“One can state, without exaggeration, that the observation of and the search for similarities and differences are the basis of all human knowledge.” – Alfred Nobel.
Two very different looking snakes, a Freshwater Snake Tropidonophis mairii (Left)& a Brown-Snouted Blind Snake Ramphotyphlops weidii (Right).
Life’s great diversity has long fascinated human kind. As a survival tool, the understanding of the varieties, behaviours, and distributions of the organisms around us has played a vital role in our advancement; from the simple survival of our ancestors, through the beginnings of agriculture when we have learned to mold these natural processes to our benefit, up to our modern global food production systems. With the tools of modern science, we can even use genetics to understand how our early ancestors migrated out of Africa (Lukic & Hey, 2012). Thorough observation, documentation, & analysis of the diversity and variation around us, we’ve improved our understanding of the biological processes driving various population demographics such as birth/mortality rates, immigration/emigration rates, effective population sizes, and much more (see Azose & Rafferty, 2015 for an interesting proposed Bayseian hierarchical modeling method for investigating global human demographics & migration).
In fact, all these processes are going on in one’s own backyard, often home to a wide spectrum of life, even near the city. Here in South-East Queensland, the local diversity is even greater than much of the world; at a glance, my own yard holds eight confirmed species of lizards, two amphibians, a dozen birds, six mammals and innumerable invertebrates. These were all seen within the first 3 months of occupancy in our lovely share-house some twenty minutes from the city center, during the rather inactive winter. There are various fungi, dozens of plant species, and surely a plethora microscopic bacteria, archaea, protists, and viruses throughout the property, not to mention my own personal microbiome, a community of organisms so specific to me that it can be used as a unique identifier (Franzosa et al. 2015). Doubtless, my property’s species count, snakes included, will rise significantly this coming spring.
This amazing diversity is a result of evolution, more specifically the process of speciation by which some form of reproductive isolation separates two populations of an organism for many generations. Perhaps a changing geographic boundary, such as an advancing glacier or continental drift, splits a population of a certain organism in half. As the now isolated populations reproduce over time, new mutations arise with each generation. Many are lost, since random mutations rarely improve such a complicated, interrelated set of systems as a living organism. Our family’s old PC in the ‘90s would hardly have been likely to improve in performance if we randomly doubled one of the components; two “F” keys would seem redundant, as would a second mouse pad on the underside of the keypad, or any massive number or random, more catastrophic changes. However, a doubling of RAM, another USB port, an even slight improvement to the heatsink or fan; such specific changes can of course be massively useful for certain tasks, such as networking with multiple devices or running higher intensity programs, for instance games or data analyses. Many changes, such as the exact colour of paint, might be practically neutral in effect and their numbers in a population therefore vary entirely at random, drifting to higher and lower frequencies. As beneficial and/or neutral mutations accumulate, over time our two populations may become so differentiated as to be unrecognizable to each other; the “original PC” populations diverged down different lineages, one now a portable, lightweight notebook, the other a high performance gaming PC, both adapted over time and small incremental change to suit a specific niche (see Kirk & Freeland, 2011 for a review of neutral vs adaptive genetic markers for molecular ecologists).
As we saw in Essay 6, this process can lead to bursts of diversity and variety in life. More impressively, such diversity often arises in the face of harsh conditions, forcing greater adaptation to specific conditions or environments, and concurrently a greater amount of speciation. One important intellectual trap comes along for the ride with this all this adaptation and diversity; the illusion of progress. This is a very powerful misconception that even biologists have been known to succumb to, particularly in the early days of evolutionary thought. Take the progenitor of Darwin’s theory of natural selection, that of Jean-Baptiste Lammark. While natural selection acts on populations, ‘Lammarkism’ was more concerned with individual behaviour, suggesting that use of a characteristic would cause it to grow, leading over generations to modification of features & greater complexity, while disuse resulted in atrophy and even eventual loss of those features (see 4 for history on Lammark). While many scientists, including Ernst Haeckel and other eminent biologists of the time, preferred Lammark’s progressive, complexity-inducing theory of evolution, the modern evolutionary synthesis (also referred to as neo-Darwinism, or simply the MES) dismisses this idea and gives us another explanation. With such a difficult conceptual wrangle, it pays to be specific; life does not strive towards increasing complexity. Rather, complexity is an accidental by-product, an emergent property of a long, ongoing process of variance, heredity, and survival (for some more contemporary evolutionary reading, see Laland et al. 2015’s discussion on the extended evolutionary synthesis, or EES). The true meaning and importance of this concept is a humbling one, and has some intriguing consequences in the natural world.
It is easy to consider complexity to be the goal of life, the direction in which evolution drives us. We tend to think of evolution increasing the complexity of organisms over time from simple, single celled cyanobacteria through to the exquisite intricacy of the human mind. What else could produce such an organ, capable of not only designing computers, but of conceptualizing theoretical populations of computers mutating through time then communicating this concept through a network computers to others? Our animal brethren further paint a picture of complexity, from wing structures to various mouthparts and more. Nonetheless, evolution is in fact not a race towards complexity. It is simply the struggle of genes to copy and replicate themselves, a self-sustaining chemical momentum which just happens to manifests as intelligent, spacefaring organisms with the overwhelming desire to survive and reproduce.
If complexity is not the goal, why the apparent trend towards increasing complexity? Here we come to the crux of the matter. Upon further examination, what in fact is increasing is the amount of variation in overall complexity of forms. As the variety of lifeforms on the planet increases, the number of “complex” animals will also incrementally grow. The variety of simpler forms will also increase, but less noticeably to us large, lumbering apes (see Hinchliff et al. 2015 or follow this link to explore the diversity in the biggest current species tree for Earth’s of 2.3 million animal, plant, fungi and microbe species tree.opentreeoflife.org). In fact, there is a lower limit to life’s complexity at the level of the single cell (aside from viruses, however their “alive” classification is up for debate…another day), whereas it is very possible to increase complexity by adding cells until gravity catches up and the skeleton can no longer support the body’s own mass. This is why large cetaceans, whales and their relatives, live in the ocean where buoyancy supports their body weight, allowing them to grow truly massive (see Herráez et al. 2013)
The “spread of variation” in complexity can only grow as the number of organisms increases, since life cannot get less complex than one cell. This is known as a statistical wall; the spread of life’s complexity somewhat “left-skewed”. Let us use mass as a proxy for complexity, at least in terms of the number of individual cells. The majority of species, by a vast number, are microbial. If we were to graph the sizes of all Earth’s species, the curve would rapidly rise, peak, drop off and continue to tail off slowly to the giants who are few and far between. Very few species are at the smallest end of the spectrum, the vast majority are small, after which species become both larger and progressively less numerous, with very few species of very large, complicated animals ever evolving, particularly when compared to the massive numbers of small fishes, insects, and other small fauna, let alone microorganisms. Arguably, life is dominated by the bacteria. Single celled organisms exist in practically every niche possible already, constantly adapting and colonizing new niches as their environments change (see 7, the incomparable Stephen J. Gould’s ‘Life’s Grandeur: The Spread of Excellence From Plato to Darwin’). Snails, whales and people are just lucky, incidental products of variation in form.
With this in mind, the idea of increasing biological complexity becomes simply another spread of variance over time, rather than a driving trend with some causal mechanism or goal. Evolution is left unhindered by our ideas of progress, complexity, or design. What a delightful side benefit our human consciousness is! But can we truly say that evolution really doesn’t aim to increase complexity? The above tirade offers no proof, only concepts, and we must make that right immediately, if we can. How can we demonstrate that life has no intrinsic trend to complexity, that life’s complexity is a consequence of variance rather than a directional trend?
Let us examine the idea of direction. The “trend hypothesis” supposes complexity increases over time. What about a change in direction towards simplicity in favour of some other selective advantage? Do animals de-evolve? It seems counter-intuitive, however many cases of selection for simplicity exist in nature. Snakes themselves evolved from lizards and still show leg-bud formation during early embryological development like many other reptiles, yet they have lost their “complicated” limbs for a simpler form of locomotion (Boughner et al. 2007). The only remaining evidence is in the form of spurs near the cloaca of the ancient pythons and boas, vestigial remnants of hip and leg bones no longer in use, except perhaps for courtship purposes (see link 9). Marine mammals like the aforementioned also once lived on land, becoming fully marine creatures over time and many such as whales and dolphins also possess vestigial hip bones. Surely these could all be considered reductions in complexity of design, no?
Without looking any further than the snakes (the suborder Serpentes) we can find more examples of reduced complexity. The blind snakes, for instance, are about as reductive in form as snakes come, with eyes all but lost through generations of living underground eating nothing but ant eggs, now little more than pigment spots underneath the head scales with severely retarded photoreceptive ability. This is not just a couple of random individuals, but by four separate families of blind snakes grouped in the infraorder Scolecophidia, represented in Australia by the most common and specious family, Typhlopidae (Webb & Shine, 1993). Another fantastic example of reductive evolution, the marbled sea snake Aipysurus eydouxii, also occurs in Australia. Despite being sister to some of the most highly venomous Hydrophiine sea-snakes on the planet, it has decreased in size, and lost its venom production glands, fang development, and connective ducts which make up the venom delivery system, in lieu of a new egg-eating lifestyle (Li et al. 2005). These smaller snakes prefer to eat fish eggs off the reefs and rocky crevices they inhabit than chase their prey, thus over time any mutations which reduced the amount of developmental energy spent on a now defunct venom system were highly advantageous. Over time, venom proteins were truncated by mutations, rendering them non-functional, and the associated systems degenerated over the years as new offspring found no more use for the highly complicated three-finger neurotoxic peptides which their ancestors used to hunt (Li et al. 2005). These caviar eating miniatures had found a new, less complicated, but highly successful niche and adapted to it over time, a process still ongoing today.
Complexity is a complicated subject. Duh. Biological complexity even more so, however despite the apparently ubiquitous nature of complex structures in the living world, we mustn’t get carried away in the flood. An objective, measured look at the nature of things shows us that our pre-conceived notions of how life’s complexity “should” arise are more than likely another one of nature’s little tricks on us. We are designers. We are also surrounded by complex life-forms, an interconnected, technological society, and an information sphere to share our complicated ideas on. We humans are somewhat obsessed with complexity & design. This is not necessarily a fault or a judgement, for in our pursuit of understanding the complexity of the universe we advance ourselves & our society. But we must not let the illusion of design in nature colour our understanding of life. Instead, we should work our faulty monkey-brains hard and to view it as a product of variation and spread, rather than a relentless drive towards complexity.
References
Lukic S, Hey J (2012) Demographic inference using spectral methods on SNP data, with an analysis of the human out-of-Africa expansion. Genetics. 192(2):619-39.
Azose, JJ, Raftery, AE (2015) Bayesian Probabilistic Projection of International Migration. PNAS. 52:1627–1650
Franzosa EA, Huang K, Meadow JF, Gevers D, Lemon KP, Bohannan BJ, Huttenhower C. (2015) Identifying personal microbiomes using metagenomic codes. PNAS. 112(22):E2930-8.
Hinchliff CE, Smith SA, Allman JF, Burleigh JG, Chaudhary R, Coghill LM, Crandall KA, Deng J, Drew BT, Gazis R, Gude K, Hibbett DS, Katz LA, Laughinghouse HD 4th, McTavish EJ, Midford PE, Owen CL, Ree RH, Rees JA, Soltis DE, Williams T, Cranston K (2015) Synthesis of phylogeny and taxonomy into a comprehensive tree of life. PNAS. 112(41):12764-9.
Herráeza P, de los Monterosa AE, Fernándeza A, Edwards JF, Sacchinia S, Sierraa E. (2013) Capture myopathy in live-stranded cetaceans. The Veterinary Journal. 196:2, Pages 181–188
Gould SJ. (1996) Life’s Grandeur: The Spread of Excellence from Plato to Darwin. Harmony Books OCLC: 35359843
Boughnera JC, Buchtová M, Fu K, Diewert V, Hallgrímsson B, Richmana JM (2007) Embryonic development of Python sebae – I: Staging criteria and macroscopic skeletal morphogenesis of the head and limbs. Zoology. 110: 3, Pages 212–230.
Webb JK, Shine R. (1992). Prey-size selection, gape limitation and predator vulnerability in Australian blindsnakes (Typhlopidae). Animal Behaviour. 45: 6, 1117-1126
Li M, Fry BG, Kini RM (2005) Eggs-only diet: its implications for the toxin profile changes and ecology of the marbled sea snake (Aipysurus eydouxii). J Mol Evol. 60:1. 81-9.
“Without a struggle, there can be no progress.” – Frederick Douglass.
Newhaven Sanctuary, Northern Territory (Photo by Guy Drory – Muse)
Australia is, perhaps surprisingly with our outdoorsy reputation, a difficult landscape for agriculture. One imagines the country, at least on the greener fringes, growing bountiful crops of fruits and vegetables, large cattle herds and sheep flocks interspersed with a lush green pasture under the hot sun and blue sky. Unfortunately this European ideal is quickly challenged anywhere aside from some of our more exceptionally productive south-eastern fruit-bowl regions. Agriculture collectively makes up less than 3% of our GDP, and while this figure is somewhat a reflection of our growing service industry, it seems lower than expected for our wide, open land, particularly compared to our neighbour New Zealand’s near 6% agricultural GDP (http://www.nff.org.au/farm-facts.html). This is not just due to our inhospitable terrain and ephemeral, somewhat unpredictable rainfall patterns. Though our national anthem sings the praises of Australia’s “golden soils”, in reality our soils and oceans are among the most nutrient poor and unproductive in the world (McBratney et al. 2016). While this is not the generally espoused picture of the country, it fits in with the much older narrative of the continent, tied to an ancient Gondwanan ancestry.
Despite the substandard soil quality of much the continent, Australia is home to a massive diversity of fauna. As of 2012, there was a whopping 946 known reptile species. This includes two crocodiles, over thirty turtles, around 700 lizards, and nearly 200 snakes (Wilson & Swan, 2012). We’re also home to a further 900 or so birds (Dolby & Clarke, 2014) and nearly 400 mammal species, including our plethora of well-known marsupials (Van Dyck et al. 2013). How can such a barren land be home to such a huge amount of animals, yet has an ongoing struggle to support our growing food demands? We in fact have one of the lowest land area to food production ratios of any nation. Fertilizer is basically a given in Australian agriculture. Both the CSIRO and various scientist have described our soils as ‘hostile’ to agriculture, citing a long list of deficiencies including low organic matter content, either hard-setting, acidic, or water repelling topsoils, subsoils that are saline, sodic, highly acidic or alkaline, toxic concentrations of elements, poor soil structure, and more (McBratney et al. 2016). Yet the continent was once, albeit during a warmer, wetter period of our climate history, a land of lush rainforests and greenery as far as the eye could see (Martin, 2006). A more contemporary representation of our landscape might contain Uluru, the giant rock towering ochre-red in the clear desert sky, surrounded by an unending sea of red sand and spinifex bushes peppered by occasional bloodwoods and desert oaks, somewhat inhospitable at first take. What happened to the vast, ancient rainforests which once covered the land? And why do we now live in a land that seems paradoxical; a continent of low productivity, yet with a great diversity plant and animal species throughout?
To understand how such a richness of species arose in such a dearth of resources, we must first understand how those resources were lost, for the same process is at work in both. As a first step, let’s see if we can determine what the continents looked like back when we still had these great rainforests. How do we know they existed in the first place? Through the fossil record; petrified wood, leaves and leaf prints in sediments, ancient preserved pollen in lake sediment core samples, fossilized fauna and their dietary specializations and more, all give us a picture of Australian landmass years ago (Flannery, 1994; Hummel et al. 2008; Sniderman et al. 2013). More than that, our understanding of plate tectonics tells us that Australia was not yet a separate continent at that time (Kumar et al. 2007). We were part of the Gondwanaland continent, still attached to South America and Antarctica, slowly being separated as rift valleys formed between the spreading continents.
Plenty of evidence points to this ancient Gondwanan origin, such as the Hoop and Bunya Pines of the genus Aracauria which occur on our East coast. This ancient genus of so-called “monkey-puzzle trees” evolved in the early Mesozoic era and spread very successfully (Kershaw & Wagstaff, 2001). Forming global forests when the continents were joined, they thrived into the late Jurassic period, after which they began suffering heavy losses likely due to a cooling and drying climate. Occurring in the northern hemisphere until the late Cretaceous period (~70 MYA), they have now retracted in species range and number significantly, except for small remnant fragments isolated by the shifting of the continents. While they are found in New Caledonia, New Guinea, and few islands off Australia’s coast, the genus is otherwise restricted to our eastern mainland (more so to the north) and South America. Their Gondwanan origins, however, can be seen in both their contemporary biogeography and the fossil record, including Late Jurassic/Early Cretaceous samples from Hope Bay, Antarctica (Gee, 1989).
In the mid-Jurassic period, some 170 million years ago, the supercontinent Gondwanaland was starting to fragment into what we call Africa, India, Antarctica, South America, and Australia (or more precisely, the continent of which Australia, PNG, and other small surrounding islands are part of, known as Meganesia). Australia and Antarctica remained connected for some time, as did Antarctica and South America, allowing for fauna and plant communities to intersperse, until they finally broke up in the Paleogene, a comparatively recent 45 million years ago. It seems Antarctica was a longstanding conduit, sometimes disconnected, between ancient South America and Australia, with fossil Araucaria samples found from the Antarctic potentially dated from the Jurassic to the Eocene (Cantrill & Poole, 2004).
Living marsupials similarly are found only in Australia/PNG and the Americas, aside from a few species from surround islands, as are other ancient plant and animal species. Through great effort and determination, mammal fossils are found through much of South America, and have also been found from the Seymour Islands in Antarctica (Reguero et al. 2002). I was personally shocked and delighted to learn that the fossil dentition of a large, voracious, tooth-bearing platypus were uncovered not in south-eastern Australia, but in South America, our apparent long lost sister continent along with Antarctica (Pascual, 1992). One migrated westward and north, splitting from Africa and India, the other to the frozen southern pole. What then is the story of Australia, last Gondwanan child?
While our continental siblings were off travelling after the split of our Gondwanan family, one needed some convincing to leave home. Australia has moved very little, and continues to trek northward relatively slowly, at a rate of 2-3cm/year, compared to 5cm/year for India, which at its peak was trekking across the globe at around 20 cm/year (Kumar et al. 2007.). While the Antarctic shot down south and now barely moves and most of the other continents play bumper cars with each other, Australia has remained rather stable, both geologically and climatically. We’ve remained in a fairly mild, mid-latitude region, a Goldilocks-ian temperate/sub-tropic/tropical area. Even during the Pangean and Gondwanan breakups, the landmass that was to become Australia moved little when compared to other continents.
Devoid of other continental shelves to batter us, our isolation further promotes geological stability, with fewer earthquakes, rifts, and volcanoes tearing at our land than other parts of the world. That is until many millions of years from now when we come crashing into Papua New Guinea, forcing their epic mountain ranges even higher, as India did some 50 million years ago, forming the Himalayas. Our geological history is one of stability, which sounds nice, but over time can get rather boring. After millions of years, it can deplete a continent of nutrients. Such was the story of our landscape. Soils need activity; earthquakes cause cracking, turnover and cycling of soil layers, volcanoes and other geological activity are essential for maintaining soil nutrition (Flannery, 1994; Martin, 2006; McBratney et al. 2016). Even climate change is a factor, with glacial advancement pushing depleted topsoils and sediments into surrounding oceans, leaving renewed soil once glaciers recede in interglacial periods. Such glacial renewal has not occurred in Australia for perhaps 300 million years (Twidale & Campbell, 2005).
With this history in mind, the diversity of Australian fauna can now be tackled. We return to the question; how do we draw such biodiversity from such an infertile landscape? The answer is intriguing. For life responds to challenges in ways that we would not expect. In times of harshness and challenge, populations and species are under greater selective pressure. Each offspring has a lower chance of survival and breeding, thus if it is successful it beats the odds and its genes will be selected for rather strongly (Subramanian, 2013). Taken to the extreme, for example, if out of 100 only 1 male gets to breed because all the others die off, that individual’s gene’s in the next generation will significantly increase in relative frequency. This chance spread of genes through a population is known as genetic drift, and in smaller populations genetic drift can act faster, encompassing an entire population in what is known as “fixation”, creating a new norm. In larger populations, the effect of genetic drift on frequencies is reduced, selection playing a greater overall role.
In the nutrient poor landscapes such as post-Eocene Australia, there was likely “fitness-premium” on one factor for survival; energy efficiency (Flannery, 1994; Parsons, 2005). Who can best exploit which small quantity of which rare nutrient? Which species’ lifestyle has the least impact on local nutrients, as to not compete with its own offspring next generation? What is the most efficient mode of reproduction/locomotion/diet? Which species can collaborate most successfully? Australian species had to answer these challenges over time as resources dwindled, and since these resources are also unevenly scattered, this leads to a mosaic landscape of various ecological niches with very specific energy requirements for their inhabitants (Flannery, 1994). But species here have had plenty of time, without significant change in their overall climate, to adapt, filling these various diverse niches with amazingly diverse species (Martin, 2006; Sniderman et al. 2013).
This is the context in which our flora and fauna has evolved. As such, energy efficient animals are generally more successful. Placental mammals, with their higher metabolic rates, breeding output, food and energy requirements, aren’t well equipped to this challenge, however the slower paced monotremes and marsupials were more successful, with generally lower energy expenditure on metabolism (Basal Metabolic Rate around 75% of an equally sized placental) and reproduction (Garland et al. 1988). Over time, as these marsupials adapted to the landscape they became even more efficient, adopting various calorie saving strategies such as hopping locomotion, using potential energy stored in elastic tendons to bounce rather than walk, or embryonic diapause, the ability to stop development of an embryo, maintaining it until better conditions arrive, then continuing gestation. Dietary specialization was widely adopted, with few generalists surviving. Birds also did well, with their ability to glide minimizing energy use, but high metabolic rates restrict many lineages, certainly hummingbirds and such, from the continent. There simply aren’t enough flowers or enough nectar to supply their high demands.
Of course, the ecosystems and the reptile fauna of early Australia was very different from today. Australian Megafauna, animals over 45kg, were common at one point, such as Zaglossus hacketti, a sheep sized echidna, the giant-wombat-like Diprotodons, and various giant kangaroos (Flannery, 1994; Musser, 2003; Saltré et al. 2016). While this seems counter intuitive, a large bodied animal can be more efficient due to scaling laws of mass; smaller animals use more energy since a larger fraction of the body is “structural mass”, containing highly active organs etc., and less “reserve mass” as in larger animals. Larger fauna also have a lower surface to body mass ratio, thus lose heat overall slower. Feasting on these were terrestrial crocodiles, fast paced predators running prey down, stalking across the landscape like monitor lizards do today. Monitors were also present and huge, Varanus priscus for instance growing to seven meters and nearly 2,000kg, the biggest lizard ever. With the demise of the megafauna soon after the arrival of modern humans some 60,000 years ago (Saltré et al. 2016), smaller reptiles and marsupials have increased in abundance.
Reptiles of course did extraordinarily well, in particular the lizards. Their broad range of lifestyles and low energy expenditure makes them ideal to adapt to such an environment (Andrews & Pough, 1985). Thanks largely to the physical and intellectual tenacity of dedicated ecologists such the prolific Eric R. Pianka, we know that in Australia’s low resource natural economy, particularly the sandy deserts, lizard species have developed overlapping, co-adapted lifestyles to minimize competition with each other. In some areas, 20 species may live in the same habitat, exploiting subtly different microhabitats and niches, and this specialization has over time lead to a great diversity of skinks, monitor lizards (a.k.a. goannas), dragons, geckoes and legless lizards, more than anywhere else on Earth (Pianka, 1973; Wilson & Swann, 2014). Moreover, it seems our lizard fauna, despite their massive diversity, have less “niche overlap” than other continents, utilizing every possible niche dimension (active period, habitat, food choice), and occupying a much broader niche space overall; they use a greater diversity of resources and lifestyles to survive (see Pianka, 1973, for a summary of over a decade of ecological observation of these diverse, remote, sandy-desert lizard communities, the most comprehensive study of lizard communities in the world).
Snakes are a more recent arrival, both to Australia and to the animal world in general, having evolved from lizards late in history. There were in fact snakes present during the time of the megafauna, however they weren’t the modern snakes we know today. The Wonambi genus, known from two species from Australia’s Riversleigh fossil deposits in Queensland, W. naracoortensis and W. barriei (Scanlon, 2005). Both were large, python-like constrictors, members of the Madtsoiidae family, one of the most successful and diverse snake families to have existed, once occurring throughout much of Gondwana. The two species of Wonambi survived well into the age of modern snakes, some 50,000 years ago, the last of the Madtsoiid snakes. Modern snakes belong to a variety of recently derived families, and here the systematic arguments often begin.
What most can agree on is that the Australian Elapids, front-fanged snakes which includes the vast majority of Australian species (Family Elapidae), and others such as cobras, kraits, and coral snakes across the globe, are a rather recent arrival, yet there are around 100 species currently known and new species are still being discovered and re-assigned from current taxa (Wilson & Swan, 2014). It’s the largest and most diverse of the Australian snake families. Moreover, molecular evidence indicates that these species all arose within the last 10 million years, most inter-generic splits occurring sometime between 10 and 6 million years ago (Sanders et al. 2008). It seems the first Australian front fanged snakes were similar to SE Asian coral-snakes, arriving by island hopping and land bridges to a land devoid of venomous snakes. Their successful spread over the continent, adapting to various microclimates, exploiting whatever small niche available, led to the great evolutionary radiation of lineages we see in the molecular data and the diversity we see today. Setting an even faster pace, the over 40 species of Hydrophis sea-snakes arose within the last 5 million years. These true sea snakes (Hydrophiini) evolved from the Elapidae very recently themselves, and seem to have further ramped up the speciation rate, a story for another time.
And so, with resources few and far between, plants and animals in this ancient continent are limited by energy. Rather than eek out a feeble, menial, uniform existence on what little there is, a great variety of organisms evolved to exploit whatever variety of resources and niches that were available (Pianka, 1073). The driver of evolution is random mutation followed by selection. Thus the solutions to life in these various niches were random, variable, and very different from each other in many cases, yet as they all arose alongside each other to exploit specific niches, or to overlap in broad niches successfully, they co-habit in a surprising harmony of commensal interrelationships.
An example; another broad spectrum of diversity is found in Australia’s ant fauna. We in fact have such an great abundance of ant species that they are frequently used as ecological indicators of the biological health of communities, with over 45 studies examining how species and functional groups can be used to assess disturbances (Hoffman & Andersen, 2003). With such a great abundance and diversity of ants, we have a large number of blind snake species as well; small, blind, noodle-like creatures who live underground eating ant eggs (Shine, 1980; Wilson & Swan, 2014). The sole Australian genus, Ramphotyphlops, containing 42 species of around 150 total globally, is itself an example of an evolutionary radiation on our stable, low resource continent. Each of these 42 species feeds on only a few species of ant eggs, again, specializing in an under-exploited resource. However it doesn’t end there. Evolution bequests us five more snake species, the aptly named Bandy-Bandy genus Vermicella, most possessing conspicuous black and white bands, all which exclusively eat blind snakes (Shine, 1980; Wilson & Swan, 2014). Aside from one species, most are restricted to small, isolated distributions and feed on a very specific set of blind snakes found locally. What a neat little trophic cascade of organisms, finding ways to survive and, in fact thrive, in a landscape of struggle.
Thus, from the poor depleted soils, because of time, stability, and the nature of niche adaptation and evolution, we have the bounty of diversity that is Australia’s fauna. However we must keep in mind that this richness of species, which we as Australians are lucky to live among and share the environment with, is, to continue our “resource economy” mindset, somewhat of a trade-off. Let us be the auditors of our biodiversity for but a moment, and cast an eye on future prospects. In this richness of species, we perhaps lose some security, for a more productive resource economy such as Europe lacks some of our diversity but makes up for it in abundance of animals and plants which we intrinsically lack. Our isolated pockets of specialized resource-miser species must remain small in number or start out-competing a neighbour, eventually taking their niche and that of others along the way, leaning ever so slowly towards instability, over-exploitation and resource collapse. Therefore traditionally, our species and communities lean towards co-adaptation, efficiency, and small population size. Perhaps we should place a similarly high value on these ourselves. It certainly seems to have been paying off for other Australians for quite some time.
Sniderman, J.M.K., Jordan, G.J., Cowling, R.M.(2013) Fossil evidence for a hyperdiverse sclerophyll flora under a non–Mediterranean-type climate. Proc Natl Acad Sci USA. 110(9): 3423–3428.
Kershaw, P., & Wagstaff, B. (2001) The Southern Conifer Family Araucariaceae: History, Status, and Value for Paleoenvironmental Reconstruction. Annual Review of Ecology and Systematics. 32: 397-414
Gee, C. T. (1989) Revision of the Late Jurassic/Early Cretaceous flora from Hope Bay, Antarctica. B 213, 149–214.
Cantrill, D.J. & Poole, I. (2005) A new Eocene Araucaria from Seymour Island, Antarctica: Evidence from growth form and bark morphology. Alcheringa An Australasian Journal of Palaeontology 29(2):341-350
Pascual, R., Archer, M., Ortiz Jaureguizar, E., Prado, J.L., Godlhelp, H. and Hand, S.J, The First Non Australian Monotreme: an Early Paleocene South American Platypus (Monotremata: Ornithorhynchidae). Platypus and Echidnas. The Royal Zoological Society of New South Wales, Sydney, Australia, pp.2-15
Twidale, C.R. & Campbell, E.M. (2005) Australian Landforms: Understanding a Low, Flat, Arid, and Old Landscape, Rosenberg Publishing Pty Ltd.
Subramanian, S. (2013) Significance of population size on the fixation of nonsynonymous mutations in genes under varying levels of selection pressure. 193(3):995-1002.
Parsons, P.A. (2005) Environments and evolution: interactions between stress,resource inadequacy and energetic efficiency. Biol Rev Camb Philos Soc. 80(4):589-610.
Garland, Jr.T., Geiser, F., Budinette, R.V. (1988) Comparative locomotor performance of marsupial and placental mammals. J. Zool., Lond. 215, 505-522
Musser, A.M. (2003) Review of the monotreme fossil record and comparison of palaeontological and molecular data. Comp Biochem Physiol A Mol Integr Physiol.136(4):927-42.
Saltré, F., Rodríguez-Rey, M., Brook, B.W., Johnson, C.N., Turney, C.S.M., Alroy, J., Cooper, A., Beeton, N., Bird, M.I., Fordham, D.A., Gillespie, R., Herrando-Pérez, S., Jacobs, Z., Miller, G.H., Nogués-Bravo, D., Prideaux, G.J., Roberts, R.G., Bradshaw, C.J.A. (2016) Climate change not to blame for late Quaternary megafauna extinctions in Australia. Nat Commun. 7: 10511.
Andrews, R.M., & Pough, F.H. (1985) Metabolism of Squamate Reptiles: Allometric and Ecological Relationships. Physiological Zoology. 58, 2, pp. 214-231
Pianka, E. (1973). The Structure of Lizard Communities. Annual Review of Ecology & Systematics. 4: 53-74
Scanlon, J.D. (2005) Cranial morphology of the Plio-Pleistocene giant madstoiid snakeWonambi naracoortensis. Acta Palaeontologica 50(1), 139-180.
Sanders, K.L.,Lee, M.S., Leys, R., Foster, R., Keogh, J.S. (2008) Molecular phylogeny and divergence dates for Australasian elapids and sea snakes (hydrophiinae): evidence from seven genes for rapid evolutionary radiations. J Evol Biol. 21(3):682-95.
Hoffman, B.D, & Andersen, A.N (2003) Responses of ants to disturbance in Australia, with particular reference to functional groups. Austral Ecology. 28, 444–464
Shine, R. (1980) Reproduction, Feeding and Growth in the Australian Burrowing Snake Vermicella annulata. Journal of Herpetology. 14(1):71-77
“There is something of the marvelous in all things of nature.” – Aristotle
“Men argue. Nature acts. ” – Voltaire
Coral bleaching is ugly. A stark contrast to the vibrancy of living reefs, bursting with life and flashes of fishy colours against vivid coral backdrops, the bony-white, seemingly skeletal remnants of bleaching events are a true, visible impact of global warming. The current sweep of coral die offs this year, including the over 90% bleaching in parts of the World Heritage listed Great Barrier Reef (GBR here on), from Cairns to Papua New Guinea, are strong indicators of things to come (1). Coral bleaching is caused by warming waters forcing the symbiotic microbes or “zooxanthelae” (a colloquial term for the genus Sybiodinium), which live within the coral endoderm and provide nutrients through photosynthesis, to abandon the coral on mass, perhaps seeking a more suitable home (2). With them goes the nutrient production they provide, leaving bleached coral frames and the living coral builders or “polyps” themselves, which will die unless cooler waters and zooxanthelae return. These events are a truly tragic loss. We may lament the loss of biodiversity, the numerous species which depend on the reef for food, shelter, nurseries for young and so forth, many now potentially at risk. We may lament the impact on local coastal communities, many who rely on ecotourism or commercial fishing, both heavily reliant on the reef. We may lament the aesthetic loss of a living marvel, the GBR, the largest living structure in existence, visible from space, drained of its colour and richness. The list continues.
With an undeniably vast scientific consensus, addressing changing global climate change is finally on the table, several decades after the first warnings were published (3). The agreements reached at the 2015 United Nations Climate Change Conference, while not as urgent as many deem necessary, placed climate change policy on the global stage (See 4 for the New York Times’ full coverage). The Paris Climate Accord and all of its signatories have made a powerful statement, many nations agreeing to a target of keeping global temperature increases below 1.5°C. Unfortunately here in Australia the message was ignored. Our latest federal budget in May 2016, has no increases for the Emissions Reduction Fund, an essential part of the current LNP government’s questionable Direct Action policy on climate (5). While $171 million has been earmarked for conserving the G GBR, this will all focus on improving water quality, minimizing invasive species, and so forth. Although these local improvements increase resilience, it will all be useless if warming waters aren’t addressed.
Conversely, other conservation areas have been cut, with $483 million simultaneously cut from the LandCare program over the next five years. Massive sweeping losses were announced to the CSIRO, Australia’s crown jewel of research and scientific innovation, in particular to the climate science sectors, causing outrage in the global science community, even a public plea from NASA to reconsider (6). Subsidizing conservation projects in one area by compromising the integrity of others, while failing to address the main cause of the problem and dismantling climate science departments, seems a less than ideal for climate progress. So does building the world’s biggest coal mine, for that matter, yet this is our current government’s plan for Queensland’s Galilee Basin, despite continuing declines in coal prices, repeated warnings about financial viability from Queensland’s own Treasury (7), and the large and growing numbers of vocal dissenters including indigenous owners, the Wangan and Jagalingou, who depend on of these traditional homelands and ecosystems.
In a more recent disgrace to Australia’s environmental reputation (8), the Turnbull government took a rather Orwellian response to a joint publication from Unesco and the Union of Concerned Scientists, entitled “World Heritage and Tourism in a Changing Climate”. After reviewing the document, the Australia’s Department for Environment apparently took issue with the factual reporting of threats to the environment, particularly the full chapter dedicated to the Great Barrier Reef, as well as sections on the horrendous treatment of Tasmanian old growth forests and the Northern Territory’s unique Kakadu region. All mentions of Australia were removed from the report, an act of screening the likes of which has never been perpetrated by any members of the UN, showing the Turnbull government’s uniquely dishonest climate position. The claim of protecting the precious ecotourism industries of these areas is particularly underhanded, shortsighted, and ultimately illogical; there will be no tourism without addressing threats to environment and climate.
While incompetence in the face of the challenge is troubling, particularly those still clinging to the climate-denial raft (9), many of us can do little more but yell from the couch until the next elections. I am rather couch bound lately by medications (though my lucidity, of course, never in question…), and shall be ranting from a prone position for a while! Rather than wallow in political ineptitude and restorative boredom, I propose we take this opportunity to discuss climate and, naturally, reptiles. Namely, how will reptile communities, and other organisms, respond to climate fluctuations, and what does this mean for their future? This is no trivial subject. How organisms respond (or not) to climate change is an essential driver of change in Earth’s biogeography (10), particularly important if we fail to curtail emissions and transition to renewable energy. How do we study the response of various organisms to a changing global climate? Can we predict how our biosphere, including our reptile fauna, will react?
One of the first challenges is to determine what makes a species sensitive to climate variation. Luckily, we ourselves need not leave the couch on this one, as the research is extensive. Literature on the subject suggests factors can include, but are not necessarily limited to, whether the species is generalist or specialist, aspects of physiology, life-history, habitat sensitivity, dispersal ability and surrounding landscapes, dependence on disturbance, climate-dependent relationships, interacting non-climatic stressors, and more (11,12). This information could be used to assess to which degree various species are susceptible to perturbations in temperature or other impacts such as changed rainfall conditions (13). While making any sense of this might seem to require a savant-like understanding of the ecology of every organism, a talent for database mining may perhaps serve better. Utilizing software or novel programs to search through published scientific works, tabulating desired statistics for target groups, is the preferred method.
Such studies tell us much about what species and groups are sensitive, however the actual vulnerability to climate change involves a more complicated relationship between sensitivity, adaptive capacity to change, and level of exposure to climate impacts. By mapping the distributions of organisms against predicted global climate impacts, sensitivity and adaptability can be compared to local threats, giving a better account of vulnerability globally (14). While there are many underlying assumptions in these studies, from the accuracy of the ecological traits assessing sensitivity to uncertainties in the climate simulation methods, these problems are somewhat unavoidable, but not unmanageable. Climate change research does have a tendency to rely on models; how else can one make predictions of such complicated, temporally dynamic systems? In fact, it appears that over the last ten years, about 55% of all scientific research papers involving computer modelling were in some way climate related (15). Our uncertainties are somewhat mitigated in various ways, like increasing samples size, looking for correlations in responses across groups, using multiple analytical methods and comparing the results, and statistical significance tests (see 16, Flannery, 2005, chapter 16. Model Worlds, for an engaging discussion on climate and models.) While this reliance on simulation and modelling seems like weak footing, there are few other options than to interpret results with caution, and as the models themselves improve with time and the diligent efforts of scientists, so do the monitoring and survey methods to validate them (16, 17, 18)
Reptiles are more reliant on environmental temperatures than mammals and birds, despite their generally wider thermal tolerance. This is particularly so at the margins of their ranges where they are likely to already be near some adaptive threshold (too hot, too cold, or perhaps just too much competition at from neighbours). Reptiles and amphibians are also less capable of long distance dispersal than other fauna, less able to migrate to more suitable habitats (13). For example, when various future climate models are applied to the reptile communities of southwest Europe’s Iberian Peninsula, a biodiversity hotspot, results suggests that while certain species may manage, adapting or expanding to historically cooler localities or newly accessible ranges, extinction is likely for at least 13 of the 37 species included. In an assessment of threatened terrestrial species, Australia’s reptiles also appear to face an unstable future (13). Despite the most climate vulnerable species in Australia being the mountain pygmy possum, Burramys parvus, birds and mammals are less at risk than plants, amphibians, and reptiles. Reptiles require daytime refuges or habitats with a temperature gradient for homeostasis, as well as environmental features such as burrows, rock/timber shelters, and certain vegetation and prey types. Such specificities narrow an organism’s adaptive options.
Already there appears to be broad changes in phenology, the timing of seasonal behaviours, such as breeding, flowering, or hibernation, around the globe. Many species in the temperate zones show an average shift in spring events to 5.1 days earlier per decade (19). This was published in 2003, hardly new information, and our climate has warmed further since then, to 1.22°C above the long-term 20th century average. One Australian reptile showing such phenological change is Tiliqua rugosa, a truly enigmatic creature a.k.a. the shingleback, sleepy lizard, bobtail, and other charming monikers. Breeding pairs are monogamous, meeting at the same location at the start of breeding season, a season which over 15 years of field observation has been commencing earlier and earlier (20). Similar early onset breeding is common in other organisms, and while potentially a reproductive boon, perhaps allowing for additional litters in a season for example, breeding cycles can become unsynchronized from necessary seasonal resource availability, leading to more failed breeding attempts (21, 22). Though some reptiles may be able to track their optimal environment, or in fact receive a fitness improvement from earlier seasons, more have suffered declines in population size and fitness, even local or global extinction events (23).
Aside from phenology, studies showing range contractions and population declines are also emerging. Significantly affected are those unable to migrate, perhaps due to lower intrinsic dispersal ability (do they crawl, run, or fly?), or due to geographical dispersal barriers such as mountain ranges, or man-made barriers like roads and walls (11; 24). Isolated alpines species are particularly vulnerable, like the aforementioned mountain pygmy possum (B. parvus, 11), however reptiles can be similarly restricted. The New Mexico ridge-nosed rattlesnake (Crotalus willardi obscurus), is such a species, trapped by its preference for colder, higher altitudes exclusively in the Madrean Sky Islands, cool, isolated pine-oak forests atop mountain ranges bordering the US and Mexico. So cool-adapted are C. w. obscurus that they’re are unable to cope below certain elevations, the intervening arid lowlands too hostile to traverse to more suitable habitat (25). As climate warms it can only go higher. Sky islands across the globe are home to many rare organisms, all similarly imperiled, suitable habitat contracting with temperature and elevation until it disappears.
A less immediately obvious concern involves sex determination in crocodilians, tuataras, many turtles, and some lizard species. Most animals use a variant Genotypic Sex Determiniation (GSD), with genes on sex-chromosomes determining gender during development. These chromosomes come in a variety of flavours, from the Z/W system of most birds and reptiles (confusing things further, the heterogametic ZW genotype are females, males are the homegametic ZZ), to the bizarre X1Y1X2Y2X3Y3X4Y4X5Y5 system of the platypus and other monotremes. Let’s not get into fungi, with their potentially thousands of “sexes”. Any such sex chromosomes are apparently rare or absent in crocodilians, turtles, and some lizards, employing Temperature-Dependent Sex Determination (TSD). This involves a thermosensitive period during development where the embryo’s sex is irreversibly determined by temperature (26, 27). With changes in seasonal temperature, sex ratios in nests are going to be skewed, and the possible implications of generation after generation of changed sex ratios are concerning to say the least.
Additionally, certain lizards such as Australian bearded dragons, the Pogona genus, who typically employ GSD, exhibit TSD under extreme conditions (27). In a phenomenon known as sex-reversal, developing dragon embryos will all become female at high temperatures, in spite of their sex chromosomes. This isn’t merely a bizarre laboratory manipulation, 11 of 131 wild caught bearded dragons had male ZZ chromosomes yet were phenotypic females, capable of having ovigenesis. Sex reversals were previously only known from fish and amphibians, but who knows how many reptile species are susceptible to such impacts at extremes? While I personally suspect human society would function much better if all-female, I suppose males do play an important role, particularly for genetic diversity in wildlife populations.
Questions about the future are inherently problematic. As discussed, trends and models predicting future outcomes have their issues. But scientists are also historians, our ideas and models of how the cosmos works are built on past events, even if to predict future events. We know the Earth’s climate has not been in its existing, rather favourable state for the last 4.5 billion years. Extremely inhospitable temperatures, unpredictable geology, lifeless terrain and unbreathable gasses would’ve been the main experience on terra firma 3.2 billion years ago. Eventually, chemosynthetic ocean microbes evolved a way to utilize energy from sunlight and chemicals in their environment to trap potential energy. After evolutionary tinkering for around one billion years, the atmosphere was slowly pumped full of the corrosive waste products from a newer energy production cycle, some 2.3 billion years ago (28). Bipedal apes later named one of these waste products ‘oxygen’, the process ‘photosynthesis’. Throughout these billions of years, the climate has not been stable, changing with cycles in solar activity, in orbital distances, the odd megavolcano, potentially life extinguishing asteroids and so forth, and a strongly fluctuating greenhouse effect. Ice ages are more common than we’d like to think. Our present flash of human existence society was only possible in the current, warm interglacial period which we refer to as the Holocene. This commenced around 11,700 years ago, coinciding with the beginning of modern civilization and culture, humanity’s Neolithic revolution, gently hinting at some significance of climate for humans and life on Earth (10, 16, 17, 28).
Earth itself can tell us a lot about how life responds to changes, particularly if we can determine how current biogeography and evolutionary evidence, like fossils and genetic architecture, fit into the narrative of past conditions. The start of interglacial periods as ice ages lose hold and temperatures rise are of interest to scientists, as they give us some precedent to compare our own plight to, if we can read the evidence. While tree ring and ice core samples, oil and mineral deposit compositions, and more, can give us a timeline about the atmosphere of the past (10, 16, 17), how organisms responded is somewhat more difficult to unravel, though not impossible, as we shall see.
We generally think of fossils as large bony objects, depicting dinosaurs, or perhaps for some, the smaller invertebrates like trilobites and nautili which adorn displays and bookshelves worldwide. These are all “macrofossils”. The “microfossils” of the world are too small for the naked eye, requiring magnification to study. But as any hay fever sufferer can tell you, pollen is freaking everywhere. This makes microfossils excellent for paleoclimatology. Fossil pollen and spore samples, for example, can be found in ice cores or in stratified lake sediments, telling us much about plant and fungi distributions of the past (10, 16, 29). Locations of fossils, both geographically and their placement in whatever sediment they were found, are of essential importance to their age. The distribution of fossils show how various species migrate, populations change, ranges expand and contract, particularly in the northern hemisphere prior to the Pleistocene warming as the ice caps waxed and waned, grew and then melted back, repeatedly reducing then re-growing whole ecosystems. Great climatic variation caused continent wide shifts in plant and animal distributions, corresponding with our accounts of the physical climate from tree rings, ice cores, their constituent Carbon and other isotope ratios, and more (30).
Thus the buried remains of the dead tell a story which matches that from our tumultuous climactic past. The living tell a similar story, with the biogeography of living animals strongly influenced by past climates. Moreover, we the living carry within us, to borrow a term, our ancestors tales, in patterns of genetic variance and diversity. Our modern molecular methods allow dating of how long until genes coalesce and converge backwards in time, allowing us to estimate the age of different species, genes, and gene families (31, 32). As demographic changes in populations are reflected in our genetics, we can infer changes to our population throughout time by examining the diversity of these variously aged genes, such as expansions and contractions in population sizes and/or range margins due to glaciation and climate (31, 32, 33). Australian geckoes, for example, show much higher diversity and older coalescent history in their montane refugia than in the lowland deserts, a genetic artefact of recent colonization of the arid lowlands, as prior Pleistocene climates kept geckoes confided to the mountains (31).
Climate change is etched in our DNA, its history shaping life on earth to a greater extent than we seem to appreciate. We need only look at the great and beautiful, multi-tonal spread of skin colours in humanity from the equators to the poles. A direct adaptation to greater and lesser amounts of UV light, a scorching, fearsome enemy to be protected against at low latitudes, and yet necessary for Vitamin D production and essential to existence at high latitudes, thus the variation in protective melanin genes and skin tones. Our population genetics also show a time when, due to wild swings in the global climate and truly harsh conditions, our human population dropped to a mere 2000 or so individuals (16). We were “endangered”, the risk of extinction was real. Various species show similar losses of diversity, genetic bottlenecks, where valuable genetic variation, including entire species, were lost in climate related population crashes (34, 35). It was only in the Holocene that our numbers began to expand in earnest.
From the study of variation and distribution living biota, their scattered, ancient remnants, and the evidence of climactic conditions, from a variety of different sources, we come to see that life in fact can, and will, adapt to changing climates. Current models predict certain factors will mitigate impacts, or allow for adaptation and range shifts to occur with minimal impacts in some species, even positive responses in some. Tropical lizards for example, a group which were considered highly at risk, have recently been predicted to adapt rather successfully to current projected changes (36). Of course, many others will be less fortunate. This is reflected in the fossil record, an account of failure and death throughout life’s history, from the KT mass extinction and various other disasters, to the ever present tooth-and-claw of survival and competition. In past times, added climate variation would’ve been seemingly unending struggle, a constant challenge for many species, including ourselves (10, 28, 29). This was at a rate of perhaps 1°C per thousand years (16). If the commonly proposed target of less than 2°C above pre-industrial levels seems somewhat arbitrary, that’s because it was chosen rather arbitrarily and more for political expediency than scientific rigor (37). The COP21 target of 1.5°C is more defensible, decreasing the risks to wildlife and ecosystems, as well as humanity. Nonetheless, models show many reptile species appear to cope successfully with some climate change, through rarely without severe impacts, and other taxa will fare much worse.
And so, we lay our hopes in models which try to predict the future, while we fight to keep the world’s carbon emissions decreasing. We fight to stop global habitat destruction, the current cause of our accelerating species loss, and we fight for growing forests to sequester as much CO2 as possible. We fight against large polluters who pay to play dirty. We fight against leaders who would sell off our very future, against anti-scientific rhetoric favoring money over facts. The stage has been set, and no greater challenge have we ever faced, as part of the ecosystem, as an intelligent, conscious being, intricately tied to the comings and goings of this, the only world that we know of with coral reefs.
Case, M.J., Lawler, J.J., Tomasevic, J.A. (2015) Relative sensitivity to climate change of species in northwestern North America. Biological Conservation. 187: 127–133
Williams, S.E., Shoo, L.P., Isaac, J.L., Hoffmann, A.A., Langham, G. 2008. Towards an integrated framework for assessing the vulnerability of species to climate change. PLOS Biol. 6: 2621–
Lee, J.R., Maggini, R., Taylor, M.F.J., Fuller, R.A. (2015) Mapping the Drivers of Climate Change Vulnerability for Australia’s Threatened Species. PLoS ONE 10(5): e0124766
Walker et al. 2008. Formal definition and dating of the GSSP (Global Stratotype Section and Point) for the base of the Holocene using the Greenland NGRIP ice core, and selected auxiliary records. JOURNAL OF QUATERNARY SCIENCE (2009) 24(1) 3–17
Susana Clusella-Trullas, S., & Chown, S.L. 2011. Comment on ”Erosion of Lizard Diversity by Climate Change and Altered Thermal Niches” Science 332: 537
Bull, M.C., & Burzacott, D. 2002. Changes in climate and in the timing of pairing of the Australian lizard, Tiliqua rugosa: A 15-year study. J Zool. 256:383–7.
Carvalho, S.B., Brito, J.C., Crespo, E.J., Possingham, H. 2010. From climate change predictions to actions – conserving vulnerable animal groups in hotspots at a regional scale. Global Change Biology, 16 (12), pp.3257
Ljungström, G., Wapstra, E., & Olsson, M. 2015. Sand lizard (Lacerta agilis) phenology in a warming world. BMC Evolutionary Biology. 15:206
Durant, J.M., Hjermann, D.Ø., Ottersen, G., Stenseth, N.C. 207. Climate and the match or mismatch between predator requirements and resource availability. Clim Res. 33:271–83
Davis, M.A., Douglas, M.R., Webb, C.T., Collyer, M.L., Holycross, A.T., Painter, C.W., Kamees, L.K., Douglas, M.E. (2015) Nowhere to Go but Up: Impacts of Climate Change on Demographics of a Short-Range Endemic (Crotalus willardi obscurus) in the Sky-Islands of Southwestern North America. PLoS One. 10(6):e0131067.
Bull, J. J.(1980) Sex Determination in Reptiles. Rev. Biol.55, 3−21.
Lance, V. A. (2009). Is regulation of aromatase expression in reptiles the key to understanding temperature-dependent sex determination? Journal of Experimental Zoology Part A: Ecological Genetics and Physiology 311A (5): 314–322
Davis, M.B., & Shaw, R.G. 2001. Review: Range Shifts and Adaptive Responses to Quaternary Climate Change. VOL 292.
Engel, M., Brückner, H., Pint, A., Wellbrock, K., Ginau, A., Voss, P., Grottker, M., Klasen, N., Frenzel, P. 2012. Geoarchaeology of Egypt and the Mediterranean: reconstructing Holocene landscapes and human occupation history. The early Holocene humid period in NW Saudi Arabia – Sediments, microfossils and palaeo-hydrological modelling. Quaternary International. Volume 266, Pages 131–141
Palombo, R. 2015. Discrete dispersal bioevents of large mammals in Southern Europe in the post-Olduvai Early Pleistocene: A critical overview. Quaternary International. 2015 In Press.
Pepper, M., Ho, S.Y.W., Fujita, M.K, Keogh, J.S. 2011. The genetic legacy of aridification: Climate cycling fostered lizard diversification in Australian montane refugia and left low-lying deserts genetically depauperate. Molecular Phylogenetics and Evolution. 61 (3): 750–759
Zhao, K., Duan, Z., Peng, Z., Gan, X., Zhang, R., He, S., Zhao, X. 2011. Phylogeography of the endemic Gymnocypris chilianensis (Cyprinidae): Sequential westward colonization followed by allopatric evolution in response to cyclical Pleistocene glaciations on the Tibetan Plateau. Molecular Phylogenetics and Evolution. 59 (2): 303–310
Janssens, S.B., Knox, E.B., Huysmans, S., Smets, E.F., Merck, V. 2009. Rapid radiation of Impatiens (Balsaminaceae) during Pliocene and Pleistocene: Result of a global climate change. Molecular Phylogenetics and Evolution. 52 (3): 806–824
Mann, D.H., Groves, P., Reanier, R.E., Gaglioti, B.V., Kunz, M.L., Shapirof, B. 2015. Life and extinction of megafauna in the ice-age Arctic. Proc Natl Acad Sci USA. 112(46): 14301–14306.
Thomas CD, Williamson M. Extinction and climate change. Nature. 2012; 482:E4–5. author reply E5–6
Logan, M.L., Huynh, R.K, Precious, R.A., Calsbeek, R.G. 2013. The impact of climate change measured at relevant spatial scales: new hope for tropical lizards.Glob Chang Biol. 19(10):3093-102.
Knutti, R., Rogelj, J., Sedláček , J., Firscher, E. M. (2016) A scientific critique of the two-degree climate change target. Nature Geoscience. 9, 13–18
“Oh, you can’t help that,” said the cat. “We’re all mad here. I’m mad. You’re mad.”
― Lewis Carroll, Alice in Wonderland
Until very recently, I’d never received hate mail. While certainly a more benign and harmless variety than that which might be faced by public figures, it did catch me by surprise. In early 2016, during a rather eventful morning of snake removal, I filmed a wild carpet python (Morelia spilota) consuming a cat which it had caught and killed perhaps an hour earlier in suburban Brisbane. Belonging to the client’s neighbor, the cat had evidently been out roaming the night/early morning in our client’s back yard when a rather hungry 2 meter long python struck. Constriction and expiration would have been quick. The client’s called us around 6am after finding the python constricted around the lifeless cat, and by the time we arrived the snake’s jaws were unhinged and beginning to consume its prey in typical head-first fashion. With no hope for kitty, the pet’s owners informed, and breakfast commencing right in front of us, what choice was there but to film this incredible feeding event? Later that afternoon, I posted online an edited, close-up, time lapse video of the cat being eaten, naively forgetting that the internet is, in large part, a hate-machine powered by cat videos.
I had hoped to perhaps inspire some discussion on cats, conservation, and pet ownership in Australia. Such hopes were largely dashed as the video went viral and torrents of emotion flooded the comment sections. While I had the genuine pleasure of many interesting and generally productive correspondences, these were overshadowed by vitriolic, abusive, often hilariously absurd or bemusing replies, including various innovative suggestions of how my clearly disturbed mind and body should be removed from existence. Hatred poured through the internet to insult the snake in the video. Commenters offered unhelpful suggestions into how they would have dealt with the situation, some involving retrieving the cat’s corpse from the dead snake after dispatching it in some cruel method or another, often simply resorting to firearms. Others even felt it necessary to call and discuss their deeply felt convictions with me. I remain fascinated at how much antipathy was generated by what is, by all accounts, a fairly normal occurrence in Australia (1, 2).
Of course, such a response is not entirely surprising. Cats are, after all, one of the world’s oldest and most beloved pets. ‘Cat’ is in fact one of the first hundred words that most children learn, and while more households in the US are dog owners, more pet cats in total are owned (around 90 million in the US alone) due to their smaller size, cost, and self-sufficiency (3,4). They provide joy and comfort to countless people around the world, and their companionship role in animal-assisted therapy is something that many people will attest to, elderly schizophrenia patients for example showing improved patient contact, communication, independent self-care, and more (5). This utility as a “modeling companion” for elderly schizophrenics exemplifies just how strong our association with these fascinating animals can be. As such, it is a difficult conversation and the source of significant cognitive dissonance when people, particularly young animal enthusiasts, are confronted with the reality of global introduced species, including feral cats.
While only a foggy childhood memory, I can personally recall the difficulty of learning in the early 1990s that cats are the source of much suffering to native animals around the country and globally. I wouldn’t believe it at first. What, surely not my cat as well? Absolutely yes, in fact we practically ensured it. Being newcomers to the country ourselves, barely speaking English, and knowing little about Australia’s delicate ecosystems, we let her roam freely with little more than a bell collar. She one day abandoned us completely, never to be seen again. To my ongoing shame, our ignorance certainly caused the demise of many native animals living in the nearby national parks of outer north-east Melbourne. Whoever said ignorance is bliss was an ignorant twat, just like I was.
Many years of self-deprecation later, the issue of feral cats is still at the forefront of the conservation movement in Australia (6). Feral populations have continued to grow and put increasing pressure on native animals. The push from environmentalists to control feral cats is also growing fast, particularly in Australia where the issue receives some media attention, although many vocal cat enthusiasts are naturally concerned with what they see as an animal rights issue. A quick internet search shows how much disagreement exists, where even simple suggestions such as keeping cats indoors or enclosed in outdoor ‘cat-runs’ may be dismissed as unhealthy or inhumane to such noble and free spirited animals. Conversely, many cat owners, animal ethics or pet associations such as PETA, suggest it’s crueler to leave domesticated cats outside exposed to diseases, predators, vehicles, or even unscrupulous cat-hating humans. While the vast majority of cat owners are caring people who truly love animals and can appreciate the difficulties of balancing wildlife conservation with society’s needs, the outraged multitudes online and those responding to our video show just how entrenched some opinions are. With many extinctions already attributed to feral cats in Australia in a rather short time period, a resolution is urgently needed to this contentious issue. Though one cannot hope to truly solve the feral cat problem from an armchair, we may at least explore some of the natural history of cats and wildlife in Australia, in the hope that a better understanding of the problems might illuminate, if not a solution, at least some common ground to walk on.
Evolving from the wildcat Felis silvesteris, one of the 38 species in the well known Felidae cat family, the domestic cat F. catus was likely a fantastic aid in rodent control to early agriculturalists, eventually becoming a somewhat more domesticated house pet. Most of us are quite familiar with the ancient Egyptian depictions of cats as house companions, omens, or even various powerful deities. Enigmatic feline-like hieroglyphs and images from around 2500 BC show just how long humans and cats have been associating, however the history of domestic cats goes back further. The oldest archeological evidence for domestication was found in Cyprus, with a cat skeleton found buried a mere 40cm from human remains, dated to some 10,000 years before present (YBP here on) , much earlier than the predicted Egyptian origins (7). This finding was further supported by Driscol et al. (8) who found genetic evidence that all domestic cats originated in the Fertile Crescent. Quoting the authors directly, “…the world’s domestic cats carried genotypes that differentiated them from all local wildcats except those from the Near East…” suggesting domestic cats are directly descended from the Near Eastern Wildcat (F. silvestris lybica). Domestication likely began up to 12,000 YBP, much sooner than dogs at around 17,000 YBP, coinciding with the beginnings of agricultural settlement of the Fertile Crescent and the Middle East, supporting the idea of domestication initially for rodent control followed by companionship.
Domestic cats and humans nowadays seem to get along as companions rather well, aside from the occasional shattered glass. This was unfortunately not always the case. While worshipped in Egypt for thousands of years, the Middle Ages were a bad time to be a cat. Seen as everything from witches in guise, dark omens of the future, or even the Devil himself, cats were persecuted by the public in horrendous fashion. Eighteenth Century Europe was in fact no better, with cats often treated as scapegoats, bearing much of the brunt for the lower class’ hatred for the bourgeoisie, or even tortured and killed on mass for cultural and ceremonial purposes (for a rather gruesome account, and more on the life of the common man in Eighteenth Century France, see (9) the Great Cat Massacre). Although thankfully no longer accepted by society the way it was only a few hundred years ago, unspeakable acts of cruelty are still unfortunately visited upon cats by people, even in our more pet-centric times with animal ethics legislation and heavy penalties in place to prevent such despicable acts.
Like much of the world, many Australians share a strong affection for our feline companions. In 2007, Australians spent over 1.3 billion dollars on caring for over 2.2 billion pet cats (10). While they have been spread around the world by humans for the last 2000 years as either shipboard rodent control, companionship, or even as food, cats arrived in Australia more recently, alongside the European invasion during the late Eighteenth Century (See 11 for an overview of feral cats in Australia). Generally kept aboard transport vessels for rodent control, later in settlements for companionship, these original invaders caused havoc wherever they went, particularly on islands where small, isolated populations had few natural predators and haven’t the necessary adaptation to avoid such skilled hunters. Furthermore, cats are a placental mammal in the order Carnivora, the only one present in Australia aside from the dingo. Australia’s native predators are generally small to medium sized marsupials, reptiles, and birds of prey, all with lower resource requirements and, to be honest, smaller brains in general. Cats are simply too adaptive for native prey compared to their usual suite of predators, and likely outcompete many of our native predators in keeping up with their higher fuel requirements, particularly medium sized marsupials like the Quolls (Dasyurus spp). The situation was not improved by deliberate releases of thousands of cats in the nineteenth century around settlements and goldmines to control introduced mice and rabbits as well as native bush rats. These secondary introductions almost certainly bolstered the genetic diversity of the already present feral cat populations, increasing their adaptive potential.
Unfortunately for everyone, our ecosystems are suffering from the massive presence of feral cats, now completely wild self-sustaining populations which have little contact with humans. Estimates range up to 20 million running around Australia’s wild areas after only a few hundred years since colonial Europeans invaded the shores, and considering these ultimately innocent cats consume five native animals on average per hunt, the sheer numeric impact of feeding alone on native animals every night is staggering (11, 12). Australian ecosystems are particularly vulnerable due to several variables such as our generally low nitrogen economy soils, thus more of our fauna lean towards what biologists call ‘K-selected’ life strategies. This means slow growing, more efficient animals, with smaller amounts of offspring but generally greater resource investment in each breeding (K for populations where limitations in some variable or resource means populations are close to carrying capacity, r for rate of reproduction where populations have expendable resources and operate at close to their maximum intrinsic reproductive capacity, see (12) for further discussion on K/r selection). One might say K-selected fauna prefer the slow and steady approach, as opposed to r-selected fauna like rabbits which live life in the fast lane, burning though abundant food resources to have as many offspring as possible, as often as possible, in a short life.
While no specific agreement has been arranged between prey and predators, adaptive selection favours K-selected life strategies in resource poor environments. Theoretically, r-selected predators would, in a low resource economy, eventually tax struggling prey populations to the limit and lower numbers, decreasing the health and fitness of both parties. Due to this new resource boundary (prey numbers), natural selection over time favours those heritable mutations which subtly mitigate the impact of the hunters, perhaps by promoting larger, slower growing, later maturing individuals and increasing investment in more moderate sized, less frequent litters. Such limitations eventually lead to healthy ecosystems with a balance between prey populations and predation rates. This selective feedback has been going on in Australia for millennia, through slowly fluctuating environmental conditions, leading to a vast diversity of specialized but very sensitive species and ecosystems. Our fauna communities are dominated by resource efficient reptiles and marsupials (though there are of course exceptions to the rule). Like the majority of non-native domestic animals brought to Australia, cats are placental mammals and are generally more r-selected than our native marsupials. Though Australia has also evolved r-selected species under certain conditions, introduced species don’t share the millions of years of co-adaptation of native plant, animal, and microbe communities. Our delicate but highly diverse and ephemerally abundant continental ecosystem would have the appearance of a snacking tour to a moderate sized, intelligent, adaptive, fast reproducing mammalian predator.
This disparity in life strategies with our native predators goes some way to explain the successful invasion and heavy impact of feral cats. While these feral populations are already self sustaining into the foreseeable future, gene flow and genomic introgression between ferals and domestics indicates that recruitment and breeding with domestic cats further bolsters wild populations (13). Unfortunately, with few appreciable borders for cats across this large and, for us primates, inhospitable continent, the total size and growth rate of wild Australian populations are extremely hard to accurately quantify, though the aforementioned figure of 20 million is certainly plausible (12). Feral cats appear to use a facultative prey choice strategy, targeting invasive rabbits initially, quickly switching to a wide variety of animals when this ideal prey is unavailable (14). On average, they may take five native animals a night. Considering this, the potential predatory impact could be well over of 20 billion native animals each year, a much higher figure than many might suspect.
How much of an impact can cats truly have? Dickman et al. 1996, by determining what ecological characteristics make a species vulnerable (factors such as mobility, fecundity, feral cat density in habitats, anti-predatory behaviours, size, and many more) then assessing how many risk-attributes a species possesses, demonstrated that 81 endangered and vulnerable species are likely at risk from feral cat impacts, however more observations are needed to fully verify these numbers. Recent studies of the impacts of cats have taken several approaches; surveying cat owners for the kills their pets return can give some indication of cat predation, perhaps even prey selection behaviour, however these estimates are obviously limited to domestics, and by various “detection biases” such as the fact that only around 20% of prey are presented to the owners while the rest are either eaten or discarded (15, 16). Camera traps or mounted cameras give more direct confirmation of predatory behaviors/rates, however these methods still often rely on many assumptions (16, 17). Extrapolating feral cat population and predation rates from trap samples is one thing but, while naturally informative, these numbers themselves tell us little of the actual causal link between cats and declines in native communities (15, 17). Studies of feeding ecology through examining the stomach contents of feral cats are excellent and with enough data can give good baseline estimates of impacts, however we still have to extrapolate from what samples are available, and any initial error in our assumptions increases with our extrapolation. So while counts of prey items are a valuable resource, even these estimates must be treated with caution (see Section 4.2 of Dickman, 1996, for an overview of feral cat diet studies in Australia).
Much better, then, to study the response of prey populations under different predation pressures from cats. This might, for example, involve studying distinctly separate communities of native wildlife under varying feral cat populations. Alternatively, one might enclose large patches of native landscape with predator proof fencing and eliminate cats within these habitats, with the outside as an effective control patch where feral cats remain present. This latter method was recently undertaken at the World Heritage Listed Kakadu National Park in the Northern Territory. Working with the NT Department of Land and Resource Management alongside Parks Australia, ecologist Daniel Stokeld and others recently reported that faunal biodiversity, but particularly reptiles, increased significantly in response to cat exclusion.
“We were quite surprised by the response of reptile numbers and diversity,” said Stokeld, speaking to ABCs AM Radio Show, “That was something that hasn’t been shown in other studies. So that was quite a significant finding signifying that cats are having quite an impact on reptile populations.” (See 6 for a link to the article and radio podcast)
The NT Government’s Director of Terrestrial Ecosystems, Dr Graeme Gillespie, further noted that despite various reptiles frequently turning up inside the stomach contents of feral cats, this is the first hard evidence of an ecologically significant impact in Northern Australia. Reptile abundance and reptile species richness within the excluded zones effectively doubled within two years. To quote Dr. Gillespie,
“That’s a very, very fast recovery, so that means the cats are having a very big influence on the number and diversity of reptiles that are out there, in particular in areas like Kakadu National Park.”
Unfortunately, very few small mammals were detected in their dataset, and with such a small sample size no reliable conclusions could be made for mammals in this particular study. One might be tempted to speculate that prior to feral cat impacts this problem of sample sizes in small mammals may have been a non-issue.
The Australian Wildlife Conservancy, a phenomenal non-profit, conservation organization, and a significant contributor to The Action Plan for Australian Mammals (12), outline the cat crisis rather succinctly on their website. Emphasizing that with 29 extinctions since white man arrived on these shores we’ve lost almost 10% of our Australian mammals. This is the highest mammal extinction rate in the world. A further 30% of our remaining mammals are currently threatened with extinction in the near future, with cats representing a major threat. I suppose with the new data from the Northern Territory we can now add threatened reptiles to the list of potential victims. Birds, of course, also suffer heavily, even from our domestic cats, leading to urban areas acting as ‘population sinks’ for native birds, actively lowering numbers in adjacent habitat stands (18). While generally a fan of prey around 200grams in weight, large feral cats can take kills of up to 2kg, securing prey with teeth and forelimbs while the rear legs tear at the flanks and body (Dickman et al. 1996). It seems that feral cats negatively impact a broad range of native wildlife, from tiny invertebrates to medium sized mammals, reptiles and birds, and while mammalian prey are generally preferred, their facultative feeding strategy means when scarce they will happily switch prey items.
These studies and more indicate a clear need for decisive action in controlling feral cats. Three methods are typically employed in cat eradication; shooting, trapping, or baiting (19). While trapping might seem like the easiest option, the amount of field effort required in transport, trap installation, monitoring etc. are rather substantial, all the more when working with a live trap and a large, distressed feral animal in a field setting. Shooting has traditionally been preferred and while seemingly a rather gruesome solution, it is arguably more humane than hours of trap stress. However this still requires a substantial amount of man hours and, due to their adaptive intelligent nature, cats have been known to become wary if the shooter happens to miss his mark. Baiting with 1080 and PAPP are generally considered the cheapest, most cost efficient methods. However, negative public perception is a continuous issue, with no effective treatment for accidental poisoning and other animal welfare concerns, although new baits, poisons, and techniques are in constant development, such as the Eradicat bait developed by the State of Western Australia Department of Parks and Wildlife in 2014 (20).
With a continent worth of feral cats to control, no doubt cost effectiveness must play a significant role in any measures used in this battle. It’s also imperative that all efforts are made to minimize any collateral damage to wildlife, such as native predators accidentally taking baits meant for ferals, with consideration of the welfare of target pest species. Previous attempts have involved various bait modifications, for example changing the scent profile or adding insecticides to mitigate breakdown of the bait by invertebrates and subsequent uptake by insectivorous native predators (20). These still rely on the animal ingesting the toxin somehow, however the latest high-tech tool involves a rather ingenious method to achieve toxin intake, capitalizing on a thorough understanding of differences in cat and native mammal ecology, lasers, and a pressurized squirt gun.
Relying on the cat’s particular penchant for hygiene and grooming, these so called “grooming traps” combine the best of all three control methods while avoiding many of the pitfalls (21). They involve a mechanized, pressurized spray gun installed alongside infra-red laser detectors, assembled into a single, field-ready trap unit. Calibrated to fire only when the target animals size and dimensions, particularly the space underneath the trunk of the body (between fore- and hind limbs) matches that of a cat and not a native animal, the trap fires a dose of adherent toxic gel between the shoulders of the targeted cat which, unlike our native animals, will fastidiously lick off the toxin within a few minutes. This allows a targeted, species specific delivery of a lethal dose of PAPP, the biological action of which the RSPCA has approved as significantly more humane than 1080, acting as a sedative first, leading to unconsciousness and a pain-free death soon after. After seven years of research and development by Mr John Read, an ecologist from the University of Adelaide, these incredible multi-faceted techno-traps are currently being trialed on the Pullen Pullen Reserve in western Queensland, purchased by Bush Heritage Australia (22). The 56,000ha conservation reserve is home to the endangered Night Parrot (Pezoporus occidentalis) thought to be extinct for over 100 years until the 1990’s. With the first traps going live earlier this month, many scientists are certainly eager to see the results, as any potential solutions or new tools in this epic losing battle for biodiversity would be rather welcome.
While all this sounds rather promising, there are still numerous challenges to solving the cat crisis in Australia. Even if these new generations of control techniques prove to be cost effective in controlling cats, public perceptions of feral cat control are still often negative. Many promote the Trap-Neuter-Release (TNR) method of eliminating cat populations, as this involves de-sexing rather than killing (see 23 for details on TNR for feral cats from the RSPCA). However the massive costs associated with trapping/desexing adults, re-homing kittens and socialized adults, and euthanizing old or sick cats are very difficult to justify, particularly considering that even a neutered animal still needs to hunt as long as it lives if returned to the wild.
Many refuse to accept that cat control is a necessary evil, and a responsibility we as humans should take very seriously. This was most apparent in 2015 when, in response to the Action Plan for Australian Mammals (12), the Australian Government announced a planned cull of 2 million feral cats over the next few years (10% of the estimated population) using trapping, shooting, and poison baits (24). Animal culls generally succeed in raising the ire of the animal welfare minded, and this was no different. Culling is an important tool in wildlife management, but is often regarded as inhumane, particularly when used on native populations. This is not the case with cats, yet still the opposition to was extremely vocal. The most prominent response came in the form of an open letter to our Environment Minister from classical French actress Brigitte Bardot, as well as an online post from Stephen Patrick Morrissey, lead vocalist for 80’s indie rock band The Smiths. Both wrote statements to the minister in response to the announced culling plans, with Morrissey making the visibly false claim that feral cats are “2 million smaller versions of Cecil The Lion”, while Ms Bardot’s much longer open letter suggested a TNR program would be more effective, humane, and less harmful to the environment since poisons would not be released, and sterilized cats would hold territory but not breed.
These statements are both wildly inaccurate. Ms Bardot’s claim that TNR campaigns are effective “everywhere” is a standard denialist position (only a Sith deals in absolutes), completely ignoring scientific evidence. Little effort is needed to find that the claims made by TNR advocates, such as that cats only negatively impact island populations not large continents, or that they don’t cause native species declines at all, or they are filling some required natural niche, and many others, are all contradicted in scientific literature by numerous authors and sources (see (26) for just one of many papers dismissing TNR). There is no excuse for such ignorance when one purports to be an animal welfare activist; science must be your guiding light. The stakes are too high, and while the public image of a pop-culture icon saving our animals is naturally appealing, it is important to remember that such advocates are not scientists and if they refuse to accept scientific conclusions, their opinion on wildlife science should be ignored. Furthermore, while we’re here dismissing the ignorant, anyone willing to accept the opinions of Ms Bardot as somehow valuable may want to read her thoughts on race relations, homosexuality, school teachers, the poor, immigration, and how the future of France might be improved by returning the public guillotine from retirement (27). This is the same ‘animal activist’ who was taken to court when in the 80’s she had her neighbour’s donkey castrated for making advances on her own donkey, which she considered “sexual harassment” (28). Perhaps we can find better role models for animal rights and conservation than these two.
Many well meaning folks perhaps do not fully understand the true extent of the feral cat crisis or the sensitivity of our ecosystems. Additionally, it seems that for some people, no matter the costs to our native wildlife, cats (and cats alone, not foxes, rabbits, or, perish the thought, the invasive cane toad Rhinella marina) are simply more deserving of protection and existence due to their value as human companions and for our emotional ties with these beautiful animals (29). One is tempted to assume this attitude is also a result of simple ignorance, an under appreciation of our endemic and unique fauna communities. If this is so, as appears to currently be the case, a broad, environmental education approach that improves local stakeholders’ ecological understanding is more likely to succeed than informing cat owners and locals about cat impacts alone (30). The government’s response to Morrissey and Bardot’s comments, in the form of open letters from Threatened Species Commissioner Gregory Andrews (31, 32), attempts to achieve this by publically laying out the basic framework of Australia’s cat crisis and why it is essential to implement a lethal control program as soon as we can, addressing such issues as welfare, effectiveness and cost.
Let’s hope it doesn’t fall upon deaf ears, after all it is we humans, not cats themselves that caused this catastrophe (couldn’t help myself, please don’t judge too harshly for this one terrible, terrible pun!) and to ignore the consequences and current declines in native species across the continent would be disastrous. Invasive species are a major driver of global extinctions, just behind habitat destruction, sometimes even the leading cause, as is the case with bird extinctions (33). To not have a heavy handed response to this crisis would be to condemn millions of native animals each night. It would assert that cats have more right to existence than other animals due to our own affections. And finally, it would have us shy away from our mistakes, rather than learning from our many and varied short-comings, as is the general tendency of human history. I find this unacceptable, the result of ignorance and fear, not knowledge and compassion.
May our efforts to repair our mistakes and contain the Australian feral cat crisis not be in vain. On that note, I leave you with the borrowed final words of a more eloquent human than I; words which I feel suitably match my own hopes and dreams for this beautiful, unique landscape, despite the various charges underneath our watch who are slowly slipping away into extinction, forever, unless we act.
“For the moment, I hope that Australasians one and all will begin to ask the right questions. For this is the first, necessarily wobbly step on the road to discovering what it means to be custodians of the wonderful and enigmatic ‘new’ lands”
– Tim Flannery, The Future Eaters.
References
Fearn, S., Robinson, B., Sambono, J., Shine, R. (2001) Pythons in the pergola: the ecology of ‘nuisance’ carpet pythons (Morelia spilota) from suburban habitats in south-eastern Queensland. Wildlife Research. 28. 573–579
Dickman, C.R. (1996) OVERVIEW OF THE IMPACTS OF FERAL CATS ON AUSTRALIAN NATIVE FAUNA. Australian Nature Conservancy: Invasive Species Program.
Woinarski, J., Burbidge, A., Harrison, P. (2012) The Action Plan for Australian Mammals 2012. CSIRO Publishing
Montague, M.J., Li, G., Gandolfi, B., Khan, R., Aken, B.L., Searle, S.M.J., Minx, P., Hillier, L.W., Koboldt, D.C., Davis, B.W., Driscoll, C.A., Barr, C.S., Blackistone, K., Quilez, J., Lorente-Galdos, B., Marques-Bonet, T., Alkan, C., Thomas, G.W.C, Hahn, M.W., Menotti-Raymond, M., O’Brien, S.J., Wilson, R.K., Lyons, L.A., Murphy, W.J., Warren, W.C. (2014) Comparative analysis of the domestic cat genome reveals genetic signatures underlying feline biology and domestication. PNAS. 111:48
Doherty, T.S., Davis, R.A., Van Etten, E.J.B., Algar, D., Collier, N. , Dickman, C.R., Edwards, G., Masters, P., Palmer, R., Robinson, S. (2015) A continental-scale analysis of feral cat diet in Australia. Journal of Biogeography 42.
Barratt, D.G., 1998. Predation by house cats, Felis catus (L.), in Canberra, Australia. II. Factors affecting the amount of prey caught and estimates of the impact on wildlife. Wildl. Res. 25, 475–487.
Meek, P., Ballard, G., Fleming, P., Falzon, G. (2016) Are we getting the full picture? Animal responses to camera traps and implications for predator studies. Ecol Evol. 10.
Van Heezik, Y., Smyth, A. Adams, A., Gordon, J. (2010) Do domestic cats impose an unsustainable harvest on urban bird populations? Biological Conservation. Volume 143, Issue 1.
Environment Australia, 2008. Threat Abatement Plan for Predation by Feral Cats. Environment Australia, Biodiversity Group, Canberra.
Fisher, P., Algar, D., Murphy, E., Johnston, M., Eason, C. (2014) How does cat behaviour influence the development and implementation of monitoring techniques and lethal control methods for feral cats? Appl. Anim. Behav. Sci.
Read, J.L. (2010) Can fastidiousness kill the cat? The potential for target-specific poisoning of feral cats through oral grooming. Ecological Management & Restoration. Vol 11, 3.
One fine spring afternoon, I was bitten on the face by a nearly one meter long snake. Certainly a result of my own stupidity, this animal decided to clamp onto my left cheek. No permanent damage was done, save for my work shirt which suffered minor stains, and after a quick clean up we were back to work. Our job of course is to relocate snakes to more suitable habitats whenever they come across fearful humans, and we knew we were in no real danger. The animal in question was a common tree snake (Dendrelaphis punctulata), an effectively harmless, fangless colubrid snake which had been mistaken by warehouse staff members for a highly venomous eastern brown snake (Pseudonaja textilis). I humbly suggest, had it been P. textilis under the shelves, I would have been much more cautious, perhaps even restraining myself from holding it up near my face, allowing it to strike precisely at the moment I was explaining to watching staff members that these animals aren’t venomous (D. punctulata, that is!) and, while they do have teeth, they only very rarely bite even when handled (they truly are quite docile…most of the time). I was also defecated on and musked, a defensive tactic of releasing a foul smelling, pungent “musk” from glands in the cloaca, by the same individual. Ah, the infinite joys of working with native wildlife.
The common tree snake is a frequent visitor of people’s properties from Australia’s east coast and across the top end, avoiding the more arid inland and colder south (See Wilson & Swan, 2013 (1) for a field guide of Australian reptiles, Cogger, 2014 (1) as a comprehensive at-home companion). These laterally compressed, lightweight, elongate snakes are perfectly adapted for their non-venomous style of prey capture, climbing up to high into forest canopies and vine thickets where tree frogs hide, or slipping stealthily around aquatic and riparian vegetation. A particular fan of frogs, they simply latch on to prey animals small enough to overpower and swallow as soon as possible, often alive. This requires nothing more than small, sharp teeth, a contrast from the highly complicated venom systems of other snakes.
Why are we discussing this rather commonplace, non-venomous, seemingly unexceptional snake? Here we take a tentative step into a yet unsettled and at times especially heated debate in the world of reptile biology (please, nobody hit me!). For according to the captivatingly titled Toxicofera hypothesis, not only D. punctulata but all other snakes, including the various pythons which have also gifted me with unpleasant facial injuries, are venomous or share a venomous ancestor. No recent theory in the world of venomous reptiles has caused as much of a controversy as this idea. Take the non-venomous snakes I was so idly handling my whole life; were they actually in possession of a venom system, even if somewhat deteriorated over evolutionary time through non usage?
The Toxicofera Hypothesis daringly goes even further. The discovery of highly dangerous venom products in the mouths of theoretically non-venomous snakes poses the question; what else out there might be venomous? The venom research team of Fry et al. went looking for venom where there should be none. They found that many lizards, including the largest in the world, the Komodo Dragon (Varanus komodoensis), also possess venom and venom glands in their jaws. The Komodo in particular caught the fascination of the science media, as these gigantic monitor lizards were previously thought to capture their prey by delivering a septic bite full of bacteria, or relying on physical trauma caused by their serrated teeth, like well maintained steak-knives (see (3)). What a phenomenal discovery to further weaponize this already powerful and captivating beast!
Since the expansive work of Fry et al. 2006 (4), the Toxicofera hypothesis had been widely accepted. The Komodo Dragon’s newly acquired venomous status had even been cemented in culture by no lesser natural history orator than the celebrated Sir David Attenborough (stand and salute, or be shot) in the BBC Life documentary series. Alas, certain aspects of their research and conclusions have come under fire in the following years from other toxinologists around the world, casting some shadow over this idea which had so captured the attention of both public and scientific audiences. What followed was a battle of words and reasoning between the two camps, taking stage on two of the grandest of battlefields known to modern scientists; the “letters to the editor” section of a specialist journal (Toxicon in this case), and a public scientific debate at Oxford. Perhaps we should closely examine the evidence for and against the Toxicofera hypothesis to better arm ourselves before we enter the fray in this venomous war of wits.
Let’s start with the origin of the Toxicofera and the work of Fry and colleagues. How did the authors determine that these animals all belong to the same clade, an evolutionary term for a grouping of related animals with a common ancestor? Traditionally, venom is thought to have arisen twice or even three times in the squamata; in the snakes (perhaps separately in the elapids/vipers and the colubrids) and in the heliodermatid lizards, the Gila Monster and the Beaded Lizard (3). After several years working on the evolution of venom systems in front fanged elapid snakes from the late ‘90s to the early 2000, Fry began investigating the venom systems of some less studied venomous snakes in the Colubridae family, an unresolved, numerous and diverse umbrella family which likely contains several separate families (see Lumsden et al. 2004 (5) for an example of some of their work). Not all colubrid snakes possess fangs or venoms, and where present they’re less sophisticated than in elapids and vipers. While the latter two families deliver a pressurized bolus of venom, passing from the temporally placed gland (venom reservoir inbuilt) through a venom-duct to the font maxilla where it is injected through modified hollow teeth or “fangs “, colubrids rely on simple enlarged teeth halfway down the back of the jaw (thus the term “rear-fanged” vs “front-fanged” for venomous colubrids and elapids/vipers respectively). The rear-fang is grooved at the back, trickling venom proteins down to the puncture site as they flood the mouth at the base of the fangs, extruded from more the simple glands referred to as Duvernoy’s Glands, often with small additional glands along the upper and lower jaw line under the labial scales (see 6, 7).
All this led to an intriguing question; what are the origins of this venom system in snakes? This issue has been debated within the herpetological community for some time, with many suggesting that the elapids and vipers evolved their venom system separately, with certain colubrids later developing their own similar system. This was cited as a case for convergent evolution, the process by which two species evolve similar adaptive traits due to similar selective pressures (7, 8). This is in contrast with shared ancestry, where homology (similarity) between features and species implies a common ancestor in possession of the shared trait, which is then inherited down many generations by separate lineages as they become separate species and groups.
Consider the evolution of flight in vertebrates. Only the birds and the bats are capable of powered flight, but we do not believe they evolved from a recent common ancestor. The birds are essentially a lineage of reptile, closely related to the dinosaurs, the bird line of crown-group Avemetatarsalia evolving within the Archosauria, trading scales for feathered plumage (although both are made of similar keratinized materials), while the mammals evolved much later in the history of life on Earth from smaller, ground-dwelling, lizard or mouse-like reptiles, perhaps similar to shrews or gerbils (9, 10). For these lightweight animals, in a world full of predators, the benefits of being able to glide, or perhaps simply control airtime and corner more precisely while bounding from log to rock to branch, are self evident. Any mutations for increased forearm feathers or perhaps thin membranes between elongate fingers might be quickly swept to ‘fixation’, that is, mutant offspring with these traits are so successful and breed so frequently that within a few generations the whole population is comprised of individuals in possession of their gene variant with the accompanying trait, and the mutant becomes the new norm. In this way, both bird-like and bat-like ancestors successively converged on the same solution independently, as opposed to sharing a flying ancestor like the modern descendents of these early birds or bats do. Flight, incidentally, seems to be a common point of convergence, first evolving in the Pterygota, the winged insects, 170 million years before any other life forms took flight (11).
Back to venom in snakes, did the colubrid and elapid/viper venom systems evolve separately in convergence? Or is the front-fanged condition a derived, more complicated and effective version of the one original rear-fanged condition? Of course, proponents exist for both ideas. Some suggest that it could be naught else but a venom system in infancy, others say that even if so, a venom is defined by its use in prey capture or defense, and can be only defined by its biological function, which has not been demonstrated yet. For example, humans also possess toxic oral compounds in our saliva, known for pre-digestion etc. rather than hunting, but we would hardly be considered venomous (7). Still, whether venom or some other protein product, the shared point of agreement was that the oral products of non-venomous colubrids, even those without fangs or Duvernoy’s Glands, needed more investigation.
Fry was in the process of studying the glands of these less dangerous colubrids when the first suggestions of the Toxicofera came to light. Using LC-MS (Liquid Chromatography–Mass Spectrometry), as well as protein isolation and sequencing from the Asian Ratsnake (12), the team could investigate what proteins were being produced and what genes may be involved. In the mouths of some putatively non-venomous colubrids, highly toxic venomous protein compounds continued to be located, albeit in small quantities. These included three-finger proteins which the team suspects may be the ancestors of the three-finger neurotoxins (3FTXs) of highly venomous elapid snakes. Where does the story of squamate venom end? In following this, Fry and colleagues spend much field time with various Australian lizards. By creating libraries of the DNA expression in oral tissues, they found similar toxic venom products in an agamid and a varanid lizard (3). These proteins closely matched those found in the venom glands of serpents.
Around the same time, another type of study was making waves. Morphological evidence from precise physical measurement of bones and fossils, and the mathematical groupings of these measurements to delineate species and higher orders of taxonomic groups, has a centuries long standing as the standard method for evolutionary research and the study of natural history. It might’ve come as a rude shock to proponents of the traditional schools when a newer style of evolutionary data, molecular evidence from examining sequence variation and expression patterns of DNA, RNA and proteins (the information storage, transcript papers, and physical matter of biology itself), began placing doubts on some of these morphological conclusions. Most notably for us, squamate phylogenies built from multiple gene sequences placed the evolution of iguanid reptiles much later history (13). In fact, they have buddied up right next to the Serpentes lineage, the latest major evolutionary and morphological radiation in the squamate reptile group, a radical difference from the basal placement suggested by morphology.
Both the molecular phylogenetic data and the protein sequence data seemed to agree upon this rearrangement of Iguania. Furthermore, according to the findings of Fry and colleagues, these lizards share the similar venom products in their mouths to all snakes. The blow to our pillar of understanding resounded throughout biology; all snakes are venomous, and so are, most probably, many lizards (excluding several lineages like the geckoes and skinks which diverged before the development of the “venom genes” typifying the Toxicofera). All share a venomous common ancestor some 170 million years ago, lizard-like in form, with some subsequent lineages losing the apparatus through lack of usage. So sayeth the Toxicofera hypothesis. Further support came in the following years with more so called “incipient venom systems” found, including that of the famous Komodo Dragon. Glands and venom proteins were discovered in the mouth tissues of various iguanid and varanid lizards, including several commonly kept commercial pet species, such as the central bearded dragon (Pogona spp). The Toxicofera hypothesis was picking up steam. That’s when someone threw a chair, and a fight broke out.
Not everyone was on board with team Toxicofera. It is easy to view such dissent for new idea as nothing more than the Old Guard complaining that the new kids are being too noisy (with their gosh darn rap music and DNA technologies), but this would dismiss two major tenants of science: that no idea is beyond review, and that an exceptional statement or revision requires exceptional supporting evidence. Scientists complain, particularly about other scientists, and this is how we improve, usually in a polite and courteous manner. While one might publically comment online in various forums, this means little in the world of peer review. What to do? Like any polite but disagreeable reader, one might feel compelled to write a strongly worded, thoroughly research letter to the editor, expressing your discontent and reasoning, for the target audience to see in the next issue of the journal.
Such was the response of Weinstein et al. 2012 (14) to the several years of Toxicofera papers that had been published since 2006. This group of toxinologists and evolutionary biologists had decided to challenge certain aspects of the Toxicofera. Namely they were targeting the definition of these animals as venomous. Team Toxicofera hit back (15), writing a letter to the editor themselves to dispute the points brought up by Weinstein et al., which was naturally replied to in kind (16). If ever the opportunity arises, I thoroughly recommend these letters not just for their scientific content but for entertainment. I truly enjoyed these papers not just for the well formed arguments, but for the salvos of criticism and rebuttal peppered with as much passive aggression as any journal can let past their editorial desk. While Fry and colleagues argued from the functional lab tests on blood pressure, homology of proteins, DNA/RNA sequences and phylogenies, as well as their mere presence in the oral tissues, the detractors maintain it is premature to call this “venom” as its ecological role has yet to be demonstrated.
Fry and colleagues do not accept this and argue instead for a revision in how we define venoms and venom systems. I personally find this hard to agree with as the already-in-use term “oral product/secretion” would suffice for any toxic compound without such a biological function (See 6). The various snakes which have bitten my face were not, in my preferential use of the term, “venomous”, despite perhaps possessing small amounts of toxic compounds in their saliva. The many, many bearded dragon (P. barbata and vitticeps) bites I have sustained on my fingers also never caused excessive bleeding, swelling, or other illness. Even if the toxic compounds in their tissues eventually were recruited to give rise to true venoms through splice variants, gene duplications, and adaptive selection, as may indeed be the case, these pre-venom products still have no natural use in prey capture in bearded dragons, which are primarily vegetarian.
While we of course do not fall within the Toxicofera phylogenetically, humans also possess some of these putative venoms in our buccal cavity (17). These include toxins with similar LD50s (a measure of toxicity) to those being used to attribute venomous status to the Toxicofera. Should we suggest humans are venomous since an intravenous injection of our saliva would disrupt the body’s delicate homeostasis? Does it not seem more consistent to continue using “toxic oral products” or a similar term to refer to any compounds produced in the oral cavity that are toxic, until the ecological function has been ascertained? Or do all snakes, many lizards, and probably a host of other species, including humans, now have the honour of being venomous fauna? In response to the need to ascertain the ecological role of these proteins, Fry has been quoted as saying, somewhat dismissively, “just give us a couple more centuries, an army of research students, unlimited funding, and we will be with you on that” (See this link (18) in the Atlantic), implying perhaps the task of confirming the ecological role of all of these proteins in every species is too arduous, an impossible and preposterous standard to set. This seems like a somewhat facetious argument as a response to genuine criticism. To suggest that every species’ oral products must be tested for function would of course be foolish. However, if it could be demonstrated in but a handful of species across the Toxicofera lineages that these proteins have an envenomation function, the venomous status of these creatures would be gloriously and righteously vindicated. Strong support indeed and hard for anyone to argue against!
Alas, there are no such examples in any taxa thus far. Even the Komodo Dragons venomous status is under debate, with detractors suggesting the amount of trauma generated by the serrated, saw-like teeth seems more than enough to cause bloodloss and shock rather quickly. Ecological function of all of these putative venom compounds thus remains a mystery. Should we perhaps withhold upgrading them from “oral products” to “venoms” until we decide whether ecological function or simple toxicity will be the standard-barer for biology as a whole, us included, from here on? Evolutionary definition can be a bumpy road, but such standards and definitions are set exactly to moderate the kind of confusion currently being generated.
What then are the roles of these oral proteins if they’re not venoms? Many functions have been suggested, for example, lubricating prey to aid swallowing, pre-digestion (just as the enzyme amylase starts digestion of starch compounds in our mouths before food even reaches the stomach), anti-putrefaction since large prey may take days to digest inside a snake, detoxifying/disinfecting prey surfaces, or general oral health and hygiene (Kardong, 1982). However, just as suggestions for venom function in lizards, the above are nothing more than suggestions. Proof requires evidence, which has yet to be gathered, thus judgments should be withheld until we know for sure.
More recent evidence may suggest that these “venom” proteins are not venom proteins at all. A 2014 publication by Hargreaves et al., using emerging technologies, surveyed DNA expression in multiple body tissues of Toxicoferan animals, including the Burmese python and the leopard gecko (19). Comparison of the genes expressed in these tissues with online databanks of gene sequences found matches where one would not expect. These “venom” genes were being expressed throughout multiple parts of the body, and in comparable levels to those found in the oral tissues. How could this happen? The authors suggest that these genes are in fact nothing more than “housekeeping” genes, used for general maintenance purposes rather than venom. Of 74 putative venom genes studies, only two (Laminoacid oxidase b2 and PLA2 IIA-c for those playing at home) showed significant expression of gland-specific splice variants as expected of true venom proteins. This was considered a heavy blow to the Toxicofera hypothesis, although Fry and colleagues maintained that true venom genes had to come from somewhere, and these housekeeping genes were recruited for their toxicity, a by-product of their original function, at some point in the early Toxicofera history. If you suspect that this was far too ambiguous an answer to satisfy everyone, particularly those opposing team Toxicofera, you would be correct.
Obviously the matter needed to be settled before the scientific community came to blows (scientists are after all known for their violent temper and rage issues). The battle in the editorial section had garnered quite an audience, but as yet seemed unresolved. The challenge was set; a public debate at Oxford University. Who wouldn’t appreciate the Schadenfreude of beating one’s opponent in debate at such a renowned establishment, in the grand public arena no less? Both parties naturally agreed and brought their best case to the fore, however the result was an almost unanimous vote against the singular evolution of venom in reptiles (for a brief rundown, albeit from only Hargreaves pen since history is always written by the victorious, see link 20).
Credit must be given here, for as arguing against the establishment is difficult, the house almost always wins, and team Toxicofera obviously stuck to its convictions. The conclusions of Hargreaves and others on the other hand are increasingly hard to deny, as demonstrated by the thoroughly one sided final score. While a convincing victory, the Toxicofera proponents are by no means licked, and not yet abandoning their hypothesis due to the opinion of the masses, be they scientists or otherwise and further interesting research is undeniably in the works from both camps. For example, a recent combined molecular morphological study claims to have resolved the squamate phylogeny once and for all, coming down on the side of the Toxicofera, however this paper’s methods (including removing what they call “rogue” taxa which don’t conform in their phylogeny, a curiously convenient way to prune a tree) have been criticized (21). Why can’t it ever go smoothly?
So, the number of times venom has arisen in the reptiles remains unsettled. But where does this leave us with the unresolved squamate phylogeny? Here I believe, or at least hope that future evidence shows, that we can have our cake and eat it too, while not being venomous people. The Toxicofera clade seems to be consistently recovered by many molecular investigations, and the homology of some oral tissues and protein products seem to suggest shared ancestry. What is the problem with assuming a non-venomous role for these oral products, particularly in light of their low expression in glands and expression throughout the body? Could not such oral products still confer some selective advantage and lead to a successful clade of animals? If, for example, the common oral products of the Toxicofera are simple anti-microbial tools to protect the delicate mouth of the snake, which gave them an immune advantage that was inherited throughout the clade, then while the clade Toxicofera may truly define an evolutionary lineage, then only the implication in the name would be misleading. While a clade of successful reptiles with an improved ability to resists oral infections (I dub this hypothetical clade “Antimicrobifera”) may be a less captivating idea than the highly toxic or bacteria laden bite of the Komodo dragon, weirder things have happened.
But this is all conjecture. For now, we must satisfy ourselves with what we know; current molecular data indicates the Toxicofera may in fact be a real evolutionary grouping sharing a common ancestor, but whether they’re truly “venomous” as the namesake suggests remains to be proven. Until the function of these products is proven, I personally shall simply say they appear to be common in much of the putative Toxicofera group, for some reason or other. Vague I know, for vagueness is our refuge in the face of uncertainty, until sufficient evidence draws us out into the light. Such caution keeps theories alive in the face of predators, for the tastier the theory, the more they shall try to tear it to shreds.
A final thought on complexity. It is tempting to view venom systems as on an upward climb in complexity through the squamata (disregarding examples of degeneration). This view is in agreement with the parsimony principle, referring to finding the simplest solution, the smallest amount of evolutionary branches on the tree, as morphological and evolutionary changes do not happen lightly. However while organs can increase in complexity, it is more important to remember that evolution does not strive for progress, only survival and reproduction. Any “progress” we perceive in biological systems is merely a by-product of life’s branching nature and the great spread of variety and form, rather than a march towards some perfect animal or system. What intricacy life generates is not simply to increase in complexity towards a particular ideal; there is no ideal, or if there is it exists as a broad, fluctuating spectrum built atop a sliding scale, and even we humans can make no claim for superiority or perfection. This, at least, we share with all snakes, lizards, and the rest of life on Earth.
References
Wilson, S. & Swan, G. (2013) A Complete Guide to Reptiles of Australia; Fourth Edition. New Holland Publishing.
Cogger, H. (2014) Reptiles And Amphibians Of Australia; Seventh Edition. CSIRO Publishing.
Fry, B.G., Wroe, S., Teeuwisse, W., van Osch, M.J., Moreno, K., Ingle, J., McHenry, C., Ferrara, T., Clausen, P., Scheib, H., Winter, K.L., Greisman, L., Roelants, K., van der Weerd, L., Clemente, C.J., Giannakis, E., Hodgson, W.C., Luz, S., Martelli, P., Krishnasamy, K., Kochva, E., Kwok, H.F., Scanlon, D., Karas, J., Citron, D.M., Goldstein, E.J.,McNaughtan, J.E., Norman, J.A.. (2009) A central role for venom in predation by Varanus komodoensis (Komodo Dragon) and the extinct giant Varanus(Megalania) priscus. Proc Natl Acad Sci U S A.106:22
Fry, B.G., Vidal, N., Norman, J.A., Vonk, F.J., Scheib, H., Ramjan, S.F.R., Kuruppu, S., Fung, K., Hedges, S.B., Richardson, M.K., Hodgson, W.C., Ignjatovic, V., Summerhayes, R., Kochva, E. (2006) Early evolution of the venom system in lizards and snakes. Nature. 439, 7076.
Lumsden, N.G., Fry, B.G., Kini, R.M., Hodgson, W.C. (2004) In vitro neuromuscular activity of ‘colubrid’ venoms: clinical and evolutionary implications. Toxicon. 43
Kardong, K.V. (1982) The evolution of the venom apparatus in snakes from colubrids to viperids and elapids. Memoirs of the Institute of Butanan 46: 105–118.
Kardong, K.V. (1996) Snake toxins and venom evolution. Herpetologica 52.1
Jackson, K (2003) Evolution Of Venom-Delivery Systems in Snakes. Zoological Journal of the Linnean Society The Linnean Society of London, 137
Brusatte, S.L. , Benton, M.J. , Desojo, J.B., Langer, M.C. (2010) The higher-level phylogeny of Archosauria (Tetrapoda: Diapsida), Journal of Systematic Palaeontology, 8:1
Close, R.A., Friedman, M., Lloyd, G.T., Benson, R.B.J (2015) Evidence for a Mid-Jurassic Adaptive Radiation in Mammals. Current Biology Volume 25, Issue 16.
Engel, M. (2015) Insect Evolution. Current Biololgy. 25
Fry, B.G., Wuster, W., Ramjan, S.F.R., Jackson, T., Martelli, P., Kini, R.M. (2003). Analysis of Colubroidea snake venoms by liquid chromatography with mass spectrometry: evolutionaryand toxinological implications. Rapid Commun. Mass Spectrom. 17: 2047–2062
Vidal, N., Hedges, S.B. (2005). The phylogeny of squamate reptiles (lizards, snakes, and amphisbaenians) inferred from nine nuclear protein-coding genes. C R Biol. 328(10-11)
Weinstein, S., Keyler, D.E., White, J. (2012) Replies to Fry et al. (Toxicon 2012, 60/4, 434–448). Part A. Analyses of squamate reptile oral glands and their products: A call for caution in formal assignment of terminology designating biological function. Toxicon. 60(4)
Jackson, T.N.W., Caswell, N.R., Fry, B.G. (2012) Response to “Replies to Fry et al. (Toxicon 2012, 60/4, 434–448). Part A. Analyses of squamate reptile oral glands and their products: A call for caution in formal assignment of terminology designating biological function”. Toxicon 2012. 1-17
Weinstein, S.A., White, J., Keyler, D.E. (2013) Response to Jackson et al. (2012), Toxicon. 64.
Bonilla, C.A., Fiero, M.K., Seifert, W. (1971) Comparative biochemistry and pharmacology of salivary gland secretions. I. Electrophoretic analysis of the proteins in the secretions from human parotid and reptilian parotid (Duvernoy’s) glands. J Chromatogr. 56(2)
Hargreaves, A.D., Swain M.T., Logan, D.W., Mulley, J.F. (2014) Testing the Toxicofera: Comparative transcriptomics casts doubt on the single, early evolution of the reptile venom system. Toxicon. 92
“No one knows the diversity in the world, not even to the nearest order of magnitude…We don’t know for sure how many species there are, where they can be found or how fast they’re disappearing.” — Edward O. Wilson
Extinction is a bitch. Unless humanity has some serious new biological technologies which I’m yet to hear about, there is no return. The loss of a species is truly a terrible thing, an artwork of nature lost to the ages, leaving nothing but memories and, if we’re very lucky, some physical remains from which we may interpret the mode of their life and demise. In these marvelous times, the early 21st century, the rates of species extinction are unfathomable. I mean quite literally, it’s impossible to count exactly how many species at any given moment we are relegating to history’s dark corners through habitat destruction, overexploitation, and…well, let’s face it, I could list the ways humanity is contributing to this decline for the next the several pages (1). Furthermore, we don’t even know how many species of plants and animals currently exist, not to mention the unfathomable numbers of fungi, bacteria, archaea and viruses, all constantly mutating and evolving. With around 1.5 million species currently described, it’s astonishing that biologists predict at least one-third of all species remain to be discovered (2) (incidentally, we don’t even have a great idea how to define a species! See (3) for a review of this issue in the Bacteria and Archaea). Human nature, it seems, is often to simply proceed at will using ignorance as a map, until the stacking negative consequences force us to reign in our “progress” and examine our actions more objectively, a skill we are apparently developing when it comes to balancing our population requirements with those of other organisms and the planet’s natural resources.
What a depressing way to start! Kill me now, or let’s have some good news! Luckily, while we will discuss population declines and extinction, I truly do intend to discuss a rather more cheerful topic; the recent rediscovery of potentially extinct species. While tempting to view these situations as a somewhat miraculous, phoenix-like revival, they often share more in common with finding a mystery five-note in the back pocket…Score! Still, for conservationists who frequently are in the painful position to observe and record the decline of their favourite study species as they attempt recovery efforts (or at least learn something about how to prevent future declines in conspecifics), these discoveries are occasions for tremendous joy, even shock, like a long deceased friend contacting you out of the blue for a meal and a catch up. Even so, the joy is short-lived, for a species so rare it was thought extinct must be either especially cryptic and/or nearly impossible to find, that or it must truly be in critically low population numbers right on the brink of collapse, and extinction is still a real threat.
It is with thus with much joy and some trepidation that I write about the findings of D’Anastasi et al. (2016) (4) describing the discovery of not one, but two sea snake species, the Leaf Scaled Sea Snake (Aipysusrus folliosquama) and the Short Nosed Sea Snake (A. apraefrontalis), which recently disappeared from their only known geographic range. Both species were known only from the Ashmore and Hibernia Reefs, an isolated area of the Timor Sea, home to an incredible diversity of sea snakes. A study in 1973, for example, collected more than 350 snakes from 9 species and observed many more, while estimates of almost 40,000 snakes were made for Ashmore Reef in 1994 (5). However, populations of all sea snakes in the region began a steep decline for completely unknown reasons in the early 1990s, and continued to do so until several species disappeared completely. Neither of these species, known only from this tiny area of the Timor Sea, had been recorded in surveys since 2002.
The severe declines in these and other sea snake species on the reefs came along quickly. Further frustration and despair would’ve been in ample supply for the conservationists working on these isolated reefs, with no explanation for the declines, and no option but to observe and record the losses while searching for answers. Extinction seemed likely for these rare, open-ocean reef dwelling snakes (both were in fact listed as “Critically Endangered” on the IUCN Red List and Australia’s EPBC Act, one step shy of “Extinct in the Wild”, or when no individuals are maintained in captivity, “Extinct”). That is until the authors of (4) discovered both species not far off the northwest coast of Australia, around Western Australia’s Ningaloo Reef and further south at Shark Bay.
The paper by D’Anastasi et al. (2016) (4) from James Cook University’s ARC Centre of Excellence for Coral Reef Studies entails the search for and successful field observations of these species. After their disappearance and listing as Critically Endangered in 2002, no more sightings occurred in their known home range, though older anecdotal evidence suggested they may occur in coastal Western Australia (5). The most interesting evidence for their presence was from just one or two specimens of each species, deposited in the WA museum. A single A. foliosquama was found washed up on Barrow Island in 2010, with two A. apraefrontalis caught in 2012, one as prawn trawling by-catch and one washing up on a beach near Broome. These were mostly dismissed as probable vagrants, washed out of their natural geographic range by powerful ocean currents. However to others, this all suggested the possibility of undiscovered populations. Why not survey the coastline in the hope of discovering the hidden outposts of these rare sea snakes?
How does one go about mounting such a survey? With sweat, for one. Let it not be said that field biologists are lazy, particularly those who are fit enough to make the marine environment their office. Aside from the technicalities of mapping out and planning a thorough but efficient search, to cover maximum territory for optimal time/cost, the physical effort was incredible. Over 200 hours of survey were conducted at Shark Bay, Ningaloo Reef and other northwest coastal regions, as well as at the Scott Reef in the Timor Sea. The team performed more than 30 hours of both snorkel and scuba surveys, as well as over 25 hours of so called “Manta Tow” survey to cover a greater area. Developed in 1969 to assess crown-of-thorns starfish densities, this method involves towing a buoyant ‘manta board’, complete with waterproof recordkeeping sheets, behind a boat constant speed while a harnessed in observer clings to the board, using a snorkel and goggles to observe underwater as they pass. Around 40 hours by-catch prawn trawling surveys were also conducted around Shark Bay and Exmouth, and opportunistic sightings were also recorded wherever possible. As said by more than one field biologist in their time, the only way to find something is to look for it.
This mammoth effort was rewarded with gusto. Several individuals of the species Aipysurus apraefrontalis, the short nosed sea snake, were spotted around the Ningaloo Reef. Imagine the elation of finding this little known species of sea snake, 15 years after the last one was seen, 1700km south of its known distribution, and when all but a few were holding out hope for its continued existence. Not only that, two individuals observed appeared to be in the middle of courtship, hopefully a sign indicating a healthy breeding population. How very sweet for this stunning, golden yellow and cream banded sea serpent which had seemed destined to join the museum cupboards of the Dodo and the Dinosaurs. Further specimens were collected near Exmouth in WA Department of Fisheries prawn trawl by-catch surveys, another good indicator of a viable breeding population in the area.
But the story continues. The second discovery came only a few hours boating further south of Ningaloo. Another of Ashmore Reef’s lost sea snakes, the Leaf Scaled Sea Snake (Aipysusrus folliosquama), was found happily drifting among the sea grass flats of Shark Bay, a significant change from their typical setting of isolated coral atolls and reefs in the Timor Sea. To find this coral reef specialist in sea grass beds is very odd indeed, and the description as a shallow water tropical reef specialist requiring significant cover and structure will need some review. As with A. apraefrontalis, can we be sure this an established breeding population? While certainty is a rare commodity, a total of 16 A. folliosquama were caught in by-catch surveys between 2013 and 2015, all from Shark Bay and surrounding areas. It seems they hit the jackpot!
All’s well that ends well, no? In fact, not, and at this point some interesting questions start to arise. Ashmore and Hibernia Reefs supported diverse, abundant populations of sea snakes. For such seemingly successful animals in what appeared a very suitable habitat, how could such rapid population declines occur? What impacts are they under threat from in the waters off northwest Australia? Furthermore, now that we know they’re here just off the WA coastline, what can we do to minimize the stresses on these potentially new populations and increase their chances of survival? Can we prevent them from slipping away again?
In Australian waters, sea snakes themselves are not harvested for any commercial purposes, however through parts of southeast Asia there continues to be a small local market for sea snakes, usually for the colourful skins of sea kraits (sea snakes of the Laticaudidae subfamily, less common in Australia than in southeast Asia, all which lay eggs on land rather than on reef/rocky substrates like the Hydrophiinae subfamily, the true sea snakes), as an imported menu item, or for traditional medicine (6). Being in Australian waters, and since 1983 within the Ashmore Reef National Nature Reserve, direct harvesting is not likely to have much impact on these isolated populations, which are themselves classified as protected marine fauna under the Nature Conservation Act of 1992.
Trawl fisheries generally pose a much greater threat. Sea snakes need to surface to breath, using lungs which, aside from a few notable adaptations (extreme elongation, one dominant lung, a devascularised posterior “scuba tank” unique to sea snakes), are rather like ours. While they obviously possess a phenomenal breath holding ability, around 4 hours under optimal conditions, they can actually drown just like a person, dolphin, emu, or a crocodile. Add to this damage from being net-dragged across the benthos or crushed in a turbulent net by hundreds of kilos of rocks, crustaceans, and fish including sharks and rays, all struggling and making repeated attempts to escape, and the impacts of these fisheries are obviously a potentially serious threat (7).
Luckily the Ashmore and Hibernia Reefs have some reprieve from our constant plundering of the ocean. At least locally, the depth just off the edge of the coral platforms and the coral itself makes for difficult-to-impossible trawling conditions. Trawling is more difficult at depths and around structure, the potential for snagging and damage to the net being an important financial consideration. Furthermore the trawling rates and rates of decline do not correlate; while rates of trawling have remained relatively steady, sea snake numbers began to decline dramatically in 1994. Trawl fisheries, an initially likely culprit, seem to be in the clear for the moment.
So, direct human harvesting and the local trawl fisheries both seem to have little impact on these disappearing sea snake populations on the reefs. What then could have caused such rapid declines? Several possible causes, at very different spatial scales, are currently under suspicion; firstly, on the small scale of cells, tissues and organisms themselves, the potential for disease or demographic reasons for these declines has to be considered; secondly, on the middle scale, habitat loss might be to blame, with coral bleaching events occurring in 2003, though these could hardly cause the declines from 1994; on a large scale, environmental changes, such as shifts in temperature and/or prey abundance due to human induced climate change, are also on the suspect list (5). Investigations into these areas will hopefully provide much needed insight in the near future, maybe even an answer as to why these populations collapsed.
As for the newly discovered coastal populations, what can the observations tell us? One thing we can infer with some confidence, from the aforementioned courting/breeding pair of A. apreafrontalis spotted off Ningaloo Reef, and the substantial number of A. folliosquama found during the rather short survey, is that these are most likely true local breeding populations, rather than ephemeral waifs floating adrift on the currents, being fed into the survey areas from some outside source population. This is further supported by the apparent strong population structure of A. folliosquama, Shark Bay populations being genetically distinct from the washed up specimen from Barrow Island, itself distinct from historical Ashmore Reef samples. This all suggests that the Barrow Island specimen may be of a separate coastal breeding population, yet undiscovered. Along with the habitat extension, it seems that populations of A. folliosquama may really be out there in hidden in the WA sea grass beds, and A. apraefrontalis may be casually courting one another of Ningaloo and other reefs without our knowing! Unfortunately, while this is all rather hopeful conjecture, we can just as easily assume that whatever afflicted the Ashmore Reef populations can also affect these “unknown” populations, and they may disappear before we ever know they existed. One can rarely ever know what diversity and complexity has been lost, or how it was lost, without the benefit of painful hindsight.
If these populations are true, established breeding populations as we suspect, one troubling thought comes to mind. Despite the relative safety of the Ashmore and Hibernia Reefs from trawling impacts, the now known extension of these two species’ geographic ranges and habitat to coastal areas including sea grass beds, and the fact that the vast majority of specimens were caught in prawn trawl by-catch surveys, suggests the impact of trawling on coastal populations may be much higher. In fact, these coastal populations might naturally be subjected to all manner of man-made coastal disturbances, such as industrial/agricultural run-off, seismic activity from mineral and gas exploration, increased recreational activities such as boating and fishing to compete with, and much more. Being so isolated, it is easy to assume that the reef populations were somewhat protected from many of these activities, and yet they’re gone. What does this mean for our chances to protect the newly discovered coastal populations? With all the increased human impacts are we doomed to fail? Or, does their mere continued presence indicate some resilience, perhaps due to the amount of structural variation in coastal environments, or their sheer size and continuity around the coastline, which the outposts in the Timor Sea did not have?
In summary, we know little, as is most often the case. What we know is that we don’t know the true population size, distribution, or spatial ecology of these rediscovered sea snakes. More field observations are necessary to understand both the ecology of these populations and the threats they face, as well as surveys of other coastal areas for more unknown populations if we are to have a thorough inventory to base conservation efforts on. Such are the difficulties involved in working with rare animals and small population sizes. For now though, let us take five to give the fine people behind these discoveries, and to all who work with endangered species, fighting for tiny populations who persevere at the edge of oblivion, a seriously deserved round of applause. It is very close to the least we could do. We can, and should, do much more.
PS On further rediscovered reptile news…
As I write this essay another small step was made in restoring our reptile biodiversity! This time in the spotlight is a lizard species which, throughout my childhood, had been presumed extinct. The Pygmy Blue Tongue Lizard (Tiliqua adelaidensis) is a true pygmy of the robust and moderate sized blue tongue lizards. Within the Tiliqua genus most species reach over 40cm in length, while the T. adelaidensis tops out at a tiny 18 cm. After an absence from their native habitats for 30 years, the future seemed uncertain for these little gems. As a kid I knew them only from pictures of deceased museum specimens in my reptile encyclopedia, the status next to them reading “Presumed Extinct”. While well preserved, they were somewhat less inspiring than the rest of the creatures in the book, perhaps due to signs of dessication and rigor, and the final shame of a finely engraved voucher label attached to the hid legs, as if just another artifact of history. Then, while driving along a country road one day in 1992, a herpetologist outside of Adelaide accidentally ran over an eastern brown snake sunning itself on the road. Upon examination, he found two “extinct” T. adelaidensis inside its stomach. Not only that, surveys found local populations living in spider holes in the surrounding native grasslands, and study taught us much about their ecology (8).
As of January 2016, Zoos South Australia confirmed the successful captive breeding of the Pygmy Blue Tongue Lizard (9). Twenty years after first being fascinated and saddened by pictures of these creatures which I thought I would never see, I am currently sipping a cup of tea and looking at images online of newly born babies. The tiny, tiny offspring of this diminutive species of blue tongue are coloured more like some of our speckled Ctenotusspecies, but the stocky little body, small tail, and big head are characteristic Tiliqua. They’re damned cute. My first pets were also in the genus (mine were Southern Blue Tongued Lizards,T. nigrolutea), and I have an inordinate fondness for the Tiliqua, from the common garden visitors and the desert dwellers to this spider-specialist dwarf. To find both of these articles, the lizards and the sea snakes, making the rounds and gaining interest on social media networks, all in one week, caught me by surprise. Perhaps there is some hope for humanity after all.
Costelo, M. J. (2015) Biodiversity: The Known, Unknown, and Rates of Extinction. Current Biology 25, R362–R383
Rosselló-Móra, R. & Amann, R (2015) Past and future species definitions for Bacteria and Archaea. Systematic and Applied Microbiology. Volume 38, Issue 4, 209–216
D’Anastasi, B.R., Van Herwerden, L., Hobbs, J.A, Simpfendorfe, C.A., Lukoschek, V. (2016) New range and habitat records for threatened Australian sea snakes raise challenges for conservation. Biological Conservation. 194. 66–70
Lukoschek, V., Beger, M., Ceccarelli, D., Richards, Z., Pratchett, M. (2013) Enigmatic declines of Australia’s sea snakes from a biodiversity hotspot Biological Conservation 166. 191–202
Snakes On The Brain 