In my previous post on tadpoles of this species I left the question of whether adult Common Asian Toads, Duttaphrynus melanostictus, can tolerate saltwater, and, if so, what strength of saltwater.
Before trying to answer that question I should point out that since the mid-1960s, the ability of a number of other amphibians to tolerate saltwater has been studied, the Green Toad (Bufotes or Bufo viridis) from Europe and the Middle East being one notable example.
In an epic of bibliographic research Gareth Hopkins and Edmund Brodie pulled together all the papers on the occurrence of amphibians in saline habitats beginning as far as I can see with Charles Darwin in 1834; their review was published in 2015. Useful though that exercise was (although I have since found at least one paper that was missed), I was less than impressed by the treatment of physiology in the review and the criteria used to extract meaningful data from individual papers, particularly those reporting observations rather than experimental evidence. I can illustrate these points by reference to a table in their review that includes Duttaphrynus melanostictus as a ‘well-studied salt-tolerant amphibian species’. Let’s look at the evidence from the papers they used to reach this conclusion.
Annandale’s paper from 1907
Quoting Nelson Annandale†, Hopkins and Brodie show a measured salinity of 12.87g/kg for where Annandale found this species in India. Please note for this article compared with the last, I am using g/kg (parts per thousand) rather than percentages for salinity in order to use the same units as Hopkins and Brodie. 12.7g/kg is equivalent to about 40% seawater and would be well above the point of isotonicity‡ between body fluids and the external environment. In other words, there would be an osmotic flow of water out of the body. However, there are important caveats. Annandale’s paper describes the brackish ponds at Port Canning on the Matla river, about 60 miles from the sea. The ponds were dug as part of an ill-fated scheme to build a port to rival Calcutta and Singapore in the 1860s; judging by what I can see on Google Earth, they are still there. This is how Annandale describes the water and its salinity:
An important factor in the environment is the nature of the water. I have described the ponds as brackish, but at some time of the year the water may contain the same proportion of soluble salts as the sea, at others it may even be more strongly saline, and again at others it is much more nearly fresh. As a rule the ponds are completely isolated both from one another and from the estuary. During the cold weather they are exposed to evaporation, which becomes intensified during the hot weather. During the rainy season, on the other hand, they become filled up with fresh water and probably often coalesce. They are also liable to be placed in temporary communication with the estuary occasionally, owing to a flood bursting the embankment but this does not occur by any means every year. When it does happen, it happens owing to the estuary being swollen with fresh water, which is flowing down from up-country so that the ponds, even under these conditions, are practically cut off from the sea.
Stoliczka*, in 1868 or 1869, had the water of the ponds analysed; but he does not say at what time of year his samples were obtained. He found that the proportion of soluble solids was 12.87 per thousand, sea-water containing from 32 to 39 per thousand. Mr. D. Hooper, Curator of the Industrial Section of the Indian Museum, has kindly examined samples taken by myself in December and March last. Two samples came from a pond in which the Hydrozoon Irene ceylonensis, as well as the Actinian, was reproducing its species, and in which the plant Naias was abundant. A sample taken from this pond at the beginning of December, a few weeks after the end of the rainy season, was found to contain 12.13 per thousand of soluble salts, while another taken on March 17th contained 20.22 per thousand. At the latter date water from the edge of the Matla at Port Canning contained 25.46 per thousand, and that from a second pond near the first 23.16…
Stoliczka noted that the water in the ponds was almost fresh during the rains…All that can be said, therefore, as regards the salinity of the water of the ponds, is that it varies considerably at different times of the year…
Listing the fauna of the ponds, Annandale had this to say:
…and the only Amphibians the equally common Rana cyanophlyctis and R. tigrina. The Indian Toad, Bufo melanostictus, is abundant at the edge of the ponds, in which it possibly breeds.
So, equating measurements of the measured salinity of the ponds at a particular season to a presumed salt tolerance of the largely terrrestrial toad (it could breed in the ponds in the rainy season when the water is ‘more nearly fresh’) is perhaps unwise. The killer blow, though, to trying to relate measured salinity to salt tolerance of this toad is the occurrence of the two species of frog. The Indian Bullfrog, Rana tigrina, now reverted to its apparently correct specific name of tigerina in the genus Hoplobatrachus, was used by Gordon, Schmidt-Nielsen and Kelly in their 1961 paper as a freshwater species to compare with F. cancrivora. Their results were clear. Adult bullfrogs could tolerate a salinities up to 9 g/kg (25% seawater). Above that physiological point of isotonicity, the frogs died in 24-48 hours, even at 11 g/kg. Therefore, the salinity quoted by Annandale cannot be equated to the presence of the amphibian species in the water at the same season.
I therefore discount the evidence taken from Annandale’s paper on D. melanostictus.
George Chakko’s paper from 1968
The only direct study on the saltwater tolerance of D. melanostictus listed by Hopkins and Brodie is that by George Chakko of Madras Christian College published in 1968. He kept four local species in various concentrations of seawater. There was a difference between species. All survived for two weeks in 25% local seawater (salinity 32g/kg), i.e. 8 g/kg. These species were Jerdon’s Bullfrog (Hoplobatrachus, then Rana, crassus), Indian Green Frog (Euphlyctis, then Rana, hexadactylus), Marbled Narrow-mouth Frog (Uperodon or Ramanella variegatus*) and, of course, D. melanostictus. Only D. melanostictus survived in 35% seawater, i.e. 11.2 g/kg. These were the maximum tolerated concentrations.
What do we now know?
Looking at the experimentally-determined salinity tolerance of a number of anurans (frogs and toads, for brevity, although there are interesting examples in caudates, the newts and salamanders) listed by Hopkins and Brodie, there are a number that show a similar tolerance to D. melanostictus. I counted 7 species in the range 10-11.2 g/kg. Above that there are only 4: Xenopus laevis at 14g/kg (reminding us salinity can be high in inland waters); the possibly aptly named Marine or Cane Toad, Rhinella marina at 16; Green Toad, Bufotes viridis, at 20-26 and then the jump to F. cancrivora at 39.
In terms of mechanisms of adaptation, it is interesting that in the four species known to tolerate higher salinities as adults, an increase in urea as well as an increase in salt concentrations in blood has been found. Is that also true of those tolerant to only slightly hypertonic saltwater like D. melanostictus, or do they rely simply on a small increase in salt concentrations in their blood?
The take-home message is that D. melanostictus just enters the physiologically interesting, in terms of adaptations needed to survive, range of salinity, in that the 35% seawater (but not the 25% seawater) would be slightly hypertonic to the body fluids of toads in freshwater. In terms of physiological adaptation, there is a question still to be answered—an ideal project for an honours year student perhaps.
On the Common Asian Toad, taking the evidence discussed in this and the previous article, I can summarise:
- Tadpoles must hatch in virtually fresh water
- Older tadpoles must live in brackish water hypotonic to body fluids
- Adults can tolerate salinities just but only just hypertonic to body fluids. The physiological mechanism has not been studied in this species.
- The evidence matches observations that these toads can live near the sea, even breed in freshwater near the sea, where they may be exposed to brackish conditions.
- D. melanostictus does not approach the capabilities of F. cancrivora in exploiting the far greater salinity of a mangrove swamp.
‡Tonicity is a measure of the effective osmotic pressure gradient, as defined by the water potential of two solutions separated by a semipermeable membrane. In other words, tonicity is the relative concentration of solutes dissolved in solution which determine the direction and extent of diffusion. It is commonly used when describing the response of cells immersed in an external solution. Unlike osmotic pressure, tonicity is influenced only by solutes that cannot cross the membrane, as only these exert an effective osmotic pressure. Solutes able to freely cross the membrane do not affect tonicity because they will always be in equal concentrations on both sides of the membrane. This Wikipedia definition is as good as any. An example of differences between isotonic and isosmotic would be the plasma composition of F. cancrivora in saltwater. Because of the impermeabilty of the membranes in question to urea, this isomotic concentration is isotonic. In a typical mammal, because urea passes rapidly across membranes, the isosmotic plasma would be hypotonic.
†Thomas Nelson Annandale (1876–1924), in 1907 Director of the Indian Museum in Calcutta.
*Ferdinand Stoliczka (1838 –1874), a Moravian (Czech) in the Geological Survey of India. An all-round palaeontology, geology and zoology, he described and named the frog Ramanella variegatus (studied by Chakko above) in 1872.
Annandale N. 1907. The fauna of brackish ponds at Port Canning, Lower Bengal. Records of the Indian Museum 1: 35–43.
Chakko G. 1968. Salinity tolerances of some Indian anurans. Proceedings of the Indian Academy of Sciences - B 67, 233–236,
Hopkins GR, Brodie ED. 2015. Occurrence of amphibians in saline habitats: a review and evolutionary perspective. Herpetological Monographs 29, 1-27. DOI: 10.1655/HERPMONOGRAPHS-D-14-00006
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