Sunday 24 October 2021

The Omnivorous Lizards of Aruba, or: Breakfast at home is never quite the same

Arriving at a hotel at around 3 am with a bad cold is not conducive to the best of tempers. And having got up to catch breakfast the next morning and then having to walk back to the room to collect the wodge of vouchers for different items of breakfast (a bizarre practice never seen before or since) that had been thrust into my hand at check-in, that temper was not improving. Eventually we emerged holding trays as if we were at an American student cafeteria and found a table on the deck close to the beach. We were on the Dutch island of Aruba, off the coast of Venezuela, in October 2002 on our way back to UK from Peru. The KLM flight stopped there to refuel on its way to Amsterdam and a few days of doing nothing before flying on seemed a good plan.

The almost entirely American clientele of the hotel had finished their breakfasts by the time we sat down. Inevitably, each table had been left with piles of uneaten food. That was being made short work of by hungry birds, Carib Grackles (Quiscalus lugubris), Eared Doves (Zenaida auriculata) and Bananaquits (Coereba flaveola). As the tables were cleared, only the sachets of sugar and artificial sweetener were left on the tables. The Bananaquits lifted each sachet in turn until they found one containing sugar. That sachet was then hauled onto a flat surface and pecked until the granulated sugar could be eaten. The day was improving and the champagne (obtained by a special voucher) in the full breakfast booked by our travel agent may well have helped.

Looking downwards we realised that food dropped on the floor by messy human eaters or by the birds was not going to waste. There was a whole squad of Common Iguanas (I. iguana) of all sizes as well as whiptails or racerunners (Cnemidophorus) I had to look up later; they were C. arubensis, as the name implies endemic to the island. Now the day was taking a very different turn and a morning catching up on sleep completed the job.

Male Aruba Whiptail eating melon

The start of each day followed the same pattern with the iguanas in particular hanging around occupied tables in the hope of handouts. The iguanas would eat pretty well anything offered; the whiptails preferred fruit but were not averse to small pieces of bread or bacon. One morning I took some video. These were the days of ‘standard definition video’ on miniDV tape with no stabilisation of the image.

Common Iguanas are well known omnivores. The Field Guide to the Amphibians and Reptiles of Aruba, Curaçao and Bonaire published in 2005 states that the whiptails on the islands are mainly herbivorous and noted ‘These island whiptails also eat insects and other arthropods and will eat carrion; they gorge on practically all other food which they can find around houses’.

With all I have written in the past few weeks about the colons of omnivorous lizards, the obvious question is does C. arubensis has ‘caecal valves’ as is well documented in I. iguana? 

Buurt G van. 2005. The Field Guide to the Amphibians and Reptiles of Aruba, Curaçao and Bonaire. Frankfurt: Chimaira.

Thursday 21 October 2021

Omnivory in the Italian Wall Lizard and Changes in Gut Structure and Function: The Results of a Translocation Experiment

My recent article on fruit-eating Italian Wall Lizards (Podarcis siculus) turned up an intriguing story about this lizard. In 1971 five pairs of this species were introduced onto the Croatian islet of Pod Mrčaru from a nearby islet, Pod Kopište, in the Adriatic Sea. Since that time the population has been studied intensively because, it was found, those on Pod Mrčaru ate far more plant material than those on Pod Kopište. Thirty-six years after the population was introduced plant material comprised 34% in spring and 60% in summer of the stomach contents, compared with 7% and 4% in the lizards of the original population.

Associated with that change in diet were a number of morphological changes. The heads were bigger and the bite force greater in the omnivorous lizards on Pod Mrčaru, changes attributed to the need to tear up plant material before swallowing. Particularly interesting to me was the finding of ‘caecal valves’ in the large intestine. In herbivorous lizards these structures are present and appear to impede the passage of digesta and thereby provide a fermentation chamber for the digestion of cellulose by micro-organisms. Nematodes were present in the gut of the omnivorous population suggesting they were ingesting the digested plant material.

The authors of this first study, published in 2008, were, in my opinion, unwise in appearing to favour the view that these changes within a species were caused by natural selection over a period of a few generations and were therefore an evolutionary event with a change in gene frequency akin to that seen in, say, industrial melanism in moths. The alternative but not mutually exclusive explanation is that lizards of this species have sufficient individual plasticity to respond in the way that they have to the ingestion of plant material. A paper published in 2010 by a largely different group not only extended the original observations but also obtained evidence that plasticity is the more likely explanation for the changes observed in the digestive system

A key experiment was of course to reverse the availability of plants in the diet. Genetically determined adaptations would not be reversed by a return to carnivory within a lifetime while adaptation brought about by a plastic response to the diet would be expected to lead to reversion. This experiment was done by the second group of researchers. Lizards from the introduced, omnivorous, were fed exclusively on arthropods for 15 weeks. One characteristic of the omnivorous lizards was a heavier and longer large intestine. In the arthropod-fed group, the size of the large intestine was smaller. Furthermore, there was no sign of a caecal valve in any of the 20 animals that had been fed exclusively on arthropods.

The second group of authors also cast doubt on whether the larger heads and bite strength of the lizards on Pod Mrčaru are directly related to their plant-rich diet. The greater population density of the lizards on Pod Mrčaru compared with Pod Kopište may have resulted in selection for greater ability for physical combat. That selection pressure rather than that from the tearing of plant material may have lead to the larger body sizes, the more robust heads and the greater bite force observed in the Pod Mrčaru lizards

While a mixture of selection and plasticity may explain the overall changes in the lizards on Pod Mrčaru, it does seem likely that with respect to the digestive system the changes are the result of plasticity not selection. This conclusion does not mean to say that in other species of lizard which are largely herbivorous the presence of a large colon containing a number of caecal valves is not genetically determined.

Worth noting here is the fact that the Wikipedia article on this lizard is misleading—as is so often the case on herpetological matters—and does not take into account later findings on the lizards of Pod Mrčaru.

If there are—as does seem to be the case—species of lizards that can change to a more herbivorous diet, develop the morphological and biochemical features necessary to digest plant material and absorb the nutrients produced in a reversible manner then three questions arise. The first is why the lizards introduced to Pod Mrčaru began to eat a larger proportion of plant material. Was it because the competition for food resources in the form of small invertebrates became intense as the population grew? The second question is the reversible mechanism by which the colon forms caecal valves.

Looking at photographs of the caecal valves in P. siculus and at those from other, mainly herbivorous species, it appears that the valve comprises a transverse infolding of the wall of the colon. It is relatively easy to envisage an area of localised cell division and development of a ridge which narrows the lumen. In reverse, local loss of cells would flatten the infolding. For those physiologists and cell biologists working on local signalling mechanisms in the intestine P. siculus is not without interest. Incidentally, research over the past forty years has shown the alimentary canal of reptiles to be highly labile in response to changes in food intake; far more so than would have seemed imaginable.

Later work, published in 2020, in again comparing the lizards on the two islets have not been so clear cut but do support plasticity as the explanation. I have some qualms about the methodology and the lack on information on the actual absorption of nutrients from the gut as opposed to concentrations found therein. However there was clear evidence that in 2013 no lizards were found on Pod Mrčaru with caecal (also known as hindgut) valves. The reason for that shift over time can be debated but these findings strongly support the view that the induction of enzyme and nutrient transport systems as well as the growth of caecal valves are part of the result of plasticity within an individual rather than the outcome of a process of natural selection.

The third question is whether lizards of this species turned to an omnivorous or largely herbivorous diet elsewhere in their large range. The current field guide to European reptiles describes Podarcis siculus as ‘an opportunistic feeder, taking a variety of invertebrates and plant matter’. The sort of response that given current knowledge would be expected could very much depend on the type of plant food being eaten. There is a world of difference in the sort of chemical digestion and nutrient absorption needed to process sugar-rich fruit, as in the grape-eating lizards from mainland Italy that made their way accidentally to UK, and other plant materials for which the digestion of cellulose by microorganisms is necessary.

The opportunistic nature of Italian Wall Lizards can be seen in the following photographs sent to me by a regular reader of these articles, David Lambert. They were taken at Punta del Capo, a small flat-topped rocky promontory near Sorrento. The lizards proved very willing to share a picnic  and his photographs show them eating banana, tomato and bread.

David Lambert's photograph of an Italian Wall Lizard eating bread

...and banana

...and tomato

The location of the islets in the Adriatic
From Wehrle et al 2020

In chronological order:

Herrel A, Huyghe K, Vanhooydonck B, Backeljau T, Breugelmans K, Grbac I, Van Damme R, Irschick DJ. 2008. Rapid large-scale evolutionary divergence in morphology and performance associated with exploitation of a different dietary resource. Proceedings of the National Academy of Sciences of the USA 105, 4792-4795 doi10.1073/pnas.0711998105 

Vervust B, Pafilis P, Valakos ED, Van Damme R. 2010. Anatomical and physiological changes associated with a recent dietary shift in the lizard Podarcis sicula. Physiological and Biochemical Zoology: Ecological and Evolutionary Approaches 83, 632-642

Wehrle BA, Herrel A,  Nguyen-Phuc B-Q, Maldonado  S,  Dang RK, Agnihotri R, Tadić Z, German DP. 2020. Rapid dietary shift in Podarcis siculus resulted in localized changes in gut function. Physiological and Biochemical Zoology 93, 396–415. DOI: 10.1086/709848 

Sunday 17 October 2021

‘Mouse’ Chaworth-Musters: gentleman zoologist and covert agent with views on how to distinguish a species

In a book published in 1979 about events zoological of the late 1940s I came across a pithy quotation about how to define a species that got to the crux of that never-ending and impossible-to-end debate.

The discussion between Leonard ‘Leo’ Harrison Matthews (1901-1986), Ronald Lockley (1903-2000) naturalist and author, and Alastair Worden (1916-1987) veterinary surgeon and Professor of Animal Health in University College, Aberystwyth, took place in 1946 on the island of Skomer where they were studying seals and collecting their livers for Alan William Davies (b. 1913) who was working on their Vitamin A content. That morning they had caught a vole in the Longworth trap Matthews had put out the night before. After commenting on the tameness of the voles—this wild vole one sat on Worden’s hand and ate a crumb before grooming its coat—the conversation turned to the taxonomic status of Skomer’s vole. Matthews ended his comment:

But whatever is right it can only be a subspecies. We ought to try Mouse Chaworth-Musters’ test—put them together and let them sniff each other’s bottoms: they’ll know if they are the same species all right.

This concept of what a species is—recognition by another individual as of the same species—seems far more sensible than those in vogue which seem to me to be akin to the drunk searching for his key under the streetlamp rather than further up the road where he lost it on the grounds that only under the lamp could he see.

But who was Chaworth-Musters? I thought he must be a scion of the Chaworth-Musters family of Nottinghamshire whose doings filled many column inches of the several newspapers published daily in Nottingham in the mid-20th century. He was—and in the position of that dying breed of gentleman scientists who did not need to work for a living.

James Lawrence Chaworth-Musters was the youngest son (of eight children) of John Patricius Chaworth-Musters of Annesley Hall in Nottinghamshire. He was born at Annesley on 1 July 1901. After Rugby School, where his main interest out of hours was natural history in the field, he was admitted to Caius College, Cambridge, as a preclinical medical student. However he gave up that idea and switched to geography which became a lifelong interest.

While still a young man Chaworth-Musters inherited an estate at Surnadal on the west coast of Norway. He spent summers there for many years studying mammals and birds both locally and more widely. For example, in the 1930s he ringed birds on the island of Utsira, arguing that birds migrating from Siberia to Britain would refuel on the Norwegian island. As a result he added considerably to the Norwegian bird list.

He was not the only member of the Chaworth-Musters family to have an interest in geography in natural history. One notable example is his grandfather’s brother. Charles Musters was on board HMS Beagle, when she left Plymouth on 27 December 1831, serving as a Volunteer, 1st Class (i.e. a boy intending to be an officer). However, he did not return; he died aged 14 on 19 May 1832 at Bahia, Brazil, possibly of malaria. Charles Darwin greatly regretted the loss of ‘my poor little friend Charles Musters who had been entrusted by his father to my care, and was a favourite with every one’.

From the late 1920s James Chaworth-Musters worked at the Natural History Museum in London on the systematics of mammals; not surprising then his nickname, ‘Mouse’. However, his life as a gentleman scientist was interrupted by the outbreak of war in 1939. At the time he was in India but travelled to Bergen as British vice-consul. He was working when the Germans arrived in April 1940. As they entered the front door he left by the back and headed east across the mountains on skis. However the German advance cut off his escape route and so he turned back to the coast. There he persuaded a fisherman, Edvin Nore from Bryggja by Måløy to take him and two British soldiers who had been hiding in a nearby village to Shetland. Norwegian sources suggest he was already working as a British agent as well as vice-consul in Bergen, that he reached the coast at Nordfjord and left Måløy on 10 May. Indeed, his rôle in the Special Operations Executive was far greater than suggested in his obituaries. My guess is that he was already working for one of the secret agencies that were constituted into SOE. Is it stretching the imagination foo far to suggest that his expeditions in the 1930s might not have been concerned solely with natural history and geography? Other British zoologists are now known to have been reporting their observations in foreign parts to the intelligence services.

Chaworth-Musters was said by Norwegian sources to have been the major player on the British side in the first sabotage measures in occupied Norway. He started irregular warfare in Norway as soon as could after he reached Lerwick following his escape across the North Sea.  A few weeks after his return, twelve men set off for Western Norway to set up an arms dump and sabotage key infrastructure needed by the Germans. He also acted as a liaison officer between SOE and the Norwegian Government in exile in London. Communications between the Shetlands and Norway were maintained by fishing vessels, or craft disguised as such, crossing during the winters between Lerwick and Norway—the ‘Shetland Bus’ carried agents, commandos, matériel and refugees.

Formally, he was commissioned as Lieutenant (Special Branch) in the Royal Navy Volunteer Reserve on 4 March 1941.

Chaworth-Musters in the uniform of a Lt RNVR

Chaworth-Musters later co-founded Kompani Linge, or Norwegian Independent Company 1, that celebrated group of Norwegian commandos who amongst other exploits sabotaged the heavy-water plants that could have been used by Germany in the development of nuclear weapons. Chaworth-Musters was also responsible for spotting Norwegian refugees who would be suitable for sabotage missions in Norway. All of the things he did must have been helped by the fact that he spoke the Surnadal dialect ‘like a native’.

Norway recognised his contribution to the British-Norwegian cause. He was awarded the King Haakon VII Liberty Medal—Norway’s War Medal. I suspect that few of his colleagues and friends at the Natural History Museum knew any detail of what he had got up to in the war. Not the done thing.

In 1946 he went back to the Natural History Museum where for a short time he held a paid post as temporary Assistant Keeper to help with the task of post-war reconstruction.

Sir Terence Morrison-Scott (1908 –1991), who before becoming Director of first the Science Museum and then the Natural History Museum, had spent his earlier career in the latter working on mammals alongside Chaworth-Musters, wrote in Journal of Mammalogy:

As a systematist his knowledge was deep and his critical judgement extremely sound. He belonged to the 'lumpers,' as indeed do all good modern workers, and all his work was directed in an uncompromising manner to defining the species. The genera and subspecies interested him not a bit—it was the fundamental thing, the real thing, the species. 

He published very little, unfortunately. This was due in part to a restlessness which made him intolerant of paper work; he had the details of his subject in his head and it was merely a bore to write them down when he could be better occupied in new research. But perhaps it was due chiefly to a passion for truth and a feeling that once a thing is published it cannot be retrieved. The thing had to be exact and perfect before being committed to print. There is much to be said for this outlook and if the badly served fare of some workers had been more carefully prepared the systematist of today would not be suffering from such indigestion. But he took far too modest a view of himself and it is a great pity that he did not publish more. His 'magnum opus' was a checklist of the Palaearctic mammals, for which he has left a great deal of manuscript. Apart from the systematic interest of the work, its publication will prove of great value on account of the remarkably erudite research on type localities which he put into it. There will be some difficulty with his handwriting which was paradoxical in being at the same time very neat yet almost illegible.

 Morrison-Scott noted his various expeditions and:

He was a very successful collector of birds and mammals and his study skins, of mammals at all events, are among the best in the Museum.

Hampton Wildman Parker (1897-1968) another colleague at the Natural History Museum expanded in an obituary for Nature on Chaworth-Musters’s expeditions: a Norwegian expedition to Jan Mayen in 1920 (Norwegian sources say 1921); Cyrenaica, now part of Libya, in 1926; Greece in 1931; USSR in 1936; Morocco in 1937; Afghanistan in 1939. 

Morrison-Scott continued:

As a man he was in many ways a paradox. In personal appearance he was Bohemian and disregarded many conventions. Yet with it all he was at heart a country squire and a strong traditionalist. In spite of his usual dress there was, in its leather case in his room at the Museum, a top hat, ready for use on formal occasions. And the narrow, plainly knitted strips of material which he habitually wore as ties were not, as might have been imagined, badges of his unconventionality. They were what schoolboys of his day wore; he was used to them and he liked them and he still wore them. And they were in a way the key to his character, for he was very much a schoolboy in his heart. He would fly all sorts of conversational kites which would lead casual, or pompous, acquaintances to think him a bit eccentric, or even a bit of a fool. How mistaken they were, and what very good value his company was to the discerning.

Morrison-Scott had begun his obituary with:

James Lawrence Chaworth-Musters died unexpectedly in London on April 12, 1948, at the age of 46. He was apparently in good health, and in the best of spirits, and filled with enthusiasm for what he referred to as his 'magnum opus.' 

The Chaworth-Musters magnum opus never made it into print. However, his work was incorporated into Morrison-Scott and J.R. Ellerman’s Checklist of Palaearctic and Indian Mammals*. The book was dedicated to the memory of their late friend and colleague and in the Introduction the authors wrote:

Our late friend and colleague, James Lawrence Chaworth-Musters, had spent much time latterly on the synonymies of the species of Palaearctic mammals, and in particular had devoted much patient research to the type localities and dates of publication of species described in the eighteenth and early nineteenth centuries. At the time of his death, in April 1948, he had nearly completed this work for the Insectivora and done much of the Chiroptera and Rodentia. His executors kindly placed his manuscript cards and foolscap sheets at our disposal, and we have made free use of the data referred to above. His death was a most untimely and unfortunate loss to the Museum and to his friends and colleagues.

Chaworth-Musters is commemorated in Norway. After his death Surnadal municipality bought his property there and turned it into parkland and a museum. A memorial plaque was unveiled in 2004. Wikipedia Norway has a biography (in Norwegian).

At Nottingham University, his drawings of whales and plants from Norway are held in the family archives.

Finally, he does have an animal species named after him. It is not a mouse, as has been reported. It is not even a mammal. It is the Paghman Mountain Salamander, Afghanodon mustersi, discovered by Chaworth-Musters in Afghanistan and named by Malcolm Smith† (1875-1958) in 1940. 

For Chaworth-Musters’s incisive view on what constitutes a species, though, we rely on the Matthews anecdote from Skomer in 1946.

The Chaworth-Musters Family's house at Surnadal, Norway

*Sir John Ellerman (1909-1973) was another gentleman zoologist working at the Natural History Museum alongside Chworth-Musters, mainly on rodents. He also ran the eponymous shipping line and was sometimes said to be the richest man in England.

†By this time Malcolm Smith was also a gentleman zoologist working at the Natural History Museum. He had been the British Embassy’s doctor and physician to the royal family in Siam.

Beolens B, Watkins M, Grayson M. 2013. The Eponym Dictionary of Amphibians. 2013. Exeter: Pelagic Publishing

Ellerman JR, Morrison-Scott TCS. 1966. Checklist of Palaearctic and Indian Mammals 1758 to 1946. 2nd Edition. London: British Museum (Natural History).

Morrison-Scott TCS. 1949. James Lawrence Chaworth-Musters. Journal of Mammalogy 30, 95-96.

Parker HW. 1948. Mr. J.L. Chaworth-Musters. Nature 161, 755.

Smith MA. 1940. Contributions to the herpetology of Afghanistan. Annals and Magazine of Natural History, Series 11. 5, 382-384.

Monday 11 October 2021

A Recently Introduced and Unwelcome New Species of Frog in Hong Kong

Only by chance I found that Hong Kong has had a relatively recent addition to its list of amphibian species—and it is one that is there because it has been introduced accidentally.

The first author of a paper published in 2016 found the then mystery frog in a container yard in what was the New Territories of Hong Kong in 2000. Up to 2015 the same frog had been found at 18 locations throughout much of Hong Kong and, furthermore, to be breeding.

Using DNA barcoding the frog was identified as Eleutherodactylus planirostris originally native to the Caribbean (Bahamas, Cayman Islands and Cuba). However, it has been accidentally introduced to a number of other countries in the tropics and subtropics, including mainland USA, several in Central and South America, Hawaii, Guam, Singapore and the Philippines. The first clue to how it has spread so easily is in its common name of Greenhouse Frog. The second is that the frog develops entirely within the egg case, from egg to tadpole and to metamorphosed froglet. Eggs were found in Hong Kong on wet leaf litter. All the indications are that the eggs are spread as part of the trade in live, cultivated plants.

Greenhouse Frog, Eleutherodactylus planirostris
Photograpg by Pierre Fidenci
Attribution Share Alike 2.5 


The authors wrote (references omitted):

Large volume of live plants was imported to Hong Kong from continental United States of America in early 2000s when E. planirostris was first detected in Hong Kong. This was supported by one frog being found in a potted Tillandsia cyanea plant bought from the flower market in Mong Kok in urban Kowloon in 2011 and another frog found in an apartment on Ap Lei Chau in 2015 that was likely to arrive together with an indoor plant. In addition, we made observations of high densities of frogs (> 30 in 200 m2) near newly renovated slopes where nursery plants were planted on. Due to the extensive trade of live plants in the region, it seems it is a matter of time that E. planirostris will spread to other places that import plants from Hong Kong. In 2015, Hong Kong exported or re-exported over 100,000 kg of plants or parts of plants to tropical or subtropical countries/cities, including Australia, China, Macau, Malaysia, Singapore, Thailand, Taiwan and Vietnam, where the climate may be favorable to the colonization of E. planirostris.

Greenhouse Frogs, although producing a relatively small number of eggs at each spawning, are prolific. There is concern in Hong Kong that this introduced species could compete with another small frog, the endemic Romer’s Frog, Liuixalus romeri, for food. This concern spreads to the possible effects of carrying the frog to other countries and regions which buy plants from Hong Kong. The authors suggested the screening of all plants for adults and eggs leaving Hong Kong. The problem with closing that stable door is that the horse may have already bolted.

I have seen no further information on the status of this introduced species in Hong Kong since the paper was published in 2016. 

Lee WH, Lau MW-N, Lau, A, Rao DQ, Sung Y-H. 2016. Introduction of Eleutherodactylus planirostris (Amphibia, Anura, Eleutherodactylidae) to Hong Kong. Acta Herpetologica 11,85-89. DOI: 10.13128/Acta_Herpetol-16491 

Thursday 7 October 2021

Stowaways: Lizards in Shipments of Grapes Arriving in UK

Stories of stowaway spiders and snakes in imported fruit often make it into the newspapers but a report in a recent Herpetological Bulletin was remarkable. Over a five-week period in 2020, eight shipment of grapes from the Abruzzo region of Italy were found to contain 29 stowaway lizards, identified as Italian Wall Lizards, Podarcis siculus (or Lacerta sicula* in old money). The grapes had all arrived in UK by sea and the lizards were found at four distribution centres in England.

The stowaway lizards when housed in vivaria fed readily on grapes but ignored mango, persimmon and banana. It would seem that the lizards were feeding in bunches of grapes when they were picked and promptly shipped to British consumers. The authors wonder if it being autumn the lizards feed on grapes as small invertebrate numbers decrease. The sugar content (around 16% of wet weight) alone could well fuel these lizards and be converted into fat stores for the winter.

Some populations of the Italian Wall Lizard, incidentally, are known to eat fruit when invertebrate prey is abundant but that fascinating story will have to wait. In the meantime I should remind you it is October one year later. If planning to take a traditional bunch of grapes on a visit to a sick friend or elderly relative it may be advisable to check for stowaways even though some of us would prefer a lizard to a grape (unless fermented and in liquid form).

This Italian Wall Lizard was in the wild--in Krka National Park, Croatia
Photographed in 2010

Clemens DJ, Allain SJR. 2001. 2021. An unusually high number of Italian wall lizards Podarcis siculus campestris entering Great Britain as stowaways. Herpetological Bulletin 156, 42. 

*The ludicrous changing of the ending of the specific name depends on whether the name of the genus, Podarcis, is considered to be be masculine or feminine in Latin; it seems the masculine supporters hold sway. Just imagine the confusion in indexing and searching. That is the sort of thing that makes other scientists look askance at taxonomists. 


Tuesday 5 October 2021

Frogs: Singin' in the Rain

Over a number of articles I have looked at whether or not—and if so how—rain triggers breeding in birds and amphibians.

If rain does trigger breeding how does it work? Is it indirect, as Maxwell Savage proposed, by stimulating the growth of algae, the smell of which attracts frogs to breeding ponds as well as acting as the trigger for breeding when they do arrive? Similarly, Ron Murton and Nigel Westwood wrote in 1977: ‘…what still needs to be determined is whether the appearance of rain or clouds causes any of the Australian desert birds to indulge in display that in turn stimulates the hypophysial-gonadal axis into activity. At present, the indications are that those species which breed with the onset of rain respond to food supplies that are made available within a day or two of rain falling’. Or is it direct, rainfall itself or an associated change in pressure, humidity or temperature, directly perceived? And how does simulated rain trigger breeding so quickly in tropical frogs kept in captivity?

The croaking of frogs is, of course, associated with breeding, as males arrive at their breeding ponds, for example. However, I was reminded by a recent article by Gordon L. Miller in Archives of Natural History that in frogs and toads there is a phenomenon, recorded since the time of the Ancient Greeks, for which there is still no satisfactory explanation: ‘Rain Calls’. Rain calls are those emitted outside the breeding season but in response to impending rain. There are two questions that spring to mind immediately. What environmental change or changes is responsible? Since it can occur before the rain actually falls as well as during and shortly afterwards such factors as a rise in humidity or a decrease in atmospheric pressure have been suggested. The second question, the ‘why’ one, remains unanswered. What was in it for the frog I saw in the garden croaking loudly a few minutes after a shower of rain in late summer? Is it, has also suggested many times, a sign that the frogs are returning to breeding condition but that further development is arrested by the low temperatures of late autumn and winter. But croaking outside the breeding season would seem to bring only disadvantage—why croak when doing so could draw the attention of predators? I will not continue because I did note that no satisfactory explanation exists.

Cicero, as noted by Miller, drew attention to the phenomenon over 2,000 years ago:

There is within frogs a kind of natural force for giving signs, sufficiently clear in itself but too dark for human comprehension.

What the phenomenon of rain calls does show is that some environmental factor acts as a short-term and powerful trigger for frogs to start croaking. Surely it is not beyond the wit of science to devise simple experiments to find what that trigger(s) is(are). Tropical frogs in artificial climate- and pressure-controlled ‘rain chambers’ would seem a good way to start (see here).

The frogs (Rana temporaria) that hang around in our garden after breeding have been known to
croak after a shower of rain. This one, disturbed by gardening, took to the bird bath.

Miller GL. 2021. The rain calls of frogs and the reigning paradigm of American herpetology. Archives of Natural History 48, 42-61.

Murton RK, Westwood NJ. 1977. Avian Breeding Cycles. Oxford: Clarendon Press.

Friday 1 October 2021

Green Grass and Triggers for Quelea Birds to Breed: 1950s Experiments, Misinterpretations and Later Research

I blanch whenever I see a statement like this one (taken from a published paper): ‘…exposure to green grass is sufficient to stimulate male nest-building behaviour in queleas’ giving the source of the information as Marshall & Disney, 1957. Or like this: tropical birds start to breed in response to the appearance green grass at the start of the rainy season’. When I read stuff like that I know that the authors have not read about or understood the experiments referred to or seem oblivious of the dangers of extrapolating findings in one species to another.

I wrote an introductory article, Rain and Seasonal breeding. An Unsolved Problem in Physiology, in December 2020 (link here). Alan John ‘Jock’ Marshall (1911-1967) was continuing the work he had started in the 1930s as a field assistant with John Randal Baker (1900-1984) on what initiates the breeding season of birds in the tropics. To that end he was studying the reproductive biology of the Red-billed Quelea or Dioch, Quelea quelea, Africa’s bird pest. Seasonal rain was clearly correlated with breeding. In the mid-1950s though Marshall was having an argument with his friend Albert Wolfson (1917-2002) of Northwestern University in Illinois. Wolfson argued that the onset of breeding was always caused by an increase in daylength. By contrast, Marshall countered that the very small changes in seasonal daylength near the equator could not be responsible and of course had lots of observational evidence on the importance of the rainy season. Incidentally, although experiments from both camps and others showed that sufficiently large changes in daylength could have an effect in the queleas, Marshall argued that just because a bird could respond in that way when in populations, or had ancestors from, outside the tropics, other factors, notably connected with the onset of rain, must be responsible for triggering seasonal breeding near the equator.

In Marshall’s autobiographical notes for 1955 written up and edited by his widow, Jane, the background to the work is explained:

…he moved on to Arusha in Tanganyika (now Tanzania) - a small town near the large game reserves and not far from Mount Kilimanjaro. There he was to meet H.J. (John) Disney [Henry John de Suffren Disney (1919 – 2014)], an officer of the Department of Agriculture in Tanganyika who had been studying a small weaver-bird, Quelea quelea. Disney was engaged in full time research into the biology and control of this bird. Like Tilapia, Quelea's success in massive reproduction was an enormous problem—and had been since its first recorded history. The charming little bird, hovering at the opening of its ball-like nest, was a ubiquitous pest over large areas of the drier parts of Africa. “It often exists in such large numbers that flocks are mistaken for locusts. A single breeding colony may consist of more than one million birds building as many as 250 nests to a single thorn bush over a closely bushed area of perhaps four square miles of uninhabited country. Although Q. quelea is less than five inches long and weighs little more than half an once, a large flock may make a physical impact sufficient to devastate an area of timber, snapping branches several inches in thickness.” The species was doing great damage to small grain crops such as wheat, rice, sorghum and millet. At times it was responsible for famines of varying severity. Much attention was being paid to the biology and control of Q. quelea in French West Africa, South Africa and Tanganyika. Explosives, flame-throwers and poison sprays have were used on roosts in attempts to reduce its numbers. Both Jock and the Tanganyika Government were interested in trying to discover more about the environmental and physiological factors which might be responsible for such reproductive success. 

On July 22nd he and John Disney set up a photo stimulation experiment with three cages of Quelea. They agreed on some investigations and later published papers together; 'It will be very good for him to get a few publications out - he is an excellent man for the job that he is doing and, I think, is not appreciated here as much as he should be.' Disney also showed Jock some of the great African animals roaming Ngorongoro crater and he 'showed me giraffe au naturel - they are as incredible in the bush as they are in the zoo.'

Marshall, then at St Bartholomew’s Hospital medical school, with Disney in Tanganyika, went on to a further large  experiment the results of which were published in Nature in 1957. I will describe those experiments because the detail is the key to understanding what as going on.

Groups of young birds (trapped soon after they left the nest) were kept in 4 aviaries and arranged as follows:

Cage I: Nesting bush (Acacia mellifera) of tradi­tional kind, dry seeds of white millet (Panicum miliaceum) and bulrush millet (typhoideum), trough-water, and long dry grass of the genus (Cynodon) the bird uses for building material.

Cage II: As Cage I, but equipped also with a sprinkler simulating natural rainfall for two hours a day (=approx. 0.5 in.). 

Cage III: As Cage I, but additionally with fresh green grass-seeds, long green nesting grass and trays of just-germinated green millet. 

Cage IV : As Cage III, but additionally with a sprinkler for two hours per day (0-5 in. of ‘rain’) and quantities of harvester termites (Hodotermes mossabicus), grasshoppers, and dipterous larvae.

The difficulty of maintaining supplies of green grass, green grass-seeds and live larvae during the dry season was overcome by growing appropriate grasses under irrigation and establishing an insect hatchery. This plantation grass was augmented by fresh grass (Echinochloa stagnina) ccollected by Africans from a distant swamp and dispatched by goods train three times a week. Grasshoppers and termites were collected daily. The cages were 10-30 yards apart, and optically isolated by hessian screens and sorghum stalks. Food, grass and water were replenished twice a day. 

The male birds in all the groups tried to build nests. There were waves of synchronous activity and some demolitions followed by rebuilding. However, a clear result was obtained. During a week two months after the experiment started the number of nesting attempts was Cage I: 1; Cage II: 3; Cage III: 21; Cage IV: 13. 

After demolishing the nests, conditions in Cages I and III were changed such that both had fresh grass and dry food.  Three weeks later, Cage I had 17 nesting attempts; Cage III had 22.

Thus, it seemed, rainfall nor the appearance of protein-rich food in the form of insects were not, by themselves or together sufficient for the building of nests acceptable to females. Marshall & Disney concluded: ‘There is, then, good evidence of the importance of long green grass as a nesting stimulus’. They continued: ‘However, the above figures refer to nesting attempts in which imperfect structures were built. It was found that complete nests were made only when the grass had produced long stems (for the frame of the nest), long blades (for tying the frame together), and seed-heads’.

This is how Jane Marshall described the outcome of the experiments from notes made about the events of 1956:

“…other work was 'going beautifully; I was up till 3 last night working on graphs showing the continuous reproductions of bats and the almost similar condition in cormorants. That's material for two papers”. Then he was going to Raymond Hook's farm to see what he had in the way of lizards, frogs, toads and glossy starlings; and then on to Dodoma to look at Quelea. “I believe that the series of studies that are under way will make our rather primitive and Bakerish New Hebridean effort look like an essay by a member of the biology class at the Tooting Grammar School. Certain I am getting results, whereas the best we could conclude in the New Hebrides was that tropical breeding seasons seem to be ‘controlled by factors not registrable by the senses or instruments of Man’ (I said ‘we’, but I was just a kid and John did all the analysis and the final report without consulting anybody else).' He was particularly happy with the experiment he designed and Disney had carried out on Quelea at Dodoma: “—it seems that it is undoubtedly the appearance of fresh grass that is the chief factor, apart from plumage change & gonad condition, that allows reproduction. This experiment may become a minor classic in the subject?”

Marshall, in a later chapter wrote of these experiments: ‘…that showed that first year diochs (Quelea quelea) were influenced by the green grass that grew after rainfall…’ He also wrote that when the experiments were repeated with older birds ‘it was found that rainfall itself, or the accompanying high humidity, also appeared to influence a strong influence to breeding’. I have been unable to find an original paper describing the experiments on older birds. I suspect some of the experiments were plagued by difficulties. Problems like the failure of plantation grass to mature and the destruction of nesting bushes by weevils were mentioned in the 1957 paper. However, as pointed out in a masterly review of reproduction in the quelea written by by Peter J. Jones, then working in Edinburgh: ‘More puzzling is the fact quelea given only dry grass and dry seed eventually bred anyway, 5 months after first assuming full nuptial plumage’. Did they use the dry stems of Cynodon provided in Cage I or had some of the green grass dried out?

But back to the effect of providing green grass. I think some of the misunderstandings that came later—and are still repeated—were down to Marshall’s choice of words. Green grass was not a ‘nesting stimulus’: green grass was the actual nesting material—it induced or enabled nest building. Indeed induction was the word used in the title of the paper. I suspect that some of those following did not appreciate this distinction and extrapolated, without much thought, the findings of Marshall & Disney to other species, believing that green grass stimulates nesting with whatever material a particular species uses to build its nest.

In terms of perception by the birds, it may not have been the fact that it was grass or green but had physical attributes (size, flexibility etc) that was recognised as suitable weaving material. The question then arises of whether other materials, neither green nor grass, would have proved just as capable of inducing nest building in the Marshall and Disney experiments. In that connexion it is interesting that raffia, soft, compliant and not green, was often used by aviculturists as nesting material for weavers. What a pity that Marshall and Disney did not try another soft material in their aviaries.

At first sight, the conclusions of Marshall & Disney seem reasonable in that the appearance of green grass with stems of length sufficient for the males to build a nest acceptable to females remains the most likely proximate cue provided by the onset of rain for queleas—and possibly other weaver birds—to nest, to lay eggs, to incubate and to rear their young. The whole process thus results in the contemporaneous appearance of young birds in the nest and the period of maximum availability of protein-rich food, in the form of insects and germinating grass seed. That abundant supply of suitable, as stressed by Jock Marshall, is the key to understanding the breeding cycles of seasonally-breeding birds:

The sexual cycle of seasonal birds is regulated by various external factors that ensure movement to the traditional breeding ground in time for the young to be produced at the period of optimum harvest if the food on which they are fed.

However, other criticisms of their conclusion in queleas have merged over the years. Male weavers, for example, will often start to build nests if provided with suitable material, outside the breeding season. It is true that much of the criticism came from the proponents of daylength being the most, if not the only, important factor in triggering breeding. They have pointed out that intensity of light, decreased by rain clouds, for example, or the peculiar, to us, twilight in the tropics may be important. Were that group clutching at straws? I am in no position to judge. However, I think it is true to say that Marshall & Disney's experiments no longer generate the same degree of confidence as to their importance as Marshall himself did.

Since the pioneering work of Marshall & Disney, a great deal of information has been obtained on the  quelea’s nomadic movements, physiological condition, moulting, ecology and whole life history. It has become the most studied small bird in the wild simply because it is of such economic importance as a pest in large swathes of Africa. This subsequent research has revealed a much more complicated picture involving food shortages, protein supply, body condition and migration. Peter Jones reviewed this field up to 1989 in two chapters for a book. Far from leading to the onset of reproduction in wild birds the start of the rainy season results in a food shortage. That shortage is brought about by the germination of the dry grass seed on which they subsist. The current view seems to be that after the onset of sufficient rainfall, the birds migrate to still dry regions. When the new grass crop (only reached with a certain amount of rainfall in a 6-week period) in the original area has matured and the rain front has passed the birds return and breed. The quelea return to a supply of fresh seed and to an increasing supply of insects. By that time of course the rain may also be starting in their temporary refuge. Instead of returning to their original site they may move to an area in a similar state after the rain front has passed. Such is the variable nature of the rainfall that the migration patterns are highly variable from year to year; the great flocks appear to be nomadic but are in fact seeking optimum conditions.

Mathematical models to aid those studying and attempting to control quelea populations, have been constructed in order to predict, given data on rainfall and the availability of grass seed, on where the vast breeding colonies are more likely to be established.

I should point out that much of the progress after the 1950s was driven by Peter Ward (1934-1979) who worked on queleas in both west and east Africa. Because the quelea became so well studied it is not surprising that the data gathered and their interpretation came to be used as evidence to question existing orthodoxies in avian ecological reproductive biology. One example is whether or not there is an endogenous rhythm of reproductive activity in the quelea, accelerated or inhibited by environmental factors (as Marshall and his team favoured). Another example is that proposed by Ward himself (following up the suggestion of others working on birds in the tropics). That is whether a threshold level of stored labile protein (needed to provide the vast quantities involved in the production of eggs) could itself be a proximate factor controlling the onset of breeding in the females of this and other species. On the latter point Peter Jones pointed out that because reproductive events in males are easier to study, the far more complex metabolic happenings in the female culminating in egg laying had often been completely ignored.

My impression on reading some of the scientific literature of the last 65 years is that some old arguments have not been settled, like, as just one example, the question of an endogenous circannial reproductive cycle. Physiological approaches have fallen out of fashion leaving a lot of activity at either end of the spectrum of biological organisation, in behavioural ecology at one end and molecular biology at the other. It is from somewhere in the middle—how organisms work—that cinderellas should be taken to the ball.

Finally, before leaving the quelea I cannot resist pointing out some remarkable attributes of its life history.

  • The complex nest is built in 4 days.
  • The production of eggs is a highly demanding process. The clutch of eggs, produced over a week, is about 30% of the hen’s body weight.
  • Incubation is only 10 days.
  • The young leave the nest at 11-13 days but cannot fly. A week or so later they are left to their own devices and the parents start breeding again, perhaps hundred of kilometres away, having found optimal conditions once more.
  • A large breeding colony may contain several million nestlings. A colony of ’50 ha may remove 50 per cent of the insects available within a 10-km radius during the rearing period’.

Cheke RA, Venn JF, Jones PJ. 2007. Forecasting suitable breeding conditions for the red-billed quelea Quelea quelea in southern Africa. Journal of Applied Ecology 44, 523–533. doi: 10.1111/j.1365-2664.2007.01295.x 


Jones PJ. 1989. General aspects of quelea migrations. Africa’s Bird Pest. Edited by RL Bruggers and CCH Elliott. pp 102-112.  Oxford: Oxford University Press.

Jones PJ. 1989. Factors determining the breeding season and clutch size. In, Quelea quelea. Africa’s Bird Pest. Edited by RL Bruggers and CCH Elliott. pp 158-180.  Oxford: Oxford University Press.

Jones PJ, Cranbrook, Lord. 1981. Peter Ward. Ibis 123, 546-547.

Marshall AJ. Breeding seasons and migration. In, Biology and Comparative Physiology of Birds Volume II. Edited by AJ Marshall. pp 307-339. London: Academic Press.

Marshall AJ, Disney HJ deS. 1957. Experimental induction of breeding in a xerophilous bird. Nature 180, 647-649.

Marshall J. 1998. Jock Marshall: One Armed Warrior, Australian Science Archives Project, Melbourne.

Murton RK, Westwood NJ. 1977. Avian Breeding Cycles. Oxford: Clarendon Press.

UPDATED 4 October 2021