Royal Tern Nesting Attempts in California: Isolated Or Significant Incidents?

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ROYAL TERN NESTING ATTEMPTS IN CALIFORNIA: ISOLATED OR SIGNIFICANT INCIDENTS?

FRED C. SCHAFFNER, Department of Zoology, San Diego State University,San Diego, California 92182 (presentaddress: Department of Biology, Universityof Miami, P.O. Box 249118, Coral Gables, Florida 33124)

Only four nestingattempts are knownfor the Royal Tern ($tema maxima) in California, all at the San Diego Bay salt evaporatingponds. This paper describesthe two mostrecent nesting attempts in detailand discussesall four attemptsin terms of coincidentalevents in California fish stocksof the close inshore area.

PREVIOUS NESTING RECORDS The firstknown nestingattempts in Californiaby both the Royal Tern and ElegantTern ($. elegar•$)occurred in 1959 on the dikes separatingthe salt evaporatingponds at the south end of San Diego Bay, San Diego County, California(Gallup and Bailey 1960). The attempt, by a singlepair of Royal Terns, failed. The egg was collectedby Gallup and is on deposit at the Western Foundation of Vertebrate Zoology, Los Angeles (WFVZ 114, 199-1). It measures 62.8 x 44.9 min. In 1960 a second nesting attempt was reported without details (Small 1960) to have involvedat least30 nestsand producedmany young, but no nestsof this specieswere found in 1961 (Small 1961).

RECENT NESTING ATTEMPTS In spring of 1980 a singlepair of Royal Terns attempted to nest on the saltworksdike separatingponds 35 and 33 (circled"a," Figure 1) in the colonyof ElegantTerns, which numbered607 breedingpairs in 1980, 861 in 1981 and 800 in 1982. The nestscrape with itssingle egg was locatedon the periphery of a group of 32 ElegantTern scrapes.Amongst this group also were three CaspianTern ($. caspia)nests--two containingtwo eggsand one containingthree eggs. (The number of Caspian Tern breedingpairs at the saltworkswas roughly400 in 1980 and 1981 and roughly 350 in 1982.) I discoveredthe Royal Tern eggon 9 May and at that time one RoyalTern could be seen nearby. Later that afternoon, from a vantage point off the breedingdike, I saw two Royal Ternstogether at the nest and observedthem for about 2 hours, until darknessset in. On 11 May I did not see the Royal Ternsat the nest site and I found the egg with a number of punctureholes, crackedand lyingin a pool of its own formercontents. This was apparently the work of Ruddy Turnstones(Arer•aria ir•terpres), which I had previously observeddestroying Elegant Tern eggs in a similarfashion, much like the Ruddy Turnstonepredation on Sooty Tern ($. fuscata) eggs on Eniwetok Island (Crossinand Huber 1970). Within a few daysthe Royal Ternswere no longer seen in the area. I collectedthe damagedegg and depositedit at the WesternFoundation of VertebrateZoology (WFVZ 125, 645). It measures68.0 x 40.8 mm, which comparesfavorably with other eggsin the WFVZ collection,as well as with

Western Birds 16:71-80. 1985 71 ROYAL TERN NESTING ATTEMPTS the measurementsof 63 x 45 mm suggestedby Harrison(1978) as average for Royal Tern eggs. The most recent breeding by Royal Terns occurred at the San Diego saltworksduring 1982. On 8 May I discoveredtwo Royal Tern nest scrapes, eachwith a singleegg, in a groupof about230 ElegantTern nest scrapes atop the north to southrunning arm of dike 33/5 (circled"b," Figure1). The first nestwas with a groupof three ElegantTern nests,placed about 1 m from the south edge of the large ElegantTern nestinggroup. The secondnest was about 10 m north of the firstnest, towards the middleof the largeElegant Tern nestinggroup and on its westernperiphery. The egg of the firstnest measured62.4 x 42.3 mm and had an off-white groundcolor with an approximatelyrandom pattern of medium-to-largedark brown spots,and was similarin appearanceto the 1980 egg. The egg of the secondnest had a palebeige or buffground color and wascompletely covered with a rather uniform pattern of small-to-medium dark brown spots. It measured 62.9 x 42.8 mm. On 10 June the firstnest contained a chickwhich may have hatchedup to 2 dayspreviously. The chickhad bright orange legs and bill.Its down wasa pale yellowcolor, lightlyoverlaid with smallbrown spots. On 18 June the secondnest contained a chick which was approximately3 days old. This chickalso had brightorange legs and bill but its down was a medium yellow-beigecolor, heavily overlaid with medium-to-largedark brown spots. On this visit I banded both chicks (USFWS bands 664-81701 and 664-81702), each on the left leg. I alsoexamined the nestscrapes and in the first nest I found two Northern Anchovies (Engraulisrnordax) measuring6.0 and 7.2 cm, standardlengths. I alsorecovered a regurgitationconsisting of a small6.2 cm (standardlength) Northern Anchovy from the older chick. The regurgitationsof the smallerElegant Tern chicks consisted of largerspecimens of E. rnordax,ranging from 8.0 to 13.2 cm (standardlength) and averaging 10.0 to 11.0 cm (standardlength). After the banding and above-mentionedcollections were completed,the older chick becameambulatory while the youngerchick remained quiet in its nest. On 23 June both Royal Tern chickshad entered the creche (nursery flock)of ElegantTern chicks. On thisvisit and againon 1 JulyI recoveredboth chicksfrom the creche and collectedtheir regurgitations.The regurgitations consistedprimarily of partiallydigested tail pieces. These appeared to be fragmentsof fairly large (15 to 20 cm) atherinids,probably the very common Topsmelt(Atherinops affinis). Some fragments were probablysurfperch (Em- biotocidae).I also recovereda 5.5 cm (standardlength) specimenof an anchovy, Anchoa. Interestingly,on all visitsup to 23 June eachRoyal Tern chick was attended by both parents,unlike the ElegantTern chicks which were usuallyattended by only one parent or left unattendedin the creche. On 1 July I found the youngerchick attended by both parentsand the older chickattended by a singleparent. Duringthe lastweek of May 1982 the ElegantTern colony was invaded by a pair of straydogs. They destroyeda sectionof the colonyon the northeastto southwestrunning arm of the dike 33/5 and on dike 36/37 (Figure1) which

72 ROYAL TERN NESTING ATTEMPTS

San Diego Bay

Silver Strand Chula Vista State Beach Wildlife Reserve

Chula Vista

SouthBay Biol. StudyArea Salt Company

Main St.

Naval Communication Station

ImperialBeach ImperialBeachBlvd.I• , Ream Field

Tijuana River Ave. Estuarine Sanctuary

Border Field StatePark

Figure 1. The south San Diego Bay area includingthe salt evaporatingponds and the Ti)uana River sloughs(Tijuana River EstuarineSanctuary): a = the locationof the un- successful1980 Royal Tern nestingattempt: b = the location of the 1982 successful nestingby two pairs of Royal Terns. 73 ROYAL TERN NESTING ATTEMPTS had few nestsof aggressiveCaspian Terns associated with it, leavingthis area almostcompletely unprotected. I found over 100 dead ElegantTern chicks, all badlymauled. Many morechicks were missing.Fortunately, however, the sectionof the colonyin whichthe RoyalTern chickswere locatedhad many associatedCaspian Tern nests.The dogsnever penetratedthis area and both Royal Tern chickswere seenin the crecheagain on 19 June, capableof short hop-and-glideflights. By thistime the RoyalTern chicks were visitedonly intermittentlyby one or both parentsand, by 1 August,either chick could be seenflying, following one or both of its parentsover the saltworksor over the Tijuana River sloughs (Tijuana River EstuarineSanctuary, Figure 1), where the Royal Terns fre- quently foraged. On such occasionsthe parent that was followed usually carried a large fish. I was seldom able to identify positivelythe fish being carried,but in very few instancesdid the fishshow the familiarsilver and black appearanceof E. mordax, whichconstitutes the greatbulk of the ElegantTern diet (Schaffner1982). I tentativelyidentified most of thesefish as Atherinidae, again, probablyTopsmelt.

DISCUSSION Although there may have been other intermittentbut unreportedRoyal Tern nestingattempts at the San Diegosaltworks during the past25 years,the possibilityseems unlikely, given the many very competentobservers visiting the saltworksover the years. The nearestRoyal Tern breedingcolony is on Isla Raza, Mexico, roughly 600 km south of San Diego in the Gulf of California, Mexico, where they breedin mixed groupswith ElegantTerns and Heermann'sGulls (Larusheer- manni; Walker 1965, Lindsay 1966). A portion of the populationsof all three speciesmigrates north into Californiaat the closeof each breedingseason and this site is almostcertainly the point of originof the Royal Ternswhich nested at San Diego, aswell as the San Diego ElegantTern breedingpopulation itself, as Isla Raza appearsto be the closestand largestregularly active colony. Schaffner (1982) discussedthe dependence of California Elegant Terns (bothbreeding and visiting)on E. mordax, notingthat the establishmentof the San Diego ElegantTern breedingpopulation coincided with the expansionof Engraulis stocks in southern California waters and that current seasonal movementsof California ElegantTerns and Engraulisare roughly similar. Royal Terns,however, have not followedthe sametrends as ElegantTerns in California.Although Royal and Elegantterns typicallyoccur together in San Diego Bay immediatelybefore and after the nestingseason, visiting Royal Terns occur in California relativelymore often in winter and lessoften in fall and spring,in contrastto ElegantTerns, which are more commonlyseen in the fall and the springthan in winter. What is especiallyinteresting is that the occurrenceof the Royal Tern in California has, except perhapsfor these recent years, decreased markedly since 1950 (Cogswell 1977). Thus, the historicaloccurrence of the Royal Tern in California is unlikelyto have been related to Northern Anchovy abundanceand distributionbut is likely to be related to the abundanceand distributionof the PacificSardine ($ardinops sagax), which experienced a tremendouspopulation crash in the 1940s resultingin near extinctionby 1950 (MacCall 1979, 1984). Ainley and Lewis 74 ROYAL TERN NESTING ATTEMPTS

(1974) and Baldridge(1973) presentedvery good evidenceregarding the severeimpact of the disappearanceof PacificSardines on cormorants,puffins andespecially on BrownPelicans (Pelecanus occidentalis) in Californiawaters farther north (FarallonIslands and Monterey). Althoughthe commercialsardine fishery was primarilycentered around Monterey,the PacificSardine was very widely distributed throughout Califor- nia waters, extendingfrom far offshoreto shallowinshore areas (Murphy 1966. 1968). Accordingto many old-timefishermen in the San Diego area, duringtheir peak populationyears such as 1936. sardinescould be foundin greatabundance inshore within the breakersand just a few metersfrom the beach. With the possibleexception of E. mordax during its period of peak abundancein the 1960s (Smith 1972. Smith and Eppley 1982). there has thusfar been no significantreplacement of the PacificSardine by any species in close inshore areas. The closeinshore components of the sardineand otherfish populations are of particularinterest because the RoyalTern tends to be a warm-waterlittoral speciesand is primarilyan inshorecoastal forager (Murphy 1936, Buckley and Buckley 1972, Blake 1977), in contrastto the small-bodied"crested terns" (Thalasseussubgenus; AOU 1976) such as the ElegantTern, which tends to forage farther offshore (Schaffner 1982). Furthermore,the other large-bodiedcrested tern, the Swift or (Greater)Crested Tern ($. bergii), is also an inshoreforager (Ashmole 1968, Hue and Etchecopar1970, Henry 1971, Feare 1975, Etchecoparand Hue 1978); in Australia $. bergii is recognizedas an indicatorof shoals(schools) of Pilchard,a $ardinopssardine (Serventyet al. 1971). Sardineabundance in Californiaremained extremely low duringthe 1950s, but during a warm-water period from 1957 to 1960, PacificSardine (and Engraulis)stocks briefly improved (MacCall 1979, 1984). RoyalTerns nested in San Diego in 1959 and 1960 (Gallupand Bailey 1960; Small 1960, 1961), and many other marine organismsalso extended their rangesnorthward during 1957 to 1960 (Radovich1960, 1961). Like most of the other crested terns, the Royal Tern tends to be non- aggressivetowards most potential predators and may require the presenceof other,more aggressivelarids at itsbreeding colonies for protection,in addition to topographicalrequirements such as relativelyisolated locations with good visibilityof surroundings.In EuropeanSandwich Tern (S. sandvicensis)col- oniesthis protectionis provided by the Common Black-headedGull (Larus ridibundus;Veen 1977), and in southeasternU.S. Royal Tern colonies,protection may be provided by the Laughing Gull (L. atticilia; Buckley and Buckley 1972). In coastal California an important aggressivepredator- mobbinglarid is the CaspianTern, whichprovides the San DiegoElegant Tern colony with predator protectionin a fashionsimilar to that of the medium- sizedgulls mentioned above (Schaffner1982). Thus, the prior establishment ca. 1940 of the Caspian Tern breedingcolony (Emblen 1954, Schaffner 1982, Gill and Mewaldt 1983) was probablya prerequisitefor Elegantand Royal tern breedingat the San Diego saltworks. Consideringthe above, it is unlikely that any adequate breedingsite for RoyalTerns existed within easy reach of the food supplyduring the periodof peak Sardinopsabundance. Significant Caspian Tern breedingcolonies did 75 ROYAL TERN NESTING ATTEMPTS

Figure 2. Royal Tern (foreground}and Elegant Tern at San Diego, May 1982.

Figure 3. Nesting Royal Tern (centerforeground} with nestingElegant and Caspian lerns at San Diego, May 1982.

76 ROYAL TERN NESTING ATTEMPTS

Figure 4. Royal Tern egg (of first nest of 1982 at San Diego), center, compared Elegant Tern egg (left) and Caspian Tern egg (right).

Figure5. Chick of firstRoyal Tern nestof 1982 at San Diego, in its nests•rape. Photos by Frea' C'. Schaffner

77 ROYAL TERN NESTING ATTEMPTS not exist in coastalCalifornia at that time; the establishmentof the San Diego and other coastalCalifornia breeding colonies was apparently the resultof ex- tensive alterationof inland nestinghabitat between 1910 and 1940 which forced Caspian Terns to seek other nestingareas. The major California CaspianTern colonies now occuralong the coastand, likethe San Diegocol- ony, tend to be associatedwith human-createdhabitats (Gill and Mewaldt 1983). The recentsuccessful nesting of two pairsof Royal Ternsis in part also due to the presenceof the ElegantTerns, with whom they sharethe important socialcharacteristics of extremelydense and gregariousnesting groups and creche formation. The recentCalifornia Royal Tern breedingprobably indicates some degree of changein the localcoastal marine environment and itsfish fauna. Southern Californiacoastal waters have been experiencinga slightwarming trend over the past few years (Alec MacCall pers. comm. 1982) and there has been a slight increasein Pacific Sardine abundance as well, though this change shouldin no way be taken as the beginningof a recovery (Klingbeil1981). The importantfactors relevant to RoyalTern breeding in California,however, arethe abundanceand availabilityof closeinshore schooling fishes in general, and not Sardinopsper se. The fishesof greatestinterest are the atherinidsand engraulidswhich in- habit the severalriver mouths and adjacent estuariesof northern San Diego County, the shallowwater areas of the Coronado Islandsand especiallythe TijuanaRiver sloughs, a principalforaging area for the Royal Ternswhich bred at San Diego. Atherinidsof variousage classesare common and abundant and may be increasingin the Tijuana River sloughsand adjacentareas; and, although detailed information is as yet unavailable, some circumstantial evidencesuggests an increasein the abundanceof larvaland juvenilestages of the engraulid,E. mordax. Larval and juvenileEngraulis of up to about 6.0 cm standard length have become increasinglyapparent over the past two breedingseasons (1981 and 1982) at the nestsites of the 1000 or so Forster's Terns (S. forsteri) which breed at the San Diego saltworks. Engraulis specimensof up to 1 year of age (roughly10.0 cm standardlength; Huppert et al. 1980) were first observedat Caspian Tern nest sitesin 1981 and were quite apparent in 1982. Specimensof 1- to 2-year-old Engraulismeasuring 11.0 to 15.0 cm were commonly found at Caspian Tern nests in 1981, somewhat lesscommonly in 1982, but not at all in 1980. Yet, Engraulisis a minor component of the local Caspian Tern diet, the major component being the large 15.0 to 25.0 cm Topsmeltfrom the Tijuana River sloughsand other nearby coastalsaltwater and brackishwater areas. Additional circumstantial evidence of an increase in the abundance of close inshore fishes comes from Black Skimmers (Rynchopsniger), which first began breeding at the San Diego saltworksin small numbers during the mid-1970s (Gerald Collier, Michael Evansl•ers. comm.). The BlackSkimmer populationincreased to some 60 pairsin 1982. Fishescollected at their nest sitesinclude 2.0 to 6.0 cm LongjawMudsuckers (Gillichthys mirabilis), 4.0 to 6.0 cm CaliforniaHalibut (Paralichthyscalifornicus) and an abundanceof larval and juvenileatherinids and engraulidsmeasuring up to about 7.0 cm. Dur- ing 1982, engraulidsmeasuring 4.0 to 6.0 cm and Paralichthysof similar lengthswere especiallyapparent. 78 ROYAL TERN NESTING ATTEMPTS

SUMMARY Royal Terns visitingCalifornia prior to 1950 probably relied heavily on PacificSardines as a food source. At presentRoyal Terns appear to feed on atherinidsand engraulids.The establishmentof the Caspian Tern breeding colony at San Diego was probablya prerequisitefor the utilizationof that site by bothRoyal and Elegantterns. The recent(1980, 1982) RoyalTern nesting attemptsin Californiamay not be mere isolatedincidents, but may indicateat leastlocal changes in the coastalmarine environment and itsfish fauna, par- ticularly increasesin some close inshore fish stocks. Future increasesor decreasesin the abundanceand frequencyof occurrenceof both visitingand nestingRoyal Ternsare likelyto reflectsimilar changes in the abundanceand availabilityof their food supply.

ACKNOWLEDGMENTS I wish to thank the WesternFoundation of VertebrateZoology for accessto its egg collectionand Ed Hamilton who measuredthe Gallup egg. For many usefulcomments and suggestionsI wish to thank Alec MacCall, Howard L. Cogswelland Michael Evans. This is Contribution 151 of the program in Ecology, Behavior and Tropical Biology of the Department of Biology, Universityof Miami.

LITERATURE CITED

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79 ROYAL TERN NESTING ATTEMPTS

Hue, F. & R.D. Etchecopar.1970. Les oiseauxdu Procheet du Moyen Orient. Editions Boubee et Cie, Paris. Huppert, D.D., A.D. MacCall, G.D. Stauffer,K.R. Parker,J.A. McMillan& H.W. Frey. 1980. California'sNorthern Anchovy fishery: biologicaland economic basisfor fisherymanagement. NOAA Tech. Memorandum, SouthwestFisheries Center, La Jolla, CA. Klingbeil, R.A. 1981. Status of the spawning biomass of the Pacific Sardine 1980-1981. California Dep. Fish & Game, Marine ResourcesAdmin. Rep. No. 81-1. Lindsay,G.E. 1966. The gulf islandsexpedition of 1966. Proc. California Acad. Sci. Ser. 30:309-355. MacCall, A.D. 1979. Populationestimates for the waning years of the PacificSardine fishery.California Coop. Fish. Invest. Rep. 20:72-82. MacCall, A.D. 1984. Seabird-fishery trophic interactions in the eastern Pacific boundary currents: California and Peru. Pp. 136-148 in D.N. Nettleship, G.A. Sanger& P.F. Springer,eds. Proc. EighthAnn. Meet. Pac. SeabirdGroup. Spec. Publ. Canadian Wildl. Serv. Murphy, G.I. 1966. The population biology of the Pacific Sardine (Sardinops caerulea). Proc. California Acad. Sci., 4th Sen, 34:1-84. Murphy, G.I. 1968. Vital statisticsof the PacificSardine (Sardinopscaerulea) and the populationconsequences. Ecology 48:731-736. Murphy, R.C. 1936. Oceanic birds of South America. 2 vols. Am. Mus. Nat. Hist., New York. Radovich, J. 1960. Redistribution of fishes in the eastern North Pacific Ocean in 1957 and 1958. California Coop. Fish. Invest. Rep. 7:163-171. Radovich, J. 1960. Relationshipsof some marine organismsof the northeastPacific to temperaturesparticularly during 1957 through 1959. California Dep. Fish & Game Fish. Bull. 112. Schaffner,F.C. 1982. Aspectsof the reproductiveecology of the ElegantTern (Sterna elegans)at San Diego Bay. M.S. thesis,San Diego State Univ., San Diego. Serventy, D.L., V.N. Serventy & J. Warham. 1971. The handbook of Australian sea-birds.A.H. & A.W. Reed Ltd., Sydney. Small, A. 1960. Southern Pacificcoast region. Audubon Field Notes 14:421,477. Small, A. 1961. Southern Pacificcoast region. Audubon Field Notes 15:439. Smith, P.E. 1972. The increasein the spawningbiomass of the Northern Anchovy Engraulismordax. Fish. Bull. (U.S.) 70:849-874. Smith, P.E. & R.W. Eppley. Primary productionand the anchovypopulation in the southernCalifornia bight: comparisonof time series.Limnol. Oceanogr.27:1-17. Veen, J. t977. Functional and causal aspectsof nest distributionin colonies of the SandwichTern ($terna s. sanduicensisLath.). BehaviourSuppl. 20. Walker,L.W. 1965. Baja'sisland of birds. Pac. Discovery18 (4):27-31.

Accepted 17 November I984