Amphibian Biology 2014
-
Upload
ana-pino-blanco -
Category
Documents
-
view
21 -
download
1
description
Transcript of Amphibian Biology 2014
07/04/2014
1
Amphibians
Biology, ecology and conservation topics and their applications in ecotoxicology
Ecotoxicology of amphibians and reptiles: from theory to practice. Aveiro, April 2014
Manuel Ortiz Santaliestra
Institute for Environmental Sciences
University of Koblenz-Landau (Germany)
Outline
INTRODUCTION
Origin and evolution
Diversity
LIFE HISTORY
Breeding migrations
Mating, fecundation and oviposition
Eggs and embryonic development
Larval development
Metamorphosis
Sexual determination
Maturation and adulthood
ENVIRONMENTAL PHYSIOLOGY
Thermoregulation and water balance
Excretory physiology
Overwintering and aestivation
Gaseous exchange
ECOLOGY
Habitat
Feeding ecology
Antipredatory strategies
CONSERVATION
Global decline
Threats
Outline
INTRODUCTION
Origin and evolution
Diversity
LIFE HISTORY
Breeding migrations
Mating, fecundation and oviposition
Eggs and embryonic development
Larval development
Metamorphosis
Sexual determination
Maturation and adulthood
ENVIRONMENTAL PHYSIOLOGY
Thermoregulation and water balance
Excretory physiology
Overwintering and aestivation
Gaseous exchange
ECOLOGY
Habitat
Feeding ecology
Antipredatory strategies
CONSERVATION
Global decline
Threats
Origin and evolution
©Geoff Simpson
©Dan Nedrelo
© Heidi & Hans-Jürgen Koch
© Dan L. Perman
An uncompleted step towards the independence from water
Amphibians = two lives Reptiles
Origin and evolution Current diversity of amphibians
Order Gymnophiona (Caecilians)
200 species (all from Neotropic)
Order Caudata (newts and salamanders)
660 species (10 in the Iberian Peninsula)
© Chris Harrison
Order Anura (frogs and toads)
6396 species (19 in the Iberian Peninsula)
http://amphibiaweb.org/ (updated on April 6th 2014)
07/04/2014
2
Overview of Iberian amphibians
African species crossing the Strait ofGibraltar during the Messinian period(5.5 million years b.p.)
Eurosiberian species searching fromrefuge during Pleistocene glaciations(80,000 years b.p.)
The cosmopolite Iberian batrachofauna (African, Eurosiberian and endemic species)
Rana temporaria
Pleurodeles waltl
Iberian endemism originated byisolation, area reduction or habitatlimitation Chioglossa
lusitanica
Outline
INTRODUCTION
Origin and evolution
Diversity
LIFE HISTORY
Breeding migrations
Mating, fecundation and oviposition
Eggs and embryonic development
Larval development
Metamorphosis
Sexual determination
Maturation and adulthood
ENVIRONMENTAL PHYSIOLOGY
Thermoregulation and water balance
Excretory physiology
Overwintering and aestivation
Gaseous exchange
ECOLOGY
Habitat
Feeding ecology
Antipredatory strategies
CONSERVATION
Global decline
Threats
Reproductive modes variability: A key for success
The common reproductive strategy:
Terrestrial adults
Aquatic breeding, eggs and larvae
Breeding migrations
0
50
100
150
200
25 40 55 70 85
Ammonium nitrate dose (kg N / Ha)
Tim
e o
f a
no
ma
lou
s
eff
ec
ts (s
)
Adults migrate from winter refuges to breeding ponds
Orientation by magnetic fields, firmament, chemical cues and conspecific or heterospecific calls.
Risks:
•Road mortality
•Pollution in fields crossed during migrations
Χ2=23.204; N=28; p=0.001
Ortiz-Santaliestra et al. (2005) Bull Environ Contam Toxicol 75, 662-669
Impact of terrestrial ammonium nitrate application on Iberian newt
Recommended level of application
Mating and fecundation in Anura
Males arrive first. Two strategies depending on size (male quality):
•Bigger males attract females (deeper calls). They wait for females within the ponds territorialism
•Smaller males do not attract females. They wait for females outside the water to couplebefore their entering the ponds
Amplexus (coupling). External fecundation
Some exceptions:Internal fecundation
(Ascaphus)
Terrestrial amplexa (e.g., Alytes)
© Brad Moon © Daniel Phillips
Inguinal
Axilar
Cephalic
Wells (2007) The Ecology and Behavior of Amphibians. Chicago University Press
Mating and fecundation in Caudata
Males arrive first and wait for females within the water
Mating after courtships which end with spermatophore deposition (internal fecundation)
Spermatophore deposition and pick up in a terrestrial courtship
© Oregon State University
Some exceptions:
07/04/2014
3
Oviposition
Although most species are oviparous, there are ovoviviparous and viviparous species
Alytes(~40 eggs)
Bottom: low predation, high asphyxia
Surface: high predation, low asphyxiaVegetation: low predation, high eutrophication
Bufo(~3000-5000 eggs)
Clutch size
Where to lay?
Streams: attached to stones, adapted to high O2 and water currents
Terrestrial eggs
© Thomas Reich
Oviposition
Isolated masses
Individual (newts)
How to lay?
Communal
© Andy Fion
© Henk.Wallays from Flickr
© Jenny Gitlitz
Parental care of the eggs
Foam nests (Chiromantis)
Wrapped by plants (Triturus)
Under stones or in cavities (Chioglossa)
Attached to the plants (Hyla)Shallow water
Direct parental protection
Carrying out (Alytes)
Covered by skin (Gastrotheca)
Gastric brooding (Rheobatrachus)
© Jack Goldfarb
© Merike Linammägi
© Louise Mentjies
© Luis Bravo
© Kevin Johnson
Egg protection beyond parental care
Jelly coat
Formed after absorptionof water once eggs havebeen laid
UnpalatabilityCamouflage
Dark top to camouflage against the bottom
Bright bottom to camouflage against the surface
Embryonic development
Gosner (1960) Herpetologica 16, 183-190
Risk of pollution during egg andembryonic stage:
•Removal of laying substrates
•Alteration of parental behaviours(oviposition, site selection, egg protection)
•Uptake of chemicals by jelly coat
•Maternal transfer of pollutants throughjelly coat
•Egg rotation
•Direct effects on embryonic development
The frog embryo teratogenesis assay - Xenopus
Standardized protocol to test teratogenesis
•Static system
•Freshly deposited embryos of Xenopus laevis
•25 embryos per glass in 140 ml + g soil
•4 replicates (total 100 embryos)
•Environment: FETAX solution
•20-25 tadpoles per tank in 10-12.5 liters
•Duration: 96 hours
•Phase 1) Screening test: control + 100% sample
•Responses are expressed as percent effect
•Phase 2) Final test
•LC50
•EC50
•Description of abnormalities
ASTM (2004) Report # E1439-98; Bantle et al. (1991) Atlas of Abnormalities: A Guide for the Performance of FETAX. OSU Press
07/04/2014
4
Larval development
Gosner (1960) Herpetologica 16, 183-190
Anura
Caudata
Larval morphological adaptations
Duelllman & Trueb (1994) Biology of Amphibians. John Hopkins University Press
Mouth morphology and position
Spiracle
Pond (low O2) Stream (high O2)
CAUDATA
Pond, benthonic
Pond, pelagic
Stream
ANURA
Larval development
Longer times(bigger tadpoles)
Shorter times(smaller tadpoles)
Juvenile survival
Reproductive quality
Avoid desiccation
Avoid predation
? Avoid pollution ?
Viviparity (S. salamandra)
Duration: from hours to years
Camouflage Unpalatability
Parental care
Exceptions:
Direct development
Protection© Tom Ray
Dendrobatidae Rhinoderma darwinii
© Fogdenphotos.com
Eleutherodactylus sp.
Grow or survive?
Advantages of phenotypicplasticity
Metamorphosis in Anura
Changes:
Respiratory system
Digestive track
Cranium and jaws
Pelvic girdle
Skin keratinization
Vision organs (cones rods)
Immunological modifications
Gosner (1960) Herpetologica 16, 183-190
Ecotoxicological interest:
Mobilization of reserves
Transport of accumulative chemicals from aquatic to terrestrial environment
Metamorphosis. Hormonal control
Amphibian metamorphosis assay for evaluation of EDCs:
Flow-through system
Water filtered and UV-treated
20-25 tadpoles per tank in 10-12.5 liters
Food: Sera Micron
Duration: 14-21 days
Endpoints:
-Periodical monitoring of developmental stage and snout-vent length
-Histological examination of thyroid gland at the end of the exposure
Duellman & Trueb (1994) Biology of Amphibians. John Hopkins University Press; OECD (2004) Report #ENV/JM/MONO(2004)17
Amphibian metamorphosis depends on thyroid hormones (major effects) and pituitary hormones
Metamorphosis. Immunological overview
-Development of adult immune system components
+
Maternal antibodies
Larval immune system
Developing adult immune system
Developed adult immune system
Rearrangement of immune defenses
Destruction of some components of the larval immune system
Thyroid hormones
Glucocorticoids
PerchlorateMalathion*Atrazine*
*Known immunotoxic effect during
amphibian metamorphosis
PCBsPCDDs
+ -
Robert & Ohta (2009) Devel Dynam 238, 1249-1270; Rollins-Smith et al. (1998) Immunol Rev 166, 221-230
07/04/2014
5
Sexual determination
Highly complex mechanism
Genetic determination (XX/XY and ZZ/ZW systems, sometimes simultaneous inthe same species), that does not correspond to the phenotypic sex in manycases
Sex determination depends on the regulation of sex-determining genes (e.g.DM-W in Xenopus) which are different among species. Some species dependon multiple genes
Influence of temperature, although apparently only at temperatures out of theenvironmental range
Sex-reversal mediated by hormonal factors that keep population withinappropriate sex ratios
Nakamura (2009) Sem Cell Dev Biol 20, 271-282
Maturation and adulthood
Sexual maturity is usually achieved earlier by males than by females
Female’s have higher probability of dying before reproduction
Sex ratios of the breeding population are sometimes skewed towards males
Mechanisms of compensation:
•Females may live longer than males
•Young males are usually unsuccessful in defending a territory or unattractive to females
Davies & Halliday (1977) Nature 269, 56-58
Outline
INTRODUCTION
Origin and evolution
Diversity
LIFE HISTORY
Breeding migrations
Mating, fecundation and oviposition
Eggs and embryonic development
Larval development
Metamorphosis
Sexual determination
Maturation and adulthood
ENVIRONMENTAL PHYSIOLOGY
Thermoregulation and water balance
Excretory physiology
Overwintering and aestivation
Gaseous exchange
ECOLOGY
Habitat
Feeding ecology
Antipredatory strategies
CONSERVATION
Global decline
Threats
Thermoregulation and water balance
Behavioural mechanisms © Ben Klocek
© Sandy Garfinkel
Basking to warm up
Use of refuges to cool down
Dermal uptake / elimination of water
10% of the body surface account for 70% of the tegumentary water diffusionHow will global warming
and increased UV radiation affect these behaviours?
Thermoregulation and water balance
Physiological mechanisms
•Evaporative cooling
•Regulation of osmolarity in body fluids
Salinity
Wright et al. (2004) J Exp Zool 301A, 559-568
Excretory physiology
Cree (1985) New Zeal J Zool 12, 341-348
Ammoniotelic or ureotelic depending on the life stage
L. ewingi
L. raniformis
Ammonia Urea
07/04/2014
6
Excretory physiology as a detoxification mechanism
Schmuck et al. (1994) Copeia 1994, 996-1007
< 1 mg/l NH4+-N < 1 mg/l NH4
+-N
5 mg/l NH4+-N 5 mg/l NH4
+-N
Physiological adaptations confer indirect protection against pollution
Ortiz-Santaliestra et al. (2010) Environ Pollut 158, 934-940
Low salinity site High salinity site
Same effects of N on growth occur at lower levels when animals are not adapted to salinity
Pelophylax perezi
Overwintering and aestivation
Overwintering places:
Aquatic (muddy bottom): avoids freezing, risk of hypoxia (only cutaneous respiration)
Terrestrial: avoids hypoxia, risk of freezing cryoprotection: glucose accumulated within the cells while water is removed from the cells:
•Extracellular crystallization releases latent heat
•Intracellular crystallization is avoided because high osmotic concentration
Aestivation behaviours:
Burrowing
Cocoons (mud cover, shedded skin, mucous layer)
Ecotoxicological considerations:
Pre-hibernation/pre-aestivation are critical periods (accumulation of fatty acids, high membrane permeabilization to facilitate transport)
As periods of low metabolic rate, depuration of chemicals is kept to a minimum
Reserves (and potential accumulated pollutants) may be mobilized
Lithobates sylvaticusLives in areas reaching -40ºC
Body temperature drops till -5ºC
Costanzo et al. (1993) J Exo Biol 181, 245-255
© Doug Waylett
Gaseous exchange
Dermal: embryos, tadpoles, and adult aquatic stages
Gills: tadpoles and neotenic forms
Gill surface area may be related to O2 availability
Lungs: late tadpole stages (gulping) and terrestrial stages
Caudata
External gills
Anura
Gills internalized shortly after hatching
© Greg Dodge
Outline
INTRODUCTION
Origin and evolution
Diversity
LIFE HISTORY
Breeding migrations
Mating, fecundation and oviposition
Eggs and embryonic development
Larval development
Metamorphosis
Sexual determination
Maturation and adulthood
ENVIRONMENTAL PHYSIOLOGY
Thermoregulation and water balance
Excretory physiology
Overwintering and aestivation
Gaseous exchange
ECOLOGY
Habitat
Feeding ecology
Antipredatory strategies
CONSERVATION
Global decline
Threats
Breeding habitat
Temporary ponds / streams
Artificial water bodies
Free from fish and other big predators
Problems:
Legally unprotected. Used as dumps
Unpredictable. High desiccation risk
Low water volume. High eutrophication risk
Accumulation of pollutants from adjacent fields
07/04/2014
7
Feeding ecology: diet
Herbivorous
(algae filtering, periphyton scrapping)
Carnivorous
(insects, worms, tadpoles and small vertebrates)
ANURA CAUDATA
Ecotoxicological considerations:
Generally opportunistic diet (sentinels of what is present in the environment)
Major effects of herbicides and insecticides
Main role in energy transfer within ecosystems (simultaneous predator andprey)
Feeding ecology: foraging
Feeding modes in larvae:
•Filter feeding
•Grazing from rocks or plants
•Syphoning
•Prey capture
•Oophagy
•Cannibalism
0
0,1
0,2
0,3
0,4
0,5
0,6
0 11.3 45.2
Ammonium nitrate (mg N/L)
Can
nib
alis
m r
ate
±SE
Low Density
High Density
** NS NS Density effects:
NS p > 0.05
** p < 0.05
Cannibalism has also an environmental component
Adaptive cannibalistic morphs
Larvae Adult
Normal
Cannibal
S. salamandra
Duellman & Trueb (1994) Biology of Amphibians. John Hopkins University Press
Ortiz-Santaliestra et al. (2012) Aquat Toxicol 110-111: 170-176
Feeding ecology: foraging
Sit and wait
(Ceratopryhs)
Jumping on prey
© Warren photographic
Lingual flips
Bolitoglossa
(7 milliseconds)
© Softpedia
Antipredatory strategies
Predator detection chemical and visual cues
Avoiding tactics Releasing tactics
Passive defenses
Camouflage / distractionAposematism / mimicry
Unpalatability
Active defenses
Running / swimmingSimulate mortality / bad smellsInflatingIntimidation
Distress callsDifficult posturesBladder emptying
© Perefct Vision Grpahics
© Brian Bevan
© Batraciens-Reptiles.com Unken reflex
© D. Maitland
© thehibbitts.net
Eleuterodactylus gaigeae
Phyllobates lugubris
Outline
INTRODUCTION
Origin and evolution
Diversity
LIFE HISTORY
Breeding migrations
Mating, fecundation and oviposition
Eggs and embryonic development
Larval development
Metamorphosis
Sexual determination
Maturation and adulthood
ENVIRONMENTAL PHYSIOLOGY
Thermoregulation and water balance
Excretory physiology
Overwintering and aestivation
Gaseous exchange
ECOLOGY
Habitat
Feeding ecology
Antipredatory strategies
CONSERVATION
Global decline
Threats
Amphibian global decline: the suspicion
1989: First World Congress of Herpetology (Canterbury, UK)
Apparent extinctions or declines
Bufo periglenes (Costa Rica)
Rheobatrachus silus (Australia)
Additional clues…
Mass die-offs associated to bacterial blooms
Malformations
Blaustein & Wake (1990) Trends Ecol Evol 5, 203-204; Wake (1991) Science 253, 860
07/04/2014
8
Amphibian global decline: the evidence
2000: Almost 1000 populations studied worldwide
Houlahan et al. (2000) Nature 404, 752-755
Amphibian global decline: the drama
2004: Global Amphibian Assessment (IUCN) concussions:
•32% of amphibian species worldwide are threatened (12% of birdsand 23% of mammals)
•165 amphibian species have become extinct during last years, whileanother 130 have disappeared recently
•43% of amphibian species are declining, by only 1% of species areincreasing
Distribution of endangered species
Threats: Habitat loss or degradation (terrestrial)
Fires Urbanization
Habitat fragmentation and road mortality
1950
1990
Homogeneization
Threats: Habitat loss or degradation (aquatic)
Absence of buffer zones Dumping
Loss of traditional uses (pools, water troughs)Desiccation
Threats: Overexplotation Threats: Invasive species
© John White
American red crayfish (Procambarus clarkii)
Bullfrog (Lithobates catesbeianus)
Red-eared slider (Trachemys scripta)
Mosquitofish (Gambusia holbrooki)
07/04/2014
9
Threats: Diseases
Red-legged frogs (Aeromonas hydrophilla)
Secondary, non-etiological pathogen
Fungi
Oomycetes (water molds)
BacteriaChytriomycosis
Saprolegniasis
Virus
© www.sosanfibios.org
Chytridiomycosis
•Batrachochytrium dendrobatidis, theetiological agent, shows low genetic variabilityaround the world
•Suspected to be originally spread byXenopus because its use as a laboratoryanimal or in pregnancy tests. Nowadays,humans are the main vector
•First cause of decline in pristine areas
•It grows on the keratinized areas of the body,affecting mainly to metamorphs
•Two theories to explain the outbreaks:
•High nutrient levels favor fungal growth
•Environmental stressors weakenamphibians
Keratin in tadpoles is limited to oral disk. Bd may cause malformations, although most tadpoles are tolerant and act as reservoirs
Olson et al. (2013) PLoS ONE 8, e56802
Threats: Ultraviolet radiation
Ultraviolet radiation
•UV-A (λ = 315-400 nm): not filtered either by ozone or oxygen
•UV-B (λ = 280-315 nm): filtered by ozone
•UV-C (λ = 100-280 nm): filtered by ozone and oxygen
Threats: Climate change
Pelobates cultripes estimated distribution
Current50 years
(dispersal)50 years (no dispersal)
Araujo et al. (2006) J. Biogeogr. 33, 1712-1728; Rohr et al. (1998) PNAS 105, 17436-17441
Threats: Pollution Why amphibians?
Impacted by stressors acting on terrestrial or aquatic ecosystems
Low vagility and high philopatry: low dispersal and colonization ability
Distribution in metapopulations: high sensitivity to isolation
Naked skins very permeable to chemicals or pathogens
Intermediate position in trophic webs