Estuarine stonefish

Synanceia horrida (Linnaeus, 1766)



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Figure 1: You are looking at the world's most venomous fish — the Estuarine stonefish (Synanceia horrida) (Source: Ria Tan)

Introduction

Based on the photograph above, it might have taken you a moment to realise that its a stonefish and not a rock you are looking at. Looking extremely well-camouflaged, the unattractive Estuarine stonefish (Synanceia horrida), as its common name suggests, looks remarkably like an eroded coral rock or stone. This marine fish could be found in the tropical regions and you might have encountered one before if you fish, dive or visit the beaches and intertidal areas. Hopefully, your experience with it had not been an unpleasant one. Why unpleasant? You might wonder, especially if you have yet to encounter one or perhaps if you have never heard of them before. As harmless as it appears to be, this Estuarine stonefish actually made it into the Guinness Book of Records 2001, holding the title of being the world's most venomous fish (9)(10). And yes, the Estuarine stonefish could be found in Singapore's waters too! Despite being most well-known for being venomous, do not be too surprised that people actually do consume them as food! Certainly, the Estuarine stonefish have many other interesting behaviour and properties which you can learn all about in this webpage.

This webpage is a consolidation of the different aspects of the Estuarine stonefish, putting these information in a easy to read manner. Starting with more basic information such as the habitat and morphological features of the fish, the page will become progressively more scientific and technical. You may follow the sequence as listed in the table of contents, or you can just click and navigate to the the parts that interest you.

Table of contents

1. Ecology
2. General description
3. The venom
4. Biology
5. Human interaction
___ in Singapore, past and present
6. Conservation status
7. Distribution
8. Taxonomic information
9. Phylogenetics
10. References




Ecology

Habitat

They live in marine or estuarine waters, mainly on or near coral reefs or in intertidal areas. They are mostly shallow-water dwellers and are often found well-camouflaged near rocks, around dull coloured plants, or found motionless in the sand or mud. They need not be completely covered in water at all times and can stay out of water for up to 24 hours.

General description


As its scientific name suggest, horrida was derived from the Latin word 'horridus', meaning rough (2). True to the meaning of its name, its body is warty with numerous bumps. Unlike most fishes, this stonefish does not have scales on its body. It certainly appears to look rather hideous with its depressed, broad head and inflated body (3). Its small eyes are well-elevated on its head, facing upwards, separated by a bony ridge. A deep depression is found below each eye, giving it a 'hollow-cheek' appearance. Its mouth is large and upturned, this is also known as a superior mouth position. Cirri, which are fine whiskery protrusions, are present on its lips. It differs from its closely related Reef stonefish (Synanceia verrucosa), which does not have hollow cheeks, but have a deep depression between its eyes (4)(5).

Colour

As seen from the pictures, its body appears to be dull and drab in colour, typically appearing in shades of brown to reddish brown. Filamentous algae and debris are often seen growing on the body (4).

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Figure 2: Photographed image of a drably coloured S. horrida specimen with warty and scaleless body. The deep depression below it elevated eye is obvious.
(Source: Australian Natural Fish Collection, CSIRO. Rights: Australian Natural Fish Collection, CSIRO. License: Creative Commons Attribution- Noncommercial-Share Alike.)



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Figure 3: The head appears broad and flattened, with a prominent bony ridge between the eyes. Its mouth faces upwards. (Source: Ria Tan)

Size

It is generally 30-40cm in size, though those observed in Singapore's intertidal areas are much smaller, at around 15-20 cm (5). The maximum recorded length of this stonefish is 60cm (7).

Venom apparatus

On its dorsal fins, 13 dorsal spines covered with thick and loose-fitting skin are present. Acute tips of the dorsal spines are observed to protrude slightly through their skin sheaths. The spines are arranged from the anterior (front) to posterior (rear end) direction, where spines 2 and 3 are usually the straightest and largest spines. Spine 1 appears to be relatively thicker and shorter, while spines 4 - 13 were on average about the same length, curving towards the posterior direction. (6) In addition, two pelvic spines and three anal spines are also present on the respective fins. These spines however, are completely embedded and covered by their thick skin sheaths (12). A pair of venom glands are found associated to each spine, one on either side of individual spines. More information is in the next section.

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Figure 4: Labelled image of a S. horrida specimen. The tips of the dorsal spines could be seen protruding out of the skin sheaths.
(Original source: Australian Museum Archives, Rights: © Australian Museum.
Original image: http://australianmuseum.net.au/image/estuarine-stonefish-synanceia-horrida)

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Figure 5: Photograph of the first dorsal spine showing the large venom glands situated on each side of the spine. (Source: Halstead et al., 1956)

The venom

Venom properties

Being one of the most venomous fish in the world, the venom properties of Synanceia horrida have been widely studied. Venom is a form of toxin secreted by an animal usually for defense purposes and is injected into the victim through a bite, sting or other sharp body features. In the case of the stonefish, its spines are the apparatus used in delivering the venom. S. horrida secretes a two-subunit protein toxin known as stonustoxin and it is capable of inducing potent hemolytic (destruction of red blood cells) activity (19). This protein however, is unstable and can be denatured by heat. For those who wish to understand more about the stonefish's venom and toxins, you may wish to read papers by Prithiviraj et al. (2012) (19) and Gwee et al. (1994) (20).

As mentioned, every spine has a pair of venom glands attached. The venom glands of the first to third dorsal spines are located approximately at the middle of the spine, while the glands of the remaining spines are more distally situated. All the glands appear to be attached to the spines by tough strands of connective tissue. The glands terminate in duct-like structures that extends to the tips of the spines.





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Figure 6: A diagrammatic drawing of the spine with its associated venom gland. Key -- S: Spine; VG: Venom gland; CA: Connective tissue attachments of gland; ED: Excretory duct; DO: Distal opening of excretory duct (Source: Halstead et al., 1956)


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Figure 7: Close up photograph of an exposed spine of the Estuarine stonefish, where the venom glands and connective tissues could clearly be seen.(Source: Australian Museum Archives, Rights: © Australian Museum,Obtained from: http://australianmuseum.net.au/image/estuarine-stonefish-spine)

When pressure is applied to the glands, fluid is observed to pass from the glands to the tip of the spine through the ducts. The GIF image below is from an experiment and it shows exactly how the venom is released and injected into you when greater pressure is applied in a violent expulsion. The full video experiment is also available below.



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Figure 8: GIF image showing how the venom is released in slow motion when pressure is applied. (Source: imgur)


Video 1: The full experiment where the world's most venomous fish is being 'milked' by a toxinologist."Milking the WORLD'S MOST VENOMOUS FISH! - Smarter Every Day 117," by SmarterEveryDay. YouTube, 26 June 2014.URL:https://youtu.be/I8yJkIuvPvM (accessed 6 Nov 2015)

These venomous spines however, are not used for hunting. It is merely just a defensive mechanism for the stonefish, against its possible predators such as sharks, rays and sea snakes(5). For greater details on the venom glands and the venom apparatus of the stonefish, it is recommended to read the works by Halstead et al. (1956) (12) and Gopalakrishnakone & Gwee (1993) (6).

Anti-venom properties

The anti-venom for stonefish was developed in 1959 in Australia and this was the world's first marine anti-venom (17). This was prepared using plasma of horses that have been immunised with the stonefish venom of Synanceia horrida and/ or its closely related Synanceia verrucosa (16). The anti- venom reduces the likelihood of death and is only used when there is clear evidence of stonefish envenoming with severe effects.

A potential hazard

Stonefishes can be a potential hazard in the natural environment, specifically to those who are careless, as they are capable of inflicting injury in humans. Those at higher risk includes mainly divers, fishermen and visitors in intertidal areas. Judging from the video above, once their venom-coated spines penetrates through the human skin, not only is it excruciatingly painful, it also causes gross oedema, which is the swelling of affected tissues due to fluid build up. Furthermore, the venom can cause envenomation, leading to local morbidity at the site where venom was injected. The venom can cause major depletion of neurotransmitter, damages the nerve and muscle fibres and also inhibits the neuromuscular function (20). In serious cases, it may lead to severe systemic morbidity, respiratory failure, pulmonary oedema and even death. It was noted that death was more likely to occur as a result of unconsciousness and possible drowning due to the severe pain rather than from the venom itself (3).

Precautions

When taking intertidal walks, one should be in covered shoes. Walk slowly and watch your step. Pull back immediately if your feel a prick through your shoe and do not exert full body weight down. Avoid murky waters and try to drag your feet instead of stepping down if you cannot see where you are going.

Treatment

Pre-hospital care should be immediate once it is recognised that the injury is a potential envenomation. The spines could gently be removed and apply direct pressure to control the bleeding. As the protein toxin can be denatured by heat, the affected limb should be immersed in hot water (around 45 degrees Celsius) as soon as possible. Inactivation of the venom can provide rapid relief. Once in the hospital, apart from treating the wound, additional analgesia for pain relief could be administered. Additional treatment such as administering tetanus for marine animal injury and antibiotics against marine pathogens are also recommended. Anti-venoms are only administered for severe envenomations with systemic symptoms. It is advisable to have at least 6 to 12 hours of observational monitoring after treatment (1). You may read about a case regarding stonefish envenomation and the treatment received here.



Biology

Other adaptations

Camouflage

Unlike most other venomous creatures that have bright warning colouration, the stonefish remains camouflaged with its surroundings through disguise. As with other stonefishes present in the Synanceiidae family, its original skin colour is actually bright orangey-red, but this is being concealed by an outer epidermal layer that is keratinised. This keratin layer accumulates algae and other fouling organisms — same as those found on the hard substrata where the fish is hiding, forming a thick brown layer. Although the keratin layer occasionally sloughs off, new fouling material would be actively recruited. It was once thought that the accumulation was purely due to the stonefish's sedentary lifestyle. However, it was observed that when the keratinised layer had been sloughed off, the stonefish would stop feeding till its cryptic mode is regenerated (13) (14). Watch the video below to see how well-disguised the stonefishes are. They have blended in so successfully that even other organisms are crawling over their algae covered body.

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Figure 9: The underside of the stonefish, showing its original orangey-red colouration. (Source: Ria Tan)



Video 2: Watch how well-disguised the stonefishes are with the environment, with the attached algae swaying along with the water currents."Estuarine Stonefish (Synanceia horrida)," by kieren curry. Vimeo, 2012.URL: https://vimeo.com/53253179 (accessed 6 Nov 2015)

Behaviours

In addition to being cryptic, the benthos-associated stonefish is solitary and it behaves sluggishly. It is often found lying motionless in cervices, holes, under rocks or buried in mud and sand, only with their eyes and mouth silt protruding out (12). It uses it pectoral fins to scoop up mud or sand to create a shallow depression for it to settle (7).

Movement
The stonefish would infrequently swim about sluggishly, or it could move about the bottom by hopping across the sand or mud using its pectoral fins (12) (13).

Feeding behaviour
This carnivorous stonefish is an ambush predator. Its method of predation is to stay completely motionless, just like how it is usually found, waiting for an unsuspecting prey to swim by. Its diet composes mainly of small fishes, cephalopods and crustaceans (4)(10). It gapes and sucks its prey in and the prey vanishes into its mouth in an instant. This is achieved by expanding their oral cavity. The difference in pressure between inside the mouth and the outside environment results in a suction force, where the prey being vacuumed into its mouth. Watch the video below to see how this is being done:



Video 3: How the stonefish ambush and feed on its prey is explained in this video."You Don't Want to Step on a Stonefish," by Smithsonian Channel. YouTube, 13 May 2013.URL: https://youtu.be/ebK-NtdkuRI (accessed 6 Nov 2015)


Mating behaviour
During mating season, the otherwise solitary S. horrida would aggregate with other individuals. In October 1997, it was observed in Australia that between 25 to 30 individuals were found concentration within a 16m² area. In addition, the females here were found to be larger than the males. Not only were they longer and broader with swollen abdomens, but the average weight of females were also found to be twice of that of the males within the aggregation (15). The mating process involves the females laying her unfertilised eggs in a thick gelatinous mass as she swims across the sea floor. The males would then complete the fertilisation by swimming over the newly laid eggs and releases his sperm over them (10). Females typically take about 3 years to mature and reach a standard length of 170mm to be able to produce eggs (18).

Human interaction

Economic importance

As food source
Despite the venomous properties and danger from capturing and handling stonefishes, they are still commonly used as food. Stonefishes are important fishery resource in the live fish trade. Once captured, they are kept alive and usually air-flown to countries such as Hong Kong and Japan, where the stonefish is considered to be a delicacy (15). When cooked, its flesh is said to resemble that of a crab, and is somewhat fibrous and coarse (12). The Japanese also eats it sliced raw on top of either boiling or deep frying it (22). You can also find this exotic delicacy in some of Singapore's seafood restaurants, serving Hong Kong styled steam stonefish at a price of about $70 per kilogram.

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Figure 10: 'Hong Kong style steamed stonefish' from one of Singapore's seafood restaurant. It is said to have green bones.(Source: Leslie Tay. Rights: Leslie Tay, ieatishootipost. Permission granted.)
Aquarium trade
Adding on to the importance of this stonefish in the live fish trade, they are often also found in the public aquariums and people do keep it as pets in aquariums at home too. As such farming of the estuarine stonefish have also been explored to keep up with the various demand.

The Estuarine stonefish situation in Singapore, past and present

The stonefish is more commonly encountered on our southern shores than our northern shores. In the past, it was reported in 1965 that there were 81 cases of envenomations reported from Pulau Bukom Hospital, Singapore just within 4 years. Back then, there were approximately 7000 people living on Pulau Bukom and its adjacent islands (21). Majority of these injured were fishermen, with injuries sustained mostly to their feet. The full report is published by Phoon & Alfred (1965) (21).

The good news is that there are now lesser envenomation cases in Singapore in more recent years, this could be attributed to our changing coastal landscape. Eight cases were reported from the Singapore General Hospital (SGH) between October 2001 to January 2003. Their injuries were sustained while fishing, swimming or while combing beaches at Sentosa, St John's Island and Changi Point (1). This places the visitors of intertidal areas and recreational beaches at risk and this is a point of concern as more people are being involved in intertidal walks and swimming in recreational beaches for example. Hence, it is important to emphasise the need for proper footwear when visiting areas where stonefishes could potentially be found. Of course, some may find this ridiculous especially in recreational beaches and there was even one victim who sued Sentosa after sustaining a stonefish injury on one of its beaches. This was a case where he unfortunately lost. A series of reports regarding this incident could be found here.

Conservation status

Although they are not listed in the IUCN Red List of threatened animals, they are nonetheless threatened by the increasing amount of anthropogenic activities, such as land reclamation, pollution, over-collection and over-harvesting.


Distribution

Native to the Indo-West Pacific region, the distribution ranges from India to China and all the way south to Australia, including the Philippines, Papua New Guinea and many small island countries like Fiji, Vanuatu and Singapore (10). It was first recorded in Japan in 1997 (8).



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Figure 11: Distribution of S. horrida. (Created with: mapchart.net)

Taxonomic information

Original name

Scornpaena horrida Linnaeus, 1766

Original description

It was first described as Scorpaena horrida by Carl Linnaeus in 1766, in the 12th edition (Volume I, Part I) of his book titled 'Systema naturae sive regna tria naturae, secundum classes, ordines, genera, species, cum characteribus, differentiis, synonymis, locis.'. Found on page 453 of this 532 page book, the description was made based on a specimen found in Ambon, Indonesia (18).


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Figure 12: Screen capture from Systema Naturae where Scorpaena horrida was first described in Latin.

Currently, the accepted scientific name is Synanceia horrida (Linnaeus, 1766). It was transferred to the genus Synanceia in 1859 by Pieter Bleeker, with a type specimen from Singapore (18). It cannot be confirmed if this type specimen is with the Natural History Museum of Leiden, where most specimens collected by Bleeker are being placed at.

Taxonomic rank

Kingdom: Animalia
Phylum: Chordata
Subphylum: Vertebrata
Class: Actinopteri
Order: Scorpaeniformes
Family: Synanceiidae
Genus: Synanceia
Species: Synanceia horrida

Accepted synonym

  • Scornpaena horrida Linnaeus, 1766
  • Synanceia trachynis Richardson, 1842
  • Synanceia horrid (Linnaeus, 1766) (misspelling)
  • Synanceja horrida (Linnaeus, 1766) (misspelling)
  • Synaneceiea horrida (Linnaeus, 1766) (misspelling)

Common names:

Estuarine stonefish, hollow-cheeked stonefish.
Visit this link for the common names in various languages.

Phylogenetics

The Estuarine stonefish belongs to the family Synanceiidae which includes all stonefishes with venom spines. Phylogenetic studies conducted on the spiny-ray finned fishes, looking at venom evolution found that the venom apparatus had evolved 11 times (24). Despite the wide taxonomic range, the venom apparatus and pharmacology of these fishes are very similar (23). From the phylogenetic tree below, we can see that the stonefish is more closely related to waspfish rather than the scorpionfish, where the Estuarine stonefish had first been classified under. For the more complex phylogeny and complete study looking at molecular phylogeny of the spiny-ray finned fishes, you may read up on the paper by Smith and Wheeler (2006) (24).
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Figure 13: A simplified version of the phylogenetic tree showing the clades of venomous fishes. (Source: Ziegman & Alewood, 2015)


While phylogenetic studies have not been specifically done on S. horrida, most studies were conducted on other Scorpaeniformes, with a few which included stonefishes from the Synanceiidae genus. The phylogenetic trees below are from analyses looking at the toxic genes of Scorpaeniformes, where comparisons between toxin genes were made using S. horrida's stonustoxin genes (25). The maximum likelihood and maximum parsimony methods were used. Do note that the relationship as shown here is based on the fishes' toxin genes, showing the evolution of the toxin gene. To find out more, you can read this paper by Chuang & Shiao (2014) (25).

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Figure 14: Phylogenetic analysis of the toxin genes of Scorpaeniformes using maximum likelihood (panel a) and maximum parsimony (panel b) methods. Only bootstrap values above 70% are shown in the figure. (Source: Chuang & Shiao, 2014)



References

1. Lee, J. Y. L., L. C. Teoh & S. P. M. Leo, 2004. Stonefish envenomation of the hand – A local marine hazard: a series of 8 cases and review of the literature. Annals Academy of Medicine, 33(4).

2. "Definition of horridus". Numen - The Latin Lexicon. URL: http://latinlexicon.org/definition.php?p1=1007189 (accessed 9 Nov 2015)

3. Sharma. R. E., 1973. Noxious and toxic animals. In S. H. Chuang (Ed) Animal life and nature in Singapore. Singapore University Press.

4. “Estuarine stonefish, Synanceia horrida,” by Dianne J. Bray. Fishes of Australia, 2011. URL: http://www.fishesofaustralia.net.au/home/species/3751 (accessed on 6 Nov 2015)

5. “Hollow-cheeked stonefish,” by Ria Tan. wildfactsheets, 2013. URL: http://www.wildsingapore.com/wildfacts/vertebrates/fish/synanceiidae/horrida.htm (accessed on 6 Nov 2015)

6. Gopalakrishnakone, P. & M. C. E. Gwee, 1993. The structure of the venom gland of stonefish Synanceja Horrida. Toxicon, 31(8): 979–988.

7. “Synanceia horrida (Linnaeus, 1766),” by Armi G Torres. FishBase. URL: http://www.fishbase.se/summary/Synanceia-horrida.html (accessed on 6 Nov 2015)

8. Yoshino, T., T. Kon & Y. Sakurai, 1997. First record of the synanceiine fish, Synanceia horrida, from Japan. Gyoruigaku Zasshi, 44(2).

9. Ng, P. K. L., R. Corlett & T. W. Tan, 2011. Singapore biodiversity: an encyclopedia of the natural environment and sustainable development. Editions Didier Millet.

10. “Synanceia horrida(stonefish),” by Trevor Olsen. 12 Sep 2013. URL: https://bioweb.uwlax.edu/bio203/f2013/olsen_trev/index.htm (accessed on 7 Nov 2015)

11. Foot, T., 2000. Guinness Book of World Records 2001. Guinness World Records Ltd, 284 p.

12. Halstead, B. W., M. J. Chitwood & F. R. Modglin, 1956. Stonefish stings, and the venom apparatus of Synanceja horrida (Linnaeus). Transactions of the American Microscopical Society, 75(4): 381–397.

13. Sim, W. L. & J. Quek, 2009. Preliminary observational study of colour change in keratinised epidermal layer of stonefish (Model: Synanceia horrida).

14. Fishelson, L., 1973. Observations on skin structure and sloughing in the stone fish Synanceja verrucosa and related fish species as functional adaptation to their mode of life. Zeitschrift für Zellforschung und Mikroskopische Anatomie, 140(4): 497–508.

15. Fewings, D. G. & L. C. Squire, 1999. Notes on reproduction in the estuarine stonefish Synanceia horrida. SPC Live Reef Fish Information Bulletin #5.

16. “STONEFISH ANTIVENOM Product Information,” by CSL Limited. 13 Apr 2011. URL: http://www.csl.com.au/docs/236/440/Stone%20Fish%20PI-%20approved%20April%202011,0.pdf (accessed on 8 Nov 2015)

17. Winkel, K. D., P. Mirtschin & J. Pearn, 2006. Twentieth century toxinology and antivenom development in Australia. Toxicon, 48(7): 738– 754.

18. Kwik, J. B. T, 2011. The biology and ecology of small tropical scorpaenoids inhabitaing shallow coastal habitats in Singapore. (PhD thesis). Retrieved from NUS Scholar Bank.

19. Prithiviraj, N., R. Sasikala & D. Annadurai, 2012. Bioactive properties of the stone fish Synanceia horrida (Thomas, 1984) spine venom. International Journal of Pharmaceuticals & Biological Archives 2012, 3(5): 1217–1221.

20. Gwee, M. C. E., P. Gopalakrishnakone, R. Yuen, H. E. Khoo& K. S. Y. Low, 1994. A review of stonefish venoms and toxins. Pharmacology & Therapeutics, 64(3): 509–528.

21. Phoon, W. O. & E. R. Alfred, 1965. A study of stonefish(Synanceja) stings in Singapore with a review of the venomous fishes of Malaysia. Singapore Medical Journal, 5(3): 158–163.

22. Yamamoto, R. M. Suzuki, S. Hori & N. Aikawa, 2010. Stonefish “Okoze” envenomation during food preparation. The Keio Journal of Medicine, 59(1): 19–22.

23. Ziegman, R. & P. Alewood, 2015. Bioactive components in fish venoms. Toxins, 7(5): 1497–1531.

24. Smith, W. L. & W. C. Wheeler, 2006. Venom evolution widespread in fishes: A phylogenetic road map for the bioprospecting of piscine venoms. Journal of Heredity, 97(3): 206– 217.

25. Chuang, P. S. & J. C. Shiao, 2014. Toxin gene determination and evolution in scorpaenoid fish. Toxicon, 88: 21–33.