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Coloniality in the Crab Plover Dromas ardeola does notDepend on Nest Site LimitationAuthor(s): Giorgio Chiozzi , Giuseppe De Marchi and Dawit SemereSource: Waterbirds, 34(1):77-81. 2011.Published By: The Waterbird SocietyDOI: http://dx.doi.org/10.1675/063.034.0109URL: http://www.bioone.org/doi/full/10.1675/063.034.0109

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77

Coloniality in the Crab Plover Dromas ardeola Does Not Depend on Nest Site Limitation

GIORGIO CHIOZZI1,*, GIUSEPPE DE MARCHI1 AND DAWIT SEMERE2

1Museo Civico di Storia Naturale, Corso Venezia 55, 20121 Milano, Italy

2Ministry of Fisheries, P.O. Box 58, Massawa, Eritrea

*Corresponding author; E-mail: giorgio.chiozzi@comune.milano.it

Abstract.—The Crab Plover (Dromas ardeola) is a little-known shorebird that breeds colonially in self-dug burrowson islands in the north-western Indian Ocean. To test whether the “nest site limitation” hypothesis could satisfacto-rily explain the high nest density in this species, 21 colonies were studied in Eritrea from 2002 to 2009. The hypoth-esis was falsified by the following observations: across the study period, nesting colonies were relocated on the samesandbanks every year and most occupied no more than 4% of the area suitable for excavating burrows; colony sizeand area suitable for burrowing were not correlated; nest density and colony size were not significantly correlated;the area occupied by nests increased steadily throughout the nest-building period; nests were closely-spacedthroughout the building phase rather than being scattered throughout the area eventually used for digging. Theseresults indicate that the Crab Plover is not site-limited but a truly colonial species. Received 9 March 2010, accepted 20August 2010.

Key words.—coloniality, Crab Plover, Dromas ardeola, Eritrea, nest limitation.

Waterbirds 34(1): 77-81, 2011

In spite of some inevitable costs of crowd-ing, such as ectoparasite and disease trans-mission, food competition, egg destruction,chick killing by neighbors and attraction ofpredators (Wittemberger and Hunt 1985;Brown and Bomberger Brown 1986; Tella2002) some 13% of bird species breed colo-nially. Coloniality is particularly prevalentamong nidicolous seabirds (98% species,Lack 1968) and was probably a preconditionfor colonizing marine habitats (Rolland et al.1998). By contrast, coloniality is uncommonamong shorebirds, most of which raise nid-ifugous chicks (Lack 1968).

Phylogenetic analyses suggest that colo-niality has evolved independently manytimes in birds and therefore that different se-lective pressures could have been at work inthe various transitions from solitary to com-munal breeding (Siegel-Causey and Khari-tonov 1990; Rolland et al. 1998; Varela et al.2007). Favored hypotheses for the evolutionand maintenance of coloniality involve selec-tive pressures connected to nest-site limita-tion, food-finding facilitation or defensefrom predators (reviewed by Wittenbergerand Hunt 1985; Siegel-Causey and Khari-tonov 1990; Brown and Bomberger Brown2001). Coloniality could also be a side effect

of sexual and/or habitat selection (Danchinand Wagner 1997; Wagner et al. 2000;Danchin et al. 2008).

The Crab Plover (Dromas ardeola) is oneof the few colonial shorebirds and the onlyone that nests in burrows. Together withcoursers and pratincoles (Glareolidae), theCrab Plover is closely related to the mainlycolonial and marine gulls, terns and auks(Sibley and Ahlquist 1990). As with manyseabirds, Crab Plovers breed on islands freeof terrestrial predators, lay a single egg, raisea nidicolous chick and regularly commutefrom breeding sites to distant feeding areas(Rands 1996; Hockey and Aspinall 1997; DeMarchi et al. 2006).

Hockey and Aspinall (1997) suggestedthat coloniality in Crab Plovers results fromtheir selection of predator-free islands closeto regionally and seasonally rich feeding ar-eas and which contain the highly specificsubstratum within which the birds can exca-vate their burrows. They further suggestedthat Crab Plovers are forced to nest at highdensities because limited by the availabilityof nesting substrata.

Surprisingly, the hypothesis that colonial-ity in birds stems from habitat limitation,perhaps the most parsimonious hypothesis,

78 WATERBIRDS

is supported by few data (Brown and Bomb-erger Brown 1996). Similarly, the suggestionof Hockey and Aspinall (1997) that Crab Plo-vers were nest-site limited was mostly basedon the study of a single colony on Abu al Ab-yadh Island, Abu Dhabi (Brown et al. 1991;Morris 1992; Hockey and Aspinall 1997).

The aim of this study, that takes advan-tage of the recent discovery of many newCrab Plover colonies in Eritrea (De Marchi etal. 2006; Semere et al. 2008), is to test the va-lidity of the “site limitation” hypothesis(Lack 1968, Wittemberger and Hunt 1985;Brown and Bomberger Brown 2001) as anexplanation for the maintenance of colonial-ity in the Crab Plover. In particular, the fol-lowing predictions of this hypothesis weretested (Brown and Bomberger Brown 1996;Brown and Bomberger Brown 2000):

1) the same burrowing areas should beused every year because no other suitablearea should be available;2) a large proportion of the suitable nest-ing habitat should be used in everybreeding season;3) birds will tend to maximize the in-ternest distance in order to minimize thenegative effects of proximity to conspe-cifics. For this reason, the first nestsshould be scattered throughout thewhole suitable nesting habitat in the bestquality sites. Therefore, nest densityshould be very low at the beginning ofthe nesting season and will increase asnew nests are built in lower quality areasamong existing nests.4) nest density should be correlated withthe number of nests: the larger the colo-ny size, the more the nests will bejammed into the small available nestinghabitat. This is the case with Cliff Swal-lows (Hirundo pyrrhonota) (Brown andBomberger Brown 1996);5) the number of nests (colony size)should be correlated with the extent ofthe suitable burrowing habitat.

METHODS

Data were obtained annually from 2002 to 2009 inup to 21 Crab Plover colonies on islands off the coast of

Eritrea, in the Southern Red Sea (De Marchi et al. 2006;Semere et al. 2008). The main research effort was con-centrated on Dahret Island (15°54’N, 39°34’E) in theDahlak Archipelago. The small island holds a typicallysized colony for the species in Eritrea as the colony size(363 nests on average over seven years) is between me-dian and average of the 21 colonies, and nest density(0.20 nests/m2) is close to the median of the 21 colo-nies. The study area has been described by Coulthard(2001), Chiozzi and De Marchi (2003) and De Marchi etal. (2006).

When colonies were visited, birds fled to nearbybeaches, the same reaction evoked by other potentialdangers, such as Sooty Gulls (Larus hemprichi), possiblepredators of chicks. The time spent by the researchersat a colony was usually less than one hour. Long breaksfrom incubation occur under natural conditions (DeMarchi et al. 2008) and disturbances of this durationwere not considered to impact incubation.

In order to obtain the most appropriate measureof nest density, groups of nests in the same sandbankseparated by at least 30 m (a situation observed onlyon Dahret Island) were classified as subcolonies, be-ing probably established by late nesters and renesters(De Marchi et al. 2006). Following this choice, thenumber of nests in the different subcolonies wassummed to estimate colony size; the unoccupied areabetween subcolonies was not included in calculationsof nest density in order not to unnaturally lower thismeasure. When data on colony size were available formore than one breeding season, an average was calcu-lated. Colony (or subcolony) areas were defined asthe smallest convex polygon including all the nests.The coordinates of the most outlying nests were ob-tained with a portable GPS and utilized to calculatethe areas.

Habitats suitable for burrowing were considered asthose located in the same sandbanks of the colony andwith similar low vegetation; the scattered presence ofdiscernible traces of older colonies proved that those ar-eas were suitable for nest digging. Beaches and areaswith bushes or tall grasses were excluded. Measures ofpotential colony area were made at ten of the 21 studycolonies; the remaining eleven colonies were inspectedduring rapid bird surveys that were part of a researchprogram by the Eritrean Coastal and Island BiodiversityProject (ECMIB Project). Areas potentially suitable forthe Crab Plovers to dig their nests were not measured(Semere et al. 2008).

Statistical tests were performed with the softwareSPSS 13. Values are given as mean ± SD. All tests are twotailed.

RESULTS

Colonies contained 411 ± 355 nests (me-dian 250, range 110-1600, N = 21). On Dahr-et Island, Crab Plovers nested in subcoloniesseparated from each other by approximately340 m (2003), 470 m (2004), 100 m (2006),55 m (2007), 550 m and 35 m (2008) and550 m (2009) (Fig. 1). Secondary subcolo-nies appeared always after the subcolony es-tablished earlier in the breeding season was

Coloniality in Crab Plover 79

raided by local fishermen in search of eggs.In 2005, the only breeding season in thestudy period when nests were not raided, thecolony was not structured in subcolonies.The smallest subcolony contained only 17nests (2007).

Overall, nest density in the study colonieswas 0.33 ± 0.26 nests/m2 (median 0.22,range 0.09-0.95 nests/m2, N = 21 colonies)and was not significantly correlated with col-ony size (Spearman r = 0.273, N = 21, p =0.231). On Dahret Island, average nest den-sity was 0.20 ± 0.07 nests/m2 (N = 7 years).

In successive years, on the same islands,Crab Plovers selected different areas of thesandbank for digging their new nests. We ob-served this pattern for seven consecutiveyears on Dahret Island (Fig. 1) and for twoyears on Sarad, Baradu and NN086 islandsand in the two colonies on Museri Island.

Moreover, all ten colonies were close to signsof older colonies in the same sandbanks.

In three years on Dahret Island the areaoccupied by the main subcolony (in 2004and 2009) or by the sole colony (in 2005)could be measured both at the beginning ofthe breeding season (7-9 May), with 6-30nests present, and at the end of the breedingseason when 300-364 nests were present.Over the breeding season nest densitychanged little despite the area occupied bythe colony/subcolony increasing enormous-ly. In 2004, nest density increased from 0.27to 0.40 nests/m2 while the colony area in-creased 8.5 times, in 2005 density decreasedfrom 0.33 to 0.24 nests/m2 while the colonyarea increased 154 times and in 2009 densitydecreased from 0.31 to 0.24 nests/m2 whilecolony area increased 23 times.

Measures at ten study colonies showedthat nine colonies used no more than 4% ofthe available nesting area, while one colonyon Museri Island occupied 35.6% of theavailable space. There was no correlation be-tween the area suitable for nesting and thecolony size (Spearman’s r = - 0.36, p = 0.920,N = 10 colonies).

DISCUSSION

As suggested by all the 21 investigatedcolonies containing crowded nests, the CrabPlover was confirmed to be highly colonial.In addition, contrary to the hypothesis pro-posed by Hockey and Aspinall (1997) basedon a single, site-faithful colony, we could findno evidence that the species is constrainedby nest-site availability.

Our research hypothesis was based onthe premise that members of a site-limitedspecies do not obtain any advantage in nest-ing close to each other and breeding pairs ofbirds should spread themselves out as muchas possible over the suitable nesting area inorder to avoid the disadvantages of close as-sociation with conspecifics (Brown andBomberger Brown 1996; Brown and Bomb-erger Brown 2001). Certainly, it is problem-atic for a human to assess whether an area issuitable or not for the breeding of a bird spe-cies, as it is even more difficult to detect mi-

Figure 1. Dahret Island showing the distribution of CrabPlover colonies from 2003 to 2009 (white areas). Colo-nies are symbolized by the year of formation while an in-creasing digit following the year indicates the sequenceof establishment of subcolonies (i.e. subcolony 2003.1was set in 2003 before subcolony 2003.2). Beach areaabove high tide mark in solid black; low vegetation(grasses and herbs up to 40 cm) area in pale grey; tallvegetation (grasses, sedges and halophytes >40 cm) areain medium grey.

80 WATERBIRDS

cro-habitat differences that could be crucialand immediately evident to the birds them-selves (Brown and Bomberger Brown 1996;Brown and Bomberger Brown 2001). How-ever, if Crab Plovers were site limited theyshould reuse the same nests or at least thesame nesting areas in following years as hap-pens in several burrowing seabirds, includ-ing Little Penguin (Eudyptula minor) andmost alcids and shearwaters (Martínez 1992;Nettleship 1996; Carboneras 1992). Such al-so happened in the colony studied by Hock-ey and Aspinall (1997) on Abu al Abyadh Is-land. In contrast, our direct observations onfive colonies and the presence of remains ofolder dug areas, demonstrated that coloniesin Eritrea shift location in sequential years(for seven consecutive years in Dahret Is-land). Therefore, site faithfulness appears tobe the exception rather than the rule.

Years after a breeding season, Crab Plo-vers’ burrows still remain discernible(Chiozzi and De Marchi 2003; De Marchi etal. 2006), even if they are gradually obliterat-ed by winter rains, wind-blown sand and peo-ple crossing the colony areas. Therefore, therotation of colony sites in Crab Plovers maybe a response to previous occupancy render-ing these sites less suitable for excavatingnew burrows (Chiozzi and De Marchi 2003;De Marchi et al. 2006). Similarly, Richdale(1963) reported Sooty Shearwaters (Puffinusgriseus) shifting from the previous year’snesting site to a new one when the soil wasfriable and the old burrows collapsed be-cause of the weather, when the vegetationgrew so thick as to obliterate the old nests orwhen the birds, while excavating their bur-rows, broke into already occupied ones. Thelatter situation caused both pairs to abandonthe nesting site. In Crab Plovers, the shift ofnesting site in consecutive years appears tobe the best solution when suitable habitat forburrowing is generally largely available, ashappens at least in pristine islands, such asthose of Eritrea, with only one colony out often being somehow site limited.

Changing colony location annually onthe same island, even if the site proved suc-cessful the previous year, and, conversely,leaving unexploited the areas that will be

used successfully the following year, stronglysupport the hypothesis that the suitable nest-ing habitat is larger than that used every sin-gle year. By evaluating the vegetation on thesandbanks and the presence of signs of oldercolonies, we estimated that 90% of the CrabPlover colonies occupied only a small pro-portion of the area suitable for the excava-tion of nest burrows (less than 4%). Interest-ingly, in a second Crab Plover colony in AbuDhabi (Umm Amin Island) the burrowingsubstratum was not a limiting factor, but col-ony size (only 35-38 pairs) could have beenlimited by food availability (Hockey and As-pinall 1997).

The observation that Crab Plovers’ nestswere densely packed from the onset of colo-ny formation and the area occupied by thecolony increased progressively further sup-ports that this species is truly colonial andnot site limited. The similar pattern is repli-cated in many truly colonial seabirds (spe-cies with Type II colony formation—Khari-tonov and Siegel-Causey 1988) and consid-ered an unambiguous proof of true colonial-ity (Brown and Bomberger Brown 2000).Conversely, species that are site limited butdo not take any advantage from closely asso-ciating to conspecifics should establish loosecolonies, as happens in some swallows(Brown and Bomberger Brown 1996). Be-sides, site-limited species should maximizetheir internest distance at the beginning ofnest occupancy and later be forced to nestamong already occupied nests, as has beenshown to happen in the Cliff Swallow (Hirun-do pyrrhonota) (Brown and BombergerBrown 2000).

Other expectations of the “site limitationhypothesis” that larger nesting habitats(sandbanks for Crab Plovers) should bearmore nests and nest density should increasein larger colonies (Brown and BombergerBrown 1996) were not statistically support-ed. Thus, Crab Plovers are truly colonial andnot site limited. Some alternative hypothesesto nest site-limitation should be examined inorder to explain why Crab Plovers breed soclose to each other and help to explain theevolution and maintenance of coloniality inthis unusual shorebird.

Coloniality in Crab Plover 81

ACKNOWLEDGMENTS

We thank the Department of Promotion and Devel-opment and the Department of Regulatory Services ofthe Eritrean Ministry of Agriculture, in particular H. Yo-hannes, for granting research permits to G. Chiozzi andG. De Marchi. We thank the staff of ECMIB Project thatcollaborated with D. Semere, in particular A. Jeudy, S.Mahmud, T. Hagos, G. Seleba, Y. Gebrezgabhier and Z.Haile. We thank J. Cohen and an anonymous referee forcomments on our manuscript.

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