Notes on biometry, sex determination and moult in Little Tern Sterna albifrons
by Henning Behmann (Schleswig-Holstein/Germany) and Christer Persson (SW Scania/Sweden). With an appendix: Bird protection aspect of Little Tern ringing.
For readers from other continents: The Little Tern Sterna albifrons breeds throughout the southern Palearctic, north to Scotland and S Sweden, and has subspecific representatives in N America, Africa and Australia. There are three moult series in a season, but there is some ambiguity surrounding the extent of the second series.
A majority of breeding Little Terns in N Europe can be sexed from the coloration of feet and tarsi in combination with the depth of the bill. The region of overlap in bill depth measured at the angle of the lower bill is 5.8 - 6.2 mm. In difficult cases the width of the loral line and the depth of the tail fork may be used as additional criteria. Breeding birds from the south Baltic had 2 - 5 new primaries from the third series in May - June. The number of black outer primaries was found to be age-independent, but slightly related to sex (more black primaries in females).
Introduction. Material and methods.
All important criteria needed for sex determination in Little Tern (Sterna albifrons) are contained in Nadler (1976) and in current handbooks (Cramp & Simmons 1982, Glutz & Bauer 1982). Our intent with this note is to assess known sex criteria according to their usefulness, in addition we present data showing the degree of overlap in measurements of male and female. Finally the possibility of age determination with moult patterns as point of departure is discussed, test procedures have been taken from Sokal & Rohlf (1994).
Since 1965 one of us (HB) has ringed adult and young Little Terns in the Baltic coastal area of Schleswig-Holstein, Germany (Behmann, 1998). The main purpose has been to monitor breeding success and to protect the colonies of this endangered breeding species (category 2 on the Red List) of the Baltic area; as a by-product of the project an overwhelming amount of biometrical data has been collected. Recent measurements: 151 males from 1995 - 2001, 117 females from 1998 - 2001 constitute the material of this paper. In all years two Little Terns, one male, one female (out of 244 birds with known age handled between 1965 and 2001) were retrapped as breeding birds in their second calendar year, while 17 males, 13 females and 2 unsexed birds bred in their third calendar year, therefore unringed breeding birds caught on the nest have been aged 3c+ (although the majority probably does not breed until its fourth calendar year). In many birds the sex characters could be checked and substantiated during a sequence of years, and both contrahents of a pair were often caught together. Maximum wing length and tail fork were measured to the nearest millimetre, bill from feathers to the nearest half millimetre, bill depth at the angle of the lower bill to the nearest tenth of a millimetre. Unusual wear in remiges and broken bills were noted particularly, these measurements have been omitted in the calculations. Furthermore the moult status of primaries has been recorded. Our hope is, that this compilation will be of use to bird-ringers faced with the problems of sex-determination in colonies or at migration sites.
Fig. 1. Facial view of female and male in Little Tern.
Fig. 2. 15-year-old Little Tern male, Bottsand, Bay of Kiel 6.7.03. Note (extreme) width of lore and "notch" of lower bill and the fact that the lower bill is slightly longer than the upper. Photo and copyright: Henning Behmann. Thanks to Per Nothagen for scanning.
Fig. 1 shows average "faces" of female and male, Fig. 2 a very distinct, masculine physionomy (all birds are not that "self-revealing"). The combination of bill depth and - in the breeding season - coloration of feet and tarsi: reddish-orange in males, more yellowish in females, will assign practically all birds to either sex. (Tarsus and foot colour alone may be misleading; some females are at least orange in colour, but the male when caught is always more reddish). Cramp & Simmons (1982), quoting from Nadler (1976), add the width of lores as complementary sex criterion: "Black loral line in male wider in front of eye, narrowing more abruptly near base of mandible; in female, narrows gradually from eye to bill, useful only for sexing of known pairs"; this feature has been indicated in the picture. Furthermore BWP measures depth of bill at the basal corner of nostril; in contrast we prefer to measure at the well-defined "angle" of the lower bill, this measurement is the most consistent. The average difference between measurements in Cramp & Simmons and our measurements is 0.25 mm, the mean difference between male and female remains c0.5 mm. One or both bill halves may be broken near the point, therefore bill measurements are more irregular in Little Terns than in larger Terns. Table I presents general statistics for the overall material:
Table I. General statistics for breeding Little Terns from Schleswig-Holstein, Germany.
mean value ± 1 s.e.; 1 s.d. (mm)
mean value ± 1 s.e.; 1 s.d. (mm)
Wing-length, maximum chord
182.6 ± 0.3; 3.9
179.9 ± 0.3; 3.5
Upper bill from feathers
31.6 ± 0.1; 1.6
29.3 ± 0.1; 1.4
Lower bill from feathers
31.7 ± 0.1; 1.5
29.5 ± 0.1; 1.3
Black point, upper bill
6.2 ± 0.2; 2.3
5.9 ± 0.2; 1.8
Black point, lower bill
5.0 ± 0.2; 2.1
4.6 ± 0.2; 1.8
6.20 ± 0.02; 0.19
5.73 ± 0.02; 0.20
40.7 ± 0.4; 4.4
34.6 ± 0.5; 4.9
From the "span" column it is evident, that there is some overlap in the bill depth character; in order to demonstrate this we have plotted bill depth on wing length and bill depth on length of upper bill, the result is shown in Fig. 3. The overlap lies in the region 5.8 - 6.2 mm; birds in this region with wings < 176 mm or bills < 27.5 mm have been females, birds with wings > 187 mm or bills > 32 mm have been males. The limits may be compressed if each measurement - 5.8, 5.9 etc - is treated individually: with bill depth 5.8 mm the overlap area in bill length is restricted to the interval 31 - 32 mm, and one single female with 184 mm wing had bill depth 6.3 mm.
Fig. 3. Bill depth on upper bill from feathers and bill depth on maximum wing length. Regressions drawn, the region of overlap shaded.
In many terns the "head + bill" measurement gives better separation between sexes than bill only, or than any combination of measurements. In 2003 Henning Behmann took this measurement from 75 German breeding birds, 43 females and 32 males. The span was 10 mm, 59 - 69 mm, 59 - 61.9 mm only females, 66 - 68.9 mm only males, mean values females: 62.2 ± 0.2 mm, s.d. 1.5 mm, males: 65.9 ± 0.3 mm, s.d. 1.7 mm. So, 95 % of males lie above 62.5 mm, 95 % of females below 65.1 mm, but both distributions are skewed. The overall distribution is shown in Fig. 4:
Fig. 4. Length of bill + head in adulte Little Terns from Germany, F = females, M = males, n = 75.
This section must start with something genuinely German: a regret and a Zurücknahme (withdrawal), or at least a relativization. In the summer 2001 we wrote about Little Tern moult, based on the general picture given in Cramp & Simmons (1982), Ginn & Melville (1983), Glutz et al. (1982), Stresemann & Stresemann (1966). According to Stresemann, Sterna albifrons has three moult series: "when 6b is growing, a c-series is started, and this may proceed till 4c". In the field, when recording the moult status of breeders or migrants, we may have been in error, however: automatically equalling the non-moulted outer primaries from series a (not moulted in series b) with the black-pigmented outer primaries, which all have a worn and neglected look in summer. According to Cramps & Simmons (1982) fresh primaries are "pale grey", older ones "duller grey" and the oldest ones "black". This implies a change of colour with wear and age. Nadler (1995) has a slightly deviating wording here, he doesn't connect colour with moult state and wear (our translation):
In contrast to the grey inner primaries, the two outermost ones are slate black in most cases. But field observations and museum skins show, that this is by no means always the case. There are more birds with one, three or four black primaries, and the number need not be the same in both wings. The number of black primaries probably declines with age. In juveniles all primaries are darker and the four or five outermost are deep black.
What we feel, after reading and comparing the statements of different authors, is that this matter should be looked into again. Is it possible, that there are A./ black primaries - say, 7b or 8b - exchanged in series b? and B./ grey primaries - say, 7a or 8a - not exchanged in series b? We need to take a closer look at the primaries (using 5x or 10x magnification) in order to know if it is justified always to equal black primaries with primaries left unmoulted in series b. The field-season 2002 will be devoted to this task. So, what we describe in the following section is the number of black outer primaries, which may coincide with the number of primaries not moulted in series b, but on the other hand may fall below or even exceed this number. We have changed the text accordingly, writing "black" instead of "old" primaries.
Preliminary comment to the above: There is more variation in Henning Behmanns larger material (cf. table II), and the following extract from a letter shows his way of attacking the problem in the spring of 2002: From 2002 I record the black primaries as 5 = "fresh" if they have a silvery gloss or hue and are unworn at tips, and as 0 = "old" if they are dull brownish-grey and (in most cases) worn at tips. It seems to me, that it is possible to discern the two feather generations in this way. On 19 June 2002 he recorded a female of unknown age: 5550055055, i.e. P8 was more worn (and seemed to be older) than P9 and P10. On 21 May 2003 CP investigated a female of unknown age with similar pattern, it had P8 + primary covert brownish-black without silvery pigment, P9 - P10 + PCs blackish with silvery pigment, P8 slightly more worn than P9 - 10. In this bird one possibility is that P8 - 10 belonged to the same feather generation, one brownish, two with silvery gloss, the other alternative is that P8 was suspended while P9 - 10 were moulted. Pictures of a 3c (first-breeding) female from Lensterstrand, Lübeck taken by Henning Behmann on 26.6.03 bring us one step towards a solution of this problem, here P7 is obviously from an older feather generation (juvenile plumage?) than P8 - 10, and P9 is black in one wing, silvery in one wing.
Fig. 5. Breeding 3c female from Lensterstrand (1y 1.6.01 - 26.6.03); P7 from juvenile plumage, P9 dark in one wing, silvery in one wing. Photo and copyright: Henning Behmann. Thanks to Per Nothagen for scanning.
By now, many individual moult-cards indicate, that one to three primaries in the region P4 - P10 (P6 - P8) may be left out in a moult series. Late breeding in the Baltic could be the cause; late juveniles from this area being slightly "out of phase" with the overall population and therefore manipulating their moult for one or a couple of years in order to make up for this original deficit. This particular bird, however, hatched at a highly normal date (but it bred at an early age, after 23 months).
Repeating: like the Roseate Tern Sterna dougallii and the White-winged Black Tern Chlidonias leucoptera, the Little Tern has three moult series; the last one (series c) running from February to April and comprising two to five inner primaries. When the birds are brooding or feeding young or when young are fledged, a new series (series a), starting with the innermost primary (P1), is initiated:
1. 3c+ brooding female, Fastensee, Fehmarn 17.6.01. P1 vane emerging from sheath, P2 pin, P3 - 5 fresh from series 3 - i.e. maximum performance in moult series 3 as well!
2. 16c+ brooding female, Bottsand, Bay of Kiel, Germany 15.6.02. P1 0.5.
3. 14c+ brooding male, 19.6.02, Germany. P1 shed
4. 11c brooding male, 22.6.02, Germany. P1 shed
5. 5c+ brooding female, 23.6.02, Germany. P1 - 2 shed in one wing, P1 shed in the other.
6. 14c+ brooding male, 29.6.02, Germany. P1 shed
In May and June 2001 - 02 we recorded the moult status of adult breeding birds in both Schleswig-Holstein and in SW Scania, the number of fresh primaries from the 3rd series is given in Table II:
Table II. Fresh primaries from the 3rd moult series in Schleswig-Holstein and S. Scania, May - June 2001 and 2002.
Germany; new primaries
Scania; new primaries
P1 - P2
P1 - P2
P1 - P3
P1 - P3
P1 - P4
P1 - P4
P1 - P5
P1 - P5
Three German birds showed irregular patterns; one having P1 - 2 older than P3 - 4, two having P1 - 3 fresh on one side, P1 - 2 on the other. Such differences are rather common In addition two were recorded as apparently having all primaries fresh in 2002. There are great individual differences in feather quality; some birds are practically unworn, others extremely worn, to the extent that separation of moult series sometimes is difficult. There seems to be a difference in third series moult between the years 2001 and 2002, but it is not significant at the 5 % level, neither in Germany nor in Scania. In order to press the material, scores from the two areas are pooled and "low performance" (P1 - 2 or P1 - 3) and "high performance" (P1 - 4 and P1 - 5) are pooled in Table III:
Table III. Fresh primaries from the 3rd moult series in Schleswig-Holstein and S. Scania pooled as "low" and "high" performance, 2001 and 2002.
Germany + Scania new primaries
P1 - P2 or P1 - P3
P1 - P4 or P1 - P5
Here an R x C test gives Gadj = 4.30, and since chi-square0.05(1) = 3.84 we conclude that the extent of moult in the third series differs between the two years in the Little Tern material obtained from the south Baltic area. The possible reasons for such a difference in moult performance will be brought up in the discussion.
With close scrutiny of both wings it is likely, that more digressions of this kind will be detected in the future; they are likely to add to our understanding of the excessive feather exchange in this and other species.
If the breeding has been successful, Little Terns abandon their breeding sites and shed their first primaries already by midsummer. In other years there will be late July and August broods in southern Scania (Högstedt & Persson 1975). Still, many Little Terns occurring with begging juveniles on the Falsterbo peninsula in August probably are transmigrants from other Baltic breeding areas: Öland, Gotland, Estonia and Poland. In a few cases the time-schedule of these birds must be strained, and the possibility of anomalies in the three-series moult pattern should be considered. The moult status of the following two birds (Skanör lies on the Falsterbo peninsula) is barely more advanced than that of the German birds moulting on nest two months earlier; has the new series begun (or will it still begin) with P1 in both cases? Compare the first aberrant bird under table II above; it had probably started its 3rd series with P3.
7. 3c+, accompanied by young, Skanör 14.8.99. P1, P2 fresh, P3 0.5, rest of primaries older; ten old tail-feathers.
8. 3c+, accompanied by young, Skanör 17.8.99. P1 - 3 "fresh", P4 - 6 worn, P7 - 10 very worn. (A writing error corrected 7.9.01)
In subsequent years three birds conducting juveniles could be sexed, all were females. The moult state of no. 9 suggests suspension after P6 - before the large primaries 7 - 10 (which are then the first to be moulted on wintering grounds) - and consecutive migration, other late birds must suspend earlier or migrate with growing wing:
9. 3c+ female, accompanied by two young, Skanör 15.8.01. P1 - 4 fresh, P5 0.9, P6 short pin; P9-10 black (from 2nd series?). S1 fresh, S2 0.4; R1 fresh, R2 0.6.
10. 3c+ female, accompanied by two young, Skanör 17.8.01. P1 fresh, P2 0.7, rest of primaries older; P9-10 black (from 2nd series?), ten old tail-feathers.
11. 3c+ female, accompanied by at least one young, Skanör 18.8.03. P1 - 2 fresh, P3 0.8; P7 - 8 less worn than P4, 5, 6, 9 and 10.
The second moult series is interrupted when breeding starts in May, in most cases the process leaves at least the two outermost primaries (P9 and P10) unmoulted. These primaries have a blackish and worn look, contrasting with silvery, rather fresh primaries 7 and 8 (but we need to investigate if there are silvery, unmoulted primaries). A bird in its 18th calendar year from the Falsterbo peninsula 25.5.01 had all outer primaries silvery and fresh (the only one with distinct silvery hue on outer primaries so far seen in Scania), while a bird in its 11th calendar year had P8 - 10 black, suggesting that the number of black primaries could be age-dependent - as suggested by Nadler (1995). The material from Schleswig-Holstein 1995 - 2001 comprises 170 birds; 83 ringed as breeding birds (in their 3rd calendar year or older), 87 ringed as pulli (i.e. of known age when retrapped in later years). Analyzing the "moult cards" of birds of known age (3c - 16c) we tested for age-dependence in the number of black primaries, numbers are given in Table IV:
Table IV. Black outer primaries in breeding birds from Schleswig-Holstein, May - June. Age in calendar years, P10/P10+P9 etc. signify different patterns on wings
3c - 6c
7c - 10c
11c - 16c
An R x C test of independence gives adjusted G = 7.65, 8 d.f. Since chi20.05(8) = 15.51, we do not reject the null hypothesis that the number of black outer primaries in May - June is independent of age. Other partitionings of the material will not alter this relationship.
Next we test for the influence of sex on the number of black primaries. Here the whole material (103 males, 67 females) can be used, numbers are presented in Table V:
Table V. Black outer primaries in breeding birds from Schleswig-Holstein, May - June. Males and females aged 3c - 18c+; P10/P10+P9 etc. signify different patterns on wings.
P10 or P10/P10-P9; n
P10-P9 or P10-P9/P10-P8; n
An R x C test of independence gives adjusted G = 6.85, 2 d.f. Since chi20.05(2) = 5.99, we reject the null hypothesis that the number of black outer primaries in May - June is independent of sex; females have slightly more black primaries than males.
A discussion will follow when older material has been incorporated, and the material from 2002 is at hand.
Appendix: Bird protection aspect of Little Tern ringing
Little Terns are best left undisturbed, any disturbance is likely to add to predation losses and decrease the breeding output of a colony. In order to merit his presence, the ringer should give a positive contribution of some kind: control of predators, habitat improvement, general watch or supervision of the breeding site. At Bottsand (Germany), the breeding is really managed, predators are persecuted, nests protected with cages, the whole area supervised, and at Lensterstrand the colony is protected by a fence and watched. Any disadvantage from human visits is more than outweighed by these contributions, and as a matter of fact the breeding success at Lensterstrand in recent years has really been a bright spot in the Baltic "darkness".
In Scania, many breeding sites are more "natural" than in Germany, and the whole production often gets predated by Herring Gulls and Great Black-backed Gulls. CP has tried the following protection measures:
Removal of broods of Great Black-backed Gull, Herring Gull and Oystercatcher. This doesn't stop gull predation, but it lessens the presence of adult, energy-demanding gulls. I also took the eggs of an Oystercatcher nest - where I knew that one adult was an egg and chick predator - and added them to other nests.
Improvement of plant cover where it has been removed by ice or high-water erosion. I simply dig up turfs of grass and Scirpus and put them on bare surfaces where I feel that they could be needed. This has been helpful, a kind of help for self-help. On the other hand, too much vegetation will make Little Terns abandon a site, this has been the problem of many colonies in urban areas (harbours of Trelleborg, Malmö). Here some degree of mowing, or removal of roots before the breeding-period could be helpful. It is believed, that the vegetation grew too dense at Lensterstrand in the summer of 2002, and part of the roots will be dug up.
Overnight watch of colonies when eggs are hatching (young "cheeping" in the eggs) in order to keep fox and badger away. This is also helpful, but only as long as you are there, the first night you are absent the predator returns.
In general the ringing should be strictly planned in order to minimize the number of visits. Watch egg-laying and calculate hatching-date, then catch one or two days before hatching. On this occasion use the maximum amount of equipment: artificial eggs (real clutches warmed in an insulated bag, then you need not worry about the time factor), walk-in traps, drop-door (the most effective type, it is to be preferred) or Potter traps, flags to mark nests and limits of the colony. Try to be scent-free: no tobacco, deodorant or perfume on hands. Finally, when you leave the area, erase all traces - in Scania most Little Tern nests lie in fine sand. The young are best ringed in the nest when two days old (before that they are too fragile and sensitive). After that, leave the colony on its own and revisit it when you expect to find large, fat young with growing quills, on this occasion make a thorough search. Keep an eye on the water and don't allow young to swim away; under such circumstances they are easily predated by e.g. Common Gulls. If there is rain, wind or low temperatures (often in combination) - cancel a planned visit!
BEHMANN, H. (1998): Zur Situation der Zwergseeschwalbe (Sterna albifrons) an der schleswig-holsteinischen Ostseeküste unter besonderer Berücksichtigung des NSG Bottsand (Kieler Außenförde). Seevögel 19, Sonderheft: 65-70. º CRAMP, S., & K. E. L. SIMMONS (1982): The Birds of the Western Palearctic III. Oxford University Press. º GINN, H. B. & D. S. Melville (1983): Moult in Birds. BTO Guide 19. º GLUTZ von BLOTZHEIM, U. N. & K. M. BAUER (1982): Handbuch der Vögel Mitteleuropas, Band 8/1. Akademische Verlagsgesellschaft, Wiesbaden. º HÖGSTEDT, G. & C. PERSSON (1975): Småtärnan Sterna albifrons i Sverige 1973. Vår Fågelvärld 34: 37-42. º NADLER, T. (1976, new ed. 1995): Die Zwergseeschwalbe. Neue Brehm Bücherei, Bd 495. Ziemsen Verlag, Wittenberg-Lutherstadt. º SOKAL, R. R. & F. J. ROHLF (1994): Biometry; the principles and practice of statistics in biological research - 3rd ed. Freeman and Co, New York. º STRESEMANN, E. & V. (1966): Die Mauser der Vögel. J. Orn., Sonderheft.