Download DO SEEDS HINDER DIGESTIVE PROCESSING OF FRUIT PULP

The Auk 115(2):319-326, 1998
DO SEEDS
HINDER
IMPLICATIONS
DIGESTIVE
PROCESSING
FOR PLANT/FRUGIVORE
MARK
OF FRUIT
PULP?
MUTUALISMS
C. WITMER •
Sectionof Ecologyand Systematics,
CornellUniversity,Ithaca,New York14853, USA
ABSTRACT.--The
seedsof bird-dispersedfruits could impose significantcostson frugi-
voresif seedbulk reducesthe effectivecapacityof the gut and, hence,reducesthe rate of
nutrientintake.This hasled to the notionthat avianfrugivorespassfoodthroughtheir digestivetractsrapidly to minimizethe effectsof seedson nutrientacquisition.Consequently,
avianfrugivoresare thoughtto utilize fruit sugarsinefficiently,
because
thispermitshigher
intakeand sugar-assimilation
ratesfrom a supposedlyenergy-dilutefood.I evaluatedthe
influenceof seedbulk on intake and absorptionof sugarsfrom chokecherryfruits (Prunus
virginiana)by Cedar Waxwings(Bombycilla
cedrorum),
AmericanRobins(Turdusmigratorius
),
WoodThrushes(Hylocichla
mustelina),
Gray-cheeked
Thrushes(Catharus
minimus),
andHermit Thrushes(Catharus
guttatus).I comparedCedarWaxwingswith thrushesto determine
if they differed in how seedbulk affectsdigestionof fruit. Cedar Waxwingshavehigher
mass-specific
intakeratesof sugaryfruitsthan do thrushes;because
waxwingsdefecateall
seeds,whereasthrushesregurgitatemany seeds,the differencein intake of sugaryfruits
betweenwaxwingsand thrushesmay resultfrom ingestion/fruit-processing
limitationsassociatedwith modeof seedprocessing.
Forall species,
seedsdid not reduceratesof intake
andsugarabsorption
fromchokecherry
fruit pulp.All birdsassimilated
sugarsfromchokecherryfruits efficiently,and digestiveprocessing
of seedsdid not reducesugarabsorption.
Ratesof fruit processingwere closelytied to ratesof sugarabsorption,rather than to the
physicalcomposition
of thediet.My resultssuggest
thatcurrentmodelsof digestivefunction in avianfrugivoresare seriouslyflawed.Becausedifferences
in intakeratesof sugary
fruits betweenwaxwingsand thrusheswere independentof the presenceof seeds,these
differenceswere not due to differentmodesof seedprocessing.Received
13 January1997,
accepted
18 August1997.
THE
MUTUALISTIC
RELATIONSHIP
between
plantsthatproducefleshyfruitsandvertebrate
seed dispersersis well known (Snow 1971,
McKey1975,Pijl 1982,Wheelwrightand Orians1982).Dispersers
benefitfromthenutrient
rewardsof fruit pulp, primarily sugarsand lipids (Herrera 1987, White 1989, Witruer 1996),
whereasplantsbenefitfrom the depositionof
seedsin suitablehabitatawayfrom thevicinity
of parent plants. Many studieshave demonstrated
increased
survival
of seeds and seed-
lings away from parent plants (Janzen1972,
Howe and Primack 1975, Webb and Willson
vores,theoreticalconsiderations
have argued
thatthereare coststo mutualisticpartners.Presumably,the costto plantsis in the resources
that they allocateto producingfruit pulp that
hasnopurposeotherthanto attractdispersers
(Howe 1993).Somefruits are photosynthetic,
suggesting
a mechanism
by whichplantsmay
minimizethe costsof fruit production(Cipollini and Levey 1991). Seed dispersers are
thoughtto incur costsassociated
with ingestion of seedsin at leastthreeways:(1) the energyrequiredto carryseedsin the gut,(2) the
energyrequiredto manipulateseeds,and (3)
theoccupation
of gutvolumewith indigestible
bulk that reducesthe rate at which fruit pulp
can be processedand nutrients assimilated
(Snow 1971, McKey 1975, Howe and Vande
1985). The specializeddispersalsystemsof
mistletoesillustratethe importantrole of dispersersin depositingseedsat appropriatesites
(Reid 1989,Murphy et al. 1993,Sargent1995,
Martinez del Rio et al. 1996).In additionto the
Kerckhove 1980, Herrera 1981, Sorensen1984,
benefitsaccruedby fruiting plants and frugiLevey and Grajal 1991, Murray et al. 1993).
Measurementsof these costs are scarce (see
•Present address: Department of Biology, Bryn Leveyand Grajal 1991,Murray et al. 1993),and
Mawr College, Bryn Mawr, Pennsylvania19010, no work has addressed how seeds in natural
fruits affect avian dispersers.Here, ! evaluate
USA. E-mail:mwitmer@brynmawr.
edu
319
320
MARKC. WITMER
[Auk, Vol. 115
the hypothesisthat seedslimit ingestionand
assimilationratesof sugarsfrom fruit pulp by
frugivorousbirds.
Severalstudieshavedevelopedthe ideathat
the indigestible seed bulk of fruits reduces
rates of nutrient assimilationby birds. Levey
and Grajal (1991)found that Cedar Waxwings
(Bombycilla
cedrorum)
fed two kinds of artificial
diets with different seedsizesbut equal seed
loads(seedvolumeper total fruit volume;seed
loadheld constantby adjustingthe numbersof
seedsper fruit) passedlarge seedsfasterthan
small seedsand consumedthe large-seeded
atedwith thisnutrient-basedpatternof diet selection,waxwingshave higher (ca. 1.5 times)
mass-specific
intake ratesof sugaryfruits than
do thrushes,and waxwingsalwayspassseeds
throughthe digestivetract, eliminatingthem
by defecation.
In contrast,thrushesregurgitate
mostmediumto largeseeds(>90% for choke-
small-seeded
ferences in intake
cherryfruits), a trait that may be associated
with efficientdigestiveprocessing
of fattydiets
(Witmer1994).The hypothesisthat passageof
seedsthroughthe digestivetractreducesrates
of nutrient intake and absorption(Levey and
Grajal 1991,Murray et al. 1993)leadsto the
fruits at faster rates. This result led them to
predictionthat seedsshouldreducesugar-asproposethat CedarWaxwingsare process-rate similationrates to a greater degree in Cedar
limitedwheneatingsugaryfruits,i.e.thatwax- Waxwingsthan in thrushes.Alternatively,uniwingsingestfruits as fast as they can process directionalpassageof seedswithin fruits conthemthroughthe gut, and that seedsrepresent taining readily assimilatedsimplesugarsmay
a significantcostbecausegutvolumethatcould enablebirds to achievehigherratesof fruit incontainnutritiousfruit pulp is occupiedby in- take and processingthan when seedsare redigestibleseeds.In a parallelstudy,Murray et gurgitated;i.e. flow of foodthroughthedigesal. (1993)found that AmericanRobins(Turdus tive tract canproceeduninterruptedby the remigratorius)
consumedlarge-seeded
fruitsfast- versal of flow from stomach to mouth that ocer than small-seededfruits. They alsoinvoked curs during regurgitation.If passageof seeds
gut-processing
limitations,attributingtheir re- throughthe digestivetractfunctionsto permit
sultto thefactthatrobinsregurgitatedseedsof high intake and processingrates of sugary
large-seededfruits and defecated seeds of fruits, then removal of seedsshould reduce diffruits.
The idea of limitation
of
rates between
Cedar
Wax-
gut-processing
ratehasfosteredthecontention wings and thrushes.
that avian frugivoresprocessfoods rapidly
METHODS
throughtheirgutsandutilizefruit nutrientsinefficiently. Presumably,rapid gut-processing I evaluated the influence of seed bulk on intake
rates are a result of selectivepressuresto re- and assimilationratesof sugarsfrom a natural fruit
duce the retentiontime of indigestibleseeds diet, chokecherry(Prunusvirginiana),by CedarWaxwithin the digestivetract becauseof high en- wings (mean body mass = 36.0 _+SD of 3.5 g, n =
ergy requirementsand volumetricconstraints 4), American Robins (72.0 + SD of 6.6 g, n = 4),
on gut capacityof frugivorousbirds. One hy- Wood Thrushes(Hylocichlamustelina;60.0 -+ SD of
Thrushes(Catharus
minpothesizedconsequence
of this scenariois the 11.4g, n = 4), Gray-cheeked
evolutionof rapidly assimilatedsimplesugars imus;38.7 + SD of 4.1 g, n = 2), andHermitThrushes
asnutrientrewardsin fruit pulp.Evenso,avian (Catharusguttatus;28.3 + SD of 1.0 g, n = 2). These
NorthAmericanfrugivores
commonly
eatcherries
in
frugivoresare reputedto utilize fruit sugarsin- the wild (Martin et al. 1951,Wheelwright1986,Witefficiently,presumablybecausethis permits mer 1996).Birdswerelong-termcaptives(morethan
rapid fruit-processing
ratesthatresultin high- one year) that had been maintained on a diet of
er ratesof sugarassimilationfrom supposedly moistened Eukanuba Brand Small Bites Puppy
Chow and wild fruits. Chokecherryfruits were colenergy-dilutefruits.
Differences in dietary specializationand lectedin September1990and storedfrozenuntil the
modes of seed processingbetween waxwings experiment.Becauseof the relatively small gape
andthrushessuggestthat seedbulk hasdiffer- width of Hermit Thrushes and Gray-cheeked
Thrushes,these two specieswere fed fruits of a
ent consequences
for digestive processingof smalleraveragesizethan thosefed to the otherspefruit by thesetwo groupsof birds.In the wild, cies.Both fruit batcheswere collectedfrom single
Cedar Waxwings selecta diet dominatedby shrubclustersat peak ripenessto maximizeuniforsugaryfruits, whereasthrushesconsumeboth mity amongindividualfruits.Thawedchokecherries
sugary and fatty fruits (Witmer 1996).Associ- were similar in appearance and texture to fresh
April1998]
DoSeeds
LimitIntake
ofFruits?
321
fruits.Watercontentof fruit pulp fromthebatchfed
mayinflateestimates
of turnovertime,themethodis
to Cedar Waxwings, American Robins, and Wood
Thrusheswas72%,andsugarcontentof thedry pulp
intended only to show the approximate direction
76% water and 58% sugarin dry pulp were reported
by Witmet (1996), whereasWhite (1989) reported
higher water (81%) and lower sugar(43% sugar in
this measure was arcsine-transformed
and magnitudeof changein retentiontime with
was63%.Watercontentof fruit pulp from thebatch changesin bulk intakeunder an assumptionof confed to Catharusspp. thrusheswas 7•%, and sugar tinuousflow througha fixedgut volume.
Becausesugar digestiveefficiencyis a proportion,
contentof the dry pulp was60%.Similarvaluesof
for statistical
analysis.Unless otherwisenoted, data were analyzed by repeated-measuresANOVA becauseindiasthe
dry pulp)contents.
Estimates
of therelativeamounts vidualbirdsweretestedonbothdiets(species
of fruit pulp and seedbulk of fruits by massand vol- between-factor and diet treatment as the within-facumewerethe same.Seedscomprised11.5%of fresh tor). When ANOVA revealedsignificantdifferences
mass(or volume)and 33% of dry massof fruits fed amongspecies,post-hocdifferences
betweenpairsof
to Cedar Waxwings, American Robins, and Wood specieswereassessed
by Fisher'sprotectedleastsigThrushes.Seedscomprised19.7%of freshmass(or nificant differencetest (Fisher'sPLSD). Becauseof
in how CedarWaxwingsand thrushvolume)and 47%of dry massof fruits fed to Catharus the differences
thrushes.
es processseeds,I also performedplannedcomparBirdswereheld individuallyin stainlesssteelcag- isonsbetweenCedarWaxwingsand the four thrushes(30 x 45 x 45 cm) with subtendingcollectionpans es to evaluatewhetherwaxwingsrespondeddifferin artificially lighted rooms maintained at 16øC. entlythanthrushesto removalof seedsfrom fruits.
Birdswere weigheddaily,2 h after nightfall.Water
was available
ad libitum at all times. Birds were fed
wholechokecherry
fruitsfortwo dayspriorto theexperimentto acclimatethem to this diet. Eachbird
was alternatelytestedwith whole and pitted fruits
of chokecherry,fed ad libitum for the 10 daylight
hoursin two consecutive
24-hfeedingtrials(16to 17
February 1991). Trial order was split evenly among
randomlychosenindividualsof eachbird species.
For each24-h trial, food intakewas quantifiedand
feces were collected, frozen, and freeze-dried for
chemicalanalyses.Becauseof the potentialfor birds
to compensate
for dilution of the diet by increasing
the durationof their daily feedingperiods,fruit intake was measured at hourly intervals to assess
short-termpatternsof consumption.I quantified
food consumptionby countingremainingfruits at
eachhourly check,returningdroppedfruits to food
dishes.To insure that birds did not selectamong
fruits offered,I replenisheddietswhen only a few
fruits remainedfrom the previousfeeding.Pulp intake was estimated from the average values for
batchesof fruits fed to birds,accountingfor lossesof
pulp whenfruitswerepitted.Sugarcontentof fruits
and feceswasmeasuredby the Anthroneprocedure
(Yemm and Willis 1951) after extractionof samples
with 80% ethanol.
RESULTS
Therewereno significanteffectsof trial day
on total intake of fresh fruit (F = 0.03, df = 1
and 11, P = 0.61), pulp intake (F = 2.55, df =
1 and 11, P = 0.14),sugardigestiveefficiency
(F = 0.01, df = 1 and 11, P = 0.95), or total sugar assimilated(F = 3.05, df = 1 and 11, P =
0.11).Therefore,trial day was eliminatedas a
factor from subsequentanalyses.Cedar Waxwingsandthrushesrespondedin parallelways
to diet treatments(speciesx diet treatmentinteractions,Ps > 0.30; planned comparisonx
diet treatment interactions,Ps > 0.50).
Relativemasschangesduringthe 24-h trials
werenot differentamongspecies(F = 2.13,df
= 4 and 11, P = 0.15), nor did Cedar Waxwings
differfromthrushes(plannedcomparison,
F=
2.86, df = 1 and 11, P = 0.12). Relative mass
changesof birdsfed wholefruits versuspitted
fruits did not differ significantly(wholefruits:
g = -2.8 -+ SD of 1.4%;pitted fruits: œ= -2.3
_+1.7%;F = 1.05, df = 1 and 11, P = 0.33).
For all species,daily mass-specificintake
ratesof wet matter (fruit pulp and seedscomWaxwings,thechangein meanturnovertimewases- bined)werehigherfor wholefruitsthanfor pitTo illustratethe potentialeffectof total intakeon
retention
time of food within
the intestines of Cedar
timated from fresh-mass(=volumetric) intake rate ted fruits (F = 22.86, df = 1 and 11, P < 0.001),
and intestinal volume (volume divided by intake but intakeratesof fruit pulp from thesetwo dirate;Van Soest1994).This methodassumesconstant
etswere not statisticallydifferent(F = 0.16,df
gut volume and continual processingof fruit food
bulk-processinglimitation (Levey and Grajal 1991).
Intestinalvolumeswere measuredon salvagedbirds
with relaxedtissues(Witmer 1994);thus, in vivoin-
= 1 and 11, P = 0.69;Fig. 1). Pulp intakerates
amongthrushspecieswere the same,whereas
the intakerateby CedarWaxwingswashigher
than that of eachthrushspecies(F = 10.89,df
testinalvolumemayhavebeenlower.Althoughthis
= 1 and 11, P < 0.001; Fisher's PLSD for each
throughthe gut, consistentwith the hypothesisof
322
A
MARKC. WITMER
[Auk,Vol. 115
1000
1'501
'7,
Cedar
Waxwing
[ ßWhole
fruit
]
,;-,
•)
800
• 400
ß
•
•.oo
I
Hermit
Thrush
200
ß
Cedar
Waxwing
Hermit
Gr.-cheeked
Thrush
Thrush
Wood
Thrush
American
Robin
O1
FIG. 1.
Daily intake rates (œ-+ SE) of wet matter
(fruit pulp and seeds)by five frugivoresfed pitted
].
versuswhole chokecherry
fruits.
Gray-cheeke
Thrush
O
comparison,Ps --<0.008).Patternsof hourly intake of pulp overthe courseof the feedingday
were indistinguishablebetweentreatmentsfor
all species(F < 0.01, df = 1 and 22, P = 0.99;
Fig. 2).
Under the assumptionsof constantgut volume and continual flow, estimated mean reten-
tiontime of Prunuspulp in theintestinesof Cedar Waxwings should have decreasedfrom
about 63 to 57 min with the inclusion of seeds
(Fig. 3). This effectwould havebeensmallerfor
thrushesbecausetheyregurgitatemostPrunus
seeds.If sugar absorptionis closelylinked to
retention time, seed bulk should have reduced
O.00
1.so]•.•
•
American
Robin
0.50
1
2
3
4
5
6
7
8
9
10
Hour
sugardigestiveefficiencyfor CedarWaxwings
to a greaterdegreethan for thrushes.However,
Fic. 2. Hourly patternsof pulp consumption(• -+
digestiveefficienciesof sugarswere similar for $E) of pitted (opencircles)and whole(filled circles)
whole fruits (96.4 ___
0.9%) and pitted fruits fruits by five fruõivores.
(96.6 + 0.8%; F = 4.37, df = 1 and 11, P = 0.061;
Fig. 4), and the responseto diet treatmentdid
not differ significantlyamongbird species.Di- and 11, P = 0.001;Fisher'sPLSD,Ps -< 0.010).
gestiveefficienciesof sugarswere not different Becausechokecherryfruit pulp containspriamong bird species(F = 0.52, df = 4 and 11, P marily sugars, with only minute amounts of
= 0.72; planned comparisonbetween Cedar lipids and protein (3.0 and 2.6%, respectively;
Waxwingandthrushes,F = 1.12,df = 1 and11, Witmer 1996),ratesof sugarassimilationcloseP = 0.31).
ly approximatedrates of energy assimilation.
Daily ratesof sugarassimilation,theproduct Energy assimilation (from sugars) among
of intake rate and digestiveefficiency,were not thrushspecieswas scaledto body massto the
significantly different for pitted and whole 0.74 power (sugar assimilated= 2.24 x body
fruits (F = 0.12, df = 1 and 11, P = 0.73;Fig. massø.74),
similar to the valuereportedamong
5). Parallelwith resultsfor dailyintakepatterns passerines(0.724, n = 35 species;Lasiewski
of fruit pulp, hourly patternsof sugarassimi- and Dawson 1967). Comparedwith the allolation were not influencedby the presenceof metricpatternamongthrushes,daily sugarasseeds(F = 0.66, df = 1 and 22, P = 0.43). Rates similationwas higher for Cedar Waxwings
of sugar assimilationwere the same among (planned comparison,F = 39.5, df = I and 14,
thrushspecies
but higherfor CedarWaxwings P < 0.001;Fig. 5).
Given the absence of detectable differences
than for eachof the thrushes(F = 9.66, df = 4
April 1998]
600-
323
100 -
70-
•'Pitted
fruit
500.
400.
DoSeeds
LimitIntakeofFruits?
[ßWhole
fruit
[]
98
• 60
-I 1•_____•Twholefrui
t
Pitted fruit
96-
50
....i_
.......
I ••.T'•
:
300,
200
e-
._•
t,,3
94-
ß--•
92
100
{33
•
90
0
Cedar
Hermit
Waxwing
Intake (g h-l)
FIG. 3.
Estimated
effect of seed bulk on the reten-
tion time of fruit pulp by Cedar Waxwings under a
Thrush
Gr.-cheeked
Thrush
Wood
Thrush
American
Robin
FIG.4. Digestiveefficienciesof sugars(• -+SE)by
five frugivoresfed pitted versuswholechokecherry
fruit
diets.
modelof continuousflow throughan inflexiblesystem. Values for inset are œ +_ SE. See Methods for de-
tails and assumptions.
among species in digestive responsesto di-
etaryseedbulk,theoverallprobabilityof falsely acceptingthe null hypothesis
if total intake
was reducedin proportionto dilution of the
diet with wet bulk (TypeII error)was16%(n
= 16);the Type II error underthe expectation
of intakereductionsproportionalto dry matter
of thechokecherry
dietwaswellbelow1%(Miller et al. 1990).Thisexperiment
wasstatistically
powerfulenoughto detectan effectof seedson
fruit-pulp intake of 6.6%,adequatefor effects
on intakeproportionalto wet or dry pulp mass.
Thiswasdemonstrated
by thesignificant
effect
pulp into the intestineis not affectedby seed
bulk (see Levey and Grajal 1991). Equivalent
ratesof sugarabsorptionby frugivorousbirds
eatingseedlesspulp versuswhole fruits sug-
gestthat intakeand assimilation
of fruit-pulp
sugarswere cuedto, or limited by, the rate of
sugarabsorption
or energyassimilation,
rather
thanby thephysicalcomposition
of thesediets.
CedarWaxwingsand thrushesalsoshowcompensatorydigestiveresponsesto dilution of artificial sugarydiets,increasingintake rate and
passagespeedas sugar concentrationdeclines
to regulate daily rates of sugar uptake to constant levels(Witmer unpubl. data).
Birds eating whole and pitted chokecherry
of seed bulk on total intake.
DISCUSSION
•'•3
5-
Cedar
WaxwingRobin
Digestiveresponses
to seedbulk.--Frugivorous
birds compensatedfor dietary seed bulk by
Thrush
..-''
passing (Cedar Waxwings) or regurgitating E
Thrush
(thrushes)seedsefficientlyenoughthat the
ratesof processing
and assimilatingfruit-pulp
sugarswere not depressed(Figs. 1, 2, 5). Com) 2ß Whole
fruit
Gray-cheeked
0 Pitted
fruit
pensationeven at 1-h intervalssuggeststhat 0"•
Thrush
chokecherry
seedsdid not constraininstanta20
•'0
4b.... do.... do.... 7'0....
neousratesof intake or sugarabsorption.UniBody maas (g)
directionalprocessing
of seedsthroughthe digestivetractby CedarWaxwingsmay be an efFIG. 5. Daily ratesof sugar assimilation(œ+- SE)
ficientmodeof processing
bulky dietsof readi- by fivefrugivoresfedpittedversuswholefruits.Sugly assimilatedsimple sugars in an aqueous ar assimilationwas not affectedby the presenceof
medium.Regurgitation
by thrushesmayelim- seedsin fruits.Dashedline showsallometricpattern
inate seedsfrom the stomachso that entry of of sugarassimilationamongthe four thrushspecies.
• 4-
Wood
324
MARKC. WITMER
[Auk, Vol. 115
mode acfruits performedequallywell on thesediets, not suggestthat seed-processing
showingthe samedegreeof massloss(<3%). countsfor the intake differencesof sugary
Thus,seedprocessing
doesnot appearto have foodsbetweenCedarWaxwingsand thrushes
exactedsignificantenergeticcoststo birds,but (Figs.1 and 5). Similarly,Cedar Waxwingsingest and assimilatesugary,low-proteinartifithis remainsto be quantified.
Implications
for frugivoredigestive
functionand cial dietsat higherratesthan thrushes(ca. 1.5
nutrientassimilation
fromfruits.--Thehigh diges- times; Witmer unpubl. data). These rates of
tive effidencies
of sugarsby thefivefrugivoresI sugar assimilationapproximatemaintenancestudiedare comparable
to thoseshownby fru- energyintakeby thesespeciesunderthe same
givorousmanakins(Worthington
1989)andnec- conditionsof captivity,suggestingthat frugitarivoroushummingbirds(Hainsworth1974, voresare not energy-limitedwhen eatingsugKarasovet al. 1986),contradicting
thecontention ary fruits (Witmer 1994).Cedar Waxwingsapthat frugivoresassimilatefruit nutrientsineffi- pear to havehigherratesof energymetabolism
ciently(e.g.Karasovand Levey1990,Leveyand when eatingsugary,low-proteindietsthan do
Duke 1992).Thelackof an effectof indigestible more omnivorousfrugivores.The relatively
bulk intakeon digestiveefficienc3•
regardless
of wide intestinalmorphologyof waxwingsis imseed-processing
mode,challenges
currentideas plicatedas a trait that enablesthis speciesto
of how frugivoresprocessfruits. Becausethe achievehighintakeratesof bulky,sugaryfruits
simplesugars(glucoseand fructose)in aqueous (Witmer 1994).For lipid-richfruits, which are
solutionsof fruit pulp do not requiredigestion not normallyeatenby waxwingsandwhichreand are readily absorbedby activeand passive quire longerretentiontimesfor digestionand
mechanisms(Pappenheimer
and Reiss 1987), absorption (Mateos and Sell 1981, Afik and
birds rarely may face tradeoffsbetweenintake Karasov 1996, Witmer and Van Soest 1998),
and nutrientabsorptionfrom sugaryfruit diets seedbulk may have a muchstrongernegative
undernaturallevelsof dietarydilutionwith in- effect on ingestion and/or absorptionrates
digestiblebulk (Witmer and Van Soest1998). than it doesfor sugaryfruits.
Seedloadsoffruits andtheevolution
ofplant/fruRapid digestiveprocessing
of sugaryfruitsis exin seed loads
pectedbecauseglucoseand fructoseare easily givoremutualisms.--Differences
absorbednutrients.Indeed,previouscontentions may accountfor the contrastingresults bethat frugivoreshaveintrinsicallyrapid passage tweenmy studyandthoseof LeveyandGrajal
ratesmay haveresultedfrom effectsof experi- (1991) and Murray et al. (1993). Seeds commentaldiettype,ratherthananimaldietaryhab- prisedabout28% (by volume)of artificialdiets
its; passagerates for Cedar Waxwings and in the previousstudiesversus12 to 20% of the
thrusheseatingthe samedietsare not different natural diet in my study.In fact,the seedloads
(Witmer1994).Thus,fastpassageof fruit diets usedin the other two studiesthat reportedefdoesnot appearto be a trait of frugivoresthat fects of seed bulk on fruit intake appear to be
resultsin impairednutrientutilization,but a re- higher than thosetypically found in sugary,
suitof howrapidlyfruit sugarscanbethorough- bird-dispersedfruits (Fig. 6). The abilityof the
ly absorbed(comparedwith lipid- and/or pro- digestivesystemsof avian frugivoresto comtein-richfoods).Rapidpassage
of seedsrelative pensatefor seedbulk may explainthe results
to pulp throughthe intestinesof CedarWax- of studies in which birds did not discriminate
wings(LeveyandDuke 1992)probablyfunctions on the basis of seed load (McPherson1987,
to minimizethe time thatindigestible
seedsare Willson and Comet 1993, Willson 1994). Alretainedwithintheabsorptive
portionof thegut, thoughfruit removalby birds hasbeencorrewhile permittingretentionof pulp until absorp- lated with the seed-to-pulpratio of natural
tion of nutrientsis complete.
The abilityof fru- fruits (Howe and Vande Kerckhove1980, 1981,
givorousbirdsto compensate
for seedsalsosug- Sallabanks1993),my resultssuggestthat the
geststhattheirgutsdistendto accomodate
indi- causes of such correlations remain obscure.
My resultssuggestthat seedsof bird-disgestiblebulk, aswell as the possibilitythatfrugivoregutsprocess
fruit foodsdiscretely,
rather persed fruits often do not impose bulk-prothancontinuously.
cessinglimitationson frugivores.The waysin
Do seeds
affectinterspecific
patternsoffruit con- which seedsinfluencefruit-intake ratespotensumptionandsugarassimilation?--My
resultsdo tially depend on the physical and chemical
April 1998]
DoSeeds
LimitIntakeofFruits?
325
ACKNOWLEDGMENTS
Birds were held under state and federal (PRTseed loadsof chokecherry
fruilsused in lhis sfudy
seed loads of artificial
studies
fruitsused in previous
721267)permitsto MCW,in compliance
with all state
andfederalregulations
regardingresearch
with captive wild birds,overseen
by the InstitutionalAnimal
Care and UseCommitteeat CornellUniversity.Peter
Van Soestgenerouslyprovidedlaboratoryfacilities
and suppliesfor chemicalanalyses.
! am gratefulto
Nina Ingle for collaborationin a preliminarystudy
0
10
20
30
40
Seed load (%)
thathelpedin thedesignof thisresearch.
Themanuscript benefitted from the commentsof Carlos
Bosque,
Nina Ingle,DougLevey,CarlosMartinezdel
Rio, RexSallabanks,and WesleyWeathers.
FIG.6. Distributionof seedloads(g seedsper g
wholefruit, freshmass)for sugaryfruitsof 38 plant
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