Granted by the Deutsche Forschungsgemeinschaft
Dr. Roland Sossinka
INTRODUCTORY REVIEW ON BREEDING PERIODICITY IN BIRDS
Birds are dependent upon environmental factors for successful reproduction more than other classes of vertebrates. “All species of birds breed at those times of the year when, on the average, young can be profitably raised (Lack 1950). This statement sums up a great number of observations and investigations on breeding periodicity and related ecological factors in many species of birds. The general correctness of Lack’s rule raises two questions: (1) Why are the birds programmed to breed only at those times when young can be profitably raised? and (2) How does the bird “know” when to breed; that is, in what way is the timing of breeding periods accomplished?
The first question deals with the ultimate control of breeding periodicities and the second with the proximate control. With the exception of very few habitats (e.g., tropical islands, Ashmole 1968), in most places on earth there is a succession of periods more favorable to reproduction and periods when reproduction is impossible (or at least requires much more energy input with a decreased probability of success). The duration of the favorable conditions can be very different: three quarters of a year, as in many tropical areas, or one month only, as in some subarctic places. The favorable period can reappear at regular intervals, linked to annual seasons (for review, see Immelmann, 1971), or irregularly, as in some deserts with sporadic rainfalls (Serventy, 1971). The favorable period is characterized by the presence of that environmental factor or combination of factors which actually guarantee the breeding success. These factors are called “ultimate factors” (Thomson, 1950). In many populations of birds, food is the most important factor. After the young are hatched, much more food is needed than before and often a special type as many species raise their young with food different from their normal adult diet (Marshall, 1951). That is why species of the same area, specialized on different food sources, often differ in their breeding periods.
Further ultimate factors are the abundance of nesting sites and nest material, protection against predators, nd the absence of adverse climatic factors such as heavy rainfalls or low temperatures. During the phylogeny, each species had its breeding period restricted to those times of the year when these ultimate factors were present. Individuals who tried to reproduce outside the favorable period had much higher energy costs and were less successful. They gave their genes – which had information for not restricting reproduction to the favorable season – to their young which, born in the absence of the ultimate factors, had a reduced chance of survival and reproduction. That is why selection favored those genomes which restricted breeding to the favorable times of the year only.
While the ultimate control acts during evolution, the proximate control of breeding periodicity takes place in the individual. The birds, whose gonads are in a state of quiescence outside the breeding period (to prevent them from breeding at the “wrong” time and to conserve energy, e.g. by reducing weight during flight) have to activate the entire sexual system. This means that the hypophysial-hypothalamal axis has to release gonadotropic hormones which activate the gonads. The ovary and testes must increase in size, the germinative cells undergo maturation, and sexual hormones must be produced. The latter substances (in some species gonadotropins also) cause some changes in seasonal secondary sex characteristics (e.g., bill coloration or nuptial plumage) and are responsible for the appearance of a variety of sexual behavior patterns. All these events have to take place before the onset of the favorable season. There are two ways to start these preparatory processes in time: (1) External factors trigger the activation or (2) Internal factors (endogenous rhythms) are responsible for the activation.
If any external factor shall start the gonadal activation, this factor must be noticeable to the bird and must occur at a certain interval before the onset of favorable conditions. It has to predict highly reliably the appearance of the ultimate factors in advance.
If such an external factor exists, then during evolution each species’ respective population will develop response mechanisms to these predicting factors which then are called “proximate factors” (Thomson, 1950).
One of the most important proximate factors in birds living in the moderate climate zones is the photoperiod. Many species and subspecies of birds respond to a certain population-specific length of daylight with gonadal recrudescence. Twelve to fourteen hours after sunrise a short light sensitive phase occurs in each individual which, stimulated by long day conditions, is able to transform this stimuli (perceived by the eyes or by extraocular receptors in the central nervous system) into neuro-secretory activity of some specialized cells in the hypothalamus, which results in the release of gonadotropic hormones (Farner, 1970). In the more equatorial zones, the resident species of birds often have a reduced or no photosensitivity. Other environmental factors are known to act as proximate factors; for example, rainfall and related phenomena (Moreau, 1950).
If the favorable season reappears regularly, the gonadal activa- tion can be started by internal factors. An endogenous circ-annual rhythm can induce gonadal maturation at intervals of nearly one year. This was proven in birds kept in laboratories under absolutely constant conditions (Gwinner, 1969). Their endogenous cycles, running free in constant illumination, had an average period length of eight to eleven months. In feral birds this endogenous rhythm becomes synchronized to the annual seasons by external factors (proximate factors in a wider sense), which then are called “Zeitgeber” (Aschoff, 1954). In many of the species of birds investigated thus far, internal and external factors both take part in the regulation of breeding periodicity.
Each population has evolved a pattern of reproductive activity and inactivity and mechanisms regulating the onset and the end of gonadal activity which are highly adaptive, according to the climatic conditions of the area from which it is derived.
MATERIAL AND METHODS
To investigate some parameters of sexual maturation, we selected three species of Estrildid Finches from very different climatic zones.
The family of Estrildidae is known to be a well-defined group of closely related genera (Delacour 1943). Therefore, one should expect to find a generally uniform type of sexual maturation, probably modified by some species specific adaptations. The Estrildids originated in the tropical areas of mid-Africa. From there they dispersed in several waves to India, Southeast and East Asia and to the Australian region (Delacour, 1943, Mayr, 1968). The three species we investigated are: (1) the Fire Finch Lagonosticta senegala from Africa, (2) the Zebra Finch Poephila (Taeniopygia) guttata castanotis from Australia and (3) the Spice Finch Lonchura p. punctulata from India.
We restricted our investigations in the first study to the process of sexual maturation in young individuals, which had the advantage that the confounding factors of prior sexual activity and gonadal atrophy were not present. The ultimate control is the same in first year breeding birds as in adults, and most of the physiological mechanisms regulating the gonadal activation should be the same as well (Sossinka, 1970).
The birds were bred in indoor aviaries or cages. Non-domesticated or only slightly domesticated strains were used (Sossinka, 1970). The young were separated from their parents at about thirty-five days of age and were kept in bisexual groups under relatively constant laboratory conditions (light-dark cycle 14 : 10 hours, temperature 21 to 24° C. relative humidity 55 to 70%). They were fed a diet of mixed millets and seeds, sprouted millet and water ad lib, and three times a week a multivitamin emulsion was added to the water. Additional egg-food and insects (beetle-larva) were given during the first thirty-five days of life when nestlings were being fed by their par-ants.
At regular intervals body size, moult and gonadal size were checked. The following measurements were taken in young males: body lengths; wing length, bill length and width; body weight; number of renewed feathers; volume of the left testis, as measured by laparotomy with an ocular micrometer in a surgical microscope (Sossinka, 1974).
Body growth slows down in all three species after a continuous linear rise. Adult measurements are reached in the Spice Finch
(13 g body weight) and Zebra Finch (12 g body weight) about day 28 to 30 and in the smaller Fire Finch (8 g body weight) at about day 25. The onset of juvenile molt, when the first feathers of the adult plumage appear, is not later than day 35 in the Fire Finch and Zebra Finch and day 40 in the Spice Finch. The end of this juvenile molt, however, differs markedly between the three species. Here the principal differences in time patterns which are typical of the maturation of all primary and secondary sex characters can be seen. The Fire Finch finishes juvenile molt at about 150 days of age, the Zebra Finch around day 90, and in the Spice Finch it takes 200 to 300 days (in some birds even more than one year).
These three differing patterns – a medium, an accelerated and a retarded development – appear even more pronounced in the growth curves of testes volume. Plotted logarithmically, in all three species an initial volume increase in the nestlings is followed by a period of quiescence. Growth is resumed at different ages in each species, and the time needed to complete gonadal growth is very different also. Adult male testes volume is reached in the Fire Finch at 130 days, in the Zebra Finch at 70 days and in the Spice Finch at 250 days. The latter shows the largest intra-individual variation while the Zebra Finch shows the smallest (Figures 1 – 3). In Figure 1, the curve of testes volume in the Fire Finch is slightly corrected to equalize the differences in both weight. For absolute data, subtract 0.2 units.
In general, the type of gonadal maturation is the same in all three species, characterized by an intermediate phase of quiescence. This takes place at the same developmental age in the three species and is comparable to the juvenile refractory period in photosensitive species (Miller, 1954). Besides this homology, the species investigated showed pronounced differences in the rate of maturation. By considering the climatic conditions in the area of origin in each species, the selection pressures responsible for these adaptations become evident.
The Fire Finch lives in and at the edge f the tropical forest of Africa. As reported by Morel (1967), its breeding period is extended to nine or ten months a year with only a short restriction. Independent of the time of the year in which they were born, nearly all young birds can reproduce successfully themselves if their maturation is not too fast or too slow. Very fast maturation means high energy costs and the risk of inexperienced parents insufficiently foraging for food for the nestlings. Very slow means a disadvantage in competing with conspecifics. This presumably primitive pattern of a moderately rapid rate of maturation is not advantageous in central Australia where the Zebra Finch is found nor in India, the native habitat of the Spice Finch. Zebra Finches live in almost all parts of Australia, especially in the arid areas of western and central Australia. Here the rainfalls, which are essential for the food supply of the young, are rare and occur irregularly (Serventy, 1971). The Zebra Finch is an opportunistic breeder, starting to breed immediately after rain (Immelman, 1962). Only those young birds which have an extremely rapid rate of maturation can reproduce in the same vegetation period in which they were born. Otherwise, they have to wait until the next erratic rain falls, which in some places may not occur for twenty or more months. For this reason, natural selection has favored an extreme precocity in this species (Sossinka, 1970, 1974).
In the Spice Finch, on the other hand, egg laying in northern India takes place only during two months of the year (Thapliyal, 1968). Outside this strongly restricted season, successful reproduction seems to be nearly impossible. That is why young birds have to wait for three quarters of a year to start reproduction themselves and, therefore, their rate of maturation is retarded.
While in the Fire Finch and the Zebra Finch, under constant laboratory conditions, the rate of sexual maturation appears rather uniform, in the Spice Finch there are great intra-individual variations. This indicates the relatively environment-independent, internal type of maturation in the Fire and Zebra Finches in contrast to some possible influence of external factors in the Spice Finch. There is evidence that a cold and wet period acts as a proximate factor inducing the onset of sexual activation.
The ultimate factors in the different climatic zones from which the species investigated come cause different patterns in breeding periodicity. According to these differences, the rate of maturation is quite different in the young of these related species: moderately
the in the tropical Fire Finch, extremely rapid in the precocious, opportunistic-breeding Zebra Finch, and retarded in the yearly breeding Spice Finch.
Aschoff, J. 1954. Zeitgeber der tierisch Jahresperiodik.
Naturwissenschaften 41:49-56, 7
Ashmole, N.P. 1968. Breeding and molt in the White Tern (Gy is alba) on Christmas Island. Pacific Ocean, Condor 70:35-55.
Delacour, J.A. 1943. A revision of the subfamily Estrildinae of the family Ploceidae. Zoologica 28:69-86.
Farner, D.S. 1970. Day length as environmental information in the control of reproduction of birds. In: La photoregulation de la
reproductiion chez les oiseaux et les mammiferes. Ed.: Benoit
et Assenmacher, Paris, 71-91.
Gwinner, E. 1969. Untersuchungen zur Jahresperiodik von Laubsaingern. J. Orn i thol . 110:1-21.
Immelmann, K. 1962. Beitrage zu einer vergleichenden Biologie
australischer Prachtfinken. Zool. Jb. Syst. 90:11-196,
Immelmann, K. 1971. Ecological aspects of periodic reproduction. In:
Avian biology. Ed.: Farner, King, Parkes, New York-London.
Marshall, A.J. 1951. The refractory period of testis rhythm in birds and its possible bearing on breeding and migration. Wilson Bull. 63:238-261.
Mayr, E. 1968. The sequence of genera in the Estrilda (Aves). Breviora 287:1-14.
Moreau, R.E. 1950. The breeding seasons of African birds. I. Land birds. Ibis 92:223-267.
Morel, M.Y. 1967. Les oiseaux tropicaux elevent-ils autant de juenes qu’ils peuvent en nourrir? Le cas de Lagonosticta senegala. La Terre et la Vie 77-82.
Serventy, D.L. 1971. Biology of desert birds. In: Avian biology.
Ed.: Farner, King, Parkes. New York-London. I. 287-339.
Sossinka, R. 1970. Domestikationserscheinungen beim Zebrafinken Taeniopygia guttata castanotis (Gould). Zool. Jb. Syst. 97: 455-521.
Sossinka, R. 1975. Quantitative Untersuchungen zur sexuellen Reifung des Zebrafinken, Taeniopygia castanotis Gould. Verh. Dtsch. Zool. Ges. 344-347.
Thaplial, J.P. 1968. Body weight cycle of the spotted Munia, Lonchura punctulata. Bull. Nat. Inst. Sci. Ind. 86:151-166.
Thomson, A.L. 1950. Factors determining the breeding seasons of birds: an introductory review. This 92:173-184.