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The Evolution of Helping. I. An Ecological Constraints ModelAuthor(s): Stephen T. EmlenSource: The American Naturalist, Vol. 119, No. 1 (Jan., 1982), pp. 29-39Published by: The University of Chicago Press for The American Society of NaturalistsStable URL: http://www.jstor.org/stable/2460654 .

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Vol. 119, No. 1 The American Naturalist January 1982

THE EVOLUTION OF HELPING. I. AN ECOLOGICAL CONSTRAINTS MODEL

STEPHEN T. EMLEN*

Center for Advanced Study in the Behavioral Sciences, Stanford, California 94305

Submitted January 10, 1980; Revised March 17, 1981; Accepted May 1, 1981

Cooperative breeding in birds and mammals refers to situations where adult individuals forego breeding and assist others in the care and rearing of young. Such helping behavior has been reported in more than 150 species of birds and approxi- mately 25 species of mammals and the number is increasing rapidly as studies based on individually marked animals are expanding. Explanations of such cooperative behavior are of importance, not merely because of the general interest in the phenomenon, but because cooperative behavior poses an apparent evolutionary dilemma since helpers appear to behave in a way that increases the fitness of recipients (breeders), but may incur a cost to themselves.

Attempts to relate the occurrence of helping behavior to ecological correlates, and thereby to identify environmental selective pressures important in the evolution of cooperative behavior, have been largely unsuccessful. Most investigators (whom I refer to as the K-selection school) have noted that many cooperative breeders are sedentary throughout the year and inhabit areas showing a high degree of environmental stability and predictability (e.g., Brown 1974; Woolfenden 1975; Ricklefs 1975). Other workers (whom I call the variable environment school) have been impressed by the fact that other cooperatively breeding species, including many in Australia and Africa, inhabit harsh, fluctuating, and highly unpredictable environments (Rowley 1968, 1976; Grimes 1976). This poses a paradox: Why do similar social organizations occur in such seemingly opposite ecological situations? As the number of species known to exhibit cooperative behavior has increased in recent years, so too has the spectrum of ecological conditions under which they have been found. Helpers at the nest among birds occur in species residing in deserts, scrub, heathlands, wetlands, savannah, and forestlands (Row- ley 1976). Given this diversity of habitat conditions, it is not surprising that most recent workers have echoed Fry (1972, p. 12) who stated that cooperative breeders "comprise a very mixed bag ecologically," or Rowley (1976, p. 665) that "no one set of circumstances has led to the parallel evolution of cooperative breeding in birds."

In this manuscript I hypothesize that there is a common thread underlying most

* Permanent address: Division of Biological Sciences, Cornell University, Ithaca, New York 14853. Am. Nat. 1982. Vol. 119. pp. 29-39. ? 1982 by The University of Chicago. 0003-0147/82/1901-0004$02.00. All rights reserved.

29



30 THE AMERICAN NATURALIST

instances of cooperative breeding. I assume that each nonbreeding individual assesses the costs and benefits of two, alternative, strategies: either dispersing and breeding independently, or remaining at home and helping rear additional offspring (usually siblings). Under most conditions, selection favors the former option. This follows from the fact that two individuals (the disperser plus its mate) normally can rear more young than can one (the disperser alone, acting as a helper; see Charnov, in press). In certain instances, however, the option of personal reproduction cannot be realized because the costs associated with independent establishment and breeding are prohibitively high. Selander (1964), Brown (1974), and Koenig and Pitelka (1981) have hypothesized that in stable environments, breeding options are restricted by a shortage of high quality breeding territories. I propose that an analogous restriction is placed upon breeding in variable environments. This restriction is a consequence of the frequent occurrence of adverse conditions that temporarily magnify the level of parental investment (Trivers 1972) necessary for successful breeding. When the option of personal reproduction is sufficiently restricted (for either of the reasons mentioned) individuals will be "forced" to remain as nonbreeders with their natal groups.

Whether or not such nonbreeding auxiliaries will participate as helpers in the breeding activities of the group will depend upon the costs and benefits of such aid giving, measured from the viewpoints of both breeder and helper (see Emlen 1982).

AN ECOLOGICAL CONSTRAINTS MODEL OF COOPERATIVE BREEDING

A necessary first step in the development of a familial cooperative social structure is the retention of grown offspring in the parental unit (Brown 1974; Gaston 1978b). Under what conditions should an offspring remain at home? This question can be rephrased (from the offspring's point of view) in terms of the relative costs and benefits of two opposing options: (1) dispersing and attempting to breed independently, or (2) postponing departure and remaining as a nonbreeder with the parental group.

At least four factors will enter into this decision: the cost (risk) of dispersal itself; the probability of successful establishment on a suitable territory (area) following dispersal; the probability of obtaining a mate; and the likelihood of successful reproduction once "established." The first factor, measurable as the difference in survival probabilities of early (p') versus late (p) dispersers, depends upon the relative accessibility of food and shelter, and the pressure from predators and competitors in the habitats available to dispersing and resident individuals, respectively. The second and third factors, which can be pooled into a single probability of becoming established as a breeder (4'), are strongly influenced by the intensity of competition for suitable areas and/or mates. Such competition, in turn, is dependent upon the population density, the number and turnover rate of territory vacancies, and the population operational sex ratio. The fourth factor, the success of the breeding attempt itself, depends upon the degree of difficulty of rearing young (measured as N, the number of young successfully produced). The fitness (WA) of a grown offspring attempting to breed in its first year thus is a function of the product, qp N.



ECOLOGICAL CONSTRAINTS OF HELPING 31

TABLE 1

ECOLOGICAL CONSTRAINTS SEVERELY LIMIT ANY POSSIBILITY OF PERSONAL REPRODUCTION

Type of constraint Cause of constraint

1. Breeding openings are nonexistent ....... Species has specialized ecological requirements; suitable habitat is "saturated" and marginal habitat is rare (stable environments)

2. Cost of rearing young is prohibitive ...... Unpredictable season of extreme environmental harshness (fluctuating, erratic environments)

Result: Grown offspring postpone dispersal and are retained in the parental unit. The population becomes subdivided into stable, social, kin groups.

When the risks of dispersal are minimal, mates and territories are plentiful, and initial breeding success is high, the likelihood of early dispersal is increased, and the establishment of familial social units (with or without cooperative rearing of young) should be rare. Conversely, when the risks of dispersal are high, the chances of mate acquisition or territory establishment are low, and initial reproductive success is poor, offspring will be selected to postpone dispersal, to remain at home, and to integrate with the parental group (table 1).

One might assume that a grown offspring should attempt to reproduce whenever WA > 0. An auxiliary that postpones breeding, however, may enhance its lifetime fitness through the accumulation of delayed benefits that result in higherp, 4i, and N values later in life.

For example, by continuing to reside in the security of an area of proven territory quality, it may increase its probability of surviving to the following breeding season. Regardless of the specific ecological factors of importance for the species, survival in an established breeding area probably will exceed that in the unoccupied, marginal areas available to dispersing individuals.

A resident auxiliary also may increase its chances for establishment as a breeder in the future. This can come about in several ways. First, the additional maturity and experience gained while a resident can improve the auxiliary's social status, making it better able to compete for mates and/or territories. Second, an auxiliary may form social bonds with other members of its natal group that lead to enhanced chances of takeover of territories. This benefit occurs in species where subgroups (usually siblings) disperse together and are better able to compete for high quality territories than are single individuals (e.g., Tasmanian native hens, Tribonyx mortierrii [Ridpath 1972]; Jungle babblers, Turdoides striatus [Gaston 1978a]; green woodhoopoes, Phoeniculus purpureus [Ligon and Ligon 1978]; helmut shrikes, Prionops plumata [Vernon, cited in Brown 1978]; acorn woodpeckers, Melanerpes formicivorus [Koenig and Pitelka 1981]). Analogous benefits may occur in lions, Panthera leo (Bertram 1975; Bygott et al. 1979) and African wild dogs, Lycaon pictus (Frame et al. 1979). Third, a nondispersing resident stands the chance of obtaining part or all of the parental territory, usually at the time of the death of one of the parents (the territorial inheritance model of Woolfenden and Fitzpatrick [1978]; the patrimony factor of Gaston [1978b]).

In addition to these beneficial effects upon future qP, a resident offspring also may increase its N as a future breeder. This would occur primarily as a result of




any helping experience gained while a member of its natal group. (Note, however, that a yearling that does become established as a breeder, even if unsuccessful in its breeding attempt, also will gain in experience and maturity.)

On top of this, a nonbreeder may gain an increment in its inclusive fitness if it acts as a helper in raising young that are close genetic relatives.

Thus we must consider the long-term trade-offs of early initial dispersal, with its lower chance of successful establishment and reproduction, against the post- ponement of dispersal with its possible compensating benefits for later reproduction. Retention of grown offspring in the natal unit will be favored when p >> p', initial (yearling) WA is extremely low, and/or when WA increases rapidly with age and experience.

Such situations are expected to be rare, and philopatry (remaining at home) should occur only when the option of early personal reproduction is severely constrained. Cooperative, familial social organizations are predicted to occur (1) during harsh years in variable and unpredictable environments (the result of a low N), and/or (2) under intense intraspecific competitive pressures in stable environments (the result of a low 4i). In essence, an individual will remain as a helper in its natal unit only when it is "forced" to do so by the prohibitive costs of the alternative option of early dispersal and independent breeding.

ECOLOGICAL CONSTRAINTS IN STABLE, PREDICTABLE ENVIRONMENTS

Most cooperative breeders reside in warm temperate, subtropical, or tropical areas. Many are sedentary, and inhabit stable, predictable environments. Further, many have specific ecological requirements such that suitable habitat is restricted, and marginal habitat is scarce (Brown 1978; Koenig and Pitelka 1981). As population numbers increase, suitable habitat becomes filled or "saturated." Unoc- cupied territories are rare, and territory turnovers are few. As the intensity of competition for space increases, fewer and fewer individuals are able to establish themselves on quality territories. The option of breeding independently becomes increasingly limited.

This hypothesis, that habitat saturation provides the primary impetus for philopatry, and through it for the evolution of group territoriality and cooperative breeding, was first formulated in detail by Brown (1974) and later expanded by Brown (1978), Gaston (1978b) and Koenig and Pitelka (1981). It has been voiced by numerous field workers, and has become the modus operandi for ecological thinking concerning the evolution of helping behavior (Selander 1964; Ridpath 1972; Zahavi 1974, 1976; Woolfenden 1975, 1976; MacRoberts and MacRoberts 1976; Ligon and Ligon 1978; Stacey 1979; Trail 1980; Koenig and Pitelka 1981).

The general pattern that is emerging from field studies of cooperative breeders in saturated environments is one of severe competition for territory vacancies. Initial breeding options are constrained because q/ is low. A new individual can become established only (1) when it challenges and defeats a current breeder on an occupied territory, (2) when it competes to fill a vacancy that results from the death of a nearby breeder, or (3) when it buds off or inherits a portion of the parental territory itself (Woolfenden and Fitzpatrick 1978; Gaston 1978b). The




nonbreeder must wait until it attains sufficient age, experience, and status to enable it to obtain and defend an independent territory. Such waiting is best done at home, on an area of proven quality, and in the company of close kin.

A parallel argument can be made emphasizing the shortage of sexual partners rather than spatial territories. Many species of cooperatively breeding birds have a skewed tertiary sex ratio, with an excess of males (e.g., Rowley 1965; Fry 1972; Ridpath 1972; Dow 1977; Douthwaite 1978; Reyer 1980). The reason for such skewing is poorly understood, but its effect is to increase competition for mates, again leading to a lowering of 4i. Although I personally feel that sex ratio argu- ments offer only a partial explanation for the evolution of helping (they bypass the major question of the determinants of the sexual imbalance), they easily are accommodated into the framework of an ecological constraints model.

The model predicts that philopatry and helping should be common when values of WA for yearling birds are low. In stable environments, where N is quite high once an individual becomes established as a breeder, the frequency of occurrence of helpers should vary inversely with 4i. To date, this has been examined for only one cooperatively breeding species, the acorn woodpecker, Melanerpes formicivorus. Studies of its behavior and ecology have been conducted in coastal California, in New Mexico, and in two areas of Arizona. These sites provide a gradient of acorn woodpecker density, territory turnover rates, and territory fidelity. Coastal California provides an example of extreme habitat saturation and high intraspecific competition for territories, with no territory vacancies occurring during the 3 yr of MacRoberts and MacRoberts' study (1976). The Magdalena Mountains of New Mexico and the Chiricahua Mountains of Arizona represent areas with somewhat lower levels of habitat saturation; at the New Mexico site, 19% of territories became vacant during a 3-yr study (Stacey 1979), while in the Chiricahuas, woodpecker density was only half that of the California site, and the territory size per breeding unit was correspondingly higher (Trail 1980). The final study site in the Huachuca Mountains of southeastern Arizona showed no habitat saturation; only 7% of territories remained occupied throughout the year, the most birds dispersed or migrated between breeding seasons (Stacey and Bock 1978). The pattern of occurrence of helping parallels this geographic gradient of de- creasing constraints upon territory establishment. In California, average adult group size was 5.1, 49% of juveniles were retained in their natal units as yearlings, and 70% of groups had helpers. In New Mexico and the Chiricahuas, average group size was 3.0 and 2.8, respectively, only 29% of juveniles remained with their natal groups (New Mexico), and the percentage of breeding groups with helpers was 59% and 56%, respectively. In the Huachuca Mountains, virtually all of the juveniles, and most of the adults dispersed; the average group size was 2.2 and only 16% of the breeding units had a helper (MacRoberts and MacRoberts 1976; Stacey and Bock 1978; Stacey 1979; Trail 1980).

Hints of an analogous trend, in this case with helping being proportionately related to intraspecific competition for mates, is found in the data of Rowley for the superb blue wren, Malurus cyaneus, of Australia (Rowley 1965). Helpers were more frequent in years when the population sex ratio was most skewed (analyzed by Emlen 1978, pp. 257-259). These correlations are consistent with the predic-




tion of the model. However, additional comparative and manipulative field work is needed to investigate the causal relationships of these factors.

ECOLOGICAL CONSTRAINTS IN FLUCTUATING, UNPREDICTABLE, ENVIRONMENTS

Researchers working in arid areas of Australia and Africa, where rainfall is variable and often unpredictable, have commented upon the high incidence of cooperative breeding among avian species in these areas (e.g., Rowley 1965, 1968, 1976; Harrison 1969; Grimes 1976). No unifying model has been presented to explain the retention of young and the evolution of helping in such species.

In long-term studies of superb blue wrens (Malurus cyaneus) and white-winged choughs (Corcorax mnelanorhamphus) in southeastern Australia, Rowley (1965, 1978) interpreted the presence of helpers as an adaptation to the widely varying climate. A similar conclusion was reached by Fry (1972) studying red-throated bee-eaters (Merops bullocki) in northern Nigeria, and by Parry (1973) observing kookaburras (Dacelo gigas) in Australia. They each came to a group-selection interpretation that the presence of helpers allowed the population to increase rapidly during favorable years, while buffering the population from rapid decline during periods of harshness.

A recent survey of cooperatively breeding avian species in Australia revealed that 42% were nomadic, rather than holding any permanent territories (Rowley 1976). Among African bee-eaters and kingfishers, some species are cooperative breeders but do not nest on group territories, rather breeding in dense aggrega- tions or colonies (Fry 1972; Douthwaite 1978; Reyer 1980; Emlen 1981; S. T. Emlen and N. J. Demong, MS). For all of these species, environmental unpredict- ability (especially erratic patterns of rainfall with their resultant effects upon food and cover) preclude the attainment of any steady-state population whose density remains at, or accurately tracks, the carrying capacity. We cannot speak in terms of habitat saturation, or cite a shortage of nest sites or territory openings as a driving factor in the evolution of helping. I believe, however, that we still can speak in terms of constraints upon breeding options.

The ecological constraints model emphasizes ecological factors that limit the option of independent reproduction. In a stable environment, we saw that habitat saturation leads to low values of 4i. In an erratic and unpredictable environment, it is the occasional harsh breeding seasons with their high costs of reproduction (low N), and not difficulties in obtaining territories or mates, that usually lead to the retention of helpers.

Whenever ecological conditions change markedly from year to year, very different amounts of parental (or group) effort may be required to rear successfully young in different seasons. N will vary greatly from year to year, mirroring the changing degrees of difficulty of independent breeding. I propose that an auxiliary living in a variable environment will behave as if assessing both P and N each season, before either remaining with its parental group or splitting off and attempting breeding on its own.

Again, the model predicts that philopatry and helping should be common when values of Wl are low. But, unlike the situation mentioned in the previous section,




helper frequency in species residing in erratic, unpredictable, environments should vary inversely with N. Furthermore, intraspecific variation in helper frequency should be greater, both between years and between locations, in species residing in variable environments.

The first prediction can be tested with an example drawn from our ongoing studies of white-fronted bee-eaters (Merops bullockoides) in Kenya. This species inhabits the savannahs and scrub-grasslands of the Rift Valley of east and south- ern Africa, and is both a cooperative and a colonial breeder. Bee-eaters are insectivorous, and appear to time their breeding to coincide with periods of insect abundance (Fry 1972; S. T. Emlen and N. J. Demong, unpubl. data). Insect abundance, in turn, is influenced by rainfall (Owen 1969; Dingle and Khamala 1972). A mechanism of timing breeding to the rains would lead to high reproductive success in areas with regular or predictable rainfall cycles. The Rift Valley of Kenya, however, is not such an area. There is tremendous year to year variation, both in the timing and in the amount of rain that falls (Brown and Britton 1980). Furthermore, the pattern of response of insect abundance to rainfall is complex, and may differ between long- and short-seasonal rains (Emlen et al., unpublished data).

If Merops bullockoides is adopting a strategy of breeding with the rains, many such breedings are unsuccessful as the rains come late or fail to materialize. Many reproductive attempts are unsuccessful and losses due to nestling starvation can be extremely high (Emlen and Demong, in press). Thus the cost of the option of personal reproduction varies considerably from year to year.

Do bee-eaters show the predicted relation between helper frequency and breeding difficulty? I tested this by examining the relationship between the frequency of occurrence of helpers and environmental harshness. I calculated the average starting group size of breeding units in each of 13 colonies that have bred during the 5 yr of our study and expressed this as the percentage of the population serving as helpers. These values were plotted aginst two measures of environmental harshness. Figure 1 (top) plots the percentage of helpers in each colony against the log of the amount of rain that fell in the month prior to egg laying. A significant negative regression emerges (r = 0.81; P < .001). with the largest nesting group sizes occurring in 2 yr when Kenya suffered drought conditions.

A more accurate indicator of environmental harshness is food availability. No such data are available for the first 2 yr (the drought years) of our study. Beginning in March, 1977, however, we initiated a regular insect sampling program using a 3-m Malaise net (Marston 1965). The net was operated from 800 h to 1600 h, 6 days each month and the daily insect samples were dried and weighed. The average dry weight of the daily insect samples taken in the 1-month period preceding egg laying was used as an index of food availability for each colony. (This assumes that any assessment of the hardship of breeding, and the corresponding shift to helper or breeder status, is made in the period immediately prior to the initiation of breeding.) The regression of percentage of helpers against food availability is shown in figure 1 (bottom). The significant negative regression (r = 0.67; P < .01) again is consistent with the prediction of the ecological constraints model. Bee- eaters are more likely to remain with groups as helpers when conditions are harsh




45 -

Y = 54-16x r = 0.81

z \ p <.001

Lu 35-

0~~~~~~~~ D h

o 25 - IL

0~~~~~~~~

15

0.4 0.8 1.2 1.6 2.0 2.4 LOG RAINFALL (MM) IN MONTH PRECEDING BREEDING

32 -

Y = 29-2.8x z 0 r =0.67 28 - P <.01

? 24 -

? 20-

0- 0~~~~ 16-

0.0 0.5 1.0 1.5 2.0 2.5 3.0 3.5 (gm dry wt.) INSECT AVAILABILITY IN MONTH PRECEDING BREEDING

FIG. 1 -Incidence of helping behavior in bee-eaters plotted as a function of environmental harshness. Top: Helping incidence is measured as the percentage of the population initially helping in any one breeding colony. (The measure of the percentage of the population serving as helpers excludes individuals that initially bred themselves, but later became redirected helpers after their own nesting attempts had failed. Thus the measure accurately reflects the proportion of the population that initially opted to help rather than to reproduce personally). Harshness is measured as the rainfall (log total mm) occurring in the month preceding the median date of egg laying for the breeding colony in question. Data from 1973, 1975, 1977, 1978, and 1979 are included. Bottom: Helping incidence measured as above; harshness measured as food abundance, the mean daily dry weight (biomass) of insects sampled by Malaise net during the month preceding egg laying. Data from 1977, 1978, and 1979 are included. Open circle = colony where insect biomass in the month following egg laying was used (insect sampling was initiated when this colony was nesting).




and the chances for successful independent reproduction are low (here indicated by low rainfall and low insect availability), and are more likely to initiate breeding independently when ecological conditions appear favorable.

The ecological constraints model helps explain why many adults among cooperative species that are nomadic or colonial, as well as those residing in saturated, stable habitats, may postpone breeding on their own. By itself, however, the model is insufficient to explain why such auxiliaries should contribute actively to the reproductive success of others-why they should "help." This second phase in the evolution of helping is addressed in Emlen (1982).

SUMMARY

The ecological factors underlying the evolution of helping behavior in birds and mammals are examined. I argue that a necessary first step for the evolution of cooperative breeding is a substructuring of the population into small, stable, social units; in most known cases these are extended-family units. The ecological conditions leading to the development of such units are explored, and a general model is presented that emphasizes ecological constraints that limit the possibility of personal, independent breeding. When severe constraints occur, selection will favor delayed dispersal and continued retention of grown offspring within their natal units. Differing proximate factors can be responsible for limiting the option of personal reproduction. In stable, predictable environments where marginal habitat is scarce, high population density and resulting habitat saturation can lead to a severe shortage of territory openings (Brown 1974; Koenig and Pitelka 1981). This decreases the chance for independent establishment by new breeders. In variable and unpredictable environments, erratic changes in the carrying capacity can create the functional equivalents of breeding openings and closures. During harsh years, the cost of successfully reproducing can be magnified to prohibitive levels. When the chance of successful reproduction is sufficiently restricted, for either reason, selection will favor individuals remaining as nonbreeders within their natal groups. In essence, grown offspring remain at home only when the cost of doing otherwise is prohibitive.

This ecological constraints model predicts that the frequency of occurrence of nonbreeders will vary directly with (1) the degree of difficulty in becoming established as a breeder (for species in stable, saturated, habitats), and (2) the level of environmental harshness (for species in erratic, unpredictable habitats). Available evidence is presented for the acorn woodpecker, Melanerpesformicivorus (representing 1), and the white-fronted bee-eater, Merops bullockoides (representing 2), in a preliminary test of the predictions.

ACKNOWLEDGMENTS

Many of the ideas in this paper were conceived while studying the social behavior of bee-eaters in Kenya. The work was made possible by grants from the John Simon Guggenheim Foundation, the National Geographic Society, the Chapman Fund of the American Museum of Natural History, Cornell University,




and the National Science Foundation (BNS7681921 and BNS7924436). Numer- ous individuals have shaped my thinking, both through discussion and reading earlier drafts of the manuscript. For their comments I am indebted to W. J. Dominey, J. M. Emlen, A. J. Gaston, R. E. Hegner, W. D. Koenig, F. A. Pitelka, M. J. Ryan, P. W. Sherman, J. A. Stamps, P. W. Trail, P. M. Waser, and M. J. West-Eberhard.

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The University of Chicago - Université...

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