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
