THE ADAPTIVE SIGNIFICANCE OF COLONIALITY IN BIRDS

Chapter 1

THE ADAPTIVE SIGNIFICANCE OF COLONIALITY IN BIRDS James F. Wittenberger Department of Zoology and Institute for Environmental Studies University of Washington Seattle, Washington

George L. Hunt, Jr. Department of Ecology and Evolutionary Biology University of California, Irvine Irvine, California

I. II. III. IV.

V.

VI.

VII. VIII.

Introduction Definition and Occurrence Toward a Better Theoretical Perspective Energetic Effects A. Competition for Food B. Geometric Considerations C. Information Transfer and Food Finding D. Net Energetic Effect Prédation Effects A. Attraction of Predators B. Critical Density Effect C. Swamping Effect D. Mobbing Effect E. Vigilance Effect F. Nest or Roost Site Packing G. Net Prédation Effect Egg Destruction and Chick Killing A. Negative Aspects B. Energetic Advantages C. Chick Killing and Relative Fitness D. Preventing Adoptions E. Net Effect Extra-Pair Copulations Other Considerations A. Competition for Space B. Theft of Nest Material C. Kleptoparasitism D. Transmission of Disease and Ectoparasites

2 3 5 6 7 11 15 24 24 24 24 27 28 30 30 32 32 32 33 34 35 36 37 39 39 42 42 43

1 Avian Biology, Vol. VIII Copyright © 1985, by Academic Press, Inc. All rights of reproduction in any form reserved. ISBN 0-12-249408-3

2

JAMES F. WITTENBERGER AND GEORGE L. HUNT, JR. IX.

X.

I.

Toward a Synthesis: Temporal Fitness Patterns A. Optimal Breeding Chronology B. Resource Chronology C. Prédation Chronology D. Chick-Killing Chronology E. Chronology of Cuckoldry F. Choice of Breeding Time G. Models of Temporal Fitness Variations H. Fraser Darling Effect Conclusion References

44 45 45 50 50 52 53 54 56 57 58

Introduction

Colonial nesting and roosting are conspicuous forms of social organization among birds. The occurrence and ecological correlates of coloniality are well documented by Crook (1964, 1965) and Lack (1968). Yet, despite extensive study by both field investigators and theorists, only a poorly integrated body of theory exists for explaining the evolution of coloniality. A wide variety of hypotheses has been advanced to explain avian coloniality, but none has been adequately tested, and little information is available for determining which hypotheses are most likely to apply to any given species. To understand the adaptive pressures modifying coloniality in birds, one must identify the costs and benefits accruing to colony members. Since a colony differs from a dispersed population by the clumping of individuals in time and space, it is important to examine the effects of colony size, spatial packing, and temporal synchrony on the demographically important param­ eters of survival and reproductive success. The impact of coloniality on social organization, as well as the role of social organization in determining colony structure, must also be considered when evaluating the adaptive significance of coloniality. Complicating the analysis of the roles of various factors in the evolution of coloniality is the problem that most, if not all, adaptations to coloniality are simultaneously dependent and independent variables. Each adaptive trait or selective pressure must be analyzed separately, although in nature all in­ teract simultaneously in a complex web of interwoven selective pressures and adaptive responses. Our task then becomes one of trying to tease apart the pieces of the large picture into coherent parts and then to resynthesize these parts into a meaningful whole. A one-factor or single-variable model is simply not a very useful way to understand a phenomenon as complex as avian coloniality.

1. ADAPTIVE SIGNIFICANCE OF COLONIALITY

3

In this chapter we examine advantages and disadvantages potentially ac­ cruing to individuals who join breeding or roosting colonies. We do not try to describe in detail the widespread occurrence or diversity of coloniality as we feel that these aspects have been adequately summarized by Lack (1968). Our discussion will focus on group phenomena related to central place sys­ tems, that is, systems in which one or more individuals move to and from a centrally located place in the course of daily activities. More specifically, we focus on selective factors that have been suggested to explain why indi­ viduals should form colonies rather than dispersing within the available foraging space. We do not consider communal breeding systems (J. L. Brown, 1978; Emlen, 1978) or flocking behavior, except as they provide tests for ideas concerning colonial existence. We also do not consider central place systems involving single individuals or family units (cf. Hamilton and Watt, 1970). Our objective is to evaluate existing hypotheses for explaining the adaptive significance of coloniality and to identify the sorts of evidence still needed to test them. In addition, we present some new hypotheses and perspectives where current thinking seems inadequate for understanding what is known about colonial systems. Our hope is to achieve a more inte­ grated body of knowledge that will enhance our current understanding of avian coloniality and help focus future research on important unanswered questions.

II.

Definition and Occurrence

We define a colony as a place where a number of individuals or pairs nest or regularly roost at a more or less centralized location from which they recurrently depart in search of food. Nests, roost sites, or territories at the centralized colony site occur in a relatively small area, whereas foraging normally occurs outside that area. Field application of this and other defini­ tions of a colony are often difficult because there is a continuum from solitary to semicolonial to colonial nesting or roosting (Coulson and Dixon, 1979). These authors point out that the determination of whether neighboring groups of birds should be regarded as belonging to separate colonies de­ pends on the degree of integration of the groups. Cooperative or mutualistic interactions may or may not occur among colony members, but competitive interactions are always evident (Alexander, 1974; see also Koenig, 1982). Our definition allows a parallel discussion of breeding and roosting sys­ tems, which is desirable because theories developed for one system are applicable to both. Nevertheless, two distinctions between breeding and roosting colonies are theoretically important and deserve emphasis.

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JAMES F. WITTENBERGER AND GEORGE L. HUNT, JR.

One distinction is that breeding pairs are tied to a colony by their nests or young, while roosting individuals are not required to return to the roost. Breeding individuals therefore cannot facultatively join the colony when it is advantageous for them to do so and avoid the colony when it is not. They must remain a part of the colony during an entire breeding cycle. In con­ trast, roosting individuals can make an independent choice each day as to whether they should roost in a colony or solitarily. The extent to which individuals make different choices about roost sites each day is not well documented, but the option at least exists and is occasionally used (Fleming, 1981). This difference in options has important implications with regard to some theories discussed below. A second distinction is that members of breeding colonies must usually make many foraging excursions from the colony each day. In contrast, colonially roosting birds may make only one foraging excursion from the colony per day, and the departure and return of all individuals is usually syn­ chronous. Departures and arrivals from roosts are often accompanied by associated social behaviors whose adaptive significance has been controver­ sial (see Wittenberger, 1981). Departures and arrivals from breeding colo­ nies are generally not associated with group displays. These differences probably reflect different foraging tactics and predator defense tactics in the two kinds of colonies. Because members of colonial roosts may travel from colony site to foraging grounds only once daily, they are less constrained by travel distance than members of breeding colonies. For this reason, and because breeding birds must provision chicks, the energetics of roosting and breeding colonies are quantitatively different. Our definition of coloniality does not include one type of nesting disper­ sion pattern that is sometimes considered colonial, namely the aggregation of type A territories (after Nice, 1943) into localized areas. Such localized breeding populations have been termed "neighborhoods" by Crook (1965) and "loose" colonies by Lack (1968). They probably arise because they allow neighboring individuals to mob predators cooperatively [e.g., Fieldfares (Turdus pihris); see Anderson and Wiklund, 1978] or occasionally to forage away from nesting territories [e.g., Dickcissels (Spiza americana) and Lark Buntings (Calamospiza melanocorys) see Zimmerman, 1966; Pleszczynska, 1978]. Colonial breeding occurs in 61 families or subfamilies of birds (Lack, 1968). It is most common among marine birds; of some 260 species, 98% nest in colonies. In contrast, of 87 passerine families or subfamilies, only 16% are primarily colonial. Within the passerines, birds that feed their young aerial insects (except forest-dwelling species, Fry, 1972) or seeds have the greatest proportion of colonially nesting species (Lack, 1968). Colony size may vary from over one million birds for some seabirds (Hickey and Craighead, 1977)

5

1. ADAPTIVE SIGNIFICANCE OF COLONIALITY

to small groups of a few nests. Within colonies, nests may be densely packed with rims touching, or loosely aggregated over a large area. The vast majority of birds that nest colonially also forage in flocks (Lack, 1968), and most of these species also probably use colonial roosts outside of the breeding season. Likewise, a large number of families that are solitary nesters forage in flocks (Lack, 1968), and some of these probably use colonial roosts. While the use of colonial roosts by large numbers of pelicans, cor­ morants, vultures, quail, herons, shorebirds, gulls, terns, pigeons, swifts, swallows, crows, starlings, blackbirds, and weaver finches is well known, the full array of species using roosts is not documented. Compiling this informa­ tion will be difficult, as it is likely that a number of passerines use in­ conspicuous small roosts for heat conservation, and these can easily go un­ detected or unreported.

III. Toward a Better Theoretical Perspective A common approach to evolutionary questions is to catalog first all of the likely benefits and costs experienced by individuals choosing a particular behavioral option. The benefit with the greatest positive effect is then ac­ cepted as the most likely reason for why a given option has been adopted, or, alternatively, the cost with the greatest negative effect is accepted as the most likely reason for why a given option has not been adopted. One problem with this reasoning is that it implies that a single selective pressure is largely responsible for the evolution of a behavioral trait, an assumption that is probably erroneous. A second problem is that many variables enter the argument as both costs and benefits. For example, in coloniality, energetics enters the argument as a benefit (increased foraging and food-finding efficiency) and as a cost (increased competition for food). Similarly, prédation enters the argument as both a benefit (group defenses against predators) and as a cost (increased conspicousness or attractiveness to predators). A better approach is to consider the net effect of coloniality on each important variable. Coloniality should evolve when N p + Ne + N m +

Ni>0

where N p is the benefit from enhanced defense minus cost of increased attraction of prédation (net effect on vulnerability to prédation), Ne is the benefit from enhanced foraging efficiency minus cost of increased competi­ tion (net energetic effect), Nm is the benefit of increased access to mates minus cost of increased competition for mates (net effect on mating oppor-

6

JAMES F. WITTENBERGER AND GEORGE L. HUNT, JR.

tunities), and Ni is the net effect of increased opportunities to exploit or disrupt neighbors (e.g., steal nest materials, kill chicks) and increased de­ grees of interference perpetrated by neighbors. In this equation it should be clear that several factors may simultaneously be enhanced by colonial behav­ ior and that it is not necessary to assume that a single factor is responsible for coloniality. This approach also allows easier assessment of fitness effects for the pertinent variables because net effects can be estimated from overall prédation rates, food intake rates, etc., without any need for separating those rates into positive and negative components. It eliminates the inevita­ ble confusion that arises when each factor is treated simultaneously as both a benefit and a cost of coloniality. For these reasons the ensuing discussion focuses on the net effect that coloniality has on prédation pressure, food intake rate, mate acquisition, and conspecific interference. We do not specifically examine the situation in which colony formation is due to habitat shortages (see Section IX, A). Although clumping of suitable nest sites may result in the formation of colonies (seabirds, Lack, 1967; herons, Lack, 1968; blackbirds, Orians, 1961a; swallows, Snapp, 1976; sa­ vannah weaverbirds, Crook, 1960, 1962, 1964), in many instances nests or roost sites are more clumped than they are required to be by the available habitat. Neighboring habitat islands remain unused while one becomes crowded, or only a small portion of an island will be occupied by a very dense colony. In at least some land birds use of inaccessible sites does not seem responsible for coloniality (Lack, 1968). For instance, swallows and swifts could often disperse their nests over cliff faces, bluffs, or other sub­ strates instead of nesting colonially. Thus, an analysis of coloniality must include a consideration of why nests or roosts occur at higher densities than habitat clumping dictates.

IV.

Energetic Effects

In this section we consider aspects of coloniality that may affect the avail­ ability of food to colony members. These effects include both positive and negative interactions. The assemblage in one place of numerous individuals with similar food requirements increases the potential for competitive in­ teractions, which could result directly or indirectly in decreased food intake rates or in an increased cost of foraging per unit of food intake for colony members. On the other hand, membership in a colony has been hypoth­ esized to increase foraging efficiency by either of two mechanisms. A geo­ metrical model predicts that the average distance individuals must travel to find food is reduced by nesting colonially in the center of the region where

1. ADAPTIVE SIGNIFICANCE OF COLONIALITY

7

foraging occurs (i.e., the foraging arena). The information center model hypothesizes that individuals learn the location of food resources from other colony members and that this exchange of information, in the long run, results in an overall increase in foraging success for all colony members. To determine the net energetic effect of coloniality, the degree of competition experienced by colony members and the two proposed energetic benefits of coloniality must be evaluated. A.

COMPETITION FOR FOOD

The concentration of organisms with similar food habits in a small area can lead to increased competition for food among those organisms relative to that experienced by a lower concentration of organisms in the same area. If competition is to occur, however, either the prey or the space needed for foraging must be in short supply. The competition may be direct, caused by depression of food resources, or it may be indirect, due to disruption of foraging activities by the presence of other colony members. In either case the cost per unit of food obtained increases. Organisms therefore get less food or have to increase their foraging effort to maintain a given rate of food acquisition. Alternatively, one might argue that colony size is adjusted so that resource availability is similar for individuals in colonies of different sizes and for solitary individuals. Fretwell and Lucas (1969) have suggested that organ­ isms choose habitats in such a way that local population density is adjusted to local habitat quality. If resource availability is the only consideration, the degree of competition faced by colonial and noncolonial members of a popu­ lation should be similar (i.e., the ideal free distribution). Under such circum­ stances one would not expect to see greater competition in colonies than elsewhere, except during brief, unexpected failures in the resource base. With unexpected resource failure, one would expect to find intense competi­ tion accompanied by mass emigration, reproductive failure, or mortality. When all members of a population occur within colonies, the two alter­ natives can be evaluated only by considering colonies of different size. To refute the hypothesis that competition is similar for all colony sizes, one must show that food intake rate per unit of effort or time varies with colony size. Even if competition does not vary with colony size, it could still be a cost of coloniality if other factors (habitat restrictions or antipredator bene­ fits) have led to coloniality. To evaluate this possibility, data are needed on the degree of resource depression experienced around colonies, along with comparative data on clutch sizes, chick growth rates, parental food delivery rates, and chick starvation rates among colonial and noncolonial individuals of the same or similar species. Lack (1968) cited a number of species in which

8

JAMES F. WI1TENBERGER AND GEORGE L. HUNT, JR.

some populations are colonial and others are solitary nesters; several of these species would be suitable for study of the costs of coloniality. Direct measures of food resource depression as a function of colony size are not available. This is a critical gap in our knowledge of the costs of coloniality. Several sorts of indirect evidence, however, may be used to test for variation in competition intensity as a function of colony size, including comparative evidence on egg and chick neglect, clutch sizes, duration of foraging trips, chick growth rates, and chick starvation rates. Some evidence of this sort is now available for evaluating the relationship between colony size and intensity of competition. Coulson et al. (1982) compared the size (weight and wing chord) and egg measurements of Herring Gulls (Larus argentatus) in a colony before and after it was reduced to 25 percent of its former numbers. Wing chord and weights of gulls increased, as did egg size, for gulls breeding for the first time after the colony was reduced in size. Coulson et al. concluded that these increases reflected a reduction of competition for food among colony mem­ bers. In the Pribilof Islands Thick-billed Murres (Una lomvia) have lower chick growth rates and lower fledging weights on St. George Island, where the breeding population numbers 1.5 million individuals, than on St. Paul Island, where the breeding population numbers about 150,000 (Hunt et al., 1981b). Interestingly, fledging success is similar on both islands. Although no estimates of food availability or resource depression are available, the density of foraging murres is greater near St. George Island than near St. Paul Island. Since colony size on these two islands is apparently determined by nest site availability, the data suggest that competition has depressed food availability near the larger colony (Hunt et al., manuscript). Gaston et al. (1983) also found a correlation between colony size and depression of fledg­ ing weights in Thick-billed Murres. Similarly, Nettleship (1972) found lower fledging weights in a large colony of Atlantic Puffins (Fratercula arctica) than in a small one, as did A. J. Gaston (personal communication). Hoogland and Sherman (1976) found that weights of 10-day-old Bank Swallows (Riparia rvparxd) are inversely related to colony size. These results suggest that com­ petition is more intense around larger colonies of these species. The avail­ able data therefore indicate that colony sizes are not adjusted such that competition for food is maintained at a similar level among neighboring colony sites of a given species, contrary to the predictions of the Fretwell and Lucas (1969) model. More extensive evidence is available for evaluating the relative intensity of food competition experienced by colonial and noncolonial populations of birds. One-egg clutches are unusual among birds and are found mainly in colonial species (Lack, 1968). Most seabirds lay one egg per breeding cycle (Lack, 1968), and some that lay two eggs frequently fail to raise both chicks

1. ADAPTIVE SIGNIFICANCE OF COLONIALITY

9

(Nelson, 1970, 1978). Among boobies, only the Blue-footed (Sula nebouxii) and Peruvian (S. variegata) lay three- and four-egg clutches, and both spe­ cies nest on islands near productive ocean upwellings. In contrast, most boobies with one- or two-egg clutches nest on islands in comparatively un­ productive tropical oceans (Nelson, 1978). Gannets are an exception. They lay single-egg clutches and nest near productive waters at high latitudes (Nelson, 1978). Experimental additions of eggs or chicks to nests of various seabirds have demonstrated that some individual parents can raise the extra chicks suc­ cessfully (Vermeer, 1963; Nelson, 1964; Harris, 1970; Corkhill, 1973; Perrins et al, 1973; J. G. Ward, 1973), while others are unable to raise more than a single chick (Rice and Kenyon, 1962; Harris, 1966; Nettleship, 1972). The ability to raise extra chicks is puzzling in view of the results of experi­ mental studies involving either supplementary feeding of chicks or broods with only one parent that point to strong competition for food in the vicinity of major seabird colonies (Nettleship, 1972; Harris, 1978). One must take the long view, however, and consider that raising more chicks, even though feasible, may have detrimental effects on adult survival, since selection max­ imizes lifetime reproductive output, not annual output (see Charnov and Krebs, 1974). Black-legged Kittiwakes (Rissa tridactyla) show variations in clutch size between age classes, between colonies, and possibly within colo­ nies over time (Beloporskii, 1957; Coulson, 1966; Hunt et al., 1981b). In the Pribilof Islands, average clutch size of Black-legged Kittiwakes appears to have decreased after colony size increased (Hunt et al, 1981b). The evi­ dence suggests that clutch size is probably tied both to the foraging ability of particular individuals and to the overall intensity of competition around colony sites. If periods of food shortage due to competition are more frequent in coloni­ al than in noncolonial species, then one would expect in colonial species a greater frequency of adaptations to cope with food shortages, such as tempo­ rary chick or egg desertion (egg neglect) and the ability of chicks to survive with slow growth rates. Physiological adaptations to permit egg neglect and slow growth of chicks are commonplace in marine and freshwater colonial birds (Ashmole, 1963; Stonehouse, 1962; Nelson, 1967a,c, 1970, 1975, 1978; Boersma and Wheelwright, 1979; Knopf, 1979; Murray et al, 1979; J. Bur­ ger, 1980b; Vleck and Kenagy, 1980; Prince and Ricketts, 1981). Swifts (Lack, 1956) also have eggs or chicks able to withstand periods of neglect when food is temporarily unavailable due to inclement weather. In many of the colonial species practicing egg or chick neglect, however, foraging suc­ cess is depressed by storms (Kazama, 1968; Salt and Willard, 1971; Dunn, 1973; Birkhead, 1976) or by movements of prey unrelated to competition. Present evidence is insufficient to show that egg and chick neglect are more

10

JAMES F. WITTENBERGER AND GEORGE L. HUNT, JR.

common in colonial than noncolonial species or that their occurrence is due to increased competition for food around colonies. Long foraging flights and long periods spent away from a colony while seeking food probably indicate that food is insufficient nearer to the colony (Gaston and Nettleship, 1981). Distant foraging areas should not be ex­ ploited unless food is scarce nearer to the colony, because long flights are energetically expensive and because long absences from the colony entail greater risk of chick loss. Moreover, longer flight distances reduce the rate at which chicks can be fed and hence the number of chicks that can be reared to fledging or increase the length of time needed to rear them. Birds in large breeding and roosting colonies often fly long distances to forage (Rice and Kenyon, 1962; Harris, 1966; Lack, 1968; Ashmole, 1971; Diamond, 1978; Nelson, 1978), and Fry (1972) has found a positive correla­ tion between coloniality and foraging range in bee-eaters. Passenger Pigeons (Ectopistes migratorius) commonly foraged 50 miles from breeding colonies (Schorger, 1955), some blackbirds and starlings forage up to 50 miles from winter roosts (Hamilton and Gilbert, 1969), and many colonial seabirds for­ age hundreds of miles offshore (Lack, 1968; Dünnet and Ollason, 1982). In tropical seabirds, offshore foragers that range over vast expanses of open ocean breed in larger colonies than inshore foragers that feed in restricted areas of shallow coastal waters (Diamond, 1978). Diamond hypothesizes that this correlation reflects long term limitations of colony size among species that are typically faced with more intense competition for food near colony sites. Alternatively, colony size could reflect a tendency for offshore foragers to congregate in relatively fewer centralized colonies (Erwin, 1977). Lack (1968) and Cody (1973) argue that the additional cost of selecting a safe nesting site is relatively little for offshore foraging seabirds and hence they should nest in large colonies at the safest possible sites. In contrast, inshore foraging species should benefit proportionately more from the energy sav­ ings obtained by accepting somewhat less safe sites closer to foraging areas. Widespread starvation is sometimes a cause of colony abandonment. Orians (1960) noted abandonment of nesting by Tricolored Blackbirds (Agefoius tricolor), presumably due to shortage of food, and Payne (1969) suggested that the abandonment of 7 of 14 colonies of Tricolored Blackbirds was the result of food shortages. Similarly, mass abandonment of breeding colonies is associated with food shortages in Peruvian Boobies (Nelson, 1964; Duffy, 1980), white pelicans (Pelecanus erythrorhynchos and P. onocrotalus) (L. H. Brown and Urban, 1969; Johnson and Sloan, 1978), and Red-billed Queleas (Quelea quelea) (Jones and Ward, 1979). In each of these cases, however, evidence was lacking to show that the number of birds present was responsi­ ble for depressing food availability below the level critical for successful nesting. Among winter roosting colonies of passerines, abandonment of small

1. ADAPTIVE SIGNIFICANCE OF COLONIALITY

11

roosts midway through winter is common, and members of such roosts move to nearby larger roosts (Neff and Meanley, 1957; Wynne-Edwards, 1962; Hamilton and Gilbert, 1969; Ward and Zahavi, 1973). Small roosts are be­ lieved to be associated with local patches of food, and abandonment probably occurs when those food patches are exhausted. Dietary specialization or foraging habitat specialization may indicate re­ source partitioning and past and/or chronic competition for food around multispecies colonies. Colonial seabirds in large colonies sometimes con­ sume a substantial proportion of the available food near the colony (Wiens and Scott, 1975; Furness, 1978a). They appear to partition resources by using different foraging zones (Ashmole, 1968; Pearson, 1968; Cody, 1973; but see Bédard, 1976), concentrating on different prey types (Bourne, 1955; Belopol'skii, 1957, Nelson, 1978; Ashmole and Ashmole, 1967; Ashmole, 1968; Pearson, 1968; Jenni, 1969; Bédard, 1969a; Schreiber and Ashmole, 1970; Hunt et al., 1981c), or taking prey of different sizes (Bourne, 1955; Ashmole, 1968; Bédard, 1969a; Hunt et al., 1981a). Specialization on prey type or foraging location by species in multispecies colonies could be evi­ dence for past competition between colony members, but, as with noncolonial species, proving that prey specialization has evolved as a form of resource partitioning in response to competition depends on a largely un­ knowable evolutionary past. If resource partitioning is to be used as evi­ dence of heightened competition in colonies, then one must show greater resource specialization among species in multispecies colonies than can be found in guilds of sympatric noncolonial species. While the above evidence generally suggests that greater food depletion and heightened competition for food exist around colony sites, few studies conclusively demonstrate that foraging efficiency of colony members varies with colony size or that resource availability around colony sites is adversely affected by the foraging activities of colony members. Without measure­ ments of food availability and direct evidence regarding the impact of colony members on prey populations, we cannot eliminate the possibility that many of the phenomena currently attributed to competition for resources are in reality due to social interactions caused by crowding or to differences in food distribution around colony sites. Nevertheless, it is likely that coloniality entails an energetic cost, although the magnitude of that cost cannot be estimated without some basis for comparison among colonial and noncolonial species with similar food distributions and foraging habits.

B.

GEOMETRIC CONSIDERATIONS

One potential advantage of coloniality is that individuals might minimize average distance of foraging flights by breeding or roosting in a central

12

JAMES F. WITTENBERGER AND GEORGE L. HUNT, JR. STABLE FOOD DISTRIBUTION Nests spaced Nests in one place

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VARIABLE FOOD DISTRIBUTION Nests spaced Nests in one place

o o o o o o o o

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o o o o o orf = 2.94 o o

o o o o A o o 3.86o o

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FIG. 1. The geometrical model for avian coloniality. Solid circles represent continuously available food sources. Open circles represent spatiotemporally variable food sources, each of which must be exploited to an equal extent during the course of a breeding season. Small triangles represent single nests. Large triangles represent colonies of four nests. Mean travel distance for food (d) is lowest for dispersed nesters if food is uniformly distributed and continu­ ously available (top), but it is lowest for central place (colonial) nesters if food is spatiotemporally variable (bottom). (After Horn, 1968, reproduced with permission of the author and The Eco­ logical Society of America, copyright 1968, The Ecological Society of America.)

location. Horn (1968) showed by means of a simple geometrical model that if food availability varies both spatially and temporally, average flight distances are shorter for individuals nesting colonially in the center of a food distribu­ tion rather than uniformly dispersed across the food distribution (Fig. 1). Although this hypothesis is often cited as one factor favoring coloniality, it has not been adequately tested. The model proposed by Horn depends on three assumptions. It assumes first that the colony is centrally located in the foraging area; second, that each individual must forage with equal frequency at every point in the foraging arena during the course of the breeding or roosting season; and third, that food resource availability is unpredictable in space and time. None of these assumptions is completely valid for real systems, and yet the effect that violation of each assumption has on the geometric advantage of coloniality for foraging has not been properly investigated. No data are currently available regarding the first assumption of central colony location. Acentric colony locations are certainly frequent in nature

1. ADAPTIVE SIGNIFICANCE OF COLONIALITY

13

(e.g., seabird colonies on the coast) but no careful measurements have been made regarding degrees of acentricity. Two sorts of information would clarify this question. First, theoretical analyses could explore the extent to which a colony could be acentric before the energetic advantages of central place foraging are lost. Mathematical analysis of circular, linear, and elliptic re­ gions indicates that a colony can be displaced as much as 60-70% from the center of its foraging region to the periphery before the energetic advantage proposed by Horn is lost for average individuals (Wittenberger and Dollinger, 1984). An important consideration that arises when a colony is acentrically located is that an impetus arises for some individuals to leave the colony and move to more centrally located areas. Second, field measure­ ments of colony locations with respect to foraging locations could provide an empirical basis for evaluating the reality of any energetic advantage that might accrue from central place foraging given acentric colony locations. In such studies, actual mean flight distances from an acentric colony site could be compared to calculated expected flight distances if nests or roosts were evenly dispersed over the same foraging arena. The analyses presented by Wittenberger and Dollinger (1984) provide a basis for making such calcula­ tions. The second assumption implies that all colony members must use the entire foraging area surrounding the colony in order to obtain food. Hence, the foraging area must be relatively small, and it must have an edge or boundary beyond which food is unavailable (Wittenberger, 1981). If the foraging area is large or unbounded, it can be partitioned among several smaller colonies or among noncolonial pairs (Fig. 2). Such partitioning would allow shorter travel distances for individuals than would be possible in a single large colony in the center of the food distribution. Thus, the model is not likely to apply to large colonies or to colonies that are not associated with isolated food patches. The third assumption implies that each foraging location is equivalent to all other foraging locations in its probability of yielding food, when averaged over the entire season, even though different locations are best at any given time. Deviations from this idealized distribution affect the "center of mass" of the food distribution and hence the best location for the colony (Fig. 3). Such deviations must be taken into account when evaluating how acentricity of colony sites affects foraging efficiency. To test the geometrical model, one must evaluate these assumptions and the model's predictions: (1) Food resources must be spatially and temporally variable while the colony is occupied. Evidence in support of this assump­ tion does not provide support for the geometrical model, since the same assumption is also made for other models (see the information center hy­ pothesis, Section IV, C) but evidence against this assumption would invali-

14

JAMES F. WITTENBERGER AND GEORGE L. HUNT, JR.

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FIG. 2. The geometrical advantage of coloniality is lost if the food distribution is un­ bounded. Each pair can nest in the center of its own foraging arena, which overlaps the foraging arenas of neighboring pairs, while still remaining dispersed. Symbols are defined as in Fig. 1. Boxes outlined by solid lines enclose foraging spaces equivalent to that shown in the bottom of Fig. 1. Boxes outlined by dashed lines enclose foraging spaces of single pairs. The shaded area shows a portion of the entire food distribution that is exploited by four neighboring pairs. With more nests added to the diagram, most of the region would be exploited to the same degree, as in Horn's (1968) original model. (After M. P. Rowe, personal communication. Reproduced from Wittenberger, 1981, with permission.)

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O

One possible deviation from the idealized distribution

FIG. 3. The effect on optimal colony location of an asymmetrical food distribution. Symbols are defined as in Fig. 1. If all food sources (open circles) are equally suitable (left), the optimal colony location is in the geographic center (X) of the food distribution. If food resources are most abundant in one part of the foraging arena (right), the optimal colony location shifts with the center of mass (Δ) of the food distribution. Size of the open circles indicates relative food availability at each foraging location.

1. ADAPTIVE SIGNIFICANCE OF COLONIALITY

15

date the model. (2) Every colony member should forage throughout the entire foraging arena exploited by the colony and not concentrate on foraging at preferred locations or territories. (3) Colony locations should be near the "center of mass" of the food distribution. (4) Most importantly, mean flight distances should be shorter for colony members than those calculated for members of a hypothetical population of equal size that is dispersed over the same food distribution. The best evidence supporting the geometrical model comes from Horn's (1968) study of Brewer's Blackbirds (Euphagus cyanocephalus). At Horn's study site this species forages primarily on young adult odonates, which emerge at night or in the morning along lake or pond shorelines and disperse into surrounding uplands during the afternoon (Orians, 1980). The result is a bounded foraging arena with spatiotemporal variability in the locations of the best foraging sites. Colony members do fly in different directions from the colony at different times of day, but the extent to which every colony mem­ ber does so was not reported. Some colonies are situated near shorelines and hence are roughly central in location, but others are not. Present evidence for Brewer's Blackbirds therefore supports assumption (1), perhaps (2), and perhaps (3). The critical prediction (4) has not been tested. A number of colonial species have foraging territories or regular foraging sites. Colonial bee-eaters maintain feeding territories away from the colony (Hegner, 1982), and some gulls and terns regularly defend feeding territo­ ries (Drury and Smith, 1968; I. C. T. Nisbet, in Hunt 1980) or use regular or preferred foraging locations repeatedly (I. C. T. Nisbet, in Hunt 1980; Davis, 1975; also alcids: Bédard, 1969a, 1976; Hunt et al, 1979, 1981c). Likewise, colonial caciques may have regularly preferred foraging areas and thus may use only a small, acentric portion of the potential foraging arena (Feekes, 1981). Such patterns clearly violate assumption (2) above. Thus, while the geometric model remains viable, a number of the required as­ sumptions are either violated or untested, as is its prediction of reduced foraging effort. C.

INFORMATION TRANSFER AND F O O D FINDING

Birds need information concerning the location and abundance of food, and under certain circumstances they can obtain this information from indi­ viduals of the same or other species. The "information center hypothesis" (P. Ward, 1965a; Ward and Zahavi, 1973) states that unsuccessful foragers use nesting colonies and roosts as centers at which information about the location of food is obtained from successful foragers. There is no suggestion that successful foragers deliberately inform others, and it has been predicted that they should be as inconspicuous as possible (Bertram, 1978). However,

16

JAMES F. WITTENBERGER AND GEORGE L. HUNT, JR.

several mechanisms have been proposed whereby information can be ob­ tained by previously unsuccessful foragers without the direct help of pre­ viously successful individuals. At least three forms of information transfer may enhance foraging efficien­ cy around colony sites. Birds may learn the types and microhabitat locations of food in a given place by observing other individuals within small foraging flocks (Turner, 1965; Krebs et al., 1972; Krebs, 1973). They may locate food clumps by opportunistically converging on places where the presence or behavior of others indicates a food patch. Finally, they may follow others from colony sites to find good foraging locations (the information center hypothesis). Only the final method depends on colonial nesting or roosting, but evidence for the first two methods has sometimes been used to evaluate the reality of the third method. Observational learning within foraging flocks has been demonstrated ex­ perimentally for Chaffinches {Fringilla coelebs), House Sparrows {Passer domesticus), Great Tits {Parus major), Black-capped Chickadees {Parus atricapillus) and Red-winged Blackbirds {Agelaius phoeniceus) (Turner, 1965; Alcock, 1969; Krebs et al, 1972; Krebs, 1973; Mason and Reidinger, 1981, 1982). None of these species except the Red-winged Blackbird is typically colonial, although House Sparrows regularly and Chaffinches occa­ sionally flock at roosts. The experimental results are corroborated by com­ parative analyses of seed-eating finch flocks in Costa Rica (Rubenstein et al., 1977) and by observations of imitative foraging tactics within Wood Pigeon {Columba palumbus) flocks and mixed-species flocks of insectivorous birds (Murton, 1971; Greig-Smith, 1978; Morse, 1978). Flock-foraging probably enhances foraging efficiency whenever food resources are patchy and search time is important. Birds may also find local food patches by opportunistically joining flocks of foraging or feeding individuals. This local enhancement (Thorpe, 1956; Hinde, 1961) is prevalent in herons and ibises, which feed in aggregations at local food concentrations (Siegfried, 1971; Krebs, 1974, 1978; Kushlan, 1976, 1977; Custer and Osborn, 1978; Pratt, 1980; Caldwell, 1981). Local enhance­ ment probably occurs among other colonial species that forage in flocks (e.g., see P. Ward, 1965a; Zahavi, 1971a; Newton, 1973; Walsberg, 1977). A special form of local enhancement involves a sparse network of indi­ viduals within visual contact, all of whom are searching independently for food. When a food source is discovered, the finder drops quickly to begin feeding. Others, seeing the rapid descent, congregate at the location to compete for the food. As soon as the food is gone, the assembled individuals disperse to resume their independent searching. A convenient term for this form of local enhancement is "network foraging." Network foraging occurs in many seabirds (J. Fisher, 1954; Ashmole and Ashmole, 1967; Murphy and

1. ADAPTIVE SIGNIFICANCE OF COLONIALITY

17

Shomura, 1972; Scott, 1973; Sealy, 1973; Gould, 1974; Baltz and Morejohn, 1977; Erwin, 1978; Baird and Moe, 1978; Wiens et al, 1978; Hoffman et al, 1981; Gochfeld and Burger, 1982), vultures (Koford, 1953; Petrides, 1959; Attwell, 1963; Kruuk, 1967), and corvids (Loman and Tamm, 1980). Howev­ er, the information transfer obtainable from network foraging is not en­ hanced by coloniality unless local population density would otherwise be too low. The amount of information transfer derived from network foraging depends only on the density of searchers being sufficient for frequent visual contacts, not on the spatial dispersion of the search population during nonsearching periods. In fact, the most efficient distribution of searchers would be uniform dispersion, and coloniality tends to reduce uniformity of search intensity because more distant areas are more costly to reach (see Hamilton and Watt 1970). Although some authors have identified "food finding calls" (Frings et al, 1955), which are said to attract others to superabundant food resources, network foraging is probably best viewed as a competitive in­ teraction in which the activity of the finder, in attempting to take quick advantage of newly located food patches, attracts the attention of others. Ward and Zahavi (1973) argue that species that benefit from local enhance­ ment should also be able to benefit by following others from a central colony site, and in support of their argument they cite the general correlation between flock feeding and colonial breeding or roosting (see Crook, 1964, 1965; Lack, 1968). They point out, however, that flock foraging is not neces­ sary for colonies to act as information centers, and colony social organization is not necessary for flock foraging or local enhancement. The correlation between coloniality and flock foraging probably reflects an association of patchy food resources with both, but it does not imply that coloniality evolved to facilitate flock foraging or information transfer by other means. The only form of information transfer that might favor coloniality arises when previously unsuccessful foragers follow successful foragers from colony sites (J. Fisher, 1954; P. Ward, 1965a; Zahavi, 1971b; Ward and Zahavi, 1973; Emlen and Demong, 1975; Evans, 1982; Bayer, 1982; Waltz, 1982). P. Ward (1972a) uses a similar argument to explain the massed drinking flights of sandgrouse, a noncolonial flock-foraging group of birds. For coloniality to be an adaptation to aid information transfer, the following assumptions must hold. First, food resources must be patchily distributed and ephemeral, or the information obtainable by following other colony members would have little value. At the same time, the duration of the food patch must not be too short, or there will be insufficient time available for newly informed birds to locate the patch (Bayer, 1982). Second, colony members must be able to distinguish between successful and unsuccessful foragers. Such discrimina­ tions must be possible on a short-term basis, as information regarding good foraging locations is only useful when it pertains to current food sources. In

18

JAMES F. WITTENBERGER AND GEORGE L. HUNT, JR.

the present context "successful" and "unsuccessful" therefore refers only to the success achieved on the immediately preceding foraging trip. Third, some constraint must prevent foragers from remaining away from colonies after successful excursions. Otherwise, individuals should visit colonies only when they require information about new food sources, and that would leave colonies devoid of successful foragers who would be worth following. Fourth successful foragers must be prone to return to the same foraging locations on subsequent trips. Fifth, unsuccessful foragers must be prone to follow suc­ cessful foragers on their next foraging excursion. Sixth, unsuccessful foragers who follow others should be more successful on their next trip than unsuc­ cessful foragers who do not follow others. There is little direct evidence to support the information center hypoth­ esis for any species. The following discussion reviews what is currently known. Considerable evidence suggests that some colonial species exploit spatiotemporally variable food resources. Aerial insect abundance is patchy, and locations of the best food sources are likely to vary on a short-term basis (see Section IV, B). Spatial clumping of aerial insects certainly occurs and is asso­ ciated with localized emergences of aquatic insects (Lewis and Taylor, 1964), the lee sides of windbreaks (Lewis, 1965), and localized convection currents (Freeman, 1945; Voipio, 1970). Aerial insect abundance also fluctuates sub­ stantially in response to local weather conditions (Glick, 1939, 1957; L. R. Taylor, 1963; Johnson, 1969; Bryant, 1975), and such fluctuations may gen­ erate spatiotemporal variability of foraging locations. Flights of aerial insects follow a diel rhythm, and different taxa fly at different times of day (Lewis and Taylor, 1964). To the extent that these taxa are patchily distributed, locations of greatest insect abundance are likely to change through the course of each day as well as through the season. Consumption of fruit is commonly associated with coloniality (Lack, 1968). Some fruit resources are spatiotemporally variable, but some are not (Leek, 1972; Klein and Klein, 1975; Walsberg, 1977; Feekes, 1981), and at least one colonial, frugivorous species, the Phainopepla (Phainopepla nitens), exploits an evenly distributed resource (Walsberg, 1977). Newly emerged adult odonates, exploited by marsh-breeding blackbirds, are also spatiotemporally variable, as discussed earlier (Horn, 1968, Orians, 1980). Fish schools, frogs, crayfish and other aquatic prey exploited by herons tend to be patchy and ephemeral, es­ pecially in tidal estuaries (Krebs, 1974, 1978; Custer and Osborn, 1978; Pratt, 1980), but direct measurements of food distribution are lacking. Seabrids depend on local food concentrations to forage efficiently (e.g., see Zelickman and Golovkin, 1972; R. G. B. Brown, 1976), and foods taken may vary greatly over fairly short periods (Hunt and Hunt, 1976b). Several mechanisms concentrate food, and their nature suggests that locations of

1. ADAPTIVE SIGNIFICANCE OF COLONIALITY

19

food do change. The most common mechanisms involve surface shoaling of invertebrates or fish, usually in diurnal rhythms, which may be caused by predatory fish or various océanographie phenomena such as convergence fronts, divergence fronts or upwellings, tidal eddies, and glacier faces (Mar­ tin and Myres, 1969; Sealy, 1973; Hamner and Hauri, 1977; Baltz and Morejohn, 1977; R. G. B. Brown, 1980). While many of these concentrating mechanisms lead to relatively stable foraging locations in a broad sense, exact locations change (e.g., due to movements of shoals or tidally driven fronts). High-arctic seabirds must often forage along cracks in pack ice, the locations of which change with the shifting movements of ice floes and the ice pack (R. G. B. Brown, 1980; Gaston and Nettleship, 1981). Some colonial birds exploit spatially clumped, but not ephemeral or tem­ porally variable, food resources. These include the Pinyon Jay (Gymnorhinus cyanocephalus) (Balda and Bateman, 1972), crossbills (Loxia), which breed near local concentrations of spruce cones, (Newton, 1970), and previously the Passenger Pigeon, which exploited local concentrations of beech mast (Schorger, 1955). Many finches and weavers breed or roost colonially near what are described as large concentrations of seeds (Crook, 1965; P. Ward, 1965a,b; Newton, 1973), but the distribution of these seed resources has never been adequately assessed for a region as a whole. There­ fore, colonial granivores may or may not benefit from information transfer at central sites, although coloniality may well allow for local enhancement within foraging flocks (see Turner, 1965; P. Ward, 1965a). Jackdaws (Corvus monedula) exploit clumped resources in winter but utilize evenly distributed resources while breeding (Röell, 1978). Yet they are colonial during both seasons. Röell concluded on the basis of food distribution that Jackdaws could rarely benefit from information transfer at colonies in either season. Few data exist on the ability of individuals to distinguish between suc­ cessful and unsuccessful foragers. Two sorts of cues are available. One set of cues includes all indications that a particular individual is in general a successful forager, but they would be very difficult for a bird to use. Possible indicators include general health, body weight, rate of chick development, number of chicks surviving to a given age, intensity of chick begging calls, and health of surviving chicks. Such cues would point to individuals who are, on average, able to find good foraging sites, but they would not serve to identify individuals who had just returned from a good foraging location on their most recent trip. They do provide information about who would be worth following, however, which may be better than no information at all. The second set of cues pertains to the success of immediately preceding foraging trips. Such cues may include food in the bill, full gullets, the length of time spent regurgitating food to chicks (which is probably an unreliable

20

JAMES F. WITTENBERGER AND GEORGE L. HUNT, JR.

cue), and the amount of time spent away from the colony. Such cues would be tricky for a bird to assess, however, because foraging success depends on rate of food intake and not just the total quantity of food obtained on a trip. A full gullet may therefore be a poor cue in that the bird may have spent an inordinately long time obtaining the food. Likewise, length of time spent away from the colony would be a poor indicator of success if part of that time was spent on nonforaging activities. Additionally, loss of food to a kleptoparasite would confound these cues (Bayer, 1982). Assessments of foraging success therefore require both kinds of cues in order to be reliable. D. N. Nettleship (personal communication) has observed marked increases in the activity and attentiveness of Thick-billed Murres in the high arctic when a bird arrives at its nest with a fish, and such individuals are sometimes followed by others from the cliff on their next foraging excursion. Gaston and Nettleship (1981) argue that information transfer of this sort is important for finding ephemeral food sources around pack ice. In some species, individuals follow others from colony sites. This occurs, for example, in Brewer's Blackbirds, Bank Swallows, and Phainopeplas (Horn, 1968, Emlen and Demong, 1975; Walsberg, 1977). In many other species individuals often depart in flocks (e.g., herons, oilbirds, gulls, murres), in synchronous waves (e.g., most or all colonial roosting pas­ serines), or in continuous streams (e.g., Tricolored Blackbirds, offshore for­ aging seabirds) (D. W. Snow, 1961, 1962; Orians, 1961a; Wynne-Edwards, 1962; Krebs, 1974, 1978; Ashcroft, 1976; Birkhead, 1976; Custer and Osborn, 1978; Ward and Zahavi, 1973; Gaston and Nettleship, 1981), although Bayer (1981) states that Great Blue Herons (Ardea herodias) usually do not leave colonies in flocks. In the case of Thick-billed Murres, outbound flocks frequently change directions and work back along flight lines of individuals who are returning to the colony with food (Gaston and Nettleship, 1981). No evidence is available to show whether individuals who do the following in these populations were unsuccessful foragers. Also, no evidence is available to show that individuals who follow others forage more successfully than individuals who do not. Indeed, little evidence is available to show that following even occurs in species that depart as flocks or waves, except in the sense that group cohesion is maintained for some distance after departing the colony (for further discussion see Ward and Zahavi, 1973; Custer and Osborn, 1978; Krebs, 1978; Wittenberger, 1981). Frugivorous colonial ca­ ciques apparently do not attempt to follow one another to food trees, and Feekes (1981) concluded that colonies of these birds do not serve as informa­ tion centers. Bayer (1982) concluded that evidence based only on flock de­ partures and apparent following cannot be used for testing the information center hypothesis unless there is direct evidence that information exchange occurred and that this enhanced food finding by followers.

1. ADAPTIVE SIGNIFICANCE OF COLONIALITY

21

The hypothesis that naive individuals gain information about the location of resources from knowledgeable or successful individuals was tested experi­ mentally by De Groot (1980) using captive, wild-caught Red-billed Queleas, a weaverfinch believed to depend upon information transfer between suc­ cessful and unsuccessful foragers at communal roosts (Ward and Zahavi, 1973). De Groot found that the naive birds had improved success in locating resources when in the presence of knowledgeable birds. He also found that the naive birds made better use of the more profitable of two food resources when in the presence of knowledgeable birds. Naive birds tended to follow experienced birds, but also naive birds occasionally preceded knowledge­ able birds into food chambers, suggesting that other cues were also used. These data support the hypothesis of local enhancement but provide little direct support for the information center hypothesis. Anderson et al. (1981) evaluated the hypothesis that successful foragers are followed from colony sites by observing 50 parent Black-headed Gulls that were foraging at a rich, artificial food source. None of the 50 birds was followed to the food source by other colony members despite the fact that many of the observations were made under adverse weather conditions when food was especially hard to find. The evidence indicates that these gulls exploit preferred food sources and do not readily switch to new sources by following other colony members, contrary to predictions of the informa­ tion center hypothesis. The hypothesis that colonial roosts act as information centers has been tested experimentally using wild Hooded Crows (Corvus corone comix) and Common Ravens (Corvus corax). Loman and Tamm (1980) placed carrion (dead pigs and chickens) at scattered sites in the foraging areas surrounding several roost sites and measured the rate at which new foragers found the food sources. According to the information center hypothesis, the number of individuals coming to each carcass in the morning should be greater than the number of birds feeding at the carcass the preceding evening. This predic­ tion follows because the hypothesis predicts (1) that successful foragers re­ turn in the morning to places they left the preceding evening, and (2) unsuc­ cessful foragers follow successful foragers to the food sources. The results of Loman and Tamm's (1980) study show a gradual buildup in the number of birds foraging at most discovered carcasses during the first day. The buildup is directly attributable to information transfer associated with network foraging and is not attributable to colonial social organization per se. The mean number of foragers present on the morning of the second day was not greater than on the evening of the first day for Hooded Crows (two colonies) but was for Common Ravens (one colony). Data for Common Ravens were obtained from only four tests, compared to 25 tests for Hooded Crows. Thus the study provided limited support of the hypothesis with

22

JAMES F. WITTENBERGER AND GEORGE L. HUNT, JR.

regard to Common Ravens but failed to support the hypothesis for Hooded Crows. Fleming (1981) also tested the information center hypothesis by providing supplemental feeding in roosting Pied Wagtails (Motacilla alba). He found that only "knowledgeable" birds fed in the experimental areas and that no "naive" birds followed them to food on the second day. This result does not support the information center hypothesis. Indirect evidence supporting the information center hypothesis comes from inverse correlations between nestling starvation rates and colony syn­ chrony. Emlen and Demorif (1975) found that nestling starvation is more prevalent among Bank Swallows nesting just after the peak of breeding than among those nesting at the peak. They also found that overall reproductive success is higher in colonies with more synchronous nesting, and this greater success could not be attributed to prédation effects. One interpretation of these results is that individuals can forage more effectively during the peak of colony activity because at that time opportunities for finding food sources by following others are maximal. The results are not conclusive, however, because seasonal declines in food availability could explain why later breeders lose more young to starvation, and differences in food availability at the various colony sites could explain the correlation between average re­ productive success and colony synchrony (see Krebs, 1978). Additionally, Bayer (1982) provides a number of other alternative hypotheses that could explain the results of Emlen and Demong (1975), including greater inex­ perience among late nesters, reduced local enhancement due to declining colony size, and reduced social stimulation for the same reason. One consideration in evaluating the information center hypothesis is that information transfer is a two-edged sword. On some days or on some forag­ ing trips, particular individuals may benefit by following others, but on other days or foraging trips they may suffer by recruiting competitors to locally abundant food patches. The net effect is likely to be positive if resource patches are sufficiently concentrated and ephemeral that resource depletion by other individuals does not hamper foraging efficiency or preclude greater exploitation of them by the initial discoverers. The net effect is likely to be negative if the opposite conditions prevail. The net effect of information transfer is also likely to be positive if individuals forage cooperatively by herding prey once a food patch is found or if group foraging provides protec­ tion from prédation in addition to enhancing foraging efficiency (see below). In these cases, information transfer leads to mutually beneficial results (Evans, 1982), at least up to some threshold flock size. Several bird species drive fish in shallow water (Taverner, 1934, p. 58; Serventy, 1939; Bar­ tholomew, 1942; Cottam et al, 1942; J. Fisher and Lockley, 1954; Nelson,

1. ADAPTIVE SIGNIFICANCE OF COLONIALITY

23

1968; Serventy et al., 1971). However, some of the species involved are not colonial (mergansers, Emlen and Ambrose, 1970) and colonial living is not a necessary precondition to cooperative foraging, although it does aid in rapid flock deployment (G. L. Hunt, Jr., personal observation). In some colonies individuals may differ markedly in their food finding ability. Adult Red-winged Blackbirds, for example, appear to be better for­ agers than young birds, and birds recruited to decoy traps in winter are significantly younger and in poorer condition than the population average (Weatherhead and Greenwood, 1981). In such cases, members of the colony do not all benefit mutually from information transfer (Weatherhead, 1983). The question of why successful foragers join a colony at all or join a colony only after unsuccessful foraging periods has not been adequately answered. Ward and Zahavi (1973) suggest that successful foragers return to colonies as a form of insurance, but this argument does not explain why such individuals return every day instead of just on days when they need information about new food sources. A more convincing argument, offered by Weatherhead (1983), is that successful foragers tend to be socially dominant and return to roosts in order to gain safer roost sites in the center or upper parts of the colony, while only less successful foragers benefit from information transfer. In addition to evaluating the importance of colonies as information cen­ ters, one must consider the availability of alternative food-finding mecha­ nisms. For example, seabirds have a variety of mechanisms that are not dependent on coloniality. They may find food concentrations by means of olfactory cues (R. G. B. Brown, 1980; Wenzel, 1980), through network foraging, and by means of remarkably accurate solar, magnetic, and possibly stellar navigation mechanisms (Matthews, 1968; Southern, 1980). Coloni­ ality can be advantageous as a means of information transfer only to the extent that it increases food-finding success above and beyond the success that is possible by means of other available mechanisms alone. The importance or frequency of information transfer at central colony sites is not known with any real assurance. Some evidence supports the hypoth­ esis that colony members can learn about good foraging sites by following others to feeding grounds, but the evidence is for the most part inconclusive or negative. The limited amount of experimental evidence supports the hypothesis in two cases but does not for two others. In the evolution of coloniality, information transfer may well represent a secondary adaptation for ameliorating the effects of competition around colony sites, by promoting beneficial group foraging (Evans, 1982). Its importance as a primary advan­ tage of coloniality is uncertain, especially for large roosting colonies, because information exchange requires the presence of a previously formed group to which successful individuals must return (Wittenberger, 1981; Bayer, 1982).

24 D.

JAMES F. WITTENBERGER AND GEORGE L. HUNT, JR. N E T ENERGETIC E F F E C T

It is not yet possible to gauge the net energetic effect of coloniality for any species. The net effect may be positive for species such as the Brewer's Blackbird, swallows, and swifts that could benefit from central colony loca­ tion through reduction of mean foraging distances (Horn's geometric model). These species exploit continuously renewing resources that are not seriously depleted at any time by the foraging activities of other colony members so there is little or no penalty from competition for food from other colony members (but see Orians, 1980, regarding the impact of blackbirds on odonate populations). The net effect is possibly also positive for colonial herons, storks and some seabirds as a result of information transfer (see Ashcroft, 1976; Krebs, 1978; Gaston and Nettleship, 1981). The net energetic effect of coloniality is probably negative for many spe­ cies, particularly for those that roost or breed in large colonies. Competition for food is great around such colonies, and benefits derived from information transfer do not seem large enough in most cases to offset the energetic costs of coloniality. This conclusion is best supported for seabird breeding colo­ nies, where clutch size and chick growth rates are low compared to noncolonial species. Inverse correlations of nestling growth rates and fledging weights with colony size in swallows and various seabirds provide additional evidence for a negative net energetic cost of coloniality.

V.

Prédation Effects

A.

ATTRACTION O F PREDATORS

Colonies represent localized concentrations of food for predators. The fact that colonies attract predators is obvious, but the question is whether préda­ tion pressure per individual colony member is increased or decreased by coloniality. No data are available on this point for typically colonial species except for those of Wilkinson and English-Loeb (1982) for swallows (see Section V,C). In Shelducks (Tadorna tadorna), breeding is substantially less successful among individuals breeding in small colonies because Herring Gulls were more often attracted to them (Pienkowski and Evans, 1982). This cost presumably explains why most individuals nest alone in isolated areas. B.

CRITICAL DENSITY E F F E C T

Two important and essentially alternative modes of nest defense in birds are concealment and use of inaccessible or relatively safe sites (Lack, 1968).

1. ADAPTIVE SIGNIFICANCE OF COLONIALITY

25

A key variable associated with both modes of defense is local population density. Effectiveness of concealment should decrease with increasing nest density, partly due to changes in predator search images and perhaps partly due to local increases in predator densities (Croze, 1970). Additionally, as prey clump, the intensity of stimulus they present to predators, and thus their detection distance may increase (Treisman, 1975). On the other hand, many types of inaccessible nest sites (though not all) are spatially clumped and thereby preclude low local nest densities (see Lack, 1968). As a result, use of inaccessible sites renders concealment ineffective in many habitats. In his comparative analysis of breeding dispersion in birds, Lack (1968) concluded that colonial breeding and roosting in many nidicolous land birds and some aquatic birds (e.g., herons) results from the combination of partic­ ular feeding habits and use of inaccessible nesting or roosting sites (see also Crook, 1964, 1965). Lack did not incorporate the role of these factors into an explicit hypothesis however. A more explicit hypothesis, nevertheless, can be developed from Lacks conclusions. The relationship between local population density and effec­ tiveness of concealment suggests the following argument. At low population density (measured as density of individuals or pairs exploiting a given forag­ ing area), dispersed nesting or roosting and reliance on concealment might be the most effective defense against prédation, while at higher population densities concealment is less effective and use of inaccessible, clumped nest sites might offer the most effective defense against prédation. The driving variable, however, is relative effectiveness of concealment versus use of inaccessible sites, not population density. While local population density may be one important variable affecting the effectiveness of concealment, it is not the only one. Also important are body size, color, and habitat struc­ ture, each of which may be important in specific cases. By framing the hypothesis in this way, the interactions between food dispersion, choice of nest site, and nesting dispersion becomes clearer. Spe­ cifically, food dispersion is hypothesized to affect local population density, which in turn affects the relative effectiveness of concealment and thereby choice of nest sites, which in turn affects nesting or roosting dispersion. The above hypothesis is not likely to provide a general explanation of coloniality, even among landbirds, as Lack (1968) makes clear, but it may provide an explanation in some groups. Coloniality is, after all, a multifaceted phenomenon, and no one hypothesis is likely0 to be completely general. To test the hypothesis, the following assumptions need to be evaluated. First, prédation of concealed nests should increase with nest density. Sec­ ond, at low population densities concealment should be a better defense than use of localized inaccessible sites, given prevailing conditions of cover

26

JAMES F. WITTENBERGER AND GEORGE L. HUNT, JR.

and nest site availability. Third, local population densities (as measured over the entire foraging space) should be high for colonial species except when body size or other constraints preclude effective concealment even at low densities (see R. J. Taylor, 1979). Fourth, colonies should be situated in safe or relatively inaccessible sites, and those sites should be spatially localized. A corollary is that colonies should be situated in relatively open habitats, where inaccessible sites tend to be patchily distributed and concealment is less feasible. Forests should not foster coloniality because inaccessible sites are generally dispersed rather than clumped (e.g., holes, tips of outer limbs). Fifth, at prevailing population densities of colonial species, nests or roosting individuals should be safer in colonies than they would be if they were as concealed and as dispersed as possible within the available foraging space. If these assumptions hold, then the critical density hypothesis would predict a shift to coloniality at some threshold population density. Several studies support the first assumption that prédation increases with nest density. Prédation rate increases with nest density in the noncolonial Common Redpoll (Carduelis flammed) (Williamson et al., 1966), Great Tit (Krebs, 1971), Field Sparrow (Spizella pusilla) (Fretwell, 1972; Dunn, 1977), and Snowy Plover (Charadrius alexandrinus) (Page et al, 1983), and for artificial birds' nests (Göransson et al, 1975). Tinbergen et al. (1967) have shown experimentally that closer spacing of eggs in gull colonies leads to an increased frequency of egg loss to predators. Andersson and Wiklund (1978) demonstrated the same effect for Fieldfares. In the Brown-hooded Gull (Larus maculipennis), 16 solitary nests fledged seven times as many young per nest as 107 pairs that nested colonially (J. Burger, 1974a). In this study, the major cause of egg and chick loss was Chimango Caracaras (Milvago chimango). The third assumption, that local population densities should be high for colonial species, seems valid for species that breed or roost in very large colonies, such as many colonial finches, weavers, blackbirds, and starlings. It is probably also valid for species that exploit very concentrated food re­ sources, such as swallows, swifts, Eleonora's Falcon (Falco eleonorae) (Wal­ ter, 1979), crossbills (Newton, 1970), and some jays (Balda and Bateman, 1971). Various constraints preclude effective nest concealment in some colo­ nial species. Large body size is probably an important constraint for colonial birds such as vultures, some crows, flamingos, herons, anhingas, ibises, storks, oilbirds, larids, pelicans, cormorants, alcids, and other seabirds. Black or white coloration, which appears important for thermorégulation (Hamilton, 1973; Howell et al, 1974), may be an additional constraint to concealment for many of these species. A shortage of terrestrial nesting substrate greatly reduces opportunities for noncolonial nesting in all marine and many freshwater birds, although they still are more concentrated than

1. ADAPTIVE SIGNIFICANCE OF COLONIALITY

27

the available space requires. On the other hand, local population densities are not particularly high as measured over the whole foraging space in waxwings, cardueline finches, some oropendolas, and some caciques. None of these face any obvious constraints that preclude concealed nesting, yet many species in these groups nest colonially. Thus, other factors are clearly involved. The fourth assumption, that safe sites are used by colonies, has been shown by Lack (1968) for many species (see also Buckley and Buckley, 1980b). However, for the Ciconiiformes as a whole, Krebs (1978) did not find a correlation between coloniality and nest vulnerability. Little evidence is currently available to evaluate the second assumption, that at low population densities concealment is the best defense, or the fifth assumption, that at higher densities colonial nesting is safer.

C.

SWAMPING E F F E C T

Swamping the ability of predators to exploit available prey is reasonably well documented, and a local increase in nest density or roost size may create a "selfish herd" effect (Hamilton, 1971; Harris, 1980; Gochfeld, 1982). The proportion of nests lost to predators is lower during peak breeding in Black-headed Gulls (Larus ridibundus) (Patterson, 1965), Common Terns (Sterna hirundo) (Nisbet, 1975), Sooty Terns (S. fuscata) (Feare, 1976), Sandwich Terns (S. sandvicensis) (Veen, 1977), Common Murres (17. aalge) and Thick-billed Murres (A. J. Williams, 1975; Birkhead, 1977b) and Redwinged Blackbirds (Robertson, 1973). Brood parasitism of Yellow Warblers (Dendroica petechia) by Brown-headed Cowbirds (Molothrus ater) was re­ duced for pairs nesting synchronously with neighbors and in proximity to Red-winged Blackbirds, and Clark and Robertson (1979) ascribed the im­ proved reproductive success to the swamping of the cowbirds. The propor­ tion of chicks lost to predators is probably reduced when young band to­ gether in creches (Pettingill, 1960; Spellerberg, 1975; Munro and Bédard, 1977; Veen, 1977) or fledge synchronously as in murres (Pennycuick, 1956; A. J. Williams, 1975; Daan and Tinbergen, 1979). Massed arrivals and de­ partures from roosting colonies undoubtedly provide protection from preda­ tors and probably evolved for that reason (Zahavi, 1971b; Wittenberger, 1981; Greig-Smith, 1982), as may have multispecies communal roosts (Gadgil, 1972; Gadgil and Ali, 1976). The swamping effect depends on two conditions. First, the surge in prey availability must be periodic or ephemeral so that a numerical increase in predator abundance cannot occur rapidly enough. Hence large roosting colo­ nies should not exist in the same regions as large breeding colonies of com-

28

JAMES F. WITTENBERGER AND GEORGE L. HUNT, JR.

parably sized species if they are to avoid creating a year-round food supply for predators. Species such as Red-billed Queleas and blackbirds, which form both breeding and winter roosting colonies, should therefore move seasonally if they are to benefit from a swamping effect. Second, predator clumping should be constrained by social interactions within the predator population or by ecological constraints imposed upon it (such as distribution of other prey species). For instance, in Cliff Swallows (Hirundo pyrrhonota) Wilkinson and English-Loeb (1982) found predator density to increase only fivefold, while colony size increased 20-fold, thus suggesting that colony size of prey may increase more rapidly than density of predators. Swamping only confers protection after some critical colony size is reached (Gochfeld, 1980, 1982). For example, Lemmetyinen (1971) showed experimentally that eggs placed near solitary nests of Arctic Terns (Sterna paradisaea) and Common Terns survive longer than eggs placed near nests in colonies because predators (especially Hooded Crows) congregate where nests are most abundant. Likewise, Ruddy Turnstones (Arenaria interpres), apparently using sitting adult terns as a cue to food location, destroyed and ate most eggs in a Royal Tern (Sterna maxima) colony (Loftin and Sutton, 1979). These results imply that the colonies had not reached a size that would swamp the exploitative capabilities of the predators (see also J. Bur­ ger, 1974a; Treisman, 1975). A species that is normally colonial may shift to solitary nesting if densities are insufficient for successful swamping of predators. Larus gulls are preda­ tors of Common Murre eggs and chicks, and losses to predators are greater when murre breeding density is low (Birkhead, 1977b). Where populations have undergone a marked decline, such as at the Farallon Islands (Ainley and Lewis, 1974), Common Murres have retreated to crevices under boul­ ders from their usual nesting ledges in order to gain protection from gulls (Chaney, 1924; see also Birkhead, 1977b). As population densities increased, murres again bred in the open in dense groups, as they had done prior to the decline. Additionally, at the northern limit of their range, Common Murres are present in very low densities and characteristically breed in concealed sites (T. R. Birkhead, personal communication). D.

MOBBING E F F E C T

Both noncolonial and colonial parent birds mob predators and brood para­ sites (e.g., Altmann, 1956; Baggerman et al., 1956; Elgood and Ward, 1963; Curio, 1975; Hoogland and Sherman, 1976; Robertson and Norman, 1976, 1977; Gottfried, 1979). Mobbing is not always an effective defense, but it presumably acts as a deterrent by increasing the costs to predators of exploit-

1. ADAPTIVE SIGNIFICANCE OF COLONIALITY

29

ing that particular type of prey. Mobbing has been demonstrated to be an effective deterrent against predators in Arctic Terns (Bullough, 1942; P. J. K. Burton and Thurston, 1959), Franklin's Gull (Larus pipixcan) (J. Burger, 1974b), Black-headed Gulls (Kruuk, 1964; Patterson, 1965; Fuchs, 1977b), Black-legged Kittiwakes (Andersson, 1976; Montevecchi, 1979), murres (many individuals threaten even while remaining on their eggs, A. J. Williams, 1975; Birkhead, 1977b), Bank Swallows (Hoogland and Sherman, 1976), Brewer's Blackbirds (Horn, 1968), Red-winged Blackbirds (against Marsh Wrens ([Cistothorus palustris], Pieman, 1980), Yellow-hooded Black­ birds (Agelaius icterocephalus) (against brood-parasitic cowbirds, Wiley and Wiley, 1980), Yellow-rumped Caciques (Cacicus cela) (Feekes, 1981), Fieldfares (Andersson and Wiklund, 1978; Wiklund and Andersson, 1980; Wiklund, 1982, although colonial breeding is not involved under all circum­ stances [Hogstad, 1983]), and weaverfinches (Crook, 1964). Experimental studies show that mobbing confers protection on artificial nests or eggs in Arctic Terns (Lemmetyinen, 1971, 1972), Sandwich Terns (Fuchs, 1977b; Veen, 1977), Northern Lapwings (Vanellus vanellus) (Göransson et al., 1975), and Fieldfares (Andersson and Wiklund, 1978). In a mixed colony of terns and skimmers, Sears (1979) found that gull numbers and predatory activity increased in the colony after all nests but one were deserted after a storm, presumably due to the lack of group defense. In general, protection is more effective against aerial predators than against terrestrial predators (e.g., mammals and snakes) (Elgood and Ward, 1963; Snapp, 1976; Blem, 1979). Prey species sometimes gain protection by nesting near colonies of other species, including colonies of potential predators (Crook, 1965). Erwin (1979) found that in mixed colonies of Common Terns and Black Skimmers (Rynchops niger) the skimmers derived protection from the mobbing of predators by Common Terns. In this colony, neither nest site limitation nor information sharing could account for the interspecific association. Cases of potential prey nesting near colonies of predatory species include ducks nest­ ing near gull colonies (Koskimies, 1957; Hilden, 1964; Vermeer, 1968), terns nesting near gull colonies (Cullen, 1960; Lind, 1963; Fuchs, 1977b; Veen, 1977), and gulls nesting near jaeger colonies (Götmark and Andersson, 1980). In each case the predatory species provides protection because its members mob corvids or larids. This protection apparently outweighs the costs associated with nesting near the predators. In an interesting reversal of roles, Wiklund (1979) found that the reproductive success of Merlins (Falco columbarius) was improved when Fieldfares chose nearby nest sites. The Merlins did not prey heavily on the Fieldfares, and Wickland hypothesized that mobbing of predatory Hooded Crows by the Fieldfares was responsible

30

JAMES F. WITTENBERGER AND GEORGE L. HUNT, JR.

for the improved Merlin reproduction. At the same time, the Fieldfares also gained protection by nesting near the Merlins (Wiklund, 1982). One potential advantage of coloniality is that recruitment of neighbors to mobbing episodes is more successful at high local population densities, as may be the potential for cultural transmission of enemy recognition (Curio et ah, 1978a,b; Vieth et ah, 1980). However, the amount of benefit derived from more effective mobbing rapidly reaches an asymptote as colony size increases. Recruitment to mobbing is generally confined to the local vicinity of the predator (Snapp, 1976; Siegel-Causey and Hunt, 1981; Drycz et ah, 1981), and no further recruitment is gained by nesting in a colony larger than the size of area from which help can be recruited.

E.

VIGILANCE E F F E C T

Improved vigilance with reduced time expenditure per individual is a well established benefit of flocking behavior (e.g., Powell, 1974; Siegfried and Underhill, 1975; Kenward, 1978; Lazarus, 1979; Caraco et ah, 1980; Bar­ nard, 1980; Bertram, 1980; Jennings and Evans, 1980; Thompson and Bar­ nard, 1983). Similarly, mutual vigilance could confer protection on members of colonies. Mutual vigilance is probably an important benefit in most breed­ ing colonies. Eggs and nestlings are the main prey at risk in most species, and early detection of predators allows parents to begin mobbing while chicks seek cover (Crook, 1964). Hoogland and Sherman (1976) found, for example, that the time elapsing before a stuffed mammalian predator was mobbed by Bank Swallows was inversely related to colony size. In contrast, Wilkinson and English-Loeb (1982) failed to find an inverse correlation be­ tween reaction time to the presentation of a predator and colony size in Cliff Swallows. Colonial caciques often flee from nests and the colony tree upon hearing calls warning of the approach of a predator capable of killing adults (Feekes, 1981). Western Grebes (Aechmophorus occidentalis) derive protec­ tion by reacting to the alarm cues of Forster's Terns (Sterna forsten), in whose colonies the grebes nest (Nuechterlein, 1981). Nuechterlein cites a number of examples in which the apparent value of multispecies colonies is that one species gains either protection from predators or warning about them from the other species in the colony.

F.

NEST OR ROOST SITE PACKING

Dense packing into the center of breeding or roosting colonies has the consequence that not all suitable space in or around a colony site is occupied.

1. ADAPTIVE SIGNIFICANCE OF COLONIALITY

31

Nest or roost site packing occurs either because peripheral nests are less safe than central ones or because higher density confers direct advantages on colony members. Peripheral nests have been shown to be more vulnerable to prédation than central nests in Adélie Penguins (Pygoscelis adeliae) (R. H. Taylor, 1962; Reid, 1964; Eklund, 1964; Penney, 1968; Tenaza, 1971), Cattle Egrets (Bubulcus ibis) (Siegfried, 1972), American White Pelicans (Schaller, 1964; but see also Knopf, 1979), Double-crested Cormorants (Phalacrocorax auritus) (Siegel-Causey and Hunt, 1981), Black-headed Gulls (Patterson, 1965), Black-legged Kittiwakes (Andersson, 1976), Sooty Terns (Feare, 1976), caciques (Feekes, 1981), Pinyon Jays (Balda and Bateman, 1971), and Fieldfares (Wiklund, 1982). Central nests recruit larger numbers of birds to mobbing episodes than peripheral nests in Bank Swallows, but the relative rate of prédation loss in these nests is unknown (Hoogland and Sherman, 1976; see also Emlen, 1971). Although central location may enhance reproductive success, it is not clear that increased density, per se, protects nests from predators. In a number of studies, chick or egg survival was either not influenced by nest density [Glaucous-winged Gull (Larus ghucescens), Vermeer, 1963; Blackheaded Gull, Patterson, 1965; Ring-billed Gull (L. delawarensis), Dexheimer and Southern, 1974; Western Gull (L. occidentalis), Hunt and Hunt, 1975] or negatively correlated with nest density [Kelp Gull (L. dominicanus), Fordham, 1970; Glaucous-winged Gull, Hunt and Hunt, 1976a; Western Gull, Ewald et al, 1980; Great Black-backed Gull (L. marinus), Butler and Trivelpiece, 1981]. Tinbergen (1952) also found that Herring Gull colonies subject to attack by terrestrial predators had nests more widely spaced than in other colonies, suggesting that nest density may be affected by the principal type of predator involved. Parsons' (1976) finding of max­ imum Herring Gull reproductive success at intermediate densities suggests that, as Hunt and Hunt (1976a) hypothesized, there are tradeoffs between interference at high densities and a lack of effective defense against preda­ tors at low densities. Thus, some optimum density is likely to exist with respect to prédation and interference effects, at least in seabird colonies (Hunt and Hunt, 1976a). That optimum, however, may well be different for long-term residents and birds newly arriving at a colony (who might not have better options elsewhere). In summary, the evidence suggests that nest packing results from advan­ tages inherent in central location and not from positive density effects per se. Indeed, increased density appears to be largely deleterious due to increased interference. Nevertheless, increased density could be advantageous if it increases the effectiveness of mobbing. A more careful separation of density effects from centrality effects should be made in future studies.

32 G.

JAMES F. WITTENBERGER AND GEORGE L. HUNT, JR. N E T PRÉDATION E F F E C T

The net effect of coloniality on prédation rates is difficult to gauge without comparative evidence for noncolonial populations existing at densities (based on the area of the entire foraging space) comparable to those of colonial populations. Present evidence suggests that the net effect of coloniality is positive, at least during peak occupancy of colony sites, owing to inac­ cessibility of sites and the swamping of predator hunting capabilities. Early and late in the season, however, breeding numbers are often considerably lower, and the pairs nesting then may suffer more prédation (due to the attraction of predators to the colony) than if they had nested noncolonially. This possibility is discussed more fully in Section IX, C. The fundamental importance of coloniality as a protection against préda­ tion is supported by the fact that predator mobbing and vigilance effects are important for colonial species in which there is apparently no transfer of information about food (Clark and Robertson, 1979). This is true for some single species colonies (caciques, Feekes, 1981) as well as for communal roosting or nesting by multispecies groups of diverse foraging habits (e.g., various Indian birds, Gadgil and Ali, 1976). VI.

Egg Destruction and Chick Killing

A.

NEGATIVE ASPECTS

Increased egg and chick loss due to the presence or activities of conspecifics represents a potentially severe cost of coloniality in some birds. Eggs are lost in Cattle Egret colonies when nest materials are stolen (Sieg­ fried, 1972). Arctic Terns, Lesser Black-backed Gulls (Larus fuscus), Her­ ring Gulls, and Carrion Crows (Corvus corone corone) have been reported to steal, puncture, and eat eggs from neighboring nests of conspecifics (Pettingill, 1939; Paynter, 1949; Harris, 1964; R. G. B. Brown, 1967; Drent, 1970; Parsons, 1971; Yom-Tov, 1975; Davis and Dunn, 1976). Chick killing by conspecific adults commonly occurs in colonies of skuas, gannets, and large gulls (Pettingill, 1939; Sprunt, 1948; Paynter, 1949; Harris, 1964; R. G. B. Brown, 1967; R. W. Burton, 1968; Vermeer, 1963; Kadlec et al, 1969; Fordham, 1970; Parsons, 1971; Spellerberg, 1971; Feare, 1976; Hunt and Hunt, 1976a; Montevecchi, 1977; Nelson, 1978; Randall and Randall, 1981). Chick killing without cannibalism primarily occurs when the chick is at the edge of its natal territory or has intruded onto a neighboring territory (Paynter, 1949; Tinbergen, 1952; Kadlec et al, 1969; Fordham, 1970; Par­ sons, 1971; Montevecchi, 1977; Harris, 1964; Feare, 1976). Most chick kill-

1. ADAPTIVE SIGNIFICANCE OF COLONIALITY

33

ing in gannets and terns takes this form. In Western Gulls, chick survival decreases as territory size decreases due to increased incidence of chick killing by neighbors (Ewald et al, 1980). The other major form of chick killing is cannibalism, which for colonial species occurs mainly in skuas, large gulls, and Carrion Crows (Paynter, 1949; Parsons, 1971; Spellerberg, 1971; R. G. B. Brown, 1967; Harris, 1964; Yom-Tov, 1975; Davis and Dunn, 1976; Burger and Gochfeld, 1981). This form of chick killing is comparable to prédation in that cannibalistic indi­ viduals often range widely in search of chicks and take chicks from unat­ tended nests. Cannibalism is sometimes common in gull colonies, but its frequency is highly variable (see below). Larger territory size may lead to a higher incidence of cannibalism from nonneighbors, as Herring Gull can­ nibalism is more prevalent in less dense parts of colonies (Parsons, 1971). The threat of chick killing or cannibalism means that one parent must attend the nest when eggs or small chicks are present, which reduces paren­ tal ability to feed chicks. Although chicks may be growing at maximal rates, increased feeding could allow a larger brood. However, parents in some cases must attend nest sites continuously anyway to guard eggs or chicks from predators (see Birkhead, 1977a; Wittenberger and Tilson, 1980), and/or to prevent eggs or chicks from becoming chilled or overheated (Pettingill, 1937; Allen, 1956; Howell and Bartholomew, 1962; Modha and Coe, 1969; Bartholomew and Dawson, 1979; Bennett and Dawson, 1979; Rahn and Dawson, 1979; Dawson and Bennett, 1981).

B.

ENERGETIC ADVANTAGES

The most obvious benefit to be derived from cannibalism is increased energy intake. Coloniality in gulls and Carrion Crows not only creates risks of egg and chick loss to conspecifics, it also affords greater opportunities to obtain food through cannibalism. The importance of cannibalism as a source of energy is difficult to assess because the proportion of food intake that consists of conspecific eggs and chicks has not been measured. Clearly, the proportion cannot be high on average, but it might be high for some individuals. For instance, Parsons (1971) found that a few cannibals substantially reduced annual Herring Gull chick productivity in a colony. Only a few individual Herring Gulls spe­ cialized on conspecific eggs and/or chicks, while most individuals were not cannibalistic. There is, however, risk attached to such a strategy, since a number of cannibals adopt chicks instead of eating them (Parsons, 1971). The result therefore could be a net reduction in fitness (Parsons, 1971; Pierotti, 1980).

34

JAMES F. WITTENBERGER AND GEORGE L. HUNT, JR.

Cannibalism could offer an alternative method of foraging during food scarcity. There is no obvious direct relationship, however, between food abundance and incidence of cannibalism. Some studies have found high rates of cannibalism in periods of high food abundance (R. G. B. Brown, 1967), while in other cases where food was abundant, cannibalism was low (Haycock and Threlfall, 1975; Burger and Gochfeld, 1981). Fordham (1964) found that frequency of chick killing in a colony of Kelp Gulls varied an­ nually, but he attributed the variation either to increased wandering of chicks in some years (due to food scarcity) or to heightened aggression of adults in some years. In that study, most chicks were killed after intruding on neighboring territories and were not eaten. The former interpretation, of increased chick wandering, is more likely, as Hunt and McLoon (1975) showed that recently fed Glaucous-winged Gull chicks were less likely to wander. No correlation should exist between incidence of cannibalism and food availability if cannibalism represents a specialized foraging strategy adopted by a few individuals. _ __

C.

CHICK KILLING AND RELATIVE FITNESS

Chick killing may decrease the fitness of other individuals and thereby increase the relative fitness of the perpetrators (Pierotti, 1980). This argu­ ment requires that chick killing reduces average fitness of all nonperpetrators more than it reduces the fitness of perpetrators. The mathematics involved in evaluating this hypothesis is identical to that presented by Pleasants and Pleasants (1979) with regard to Verner's (1977) "super-territory" hypothesis. The calculations show that chick killing can increase relative fitness only if the cost to perpetrators is less than the cost to the victims divided by the number of victims. For example, if perpetrators affect the fitness of only one pair in 10,000 initially, the cost to perpetrators must be less than one ten-thousandth of the loss felt by their victims. Whether such a disparity exists is problematical, but it may be present if the cost for perpetrators of chick killing is virtually zero. One must in addition consider that perpetrators of chick killing can also be victims. If that is done, the calculations show that perpetrators can never gain in relative fitness through such behaviors. Hence, indiscriminate chick killing cannot be explained by Pierottis (1980) hypothesis unless chick killing is selectively directed at individuals who lack the behavior themselves and then only if the cost to the perpetrator is very low. Since there is presently no evidence for the existence of such selectivity, Pierotti's (1980) hypothesis appears unlikely. Facultative chick killing that is perpetrated by individuals only after they have lost their own

1. ADAPTIVE SIGNIFICANCE OF COLONIALITY

35

clutches or broods, such as occurs infrequently in Lesser Black-backed Gulls (Davis and Dunn, 1976), does not overcome the problems of the hypothesis, because other perpetrators would still be vulnerable.

D.

PREVENTING ADOPTIONS

Some other hypothesis is needed to explain the attacking or killing of intruding chicks. One such hypothesis is that attacks on chicks are a form of territory defense (e.g., Hunt and Hunt, 1976a), in that wandering chicks might increase conflict between territory neighbors. There is no evidence at present, however, to support this argument. Another hypothesis is that chick killing is a means of preventing inadver­ tent adoption (Ashmole, 1963) or feeding (Feare, 1976; Elston et al, 1977) of neighboring chicks. Such feedings and adoptions occur regularly, though infrequently, in some gulls and terns (Vermeer, 1963; Howell et al., 1974; Hunt and Hunt, 1975; Feare, 1976; Elston et al, 1977; Graves and Whiten, 1980; Holley, 1981), which are unable to recognize their own chicks for the first few days following hatching (Goethe, 1937; Tinbergen, 1953; Davies and Carrick, 1962; Thompson and Emlen, 1968; Buckley and Buckley, 1972; Miller and Emlen, 1975). Chicks also do not recognize their parents during that period (Beer, 1970; Evans, 1970a,b, 1980). Thereafter, adults are ag­ gressive toward strange chicks. Without such aggression intruding chicks might regularly solicit and obtain food (Elston et al, 1977) or become foster chicks. Marsh-nesting and cliff-nesting populations where chicks cannot wander do not show chick recognition at such an early age (Cullen, 1957; J. Burger, 1974b; Berens von Rautenfeld, 1978; Beecher et al, 1981). Reasons why chicks are killed instead of merely chased out of territories are at least threefold. First, chick killing is not much more costly or risky than chasing chicks away. Second, chick killing prevents recurrences of chick intrusions. Third, the probability of adoptions occurring increases with the length of time that chicks remain on the territory (Graves and Whiten, 1980). Despite these advantages, limited threatening or pecking of intruding chicks does occur in a wide variety of colonial birds, including penguins (Stonehouse, 1960; Warham, 1963; Penney, 1968; Thompson and Emlen, 1968; Spurr, 1975a), albatrosses (M. L. Fisher, 1970; Harris, 1973), boobies (Dorward, 1962; Nelson, 1967a,b, 1978), cormorants (B. K. Snow, 1963), pelicans (Schaller, 1964; L. H. Brown and Urban, 1969), gulls (Fetterolf, 1984), alcids (Tschanz and Hirbrunner-Scharf, 1975), and swallows (Hoogland and Sherman, 1976; C. R. Brown and Bitterbaum, 1980; Beecher et al, 1981), and it is often a more common response to trespass than killing of chicks. The feeding of chicks other than the parents' own occurs in cases of

36

JAMES F. WITTENBERGER AND GEORGE L. HUNT, JR.

chick trespass in several of the above taxa, and attacks against them serve to diminish the stealing of food. If the adoption prevention hypothesis is correct, chick killing should be directed only at chicks who are intruding or about to intrude on the per­ petrator's territory, except when chick killing is associated with cannibalism. This is in contrast to the prediction to be drawn from Pierotti's (1980) hy­ pothesis, namely that chick killing should occur on an opportunistic basis anywhere in the colony. Second, egg destruction should only occur when associated with cannibalism, since egg adoptions rarely occur inadvertently. This prediction also is in contrast to Pierotti's (1980) hypothesis, which im­ plies that "spiteful" egg destruction should be just as advantageous as "spiteful" chick killing. Third, adults without chicks should be less prone to kill intruding chicks unless the presence of chicks hampers future mating prospects or chicks are cannibalized. Fourth, adults should be most prone to kill intruding chicks while they are feeding chicks of their own and should be less prone to kill chicks while they are still incubating (Hunt and Hunt, 1976a). This last prediction does not allow for a conclusive test of the hypoth­ esis, however, because there are other ways to explain any contradictory evidence. For instance, incubating Herring Gulls and Black-headed Gulls sometimes stop incubating their own eggs after adopting strange chicks (Beer, 1966; Kadlec et al., 1969). Also, if chick killing entails little risk, it would eliminate future intrusions that might occur after the parents' own brood hatches. As discussed above, present evidence supports the first and second pre­ diction. Little evidence bears on the third prediction, although some male Lesser Black-backed Gulls remain on territories following clutch or brood loss and attack eggs or, less frequently, chicks of neighbors (Davis and Dunn, 1976). These attacks are always cannibalistic and hence do not contra­ dict the third prediction. No evidence pertinent to the fourth prediction currently exists.

E.

NET EFFECT

A few cannibals may obtain a net benefit from egg destruction and chick killing, but for most colony members the net effect is negative. This cost is especially important in colonial skuas, terns, and gulls, where egg destruc­ tion and chick killing are common. Chick killing at territorial boundaries and cannibalism should be treated as separate phenomena, since they vary in different ways with such factors as territory size, food abundance, and time of season.

37

1. ADAPTIVE SIGNIFICANCE OF COLONIALITY TABLE I

SPECIES OF BIRDS WITH REPORTED EXTRA-PAIR COPULATIONS NOT CITED BY GLADSTONE (1979) Species

Mating forced?

Are both birds mated?

Reference

Lesser Snow Goose (Anser c. caerulescens) Common Murre (Uria aalge) Lesser Black-backed Gull (Larus fuscus) Western Gull (L. occidentalis) Glaucous-winged Gull (L. glaucescens) California Gull (L. californicus) Ring-billed Gull (L. delwarensis) Red-winged Blackbird (Agefoius phoeniceus) Tricolored Blackbird (A. tricolor)

Yes

Usually

Mineau and Cooke (1979)

Usually not

Usually (?)

Sometimes

Usually

No

Usually (?)

Yes

Yes

?

?

Conover et al (1979)

?

?

?

?

Conover et al. (1979) Ryder and Somppi (1979) Bray et al. (1975)

VII.

promiscuous behavior seen, but not completed

Birkhead (1978a) MacRoberts (1973) Hunt and Hunt (1977) Vermeer (1963)

Lack and Emlen (1939)

Extra-Pair Copulations

Although extra-pair copulations (cuckoldry) occasionally occur in monog­ amous noncolonial birds (Power and Doner, 1980 and references therein), cuckoldry is a more common phenomenon in otherwise monogamously mated colonial birds. In addition to the 18 colonial species listed by Gladstone (1979), there are at least 12 others in which extra-pair copulations have been reported (Table I). Although it is difficult to detect successful inseminations or their effect on paternity, sperm transfer has been demon­ strated in several species [Bray et al, 1975; Hoogland and Sherman, 1976; Hunt and Hunt, 1977; Ryder and Somppi, 1979; Conover et al, 1979; Roberts and Kennelly, 1980; E. Davies, unpublished data on Yellow-headed Blackbirds (Xanthocephalus xanthocephalus)]. The preponderance of extrapair mating appears to be between members of neighboring pairs (Birkhead, 1978), but at least a few copulations apparently involve unmated males (Mineau and Cooke, 1979; MacRoberts, 1973). Aside from any genetic costs that males might accrue through lost pater­ nity (Gladstone, 1979), males always suffer energetic costs by having to defend against cuckoldry and competing for extra-pair copulations. These

38

JAMES F. WI1TENBERGER AND GEORGE L. HUNT, JR.

costs may be substantial (Allen and Nice, 1952; C. R. Brown, 1978; Birkhead, 1978, 1979, 1982; Beecher and Beecher, 1979; Gladstone, 1979; Power et al, 1981). One relevant consideration here is that males should be most willing to seek extra-pair copulations after they can no longer be cuckolded themselves (McKinney, 1975; Mineau and Cooke, 1979). The best support for this prediction comes from Lesser Black-backed Gulls and Lesser Snow Geese (Anser caerulescens), where males seek extra-pair copu­ lations mainly while their mates are incubating (MacRoberts, 1973; Mineau and Cooke, 1979). In Bank Swallows, males attempt extra-pair copulations only before or after the period when their own mates are fertile (Beecher and Beecher, 1979). Females may also suffer an energetic cost if avoiding extra-pair matings is to their advantage. This is certainly true in cases where females are sub­ jected to harassment and forced copulations, as occurs widely in noncolonial ducks (see Johnsgard, 1975; McKinney, 1975) and regularly in Purple Mar­ tins (C. R. Brown, 1978). Another possible reason why cuckoldry might be disadvantageous to females is that reduced paternity assurance could lower the willingness of males to provide parental care (Gladstone, 1979; Power and Doner, 1980). This factor should at least cause females to be secretive about being unfaithful. In herons and egrets, females resist extra-pair copu­ lations but are less resistant to them after their eggs are laid (Meanley, 1955; Fujioka and Yamagishi, 1981), suggesting that cuckoldry is detrimental to females. In Western Gulls, females rebuffed advances by males in a dense colony but accepted them in a less dense colony in which there was an excess of females (Pierotti, 1981). In some communally nesting species, promis­ cuous copulations lead to the sharing of parental duties by more than one male and this sharing of parental duties is hypothesized to increase fitness for both males and females (Stacey, 1982). Additional tests of these hypotheses are needed. The net average effect of cuckoldry can only be negative for males. The genetic consequences for average breeding males can be either zero or negative (except under unusual circumstances; see below), while the ener­ getic consequences are always negative. Cuckoldry does not affect the number of young fathered by the average male whenever all extra-pair copulations involve only other mated males, because the same number of eggs are still fertilized by the same number of males (see Gross and Shine, 1981). What cuckoldry does affect is variance in male reproductive success, which probably increases, and the distribution of each males genetic off­ spring among the various females' nests. Cuckoldry may also affect each male's willingness to provide parental care, although such an effect has not been demonstrated. Cuckoldry reduces the number of young fathered by each paired male if it allows unpaired males to father some young, or in-

1. ADAPTIVE SIGNIFICANCE OF COLONIALITY

39

creases that number if it enables female-female pairs to lay fertile eggs (Hunt and Hunt, 1977; Conover et al, 1979; Ryder and Somppi, 1979). In contrast, if the colony consists of inbred, closely related individuals, as in the case of Flightless Cormorants (Phalacrocorax harrisi), serial polyandry by females can benefit male inclusive fitness (Tindle et al., 1982). Extra-pair copulations could increase female fitness if females benefit from greater genetic diversity among offspring. Female fitness would decrease if females are subjected to harassment, forced copulations, the continual need to resist male copulation attempts, or reduced male parental assistance. The net effect of cuckoldry has not been evaluated carefully for any species, but it is probably negative in most or all colonial species.

VIII. Other Considerations A number of other factors add to the costs of nesting or roosting in colo­ nies. These are important mainly for large or dense colonies and hence affect models of optimal colony size. They are less important as immediate costs during early stages of colony formation.

A.

COMPETITION FOR SPACE

The quality of available space varies within breeding and roosting colo­ nies, with the result that significant differences in fitness arise between individuals occupying the most and least desirable locations (Coulson, 1971). For individuals who are forced into poorer sites, the costs of coloniality are therefore increased. In polygynous colonial species, competition for desirable space may limit access to mates. In an experimental study of the Village Weaver (Ploceus cucullatus), the size of a males territory determined the number of nest sites available to him, and hence the number of females he could inseminate (Collias et al., 1971). Crook (1964) found that in colonial weaverbirds a number of males were excluded from breeding. In some colonial birds poly­ gyny apparently arises because not all males can obtain territories in suitable habitat, and males with the best habitats usually obtain the most mates (Wittenberger, 1976, 1979). Some members of colonies may be forced to select poor nest sites or delay breeding. In the European Shag (Phalacrocorax aristotelis) there is strong competition for protected nest sites, and young birds that are forced to nest in poorer sites have lower reproductive success than those that can gain

40

JAMES F. WITTENBERGER AND GEORGE L. HUNT, JR.

access to the preferred sites (Coulson, 1971; Potts et al., 1980). In various other seabirds, individuals nesting late may be forced to accept peripheral sites subject to greater exposure to predators or flooding (N0rrevang, 1960; Patterson, 1965; Dexheimer and Southern, 1974; Blus and Keahey, 1978; J. Burger, 1978; Montevecchi, 1978; Burger and Lesser, 1979; Burger and Gochfeld, 1981, Duffy, 1983). However, in one gull colony that lacked a strong differential in age structure between the center and the edge, there was little spatial variation in reproductive success (Ryder and Ryder, 1981), and Pugesek and Diem (1983) found that when parental age was taken into consideration, most effects of nest site location within a colony were rela­ tively unimportant. In African cormorants and in tropicbird colonies, nest site shortages prevent individuals from all breeding at the same time (Marshall and Roberts, 1959; Stonehouse, 1962; D. W. Snow, 1965). Many pairs must delay breeding until a suitable site becomes vacant, and on the Galapagos Islands the Band-rumped Storm-Petrel (Oceanodroma castro) has two peaks of nesting, one from April to June and one in December and January, with some nest holes being used sequentially (Harris, 1969). In tropicbirds, intraspecific competition for nest sites is a major cause of nest­ ling mortality (Stonehouse, 1962). Interspecific competition for nest holes between Atlantic Puffins and Manx Shearwaters (Puffinus pufflnus) on the Isle of Skomer is a significant cause of reproductive failure for the puffins (Ashcroft, 1979). These examples suggest that, at least in some cases, colony size may be limited by the nest sites available. Thus, some instances of coloniality may result solely from the limited distribution of available nest sites. Colonial nesting may also result in increased energetic costs, with territo­ ry size inversely related to intrusion pressure, indicating that the cost of territory defense increases with nest density (Ewald et al., 1980). In Com­ mon Murres and Razorbills (Alca torda) some adults return to their breeding sites for up to 14 days after chick departure in order to protect the site from prospecting immature birds (Birkhead, 1977a, 1978). Salomonsen (1955) be­ lieved that winter colony attendance by Northern Fulmars (Fulmarus glacialis) in the Faroe Islands was a response to competition for nest sites, as is the protracted period of colony occupancy by murres prior to breeding (Birkhead, 1978). Alternatively, Macdonald (1980) suggested that winter attendance of fulmars in Scotland was not due to competition but might aid in pair formation. Thermoregulatory considerations may also be important for nest or roost site selection within colonies. Some small passerines roost together to con­ serve heat (Löhrl, 1955; Armstrong, 1955; Brenner, 1965; Lack, 1968; Welty, 1975, pp. 129, 131; Chaplin, 1982). The large compartmented nest

1. ADAPTIVE SIGNIFICANCE OF COLONIALITY

41

structure of the Sociable Weaver (Philetairus socius) provides significant thermal insulation and energy savings in both breeding and nonbreeding seasons (White et al., 1975; Bartholomew et al., 1976). These savings are greatest in large nests (and presumably at the center of large nests). Since nests are used generation after generation, one might expect competition for central nests in the largest colonies. In colonial roosts, young Rooks (Corvus frugilegus) with low social status usually spend the night on branches be­ neath birds of higher status, who prefer the upper branches on all but windy nights (Swingland, 1977). The lower birds are exposed to a constant rain of droppings, which Yom-Tov (1979) has shown diminishes the water repellent quality of feathers and hence is likely to increase the probability of suffering exposure on rainy days. The preference shown by high-status Rooks for lower, more sheltered branches on windy nights further demonstrates com­ petition for energetically better sites (see Swingland, 1977). Nest sites in most breeding colonies do not seem to differ much with regard to thermal characteristics, although some sites may be more exposed than others. In the Channel Islands of California, Western Gulls and Brandts Cormorants (Phalacrocorax penicillatus) nest primarily on the windward side of islands (Hunt et al., 1979; Salzman, 1982), where poten­ tially detrimental high temperatures are less likely. The extent to which nest sites vary in thermal or shelter characteristics within colonies is essentially unstudied, but one probable cost of breeding in a colony is the frequent need to accept thermally less suitable nest sites than would be necessary if nesting were solitary. Other effects may be important in determining nest site quality as well. Heavy rainfall can cause flooding of nests in low-lying areas, and Laughing Gulls (Larus atricilla) are sometimes forced into such areas by competition with Herring Gulls (J. Burger, 1979b). Tidal flooding is often important in reducing the quality of low-lying areas in some gull, tern, and Black Skim­ mer colonies (Burger and Lesser, 1978a,b; J. Burger, 1979b; Buckley and Buckley, 1980b). In the high arctic, sea-facing cliffs are free of ice and snow earlier than landward-facing cliffs, which allows birds to breed earlier on them (Buckley and Buckley, 1980a). Indirect evidence for chronic competition for space is the partitioning of nest sites among species in mixed-species colonies (N0rrevang, 1960; Swales, 1965; Bédard, 1969b; Kepler, 1978; McCrimmon, 1978; J. Burger, 1978, 1979c; Burger and Shisler, 1980; Duffy, 1983; Squibb and Hunt, 1983). Common and Thick-billed Murres show consistent differences in their preferences for nesting ledges of different depths in both the Bering Sea (Hunt et al, 1981b) and the North Atlantic (Tuck, 1960; A. J. Williams, 1974). In contrast, however, Beaver et al. (1980), concluded that for herons

42

JAMES F. WITTENBERGER AND GEORGE L. HUNT, JR.

variations in nest sites were greater between colonies than between species and they suggested that the dispersion of nests within colonies was related primarily to local vegetation patterns. B.

T H E F T O F N E S T MATERIAL

Nest material may be in short supply or costly to obtain. As a result, competition for, or stealing of, nest material may be a disadvantageous con­ sequence of colonial breeding. Not only may nest materials be in short supply locally, but the risk of unguarded materials being stolen requires that one member of a pair be on territory at all times. The need to guard nests means that at any one time one individual is unable to gather nest material or to forage. Coloniality not only increases the chance of losing nest materials but also increases the chance of acquiring nest materials. Exposure to theft is greatest for early breeders and least for late breeders. Conversely, opportunities to benefit from theft are least for early breeders and greatest for late breeders. Hence early breeders probably experience a net cost, while late breeders probably obtain a net benefit from thievery. Theft of nest material occurs, for example, in penguins (Ainley, 1975; Spurr, 1975b; Yeates, 1975), cormorants (L. Williams, 1942; G. L. Hunt, Jr., personal observation), frigatebirds (Nelson, 1975), gannets (Nelson, 1978), some gulls (J. Burger, 1974b), herons (Lowe, 1954; Siegfried, 1972), swal­ lows (Emlen, 1952; Hoogland and Sherman, 1976), Rooks (Coombs, 1960), and Pinyon Jays (Balda and Bateman, 1972). In mixed colonies, herons sometimes completely dismantle Anhinga (Anhinga anhinga) nests (Meanley, 1954). For many of these species nest materials are apparently not in short supply, but absences from the territory or colony are required to gather them. Deleterious consequences of such absences may therefore be the primary selective pressure promoting theft of nest materials. Sociable Weavers salvage fallen, used material from nests in preference to searching widely for new material, thereby conserving energy (Collias and Collias, 1978). Hence energy conservation may also be an important factor favoring theft of nest materials. C.

KLEPTOPARISITISM

Colonies may provide the focus for interspecific or intraspecific kleptoparasitism, which is the stealing of food from others (reviewed by Rand, 1954; Brockmann and Barnard, 1979). Skuas, gulls, and terns commonly steal fish from puffins returning to colonies to feed young (N0rrevang, 1960;

1. ADAPTIVE SIGNIFICANCE OF COLONIALITY

43

Grant, 1971; Nettleship, 1972; Andersson, 1976; Arnason and Grant, 1978, Furness, 1978b), and gulls and some species of terns frequently force other terns carrying fish to their young to give up this food (Rand, 1954; Hatch, 1970, 1975; Hays, 1970; Hopkins and Wiley, 1972; Dunn, 1973). Fuchs (1977a,b) and Elston et al. (1977) described instances of gulls patrolling colonies on foot while stealing food and Fetterolf (1984) showed that foodstressed large young in Ring-billed Gull colonies often attempt to steal food from neighboring chicks. Frigatebirds frequently pirate food from boobies near colonies, although they usually catch their own food (Nelson, 1975). Black-faced (Lesser) Sheathbills (Chionis minor) are possibly obligate kleptoparasites on penguins (A. E. Burger, 1981). While some colony members probably obtain a net benefit from kleptoparasitism, most can be expected to lose not only the value of the food, but also the cost of trying to avoid theft of food, which disrupts normal parent-offspring interactions. Species that spe­ cialize on pirating food gain from nesting near other colonial species (Nelson, 1975).

D.

TRANSMISSION O F DISEASE AND ECTOPARASITES

The impact of a wide variety of diseases and ectoparasites on birds in general and on colonial birds in particular is unknown. Diseases and ecto­ parasites are most easily transmitted between individuals who are in close proximity or contact (Stefferud, 1956; Rothschild and Clay, 1952), so indi­ viduals in dense roosts or colonies would be infected more often than indi­ viduals of related noncolonial species. Colonial seabirds are frequently cited as victims of disease (Aldous, 1941; Dane, 1948; Kaschula and Truter, 1951; Dane et al., 1953; Hadley, 1961; Vermeer, 1969). Certainly, the most se­ rious outbreaks of disease among waterfowl occur where birds gather in dense aggregations on small, shallow ponds (Quortrup, 1946; Petrides and Bryant, 1951; Wobeser et al., 1979; Forrester et al., 1980). The frequency of disease increases with colony size or density in Black-headed Gulls and Northern Fulmars (J. Fisher, 1952; Jennings and Soulsby, 1958). Hoogland and Sherman (1976) showed that the percentage of Bank Swallow burrows containing at least one flea and the mean number of fleas per burrow in­ creased with colony size; in contrast, the noncolonial Northern Rough-wing­ ed Swallow (Stelgidopteryx serripennis) rarely harbors ectoparasites (Lunk, 1962). Similarly, nestlings of the Red-winged Blackbird, Yellow-headed Blackbird, and several oropendolas are regularly infested by body mites, while those of a noncolonial blackbird, the Bobolink (Dolichonyx oryzivorus), rarely or never are (Smith, 1968; J. F. Wittenberger, personal observation).

44

JAMES F. WITTENBERGER AND GEORGE L. HUNT, JR.

The potential cost of ectoparasite and disease transmission should not be underestimated. While deaths caused by disease or parasitism are rarely identified as such in field studies due to the difficulties of diagnosis, they may commonly result at least in part from these factors. At the very least, disease and severe ectoparasite infestations represent a significant energy drain that could well make the difference between starvation and survival in marginal situations. Ectoparasites occasionally cause nest abandonment (Camin and Moss, 1970) or chick loss (Allen and Nice, 1952) in Purple Martins (Progne subis), and an outbreak of ticks apparently caused mass abandonment of a Sooty Tern colony (Feare, 1976). Ticks have been a cause of breeding failure in Brown Pelicans (Pelecanus occidentalis) (King et al., 1977). In the large seabird colonies off Peru, tick infestations caused up to fifteen percent of nesting pairs to desert, and in individual colonies up to 75% of Peruvian Boobies abandoned their chicks due to outbreaks of ticks (Duffy, 1980). Houston (1979) suggests that tree nesting without nest construction evolved in White Terns (Gygis alba) to prevent ectoparasitism. Ectoparasitism effects could be analyzed by recording frequencies of ecto­ parasite infestations in nests from colonies of different sizes of the same species, or in nests of colonial and noncolonial species in the same habitat. They could also be studied by comparing chick starvation rates among in­ fected and noninfected individuals or broods.

IX. Toward a Synthesis: Temporal Fitness Patterns The net effect of all the factors discussed above must be compiled before the adaptive pressures affecting coloniality can be understood. Such a com­ pilation must take seasonal chronology, colony size, and social status into account. Chronology is important because resource availability, demand for resources, weather conditions, prédation rates, and colony size all vary sea­ sonally. Colony size is important because it influences the rate of resource depletion, intensity of competition for food and preferred sites, degree of potential information transfer, prédation rate, incidence of cannibalism, and colony density, which in turn influences rate of disease and ectoparasite transmission, possibly the extent of cuckoldry and possibly the incidence of chick killing. A true synthesis must consider the net costs and benefits of coloniality in terms of both colony size and (for breeding colonies) seasonal chronology of reproductive activities within colonies.

1. ADAPTIVE SIGNIFICANCE OF COLONIALITY A.

45

OPTIMAL BREEDING CHRONOLOGY

The usual pattern is for individuals or pairs to make independent decisions regarding the initiation of breeding activities. The result is a gradual buildup in colony size until a peak is reached in number of new pairs joining the colony, followed by a tapering off of further recruitment and, finally, a decline in colony size as pairs fail or finish breeding. An important conse­ quence of this typical chronology pattern is that the costs and benefits of coloniality may differ depending on when breeding is initiated. This effect is most likely to occur if the length of the nesting cycle for a given pair is substantially shorter than the length of the breeding season for the colony as a whole. In such cases the advantages to be gained by breeding in colonies may vary seasonally and a temporal component must be added to adaptive explanations of coloniality. In seabirds and some other colonial species, a temporal component adds less to the analysis because the nesting cycle of individual pairs requires most of an entire breeding season. To assess the consequences of coloniality on fitness, one must sum all the net effects discussed above across the period of colony occupancy. This sum may differ for early, peak, and late breeders, since competition, prédation, cuckoldry, and interference effects are all likely to vary during a season. In other words, the net effect of each variable cannot necessarily be investigat­ ed just for the average colony member. It must often be evaluated for colony members as a function of time of breeding. In this analysis, we ignore secondary peaks in the breeding population that may result from renesting attempts or trial attempts at nesting by younger birds breeding for the first time (Massey and Atwood, 1981). The following sections discuss what is presently known about how the net effect of each important variable varies through time.

B.

RESOURCE CHRONOLOGY

Temporal variation in the net energetic effect of coloniality should depend on resource availability, demand for resources, and rate of information trans­ fer. As resources become more abundant, competition relaxes and har­ vesting efficiency increases. As demand for food increases, competition in­ tensity increases and hence foraging efficiency decreases. As rate of informa­ tion transfer increases, ease of finding food and hence harvesting efficiency increases. All three factors are positively correlated with colony size, al­ though the slope of the correlation no doubt differs for each. The two most important factors affecting harvesting efficiency are proba-

46

JAMES F. WITTENBERGER AND GEORGE L. HUNT, JR.

Resource Depletion Curve

Resource Renewal Curve

£,(b)

tt

Time of Season

FIG. 4. When the resource depletion curve is more peaked than the resource renewal curve (a), resource availability peaks early in the season and then declines until relatively late in the breeding cycle (b). Hence early breeders gain an energetic advantage over late breeders.

c— Resource Renewal Curve A Resource Depletion Curve

Renewal Rate >Depletion Rate Renewal Rate= Depletion Rate

Time of Season FIG. 5. When the resource renewal curve parallels the resource depletion curve (a), re­ source availability either increases steadily, remains constant, or decreases steadily, depending on the relative positions of the renewal and depletion curves (b).

1. ADAPTIVE SIGNIFICANCE OF COLONIALITY

47

bly resource availability and resource demand. The net change in harvesting efficiency through time should therefore depend mainly on the rate of re­ source renewal or accretion and the rate of increase in demand. The latter is a direct function of colony size, which increases as the season progresses. A simple model shows three possible patterns of resource chronology. The first possibility is that resource depletion rate is more peaked than resource renewal rate (Fig. 4a). That is, breeding is more seasonal than is predicated by the resource base. The result is that resource availability increases early and late in the season but decreases during peak breeding (Fig. 4b). The second possibility is that the resource depletion rate parallels the resource renewal rate (Fig. 5). Then, resource availability continually increases if depletion rate is less than renewal rate, remains constant if depletion rate equals renewal rate, and continually decreases if depletion rate is greater than renewal rate (Fig. 5). The third possibility is that the resource renewal curve is more peaked than the resource depletion curve (Fig. 6). Then resource availability is lowest early and late, and it peaks during peak breed­ ing (Fig. 6). More complicated versions of these relationships are, of course, possible, but the concepts remain essentially the same. The expected consequences of these patterns on fitness are straightfor­ ward. If the first possibility arises, the net energetic benefit is highest or the net energetic cost is lowest for early and late breeders. The net energetic benefit is lowest or the net energetic cost is highest for pairs breeding at the

Time of Season

FIG. 6. When the resource renewal curve is more peaked than the resource depletion curve (a), food availability peaks relatively late in the breeding season (b). Hence early breeders are at an energetic disadvantage compared to late breeders.

48

JAMES F. WITTENBERGER AND GEORGE L. HUNT, JR. TABLE II RELATIONSHIP BETWEEN THE RELATIVE SHAPES O F THE RESOURCE DEPLETION AND RENEWAL CURVES AND OPTIMUM TIMING O F BREEDING Relationship of resource depletion and renewal curves

Depletion curve more peaked than renewal curve Depletion curve parallels renewal curve, depletion curve higher Depletion curve parallels renewal curve, depletion curve coincident with renewal curve Depletion curve parallels renewal curve, depletion curve below Depletion curve less peaked than renewal curve

Optimum breeding time

Early or late season best Early season best No optimum, all times equal

Late season best Mid-season best

peak of the season. If the second possibility arises, the net energetic benefit steadily increases or the net energetic cost steadily decreases through time when the resource renewal rate is greater than the resource depletion rate. The opposite is true if the resource renewal rate is less than the resource depletion rate. The net effect is constant when resource renewal rate equals resource depletion rate throughout the season. If the third possibility arises, the net energetic cost is highest for early and late breeders. The net energet­ ic benefit is highest or the net energetic cost is lowest in pairs breeding at the peak of the season. These relationships are summarized in Table II. Hunt and Hunt (1976a) examined experimentally the relationship be­ tween chick growth rate, quality of parent (as measured by laying date), and time of breeding (as measured by hatching date) by exchanging eggs be­ tween nests of Glaucous-winged Gulls to provide early breeding adults with late hatching eggs and vice versa. They found no significant correlation between laying date and chick growth rate, suggesting that parental quality (as measured by time of egg laying), had relatively little influence on chick growth. In contrast, chick growth rates were greater for earlier hatched chicks than later hatched chicks, regardless of the date on which the foster parents originally laid their eggs. This result shows that seasonal fluctuations in food affect chick growth and suggests that food was more available earlier in the season. Bédard (1969a) concluded that the breeding season of auklets on St. Law­ rence Island is closely tied to availability of preferred foods. Likewise, Feare (1976), working in the Seychelles Islands with Sooty Terns, found that some of the lower success of late nesting birds was due to seasonal declines in food

1. ADAPTIVE SIGNIFICANCE OF COLONIALITY

49

availability (as judged from lower eggs weights and longer incubation shifts) rather than just the age or experience of the birds themselves. Mills (1973, 1979) found that, for Red-billed (Silver) Gulls (Larus novaehollandiae scopulinus), both egg size and clutch size decreased as the season progressed, at least in part because of decrease in the availability of their main food, euphausiids. Egg size in turn is correlated with hatching success and chick survival (Parsons, 1970; Nisbet, 1973, 1978). While seasonal decreases in clutch size are widespread (due to either decreases in food availability or the age of the birds), there are occasional instances when clutch size increases during the season (Mills and Shaw, 1980). No data are available, however, to show that such increases result from heightened food availability. The fitness consequences predicted above (see Table II) assume that chick survival is directly correlated to the rate at which parents can feed them. They do not incorporate potential long-term consequences resulting from an earlier start in the growing season. Postfledging survival of young has been shown to be influenced by the timing of chick hatching or fledging in Manx Shearwater (Perrins, 1966), Herring Gulls (Nisbet and Drury, 1972), Frank­ lin's Gulls (J. Burger, 1972), and Cape Gannets (Sula capensis) (Jarvis, 1974). Nisbet and Drury (1972) were able to separate timing of hatching from parental quality by causing birds to re-lay, and they suggest that the better survival of Herring Gull chicks that fledge early results from the ability of early chicks to establish and maintain dominance over younger chicks after fledging. Western Gull chicks that fledge early establish foraging territories in prime locations and force newly arriving fledglings into less suitable winter foraging sites (Briggs, 1977). This sort of effect leads to a long-term and more indirect energetic benefit to early breeding, but it should be treated as a separate variable that can be incorporated into more sophisti­ cated models. Net energetic effects should vary through time and must be summed across the entire time span during which an individual or pair occupies the colony. Breeding is not instantaneous, and the net energetic effect must be evaluated across the entire breeding cycle. Length of breeding cycle relative to length of breeding season is an important consideration for such an evalua­ tion. In seabirds the breeding cycle is relatively long (see J. Burger, 1980b), and successful breeders remain in or near colony sites for much of the season, but this is not true of many other colonial birds. Earlier breeding does potentially allow pairs to ameliorate competition for food, but it also exposes them to severe weather (as does late breeding) (Sealy, 1975; Hunt and Hunt 1976a; Ensor 1979). In colonial passerines, length of the breeding cycle is often shorter relative to length of breeding season, which may lead to substantial differences in the net energetic consequences of coloniality for early, peak, and late breeders.

50 C.

JAMES F. WI1TENBERGER AND GEORGE L. HUNT, JR. PRÉDATION

CHRONOLOGY

Prédation rate is dependent on both colony size and seasonal activity patterns of predators. As a general rule, proportional loss to predators de­ creases as the number of nests at risk increases, once a colony becomes large enough to swamp the exploitative capability of all predators in its vicinity. This pattern has been demonstrated for Black-headed Gulls, Common Terns, Sooty Terns, Sandwich Terns, murres, and Red-winged Blackbirds (Patterson, 1965; Kruuk, 1964; Nisbet, 1975; A. J. Williams, 1975; Feare, 1976; Caccamise, 1976; Veen, 1977; Birkhead, 1977b). Fuchs (1977b) found that Sandwich Terns breed earlier in the season when associated with Blackheaded Gulls than when alone, presumably to gain protection from the laternesting gulls. For colonial birds that synchronize breeding, prédation risk is lowest during peak breeding. Colony size at any given time depends partly on the extent to which breeding activities are synchronized among colony members. The relationship between chronology of breeding events in a colony and predator breeding activity is not well studied. For the most part, predators should breed when food is more available, so hunting activity of predators should parallel the breeding chronology of their prey. In some cases, howev­ er, external constraints may cause predators to breed out of phase with colony activity. For example, marsh-breeding blackbirds begin breeding relatively early in the spring, before temperatures are warm enough for snakes to become active. Snake prédation increases as the season progresses, causing late nesters to be affected more by snakes than early nesters (C. Monnet, unpublished data). The fitness consequences of predator activity through time are clear for average colony members. When predator activity parallels colony activity the net benefit derived from predator defense is typically greater, on aver­ age, for pairs breeding at the peak and lowest for pairs breeding earlier or later. When predator activity peaks earlier than colony activity, early or late breeders are at a disadvantage or advantage, respectively. If colony size never reaches the point where it swamps the exploitative capabilities of predators, the benefit of nesting in an inaccessible site rather than dispersing and relying on concealment should be inversely related to colony size (due to density-dependent prédation effects), provided that shortages of nest sub­ strate do not preclude dispersing. The benefit derived from mobbing ac­ tivities should be positively related to colony size or density. D.

CHICK KILLING CHRONOLOGY

The net effect that chick killing has on fitness as a function of time depends on the form of chick killing that occurs. The loss rate (per nest) to can-

1. ADAPTIVE SIGNIFICANCE OF COLONIALITY

51

nibalism is highest for early and late breeders in Herring Gull and Carrion Crow colonies and is lowest during peak breeding (Harris, 1964; R. G. B. Brown, 1967; Parsons, 1971, 1975; Yom-Tov, 1975). The pattern is the same for both egg and chick losses (Yom-Tov, 1975). The loss rate due to killing of trespassing chicks is highest during peak breeding and lowest for early breeders in Herring Gulls, California Gulls, and Ring-billed Gulls (Paynter, 1949; Vermeer, 1970). In Lesser Black-backed Gulls, however, the rate of chick killing (per nest) appears lowest during peak breeding, particularly for birds breeding in cover (R. G. B. Brown, 1967). When nesting cover is sparse, late nesting birds do progressively less well (R. G. B. Brown, 1967). J. Burger (1980a) argued that synchronization of local subcolonies of groundnesting Herring Gulls will result in reduced chick killing by neighbors be­ cause pairs in the same stage of the reproductive cycle as their neighbors are less likely to eat eggs or kill chicks. Fetterolf (1984) developed a similar model based on observations of Ring-billed Gulls, in a colony undisturbed by observer intrusion (Fetterolf, 1983). Synchrony is important because territory size and modes of defense change over the course of the reproduc­ tive cycle. Cannibalism apparently has its greatest impact early and late because most attacks are attributable to relatively few individuals, most of whom are present at the colony (if not actually breeding) throughout the season (Par­ sons, 1971). The number of chicks cannibalized therefore remains relatively constant, with the result that a decreased proportion of chicks are taken as colony size becomes larger. This conclusion is based on only one study, however, and further data are needed to determine how general the pattern is. The more frequent killing of chicks during peak breeding may reflect intensified competition for resources, although it could be due partly to higher nest densities. Killing of intruding chicks is associated with nutrition of killed chicks (Hunt and Hunt, 1976a) and nesting density (i.e., territory size) (Hunt and Hunt, 1975, 1976a; J. Burger, 1980a; Ewald et al, 1980). Hunt and McLoon (1975) showed that unfed Glaucous-winged Gull chicks wandered further from their parents and were attacked more frequently by neighbors than were recently fed chicks. In addition, the mortality rate stemming from chick killing is higher in years of low food availability than in years of high food availability (Hunt and Hunt, 1976a). The incidence and type of chick killing is highly variable, and chick killing is important only for some colonial birds (notably gulls and skuas). Its fre­ quency not only varies with season, but also from colony to colony and year to year. Hence generalizations about its effect on fitness cannot be made. Essentially, cannibalistic chick killing has the same effect as prédation. That is, it makes synchronous breeding at the peak of the season more advan­ tageous and early or late breeding less advantageous. Killing of intruding

52

JAMES F. WITTENBERGER AND GEORGE L. HUNT, JR.

chicks from neighboring territories has the opposite effect. It makes early or late breeding more advantageous than breeding at the peak.

E.

CHRONOLOGY O F CUCKOLDRY

Little is known about the incidence of cuckoldry. However, a number of predictions can be made. As a general rule, cuckoldry should become in­ creasingly prevalent as the season progresses because males become more prone to seek extra-pair copulations once their own mates have begun laying (see MacRoberts, 1973; Mineau and Cooke, 1979). Early in the season, males are less likely to be cuckolded because they are very attentive of mates (Power et al., 1981) and because most males, other than subadults, are preoccupied with mates of their own. Data for Lesser Black-backed Gulls generally support this prediction (MacRoberts, 1973); extra-pair courtships that terminated in mounting were most prevalent during and after the breeding peak and were less prevalent early in the season. In contrast, males of noncolonial European Starlings (Sturnus vulgaris) delay breeding appar­ ently as a mechanism to avoid being cuckolded (Power et al., 1981). Knowlton (1979) argued that breeding synchrony is a female sexual strat­ egy for ensuring male investment in offspring by minimizing chances for cuckoldry (see also Maynard Smith, 1977; Rails, 1977; Emlen and Oring, 1977). While females probably are less likely to mate outside the pair bond before or during the breeding peak, other explanations can be advanced to explain such a pattern. For instance, fewer males are likely to be seeking extra-pair copulations at those times because more males are preoccupied with their own mates. No evidence to date indicates that males of early or peak-breeding pairs are any more prone to provide parental investment than males of late pairs. Indeed, while confidence of paternity may be higher for early or peak-breeding males, opportunities for cuckolding later breeders are also higher. Exploiting such opportunities could make early and peakbreeding males less prone to providing parental care despite their higher confidence of paternity. Risk of cuckoldry could help explain local breeding synchrony within large colonies, as occurs in Magnificent Frigatebirds (Fregata magnificens) (Nelson, 1967c), White Pelicans (Behle, 1944; Schaller, 1964), Herring Gulls (Paynter, 1949; Parsons, 1976) Brown-hooded Gulls (J. Burger, 1974a), Swallow-tailed Gulls (Creagrus furcatus) (Hailman, 1964; Snow and Snow, 1967; Nelson, 1968), Sooty Terns (Feare, 1976), Sandwich Terns (Veen, 1977), Black Skimmers (Gochfeld, 1978a), Cliff Swallows (Emlen, 1952), Bank Swallows (Hoogland and Sherman, 1976), Village Weaverbirds (Hall, 1970), and Tricolored Blackbirds (Lack and Emlen, 1939; Orians, 1960). If

1. ADAPTIVE SIGNIFICANCE OF COLONIALITY

53

cuckoldry mainly involves nearby territorial males, as has been shown for Red-winged Blackbirds (Bray et al., 1975), it could be minimized by syn­ chronizing courtship with neighboring pairs. Local synchrony may be en­ hanced by a variety of contagious displays, such as copulatory calls and wingflagging (Horn, 1970; Southern, 1974; Gochfeld, 1978b). When the entire colony cannot breed synchronously because not every individual is ready to breed at the same time (see Section IX, F), local synchrony should be great­ est in species in which the proclivity for cuckoldry is greatest.

F.

CHOICE O F BREEDING TIME

The net effect of all factors affecting fitness at any given time depends on how many individuals begin breeding at that time. Therefore, a temporal analysis of fitness effects depends on how individuals choose when to breed. Theoretically, these choices should be made such that breeding is initiated at the point where higher fitness cannot be attained by delaying the start to a later date. Two factors are important here: the degree of success attainable by an individual in peak physiological condition at each point in time and the degree to which individuals are in peak physiological condition. In ideal circumstances when all individuals are in peak condition at the time breeding first becomes feasible, the temporal pattern of breeding starts should result in constant fitness among all individuals who start breeding before or during the breeding peak. The argument is similar to the ideal free habitat distribution model of Fretwell and Lucas (1969), except that indi­ viduals must compare present breeding prospects to predicted future pros­ pects and cannot sample options before making a choice. Under less than ideal conditions, fitness among early and peak breeders may or may not be constant, depending on how many pairs are physiologi­ cally ready to start breeding at each time. If physiological constraints affect enough pairs, not all pairs can breed at the optimal time and early breeders should attain higher fitness than later breeders. The main physiological constraint is the nutritional condition of potential breeders at the end of the nonbreeding season. Food is probably scarcer early in the season, and the ability of many females to begin nesting may depend on how much energy they can allocate to egg production. A second important constraint, at least for many seabirds, pertains to the success or failure of reproductive efforts the previous year, along with the survival of both birds of a pair to the next year. In many species, breeding is earlier when the same individuals remain paired from the previous year, and that is predicated in turn on successful breeding that year. Individuals who breed with new mates have no experience together and hence do not breed as

54

JAMES F. WITTENBERGER AND GEORGE L. HUNT, JR.

successfully as intact pairs, at least early in the season (Coulson, 1966, 1972; Nelson, 1966, 1972; Wood, 1971; Mills, 1973; Davis, 1976; Brooke, 1978; Ollason and Dünnet, 1978).

G.

MODELS O F TEMPORAL FITNESS VARIATIONS

A number of models can be devised to show how the net effect of all costs and benefits associated with coloniality should change through time. The models discussed here are restricted to the net effects stemming from ener­ getic considerations and prédation. We propose two models: first, a simple, single-variable model based on energetic effects alone, and second, a more complicated two-variable model. Each model is based on the assumption that every pair chooses the optimal time to breed. Hence, the fitness curves are drawn such that fitness remains constant until after the peak of the season has been reached. In the first and simplest model, only energetics is assumed to be impor­ tant. Given that assumption, the net effect of energetics should lead to a flat or decreasing fitness curve, as shown in Fig. 7. Moreover, the net energetic effect must be positive because otherwise coloniality could not be adaptive. For these conditions to hold, food resources must be harvested as fast or faster than the resource renewal rate (cf. Figs. 4 and 5). Otherwise, food availability would increase as the season advances and late breeders would achieve higher fitness than early breeders (cf. Fig. 6). The net energetic effect at each time of season can be positive either through geometrical advantages in travel distance (Horn, 1968) or through information transfer (Ward and Zahavi, 1973; Gaston and Nettleship, 1981). In the second model, net prédation effect is added to net energetic effect to obtain a combined effect (Fig. 8). The net energetic effect is drawn so that Peak of Season

1 Energetics A

Energetics B Time of Breeding Start

FIG. 7. When energetics is the main factor affecting fitness, the net effect of energetics must be positive for coloniality to evolve, and it should be constant through the breeding peak (curve A). If physiological constraints prevent many individuals from breeding early, the net effect should lead to decreasing fitness through the breeding season (curve B).

1. ADAPTIVE SIGNIFICANCE OF COLONIALITY

55

Breeding Peak

Time of Season

FIG. 8. If fitness of breeders is constant through the breeding peak, and the net prédation effect is greatest at the breeding peak, the net energetic effect must decline until after the breeding peak.

the combined effect of prédation and energetics on fitness is constant through the breeding peak, but it could have been plausibly drawn so that the combined effect on fitness steadily decreases through time. The relative positions of the two curves should be as shown in either case. The curve shown in Fig. 8 for the net energetic effect approximates that shown in Fig. 6B, suggesting that resource depletion should be more peaked than resource renewal when swamping or mobbing of predators is an important benefit of coloniality. A still more complicated model could be drawn to incorporate the effect of chick killing or other variables. No new insights, however, are gained by doing so here. Suffice it to say that inclusion of cannibalism would require a steeper decline in the net energetic effect in order for fitness to remain constant or decrease through the season. Conversely, inclusion of chick killing in territorial contexts would require a less steep decline in the net energetic effect for fitness to remain constant or decrease through time. The models presented here are theoretical in nature, but they can be adapted to field situations by changing the label on the vertical axes from fitness effect to percent of chicks surviving each type of mortality agent. Conversely, mirror-image curves could be drawn to show expected chick mortality patterns with respect to each mortality agent as a function of time. One could then test the hypothesis that decreased prédation on chicks is offset by increased starvation or chick killing and vice versa. The expected result should be constant chick survival rates or gradually decreasing chick survival rates through the breeding peak. A peak in chick survival rates midway through the season should not occur unless early breeders can benefit from multiple breeding attempts or opportunities to renest following failure.

56 H.

JAMES F. WITTENBERGER AND GEORGE L. HUNT, JR. FRASER DARLING E F F E C T

As can be seen from the above analysis, increased breeding synchrony is sometimes advantageous and sometimes not. In species where the former condition generally prevails, one might expect proximate mechanisms that promote greater synchrony to occur. Fraser Darling (1938) was the first to propose that social stimulation serves such a purpose, but the evidence for his hypothesis is mostly indirect and mostly inconclusive (Fisher, 1954; Collias et al., 1971). It involves direct observation of contagious spread of courtship activity in gull colonies (R. G. B. Brown, 1967; Southern, 1974) and a variety of correlations between nesting synchrony and colony size or density (Coulson and White, 1960; Hall, 1970; MacRoberts and MacRoberts, 1972; Veen, 1977; J. Burger, 1979a; Montevecchi et al, 1979; Birkhead, 1977b, 1980; reviewed by Gochfeld, 1980). Interpretation of these condi­ tions is made ambiguous, however, by possible uncontrolled effects of en­ vironmental stimulation (Hall, 1970), age, and/or geographical hetero­ geneity in the data set. Orians (1961b) was unable to find evidence of social stimulation in Tricolored Blackbirds and concluded that timing of breeding was controlled by the nature of the marsh colony site and not by the size of the breeding population. Similarly, Snapp (1976) found that the degree of breeding synchony of Barn Swallows was determined by weather and was unrelated to colony size. Burger (1979a) showed that synchrony (as defined by a decrease in the standard deviation of laying date) increases with colony size only up to about 200 pairs, after which synchrony is only evident at the subcolony level (Paynter, 1949; Feare, 1976; Veen, 1977; Gochfeld, 1977, 1978a, 1980). In Herring Gulls these subcolonies originate as separate epi­ centers of nesting (Burger and Shisler, 1980). Some experimental evidence shows that the presence of other conspecifics outside the pair bond acceler­ ates ovulation in females (Brockway, 1964; Lehrman, 1965; Lott et al., 1967; Erickson, 1970). The presence of conspecifics may also serve as social attractants for nesting habitat selection (Klopfer and Hailman, 1965). The main significance of the Fraser Darling effect, aside from its physio­ logical interest, is that it suggests the existence of positive selection for more synchronous breeding, above and beyond that predicated by seasonal timing of resource availability and weather conditions. It should be realized, how­ ever, that not all individuals necessarily stand to benefit from more syn­ chronous breeding, even in species where the Fraser Darling effect is important. Many individuals may be most successful by breeding early, which may or may not be promoted through social stimulation. In such cases, mechanisms may exist to allow early breeding in the absence of social stimulation. Other individuals may be most successful by not breeding early, even if they are capable of doing so. Mechanisms should therefore exist for

1. ADAPTIVE SIGNIFICANCE OF COLONIALITY

57

allowing deferred breeding. To date, no such mechanisms have been sought or reported. In summary, the physiological mechanisms associated with initiation of breeding should be designed to facilitate breeding at the best possible time.

X.

Conclusion

The adaptive significance of avian coloniality is not yet understood. A variety of hypotheses have been adduced to explain why coloniality evolves, but to date the evidence available for testing those hypotheses is at best incomplete. Many of the more important predictions arising from each hy­ pothesis have been tested barely or never, and much of the evidence brought forth in support of particular hypotheses is equally supportive of several alternative hypotheses. This circumstance has been true particularly with regard to predictions made about food distribution patterns, as several different models predict that coloniality should be associated with spatiotemporally clumped food resources. Such evidence has little value in dis­ tinguishing between alternative hypotheses, and yet evidence on food dis­ tribution represents the main basis of support for some of the energetic models. No single hypothesis is likely to provide a general explanation of avian coloniality. Breeding and roosting colonies have both evolved in a wide variety of circumstances and probably for a variety of different reasons. Our task should therefore be concerned with delineating different forms of colo­ niality, with each being associated with a distinctive set of selective factors. Some colonial systems, for example, may have evolved primarily because they allow individuals to harvest resources in the most efficient possible manner (e.g., the geometrical model). Others may have evolved to facilitate food finding through information transfer. Still others may have arisen in response to habitat shortages or because nesting or roosting in a few rela­ tively safe habitat patches is the best defense against prédation, given pre­ vailing local population densities. These different forms of coloniality need to be distinguished, and the common ecological denominators underlying each need to be identified. At present, relatively few patterns are clear. Seabird colonies may have evolved at least in part as a response to limited nest site availability and perhaps in some species also as a means for facilitating food finding. Large breeding and roosting colonies of landbirds may well have evolved as a superior defense against prédation, but the evidence is not yet conclusive. Smaller colonies have quite possibly evolved to allow more efficient foraging

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JAMES F. WITTENBERGER AND GEORGE L. HUNT, JR.

or to facilitate information transfer. Most of these suppositions are not firmly established, however, and empirical tests of every hypothesis are still needed across the entire spectrum of colonial species. Post hoc explanations of evidence will remain unsatisfactory. Two important aspects of coloniality are degree of spatial packing and degree of breeding synchrony. More detailed analysis is needed regarding the factors that predispose individuals to nest closer together or farther apart. The same is true of factors predisposing individuals to breed more or less synchronously. Of particular importance here is the need to evaluate how the effect of each mortality agent varies through the course of a breed­ ing season. The costs and benefits of coloniality vary with both nesting density and breeding time, and hence they will not be fully understood until density effects and temporal variations in mortality are adequately taken into account. Avian coloniality is not a simple or unitary phenomenon. Breeding and roosting colonies are obviously organized differently, though a common body of theory potentially applies to both. Not all breeding colonies are adaptive for the same reasons, and the same can be said for roosting colonies. Finer distinctions between the various forms of coloniality will need to be made before the adaptive significance of avian coloniality can be truly understood. ACKNOWLEDGMENTS We thank T. Birkhead, M. Harris, J. Hoogland, J. King, W. Koenig, I. Nisbet, and A. Zahavi for helpful suggestions on earlier drafts of this chapter. Zoe Eppley and Barbara Braun provided invaluable bibliographic aid. K. C. Parkes and Z. Eppley edited the manuscript. J. Farmer, P. McDonald, and Z. Eppley typed the several drafts of the manuscript, and Karin Christiansen drafted the figures. REFERENCES Ainley, D. (1975). Displays of Adélie Penguins: A reinterpretation. In "Biology of Penguins" (B. S. Stonehouse, ed.), pp. 503-534. University Park Press, Baltimore. Ainley, D., and Lewis, T. (1974). The history of Farallon Island marine bird populations, 18541972. Condor 76, 432-446. Alcock, J. (1969). Observational learning in three species of birds. Ibis 111, 308-321. Aldous, C. M. (1941). Report of a wholesale die-off of young Herring Gulls at Hogback Island, Moosehead Lake, Maine. Bird-Banding 12, 30-32. Alexander, R. D. (1974). The evolution of social behavior. Annu. Rev. Ecol. Syst. 5, 325-383. Allen, R. P. (1956). "The Flamingos: Their Life History and Survival." National Audubon Society, New York. Allen, R. W., and Nice, M. M. (1952). A study of the breeding biology of the Purple Martin (Progne subis). Am. Midi. Nat. 47, 606-665. Altmann, S. A. (1956). Avian mobbing behavior and predator recognition. Condor 58, 241-253.

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