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Bayberries and Yellow-Rumped Warblers

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Bayberries and Yellow-Rumped Warblers The Auk 109(2):334-345, 1992 LIVING OFF THE WAX OF THE LAND: BAYBERRIES AND YELLOW-RUMPED WARBLERS ALLEN R. PLACE • AND EDMUND W. STILES 2 •Centerof MarineBiotechnology, University of Maryland,600 EastLombard Street, Baltimore, Maryland 21202, USA; and 2Departmentof BiologicalSciences, Rutgers-The State University of New Jersey, Piscataway,New Jersey08855, USA ABSTRACT.--Yellow-rumpedWarblers (Dendroica coronata) and Tree Swallows(Tachycineta bicolor)are among a small group of birds in temperateNorth America that regularly eat waxy fruits. During the autumn,winter, and spring,these species feed extensivelyon fruits of the bayberry (Myrica spp.). Covering the pulp of these fruits is a solid, waxy material consisting primarily of saturatedlong-chain fatty acids.For mostanimals, saturated fatty acidsare poorly assimilated(< 50%).Using 3H-glyceroltriether as a nonabsorbablefat marker, we determined that Yellow-rumpedWarblers are capableof high assimilationefficiences (> 80%)of bayberry wax when fed berries recoatedwith radioactivewax tracers.Efficient fatty-acidassimilation extendsto berriescoated with cetyl palmitate,a commonmarine, saturatedwax ester(> 90%). The fatty-alcoholmoiety of the marine wax was assimilatedwith a much lower efficiency (<50%). A beeswaxcoating of the berries is assimilatedwith an efficiencyof approximately 50%.Similar assimilationefficiencies of each wax are recordedfor Tree Swallows feeding on recoatedbayberries. Yellow Warblers(D. petechia)rejected recoated bayberries and exhibited little (< 5%) lipid assimilationof radiolabeledlipids. Yellow-rumped Warblerspossess several gastrointestinaltraits that permit efficient saturated-fatassimilation. Among these are an apparent retrograde reflux of intestinal contentsto the gizzard, elevated gall-bladder and intestinalbile-salt concentration, and a slow gastrointestinaltransit of dietary lipids. These gastrointestinaltraits permit efficient assimilationof saturatedfatty acidson bayberry fruits and may allow these small passerinesto maintain more northerly wintering rangesthan closelyrelated species.Received 24 May 1991,accepted 5 November1991. THE ASSOCIATIONbetween Yellow-rumped monly observed over much of its wintering Warblers (Dendroicacoronata) and Myrica (bay- range.The TreeSwallow winters along the coast, berry and wax myrtle) is one of the mostwidely occasionallyas far north as Massachusettsand recognized bird-plant associationsin North south into Central America. In autumn, large America (Brewer 1840, Hausman 1927, Martin flocks (some over 50,000; Stewart and Robbins et al. 1951). In fact, until 1983 one form of the 1958),move southalong the coastand may strip Yellow-rumped Warbler was referred to as the Myricashrubs of all fruits in a matterof minutes Myrtle Warbler(AOU 1983).A similarbird-fruit (E. Stiles, pers. observ.). relationship is found between Tree Swallows Generally, bayberry is found on dunes, old- (Tachycinetabicolor) and Myrica (Hausman1927). fields, and dry hills from Quebecto Louisiana; During the breeding season Yellow-rumped wax-myrtle typically is found on damp, sandy Warblers and Tree Swallows feed primarily on soils from New Jersey to Florida and Texas insects,but during the autumn, winter, and (Gleason and Cronquist 1963). Fruits ripen in spring their diets include large proportions of August through October and persistwell into fruit, especiallybayberry (Myricapennsylvanica the winter, providing an energy-rich resource Loisel.),wax-myrtle (M. ceriferaL.) and M. pus- for birds residing or wintering in northern and silla Raf. coastalregions of the United States. In easternNorth America, the Yellow-rumped Bayberry pulp includes a waxy coating of Warbler winters from central Maine and south- mono-and diglyceridesof myristic,palmitic and ern Nova Scotia, west to Kansas and Missouri, stearic fatty acids. Most animals exhibit low as- and south to Panama, which coincides with the similation (<50%) of these high-melting-point entire range of the above Myrica species.The lipids. For example, with chickens,absorption Yellow-rumped Warbler is the most northerly of thesefatty acidsdecreases monotonically with wintering wood warbler, and it is very com- increasingmelting point (Rennerand Hill 1961; 334 April 1992] BayberryWax and Yellow-rumped Warblers 335 Fig. 1). Similar results have been documented 100' in rats feeding on high-melting-point triglyc- erides (Clifford et al. 1986). 80- It may be that Yellow-rumped Warblers and Tree Swallows are able to successfullyoccupy 6O northern regions in winter becausethey can assimilateefficiently the high-melting-point 4O fatty acidsin bayberrywax that few fruit-eating animalscan digest.To investigatethe capacity 2O of Yellow-rumped Warblersand Tree Swallows 0 to assimilatewaxy coatingson bayberries,we removed the natural wax from bayberriesand -20 recoatedthem with radioactivelylabeled lipids. 2'0 4'0 6'0 80 We includedbayberry wax in our coatings,as well astwo othernaturally-occurring solid wax- Melting Point (øC) es known to be eatenby birds--cetyl palmitate Fig. 1. Absorbabilityof fatty acidsvs. melting and myrcin--the alcohol-insolublefraction of points in domestichens (solid squares)and chicks beeswax.Wax esters,like cetyl palmitate, are (opensquares; Renner and Hill 1961).Melting points majorfood sources for high-latitudemarine an- of saturatedfatty acids increase with chainlength and decreasewith degreeof unsaturation.Feeding studies imals, especiallypelagic seabirds(Roby et al. performedwith unesterifiedfatty acids.Saturated fat- 1986, Place and Roby 1986, Jacksonand Place ty acidsused were myristic,palmitic and stearicacid. 1990),and myrcin is consumedand digestedby Unsaturatedhomolog of stearicacid (i.e. oleic acid) Black-throatedHoneyguides (Indicator indicator; wasassimilated at greaterthan 85%efficiency. Diamond and Place 1988). We also measured the rate of bayberry-fruit consumptionof cap- tive Yellow-rumped Warblerswith fruits avail- able ad libitumto assesswhether fruit handling cation, an aliquot of extractedwax was hydrolyzed might limit ingestion rates. Finally, we char- with methanolic HCL, the methyl esters extracted acterized in Yellow-rumped Warblers the bili- into hexane,and an aliquot of the hexaneextract sub- jected to gas chromatographydirectly on a Hewlett- ary and pancreatic components known to be Packard model 5890A instrument fitted with a DB-% essentialfor efficient lipid assimilationin other column (30 x 0.25 mm i.d., 0.25-/•m-thick film, J. & species(Carey et al. 1983). W. Scientific Inc., Rancho Cordova, California) and a flame ionization detectorat 280øC.The oven temper- IV[ATERIALSAND METHODS ature was programmedfrom 50 to 255øCat a heating rate of 18øCmin • up to 125'C (thereafter4'C min-'). Studyspecies.--Yellow-rumped Warblers and Yel- Helium was usedas carrier gaswith a flow rate of 3.6 low Warblers(Dendroica petechia) were capturedwith ml min -1 . mist nets on 10 March and 7 November 1986 at the De-waxed bayberrieswere recoatedwith radioac- RutgersEcological Preserve in Piscataway,New Jer- tively-labeledwaxes by placing them in a melt of one sey. The Yellow-rumpedWarblers had been eating of the following materials:(1) bayberrywax contain- bayberry at the time of capture.Captured birds were ing 9.1 /•Ci of 3H-GTE/berry and 6.99/•Ci of [1-a4C] held at roomtemperature in darkenedholding cages palmiticacid/berry; (2) cetylpalmitate containing 7.33 until initiation of experimentson the sameday or the /•Ci of •H-GTE/berry and 5.5/•Ci of [1-a4C]cetyl pal- following morning.During the two- to three-daycap- mitate/berry or 4,7/•Ci of cetyl [1-'4C]palmitate/ber- tivity, birds were given water and food regularly ry; (3) myrcin (alcohol-insolublefraction of beeswax) (strainedpeaches and pears baby food mixed with containing 9.1 /•Ci of •H-GTE/berry and 8.2 /•Ci of hard-boiledegg). The TreeSwallows used in our study triacontanol[1-a4C] palmitate/berry. Each berry was were part of an experimentalcolony at the Monell recoatedwith 6 to 10 mg of lipid. Institute. Bayberry fruit structure was examined with and Bayberrywax removal and recoating.--Bayberries were without the wax coatingwith an Hitachi S-450Ascan- de-waxedby placingthem in a 2:1 mixtureof hexane ning electron microscopeusing an acceleratingvolt- and chloroformat roomtemperature for 15 min. The age of 10 KV. berries then were removed and air dried for 24 h. Feedingstudies.--Twelve Yellow-rumped Warblers The bayberry wax (24.3% of fruit mass or 54.1% of were included in the feeding trials with recoatedra- pulp mass)was recoveredby removing the solvent dioactively-labeledbayberries. Five were spring-cap- under nitrogen. For fatty-acidmethyl esterquantifi- tured birds (three males and two females), and seven 336 PLACEA!qD STILES [Auk,Vol. 109 were fall-captured birds (four males and three fe- used in the radiometric scanning was P-10 (90% ar- males).Sets of three birds were fed each type of re- gon, 10% methane) at a flow rate 0.5 to 1.0 L min-'. coatedbayberry. Only two Tree Swallowswere tested The spatial resolution for each scanwas set at 4 mm. (each three times). We also attempted feeding trials The distribution of label among the lipid classeswas with six Yellow Warblers.Two to three recoatedbay- estimated by integration of the counts under each berries were force fed to each bird. All birds took the peak after subtractionfor background.The overall feeding without regurgitationexcept for Yellow War- counting efficiencyfor •4Caveraged 10.5%, while that biers. for 3H averaged0.5% acrossthe plate. Labeled
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