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Physiological and morphological correlates of extreme acid tolerance in larvae of the acidophilic amphibian Litoria cooloolensis

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Abstract

The Cooloola sedgefrog (Litoria cooloolensis) is one of a number of frog species endemic to the coastal sandy lowlands of east Australia exhibiting remarkable tolerance to dilute waters of low pH (< pH 3.5). To investigate the physiological and morphological underpinnings of acid tolerance in L. cooloolensis larvae, we compared Na+ balance, uptake and efflux rates, and gill and skin morphology in larvae reared in circum-neutral (pH 6.5) and pH 3.5 water. We hypothesised that L. cooloolensis larvae would be more resistant to ionregulatory disturbance and epithelial damage at low pH relative to acid-sensitive species. Net Na+ flux rates were not significantly different from zero in L. cooloolensis larvae reared at pH 3.5 and in acid-naïve animals maintained in pH 6.5 water. Animals reared at pH 6.5 and acutely exposed to pH 3.5, however, exhibited a net loss of Na+ due to inhibition of Na+ uptake. In contrast, L. cooloolensis larvae reared at pH 3.5 maintained Na+ balance at pH 3.5 and did not exhibit inhibition of Na+ uptake at this pH. Investigation of Na+ transport kinetics and the morphology of the gills and integument suggests tolerance of L. cooloolensis larvae to low pH may be attributed to a high capacity for branchial Na+ uptake, increased tight junction length and elevated mucus production at the gills and integument. These factors confer resistance to acid damage and disruption of ionic homeostasis which would otherwise result in the death of amphibian larvae exposed to waters of pH 4.0 and less.

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Abbreviations

ASW:

Artificial soft water

ICPOES/ICPMS:

Inductively coupled plasma optical emission spectroscopy/inductively coupled plasma mass spectroscopy

MS222:

Ethyl 3-aminobenzoate methanesulfonate

J in :

Rate of Na+ uptake

J out :

Rate of Na+ efflux

J net :

Net Na+ flux

WBA:

Counts per minute of whole tadpoles

SA:

Average specific activity

m:

Dry mass of the tadpole

t :

Time

J max :

Maximum Na+ uptake rate

K m :

Na+ concentration at 50% of Jmax

DBM:

Dry body mass

TEM:

Transmission electron micrograph

LM:

Light micrograph

SEM:

Scanning electron micrograph

TJ:

Tight junction

MR:

Mitochondrion-rich cell

ECaC:

Epithelial Ca2+ channel

ENaC:

Epithelial Na+ channel

MSV:

Mucus secretory vesicle

CCA:

Cell cross-sectional area

TMSVA:

Total cross-sectional area of mucus secretory vesicles

bl:

Basal lamina

cap:

Capillary

cc:

Ciliated cell

ct:

Connective tissue

d:

Desmosome

ec:

Squamous epithelial cell of outer integument

fp:

Filter plates

ga:

Gill arch

gt:

Gill tuft

hd:

Hemi-desmosome

mf:

Mucus fuzz

mr:

Microridge

mt:

Mitochondria

n:

Nucleus

pc:

Pavement cell

rbc:

Red blood cell

tj:

Tight junction

v:

Velum

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All authors contributed to the study conception and design. Material preparation, data collection and analysis were performed by EAM and RLC. The first draft of the manuscript was written by EAM and all authors commented on previous versions of the manuscript. All authors read and approved the final manuscript.

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Correspondence to Rebecca L. Cramp.

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Meyer, E.A., Franklin, C.E. & Cramp, R.L. Physiological and morphological correlates of extreme acid tolerance in larvae of the acidophilic amphibian Litoria cooloolensis. J Comp Physiol B 191, 159–171 (2021). https://doi.org/10.1007/s00360-020-01316-y

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