Thursday 26 April 2018

What sort of thinkers are today’s zoologists?

Bob Martin in 2013 at the Field Museum
Photograph by Yu Lao (Wikimedia Commons)

Some essays stand the test of time. One such is that written in 1976 by Bob Martin, then running the Wellcome laboratory at London Zoo and now Emeritus Curator at the Field Museum in Chicago. It was entitled A Zoologist’s View of Research on Reproduction and was based on the talk he gave at the symposium of the Zoological Society of London to celebrate its 150th anniversary. He took the opportunity to provide a wide-ranging forward look and asked how things would turn out in the future. Amongst those topics was this one:

At this point, it is relevant to consider some evidence concerning the psychological background to scientific research. In his studies of the mental aptitudes of schoolboys, Liam Hudson[*] (1966, 1968) drew a crucial distinction between "convergent" and "divergent" thinkers. The former performed well on standard IQ tests requiring specific answers to well-defined questions. The latter performed best on "open-ended" intelligence tests requiring imaginative answers to questions which did not prescribe specific answers. This distinction, which is usually one of degree rather than sharp demarcation in individual cases, is in some ways parallel to a distinction between "specialists" and "generalists". As a rule, Hudson's convergent thinkers were more likely to study science at university, while divergent thinkers were more attracted to arts subjects. It is interesting, however, that zoology seemed to attract convergent and divergent thinkers in roughly equal proportions (or people who combined aptitudes in both directions). Different interpretations may be drawn from this observation. It could be said that zoology as a subject attracted a proportion of divergent thinkers because it traditionally lacked the apparently sharp scientific rigour of the physical sciences. At the same time, it is probably true that zoology as a subject has owed many of its major advances to the flair and imagination of those who could both identify and dissect general principles despite the complexities of whole animals in their natural habitats. The question that remains to be answered is: does the future development of zoology depend upon the same aptitudes as the past? For those who view zoology as a domain to be progressively replaced by current approaches to molecular biology, the answer is probably "No". For those who see in zoology a hierarchy of general principles, only some of which may be "explained" in molecular terms, the answer is probably "Yes". Whatever the answer may be, it would seem to be true that the greatest promise for future developments in zoological research lies in a combination of "divergent" and "convergent" thinking. Technical expertise and knowledge of fundamental life-processes should ideally be matched by a comprehensive understanding of whole animals and their interactions in natural environmental systems.

Since 1976 there has been a progressive horizontal slicing of the biological sciences, rather than the vertically integrated, explanatory reductionist approach of the zoologist of the middle of the 20th Century. I warned of this problem in a commentary I wrote in 1989:

It is a strange aspect of scientists’ behaviour that they condemn work at the levels of complexity above that at which they work as out-of-date and as mere natural history. Unfortunately, the divisions and intellectual isolation that lead to these attitudes appear to be increasing as universities reorganize their administrative and teaching structures for the biological sciences. The fashion is for organismal biology to be split from the rest of the biological sciences, while cell biology and molecular biology are being isolated at the other end of the scale. Thus the new disciplines are becoming horizontal divisions corresponding to the level of biological complexity…

It is true that organismal biologists have made more and more use of molecular techniques but the intervening levels like physiology have been pulled either upwards or downwards to an extent such that in Britain at least, comparative physiology has virtually disappeared and explanatory reductionist approaches abandoned.

But what of the people, to return to Bob Martin’s question? Are those working at the molecular and cellular levels of biological organisation more likely to ‘convergent’ and those working  on whole animals in their environment ‘divergent’ thinkers? And are we getting the right people into the right jobs? The latter is an important question because what has not changed is the fact that the subject studied at school, for example biology, will bear very little resemblance to that subject at university level even allowing for the fact that different university departments have different emphases and interests.

*1933-2005. Obituary - see here.

Martin RD. 1976. A Zoologist’s View of Research on Reproduction. In, The Zoological Society of London 1826-1876 and Beyond. Ed. Zuckerman. Symposia of the Zoological Society of London 40, 283-319.

Peaker M. 1989. Commentary: Molecular endocrinology: a welcome extension to, but not a replacement for, endocrinology. Journal of Endocrinology 120, 361-362.

Sunday 22 April 2018

The Complicated History of Monkeys in Hong Kong

There are monkeys in Hong Kong. Forget Hong Kong Island for the time being—in the first part of this article I am concentrating on ‘New’ Kowloon and the New Territories. Unfortunately, the view has been promulgated by some primatologists that these monkeys have been present continuously from before the Second World War, either as original inhabitants or as the result of introduction in the early years of the 20th Century. Sadly, this story seems to have been accepted by the Hong Kong Government’s Agriculture, Fisheries and Conservation Department as the explanation, in part, for the current population of monkeys.

Mainland Hong Kong

The monkeys which at present inhabit the country parks are Rhesus Macaques (Macaca mulatta) or crosses between Rhesus and Long-tailed (also known as Crab-eating) Macaques (M. fascicularis) together with Japanese Macaques (M. fuscata). Because they have been fed by the human population (feeding is now illegal) they make a thorough nuisance of themselves by lining the paths at weekends and stealing food with menaces from passers-by. The males can also be aggressive.

Hong Kong is well within the natural range of the Rhesus Macaque and there are records from the 19th Century. However, it seems that the numbers decreased possibly because of hunting for food as the human population increased. In the early years of the 20th Century Rhesus Macaques were imported and released in the area of the newly-constructed Kowloon reservoir for a bizarre reason. There was concern that fruit from overhanging strychnine trees would fall into the water and poison the public. Because monkeys were thought to be able to eat the fruit without ill effect, some Rhesus Monkeys were introduced in order to reduce the risk of poisoning those drinking the water.

However—and this is the big however—Rhesus Monkeys—and note Rhesus—whether remaining wild or the introduced population appear to have died out completely by the late 1950s to early 1960s. They may have been present in the late 1940s in small numbers. Herklots wrote in his book The Hong Kong Countryside (completed and published after he left Hong Kong in May 1948):

The monkeys that live in the woodland near the Kowloon reservoir are not descendants of the wild stock but of monkeys released during the first world war. During the Japanese occupation of the Colony in the second world war, after the trees had been cut down, the surviving animals scattered. Since the war they have been reported from several districts in the New Territories including their old haunts…

My guess is that the Rhesus Macaques were hunted to extinction or near extinction during the Japanese occupation. Monkeys did feature in Cantonese cuisine and medicine and, moreover, the population was short of food as all accounts of life during that period testify.

The naturalists around in the mid-1960s all seemed to agree that the Rhesus Macaque was extinct in mainland Hong Kong. However, there were monkeys around Kowloon reservoir but of an entirely different species: the Long-tailed Macaque*.

There is also the possibility that Herklots’s book was misleading. When as described above, he wrote that monkeys had been reported in the New Territories after the Second World War it is possible that what had been seen in the late 1940s and early 1950s were not Rhesus Macaques but Long-tailed Macaques. 

In the mid-1960s Patricia Marshall of the Zoology Department wrote in her book, Wild Mammals of Hong Kong (published in 1967):

The group of monkeys living in the Kowloon reservoirs catchment area are long-tailed macaques which were probably released or escaped from captivity during or shortly after the 1939-1945 War. The rhesus monkey (Macaca mulatta) which was once abundant on Hong Kong island and in the New Territories now appears to have died out.

These are photographs I took in December 1967 of the Long-tailed Macaques at the well-known spot near Kowloon reservoir at the 4½ milestone on the Taipo Road:

Long-tailed Macaques near Jubilee Reservoir
on the Taipo Road. December 1967

Later, Rhesus Macaques re-appeared. In 1976, Valentine Lance, also then in Zoology, surveying  the land vertebrates of Hong Kong wrote:

On a bright note in this sad tale is the addition of an animal once lost from Hong Kong and now successfully re-established. This is the Rhesus Monkey (Macaca mulatta). In 1866 Swinhoe noted that they were common on most of the small islands near Hong Kong…and number of them lived in Tai Tam before the second World War. By 1962 they were no longer present in the Colony. Another closely related species, the Crab-eating or Longtailed Macaque (Macaca fascicularis), a more southern common Malayan monkey, successfully established a breeding colony at Kowloon Reservoir (Romer, 1966). This group originated from escaped or released pets. Today there is a flourishing colony of more than twenty individuals in the Kowloon Reservoir catchment area. The rhesus monkeys have only successfully established themselves in the same area in the past few years. Again they are escapees. The criteria for establishing residence is successful breeding. A family with a young baby was seen recently and there are believed to be more breeding pairs in the same area. The two species seem to live fairly amicably side by side in the same restricted habitat. In addition to the colony at Kowloon Reservoir isolated individuals have been seen at Pokfulam Reservoir [Hong Kong Island], Tai Tam Reservoir [Hong Kong Island], and recently at Ma On Shan.

All this seems pretty clear: the present Rhesus Monkey population appears to be derived from animals that escaped or were released in the late 1960s or early 1970s. Unfortunately, as is so often the case, other researchers have not read the relevant literature and ascribe the monkeys to descendants of the pre-Second World War population. Such errors and misinterpretations which omit mention of evidence from the 1960s are, of course, repeated and repeated not only websites, in publications and in newspaper articles but in books on primate conservation. For example, in one relatively recent book it is stated that the introduced Long-tailed Macaques interbred with the existing population of Rhesus. Photographic and observational evidence from the mid-1960s shows that not to be the case; the Long-tailed Macaques were not interbreeding at that time since they alone occupied the Kowloon Hills. Nevertheless, it is true, as David Dudgeon and Richard Corlett remarked in their excellent book on the ecology of Hong Kong, ‘we cannot be certain…that none of the current population are descended from survivors of the original Hong Kong macaques’. The negative is impossible to prove but the probability is highly weighted against a remnant population.

Since the 1970s the population of Rhesus Macaques has increased massively. By 1992 there were around 800 macaques in Hong Kong, 700 of them in the Kowloon Hills and other country parks. But they were not all Rhesus or Long-tailed. Other species kept for some reason either escaped or were released. There are records of Japanese Macaques, Tibetan Macaque (M. thibetana) and a single Pig-tailed Macaques (either M. leonina or M. nemestrina). Hybridisation between three of these species is known, with the production of fertile offspring. (There is a hybrid zone, in northern Thailand, for example, where the Rhesus and Long-tailed meet naturally.) A survey by John Fellowes for the World Wildlife Fund in 1992 found evidence of four species and possible hybrids, as far as they could be identified: Rhesus (pure) 50% of the population; Long-tailed x Rhesus or x Japanese 40%; Japanese (pure) or Japanese x Rhesus 9%; Long-tailed (pure) 1%; Tibetan (0-1%).

The number of Long-tailed Macaques was said to have declined in 1967. Reports in the newspapers blamed trappers for catching the monkeys and selling them as a delicacy for human consumption.  However, there seemed a healthy population in December 1967 when we watched them. In the 1980s in the Kowloon reservoir area, the proportion of Long-tailed in the monkey population fell from 26% to 7% between 1981 and 1987; hybrids between these two from 13 to 3 while the Japanese Macaques fell from 5% to 0.

It appears then that the Long-tailed Macaque population has virtually disappeared together with easily-recognisable hybrids. How much of the Long-tailed genome is present in the present Rhesus population seems to be unknown. Since large traps are available from the sterilisation programme aimed at keeping the population in check, molecular studies are just waiting to be done. But as Dudgeon and Corlett state: ‘It would be interesting to know if the predominance of rhesus macaques reflects a larger founder population (i.e. more releases or survivors) or superior adaptation to an environment which is within the native range of the species’.

Were the Rhesus and other species of monkey recorded escapees or were they released? Explanations I have seen include release by a travelling circus after being prevented from taking the animals to the next destination. Did some escape from food markets? Did well-intentioned individuals buy some from pet shops or markets and release them? Did pet owners release adult monkeys when they turned vicious? Did some escape from private collections?

I do get the impression that the Rhesus Macaques must have been released in substantial numbers, says tens at least, to have multiplied so rapidly and so visibly, rather than in the dribs and drabs of the odd pet escaping or being released and then finding the troupe of Long-tailed Macaques to join. I awoke the other night with a possible explanation. When we arrived in Hong Kong in November 1965, John Phillips (1933-1987, FRS 1981 and later of the University of Hull and Vice-Chancellor of Loughborough University) my PhD supervisor was Professor of Zoology. He told me to get an animal experimentation licence from the government. The government had recently introduced licensing, he said, because some commercial animal testing operations had set up in Hong Kong in order to bypass legislation in their countries of origin and the Hong Kong government wanted to make sure nothing untoward was going on. Yesterday I checked my memory and, indeed, the Animals (Control of Experiments) Ordinance was passed into law on 24 May 1963; it is still in effect. I knew nothing of these laboratories and I don’t think John did either but is it just possible that they had the favourite and cheap primate of the time, the Rhesus Monkey and that after ceasing operations considerable numbers were released into the New Territories?

I know that possible explanation is a long shot but I was intrigued by a paragraph in John Fellowes’s report from 1992. In Tai Po Kau forest reserve, the population seemed to be entirely Rhesus and he wondered if that could reflect a relict population. However, Tai Po Kau was well visited by birders and other naturalists in the 1960s who would surely have spotted a troupe  of monkeys. Is it just possible that the main release of Rhesus Macaques was at or near Tai Po Kau, and that some then made their way to the Kowloon Reservoir area where they found and interbred with the Long-tailed Macaques?

One possibility that I have never seen discussed is that the 'new' wave of Rhesus Macaques from the late 1960s/early 1970s actually arrived from a wild population across the border. By 1985, the nearest wild populations were a long way away in Guangdong or on islands but who knows about the 1960s? Looking at China then from the lookout at Lok Ma Chau, there was just farmland and woods. Could the woods have held a population of monkeys even ones that could have made their way there from Hong Kong in the early decades of the 20th Century?

In summary, the present Rhesus Macaque population of mainland Hong Kong has an interesting history and genetic origin. With molecular techniques already used on two of the species involved†. it should be possible to determine to what extent, if any, the genome of the other macaques (other than the Tibetan which did not appear to have interbred) is still present in the gene pool as well as the size of the founder populations. It is also possible that the geographical origins of the Rhesus Macaques could be determined; are they originally from China or elsewhere in the range, India, for example, which was a major exporter at that time?

Hong Kong Island

Herklots wrote:

On the Island of Hong Kong a monkey family was watched early one morning near Tai Tam reservoir in 1947, and I have had occasional accounts of monkeys having been seen on the Peak and in Deep Water Bay valley. It is possible, but not certain, that these are descendants of the original wild stock [i.e. Rhesus Macaques]…

The monkeys at Tai Tam seem to have disappeared by the early 1960s. Patricia Marshall considered the monkeys on Hong Kong Island, like the Rhesus on the mainland, to have died out. However, monkeys were seen on the Island throughout the 1960s after she wrote her book. There were newspaper reports and a recent request for information from the Facebook Group, Hong Kong in the 1960s, confirmed the presence of small numbers monkeys around various blocks of flats. Lancelot Vance also reported the sighting of individual animals at Pokfulam reservoir and at Tai Tam reservoir. In 1969 a monkey living on Bowen Road was shot by John Romer after it bit a child. There was a considerable fuss in the letters columns of the South China Morning Post. Sightings continued throught the 1970s into the 80s.

The question, as usual, is, were the sightings in the 1960s of descendants of the family group Herklots had seen or of monkeys that had escaped or had been released into the wild more recently? The question is, of course, unanswerable but there were certainly plenty of opportunity for the latter. The British army’s Lyemun barracks had a small zoo; Rhesus Macaques bred there in 1962. Other individuals had wild animal collections in the 1960s and 70s including a Dr Vio who lived on the Peak. The PG Farm, on the site of Ocean Park, a popular attraction for children in the 1960s, had Rhesus Monkeys; at least one escaped—and was recaptured. There were newspaper appeals for people not to keep monkeys as pets. It is fair bet that a few escaped from owners or were released after a first—and usually inevitable—bite.

I have not seen any recent reports of monkeys on Hong Kong Island.

Opportunities for Research

‘Natural’ experiments such as the various introductions of macaques in Hong Kong offer opportunities for research. I have outlined some of the lines which could profitably be pursued and which would throw light on the selective pressures operating to favour, perhaps, the originally native Rhesus Macaque over the closely-related Long-tailed. But as I have also pointed out, we might also get an indication of the origin or origins of the currently highly successful population of Hong Kong monkeys.

And finally…

A photograph of a Rhesus Macaque almost exactly 50 years since I photographed the Long-tailed Macaque within a few hundred metres of this one.

Rhesus Macaque near Jubilee Reservoir catchment. November 2017

*The Hong Kong Government only appears to have realised this in 1966 with the publication of Romer’s note. The Annual Report for 1965: Rhesus monkeys are still found in the vicinity of Kowloon Reservoir in the New Territories, but those which inhabited woods in the Tai Tam area of Hong Kong Island are not known to have been seen during 1965. The 1966 Report had the nearly correct story: Long-tailed or Crab-eating Macaques, a sub-species of those found in Singapore, occur in small numbers in the Kowloon reservoir area and can often be seen near the Kowloon-Taipo Road and at Pipers Hill. These are probably descendants of escaped or released individuals. The indigenous Rhesus Macaques which were present on Hong Kong Island and in the New Territories have now apparently disappeared. No source of information is given in the 1965 Report but the 1966 Report acknowledges the help of Patricia Marshall for the section on wild life.

†Bunlungsup S, Kanthaswamy S, Oldt RF, Smith DG, Houghton P, Hamada Y, Malaivijitnond S. 2017. Genetic analysis of samples from wild populations opens new perspectives on hybridization between long-tailed (Macaca fascicularis) and rhesus macaques (Macaca mulatta). American Journal of Primatology 79. doi: 10.1002/ajp.22726

Dudgeon D, Corlett R. 1994. Hills and Streams. An Ecology of Hong Kong. Hong Kong University Press.
Fellowes JR. 1992. Hong Kong Macaques. Final Report to the WWF Hong Kong Projects Committee. Hong Kong: WWF.
Herklots GAC. 1951. The Hong Kong Countryside. Hong Kong: South China Morning Post.
Hong Kong. Report for the Year 1965. 1966. Hong Kong Government Press.
Hong Kong. Report for the Year 1966. 1967. Hong Kong Government Press.
Lance VA. 1976. The land vertebrates of Hong Kong. In, The Fauna of Hong Kong, edited by B. Lofts. Hong Kong: Hong Kong Branch of the Royal Asiatic Society.
Marshall PM. 1967. Wild Mammals of Hong Kong. Hong Kong: Oxford University Press.
Romer JD. 1966. Long-tailed Macaques in Hong Kong. Memoirs of the Hong Kong Natural History Society 7, 16. I have not been able to track down an easily accessible copy of this paper; therefore I have not read it.
Southwick C, Manry D. 1987. Habitat and population changes for the Kowloon macaques. Primate Conservation 8, 48-49.

Updated 24 April 2018

Monday 16 April 2018

Huxley v Wilberforce. How a provincial newspaper reported the Oxford debate of 1860

Any sense of achievement gained from doing a job once done by Thomas Henry Huxley—Vice-President of the Zoological Society of London—is at once nullified by the knowledge that another predecessor was the ‘unctuous, oleaginous, saponaceous’ Samuel ‘Soapy Sam’ Wilberforce, Bishop of Oxford and later Lord Bishop of Winchester.

New light on who said what at and when at the famous 1860 British Association meeting in Oxford during the famous debate on Darwin’s work was published last year in Notes and Records of the Royal Society in a paper by Richard England.

After the debate, what was said was largely passed by word of mouth since the semi-official record in The Athenaeum magazine (eventually merged into what is now the New Statesman) was censored in order to remove material that was considered objectionable in that it emphasised the chasm between science and faith and, given the morality of the day, a little risqué on account of Wilberforce’s question to Huxley. However, it has now been found that the Oxford Chronicle carried a much fuller account which does contain Wilberforce’s ape as grandfather or grandmother jibe and Huxley’s devastating riposte:

…Glancing at Professor Huxley’s remarks, on the previous day, in a discussion with Professor Owen, the Bishop facetiously asked if he had any particular predilection for a monkey ancestry, and, if so, on which side - whether he would prefer an ape for his grandfather, and a woman for his grandfather, or a man for his grandfather, and an ape for his grandmother. (Much laughter.)…

Wilberforce continued with his diatribe so the rejoinder when it came was not so spontaneous as some of us may have thought. But it did come:

Professor Huxley followed. In reply to the Bishop’s query he said that if the alternative were given him of being descended from a man conspicuous for his talents and eloquence, but who misused his gifts to ridicule the laborious investigators of science and obscure the lights of scientific truth, or from the humble origin alluded to, he would far rather choose the latter than the former. (Oh. oh, and laughter and cheering.)…

It is often remarked that in later years Wilberforce and Huxley served together on the Council of the Zoological Society. But in that mannerly fashion that can still be found, if less commonly, in academia and public life, I cannot but wonder what Huxley actually thought of having to deal with Wilberforce whom he had, by implication, described in Oxford as an amateur in science.

The famous Vanity Fair cartoons of Wilberforce and Huxley by
Carlo Pellegrini (1839-1889), 'Ape'

England R. 2017. Censoring Huxley and Wilberforce: A new source for the meeting that the Athenaeum ‘wisely softened down’. Notes and Records of the Royal Society 71, 371-384. DOI: 10.1098/rsnr.2016.0058

Friday 13 April 2018

Spring in Hong Kong: Brown Tree Frog

April is the height of the breeding season for many Hong Kong amphibians. Our correspondent found this Brown Tree Frog (Polypedates megacephalus) in the bushes of a garden in Kowloon Tong earlier this week.

This species is a foam nester positioning the nest of foam whipped up by the hind legs above the water line on a branch or on the side of a tank or a well.

Monday 9 April 2018

Time to kill off the term ‘brumation’ for hibernation in reptiles

Amateur herpetology circles and zoo keepers tend to obsess over using the term ‘brumation’ instead of hibernation for what reptiles and amphibians from temperate climes do in winter. In fact the internet is infested with those correcting others on what they see as an error of terminology.

"Bill" Mayhew
From here
Brumation was a word coined in 1965 by Wilbur "Bill" Waldo Mayhew (1920-2014) of the University of California at Riverside as a result of his work on hibernation in the Flat-tailed Horned Lizard, Phrynosoma mcallii (then known as P. m’calli). Mayhew was working in the heyday of research on thermoregulation and metabolism in lizards. He had arrived at the new campus of Riverside in 1954 after education (BA, MA, PhD) at Berkeley under the G.I. Bill. He had a distinguished war record as an air gunner in B17 (Flying Fortress) and B24 (Liberator) bombers in North Africa, China and Burma*.

Mayhew called his lizard an ‘obligatory’ hibernator because no matter what the outside temperature was, those kept in his laboratory ceased to eat and became torpid at the onset of winter. Other lizards—‘facultative’ hibernators could be kept active all winter by maintaining a high temperature. Mayhew recorded that metabolic rate (oxygen consumption) fell to an extent greater than that which would be expected from a fall in environmental temperature. For example, if the lizards were cooled during summer, metabolic rate fell but not to the extent seen in winter at the same body temperature. In other words, hibernation is some special physiological process that alters the normal relationship between body temperature and metabolic rate.

Phrynosoma mcallii
Photograph by Gary Nafis (
A decrease in metabolic rate independent of a decrease in temperature means of course less energy expenditure even if the temperature of the hibernaculum is high in the desert sunshine of autumn or early spring. In terms of running off body stores to maintain life during winter, a metabolic rate lower than that brought about simply by a fall in temperature would be of obvious survival value.

In the summary of his paper, Mayhew wrote:

The term brumation is proposed to indicate winter dormancy in ectothermic vertebrates that demonstrate physiological changes which are independent of body temperature.

In the paper itself he expanded that argument:

Results to date show that relatively complex physiological changes occur during or immediately preceding winter dormancy in some ectothermic vertebrates. To this extent, these animals are similar to hibernating birds and mammals. However, they differ from these heterotherms (see Cowles, 1962) in their inability to control their body temperatures. Consequently, it seems advisable to have one term to designate winter dormancy in heterotherms and another for such ectotherms. Hibernation has been used to denote this condition in heterotherms particularly, so it seems best to retain this term for that group of vertebrates. Therefore, I propose the term brumation (from bruma, L. winter) to indicate winter dormancy in ectothermic vertebrates that demonstrate physiological changes which are independent of body temperature.

Now, there are three points. Firstly, the similarity between ‘heterotherms’ and Mayhew’s ectotherms is greater than the difference. Both have mechanisms to lower metabolic rate, irrespective of the body temperature. Secondly, Mayhew’s definition limits it application to reptiles, or amphibians, or fish, in general since it applies to those ‘that demonstrate physiological changes which are independent of body temperature’. Mayhew did not know what happened in other reptiles—or amphibians—or fish. To apply ‘brumation’ to all would imply one adaptation for hibernation in all poikilotherms and that notion would need to be tested in a wide number of species. Thirdly, I have found nothing to suggest that Mayhew himself intended his term to apply to all reptiles or all poikilotherms. Therefore, if you use the word hibernation to describe winter dormancy, which makes no assumption about the physiological mechanisms involved, you will never be using the wrong term; with brumation you may well be wrong.

Others have questioned, indeed, slightly ridiculed, Mayhew’s now 50-odd year old neologism, as explained here in what seems to be a defunct blog.

This house gecko, Hemidactylus bowringii, I photographed
in Hong Kong in 1966
I was reminded of my long-standing objection to the use of brumation when I found in a pile of papers the notes for a talk I had given in May 1967 to the Hong Kong Natural History Society. I must have just read Mayhew’s paper because I asked the question not only what happened to reptiles during the winter in Hong Kong but also what happened to their metabolism. The reason I did so is because Hong Kong lies just within the tropics but does experience spells of relatively cold winter weather. Hibernation, I argued, would be short and perhaps interrupted. Indeed, when I was looking up John Romer’s early herpetological activities in Hong Kong during the late 1940s, I came across his observations:

In the colder weather [in Hong Kong] geckos either disappear altogether into hibernation or are very much less active. Here is my house there are several specimens of our very common house gecko, Hemidactylus bowringii and since their disappearance into hibernation last year I noticed two of these for the first time on the 15th February. I did not see either of them again until the 29th February [1948 was a leap year] when one of them was seen. They seemed to disappear again until the 7th March and were then seen quite frequently always in the same part of the house.

The question I asked then—and still have no answer now—is whether Hong Kong reptiles and amphibians faced with variable winters of relatively short duration behave like the North American desert lizards studied by Mayhew and others, in that they have a mechanism to lower their body rate independently of their body temperature, i.e. brumate by Mayhew’s definition, or do they simply lapse into cold torpor for a few weeks or even days, with their metabolic rate simply matching the decrease in temperature?

Golden Kukri Snake. Just off Route Twisk near the road to
the summit of Tai Mo Shan. 1968
But there is a second question. Do all Hong Kong reptiles and amphibians use the same mechanism to cope with low winter temperatures? House geckos living on, say, the tip of Kowloon near the sea could face a very different set of circumstances from the Golden Kukri Snake (Oligodon cinereus) we found in 1968 at about 500 metres altitude just off Route Twisk or the Mountain Pit Vipers (Trimeresurus monticola) found around 900 metres on Tai Mo Shan where frosts are sometimes recorded.

In summary, brumation: (i) unnecessary since it has no explanatory value (ii) can, possibly, be positively misleading when applied indiscriminately, (iii) time, therefore, for the term to join the dead parrot in the choir invisible.

My binning of brumation in no way detracts from the work that Mayhew did nor his reputation as a  physiological ecologist and academic field naturalist. He was a co-founder of the University of California’s Natural Reserve System for field studies. A dormitory for visiting scientists on the Philip L. Boyd Deep Canyon Desert Research Center is named in his honour, as is a new chair in the university.

*In his retirement he wrote Pictorial History of the 7th Bombardment Group Wing 1918-1995, published in 1998.

Mayhew WW. 1965. Hibernation in the horned lizard, Phrynosoma m'calli. Comparative Biochemistry and Physiology 16, 103-119.

A useful summary of the early work on hibernation in reptiles:
Bennett, A. F. and Dawson, W. R. (1976). Metabolism. In Biology of the Reptilia, Vol.5 (ed. C. Gans and W. R. Dawson), pp.127 -223. London, England: Academic Press.

Saturday 7 April 2018

Two jaguars on a quiet river in the Brazilian Pantanal

We set off before dawn from South Wild on the banks of the Pixaim River. This time, in contrast to previous days, we were being paddled along in silence. You can see what happened next in this video, my best example yet, of slow, relaxed wildlife watching:

We had already had 16 sightings of at least 10 individual jaguars further south, so the sighting of this mother and daughter was completely unexpected and a spectacular finale to our trip.

Thursday 5 April 2018

Oldfield Thomas. Mammalogist and Valetudinarian

This story does not end well. 

In my previous post on Chinese species of pika I mentioned that Thomas’s Pika (Ochotona thomasi) had first been described in 1948 by the Russian zoologist A. I. Argyropulo in memory of Oldfield Thomas of the Natural History Museum in London. Thomas himself had named the Tsing-ling or Qinling Pika, Ochotona syrinx, in 1911.

Michael Rogers Oldfield Thomas (1858-1929) was elected to the Royal Society in 1901. Along with several other museum workers of the time he had no university degree. He was extraordinarily prolific. He was author of 1,090 publications and proposed 2,900 new names for genera, species and subspecies.

Oldfield Thomas
Painting by John Ernest Breun
Courtesy of the Natural History Museum

Nearly 90 years after his death, his obituaries shed light on a very different world. For the Royal Society his memorial memoir was signed, appropriately for such a rôle, ‘R.I.P.’ Those were the initials of his colleague and friend, Reginald Innes Pocock FRS.

Pocock wrote that Thomas was always known by his third name, Oldfield. Indeed, he appears without the first two names in official records such as national censuses. In 1876, after school, he got a job as a clerk in the British Museum (Natural History), as it was then known, when it was still physically part of the British Museum in Bloomsbury. He attended T.H. Huxley’s lectures and in 1878 was transferred to the zoological staff as an Assistant. He was greatly disappointed though when Albert Günther, Keeper of Zoology, moved him from invertebrates to be put in charge of mammals. He stayed with mammals and at the grade of assistant for the rest of his life despite every effort made to get him to accept a senior post.

I will not dwell on Thomas’s work at the museum other than to point out that he was responsible for introducing the American system of collecting for a museum, one begun by Clinton Hart Merriam (1855-1942) on the mammalian fauna of North America. That involved the large scale collection of specimens in order to throw light on such topics as geographical variation. The cost involved in such intensive collection was much greater than that needed to finance the steady trickle of specimens from overseas expeditions and residents. Fortunately, for Thomas, the financial problem was solved by his marriage.

In 1891 Oldfield Thomas married Mary Kane Clark, the daughter of Sir Andrew Clark, Baronet, President of the Royal College of Physicians and a Fellow of the Royal Society. Clark had become one of the most fashionable physicians in London. When he died in 1893, he had made a fortune and Mrs Thomas became a very rich woman. The Thomases had no children but they used her money to support the museum by recruiting an army of collectors overseas (recruited from local residents, colonial officials and big game hunters, for example) and a number of volunteers and paid visiting scientists to work on the mammal collection with Oldfield. 

The extent of the family fortune can be judged by his legacy, also used to support the Museum. As a widower, at probate he left £44,000, the equivalent of about £2.6 million today, even after his support for many years of what would now be called his own research programme. As well as his solicitor the other executor of will was another friend and fellow mammalogist, Martin Alister Campbell Hinton FRS (1883–1961); Hinton wrote the Thomas’s obituary for Nature.

This is what Pocock wrote for the Royal Society:

     Since I knew Thomas intimately throughout the greater part of his indus­trious life, perhaps some personal impressions of him, written with as little bias as a close friendship of forty years permits, may be of interest. I joined him as a colleague at the Natural History Museum late in 1885. At that time, when he was verging on 30, he was like the average young Englishman of the period who had been brought up in a well-ordered household of gentle people, had found his level at a public school, learnt the bad taste of self-advertisement and acquired the quality implied by the expression "fair play”. But his mind was rather of the practical and methodical than of the intellectual or aesthetic type ; and he had profited only to a small extent by the educational system then practised. He had no appreciation of literature, classical or otherwise; and neither then nor subsequently did the perusal of imaginative prose, novels or poetry give him any real pleasure or satisfaction, his reading, such as it was, being restricted mainly to the newspaper, an occasional magazine or volumes of travel. His disposition was eminently sociable. He preferred conversation and argument to books; and aversion to solitude, a curious trait in his character was evinced by his liking for the presence of someone, if only a clerk, in his room when he was hard at work, and by his invariable choice of an occupied carriage when travelling by train. He liked music in a measure; but his faculties in that direction were not of a high order. In no sense of the word was he artistic. He could neither draw nor paint, nor tell a good picture from a bad one. It cannot even be claimed for him that he was a naturalist in the broadest sense of the word. Beautiful scenery or a night of stars had no special attraction for him, and he was bored by the sea, unless there was shipping to watch, a boat to sail or fish to be caught from a smack. He was uninterested in the geology of the countryside, knew next to nothing of its flora, and very little of its fauna.* As a field naturalist he was rather a collector than an observer. But collecting was, I think, mainly, if not solely, a pleasurable pastime to him when it served the definitely practical purpose of providing for himself or his colleagues specimens which he knew would be useful for work.
     I have dwelt at some length upon Thomas’s limitations with regard to interests and pursuits because of the important bearing they had upon the latter half of his life. But while still a comparatively young man he was at no loss for recreations. He had an innate proficiency for games, both outdoor and indoor, involving accurate adjustment of eye and hand, like cricket, lawn tennis and billiards. He was also a keen Volunteer in the Artists’ Corps, and a very tolerable marksman. Lacrosse and golf he also played for a short time ; but the game best suited to his temperament was croquet, which he was happily able to keep up to within six months of his death, spending most of his summer afternoons at Roehampton and devoting his holidays to tourna­ments at Bournemouth or similar south-coast resorts.
     In 1891 he married Mary Kane, the daughter of the late Sir Andrew Clark. She was a charming lady of the Victorian type, a good amateur pianist and artist, with literary tastes and orthodoxly religious, his complete opposite in many ways. Unfortunately they had no family; and his wife’s inheritance of a small fortune a few years later placed Thomas in a position of complete independence of the struggle to make both ends meet, to which most scientific men are subjected, thus freeing him from the necessity of supplementing his income by popular writing or lecturing and enabling him to refrain from seeking higher distastefully administrative appointments  at the Museum to which his seniority entitled him.
     To fame and social advancement Thomas was supremely indifferent. Well aware of his own limitations, he was entirely without conceit, never tried to impress by pretentions of any kind and was generously appreciative of ability in others. He was also mentally alert, gifted with a fund of shrewd common- sense and penetrative ability in reading the characters of his friends. Great determination in carrying through any project that interested him was another of his attributes, and lie would never allow himself to be led by specious argu­ments into a course of action he did not approve. These qualities made him a valuable member of the Council of the Zoological Society, on which he actively served many years after his first election to it in the last decade of the nineteenth century.
     Within a few years of his marriage he began to worry about his health. Troubled by heart palpitations and other symptoms of illness he did not understand, and knowing the physical debility of his family, he gave up all games involving exercise, gradually drifted into the condition of a confirmed invalid, and was so obsessed by the conviction that he had only a few years to live that, when he went to the Argentine for his health, he feared he might never come back to resume his duties at the Museum. This depressing state of mind was fortunately in a measure relieved by a course of treatment which he followed after a consultation with the late Dr. Haig. Of the greatest value to Thomas was the assurance he received that the adoption of a mainly vege­tarian diet would at once make a change for the better, and perseverance with it perhaps work a permanent cure. Instilled with this new hope, Thomas entered upon the new dietary regime with the tenacity of purpose characteristic of every scheme he embarked upon; and was so impressed by the verification of Haig’s prediction that he tried to induce all his friends to follow his example in the matter of food.
     It is only fair to point out that his ardent advocacy of this course was based upon the benefit he derived from it, because most of his friends and acquaintances regarded him unjustly, if kindly, as a hypochondriacal crank. Thomas became, it is true, a confirmed valetudinarian, absorbed in the study of his health as affected by diet, reducing himself at times to the verge of starvation, undergoing daily a course of massage and becoming more and more averse to physical exertion of any kind. Probably the distraction and anxieties of children and an interest in literature or art would have prevented the lapse into this deplorable state of mind. Deprived of these, he was hard put to it to find home occupations and, instead of reading, would sit doing some manual work, like knitting, or later in life listening to the wireless. His wife, upon whose company and attentions he was very dependent, unfortunately pre­deceased him. For a time after her death he carried on his work as before; but as the months went by, he missed her more and more, and finally when he ceased to be interested any longer in his zoological work and showed unmis­takable signs of mental derangement, few of his friends were surprised that he died by his own hand in June, 1929.
     He left the bulk of his own and his wife’s fortune as a collecting fund for the Museum ; and shortly before his death he paid for the installation at the Museum of a much-needed lift for the use of the official staff. This was completed and formally opened in May, 1930.
*I learn, however, from Mr. M. A. C. Hinton, who was more intimately associated with Thomas during the last fifteen year’s of his life than I was, that, when he was about 50, he began to take an interest in trees and in the heavens. A humorous remark he once made about the stars is worth repeating as characteristic of his type of mind :—“What a pity it is we cannot collect them !”

In 1990 a memoir, bibliography and index to the names of animals proposed by Oldfield Thomas was written by John Edwards Hill (1928-1997) and published by the Museum. 

Hill recorded that Thomas wrote letters to newspapers and magazines:

His pragmatic outlook characterises his suggestions for an easily made ear-plug for soldiers in the firing line, that pedestrians should use the road and footpath in a disciplined fashion to avoid collisions with traffic or with bearers of advertising sandwich-boards, or his proposal after the First World War that the German Fleet should be sunk in such a way and position that the wrecks would provide a breeding ground for fish. Interested in the merits of simplified spelling, he also enthused over starvation as a cure for influenza, and advocated the learning of Braille by the sighted as an aid to sleep: in this way it was possible to read in bed in a darkened room, or with arms, hands and book or magazine in the warmth under the bed linen. He had pronounced views on 'legalised suicide' as a form of euthanasia that eventually he was to carry to their logical conclusion.

It is hard to believe today that suicides—illegal and judged immoral at the time—were not talked about in polite society and it is certain that no explanation was offered to junior staff of Thomas’s death. It is not surprising that rumours spread that Thomas’s office—kept locked for some time—was the place he had killed himself. Hellen Pethers in a 2015 blog post from the museum finally sorted out what had happened. Thomas shot himself at home (46 Edwardes Square, Kensington), not in his office. He was cremated and his ashes buried with his wife at Uxbridge Cemetery where their eroded gravestone can be found.

Oldfield Thomas's photograph and signature
for the Royal Society

Hill JE. 1990. A memoir and bibliography of Michael Rogers Oldfield Thomas, F.R.S. Bulletin, British Museum (Natural History), Historical Series 18, 25-113.

Pocock, RI.1930. Michael Rogers Oldfield Thomas—1858-1929. Proceedings of the Royal Society B 106, i-v.

Monday 2 April 2018

In a forest near Baxi in Sichuan: What Pika was this?

During a walk through a natural pine forest at an altitude of approximately 3,200 metres last November near Baxi in northern Sichuan we saw Chinese Grouse, Crested Tit-warbler, Przewalski’s Nuthatch, Grey Crested Tit, Giant Laughingthrush, Snowy-cheeked Laughingthrush and a flock of Sichuan Jays. A mature Sika stag appeared on the other side of a valley and Paul spotted three Yellow-throated Martens which left at high speed. But we also saw, and photographed, a pika. The question was: which species of pika?

A considerable amount of time has been spent and a considerable volume of email traffic has been generated in trying to determine the answer to that question. There have been false leads and false trails. The reason for that is severalfold: (i) we were in a little-studied area; (ii) the taxonomy and distribution of pikas is complicated and confused; (iii) published accounts of species and sightings are often inaccurate both in the scientific and popular literature; (iv) accounts of known types of habitat may be inaccurate or incomplete; (v) the similar appearance of a number of species.

Of one thing we were certain. The ear showed a narrow white margin.

Thomas's Pika
Photograph by Tim Melling

The most modern account of pikas is that in Handbook of Mammals of the World. Volume 6 published in 2016. This differs from the account and distribution maps shown in the standard field guide, published in 2008, since more has been discovered and some earlier errors sorted out. By locating Baxi Forest on the small-scale distribution maps in the Handbook (a major bend in the Yellow River provides a major feature to plot the position of Baxi), the following three species of pika, all with the white ear margin enter the field of possible candidates: Gansu Pika (Ochotona cansus), Tsing-ling (or Qinling) Pika (O. syrinx), Thomas’s Pika (O. thomasi).

From the Handbook of Mammals of the World, Volume 6, I have outlined the distributions of three species
of pika that are said to occur in the Baxi area plus the Moupin Pika now thought to occur to the south. Note
the discontinuous distribution. The published ranges of Thomas's, Gansu and Tsing-ling all incude Baxi.

'Our' pika has previously been identified by mammal watchers and photographers as the first and last of these as well as the Moupin Pika (O.thibetana). However, the latest published information is that the last species does not occur so far north.

The taxonomic scheme I am using here is that being used by IUCN and in the Handbook. It is based on the taxonomic revision published by Andrey Lissovsky of Moscow State University in 2014. Lissovsky had to pick apart a real can of worms found in past publications including lost type specimens, assignation of specimens or subspecies to a species without examination of the type specimens, the poor provenance of specimens used in DNA analysis as well as different interpretations made from examination of a limited number of specimens by earlier authors. He also did his own morphometric analysis on the skulls of 1090 pikas as well as an analysis of the cytochome b mitochondrial gene.

The detail of Lissovsky’s revision need not concern us. However, the three candidate species did emerge as full species, with the caveat that he recommended more work should be done on all but O. thomasi. A possible key finding, of relevance to our problem, is that Lissovsky showed that statistical analysis of all the skull measurements clearly distinguished Thomas’s Pika from those in the group which includes the Gansu, Tsing-ling as well as the Moupin Pika. The descriptions of Thomas’s Pika note the shape of the skull. Thus the Handbook states: ‘In general, Thomas’s Pika can be distinguished from all pika species by its elongated, narrow skull’.

We did not of course have another handy pika to compare ours with. However it is on the basis of the long, narrow skull that Vladimir Dinets an expert on the identification of Asian mammals with field experience in Sichuan also considers the species we saw as Thomas’s Pika. In an email to Sid Francis he did so also on the coloration of the throat. O. thomasi has a grey throat whereas O. syrinx has a rufous throat and chest. In addition, O. syrinx has a flat top to its skull.

Therefore, in terms of anatomy, pelage and distribution, it would seem our pika was indeed Thomas’s.

However, there is a problem in reconciling the identification as Thomas’s Pika with the published habitat of our animal. As I remarked earlier, our was in a natural pine forest. But the habitat stated in the Handbook and the field Guide is as follows: ‘Alpine shrub mountain zone at elevations of 2800-4100 m. Thomas’s Pika occurs in shrubby areas and does not penetrate subalpine meadows; it is a shrub dweller’ and ‘Inhabits hilly shrub forest (rhododendron, Salix, Caragana jubata, Potentilla fruticosa)…’. By contrast the habitat of the Gansu Pika is ‘subalpine meadows, inhabiting spare shrubs and thickets at forest edges’. But then the habitat of the Tsling-ling Pika is given as ‘forests at elevations of 1800-3100 m’. Initially I discounted Thomas’s because of the pine forest habitat of our pika. However, we were not far above the rhododendron forest so it is possible that the scrub forest habitat could extend to the scrubby understory of contiguous pine forest, possibly at different times of year. Indeed, Sid had seen the same species previously in nearby willow and rhododendron scrub forest. Clearly, more observations are necessary in the field but it does seem that a habitat extension is in order since O. thomasi may be found in pine forest too. Vladimir Dinets also noted that at another site he had found O. thomasi at higher elevations than O. syrinx; again this accords with our sighting at about 3,200 metres just outside the altitudinal range given for O. syrinx.

Vladimir Dinets shows photographs of pikas he has seen here.

Given the alleged presence of three small pika species with white ear margins in the Baxi area, we should expect each to occupy a different ecological niche and that the morphology of the skull should reflect that difference in habitat and the manner in which food is gathered in that habitat. O. thomasi has a long, narrow skull. This shape, one could predict with confidence, is related to its scrub forest habitat where grass, herbs and leaves would be nibbled out from between branches and stems. In short, Thomas’s Pika could be as adapted to life in the understory of a pine forest as to the scrub of a rhododendron forest.

I do not know whether the present taxonomy of the pikas will hold. All the molecular phylogeny is from mitochondrial DNA rather than or as well as nuclear DNA. We should, I suppose, expect to see a complicated picture for the number of species or lineages. The geological upheavals of the region are ones likely to have caused geographical isolation of populations, speciation or partial speciation and, possibly, later hybridization between temporarily isolated lineages.

Thomas’s Pika is endemic to China. It has the reputation of being rare but given its habitat that may be better expressed as rarely seen. It was first described in 1948 by the Russian zoologist A. I. Argyropulo in honour of Oldfield Thomas of the Natural History Museum in London. Thomas himself had named the Tsing-ling Pika, Ochotona syrinx*, in 1911; that specimen was collected on the Duke of Bedford's expedition. I will return to Oldfield Thomas in future posts on this blog.

So there we are. It does seem that our little pika, officially classified as ‘cute’ (but not quite so cute as the Plateau Pika) by its admirers in the Baxi Forest last November, was indeed Thomas’s Pika (Ochotona thomasi). Trying to identify and learn more about it has occupied a fair amount of time but uncovered how much more needs to be known about the natural history  and evolutionary history of these small mammals.

I am most grateful for the various exchanges and ideas being bounced around between Tim Melling (who also took the still photographs), Paul Markley and of course Sid Francis who also took us to the site. We can also give Sid the challenge of finding the other species of pika with white ear margins said to be in the Baxi area during his future trips. This is an area where citizen science can contribute to knowledge of little-studied species.

Finally, this is the video I took of the pika:

*With Lissovsky’s taxonomic revision and the application of the rule of priority to scientific names, the Tsing-ling Pika emerged as Ochotona syrinx. It was previously known as Ochotona huangensis but that name now appears to apply, as a junior synonym, to another species entirely:
As a consequence, the name for the taxon of pikas considered as a subspecies of Ochotona thibetana (Hoffmann 1993), or as the species O. huangensis (Yu et al. 2000, Hoffmann and Smith 2005) from the Qinling Mts, should be changed. The senior synonym for the pikas of the thibetana group from the territory, inhabited by taxon under discussion, is O. syrinx Thomas, 1911. According to the present analysis, the type specimen of O. syrinx from Tai Bai Shan Mt. within Qinling Range falls within the morphological variation of this thibetana-like taxon.… Thus, the valid name for this taxon should be O. syrinx.
Lissovsky AA. 2014. Taxonomic revision of pikas Ochotona (Lagomorpha, Mammalia) at the species level. Mammalia 78, 199-216.

Smith AT, Xie Y. (Editors). 2008. A Guide to the Mammals of China. Princeton University Press.

Wilson DE, Lacher TE, Mittermeier RA. 2016. Handbook of Mammals of the World. Volume 6. Lagomorphs and Rodents I. Barcelona: Lynx Edicions.