THE JOURNAL OF RAPTOR RESEARCH · 2019. 1. 10. · eses assume the resource of interest is food, that the food in question is patchily distributed and ephem-eral, ... formation of

THE JOURNAL OF RAPTOR RESEARCHA QUARTERLY PUBLICATION OF THE RAPTOR RESEARCH FOUNDATION, INC.

VOL. 52 NO. 4DECEMBER 2018

J. Raptor Res. 52(4):407–419� 2018 The Raptor Research Foundation, Inc.

EVOLUTION OF COMMUNAL ROOSTING:A SOCIAL REFUGE–TERRITORY PROSPECTING HYPOTHESIS

JAMES F. DWYER1

AND JAMES D. FRASER

Department of Fish and Wildlife Conservation, Virginia Tech, 100 Cheatham Hall, Blacksburg, VA 24061 USA

JOAN L. MORRISON

Department of Biology, Trinity College, Hartford, CT 06106 USA

ABSTRACT.—Avian communal roosts provide insight into evolution and serve as focal points for conservation.Nonbreeding Crested Caracaras (Caracara cheriway; hereafter caracaras) use communal roosts, butevolutionary implications have not been explored. Though nonbreeding caracaras are nonmigratory, thescientific literature fails to explain seasonal differences in their movement and survival concurrent withseasonal consistency in their habitat and social ecology. In the Social Refuge–Territory Prospectinghypothesis we propose, socially subordinate nonbreeding caracaras precluded from breeding by habitatlimitation use communal roosts as social refuges to avoid aggression from dominant territory holders duringnonbreeding seasons, and engage in territory prospecting during breeding seasons. Communal roosts thusbecome central places from which to forage not for food, but for a breeding territory. Because foraging gainsare stored as remembered information, competition costs resulting from public information are preempted.For the Social Refuge–Territory Prospecting hypothesis to be valid, two criteria need to be met. First,communal roost use needs to be higher during nonbreeding seasons. Second, a measure of fitness needs tobe used to evaluate the hypothesis as an evolutionarily stable strategy. To meet these criteria, in this study wereport that numbers of nonbreeding caracaras using a communal roost in Florida are higher duringnonbreeding seasons (mean ¼ 111.8 individuals / night) than during breeding seasons (mean ¼ 60.7individuals / night) as counted from August 2006–April 2009 (n¼407 counts). We also compare differentialsurvival by season from previous work to demonstrate that by limiting exploratory movements to times whenprospecting is most informative, nonbreeding caracaras balance maximizing survival against the likelihoodof securing a breeding territory. Our hypothesis provides a unifying explanation for otherwise unexplainedparadoxes in the ecology of nonbreeding caracaras, and may be useful in guiding conservation andexpanding our understanding of the ecology of other communally roosting birds.

KEY WORDS: Crested Caracara; Caracara cheriway; floater; habitat limitation; information center hypothesis;nonbreeding; public information.

EVOLUCION DE LOS DORMIDEROS COMUNALES: UNA HIPOTESIS PROSPECTIVA SOBREREFUGIO SOCIAL-TERRITORIO

RESUMEN.—Los dormideros comunales de aves proporcionan informacion sobre la evolucion y sirven comopuntos focales para la conservacion. Los individuos no reproductivos de Caracara cheriway (en adelantecaracaras) usan dormideros comunales, pero las implicancias evolutivas no han sido exploradas. Aunque loscaracaras no reproductivos no son migratorios, la literatura cientıfica no explica las diferencias estacionalesen su movimiento y supervivencia concurrentes con la consistencia estacional en su habitat y ecologıa social.La Hipotesis Prospectiva de Refugio Social-Territorio propone que los caracaras no reproductivos

1 Present address: EDM International, Inc. 4001 Automation Way, Fort Collins, CO 80525, USA; email address:[email protected]

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socialmente subordinados, excluidos de la crıa por limitantes de habitat, utilizan dormideros comunalescomo refugios sociales para evitar la agresion de los individuos dominantes, poseedores de territorio durantela estacion no reproductiva, y participan en la prospeccion del territorio durante las estaciones de crıa. Losdormideros comunales se convierten ası en lugares centrales para buscar, no alimento, sino un territorioreproductivo. Debido a que la ganancia de las busquedas se almacena como informacion registrada, seanticipan los costos de competencia resultantes de la informacion publica. Para que la Hipotesis Prospectivade Refugio Social-Territorio sea valida, se deben cumplir dos criterios. Primero, el uso de dormideroscomunales debe ser mayor durante las estaciones no reproductivas. Segundo, se debe usar una medida deeficacia biologica para evaluar la hipotesis como una estrategia evolutivamente estable. Para cumplir conestos criterios, en este estudio constatamos que la cantidad de caracaras no reproductivos que utilizan undormidero comunitario en Florida es mayor durante las estaciones no reproductivas (media ¼ 111.8individuos/noche) que durante las estaciones reproductivas (media¼60.7 individuos/noche), contados deagosto 2006 a abril 2009 (n¼407 conteos). Tambien comparamos la supervivencia diferencial por estacion apartir de trabajos previos para demostrar que al limitar los movimientos exploratorios a los tiempos cuandola prospeccion es mas informativa, los caracaras no reproductivos equilibran la maximizacion de lasupervivencia con la probabilidad de asegurarse un territorio reproductivo. Nuestra hipotesis proporcionauna explicacion unificadora para las paradojas, de otro modo inexplicables, sobre la ecologıa de loscaracaras no reproductivos, y puede ser util para guiar la conservacion y expandir nuestra comprensionsobre la ecologıa de otras aves que usan dormideros comunales.

[Traduccion del equipo editorial]

The evolution of avian communal roosting hasbeen a focal point for study and debate since Wardand Zahavi (1973) first presented what wouldbecome known as the Information Center Hypoth-esis (ICH; Bijleveld et al. 2010). The ICH proposedthat avian communal roosts served as social centerswhere birds actively recruited peers to foragingareas, and proposed this as the primary mechanismdriving the evolution of communal roosting. Thereare two problems with the ICH. First, it relies onreciprocal altruism to explain why knowledgeableindividuals choose to incur the costs of increasedcompetition resulting from recruiting peers toforaging areas (Bijleveld et al. 2010). To be anevolutionarily stable strategy, reciprocal altruismrequires multiple interactions among pairs ofindividuals (Suzuki and Akiyama 2008), an uncer-tain benchmark when communal roost compositionis dynamic (Conklin and Colwell 2008). In theabsence of demonstrable altruism, some comple-mentary factor, such as intraspecific competition(Marzluff et al. 1996, Wright et al. 2003), predation(Krause and Ruxton 2002, Rogers et al. 2006) orinclusive fitness (Rabenold 1986) is needed toexplain the behavior of knowledgeable birds atcommunal roosts. Second, the various life-historystrategies of the wide spectrum of communallyroosting birds makes it unlikely that a singleexplanation can encompass the evolution of com-munal roosting in all species. Though support forthe ICH has been limited, the cost-benefit approachwith which the ICH has been evaluated remains an

essential tool in developing evolutionary hypotheses(Bijleveld et al. 2010).

Given the poor fit of the ICH to various species,many more hypotheses for the evolution of commu-nal roosting have been proposed. For example, theevolution of communal roosting in birds has beenattributed to fitness increases related to avoidance ofcompetition with socially dominant conspecifics(Ferrer and Harte 1997, Beauchamp 1999, Penter-iani et al. 2008), obtaining information about thedistribution and abundance of food (Buckley 1996),avoidance, detection, or saturation of predators(Krause and Ruxton 2002, Rogers et al. 2006,Conklin and Colwell 2008), opportunities to findmates among the communal roosting population(Blanco and Tella 1999), identification of vacantterritories (Blanco and Tella 1999), and collabora-tive thermoregulation (Krause and Ruxton 2002,Chappell et al. 2016). Each hypothesis appears toapply well to particular species, and once in place,the evolutionary driver of communal roosting in anygiven species does not preclude secondary benefitsconsistent with other hypotheses (Krause andRuxton 2002).

A weakness in many existing hypotheses is theunstated assumption that individuals using commu-nal roosts perceive the roost positively, i.e., thatindividuals want to be at the communal roost. Incontrast to this, we begin from a hypothesis that insome cases individuals may not view a communalroost positively, but may use it anyway to make thebest of a bad situation. To illustrate this, we begin as

408 VOL. 52, NO. 4DWYER ET AL.

Clobert et al. (2001) did, with a thought experiment.Consider the following thought experiment for ahypothetical species which uses communal roosts.Imagine a closed and isolated patch of habitat 10km2, similar conceptually to the Crested Caracaras’(Caracara cheriway) range in the Florida peninsulawhere neither immigration nor emigration occurs(described below). In the thought experiment,breeding pairs of species X occupy 1-km2 breedingterritories year-round from the second year of lifethrough the sixth year of life, so breed for 5 yr, andthen die. Breeding occurs annually, and territoriesabut one another so no intra-territorial spaces occur.If one breeding pair is introduced into the habitat,then assuming an ideal free distribution (Fretwelland Lucas 1970), all 100 of the 1-km2 breedingterritories will be occupied within 8 yr (Fig. 1).Thereafter, most of the additional young producedcannot occupy a breeding territory and none canemigrate. They must go somewhere. One solutionmight be for the nonbreeding individuals to

aggregate at a single location, regardless of age orphysiological breeding potential, overwhelming theterritorial defense of a single breeding pair, andforming a communal roost. None of the individualsusing the communal roost necessarily perceives theirresidency there as positive. They would presumablyrather establish breeding territories of their own, butthey have no viable path to do so. In this waycommunal roosting could evolve as a response toterritoriality and habitat limitation. Thereafter,proximate secondary foraging benefits could devel-op, but these benefits would not ultimately beresponsible for the evolution of communal roostingin this scenario.

A second weakness of many hypotheses for theevolution of communal roosting is that the hypoth-eses assume the resource of interest is food, that thefood in question is patchily distributed and ephem-eral, and that successful foragers can be distin-guished from unsuccessful foragers. If the limitingresource is not food, but instead breeding territo-ries, then the resource may not be ephemeral,successful foragers will gain information that isstored in memory, and information gained will notbe available as public information to their commu-nally roosting competitors. A third weakness of manyhypotheses for the evolution of communal roostingis that they focus on migratory species breeding inthe northern hemisphere, and thus avoid the needto explore or explain seasonal differences incommunal roost use in breeding and winteringareas.

Though the movements of individuals, and thecauses and consequences of those movements aresome of the most-studied concepts in ecology, theyremain poorly understood (Clobert et al. 2001),perhaps due in part to weaknesses in existinghypotheses and their underlying assumptions. Re-evaluations of the assumptions that (1) communalroosts may in some cases be occupied more-or-lessinvoluntarily, (2) the limiting resource drivingcommunal roosting may not be ephemeral, and(3) seasonal differences in communal roost use arerelated to migration form the basis for the alternateevolutionary explanation for communal roostingproposed here.

The Social Refuge–Territory Prospecting Hypoth-esis. Here, we propose the Social Refuge–TerritoryProspecting hypothesis to explain the evolution ofcommunal roosting in a nonmigratory speciessubject to year-round territoriality and habitatlimitation. We define social refuges as locations that

Figure 1. A simplified thought experiment illustratesformation of a communal roost in a closed habitat patchwhere one breeding pair is introduced and breedingterritories are defended for 5-yr lifespans. Gray cells:occupied territories. White cells: vacant territories. Blackcell: communal roost. Straight arrows: accumulation ofnonbreeders at a communal roost. Circular arrows:prospecting for territories by nonbreeders from a commu-nal roost. In this scenario, nonbreeders use the communalroost because no better options (breeding or emigration)exist.

DECEMBER 2018 409SOCIAL REFUGE–TERRITORY PROSPECTING

socially subordinate individuals occupy to avoidfitness-reducing interactions with socially dominantconspecifics. The term social refuge consolidatesvarious observations into a unified concept. Forexample, temporary settlement areas (e.g., Penter-iani et al. 2008, Balbontın and Ferrer 2009, Tanfernaet al. 2013), temporary settling areas (e.g., Ferrer1993, Ferrer and Harte 1997), staging areas (Mel-lone et al. 2011), and dispersal areas (Moleon et al.2011) each are slightly different ways of conceptu-alizing spatial arrangements of socially subordinatenonbreeding birds and socially dominant breedingbirds. Social refuges also may occur at territory edgeswhere non-territorial individuals can escape aggres-sion of territory holders by moving into adjacentnonbreeding habitat (Dwyer et al. 2013), or anadjacent territory without that territory-holder im-mediately noticing (Rohner 1997). Social refugescan include indefensible areas around point subsi-dies, such as landfills, that create perpetual, abun-dant, spatially fixed resources (Webb et al. 2004), oraround carcasses if the numbers of non-territorialbirds overwhelm a territory holder’s ability to defendan area (Marzluff et al. 1996). Any of thesegatherings can function as social refuges if theyfacilitate access to resources that otherwise would bedefended by a breeding pair of territorial birds.

Communal roosts could develop, and communalroosting evolve, where non-territorial individualsaggregate at social refuges to avoid fitness-reducingconsequences of intraspecific conflict with socialdominants. A substantial fitness-reducing cost tousing a social refuge is that the same mechanismsthat prevent territorial defense of the site inherentlycreate a conflict between short-term (survival tobreeding) and long-term (breeding) fitness goals,where fitness is defined as a measure of the extent towhich an individual contributes genes to futuregenerations (Freeman and Heron 1998). Specifical-ly, staying at the communal roost may be relativelysafe, leading to long life, but mostly precludesbreeding, either due to insufficient resources toraise offspring, or due to high competitive pressurefrom communal roost-mates (though inclusivefitness benefits may accrue).

Territory prospecting facilitates nonbreeding in-dividuals gathering information on the local qualityof potential future breeding sites (Ponchon et al.2013), and occurs when reliable information onterritory quality is most available, with productivityserving as that information (Boulinier et al. 1996,Boulinier et al. 2008). Prospecting birds evaluate the

presence and quality of offspring produced in aterritory as an indicator of their own likely success.Prospecting may also provide cues on whether anexisting territory holder might be vulnerable toreplacement. Thus, prospecting occurs primarilyduring breeding seasons and can involve relativelylarge movements across multiple territories byprospecting individuals (Reed et al. 1999, Toblerand Smith 2004, Ward 2005). Other cues, such as anunmated individual of the opposite sex residentwithin a potential territory, may indicate that abreeding attempt might be possible in a givenlocation, but do not indicate whether that attemptis likely to be successful.

Evaluating the relative quality of specific potentialbreeding sites (territory prospecting) prior toattempting to occupy a site is hypothesized to bean ideal dispersal strategy if the environmentcontains a low proportion of high-quality habitatpatches, even if doing so is associated with a cost(i.e., loss of a low-quality breeding opportunity;Boulinier and Danchin 1997). This may be particu-larly true for long-lived species that hold permanentterritories throughout their breeding years becauseholding a high-quality territory for a shorter periodmay lead to greater lifetime reproductive successthan holding a low-quality territory for a longerperiod.

The Social Refuge–Territory Prospecting hypoth-esis proposes that seasonal changes in communalroosting reflect seasonal changes in the relativeweight of the multiple selective pressures acting oneach individual. Specifically, we propose that indi-viduals avoiding year-round territoriality of sociallydominant conspecifics (as occurs in Crested Cara-caras; described below), should use social refugesduring nonbreeding seasons when there is relativelylittle to be gained from trespassing on breedingterritories, and should engage in territory prospect-ing during breeding seasons when there is much tobe gained from trespassing.

Here we examine the behavioral ecology ofCrested Caracaras (hereafter caracaras) to examinewhether the Social Refuge–Territory Prospectinghypothesis may offer an explanation unifying mul-tiple components of the seasonally asymmetricbehavior of nonbreeding individuals of all ageclasses in this enigmatic species. Caracaras arenonmigratory facultative avian scavengers distribut-ed from central South America to southern NorthAmerica, with an apparently isolated population insouth Florida from which no emigration or immi-


gration is known to occur (Morrison and Dwyer2012). Breeding caracaras defend territories year-round and do not use communal roosts (Morrisonand Dwyer 2012).

Nonbreeding caracaras are highly social (Dwyer2014), do not defend territories (Morrison andDwyer 2012), and use communal roosts extensively(Lasley 1982, Johnson and Gilardi 1996, Dwyer2010). These nonbreeders include juveniles notcapable of breeding (Morrison and Dwyer 2012),immatures apparently capable of breeding thoughthey do so only rarely (Nemeth and Morrison 2002),and floaters persisting in the nonbreeding popula-tion for at least 3 yr (Dwyer et al. 2012). Floaters areindividuals that are presumably physiologicallycapable of breeding but which do not hold aterritory (Newton and Rothery 2001, Penteriani etal. 2008). In one study of nonbreeding caracaras inFlorida, floaters made up an average of 37% (95% CI32–42%) of nonbreeders occupying communalroosts (Dwyer 2010), persisting for years in arecirculating transient phase of dispersal. Theecology of nonbreeding caracaras is distinctlyseasonal, though this seasonality has not beenpreviously explained. Specifically, nonbreeding ca-racaras have higher survival during breeding seasonsthan during nonbreeding seasons (Dwyer et al.2012). Nonbreeding caracaras also move morewidely around the species’ range during breedingseasons than during nonbreeding seasons (Dwyer etal. 2013), blurring the line between dispersal andmigration. To resolve these various unusual life-history traits, we propose that communal roostsfunction as social refuges to allow nonbreedingcaracaras to remain adjacent but external toterritories defended by breeding caracaras, and thatduring breeding seasons, nonbreeding caracarasdisperse from these social refuges to prospect forterritories.

METHODS

As applied to caracaras, the Social Refuge–Territory Prospecting hypothesis hinges on anassumption that most of the costs and benefits thatnonbreeding caracaras balance day-to-day are rela-tively consistent year-round, and that the onlysubstantial seasonal variation is the relative value ofinformation available from territory prospecting. Toevaluate this, we made 13 predictions based on theSocial Refuge–Territory Prospecting hypothesis (Ta-ble 1). We then reviewed the existing literature oncaracaras to identify whether and which of these

hypotheses were supported or refuted. A keyprediction was that the number of caracaras usinga communal roost should be relatively low duringbreeding seasons when territory prospecting wouldbe beneficial and relatively high during nonbreed-ing seasons when prospecting offered little benefit.Important to this prediction is an understandingthat most (96%) nesting attempts (i.e., egg-laying) inFlorida are initiated from October through March(Morrison 1999), with hatching approximately 1 moafter egg-laying, and fledging 2 mo after that(Morrison and Dwyer 2012). Young then remainon natal territories for as little as 2 mo or as many as10 mo (Morrison and Dwyer 2012), resulting in atrickling, rather than a pulsed entry into thenonbreeding population.

Because no information on year-round communalroost use was available, we tested our prediction ofroost use by counting nonbreeding caracaras using acommunal roost from August 2006 through April2009. We conducted these counts from a vantagepoint with an unobstructed view of the communalroost (cf. Sykes 1985, Sweeney and Fraser 1986).During counts, we recorded caracaras entering thecommunal roost in 1-min intervals relative to sunset(cf. Sykes 1985) from 1 hr before sunset until 0.75 hrafter sunset. This protocol could have allowed birdsto enter the communal roost undetected if theyarrived after it became too dark for us to see. Weevaluated that possibility via simultaneous visual andsignal identification of the arrival of individualsradio-tagged in a related study (Dwyer 2010, Dwyeret al. 2013). This also allowed us to confirm thatbreeding caracaras with territories nearby did notenter the communal roost, reconfirming our earlierassertion (Morrison and Dwyer 2012).

The communal roost we studied was near thecenter of the caracara’s range in Florida (Fig. 2;Dwyer 2010, Dwyer et al. 2013, Smith et al. 2017),adjacent to the MacArthur Agro-Ecology ResearchCenter near Lake Placid, Florida (27890N, 818120W).The communal roost was composed of approximate-ly 0.015 ha of Sabal palms (Sabal palmetto) embeddedin a matrix of pastures, palm hammocks, oak-palmhammocks, seasonal wetlands, and commercialcitrus groves typical of caracara habitat (Morrisonand Humphrey 2001, Dwyer et al. 2013, Smith et al.2017). The subtropical study area was characterizedby a rainy season (June–September), and a dryseason (October–May; Chen and Gerber 1990).

Statistical Analyses. Caracaras in Florida breedyear-round, but most nesting occurs during the 6 mo


from October through March (Morrison 1999). Asin Dwyer et al. (2012, 2013), we defined Octoberthrough March as the breeding season, and Decem-ber and January, when 61% of nests are initiated, asthe peak of the breeding season. We defined Aprilthrough September as the nonbreeding season.These assignments allowed us to compare counts atthe communal roost during the peak of breedingseasons to counts during the tails of breedingseasons, and to counts during nonbreeding seasons.We used analysis of variance (ANOVA) to exploreseasonal and annual variation in the number ofcaracaras counted at the communal roost eachmonth. For these analyses, we calculated the averagenumber of caracaras observed entering the commu-nal roost across counts within each month, and usedmonthly averages in ANOVAs. This helped reducepseudoreplication of counts on adjacent days andreduced the influence of large or small outlyingcounts, though some autocorrelation inevitablypersists in data where some of the same birds usedthe roost for long periods. We considered statisticalresults significant at P � 0.05.

RESULTS

We identified 13 predictions that must be met forthe Social Refuge–Territory Prospecting hypothesisto be supported. Of those, 12 were evaluated basedon published literature, and one is tested here.

Hypotheses Supported by Existing Literature.With regard to the social refuge half of ourhypothesis, the breeding habitat of caracaras inFlorida is limited (Morrison and Humphrey 2001)and defended year-round by territorial breeders(Morrison and Dwyer 2012) that do not usecommunal roosts (Morrison and Dwyer 2012).Breeding and nonbreeding caracaras coexist inoverlapping space however (Dwyer et al. 2013),which leads to intraspecific aggression when non-breeding birds trespass on breeding territories(Morrison and Dwyer 2012). Survival of nonbreed-ing caracaras is reduced during breeding seasonscompared to nonbreeding seasons (Dwyer et al.2012). Specifically, based on year-round radiotelem-etry, monthly survival (mean, SE) is highest duringnonbreeding seasons (0.995, 0.004), lower duringthe tails of breeding seasons (0.984, 0.007), and

Table 1. Predictions supporting the Social Refuge–Territory Prospecting hypothesis.

HYPOTHESIS PREDICTION SUPPORT

Social Refuge Breeding habitat is limited Morrison and Humphrey 2001Breeding caracaras do not use communal roosts Morrison and Dwyer 2012Breeding and nonbreeding caracaras co-exist in overlapping

spaceDwyer et al. 2013

Breeding territories are defended from nonbreedingcaracaras year-round

Morrison and Dwyer 2012

Aggressive encounters occur when nonbreeding birdstrespass on breeding territories

Morrison and Dwyer 2012

Nonbreeding caracaras’ survival is lower during breedingseasons

Dwyer et al. 2012

Territory Prospecting Nonbreeding caracaras are not food limited during anyseason

Morrison and Pias 2006

Nonbreeding caracaras are physiologically capable ofbreeding

Nemeth and Morrison 2002

Nonbreeding caracaras trespass more frequently duringbreeding seasons

Implied from Dwyer et al. 2013

Nonbreeders’ home ranges are greater during breedingseasons than nonbreeding seasons

Dwyer et al. 2013

Nonbreeding birds seek undefended areas when there islittle benefit to be gained by trespassing

Typical of territory prospectinga

Nonbreeding caracaras acquire territories where they engagein territory prospecting

Typical of territory prospectingb

Nonbreeding caracaras show seasonal variation in communalroosting

Presented here

a Boulinier et al. (1996), Reed et al. (1999), Ponchon et al. (2013).b Blanco and Tella (1999).


lowest during the peak of breeding seasons (0.953,0.019).

With regard to the territory prospecting half of ourhypothesis, nonbreeding caracaras are physiologi-cally capable of breeding (Nemeth and Morrison2002). The pellets of nonbreeders consistentlycontain lower-quality forage than the pellets ofbreeders (Morrison et al. 2008), indicating non-breeders occupy lower-quality habitats year-round(Morrison and Pias 2006), but suggesting nonbreed-ers are not food-limited during breeding seasons,i.e., not wandering more widely during breedingseasons in search of food (Dwyer et al. 2013).Nonbreeding caracaras use home ranges that areapproximately five times larger during breeding

seasons than during nonbreeding seasons, appar-ently because trespassing occurs more frequentlyduring breeding seasons in caracaras (Dwyer et al.2013).

Hypothesis Tested Here. From 9 August 2006through 17 April 2009 (n ¼ 407 counts, mean ¼ 1count/2.4 d), we counted nonbreeding caracaras ata communal roost that had not been documentedprior to this study (Fig. 3). We found nonbreedingcaracaras were present year-round during eachcount for 33 mos (nightly mean ¼ 91 individuals,median¼ 73, SD¼ 62, SE¼ 3, min¼ 6, max¼ 304).Our counts included 6 mo during the peak ofbreeding seasons, 12 mo during the tails of thebreeding seasons, and 15 mo during nonbreeding

Figure 2. Locations of communal roosts used by caracaras in Florida (Dwyer 2010). Grey arrow indicates the communalroost near the center of the species’ range where count data were collected August 2006 through April 2009.


seasons. Average monthly counts of nonbreedingcaracaras were lowest (mean ¼ 40.9, SD ¼ 7.4) inDecember and January (F2,30 ¼ 4.53, P ¼ 0.019)during the peak of the breeding season, higherduring the tails of the breeding season (October,November, February, and March; mean¼ 80.1, SE¼15.6), and highest during the nonbreeding season(April through September; mean ¼ 109.9, SE ¼17.3).

Every radio-tagged nonbreeding caracara thatarrived at the communal roost was confirmed witha visual observation (n ¼ 855 observations of 19radio-tagged individuals, mean ¼ 45.1 observationsper individual, min ¼ 2, max ¼ 161). These radio-tagged birds did not consistently share the commu-nal roost however, with some birds using it on somenights, and others on other nights, indicatingdynamic communal roost composition. Duringcounts at the communal roost, we never detectedbreeding caracaras that had been radio-tagged in thearea.

DISCUSSION

Ward and Zahavi (1973) postulated the ICH toexplain central place foraging for food. Becauseneither the ICH, nor other existing hypotheses forthe evolution of communal roosting adequatelyexplained all aspects of communal roosting innonbreeding caracaras, we developed the SocialRefuge–Territory Prospecting hypothesis. Under the

Social Refuge–Territory Prospecting hypothesis,communal roosts may serve as social refuges andmay also function as central places from whichnonbreeders forage not for food, but for territoriesin a prospecting context.

To propose our Social Refuge–Territory Prospect-ing hypothesis as a driver of the evolution ofcommunal roosting in nonbreeding Crested Cara-caras, we must offer a link between the behavior wereport and the fitness implications for individualsundertaking that behavior. Previously publisheddifferences in seasonal survival of nonbreedingcaracaras (Dwyer et al. 2012) facilitates such anassessment. Nonbreeding caracaras’ monthly surviv-al is highest during nonbreeding seasons when theydisproportionately use communal roosts (April–September), lower during the tails of the breedingseason (October, November, February, March), andlowest during the peak of breeding (December–January). Actual annual survival is intermediatebetween what might be expected if nonbreedingcaracaras remained at communal roosts year-roundand what survival might be if nonbreeding caracarasavoided communal roosts year-round (Fig. 4).Comparing these survival rates year-round illustratesthat a nonbreeding caracara using a communal roostyear-round would likely survive longer (probabilityof survival to 5 yr . 0.80), but would be unlikely toidentify and secure a breeding territory. A non-breeding caracara engaged in territory prospecting

Figure 3. Mean monthly counts of Crested Caracaras at a communal roost near Lake Placid, Florida. Bars indicatestandard errors within months. The breeding and nonbreeding (nb) seasons for Crested Caracaras are denoted on the x-axis n¼ 407 counts. Data collected August 2006 through April 2009.


year-round would not likely live very long (probabil-ity of survival to 5 yr , 0.10). The Social Refuge–Territory Prospecting hypothesis unifies document-ed seasonal variation in survival with fitness decisionsby demonstrating an evolutionarily stable strategywherein nonbreeding caracaras increase the risksthey take only when the likelihood of a fitness payoffis high (probability of survival to 5 yr approximately0.40). Individuals balancing these conflicting costsand benefits have the best chance of maximizingtheir fitness through surviving long enough tosecure a breeding territory.

Food Availability. A potential weakness in our testof the Social Refuge–Territory Prospecting hypoth-esis is that we did not directly evaluate foodavailability across seasons. If food were particularlylimited during breeding seasons, when nonbreedingcaracaras range most widely and die most frequently,then variation in food availability might drive thecommunal roosting patterns we observed. However,because birds consistently breed during the seasonwhen food is most abundant, it is unlikely that thereare sufficient food resources for breeding caracarasto not only survive, but also raise young, whilenonbreeding caracaras lack sufficient food for basicsurvival. Instead, Occam’s razor would suggest thatfood is abundant for this generalist forager acrossbreeding classes, and that a failure to recognize thismay stem more from the human’s inability to

conceptualize the reality that animals can act onmemories formed during territory prospecting, thanfrom any ecologically relevant obstacle.

Application to Other Species. Spanish ImperialEagles (Aquila adalberti) spend the first 3–5 yr of theirlives as non-territorial immatures, occupying tempo-rary settlement areas that are not used by adults(Ferrer and Harte 1997). Adult Spanish ImperialEagles defend permanent breeding territories,presumably incorporating the highest-quality habi-tats, while a series of nonbreeding birds use the sametemporary settling areas in sequential years (Ferrer1993). Using the terminology of our hypothesis,immature Spanish Imperial Eagles may be relegatedto social refuges while developing to sexual maturity,and then once maturity is reached, they can beginprospecting for breeding territories. Similarly, dur-ing the transient phase of dispersal in juvenileBonelli’s Eagles (Aquila fasciata), individuals usecommunal roosts in dispersal areas (Moleon et al.2011), but also spend large parts of their timeexploring surrounding areas, probably with the aimof searching for vacant territories or mates(Balbontın and Ferrer 2009). The on-again-off-againuse of communal roosts in temporary settlementareas may be seen as moving back and forth betweensocial refuges and territory prospecting, balancingshort-term oscillations in the costs and benefits ofthe social refuge and territory prospecting. In Short-

Figure 4. Actual probability of survival for nonbreeding caracaras (from Dwyer 2012; middle line). Predicted probabilityof survival for nonbreeding caracaras if survival rates during nonbreeding seasons (from Dwyer 2012) are extrapolatedyear-round (top line). Predicted probability of survival for nonbreeding caracaras if survival rates during breeding seasons(from Dwyer 2012) are extrapolated year-round (bottom line).


toed Snake-Eagles (Circaetus gallicus), immatures usesummer staging areas where intraspecific competi-tion is likely lower than within breeding areas(Mellone et al. 2011). In this case, immature birdsincapable of breeding may use social refuges to avoiddominant conspecifics.

Some colonial species engage in territory pros-pecting while breeding, and shift nest sites betweenbreeding seasons based on the success of theirneighbors. For example, in Black-legged Kittiwakes(Rissa tridactyla; Boulinier et al. 1996, Boulinier et al.2008), Lesser Kestrels (Falco naumanni; Aparicio etal. 2007), Cliff Swallows (Petrochelidon pyrrhonota;Brown et al. 2000), and Collared Flycatchers(Ficedulla albicollis; Ponchon et al. 2013), nestingindividuals are socially dominant at their own nests,but socially subordinate elsewhere throughout thecolony. Under the Social Refuge–Territory Prospect-ing hypothesis, the existing nest site can be viewed asa social refuge from which individuals prospectwhen evaluating other sites within the colony. Nosingle evolutionary explanation is likely to explaincommunal roosting in all species engaged in thebehavior, but our hypothesis nevertheless appears tohave the potential for application beyond caracaras.

Application to Other Communal Roosts. Varioustypes of communal roosts exist. Main roosts (Blancoand Tella 1999), permanent roosts (Sweeney andFraser 1986), and persistent roosts (Buckley 1999)are used year-round, though there is often highturnover among individuals (Rabenold 1987). Sea-sonal roosts (Sweeney and Fraser 1986) and sub-roosts (Blanco and Tella 1999) are used annuallyduring specific periods, and ephemeral roosts areused briefly to facilitate access to temporary foragingresources (Sweeney and Fraser 1986). Central roosts(Coleman and Fraser 1989), or primary roosts(Coleman and Fraser 1989) are used relativelyfrequently as birds move within a roost system(Rabenold 1987), which is defined as a series ofadjacent communal roosts used by a local popula-tion (Rabenold 1987). Formation and dissolution ofseasonal roosts appear to contribute to cyclesobserved at permanent roosts (Sweeney and Fraser1986). Subroosts and seasonal roosts may offeraccess to more potential breeding sites than domain roosts (Blanco and Tella 1999), providingdifferent functionality to different roost types. In thelanguage of the Social Refuge–Territory Prospectinghypothesis proposed here, main roosts may serveprimarily a social refuge function, and subroosts,which are called ‘‘pairing centers’’ by Blanco and

Tella (1999), may serve primarily a territory pros-pecting function.

Future Research. A weakness in our work is thatthe communal roost data we present here is drawnfrom a single site. However, because no counts ofcaracaras at communal roosts had ever beenconducted prior to our work, no other data wereavailable for comparison. Future research shouldseek to evaluate elsewhere the patterns we observedat the communal roost we studied. Future researchcould also focus on exploring how recruitment andmortality occurs in caracaras by attempting long-term tracking of birds from their natal territories,through the nonbreeding and floater life stages, tobreeding territories, and by evaluating the potentialfor inclusive fitness when doing so. If the SocialRefuge–Territory Prospecting hypothesis is correct,then long-term tracking should indicate settlementin areas explored during previous breeding seasons,and mechanisms of mortality of nonbreedingindividuals during the breeding season shouldindicate intraspecific conflict with breeding birdsas a cause.

Another weakness in our study is the lack ofinclusion of a formal mathematical model for theSocial Refuge–Territory Prospecting hypothesis.Future research focused on evaluating our hypoth-esis with a multiple-competing-hypotheses frame-work may benefit from (1) creating and framingtesting around a formal mathematical model, and(2) using that model to guide a more statisticallyelegant analysis of seasonal differences in count dataat communal roosts.

Conservation Implications. Though communalroosting by caracaras has been known since the1980s and 1990s (Lasley 1982, Johnson and Gilardi1996), and continues to be reported (Dwyer 2010,Morrison and Dwyer 2012), our observations providethe first long-term record of year-round use. Theconservation implications of such roost use areundeveloped for caracaras (Smith et al. 2017), butin general management strategies that omit non-breeding individuals in species where floaters arepresent may fail to correctly identify why manage-ment goals are unmet (as they are in caracaras;USFWS 2008), and may consequently lead toineffective or even counterproductive managementactions (Penteriani et al. 2011).

If communal roosts function in the dispersal ofcaracaras as hypothesized here, then the currentconservation efforts, which focus entirely on breed-ing sites, may be ineffective in the long term.


Specifically, during the social refuge phase, loss ofcommunal roosts could reduce survival of nonbreed-ing birds during nonbreeding seasons, and duringthe territory prospecting phase, loss of communalroosts could limit nonbreeder’s ability to visitpotential breeding territories. Together these nega-tive impacts could reduce recruitment to thebreeding population if existing breeding birds dieand are not replaced. We don’t know for certain howcommunal roosts function in the ecology of non-breeding caracaras, but we do know that there are atleast 13 communal roosts spaced regularly through-out the species’ range (Dwyer 2010), that individualnonbreeding caracaras move regularly among thesesites (Dwyer 2010), and that 10 of the 13 knowncommunal roosts are within habitat identified ashaving high or very high probabilities of nestingcaracaras (Smith et al. 2017).

Until managers better understand the role ofcommunal roosts in the ecology of Florida’s caraca-ras, management of this population should focus onprotecting roosts along with nest sites. Futureconservation-oriented research should examine ad-ditional communal roosts, compare communalroosting habitat to breeding habitat, and identifywhether individuals move among communal roosts.

ACKNOWLEDGMENTS

All procedures herein were approved by VirginiaPolytechnic and State University’s Institutional AnimalCare and Use Committee (Protocol No. 10-011-FIW).This work was supported by the United States Fish andWildlife Service (Agreement number 401815G060); and aCunningham Doctoral Scholar Fellowship from theGraduate College of Virginia Tech (2006). We thank H.Swain, G. Lollis, and P. Bohlen of Archbold BiologicalStation’s MacArthur Agro-Ecology Research Center(MAERC) for providing access to the location fromwhich we counted the communal roost. This is contribu-tion number 194 from MAERC. S. Chiavacci, J. Dowling,A. Fleming, M. Hanson, L. Hunt, A. Mangiameli Dwyer,M. Scholer, N. Swick, and N. Thompson assisted withcommunal roost counts. We thank A. Dwyer and theanonymous reviewers whose contributions substantiallyimproved this work.

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Received 30 December 2017; accepted 3 May 2018

Associate Editor: Pascual Lopez-Lopez


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