larvae causing a reduction inpredation[38].
Parasites are another important biological stressor inanuran ecology. Although parasites have always beenpresent in the environment, parasite infection has beenidentified as the leading cause for recent increases inprevalence of amphibian limb deformities[39]. Moreprecisely, it is the interaction between parasites and theeffects of agricultural run-off. As previously described,eutrophication of water sources alters the composition of
the snail community, increasing populations of the firstintermediate hosts for Ribeiroia [33], and exposure to thepesticide malathion reduces immunocompetence allowing for greater infection rates of[31]. The life cycle of a typicalRibeiroia trematode is explained in Box 2. Most trematodeshave similar complex life cycles but may differ inencystment site, thus not all trematodes induce limbdeformities, but most will reduce body mass andcompetitive ability.
Further complexity is added to the interactionsbetween pesticide, parasite, and frog, when the free living stage in the parasites life cycle is considered. The cercariaeare also exposed to contaminants in the water, and it hasbeen shown that exposure to atrazine can reduce activity and increase mortality of free living cercariae decreasing infection levels in larval amphibians[40]. Pesticideconcentrations in pools are highly variable with a suddenpulse immediately after field application or a rain shower,followed by lower concentrations as the chemicalsdegrade[41]. Therefore, the relative effects of atrazine onparasite and frog may differ from year to year. This meansthat the level of parasite infection, and thus amphibiandeformities, changes from between years and is difficultto predict due to the interactions of timing in breeding,release of cercariae, application of pesticides to crops andrainfall patterns.
Finally, emerging infectious disease has been a
popularised cause for widespread amphibian declines.Primarily, the fungal disease chytridiomycosis, caused by
the chytrid fungus Batrachochytrium dendrobatidis (Bd), hasbeen identified as causing declines and extinctions of species around the world[42]. This disease is highly
virulent and is particularly dangerous for isolatedpopulations or species with small distributional ranges,due to the lack of re-colonisation possibility post-infection[43]. A recent review by Kilpatrick andcolleagues provides a complete report on the ecology andthe impact of Bd on host populations and identifies futureresearch needs in order to answer important questions.
These include the origin of Bd, variation in thetransmission and impact of Bd, and how host andenvironmental factors interact to affect impact,persistence and evolution of the disease. Despite thedevastating nature of this disease, there is some evidenceof populations persisting and even recovering after
infection, sometimes with low levels of infection,suggesting an evolving immunity to Bd infection[44].
Interacting stressors
In 2008, the Freshwater Biological Association (FBA)launched a series of „FBA Conferences in Aquatic biology‟in order to tackle, and promote key issues in the field of research. The first of these conferences was entitled„Multiple Stressors in Freshwater Ecosystems‟[45].Reporting on the conclusions of this conference in arecent special issue of the journal Freshwater Biology,Ormerod and colleagues highlighted the diversity of
multiple stressor problems in freshwater ecosystems andemphasised the need for more research into tackling theseproblems. It is with this incentive that this review now attempts to develop a model for analysing multiplestressor effects in anuran ecology.
From the above evidence it can be clearly seen thatthere is a great number and diversity of factors affecting larval survival in the anurans. However, it is misleading tosuggest that all of these stressors affect all anuran species,or even affect different species in the same way. Forexample, the presence of fish along the freshwatergradient between ephemeral and permanent ponds[46]can have highly significant effects upon larval survival,
which may differ greatly between species.
Box 1. The process and effects of eutrophication
Cultural eutrophication is caused by the addition of nutrients into the aquatic environment. As with nutrient input in
terrestrial environments, the fastest growing species benefit the most from nutrient input. Therefore there is a rapid
proliferation of bacteria, periphyton and phytoplankton, therefore resulting in a general increase in biomass. Blue-green
bacteria (cyanobacteria) are particularly responsive to nutrient inputs and thus the general algal composition shifts. The
increased algal concentration increases turbidity of the water body. As there is an increase in photosynthetic matter,during the daytime dissolved oxygen levels are higher than average, however during the night when photosynthesis does
not occur, the increased level of respiration can lead to intensely anoxic conditions. Furthermore, a rapid build-up of
sedimentary material and the intense respiration associated with the degradation of this material, results in constant
anoxic conditions at the pond bottom.
Reference
Smith, V.H., Tilman, G.D., et al . 1999. Eutrophication: impacts of excess nutrient inputs on freshwater, marine, and terrestrialecosystems. Environ. Pollut. 100: 179-196.
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Disparity between species responses was shown by Smith et al. (1999)[2] who experimentally manipulated
concentrations of the predatory Bluegill sunfish ( Lepomis macrochirus ) and measured the response of two anuranspecies, the gray treefrog ( Hyla versicolor) and the bullfrog ( Rana catesbeiana) and one caudate, a red-spotted newt( Notophthalmus viridescens ). L. Macrochirus predates heavily on H. versicolor tadpoles, but avoids the toxic larvae of R.catesbeiana. However, L. macrochirus also feeds on dragonfly larvae, these predaceous invertebrates are not affected by the toxicity of the bullfrog tadpoles, and feed heavily upon them. H. versicolor is less prone to predation by odonate larvae. Smith‟s experiment effectively highlightsthe differences in species responses to stressors:Exclusion of H. versicolor from ponds containing theBluegill sunfish is due to direct predation, whereas theincrease in R. catesbeiana densities is indirect, via areduction in predatory invertebrates[2]. N. viridescens were
not prone to predation by either fish or invertebrates;however, presence of the newt was negatively correlated
with presence of L.macrochirus . Smith and colleaguesconclude this to be a result of N.viridescens adults being outcompeted for their primary food source, cladoceranssuch as Daphnia sp[2].
In the above example community, predationdrastically affected probability of survival for individuals. At the population scale, however, the effect of predationis mediated greatly by behavioural changes, altering species distributions between ponds of varying permanence, therefore varying predator distribution[47].Presence of the fish in the breeding ponds altered theoviposition behaviour of adult females resulting insignificant differences in choice of oviposition site.Female H. versicolor preferentially deposited eggs in ponds
without L. macrochirus , with the converse being true for R.Catesbeiana, thus avoiding their respective predators.
In addition to illustrating the differences in speciesresponses, the above example highlights the differentmechanisms via which stressors affect individual survival.Predatory fish reduce survival of one species throughdirect predation, but indirectly increase survival of another through reducing densities of a secondary groupof predators, odonates in this case.
Producing a model
Having reviewed the factors affecting anuran larvalsurvival and considered the interactions between thesefactors, it has become apparent that as well as there being clear groups of stressors (physical, chemical, biological),there are also distinct mechanisms through which
individual survival can be affected. Firstly, there are directeffects; these are often obvious and easily measured. Forexample, increased temperatures or drought may dry outephemeral ponds resulting in desiccation[18]. Second arethe stressors which reduce survival indirectly by acting upon development. These might be obvious, such asparasites causing developmental deformities which reducehunting ability of the adult frogs and increasesusceptibility to predation by birds and wild canids[39]etc. Alternatively, indirect stressors may be less obviouslike pesticides reducing immune function causing greatersusceptibility to diseases. Finally, many factors affect thebehaviour of the larvae, adult, or both life stages.
Behavioural changes can be easily observed in thelaboratory, but the impact they have upon wildpopulations is more difficult to estimate: In essence, any behavioural change which reduces developmental rate orsize at metamorphosis will indirectly impact probability of survival. For example: when exposed to hypoxicconditions, larvae may change behaviour by reducing overall activity, therefore reducing demand for oxygen, orthey may increase their aerial oxygen consumption[37],[32]. In either case, time spent feeding is reduced, thusreducing developmental rate. Any reduction in rate of development has twofold effects: firstly, prolonging timein the aquatic environment increases probability that the
larvae will fall victim to any one of the highlightedstressors. Secondly, evidence suggests that post-metamorphic populations show high levels of
Box 2. Life cycle of a typical trematode parasite
In this Ribeiroia life-cycle, the trematode miracidia
develop inside the snail hosts, into free swimming
cercariae. These then encyst the tadpoles at the
developing hind limb buds. High levels of infection
(multiple encystments) result in limb malformations such
as extra limbs and digits. This deformity impairs
movement of the metamorphosed frogs, increasing
susceptibility to predation by the definitive hosts, usually
birds but can be other predators such as canids, where
the parasite completes its life cycle. Finally, the eggs
transfer back to the first intermediate host via the faeces
of the definitive host.
References
Picture source: http://www.science-art.com/image/?id=3561&search=1
Koprivnikar, J., R.L. Baker, and M.R. Forbes, Environmental
factors influencing trematode prevalence in grey tree frog (Hyla versicolor)
tadpoles in southern Ontario. Journal of Parasitology, 2006. 92(5):
p. 997-1001.
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mortality[10] and size at metamorphosis is strongly correlated with survival probability[48]. Not allbehavioural changes necessarily effect survival, oftenthere are simply distributional changes such as larvaealtering microhabitat within a pond as a result of predatorpresence[2].
In conclusion, stressors can impact upon tadpolesurvival directly, or indirectly either through interactions
with other stressors or through interactions with
behavioural or developmental mechanisms. I propose the
synthetic model in Figure 2 as a way to visualize this
system.
In order to demonstrate use of this model, the
example used above from the experiments of Smith et al.
(1999) is once again used. Here, the abiotic factor of
interest in this system is pond hydroperiod. This may be
affected by temperature or rainfall, but there is no current
evidence that hydroperiod of the ponds is a limiting factor
on amphibian survival, rather is simply a measure of theprimary biotic factor, fish occupancy. Studies have shown
that the qualitative presence/absence of fish is more
important in systems like this, than any quantitative
density effects[49]. The secondary biotic factor in this
system is the presence of invertebrate predators. Figure 3
shows how the synthetic model in Figure 2 can be used to
visualize the experimental system explained by Smith et al.
(1999).
Quantification of the model
So far, this model produces a list of multiple, interacting
stressors which may or may not impact anuran survival.
In order to add strength to the model it would be
desirable to develop this further by completing an effect
size analysis to indicate which stressors are important and
have the largest impact in the system, thus giving a focus
for possible future research or conservation efforts. An
example of an effect size analysis is given in Figure 4.
The multiple stressors included are the abiotic factor
atrazine, and a biotic stressor, the parasitic trematode
Echinostoma trivolvis . This form of analysis shows how
atrazine has a „moderate effect size‟ (Cohen, 1969 in [50])
directly on survival,and on growth, cumulatively, a larger stressor than the
parasite which has little effect on growth and less of a
direct effect than atrazine. Additionally, atrazine also
increases prevalence of parasite infection, recorded here
as an effect on immunocompetence.
Figure 2. A synthetic model to illustrate the multiple
interacting stressors impacting anuran survival and the
mechanisms through which they act. Black lines= possible
interactions/pathways. Red lines= Direct effects on survival.
Solid blue lines= Indirect effects via some aspect of
development. Dashed blue lines= Potential indirect effects via
behavioural changes
Figure 3. Visual representation of the findings of Smith et al. (1999)[2]. Black lines= possible interactions/pathways. Red lines= Directeffects on survival. Solid blue lines= Indirect effects via some aspect of development. Dashed blue lines= Potential indirect effects via
behavioural chan es
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Critical assessment of the model
It will be noticed that the stressors are listed as abiotic,
primary biotic then secondary biotic, this is not to suggest
that this is always the case. Perhaps more appropriate
would simply be primary, secondary and tertiary stressors.
The reason this was not done here, is to symbolise how
the majority, if not all, systems will be influenced by one
or more abiotic factors. These factors could therefore be
three, or more, interacting biotic stressors, or a primary
abiotic factor, affecting a secondary abiotic factor whichin turn affects a primary biotic factor, and so on. This
gives the model great versatility, allowing the researcher to
adapt the input of stressors to those appropriate for the
study of a specific amphibian community.
The model produced here is not a predictive tool to
indicate common results of multiple stressors across
species. What has been highlighted several times is that
anuran species show great variety in habitat, exposure to
stressors, and, responses to common stressors. For
example, an assessment demonstrating the positive effects
of global warming on natterjack toad populations are not
valid for inferring the interactions of the same stressorson northern leopard frogs. Nor does this model help with
predicting the state of species currently listed as data
deficient by the IUCN for the same reasons. Currently
there is no substitute for direct surveying of populations
to determine population size and trends. However,
comparative assessments can be conducted to infer likely
common affects across closely related species.
The strength of this model is in application to specific
species or communities just as it has been above in figure
2. The model can be used to assess the interacting
stressors in the environment, and the responses of thespecies in question, to these stressors. This potentially has
two major benefits; firstly, this may lead to options for
conservation. Again from the above example, if there was
a need for increased conservation of Hyla versicolor , one
possible strategy would be to either increase the number
of temporary ponds, or to remove Lepomis macrochirus
from ponds within the breeding range of H. versicolor .
Secondly, the model can be used to highlight current gaps
in our understanding of the ecology for particular species.
For example, exclusion of H. versicolor to ephemeral ponds
increase their likely exposure to UV radiation, which has
been shown to reduce feeding behaviour in this
species[21], however this is an example in the tradeoffs
made by anurans to balance the effects of multiple
stressors. Also, eutrophic conditions are likely to have
larger impacts on fish populations causing a community
shift, increasing odonate populations, thus reducing the
population of Rana catesbeiana and increasing H. versicolor .
These interations can be inferred by inputting the currentknowledge into a synthetic model like those produced
above; it is much easier to look for further interactions
among the stressors, which can be easily overlooked
otherwise.
One flaw of the model is the issue of what is implied
by a lack of an interaction. It is not necessarily clear
whether no link in the model is a lack of an effect, or
rather a lack of knowledge, e.g. in the quantified example
above, there is no link identified between “growth/size at
metamorphosis” and survival. It‟s known that an effect
does exist, however the data presented in the studies
analysed was insufficient to allow for analysis. Therefore,
the model has been used to highlight a gap in our
knowledge and a potential direction for future research- in
this case, the quantification of the effect of anuran size
and survival.
Conclusion
The research reviewed here has focused on anuran larval
survival or mortality as a sole measure of the population
dynamics. Obviously this is less than ideal, but is
unavoidable due to the currently available literature. Many studies have highlighted the desire for more complete
anuran life histories and population effect studies
e.g.[10],[29]. This review has successfully used the current
understanding of anuran ecological stressors to develop a
model to present these stressors in a complete and
concise way. An example of how this model can be
quantified was shown. A more extensive meta-analysis
may be possible but is beyond the scope of this review.
Analyses could include more interacting factors and more
studies by accounting for variation in experimental design,
and therefore giving more valid results. An exciting result
of this form of analysis is the potential to isolate key
ecological stressors in the system. This will then provide a
Figure 4. Brief effect size analysis for the stressors atrazine and
Echinostoma trivolvis . Black line= effect of atrazine on survival of
parasite. Red arrows= direct effect of stressors on tadpole
survival. Blue arrows, indirect effects on tadpole survival via
growth or developmental mechanisms. “Immunocompetence”
is measured by susceptibility to E.trivolvis. See Appendix 1 for
full analysis details.
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focus to conservation efforts and hopefully bring an end
to the global amphibian decline crisis.
References:
1. IUCN. IUCN Red List of Threatened Species. Version 2010.4. 2010 30 November 2010]; Available from: www.iucnredlist.org.
2. Smith, G.R., et al., The effects of fish on assemblages of amphibians in ponds: a field experiment. Freshwater Biology, 1999. 41(4): p.829-837.
3. Stuart, S.N., et al., Status and trends of amphibian declines and extinctions worldwide. Science, 2004. 306(5702): p. 1783-1786.
4. Houlahan, J.E., et al., Quantitative evidence for global amphibian population declines. Nature, 2000. 404(6779): p. 752-755.
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6. Collins, J.P. and A. Storfer, Global amphibian declines: sorting the hypotheses. Diversity and Distributions, 2003. 9(2): p. 89-98.
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8. Skelly, D.K., et al., Estimating decline and distributional change in amphibians. Conservation Biology, 2003. 17(3): p. 744-751.
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11. Carey, C. Factors Limiting the Recovery of Boreal Toads (Bufob.boreas). 2003 Dec 11, 2010]; Available from:http://wildlife.state.co.us/NR/rdonlyres/3DE2B984-9FEB-45F2-BBA7-411C994E31F7/0/Chapter31.pdf.
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