1969 JEAN BbARD: ADAPTIVE RADIATION IN ALCIDAE 189

ADAPTIVE RADIATION IN ALCIDAE

JEAN BBDARD

Received on 25 December 1967

The present article is an outgrowth of a long-term study on ecological segregation among three species of plankton-feeding Alcidae (BCdard 1967). It represents an attempt to integrate our knowledge of the relationships between the various species of this large group of marine birds.

The family is interesting among birds in being the only one that in the Northern Hemisphere has achieved adaptive radiation within a broad and diversified ecological zone, the subsurface waters of the ocean. Since no other sea-bird family occupies this ecological zone, the family Alcidae gives us an opportunity to examine a group remarkably free of interactions with other groups, a condition seldom encountered in terrestrial situations. The only other sea-birds that could " compete " with Alcidae are several Pelecaniformes; but the latter are exceedingly different from the auks in build and in general adaptation ; moreover, they are not generally abundant in the Northern Hemis- phere and most of them are inshore feeders. For these reasons, they can hardly be considered to interact to any significant extent with the auks. The bulk of the remaining species of marine birds are Procellariiformes or Laridae: all of these are surface feeders, basically dependent on the neuston for their food, a resource generally not utilized by any of the auks.

General information on the diversity of the family and on the biology of its members will be found in Bent (1921), Kartaschew (1960) and Kozlova (1957), as well as in a number of monographs dealing with various species (Drent 1965, Myrberget 1962, Paludan 1947, Tuck 1961, etc.). It may be emphasized that the family is both taxonomic- ally and ecologically homogeneous." All alcids are solitary feeders which propel them- selves under water with partly opened wings and which capture relatively small, individual prey organisms in pelagic environments and swallow them one by one under the water. The Black and Pigeon Guillemots Cepphus grylle and C. columba are partial exceptions as much of their feeding may be done on or close to the bottom and in littoral waters.

Auks are either specialized plankton-feeders, specialized fish-feeders, or feeders on both plankton and fish. Plankton-feeders include Aethia, Plautus and Ptycoramphus. Aethia spp. are known to feed, at least during the summer, upon herbivorous plankton such as Calanus and Thysanoessa (BCdard 1967); Plautus is reputed to take a variety of planktonic organisms, but apparently relies mostly upon the abundant calanoid copepods and euphausiids (Bateson 1961, Kartaschew 1960, Salomonsen 1951); Payne (1965) has reported that Cassin's Auklet Ptycoramphus aleuticus depends for its feeding upon shoals of euphausiids.

Fish-feeders include Uriu, Aka and Cepphus (see Belopol'skii 1957, Tuck 1961, etc. for information on food habits). Abundant shoaling fishes such as capelin (Mallotur), herring (CZupea), polar cod (Boreogndus) and sand eels (Ammodytes) make up the bulk of their diet.

The puffins (Fratercula, Lunda, Cerorhinca) are known to feed on both plankton and fish. All species bring exclusively fish to their nestlings, but do a large amount of their own feeding upon marine invertebrates (Swartz 1966, for Lunda; Belopol'skii 1957, for

" The recent contention that the genus Utiu needs to be removed from the Alcidae (Gysele & Rabaey 1964), though entirely acceptable to me, is ignored in the present discussion.

190 JEAN B h A R D : ADAPTIVE RADIATION IN ALCIDAE IBIS 111

Fraferculu mctku ; Kozlova 1957, for Cerorhinca). The Parakeet Auklet Cyclwrhynchus psiftacula is somewhat intermediate between the true plankton-feeders and the puffins in that it feeds largely on carnivorous planktonic forms such as pelagic amphipods, arrow- worms, fish larvae, polychaetes, cephalopods, etc. (BCdard 1967).

Finally, much less is known about the feeding habits of Endomychusu, Synthliborumphus and Bruchyrumphus. These murrelets are restricted to coastal waters (except Synthlibo- ramphus). Though some forms are known to pursue shoals of small fishes (B. murmorutum -Grinnell, quoted in Bent 1921 ; unpubl. obs.), they probably depend mainly upon marine invertebrates (B. brevkosfre-Kischinskii 1965). Worms, gammarids, molluscs and other small hard-bodied organisms probably make up a substantial part of their diet.

THE BILL AND TONGUE IN ALCIDAE In several genera (notably the Homed and Atlantic Puffins Fruterculu spp., the

Tufted Puffin Lunda cirrhutu, and the Crested Auklet Aethiu cristatellu) the bill has acquired characteristics whose obvious function lies in courtship and communication. These radical modifications prompt the use of caution in the use of standard measurements of bill length and depth that may have validity in some other groups for the type of comparisons intended.

The relative width of the bill at the base is the major variable within the family which appears to be independent of secondary bill characteristics. Species which prey on small, soft-bodied organisms such as calanoid copepods require a wide beak and a flattened palatal surface (similar trends have been described by Murphy & Harper (1921) in the small, Southern Hemisphere plankton-feeding divers, the Pelecanoididae), whereas those preying on fast-swimming, hard-bodied pelagic fishes have much narrower bills with a much reduced palatal surface often marked with grooves and ridges.

The mechanics involved in this fundamental difference of adaptation remain to be studied in detail, but the basic difference between the two types is apparently the following: in the plankton-feeders, the stresses in capturing prey organisms are distributed in the anterior region of the bill, or in the region anterior to the choanal slit; in the fish-feeders, the point of maximum stresses moves back to a point located at the level of the anterior end of the choana. The relative extent of the anterior region of the palate in these two types can be compared by examining Figs. 1 and 3. Mutual similarities of structure within the group of plankton-feeders and within the group of fish-feeders are readily apparent in these two figures. These modifications are perhaps related to, or accompanied by, modifications in the kinetic properties of the skull. Such differences in kinetic capabilities were found in waterfowl; the fish-feeding species in the latter group show the highest degree of jaw protraction while the small " grazers " exhibit limited abilities in this respect (Goodman & Fisher 1962). The kinetic property of the skull may have much to do with the manipulative capabilities of the bill and the type of food eaten (Zusi 1967), but this important aspect remains to be investigated.

Other adaptations in the feeding apparatus can be followed through a gradient from the plankton-feeders to the fish-feeders. In the former group, one observes a maximum development of blade-edge and irregularly arranged hornue papillae (denticles) in the anterior region of the palate. This condition reaches an extreme in the Dovekie Plaufus alle (Fig. 1). In the fish-feeders, the total number of palatal denticles is reduced to only a few arranged in fairly regular rows in the anterior region of the palate (Fig. 3). More- over, the denticles tend to be sharply pointed when compared with those of the first group.

Finally, in the puffins, Rhinoceros Auklet Cerorhinca mnocerata and Parakeet Auklet Cyclorrhynchlu psitfuculu the above characters are intermediate: the palatal region anterior to the choanal slit is moderately broad and the number of denticles lies between the numbers found in the two basic groups.

1969 JEAN BhARD: ADAPTIVE RADIATION IN ALCIDAE 191

This is believed to be instrumental in two ways: first, the handling of small food particles would be difficult, if not impossible, with a cornified and rigid tongue as is typical of the fish- feeders; second, the presence of a sublingual diverticulum (used to transport food to the nestling and developed only during the breeding season) requires a flexible tongue to

In the plankton-feeders, the tongue is broad, thick and fleshy (Fig. 1).

FIGURE 1. Profile of the bill, palatal surface, tongue it2 situ and extruded tongue in profile in (a) Pluutus alle (tongue in profile and from below), (b) Ptycorumphur uleuticu, (c) Aethirc pusiUa. The shading on the extruded tongue shows the extent of cornification.

The arrow indicates the position of the commissural point. Approx. x 1.4.

FIGUIW 2. Profile of the bill, palatal surface, tongue in sitri and extruded tongue in profile in (a) Cycforrhynchus psittuculu (tongue in profile and from below), (b) Fruterculu conticuluta. The arrow indicates the position of the commissural point. The shading on the extruded tongue shows the extent of cornification. (a) appros. x 1.2; (b) approx. ~ 0 . 6 .

192 JEAN B ~ D A R D : ADAPTIVE RADIATION IN ALCIDAE IBIS 111

FIGURE 3. Profile of the bill, palatal surface, tongue in situ and extruded tongue in profile in (a) Brachyramphus marmoratum, (b) Cepphus columba, (c) Uria aalge (extruded tongue in profile and from above). The arrow indicates the position of the commissural point. The shading on the extruded tongue shows the extent of cornification. (a) approx. x 1.4; (b) and (c) approx. ~ 0 . 6 .

push the food particles at the floor of the buccal cavity into the diverticulum itself. At the other extreme, a long and slender tongue enclosed to a large degree in a rigid horny shield gives excellent leverage in firmly ‘ I locking ” large prey organisms against the palatal denticles. The maximum development of this condition is reached in the Common Murre Uria aalge (Fig. 3 ) but it is also clearly exemplified by the murrelets Bruchyrumphus and the guillemots Cepphus.

The puffins (Fraterala and Lunda were examined) have an intermediate type of tongue that is only enclosed in a horny covering in its distal third and not on the upper surface, which is fleshy. This condition may be adaptive in two ways: it allows the successive capture of several prey items; it is also related to a definite increase in the proportion of invertebrates making up their diet. (The Razorbill Alca tor& also shares with the puffins and the Rhinoceros Auklet the ability to capture and carry several prey organisms held crosswise in the bill; unfortunately the tongue of Alca could not be examined .)

Two species of auklets considered in an earlier study (Aethiu pusillu, Aethia cristatella, BCdard 1967) show, as expected, great similarity in feeding adaptations: the denticles are about equally abundant and have an irregular distribution in the anterior palatal region; tongue cornification is of the same extent, that is limited to the very tip. The bill, palate and tongue of Cyclorrhynchuspsittacula are shown in Fig. 2 and can be compared with the same structures in Aethia pusillu in Fig. 1 : in the former, there is a marked reduction in the number of palatal denticles, though the palatal surface remains relatively broad. Tongue characteristics are quite similar in the two genera.

ANALYSIS OF ADAPTIVE TRENDS

Is it possible to find a ratio, independent of body-size, which reflects the major adaptive trends in feeding in a quantitative manner? Can we arrive at a graphic expression of this

1969 JEAN BEDARD: ADAPTIVE RADIATION IN ALCIDAE 193

radiation? The use of the ratio bill-width/bill-length is not satisfactory for reasons out- lined earlier and the ratio bill-width/gape was preferred (gape is here taken as the distance between the commissural point and the tip of the culmen). Some disadvantages of this ratio must, however, be mentioned. For standardization of the measurements, width was measured at the posterior edge of the nostrils, as close as possible to the tomial edges, avoiding the operculum which, in some species, extends further out than the tomia. In Fraterala, this measurement happens to be a good approximation of the maximum bill- width since it is taken close to the commissural point: in Aka, the posterior edge of the nostrils is approximately at the mid-point of the distance between the culmen tip and the commissural point. For this reason, small differences in the value of this ratio for different species are probably meaningless. Moreover, the measurement of the gape is not always an adequate measurement on skin specimens. These difficulties could be avoided if dissected specimens were used, but this is hardly feasible at the present time owing to the lack of material in the collections.

Measurements of the bill and values of the ratio bill-width/gape for most members of the family Alcidae are given in Table 1 . The graphical representation of the ratio

TABLE 1. Bill characteristics, body wetght and ratio bill-widthlgape in various Alcidae. SPECIES CODE BILL-LENGTH" RILL-DEPTH" BILL-WIDTH~ CAPE" BODY-WEIGHT ?BODY-WEIGHT BILL-WDTH/ N

Pbutus alle A 14'00, 8.62(15) 8.53 22.56 166.2(8)' 5.51 0.377 16 Pinguinus B 80.01 - 16.73' 1O7.9Sy c. SOOO' 17.09 0.155 - AIca tor& C 32.34 22.87 9.07 5 2 4 0 737.7(81)' 9.02 0.173 7 Uria lomviu' Dd 37.24 15.41 10.54 59.27 975.5(79Y 9.9 I 0.177 7 Urla aalge' Ee 48.11 15.04 9.97 68.77 9304(41)j 9.94 0.145 10 Cepphus gryllc F 3016(8) 9.60(6) 7.68(7) 4431(8) 431.2(78)' 7.55 0.173 -

0183 11 Cepphus g 33.30 11.28 8.03 43.86 4834(6)' 7 4 5

0.147 13 Brachyramphus h 16.50 6.00 4.71 32.03 234.5(3) 6.16

0.168 15 B. brevirostre i 10.48 5.09 4.64 27.15 237.0(3)' 6.19 Eirdomvchura i 1845 6.06 4 7 2 31.26 155.9(7P 5.38 0.151 6

(B) OAPB

lmpennis

columba

marmoratunr

. . hypokuca

crnllquum 1 14.01 7.18 529 2640 2333(2)

E. craveri k 19.11 5 4 8 4.66 29.55 151.1(8)' 5.34 0.158 8 Synthliboranrphirs

6.15 0,197 13 Ptycaramphus m 19.09 9.31 8.01 22.91 1726(19)' 5.57 0349 8

aleutica

psittacula

crlstalella

0.302 14 Cyclarrhynchirs n 16.07 1433 7.85 26.01 317.6(7) 6 4 2

12.48 12.45 7.97 24.41 284.5(16) 6.57 0.326 21 Aethia

A. pusilla p 8.86 7.74 6.24 16.48 86.3(26) 4.42 0,379 16

Cerorhlnca r 344a 17.74 10.54 44.76 571.0" 8.30 0.235 12

0

A.pygmaea q 1017 6.50 5.42 16.27 118.0" 4?40 0333 4

monocerata

arctlca Fratemula S 49.26 37.94(14) 10.71 36.68 5104(70)s 7.99 0,291 I5

F. cornlculata t 51.17 43.63 10.74 39.46 647.3(12)" 8.65 0.262 10 Lunda cirrhata u 59.69 43.55 14.35 47.9Y 838.2(7) 9.43 0.299 12

Notes. The code letters refer to Fig. 1. Atlantic species are characterized by a capital letter; Pacific species by lower case; amphioceanic species by juxtaposed letters. The order is from Peters (1934). Sample size is given in the last column except when it differs between columns: in such cases, it is given in brackets immediately following the measure- ment. Italicized sample size indicates that both sexes are included in the sample which otherwise comprises only adult breeding males. Unless otherwise indicated, all measure- ments were obtained by myself, either in Alaska (body-weight of several species in particular) or on specimens in collection at the University of British Columbia, at the Museum of Vertebrate Zoology, Berkeley and at the Redpath Museum of McGill University. A few species of restricted distribution are omitted.

a, Exposed culmen; b, maximum depth: in Aethiu pusillu, it includes the horny pro- jection on the bill, but not in Cerorhincu monoceruta; c, at the posterior edge of the nostrils; d, from commissural point to tip of culmen.

1, One measurement obtained on St. Lawrence Island, Alaska (SLI) and seven values from Johnson (1935); 2, from data in Coues (1868): weight estimated; 3, from Belopol'skii (1957); 4, mixed subspecies; 5, from Swartz (1966); 6, five measurements obtained on SLI; one given in Swartz (1966); 7, one measurement obtained on S L I ; two on specimen labels in Berkeley; 8, weights given on labels of specimens in Berkeley; 9, from Thoresen (1964); 10, calculated from regression line; 11, mid-point of extremes given in Kozlova (1957); 12, five measurements obtained on SLI; seven given in Swartz (1966).

Subspecies are not indicated.

194 JEAN BEDAHD : ADAPTIVE RADIATION IN ALCIDAE IBIS 111

bill-widthlgape versus body-size for these birds is given in Fig. 4. ‘The horizontal clusters can be taken to represent various trophic levels and have, needless to say, been determined afterwards, on the basis of our knowledge of the feeding habits of the key species.

.t/ Body-weight

FIGURE 4. ‘The relationship between size (cubic root of body-weight) and the ratio bill-width/gape in Alcidae. Explanations in the text. The letter code is givcn in Table 1 .

EVOLUTION OF THE ALCIDAE Storer (1945) suggested that Endomychura is the most primitive member of the family

as indicated by its two eggs, small I ‘ primitive ’’ bill, small body-size and absence of difference between summer and winter plumages. In the present discussion, Endomy- chum is considered to be a specialist (see below). Storer further says that the Alcidae, rather than showing adaptive radiation, show a series of “ parallel trends ”. He then continues: ‘ I . . . trends toward deepening and lateral compression (of the bill) are to be found in Synthliboramphw and the auklets, auks and puffins” (p. 155). Storer is neglecting the fact that the bill, in this family in particular, is not exclusively a food-getting tool but is also used extensively as a social releaser (sensu Tinbergen) and hence is subject to many different types of selective pressures. When considered as a social releaser, the bill in the family does show parallel trends, but when considered as a feeding apparatus, we observe rather a continuum, or a gradation, which is equivalent to adaptive radiation.

This gradation from one trophic level-plankton feeding-to another-fish feeding- has been accompanied by a relative increase in body-size with an increase in prey-size; this is borne out in Fig. 4. There are clearly limits to the s u e of a bird feeding on any given prey. A plankton-feeder must not exceed a certain body-size or its energetic balance quickly becomes unfavourable. In the same manner, too big a reduction in size for a plankton-feeder, though it could theoretically open the possibility of exploiting a very rich food source made up by the microplankton (Pseudocalanus, copepod nauplii, etc.), is impossible for it would create an unfavourable surface to volume ratio.

The acquisition of diving habits has entailed structural modifications which consist mostly in a marked increase in compactness and strength of the skeleton and in a reduction of the wing for

In the same way, there is an optimum size for feeding on fishes.

1969 JEAN BBDARD: ADAPTIVE RADIATION IN ALCIDAE 195

increased efficiency in underwater propulsion. The largest fish-feeders (&a) are already close to a critical upper threshold of body-weight compatible with the power of both aerial and submarine flight, and any increase above that threshold could not be made without the loss of one or the other attribute (Storer 1960).

special ” adaptation (such as modified rictal feathers to ‘ I skim ’’ the microplankton, or the loss of aerial flight to allow the exploitation of medium-sized pelagic schooling fishes), one may expect an ideal combination of body-size and feeding adaptation for any one of the levels illustrated in Fig. 4, and this seems to be the case. In the North Pacific and the Bering Sea, plankton-feeders are represented by five species whose ranges overlap (or overlapped before disturbance by man) in parts of the Aleutian chain. In the North Atlantic, only one form fills the equivalent niche, namely Plautus alle. In the eastern North Pacific, Ptycoramphus aleuticus alone occupies the niche in boreal and subtropical waters from the Alaska Peninsula to Baja California. Both Plautus and Ptycoramphus are of intermediate body-size for plankton-feeders.

Similarly Fratercula urcticu, the only North Atlantic representative of the intermediate level, is also of intermediate body-size for that particular cluster. Cerorhinca, a medium- sized puffin, could perhaps be considered another example of this phenomenon. Alone in the southernmost portions of its range, however, it has a distribution that overlaps with Lunda and to a lesser extent with Fratercula on both sides of the Pacific.

The spread in body-size at the level of the fish-feeders(Fig. 4) is, however, considerable and requires special attention. The murrelets Endomychura and Synthliboramphus are so small in both body-size and bill-size that it is doubtful if they feed much on fishes (Howell 1917) and doubtful that they could catch and carry fish to the nestling. The true plankton-feeders have evolved the sublingual diverticulum to facilitate the transport of a sufficient volume of food to the nest. Synthliboramphus and Endomychura, lacking such a structure, have instead greatly shortened the nestling stage to one or two days during which, so far as is known, the chick is not fed (Bent 1921, Howell 1917). The biology of Brachyramphus is not well known but the parents of at least one species, B. marmoratum, are known to carry fishes to the nest. Moreover, the evidence reviewed by Drent & Guiguet (1961) seems to indicate that the chick leaves the nest before the acquisition of the power of flight and there could well be a tendency toward a shortening of this stage. Virtually nothing is known of Kittlitz’s Murrelet B. brewirostre, though a recent nest discovery revealed the presence of a partly grown chick (Thompson et al. 1966) and the pattern is probably similar to what has been described in marmoratum.

So the murrelets display at least one important adaptation that seems directly related to their general reduction in body-size. But as far as morphology of the feeding apparatus is concerned, there is little doubt that they are true fish-feeders.

As I have hinted earlier, by sacrificing the power of flight, the Great Auk Pinguinus impennis, which figures at the extreme right of the fish-feeders’ cluster, also diverged widely from the ideal central type.

Within any one of the clusters, a number of factors-long-term differentiation, character displacement, etc.-have presumably played a role in ensuring further radiation and diversification; but their roles cannot now be assessed. However, the family contains a number of groups or pairs of species that offer interesting grounds for specula- tion and good material for the study of those evolutionary forces that tend to promote ecological diversification: for instance, the two closely related and poorly differentiated murres (Uria lomoia, U . aalge) with broadly overlapping ranges and habits; the auklets of the genus Aethia which show marked divergence in characters of body-size and plumage but little ecological differentiation (BCdard 1967); the two murrelets (Brachyramphus) that replace each other around the coasts of the North Pacific but yet have diverged considerably in the dimensions of their feeding apparatus (Table 1) though maintaining great overall similarity in habits and plumage.

So, excluding any

196 JEAN B~DAFUI: ADAPTIVE RADIATION IN ALCIDAE IBIS 1 1 1

MacArthur & Levins (1964) generalized that there exist two extreme types of niche- exploitation: in one, the different species living at the same trophic level remain adaptable and are able to coexist because of specific behavioural differences that keep them ecologic- ally separate; in the other, they can have broadly overlapping responses to the environ- ment, but they usually differ in size and this difference is of the order of 130 : 100. This alone forces them to feed upon different portions of the food resources. The ratio- for which the term “ ratio of character difference ” has been coined-was first proposed by Hutchinson (1959), who also suggested that a difference of this nature in the trophic apparatus alone need not be accompanied by an equivalent difference in body-size; in practice, however, the latter will usually follow.

I have calculated the ratio of character difference for some auk species pairs on the basis of culmen-length. Aethia cristatella and A. pusilla differ in culmen-length in the proportion of 141 : 100 and there is a corresponding difference in body-size. The available evidence on food habits (BCdard 1967) indicates that A. cristatella and A. pusilla belong to the same trophic level; they also exhibit a large degree of overlap in habits and in behavioural reactions to the environment (daily pattern of activity, choice of nesting terrain, etc.).

The case of the trio Aethia cristatella, A. pygmnea and A.pusilla is much less clear owing to the lack of information on the biology of A. pygmaea, but the fragments we have accord well with expectation. In the Aleutian Islands, pygmaea is sympatric with its two congeners and is scarce and sparingly distributed (Murie 1959, Gabrielson & Lincoln 1959). In the Kurile Chain, Gizenko (1955) considers pygmaeu to be abundant (“ large flocks everywhere ”) possibly becausepusilla, a potential competitor, is absent. The ratio of character difference for pygmaea and pusiZZu is 114 : 100.

Both species of Brachyramphus overlap in southeastern Alaska where they occur together in inlets and around glacier outlets. Though they do not differ appreciably in body-size, the ratio of the culmen-length of marmoratum to that of brevirostre (taken in the area where both occur) is 157 : 100. I t is quite probable that this alone restricts the two species to very different portions of the available food resources. There is no information on the ratio of character difference for allopatric populations of the two species.

Both species are of recent origin, lomvia having most likely evolved on the margins of the Polar Basin during one of the glacial periods (Udvardy 1963). Both species now have widely overlapping distributions in the sub- arctic waters of the North Atlantic and North Pacific (Tuck 1961). The case is further complicated by the presence in the North Atlantic of a third ecologically allied species, Aka torda.

The plasticity of Uria makes comparison between them difficult, especially as they do not always vary in the fashion expected and in at least one geographic area (the Pribilof Islands, southern Alaska) the two species have a very similar bill-length. Storer (1952) gives 48.80 mm as the average bill-length of nalge males in southern Alaska and 45.26 mm for lomvia males: ratio of character difference, 108 : 100.

It appears that lomvia has a tendency to eat more invertebrates than aalge: from Swartz’s analysis (1966), the percentage of stomachs containing invertebrates and fish remains respectively was 34 and 63 for lomvia, and 6 and 95 for aalge. The bill-width/ gape ratio is higher in lomeria than in aalge (0.173 against 0.145, Table l), but, as mentioned earlier, it is difficult to compare small differences in this ratio owing to the defects inherent in the gape measurement and also, in the present case, owing to the fact that it was im- possible to measure sympatric races. However, examination of several specimens of the two species revealed consistent structural differences between them that reinforce the ratio difference: the tongue of lomvia is wider and fleshy throughout its entire upper sur- face; the extent of its cornification below and on the sides is much reduced when compared to aalge; moreover, there is a substantial increase in the number of palatal denticles,

The case of Uria is more difficult.

1969 JEAN B h A R D : ADAPTIVE RADIATION IN ALCIDAB 197

especially in the anterior portion of the palate. As we have discussed earlier, these traits are associated with an increase in the proportion of invertebrates in the diet. The elucidation of these relations within the Uriu species-pair would be a promising subject of investigation. In this connection it is interesting that several observers have mentioned large oscillations in the relative abundance of the two species from year to year (Fay & Cade 1959, Preble & McAtee 1923, Sergeant 1951, pers. obs.). Unfortunately, insufficient quantitative data are available; but these reports, together with the clustering of three ichthyophagous forms ( W u spp., A h ) in the same area of the model (Fig. 1), point to a rather “ unstabilized ” system, possibly as a result of its recent formation.

ACKNOWLEDGMENTS The present article is a part of a dissertation submitted to the Faculty of Graduate Studies,

University of British Columbia, in partial fulfilment of the requirements for the degree of Doctor of Philosophy. Researches in the field were supported by a grant from the National Research Council of Canada to Dr. M. D. F. Udvardy, who also supervised the study in conjunction with Dr. I. McT. Cowan. A generous grant from the Frank M. Chapman Memorial Fund enabled me to do a preliminary study of Brachymmphus.

I am grateful to Magnar Norderhaug and Lowell Spring who kindly provided some of the specimens used in the study of feeding adaptations. Drs. M. D. F. Udvardy, I. McT. Cowan and especially D. Chitty helped greatly in improving the manuscript. Their generosity in helping carries no implicit sanctioning of the views expressed in this article.

SUMMARY Because of its homogeneity, both taxonomical and ecological, the sea-bird family Alcidae

constitutes an appropriate group for the study of adaptive radiation. This radiation involves mainly the acquisition of specialized feeding habits and the consequent specialization of the various species of the family at different trophic levels.

The plankton-feeders, exemplified by the Least Auklet Aethia pusillu, have a relatively wide beak with a fleshy tongue and a broad palate with numerous denticles. The fish-feeders, exemplified by the Razorbill Alca torda, have a narrow bill, a certain degree of tongue cornification and few, but sharp and regularly arranged palatal denticles. A few species, including the pufins and one auklet (Cyclorrhynchus), have characteristics intermediate between these extremes and feed partly on fish and partly on plankton.

Body-size in the predator is related to the size of the prey and these relations are emmined within the family. Within a group with similar adaptations, species which are alone in their niche in their area tend to be of intermediate body size for that group. Finally, though the family may exhibit a series of parallel trends in bill shape when the bill is considered as a social releaser, it exhibits a gradation in shape and structure (adaptive radiation) when considered as a food-getting tool.

REFERENCES BATESON, P. P. G. 1961. Studies of less familiar birds. 112. Little Auk. Br. Birds 54 : 272-276. BBDARD, J. H. 1967. Ecological segregation among plankton-feeding Alcidae (Aethiu and Cyclor-

BELOPOL’SKII, L. 0. 1957. [Ecology of sea colony birds of the Barents Sea] Izv. Akad. Nauk SSSR, (Seen in English translation prepared by the Israel Program for

BENT, A. C. 1921. Life histories of North American diving birds. Order Pygopodes. Bull. U.S.

COVES, E. 1868. DRENT, R. H. 1965. Ardea 53 :

DRENT, R. H. & GUIGUET, C. J. 1961. A catalogue of British Columbia seabirds colonies. Occ.

FAY, F. H. & CADE, T. J. 1959. An ecological analysis of the avifauna of St. Lawrence Island,

GABRIELSON, I. N. & LINCOLN, F. C. 1959. W-ildl. Mgmt. Inst., Washington

GIZENKO, A. I. 1955. [Birds of the Sakhalin Territory] Izv. Akad. Nauk SSSR, Moscow : 1-327. GOODMAN, D. C. & FISHER, H. I. 1962. Functional anatomy of the feeding apparatus in water-

GYSELS, H. & RABAEY, M. 1964. Taxonomic relationships of A k a tor&, Fratercdu arcticn and Ibis 106 : 536-541.

rhynchus).

Moskva-Leningrad. Scientific Translations, Jerusalem, 1961, 346p.)

natn. Mus. 107 : 1-237.

P1i.D. thesis, University of British Columbia.

A monograph of the Alcidae. Proc. Acad. nat. Sci. Philad. 20 : 2-81. Breeding biology of the Pigeon Guillemot, Cepplrrrs columba.

99-160.

Pap. Br. Columb. prov. Mus. 12 : 1-173.

Alaska. Univ. Calif. Publs. 2001. 63 : 73-150.

D.C. Birds of Alaska.

fowl (Aves: Anatidae).

Uriu aalge as revealed by biochemical methods.

Carbondale: Southern Illinois University Press.

198 JEAN B b A R D : ADAPTlVE RADIATION I N ALCIDAE IBIS 111

HOWELL, A. B. 1917. 12 : 1-127.

HUTCHINSON, G. E. 1959.

JOHNSON, R. A. 1935. KARTASCHEW, N. N. 1960. Die Alkenvogel des Nordatlantiks. KO. 257. Wittenberg: Neue

Brehm Bucherei. KISKCHINSKII, A. A. 1965. [On the biology of the Short-billed and Long-billed Murrelets (Bruchy-

rumphus brevirostre and B. mrmorutum)] Novosti Ornitologii, Contributions of the 4th All-Union Ornithological Conference, 1-7 September 1965, Alma-Ata : 169.

KOZLOVA, E. V. 1957. [Charadriiformes, suborder Alcae] Zool. Inst. Akad. Nauk SSSR, Nov. Ser. 65 : Fauna SSSR Ptitsy I1 (3). (Seen in English translation prepared by the Israel Program for Scientific Translations, Jerusalem, 196 1 .)

MACARTHUR, H. H. & LEVINS, R. 1964. Competition, habitat selection and character displacement in a patchy environment.

MURIE, 0. J. 1959. U.S. Department of the Interior, U.S. Fish and Wildlife Service, North American Fauna 61.

MURPHY, R. C. & HARPER, 1:. 1921. Bull. Am. Mus. nat. Hist. 44 : 495-554.

MYRBERGET, S. 1962. Underscakelser over forplantningsbiologien ti1 lunde (Fruterculu arcticu (L.)). Egg, ruging og unger. Papers of the Norwegian State Game Research Institute, No. 11, Series 2.

PALUDAN, K. 1947. Alken. Dens Ynglebiologi og dens Forekomst i Danmark. Kebenhavn: Ejnar Munksgaard.

PAYNE, R. B. 1965. PBTERS, J. L. 1934. Cambridge: Harvard University

Press. PRELILE, E. A. & MC.~TEE, W. L. 1923. Part I.

Birds and mammals. U. S. Department of the Interior, U S . Fish and Wildlife Service, North American Fauna 46 : 1-128.

SALOMONSEN, F. 1951. The Birds of Greenland. Vol. 111. Kebenhavn : Ejnar Munksgaard. SERGEANT, D. E. 1951. Ecological relationships of the guillemots Uriu ualge and Uriu lom’u.

Proc. X. Int. om. Congr. L’ppsala, 1950 : 578-587. STORER, R. W. 1945. The systematic position of the murrelet genus Et,domychuru. Condor 47 :

154-160. STORER, R. W. 1952. A comparison of variation, behavior and evolution in the sea bird genera

Uria and Cepphrts. STORER, R. W. 1960. Evolution in the diving birds. Proc. XI1 Int. orn. Congr. Helsinki, 1958 :

694-707. SWARTZ, L. G. 1966. Sea-cliff birds. Chapter 23 : 611-678. In N. J. Wilitnowsky and J. N.

Wolfe (eds.): Environment of the Cape Thompson region, Alaska. U.S. Atomic Energy Commission, Division of Technical Information.

THOMPSON, M. C., HINES, J. Q. & WILLIAIMSON, F. S. L. 1966. Iliscovery of the downy young of Kittlitz’s Murrelet.

THORESEN, A. C. 1964. TUCK, L. M. 1961. The Murres. Their distribution, populations and biology. Canadian

~ D V A R D Y , M. D. F. 1963. In J. L. Honolulu : Bishop Museum

ZUSI, R. 1967. Proc.

Birds of the islands off the coast of California. Pacif. Cst. Avifauna,

Homage to Santa Rosalia or \?Thy are there so many kinds of animals? Am. Nat. 93 : 145-159.

Additional Dovekie weights. Auk 52 : 309.

Proc. natn. Acad. Sci. U.S.A. 51 : 1,207-1,210. Fauna of the Aleutian Islands and Alaska Peninsula.

-2 review of the diving petrels.

The molt of breeding Cassin Auklets. Check-list of Birds of the World, Vol. 11.

Condor 67 : 220-228.

Biological surtey of the Pribilof Islands, Alaska.

Univ. Calif. Publs. Zool. 52 : 121-222.

Auk 83 : 349-351. The breeding behavior of the Cassin Auklet. Condor 66 : 456476.

Wildlife Series, No. 1 : Ottawa.

Gressit, (ed.) : Pacific Basin Biogeography, a Symposium. Press.

U.S. natn. Mus. 123 : 1-28.

Zoogeographical study of the Pacific Alcidae. p. 85-111.

The role of the depressor mandibulae muscle in kinesis of the avian skull.

Jean Btdard, Department of Zoology, University of British Columbia, Vancouver 8 , B.C., Present address : Dkpartement de Biologie, Facultt des Sciences, Univmsitt

Laval, Qiitbec, Canada. Canada.