BehavioralEcology Behav. Ecol. Sociobiol. 6, 219-227 (1980) and Sociobiology ?) by Springer-Verlag 1980 FlexibleHelper Structure as an EcologicalAdaptation in the Pied Kingfisher(Ceryle rudis rudis L.) Heinz-Ulrich Reyer Max-Planck-Institut fur Verhaltensphysiologie, D-8131 Seewiesen, Federal Republic of Germany Received April 5, 1979 / Accepted October 9, 1979 Summary.The pied kingfisherhas two types of hel- satisfactorycorrelations between social structureand pers at the nest: primary ones, helping their own environment- a prerequisitefor understandingthe parents,and secondaryones, helpingbirds other than adaptivesignificance and evolution of behavior- are parents. Primary helpers are always accepted by lacking. Most investigatorsof cooperative breeding breedingpairs, secondaryhelpers only in poor envi- did not pay enough attention to ecological parame- ronmental conditions where the time and energy ters. With a few exceptions(Brown and Balda, 1977; budget of parents is not sufficient for rearing the Vehrencamp,1978), habitat qualities have eitherbeen offspring alone. Under these conditions, helpers in- ignoredtotally, or the categoriesemployed in ecolog- crease the breeding success of pairs (Tables2 and ical investigationshave been relativelycrude (Gaston 3) by providingadditional food for the young (Ta- and Perrins,1975). We cannot expect to discoverany ble 4). Thus the flexible helper structurecan be seen satisfactorycorrelation between social structureand as an ecologicaladaptation. It is arguedthat - origi- environment,however, as long as we continueto clas- nating from a skewed sex ratio and breedingin co- sify the distributionof animalsand their food merely lonies- this adaptationevolved through the combined as either stable or unpredictable;habitats merely as effects of individualand kin selection. desert, savannah, bushland, forest, or marsh; and food no more preciselythan as grain, fruit, nectar, or insects(for summariessee Emlen, 1978;Fry, 1977; Grimes, 1976; Woolfenden,1976). Introduction The presentand a followingpaper will show that finermeasurement of ecologicalparameters can reveal Helpersat the nest, as definedby Skutch(1961), have relationshipsbetween helper structureand environ- been reported to date in over 150 bird species ment, even for different populations of the same (Grimes,1976; Rowley, 1976; Woolfenden,1976; Za- species.These relationships,which are not biased by havi, 1976).The few featuresshared by most coopera- species-specificdifferences, can be interpreted in tive breedersare easily outnumberedby the diver- terms of ecological adaptation. They also can help sities. Consequentlythe adaptivesignificance of such to assess the importanceof individualand kin selec- cooperative (communal) breeding is poorly under- tion in the evolution of cooperativebreeding. stood and the drivingforces in the evolution of help- ing are controversial.Some scientistsfavor individual selection, others favor kin selection (Brown, 1974, Materials and Methods 1978; M. Dyer and C.H. Fry, unpublishedwork; rudis rudis 1978, 1980; Fry, 1977; J.D. Ligon, unpub- Two breeding populations of the pied kingfisher (Ceryle Emlen, L.) in Kenya (East Africa) were compared, one (20-30 pairs) at lished work; Ligon and Ligon, 1978; Ricklefs, 1975; the Winam Gulf of Lake Victoria (34?18' E, 0O21'S), the other Woolfenden, 1975, 1978; Woolfenden and Fitzpa- (15-20 pairs) at the southern end of Lake Naivasha (36?42' E, trick, 1978). 021' S). Most of the birds in these two colonies had been mistnet- This controversyseems to arise partlyfrom exist- ted and were individually color-ringed or wing-tagged. Some casual observations in a colony of over 50 pairs at Lake Simbi (34?38' E, ing species-specificdifferences, and partly from the 0O21'S) were also recorded. These investigations are part of our lack of data regardingthe effects of helping on inclu- continuing studies, commenced in 1975, on the ecology and the sive fitness,both for breedersand helpers.Moreover, behavior of various East African kingfisher species (Alcedinidae). 0340-5443/80/0006/02 19/$01.80 220 H.-U. Reyer: Flexible Helper Structure as an Ecological Adaptation Results Hand-reared yearling pied kingfishers bred success- fully in our aviaries, their first clutch containing five General Remarks on the Biology eggs from which four young hatched. These figures of the Pied Kingfisher do not differ from those which we found in older breeders. Further information on the biology of the Within their East African range, pied kingfishers in- pied kingfisher is given by Douthwaite (1970, 1973, habit many lakes and rivers and are particularly fre- 1976, 1978), Sugg (1974), and Migongo (1978). quent in the marginal regions of the big freshwater lakes. They live almost exclusively on fish. To catch their prey, they fly over the water searching, some- Comparisonof Two Colonies times hovering above the surface, and plunge swiftly when they see a fish. They swallow small fish while Sex Ratio and Population Structure in the air, and continue searching. Bigger fish are carried to perches on the shore and battered before In both study areas there was a significant surplus being swallowed. Direct dives from such perches were of &d. At Lake Victoria, SS outnumbered Y? by rarely observed in the areas investigated. 1.8:1 (107,3S, 61 ?Y; P<0.01, x2 test), at Lake Nai- Outside the breeding season, pied kingfishers can vashaby 1.7:1 (33 SS, 19 YY;P<0.05). These figures be seen singly, in pairs, or in small groups along are based on counting both ringed and unringed birds. the whole shore area. In the evening, they congregate For the same L. Victoria colony, Sugg (1974) obtained at communal roosting sites. During this time of the a figure of 2: 1, both in 1971 and 1972. Similar sex year, considerable local movements may be under- ratios ranging from 1.5 to 2.5 have been reported taken; these can carry individuals over hundreds over by Douthwaite (1973, 1978) for breeding and non- kilometers (Backhurst, 1974). In the breeding season, breeding populations in Uganda and Zambia. Only the birds usually concentrate at rivers, canals, road one of his counts, made at a roost, resulted in an embankments, and other places having sandy or clay even sex ratio. All these data taken together suggest banks, not too far from the lake. Here 20, 50, 100 that in populations of adult pied kingfishers, there or more birds excavate nesting holes. In this way, are 1.8 as many SS as Yy (1074 S, 610 yy; breeding colonies are formed. The average distances P<0.001). Among the young, however, an even sex between adjacent nesting holes were 5.2 m at L. Victo- ratio seems to exist. Out of 40 nestlings and fledglings ria and 1.6 m at L. Naivasha. Both are well above which were sexed either by laparatomy of by hand- the possible minimum (0.5 m) found in the pied king- rearing them to maturity, 21 were 3S, 19 ii (1. 1:1). fisher and in other colonial breeders such as bee One reason for the later-occurring skew toward eaters. Therefore - and because suitable, unused nest- a surplus of S3 probably lies in a higher mortality ing places were in the vicinity of both colonies - rate of breeding Yy. Incubating and brooding at night the carrying capacity of the habitat was probably fall to the Y exclusively, and even by day the Y per- not exhausted in respect to nesting sites. It was not forms the greater part of these activities. Conse- exhausted in respect to food either. All members of quently it is more endangered if nesting holes cave the colony hunted in the same area over the lake in or are flooded, as well as by nest predators such and did not defend individual fishing grounds. Only as the monitor lizard ( Varanusniloticus), cobras (Naja in the vicinity of the nesting holes did SS and ? spec.), and the ichneumon (Herpestes spec.) (Douth- behave territorially. waite, 1970, 1978). All four breeders which disap- The sexes can be distinguished by plumage differ- peared during our study were Yy, and though this ences: ?? have only one broad, interrupted chest- toll on breeding Yy was low in our colonies (6%), band; SS have in addition a second narrower, unin- it may be much higher in other colonies where preda- terrupted band. This is more pronounced and even tion rates of more than 40% have been found (Douth- in older SS than in yearling &S. The SS and ?W waite, 1978). take turns incubating the eggs from which the blind, A second reason for the skeward sex ratio may naked young emerge after 18 days. From the first be a higher mortality rate of juvenile YY. In contrast day, they are fed with fish brought from the lake to yearling SS, yearling Yy do not apparently return mainly by the X, and possible helpers; later, when to their natal colonies (Table 1). A stronger dispersal brooding declines, the ? joins increasingly in feeding of Yy has also been observed in other bird species. the young. Nestlings are fully fledged after about It has been suggested that on their routes into distant, 26 days and can fish for themselves roughly 14 days unknown areas, Yy might be endangered more than later, but stay with their parents for several months. &S remaining in familiar areas (e.g., Zahavi, 1974; Sexual maturity can be reached within the first year. Woolfenden and Fitzpatrick, 1978). This phenome- H.-U. Reyer: Flexible Helper Structure as an Ecological Adaptation 221 Table 1. Recaptures and resightings of juvenile and adult pied king- Table2. Number of pairs with and without helpers in two pied fishers, ringed in the same colony at L. Victoria the previous year. kingfishercolonies. The differenceis significant(P<0.005) when Data from 1976 to 1979 pooled. Juvenile birds were nestlings when in both colonies only the categoriespairs withouthelpers and pairs ringed, adults were ringed as > yearlings. The data ca. 32 O'S and withhelpers are considered (x2 test). No differenceis madebetween ca.