Breeding

All crested terns share, with minor differences, suite of ecological and behavioral characteristics setting them apart from all other terns. These include: extremely dense nesting, with nests often hexagonally packed; clutches of single (usually) very large eggs; within species, chicks more variable morphologically than possibly all other birds; formation of crèches into which all young move a few days after hatching and remain until fledging; individual visual recognition of egg and nest site by parents, and vocal mutual individual recognition of parents and chick; and greatly extended parental care. This tight suite of features (whose interrelationships depicted for boreal S. m. maxima in Fig. 2) shared by most if not all crested terns (differing only in degree), suggests their adaptive nature and crested terns’ monophyly. Close relationship among crested terns further supported by successful hybridization between several normally allopatric taxa when vagrants have appeared in colonies far from normal range.

Unless otherwise indicated, all references are to boreal S. m. maxima, with data from Buckley and Buckley 1969, 1972a, 1972b, 1974, 1976, and 1977; Buckley et al. 1985; and Blus et al. 1979; austral S. m. maxima data from Quintana and Yorio 1997, 1998, and 1999 and Yorio and Quintana 1997; and S. m. albididorsalis data from de Naurois 1959 and Dragesco 1961 .

Pair Formation

Although courtship and copulation occur away from, or en route to, colony site and on wintering grounds, most probably occurs at or near colony site. At both Cape Charles, VA, and in S. Carolina, first courting boreal S. m. maxima arrivals in last week of Mar; by early Apr, courtship in full swing as more birds arrived. Unknown how long individual pair engages in courtship. In S. Carolina, egg-laying initiated in 2 different colonies in 1975 on 29 Apr and 4 May (75% of eggs laid in first 2 wk May), while in another colony, not far away, not until 16 May in 1974 and 27 May in 1975—not ending until 30 Jun (Blus et al. 1979).

Nest-Building

Nest-building in boreal S. m. maxima begins within few days of site occupation, and is completed after 1–2 d.

First/Only Brood Per Season

See Figure 3 . For boreal S. m. maxima, single (rarely 2) egg laid in early May at Cape Charles, VA, and Outer Banks of N. Carolina; egg-laying in both areas frequently completed by late May–early Jun. Bent (1921) gives egg dates as follows: N. Carolina, 15 May–26 Jun; Mississippi and Louisiana, 18 May–19 Jun; Texas, 8 Apr–18 Jun. Single-brooded, but re-lays when flooded out; one group in Virginia re-laid 5 times over a 7-d period of extreme tides.

In Argentina, austral S. m. maxima laid most eggs in second and third weeks of Oct, with most birds laying day of arrival in colony. In the Banc d’Arguin, Mauritania, S. m. albididorsalis ’s main egg-laying period last 10 d in Apr. Chicks generally hatch after 30 d. Incubation (25 d in austral S. m. maxima); 2 d after hatch, chicks leave nest site to join crèche (3–4 d in austral S. m. maxima, but S. m. albididorsalis young did not leave nest until 1 wk after hatch, or depart crèche until 15 d after). Fledgling’s first flight probably 30–31 d posthatching in all 3 populations, but more precise data needed.

Selection

Both members of pair select nest site. As they inspect chosen area of colony in Forward-Erect or normal walking posture, much pointing at feet and ground by both birds. After circling particular spot several times, pointing to ground assumes extreme form, with bill directed between legs while body plumage relaxed, and wings folded or held slightly out (perhaps a display). Both spend much time sitting in one spot, or one sits while other stands nearby. Several scrapes made before final choice. Mate-guarding undescribed.

Site/Microhabitat Characteristics

Breeds in tropical and subtropical (but austral S. m. maxima in temperate) lower–midlatitudes, coastally, usually on low-lying islands (<0.1 ha to >50-km-long barrier islands) subject to frequent flooding; sometimes higher dredge-spoil islands used with great success. Study of 5 colonies in Virginia revealed 4 site requisites: (1) absence of quadruped predators; (2) inaccessibility and excellent visibility of surroundings; (3) extensive areas of adjacent shallows for feeding; (4) location at or near oceanic inlet—in broad outline all subsequently confirmed at other locations. Sandy substrate most common but not requisite: some colonies on oyster shellbanks, and austral S. m. maxima colonies on silt-covered gravel beaches. Nests on ground in the open, sometimes on wrack, occasionally alongside beach-cast debris, or shells. Occasionally found nesting on flat roofs in Florida (known in other larids in Florida), but uncertain how frequent or widespread (Toland and Gilbert 1987).

Construction Process

By both parents, with foot-scraping and seated swiveling to round out nest cup. Construction diurnal, usually in morning, but may also be nocturnal, as colonies active at night. Pair alternates in sitting at potential sites, pivoting body, kicking sand rearward with feet, and pushing it forward with breast until both satisfied with shape and depth.

Structure And Composition

On ground in the open, sometimes on tideline of seaweed, etc.; shallow depression, unlined or with few pieces of debris, fish bones, etc. Defecation directly on nest rims reinforces nests against flooding; after few weeks, nest rims harden and colony assumes whitewashed appearance.

Dimensions

Unavailable.

Microclimate

No data, but substrate normally hot, in open, exposed areas.

Maintenance And Reuse Of Nests

Little or no maintenance. Wind or tidal damage to colony site from year to year (or even in same season) generally precludes reuse of old nests. However, austral S. m. maxima nests sometimes reused by austral Cayenne Terns, and 11% of Cayenne nests were reused by Royal Terns (Quintana and Yorio 1997).

Shape, Texture, Color

Subelliptical, somewhat smooth and glossy. Ground color varies from whitish to rose- and dark brown; heavily spotted, usually at broad end. Pattern and color extremely variable, used by adults to recognize own egg (Buckley and Buckley 1972b).

Size

For boreal S. m. maxima, Bent (1921) recorded mean dimensions of 63 × 44.5 mm, with length extremes of 57.5 and 74.5 and width extremes of 48.5 and 40.5 mm. Buckley and Buckley (1972a) found same mean dimensions in N. Carolina. No data for austral S. m. maxima or S. m. albididorsalis.

Mass

Only published boreal S. m. maxima data from Buckley and Buckley 1972a: mean 64 g (range 58–70, n = 25); S. m. albididorsalis, mean 55 g (range 53–56, n = 6; Cramp 1985). Biological significance of difference unknown, and no data for austral S. m. maxima .

Shell Thickness

Blus et al. (1979) compared S. m. maxima eggs from S. Carolina taken pre-1947 (pre-DDT; n = 170) with samples taken 1970–1975 (n = 228). Unexpectedly, recent eggs (0.28–0.39 mm) averaged 0.3–6.6% thicker than pre-DDT era eggs (0.24–0.38 mm), although difference significant only between pre-1947 and 1975 datasets.

King et al. (1983) compared pre-1947 Texas coast eggs: 0.358 mm ± 0.0004 SE (n = 18) with pesticide-era eggs, finding following thicknesses: 1970 Texas coast: 0.330 mm ± 0.0007 SE (n = 12); Pelican I., TX, 1978: 0.367 mm ± 0.0004 SE (n = 40); Sundown I., TX, 1978: 0.347 mm ± 0.0004 SE (n = 37). Oddly, all 1970s eggs significantly different from pre-1947 eggs: those from Texas coast and Sundown I. thinner, but those from Pelican I. thicker. Maness and Emslie (2001) found shells in N. Carolina colonies in late 1990s in high end (0.38–0.43 mm ± 0.03 SE) of mean thickness values reported in above studies. Autologous cracked or crushed eggs unknown from Royal Tern colonies.

Clutch Size

Normally one. Of 911 boreal S. m. maxima clutches, 1.4% were 2, with none 3 (Buckley and Buckley 1972a), although Blus et al. (1979) re-ported <0.1% 3-egg clutches out of 31,369, and Clapp et al. (1983) some with 4 eggs—surely egg-dumping or female-female pairs. In w. Africa (S. m. albididorsalis), de Naurois (1959) found only 2 or 3 two-egg clutches (no 3-egg clutches) out of 1,000. In Argentina (austral S. m. maxima), however, Quintana and Yorio (1997) found 33–41% 2-egg (no 3-egg) clutches. If not egg-dumping, this might have tax-onomic significance.

One brood, although any colony potentially active across several months, with intracolony laying synchrony highly localized (see below).

Egg-Laying

Synchronous within subsections of a colony; usually begins within 1–2 d of mass ar-rival on colony site, preceded by site-prospecting by both members of pair. At one Virginia colony, 33 new 1-egg nests on 5 May, 48 on 6 May, and 500–600 by 10 May; through most of North American range, peak from mid-Apr on Gulf Coast to May–Jun in N. Carolina and Virginia, but may span Apr–Aug in any colony.

In Argentina (austral S. m. maxima), first eggs laid second–third week in Oct, often on day of arrival at colony (Quintana and Yorio 1997). Re-placements laid after egg loss. Colonies expand from initial nuclei in linear or oval pattern determined by habitat and substrate. Adjacent sub-colonies frequently coalesce, and if conditions permit, many/most eventually attain round/ovoid shape. Diel laying peak unknown, possibly nocturnal.

Royal Tern nests frequently intermingled with those of Sandwich Terns in North America, latter almost always forming monospecific subclusters surrounded by Royals. In austral S. m. maxima, this role assumed by austral Cayenne Terns (although they apparently freely intermingle with S. m. maxima in colonies, rather than forming discrete conspecific clusters; Quintana and Yorio 1997), and in Netherlands Antilles by boreal Cayenne Terns (Ansingh et al. 1960). In S. m. albididorsalis at Banc d’Arguin, Mauritania, main egg-laying period last 10 d in Apr (de Naurois 1959).

Nest Density

Forms large and dense colonies from a few to ≥10,000 pairs, often divided into sev-eral adjacent subcolonies. Nest density exceedingly high: in boreal S. m. maxima, mean 7.4 ± 0.3 C.I. and 6–8 ± 0.3/m²; mean mixed austral S. m. maxima and Cayenne Tern densities from 9.8 to 11.1/m², and mean mixed internest distances from 29.8 to 31.4 cm (Quintana and Yorio 1997); in S. m. albididorsalis, 6–9/m². Distance between neighboring boreal S. m. maxima in Virginia and N. Carolina 0.08–0.7 m, and in S. m. albididorsalis mean 0.37 m (range 0.25–0.4; de Naurois 1959). Densities in boreal S. m. maxima typically peak in hexagonal pattern, with nests sharing common boundaries with 4–8 others and minimum distances between nests dictated by reach of incubating adults. Similar pattern occurs in austral S. m. maxima (Quintana and Yorio 1997) and likely in S. m. albididorsalis, but never described.

Onset Of Broodiness

Begins immediately with laying of first egg.

Brood Patches

Both parents; double brood patches on lower abdomen.

Incubation Period

Mean of 30–31 d (28–35 d for boreal S. m. maxima in Virginia–N. Carolina–Texas). Six austral S. m. maxima averaged only 25.7 d (Quintana and Yorio 1997), another difference possibly of taxonomic significance.

Parental Behavior

Adults share incubation, leaving eggs untended for hours. No specific nest-relief ceremony. Incoming bird, with or without fish, gives Advertising Call. Incubating bird looks up, answers with Aack Call. Incoming bird locates mate, lands at nest or nearby, approaches. Sitting bird may leave nest just before mate arrives, or remain sitting, causing returnee to depart again, to peck at sitting bird, or to gently nudge it off nest. Pair often stand at nest for several minutes before one leaves. On very hot days, incubating bird may leave to drink or forage before mate’s return. Bird hesitant about sitting on egg gives Aack Call.

Egg Recognition

Egg-switching experiments confirm that parents easily recognize own egg, apparently using extreme variation in superficial markings, but unknown how much time parents need to recognize own eggs (Buckley and Buckley 1972a).

Hardiness Of Eggs

Not specifically studied, but cracked/broken eggs of boreal S. m. maxima nearly unknown, although sometimes punctured by marauding gulls, turnstones (Arenaria spp.), crows (Corvus spp.), or grackles (Quiscalus spp.). Routinely subjected to temperatures likely >50°C on unsheltered sandy substrates when both parents simultaneously away foraging.

Preliminary Events And Vocalizations

Not studied, but prehatch piping from pipping egg induces attention by parents. As most colonies grow centrifugally, center eggs typically hatch first, peripheral eggs last.

Shell-Breaking And Emergence

Chicks break egg with prominent egg tooth.

Parental Assistance And Disposal Of Eggshell

Parents do not assist chick in hatching; eggshells not removed or eaten.

Condition At Hatching

Once dry (several hours), chicks (semi-) precocial and (semi-) nidifugous, leaving nest scrape within 24 h; usually move into crèche after 2–3 d. S. m. albididorsalis chicks remain at nest for 7 d, not entering crèche until 14 d (Quintana and Yorio 1997). Austral S. m. maxima chicks do not leave nest until 3–4 d of age, nor join crèche until 20 d (de Naurois 1959). Chicks fed entirely by parents until fledging. Body mass of newly hatched boreal S. m. maxima 50–62 g; no data on S. m. albididorsalis or austral S. m. maxima .

Extreme Variability In Plumage And Bare Parts

Highly variable in down and soft-part color and pattern. Ground color of down varies continuously from white to dark beige, but uniform over body, and uncorrelated with any other colors; superficial spotting (if present) always dark brown to black, but extent of spread over body also varies continuously and correlated only with pigmented bill-tip. Bill color scored as pinkish, yellow/orange, or greenish, and leg color as pink, yellow/orange, greenish, or black. Blackish bill-tip either present or absent, irrespective of color. Cumulative pigment scores for down and bare parts distributed unimodally, but skewed to white/light end, suggesting thermoregulatory pressures. Separate genetic control for bill-tip; bill color; leg color; down ground color; and spotting ex-tent indicated, last 4 probably polygenic (Buckley and Buckley 1970). Complex and continuous nature of color completely repudiates loose reference to Royal Tern “chick color morphs.” Such extreme variation undescribed for austral S. m. maxima or S. m. albididorsalis but probably typical of all crested-tern populations worldwide.

Growth And Development

No data for mass in-crease, growth of body parts, molt into Juvenal plum-age, or control of body temperature.

Behavior

Chicks still in egg, or up to 4 d after hatching, fall silent in response to parental Alarm Call. Young in nest freeze, or run/hide under vegetation. Chicks in crèche occasionally make new scrapes for themselves or crouch in existing ones. Young may lunge, gape, peck, regurgitate, or defecate when handled. As young approach fledging, they adopt juvenile food call and begging posture similar to adult Whinny Call; used for several months after fledging. Downy chicks solicit feeding from any adult with food, but rarely if ever fed by other than parents (Buckley and Buckley 1976).

Locomotion

No data.

Crèche Formation And Dynamics

Presence of large, mixed crèches containing young of all ages between 2 and 35 d most typical aspect of posthatching Royal Tern colony. Boreal Royal and Sandwich/Cayenne terns and austral Royal and Cayenne terns mix completely in common crèche. Parents induce boreal S. m. maxima young to leave nest for crèche with difficult-to-hear call at 2–3 d of age, chicks remaining in crèche until fledging; austral S. m. maxima chicks do not crèche until 20 d; and S. m. albididorsalis chicks remain in or near nest 7 d, not joining crèche until 14 d (Dragesco 1961). Age at which young leave nest could reflect differing levels of disturbance, but relative uniformity within boreal S. m. maxima suggests otherwise (Blus et al. 1979). Crèche formation in boreal S. m. maxima apparently obligate, but form it takes (relaxed or alarmed) a function of disturbance by humans, predators, etc., and changes constantly. Obligate/facultative nature of crèching in all S. m. maxima populations obscured by confusion of “relaxed crèche” with “absence of crèching.” At fledging, parents abandon colony site, and young accompany them to fishing grounds, where fed on sea surface or shore. During winter, young increasingly begin to fish for them-selves.

Crèches eventually embrace all chicks in colony, up to 10,000+. When relaxed, crèche breaks into many small clusters or even single pairs, attended by perhaps 10% of adults at minimum, up to 100% at night. Young in crèche lunge, gape, peck, regurgitate, or defecate if handled. When alarmed, crèche coalesces and moves rapidly away from disturbance, easily taking to water where young swim in amoeboid formation behind noticeable leaders, arcing first away from, then back to shore. If closely approached on land or water, crèche scatters and re-forms farther away. Parents feed only their own chick in crèche. Parental antipredator behavior intensifies on hatching, peaking in boreal S. m. maxima when young leave nest to join crèche.

Present adaptive value of crèche possibly confused with selection that favored its original and subsequent evolution. Many interlocking factors (several unique to crested terns) typifying S. m. maxima ’s breeding biology present throughout other crested terns and argue strongly for monophyletic origin of group. Crèching allows parents to forage away from colony for extended periods, seeking difficult-to-catch prey while at same time young afforded protection from avian predators by noisy crèche scene; occasional mammalian predators (Royal Terns sedulously seek quadruped-free nesting islands) possibly deterred by crèche’s smell, din, and intimidating mass of attending adults.

Brooding

Parents also share brooding and feeding of young at nest until chick joins crèche, where it remains, even at night; parents brood it there. Crèche formation appears obligate in boreal S. m. maxima, not facultative as in Sandwich Tern. Parents feed only own chick in crèche and continue to accompany and feed it during migration and often in winter quarters, generally for at least 5–8 mo after hatching.

Individual Chick Recognition

Parents recognize own young by voice and appearance within 1–2 d of hatching, while offspring recognize parents by voice in same period in what appears to be a redundant identification system facilitating chicks’ location in crowded crèches, and precluding parents’ feeding of any but their own chick (Buckley and Buckley 1972a).

Feeding

Adults attempt to feed chicks on day of hatching, but often bring in inappropriately large food items, chick appearing either not to recognize food or not hungry (perhaps still consuming yolk reserves), so incoming adult may swallow food itself, feed it to its mate, drop it on the ground, or fly off with it. Most adult foraging is done before 10:00, with a resurgence beginning around 16:00. Adults commonly heard calling over marine feeding areas during night, so presumably bringing prey to chicks 24 h/d, perhaps at reduced rates by night. Mean mass of fishes fed chicks in crèche 15.4 g, and food delivered on average every 147 min (Erwin 1977).

Downy chick solicits food by soft peeping and by pecking at prey item or bill. If chick rejects food, brooding parent may eat it. Not infrequently, one parent remains with small young, brooding it under wing in heat of day, while other parent forages. When small chicks of boreal S. m. maxima feed, one parent generally attends and defends it with Aggressive-Upright, while other offers fish in appeasing posture (bill low, plumage sleeked) typical of other terns. Once food is successfully transferred, both parents adopt Aggressive-Upright. Older chicks beg with Hunched Posture, call resembling Whinny Call of adult female (Buckley and Buckley 1976); this display continues into winter quarters.

Nest Sanitation

Adults and young defecate directly on nest rims, strengthening them against flooding, while giving colony strong odor of ammonia and providing mottled, heterogeneous substrate against which chicks may be afforded protection by crypsis.

Unknown, but unlikely.

Unlikely. Some 2- and probably all 3- and 4-egg clutches possibly result of egg-dumping, but unknown if accidental or result of polygyny or female-female pairs (both unreported).

Departure From Nest

Once chicks leave nest to join crèche (see above), they never return, although some occasionally occupy “pseudonests” while in crèche. Fledging period not precisely recorded but between 28 and 35 d, with 30–31 d average.

Growth

Unstudied, but crèche demands and chick weight gains suggest accelerated, even allometric growth to prepare chicks for crèche. At hatching, 7 boreal S. m. maxima chicks weighed 50–58 g (dry); at 2–3 d of age (just before joining crèche), 2 weighed 73 and 79 g; 9 still-downy chicks in crèche (8–10 d) averaged 138 g, and 6 prefledging juveniles in crèche ranged from 213 to 300 g.

Association With Parents Or Other Young

As juveniles begin to fledge with some synchrony, size of crèche may diminish rapidly, but often many still left, ranging from very small to near-fledging if late breeders in colony. After fledging, juveniles remain with parents (see Immature stage, below), constantly and noisily begging food, and form mixed feeding and roosting flocks with conspecifics of all ages. Juveniles follow parents to wintering grounds where same conspecific associations and food-begging persist.

Ability To Get Around, Feed, And Care For Self

Generally able to manage on own, although highest visible mortality seems to occur immediately post-fledging. Flying obviously inferior for some time, while foraging skills learned slowly over long period, so dependent on parents for food well into winter (see below).

Overwintering

Immediately postfledging, immature and adult boreal S. m. maxima (at least) disperse widely, often northward, until eventually migrating south to wintering grounds. Immatures follow adults and remain with them. Although data few, it seems immatures remain on wintering grounds for their second and third summers at least, perhaps moving increasingly northward with each subsequent spring until finally returning to breed.

Extended Parental Care

Royal Tern’s extreme parental care, first discussed by Ashmole and Tovar (1968), manifests itself in complex of complementary reproductive biology features including: delayed first breeding; single, large egg; crèching of young; parents’ vocal and visual recognition of own chick; extenuated time for juveniles’ learning fishing skills; and adults accompanying young to wintering ground and feeding it through the winter, perhaps until as late as Mar of year following hatch (it is assumed that adult Royal Terns attempt to breed annually, but unknown if they might not breed in alternate years, as do albatrosses [Diomedeidae] and other seabirds).

Adult-Juvenile Foraging Differences

Buckley and Buckley (1974) contrasted details of foraging behavior and time budget of adult and juvenile boreal S. m. maxima, through latter’s first winter in Netherlands Antilles, finding following differences: Adults spent less time foraging over given stretch of beach, making almost twice as many dives/min as juveniles; while initial prey-capture rates were the same in both age classes, adults dived more frequently, and therefore caught more prey/unit time; both rarely dropped prey without recovering it, but juveniles dropped prey and subsequently recovered it about 14 times as often as adults, thereby expending considerably more energy/prey capture than adults. Feeding adults avoided all other birds except their offspring, but when resting, avoided even juveniles more than expected. Feeding juveniles occurred almost equally frequently alone, with adults, or in small flocks (which adults never did on wintering grounds). Adults appeared to forage more in early-morning hours, resting or foraging for their young later in the day; juveniles apparently did most solo foraging between 09:00 and 12:00 and spent less day time roosting than adults. Lastly, band-recovery analysis confirmed that juveniles were caught significantly more frequently on fishhooks than adults, emphasizing that adults’ ability to recognize suitable prey was a prime factor in their fishing success and survival.