CHAPTER 2

A seven-year study of individual variation in fruit production in tropicalbird-dispersed tree species in the family Lauraceae

NATHANIEL T. WHEELWRIGHT*Section o/Ecology and Systematics, Cornell University, Ithaca, New York 14853, USA

Key words: Lauraceae. seed dispersal. frugivory. tropics. roasting. phenology. plant reproduction. annual variation in fruit production

Introduction

Lifetime patterns of fruit production, like otherfeatures of a plant's reproductive biology, havebeen molded by natural selection by seed disper-sers over thousands of generations. At least, that iswhat most researchers interested in frugivory andseed dispersal assume. It is daunting to recognize,however, that we make such an assumption in theabsence of crucial information on the heritability ofreproductive traits, or on the strength of selectionimposed by different kinds of interactions withseed dispersers. We know very little about thescheduling of reproduction or the magnitude ofannual and individual variation in fruit productionin most tropical tree species (Janzen, 1978). Sel-dom do we know if we are witnessing a 'normal'year, or even what a 'normal' year is in terms of

plant reproduction.The earliest systematic studies on flowering and

fruiting in tropical plants were conducted only re-cently (McClure, 1966; Medway, 1972; Frankie etal., 1974; Hilty, 1980; Opler et al., 1980). The workwas directed chiefly at determining broad within-year patterns such as .the number of species flower-ing or fruiting within a given month or forest stra-tum. From these descriptive studies, the focus ofresearch shifted to the question of how competitionfor pollinators or seed dispersers might select forstaggered phenologies within years (Frankie, 1975;Stiles, 1977; for a review see Wheelwright, 1985a)or how the timing of fruit production related to the

Abstract. Fruit crop sizes varied from year to yearamong 22 sympatric, bird-dispersed tree species inthe Lauraceae. Each species in the lower montaneforests of Monteverde, Costa Rica fruited at acharacteristic season, but there was wide year-to-year variability in the porportion of each popu-lation that produced fruit and in the average size offruit crops. Over a 7-year period (1979-1985), over-all fruit production was high during three noncon-secutive years and low during four years. Withingenera, tree species displayed distinct fruitingschedules. Even within populations, individualtrees ~ometimes fruited in different years or failedto fruit altogether.

Yearly rainfall and temperature patterns did notexplain annual variation in fruit production. Unex-pectedly, neither did previous reproductive histo-ries: there was little correlation between an indi-vidual tree's fruit production in a given year and itsfruit production the previous year. On the otherhand, vegetative growth was negatively correlatedwith reproduction in 12 of 15 species.

Lauraceous fruits make up 60-80% of all fruitseaten by bird specie$ such as Three-wattled Bell-birds and Resplendent Quetzals. These birds mayrespond to annual variation in the availability oflauraceous fruits by migrating locally, by expand-ing their diets to include previously ignored foodsor unripe fruits, or by delaying breeding.

.Present address: Department of Biology. Bowdoiff CollegeBrunswick. Maine 04011. USA

Estrada. A. and Fleming, T.H. (eds.), Frugivores and seed dispersal.cg/986, Dr W. Junk Publishers. Dordrecht. ISBN 90-6193-543-1.

20

to the cloud forest on the divide itself. 4 km to theeast. The habitat consists of undisturbed forests(including the 2700 ha Monteverde Cloud ForestReserve. which borders the 33.000ha Arenal For-est Preserve), small cattle pastures. and woodlots.For a more complete description of the area. seeLawton and Dryer (1980) and Wheelwright et a/.

(1984).A mean of 2529 (SD = 394) mm of rain falls

annually in Monteverde (n = 28yrs). About 85~/oof the yearly precipitation comes during a distinctwetseason. which typically begins in mid-May andlastS until late-December. The dry season averages144 (SD = 21) days (n = 19 yrs). During the periodof this study, rainfall averaged 2703 (SD = 469)

mm. The period included one of the rainiest years(1981: 3234mm) and one of the driest years (1983:1971mm) in which meteorological records havebeen kept. Daily minimum temperatures from 1979to 1983 averaged 14.9°C (SD = 0.30 C); daily max-imumtemperatures averaged 21.90 C (SD = 0.60 C).

Unlike rainfall, temperatures remain relativelyconstant throughout the year. Mean annual rela-tive humidity in MQQteverde is estimated to rangebetween 85% and 90% (R. Lawton. pers. comm.).The lengths of the longest and shortest days of theyear differ by only 69 min.

behavior of seed dispersers (Thompson and Will-son. 1979). Other studies searched for the proxi-mate cues responsible for observed phenologies.especially in relatively aseasonal tropical forests(Alvim and Alvim. 1978; Putz. 1979). What hasrarely been reported are long-term studies ofmarked individual plants. Janzen (1978) andMilton et al. (1982) presented unusually completephenological data on individuals of four tropicaltree species. and research currently in progress (G.Frankie. pers. comm.) promises to detail reproduc-tion over more than a ]O-year period for many more

plant species.This paper describes individual variation in fruit

production by 22 plant species studied over a six-year period; among these species are six studied ina seventh year. I have focused on 16 of tht: com-monest species. The plants. all sympatric bird-dis-persed trees in the Lauraceae. are conspicuousmembers of the lower montane forests of CostaRica. They provide fruit for at least 18 bird species,several of which depend on the Lauraceae for food(Wheelwright et al.. ]984). The purpose of thepaper is (1) to document year-to-year variability infruit produL"tion by a group of related plant speciesin a tropical forest. (2) to demonstrate between-year differences in reproductive output among in-dividual trees of the same species. and (3) to con-sider some of the life history trade-offs and en-vironmental cues that may produce community-level reproductive patterns.

Tree species

At least 22 bird-dispersed lauraceous tree speciesoccur in the same or adjoining habitats at Mon-teverde. Their taxonomy is still being resolved (W.Burger. pers. comm.). For consistency. if not no-menclatural accuracy. this paper retains the namesused in previous publications. Except for two un-derstory species. the species are shade-tolerantcanopy trees which together constitute much of thebiomass of the forest. The basic reproductive pat-tern for most lauraceous species at Monteverde isto fruit once a year. four to 12 months after flower-ing (Fig. la-y). As this paper demonstrates. thatbasic pattern is commonly violated. During flower-ing. lauraceous species display thousands or mil-lions of small (2-4 mm diameter) light-coloredflowers in panicles. The flowers are visited (andpresumably pollinated) mainly by flies. bees. and

Methods

Stlldyarea

The study area covers 15 km:! of lower montane wetand rain forests (Holdridge. 1967) in Monteverde.Costa Rica (10018' N. 84048' W). Monteverde lieson a plateau along the continental divide at anelevation of 1350 to 1550 m. The soils. volcanic inorigin. are quite fertile. They support a diverseforest. comprising approximately 800 woody plantspecies. many of which are bird-dispersed (Wheel-wright et al.. 1984). In 1980 I established a transectfrom the relatively dry western edge of the plateau

21I

i ",;" ,~>, "'" ".~~O~~., , ;

J A SON D.J F M A M J J A

MONTH

wasps. In any month of the year. at least one lau-raceous species can be found with ripe fruit atMonteverde (""heelwright. 1985a). Two speciesare dioecious. including one (Ocotea bernouiiana(= O. lenera: B. Hammel. pers. comm.) in whichsome individuals switch from the production offemale flowers to the production of male flowerswith age (N.T. Wheelwright. unpublished data).Lauraceous fruits are distinctive because of their

large size. high protein and lipid content. and largesingle seed (Snow, 1973: Wheelwright et af., 198~).Because they produce 'high investment' fruits. theLauraceae allegedly exemplifies one extreme fruit-ing strategy in McKey's (1975) model. in which fruitquality is predicted to be positively correlated with

dispersal quality by specialized seed dispersers.The Lauraceae has accordingly played a ke~! role inthe development of the theory of coevolution be-

22

~C

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~

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Z

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Ocoteo bernoulianG

N'15-16NI""

Perseo sp PF

N'~4Ocoteo spOQN*4-7

p u

Neclandra hypaglauca

N"27-29Q

~

S.i/schmledio costorlc.ns;sN=IO-II

v

,.

J AS ON OJ FMAMJ J A

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J AS ON OJ FMAMJ J A

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Fig. la-v. Seasonal flowering and fruiting phenologics of 22 bird-dispcrscd trcc species in the Lauruccac of Montcvcrdc. Costa Rica in1980-1981. Solid lines = percent of population with opcn flowers. Bars = pcrccnt of p<)pulation with ripc fruits. Shading of barscorresponds to mean level of fruit production (doublc-hatchcd = hcavy: single-hatched = modcratc: opcn = light).

nias tricarunculata), Emerald Toucanets (Aulaco-rhynchus prasinus), and Mountain Robins (Turdusplebejus), swallow lauraceous fruits entire, reg-urgitating the seeds 15-60 min later. Only one tofive fruits (depending upon fruit and bird size) areconsumed per feeding bout.

tween fruiting plants and their seed dispersers(McKey, 1975; Howe and Estabrook, 1977; Wheel-wright and Orians, 1982).

Annual crop sizes range from a single fruit inunderstory species to as many as 100,000 in fecundindividuals of small-fruited species. The modalcrop size among the group as a whole is about20,000 fruits. The trees' major seed dispersers,birds such as Resplendent Quetzals (Pharoma-chrus mocinno), Three-wattled Bellbirds (Proc-

Quantifying reproduction in the Lauraceae

Since June 1980 I have monitored reproduction in

2~

286 marked trees, representing 22 species. Individ-ual trees of six of these species were observedduring 1979 as well. For the 16 commonest species,I was able to observe five or more individuals (theminimum sample size recommended by Fournierand Charpentier, 1975) over at least a six-yearperiod (median = 10 trees/species; total = 265

trees); all but three of those species generally haddeveloping fruits during each census period (seebelow). The reproduction of the other six lau-raceous species, which are rarer or more local indistribution, is discussed only briefly here. A de-tailed analysis of seasonality in flowering and fruit-ing within the 'guild' of lauraceous species is pre-sented in Wheelwright (1985a), where the methodsof recording reproductive states are described indetail.

The periods of this study included June throughAugust 1979; June 1980 through July 1981 (Fig.la-v); and 10-14 days in each of the followingmonths: March 1982, February 1983, August 1983,February 1984, and March 1985. At biweekly inter-vals during these periods (except 1979) I censusedall 286 trees along the transect. Censuses were alsoconducted monthly from August 1981 through July1982 for a subsample of three trees per species.

During each census I examined every tree withbinoculars or a spotting scope from a distance offive to 30 m (depending upon the height of the tree)and noted the production of new leaves, flowers, orfruits. I also recorded the developmental stage offruits during each census. The intensity of vegeta-tive growth, flowering, or fruiting for each individ-ual was scored as 0,1,2 or 3, depending on whether0%,1-25%,26-75%, or >75% of the canopy areashowed activity. This method estimates total fruitavailability in the forest in only a general way be-cause trees differ in size. However, the method hadseveral advantages over methods such as countingfruits on each tree (although the results of bothmethods are correlated). By being less time-con-suming, it allowed me to monitor a larger propor-tion of the population. Additionally, it yields anestimate of reproductive effort unbiased by the sizeof trees: the method distinguished modestly fruit-ing, massive individuals from massively fruiting,modest-sized individuals, even when the two havesimilar fruit crop sizes.

My estimates of mature fruit crop sizes are basedmainly on crop sizes of developing fruits noted atthe same time each year. Observations of re-productive status in February or March give areasonable estimate of fruit crop size at ripening formost species, irrespective of the stage of fruit de-velopment at the time of the census. Lauraceousspecies at Monteverde require an average of 8.6months to develop ripe fruits following flowering(cf. Fig. 1a:-v). Fruit crop sizes can be easily mea-sured even when developing fruits are minuscule.Most species ripen their fruits within a few monthsof my annual censuses (Fig. la-v; Wheelwright.1985a; cf. Foster, 1982a). Moreover, the majorityof species bear fruits in brightly colored expandedpedicels which remain on the plant for up to severalweeks after fruits have been removed, so fruit cropsizes can be estimated even for species that have

already begun fruiting.Fruit abortion (which usually takes place within

several weeks of flowering) and pre-dispersal seedpredation reduce absolute fruit numbers in manylauraceous species (N. T. Wheelwright, unpub-lished data). However, given the general scoringsystem used in this study, my dry season censusesaccurately indicated both the proportion of thepopulation that ultimately fruited as well the size ofthe ultimate fruit crop size. This was confirmed bycomparing mid-February census estimates of fruitcrop size with estimates when fruits of each specieshad matured in 1981, the year for which I havecomplete annual records for the entire sample oftrees. Fruit crop sizes in February were stronglycorrelated with fruit crop sizes at ripening (meanr = 0.79 :t 0.22, range = 0.42-1.00, P<0.5, N = 13

species). Space constraints prevent the presenta-tion of complete records for individual trees. Cop-ies of the original data may be obtained by writingthe author.

Results

Variation in fruit production: differences betweenyears and species

Fruit production fluctuated annually (Fig. 2, Fig

i

1980

--1981

-

-year during which over 50% of the population ofmost species bore fruit. Both 1982 and 1983 wereyears of low fruit production. In 1984, as in 1979and 19R1. most trees of most species produced fruit.In 1985 fruit levels were exceedingly low: in 14 ofthe 16 commonest tree species. less than 4()% of thepopulation set fruit (Fig. 2). Thus. considering theLauraceae as a whole. there were three 'boom'years and four 'bust' years over the course of thisstudy. 'Boom' years were always separated by atleast one 'bust' year.

o.ifferent tree species skipped reproduction indifferent years (Fig. 3a-m) -a 'boom' year for onespecies was not necessarily a 'boom' year for an-other. Even congeners varied in annual fruit pro-duction, 1980 was a prolific year for three lau-raceous species favored by birds (B. cosraricensis.N, hypoglacua, and 0, wachenheimii); the sameyear was barren for three congeners that are alsocritical for birds {B. mexi~ana, N. salicina, and O.tonduzii) (Fig. 3a-m) , 1985 was an unproductiveyear for most species. including B. cosraricensis.but one of the most productive years for B. me.\"-icana. Thus. if ther~:were specific environmentalcues responsible for between-year variation in fruitproduction in the Lauraceae. related tree speciesresponded differently to them,

1982

--1983

1984

1985Bei/schmied;o costoricens/s

A

Fi,l;'. 2. Frequency distril1ution or the percent or the population

of each of 16 lauraceous species producing fruits in different

years. n#

19841985

1982

,

.-,

:.;c

I 1983

YEAR

1

~zi=5a:u.

25

Beilschmiedia sp. BC

z 100af=~~Z-l-

~~50oa:nU-

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* ~II n-11 11-

1980~_- .1982

YEAR

Nectandra saticinal-S,a:u.

IX

z 1000i=

E

~ ~0 - LJ UI i ,. I I

-19841983 19851981

YEAR YEAR

Annual variation in fruit production among individ-uals

individuals failed to fruit during the entire studyperiod, Fruit production within a given year wasrarely uniform within a population; seldom dideither 0% or 100% of a population produce fruit.More typically, an intermediate proportion (4{)-80%) of each population produced fruit in a givenye~r (Fig. 3a-m). Even in 'boom' years, a portion

Individual trees within species fruited in differentyears (Fig. 3a-m, lower graphs). Trees that didfruit also varied with respect to how much fruit theyproduced each year (Fig. 3a, upper graphs). Some

3

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1980 19821981

19841983 1985

YEARYEAR

1980 1982 19841983 19851981

YEARYEAR

individual trees of one species, B. costaricensis.The species bears moderate crops of bulky fruitstypically produced at about two-year intervals. Yetsome trees missed fruiting periods, bearing fruitsonly twice during six years. Other trees fruited (atlow levels) during six of the seven years. Even treeswith relatively regular reproductive cycles fruitedasynchronously. Trees 51,55,61,67,69,70, and 71all occur within several hundred meters of each

of the population of most species failed to fruit.Because the seasonal timing oftlowering and fruit-ing in reproductively active individuals was quitesynchronous (Fig. la-v), and all individuals in thestudy were mature trees, between-year asynchronyin fruit production did not result from individuallystaggered seasonal phenologies or the inclusion ofreproductively immature trees in the sample.

Table 1 illustrates year-to-year variation among

LUN00a..0a:()

3

2

1

00

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Fig. 3a-m. Above: Annual variation in mean value of index of fruit production (:t 1 SO) from 1980 through 1985 for reproductivelyactive individuals of 13 lauraceous tree species. The index corresponds to no (0). low (1), moderate (2). and high (3) fruit production(see Methods). Below: percent of the population producing fruit in different years. Sample sizes presented in Table 2.

in 1985, a year in which less than a third of the N.salicina population fruited. On the other hand,annually fruiting species such as N. davidsonianaand o. bernouliana ( = o. tenera) seemed remarka-bly synchronous and constant in their annual fruitproduction (c/. Table 3).

other, yet they showed distinct cycles (Table 1).Examples of such variability within populationscould be drawn from other species. One large,vigorous individual N. salicina, for instance, failedto fruit from 1980 to 1984; it produced a large crop

..:. j

Previous reproductive efforts and variation in frllitproduction between years

Year-to-year differences in climate and fruit production

In some species. an individual tree that producedmany fruits one year was likely to produce fewfruits the next year (Table 2). I examined the rela-tionship between fruiting efforts in consecutiveyears. and found negative correlations in nine of 15species. suggesting the possibility of trade-offs inreproductive allocation between years. However.fruiting efforts in successive years were positivelycorrelated in the other six species. Sample sizeswere too small or seasonal phenologies inappropri-ate for examining the remaining species. In mostcases absolute correlation coefficients were ratherlow (r<O.30) and insignificant (P>O.10); there wasonly a slight trend toward reduced fruiting follow-ing a year of heavy fruiting. If I considered onlytrees that fruited at least twice during the study. thecorrelation between successive reproductive ef-forts was negative in 11 of the 15 species. with largerabsolute correlation coefficients. The trend mayhave been greater had there not been an inexplica-bly positive correlation b~tween flowering levels insuccessive years in nine of 15 species. The relation-

There was no straightforward relationship betweenfruit production and rainfall during the precedingyear as might have been expected (Alvim and AI-vim. 1978: Opler et al.. 1976). For example, 19ROwas unusually wet (3051 mm of rainfall) and wasfollowed by a year of high fruit production; 1983was unusually dry but was also followed by a yearof high fruit production. Likewise. 1982 and 19R3.both years in which fruit production was quite low.were preceded by years of high (3234mm) andaverage (25Rl mm)rainfall, respectively. Mean an-nual rainfall for the years preceding the three'boom. years was 2483 mm. only slightly below the28-yr mean. In terms of the monthly distribution ofrainfall. the three 'boom' years shared little in com-mon except abnormally dry Aprils. Temperatureextremes and average annual temperatures. whichmay have affected floral initiation (Buttrose andAlexander. 1978). differed little over the course ofthe study and indicated no correlation with sub-sequent fruit production...

Tahle I. Reproductive records for Beil,\'('hmiedia cos/arice/lsis illustrating individual variability in fruit crop size and reproductivepcriodi<;ity in onc spccies in the Lauraceac. Other species show similar variability. although with lessofa tendency towards biennial fruitproduction. Although the proportion of thc population that fruited each year varied relatively little and the mean size of fruit crops wassimilar (Fig. 3al. individual trees fruited out of synchrony with each other and differed in the number of fruits produced in differentycars. 3 = heavy fruit production. .; = moderate fruit production. I = light fruit production. 0 = no fruits produced. -= not obscr\.ed

(see Methods).

-~

Year

:.:

No

19M2 19113 198* 1985197tJ 19"';0

0

33

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ship between fruit production in a given year andfruit production two years later was even less clear(r<O in seven species, r>O in eight species). Fruitproduction and the production of new leaves in thesame year were negatively correlated in 12 of the 15species, with greater absolute correlation coeffi-cients (Table 2).

Reproductive patterns ~'ithin the Lauraceae

group is that they produced little or no fruit duringmost years of the study but produced substantialcrops during one Qr two y~ars. Individuals andpopulations alike were inconsistent in reproduc-tion. The group includes all three species in thegenus Phoebe. plus species in three other genera.Of 38 individual Phoebe trees. only four fruitedmore than. twice during the study period. and nonefruited more than three times.. despite requiringrelatively little time (four to six months) to developtheir fruits (Fig. .1 m. p). (Even though Phoebemexicana flowers and fruits between censuses. thelack of flower primordia. empty cupules. and vege-tative growth indicated no reproduction.) On aver-age. individual trees within species in this groupfruited during 18% (SO = 9%. range = 11-29%) of

the years of the study. Many trees fruited only onceor not at all during six years of observation. Whenfruit production was high. however. birds fed read-ily on fruits of these species.

The periodic prolific fruiters seemed to showmore regular. although supra-annual. fruiting cy-cles than the erratic. mnderate-level fruiters: when

There appear to be three general reproductive pat-terns within the Lauraceae: erratic moderate-levelfruit production, periodic prolific fruit production,and consistent low-level fruit production. Mostspecies can be assigned to one, depending upontheir average fruit crop sizes and the regularity withwhich they produce fruit (Table 3), although thereis some overlap between the groupings. The group-ings cut across generic classifications. fruit traits.seasonal phenologies, and habitats (cf. Monasterioand Sarmiento. 1976).

The erratic moderate-level fruiters have fruitcrops of variable sizes. What unites species in this

Table 1. Correlation (r) between fruit production in present vs. previous years. and between fruit production !".I". vegetative growth in thesame year from 19XO through 1985. There was a relatively weak trend towards reduced fruit production following a year of he.lvy fruit

production. Vegetative growth and reproduction were more negatively correlated in most species.

No. successiveplant-years

Tree species Correlation

coefficient:current vs.

previous fruiting

No. successivcplant-years

No. individualtrees

Correlationcoefficient:fruiting vs.

vegetative growth

B. me.ricanaB. costaricensisN. gentleiN. h.l"po,~laucaN. .ialicinaO. austiniiO. bernoulianaO. sr. FlO. .ip. K2o. sr. RPO. tonduziiO. lI'achenheimiiPersea \'eraguensisPh. mexicanaPh. neuroph.\'lla

-.33

-.56

-.()9

-.2/!'

.14

-.67

-.15

.09

-.()6

.11

-.09

-.31'

-.12

-.07

-.16

-.22

-.44* *

-.07

.(XI

.05

-.~3.58* *

-.28

-.07

.13-.~2* *

-.18

.~l

.23*

-.03

2142

24

102

104

21567

2039

11034

128539

175531

1351351773141752

14249

1511356

6

127

3029

6

16

56

12

30113

~51~

.p<.O\

P<.O5

30-= )

The consistent low-level fruiters annually pro-duced small crops of fruits that were removedslowly. These species are the between-year analo-gues of within-year 'tricklers' (Smythe, 1970).Trees of different species fruited during an averageof 84% of years (SO = 6%), with a CVoffruit cropsize index of only 0.29-0.47 (x = 0.37, SO = 0.09).

N. davidsoniana, with moderate to large fruitcrops, is distinct, but like the other species in thisgroup, its fruits are not highly favored by birds. Byand large, the group is of minimal importance tofruit-eating birds. There was no correlation be-tween fruit size and reproductive pattern (Table 3),but consistent fruiters tended to be species ofsmaller stature (cf. Silvertown, 1980).

they did fruit, they did so abundantly. Their repro-duction is reminiscent of temperate zone mastseeders (Rehfeldt et ai., 1971; Silvertown, 1980).The reproductive behavior of these trees stronglyinfluenced the movements and behavior of fruit-eating birds and set the rhythm of the forest fromthe standpoint of birds that depend on lauraceousfruits. Yet these tree species have low constancyand only moderate consistency (sensu Colwell,1974; Putz, 1979) of fruit production. On average,individual trees in this group fruited during43-72% of the years of the study, depending uponspecies (x = 55%, SD = 9%). The coefficient of

variation (CY) of fruit crop size index ranged from0.48-1.16 (x = 0.64, SD = 0.25).

Table 3. Three general patterns of fruit production within the Lauraceae at Monteverde. Mean crop size and variability in crop size referto annual levels in the population as a whole. Consistency of population refers to the regularity with which populations fruited during thestudy period; consistency of individuals reflects the mean frequency during the study period that individuals of each species producedfruit. Note that phenological patterns cut across genera. Species designated with asterisks were classified on the basis of observationsduring only two years (*) or censuses of fewer than five individuals (* *).

Variability in crop Consistency ofsize population

Tree species Mean fruit cropsize

Consistency ofindividuals

Fruit size (g)

Erratic moderate level fruitersPhoebe mexicanaPh. neuroph.vllaNectandra gentlei.Persea sp. RPOcotea $p. FL.* N. sp. NC

moderatemoderatehighmoderatemoderate?

lowlowmoderatelowlowlow

lowlowlowmoderatemoderatelow

1.41.61.00.39.31.0

moderate

highmoderatelowlowlow

Periodic prolific fruitersN. salicin aO. wachenheimiiO. tonduziiO. austiniiBeilschmiedia mexicanaB. costaricensisN. hypoglauca..B. sp. BIP. veraguensis..P. sp. PF

moderatelow

high

highmoderatehigh

high?high?

7.42.9

moderate

moderatemoderate

highhighhighhighlow

low

1.312.912.45.515.20.75.0

lowmoderatelowmoderatelowmoderate

moderat~?lowlow

moderatehighhighhighmoderate

highhighmoderate

highhigh

3.1

Importance of lauraceous fruits for birds

The 'failure' of lauraceous fruit crops in certainyears must affect the birds that rely on these fruitsfor food, just as fruit failure on Barro ColoradoIsland led to diet shifts and emigrations in fruiteating animals (Foster, 1982b). The diet of maleThree-wattled Bellbirds consists chiefly of lau-raceous fruits during the birds' breeding season

(Snow, 1977; Table 4). I collected seeds from 'seedtraps' (see Snow, 1970; Wheelwright, 1985b) sus-pended beneath the display perches of five malebell birds from different parts of the study area.Lauraceous fruits made up the majority of fruitseaten by each bell bird (60-78%; Table 4). In termsof fruit mass or caloric content, lauraceous fruitscomprised a substantially higher proportion of bell-birds' diets because of the large size and high lipidconcentration of lauraceous fruits (Snow, 1971;Wheelwright et a/., 1984). tauraceous fruits wereclearly critical elements of bellbirds' diets, but thebirds did not appear tied to anyone species.Rather, lauraceous species appeared interchangea-ble in space and time: Bellbirds whose percheswere located in different habitats consumed dif-ferent fruit species (Table 4). During the course ofthe five-month breeding season, birds shifted in

their use of different lauraceous fruit species assome species became scarce and others abundant.

Resplendent Quetzals depended on lauraceousfruits too, both for nestlings (81% of individualfruits delivered to the nest) and adults (80% offruits whose seeds were recovered in seed trapsbeneath quetzal nest-guarding perches) (Wheel-

wright, 1983). Many other bird species, especiallytoucans and thrushes, commonly ate lauraceousfruits (Wheelwright et al., 1984). A preference forcertain fruits is not necessarily indicative of a de-pendence on them, of course. But in the case of

quetzals,toucanets, andbellbirds, at least, there isevidence that the birds are strongly affected bylauraceous fruit abundance. During years of lowfruit production, quetzals fed on unripe or low-growing fruits of other families (e.g., Rubus rosae-folia (Rosaceae» or left the area entirely (Wheel-wright, 1983). Toucanets began following army antswarms or consumed fruits that they normally ig-nored (e.g., Piper spp.). Breeding by quetzals,bellbirds, and toucanets was apparently delayedduring fruit shortages in 1983 and 1985 (pers. obs.).Quetzals' seasonal migrations between forest typesappear linked to the phenologies of different lau-raceous species (Wheelwright, 1983), and the mor-phology and geographical distribution of the genus

B. coslaricellSisN. sP... NCN. gelllleiN. h.\'poglaucaN. salicinaN. sp. NYo. auslilliio. sp. RPO. londuzii

3.90.500

1.11.1

2.20

91.2

2300003

090

0000

72.6000

27.4

02.000002.00.4

95.6

000

30.020.0000

50.0

.0

.3.2

.8

,7

"'.,.)..

Procnias seems related to their dependence on lau-raceous fruits (Snow. 1973; see also Crome. 1975).Irregular irruptions of Emerald Touca~ets to thelowlands of Costa Rica (G. Stiles. pers. comm.)conceivably OCcur during years in which lauraceoustrees fail to produce fruit in highland forests.

Discussion

-= )

within the population. But many individuals by-passed reproduction in a given year or fruited irreg-ularly. Occasionally individual trees fruited heavilyat a time when their conspecifics had small fruitcrops. Species within a genus seemed no moresynchronous in between-year fruiting than speciesin separate genera. The family as a whole showedlittle consistent synchrony. even though there wereyears of gent:ral fruit scarcity or abundance.

Foster (1982b). among others. has hypothesizedthat supra-annual reproductive rhythms in tropicalforests may be caused by cycles of depletion andreplenishment of energy and nutrient reserves.entrained or reset by irregular climatic events (cf.Eis eta i.. 1965), Alternatively. annual variation inreproduction could be favored by the advantage ofescaping seed predators in time or discouraging thebuildup of large predator populations (Janzen.1976; Silvertown. 1980). designed to minimize com-petition for space during vegetative growth (Jan-zen. 1967). or caused by annually varying pollinatorlimitation (Baker et ai.. 1983). competition for dis-persers (Snow. 1965; Stiles. 1977).. or climatic fluc-tuations (Alvim antj ;Alvim. 1978).

None of these hypotheses completely explainsannual variation in fruit production within the Lau-raceae of Monteverde. The 'allocation' hypothesis(Harper, 1977; Foster. 1982b) receives some sup-port from this study. Fruit production in a givenyear was negatively correlated with the previousyears's reproductive effort in the majority of spe-cies. Nonetheless. absolute correlation coefficientswere low and mostly insignificant. More con-vincing is the evidence that vegetative growth andfruit production in the same year are negativelycorrelated in 12 of 15 species. Larger sample sizeand more detailed estim~tesof fruit crop size ma~'clarify the relationship between fruit productionand vegetative growth or previous reproduction,

The 'seed predation' hypothesis, unlike the 'al-location' hypothesis. predicts tight between-yearsynchrony within populations (see Augspurger1981). Such was not the case in the Lauraceae ofMonteverde. The fact that seed predation is ex-tremely high suggests that the selection pressurefor synchronous fruiting exists. Moreover, pre-dis-persal predation (chiefly by weevils) was most se-

Fruit production in tropical forests is inconstant.both within years (Snow. 1965; Hilty. 1990; Foster.1982a: Wheelwright. 1985a) and between years(Foster. 1982b; Howe. 1983). This study demon-strates that reproduction in an important group ofbird-dispersed tree species varies annually. Duringseven years. most Lauraceae at Monteverde. CostaRica fruited prolifically in three years and pro-duced relatively little fruit during four years. Still.individual trees and species fruited out of phasewith the broader pattern. Consistency and predic-tability (Colwell. 1974) were higher at the commu-nity level than at the species or individual level(Putz. 1979). Although the data suggest a two- tothree-year cycle in fruit production among Mon-teverde.s Lauraceae. seven years is too short a timeto detect such periodicity. Nonetheless. supra-an-nual reproductive cycles are known for many tem-perate tree species. especially conifers. oaks andbeech (Gysel, 1956.1971; McNeill. 1954; Rehfeldtt't ClI.. 1971; Silvertown, 1~8U; Svardson. 1957). andare suspected for certain tropical trees (Foster.1982b). Surprisingly. only the studies of Gysel(1956) and Janzen (1978) present long-term data onmarked individuals. The dearth of such studies haspermitted a misconception about mast fruiting.Oefined as synchronous reproduction at irregularintervals at a periodicity characteristic of the spe-cies (Silvertown. 19~O). mastingis probauiy rarelycompletel~' synchronous or periodic. and it is per-haps ~haracteristic oniy oi indi\'iduals. judgingfrom this study.

Despite the high variation observed among indi-\'iduals. fruiting was not random within species.Most individu.us ill .1 populatioll at Montevt:rdetellded to fruit at the same time within and betweenyears. and fruit crop sizes were grossly similar

33)

vere among the erratic and periodic fruiters (Table3), and rather low in most species of consistent,low-level fruiters (although it is not obviouswhether this is cause or effect of phenology). Post-dispersal seed predation rates (caused mainly byheteromyid rodents) were uniformly high (ap-proaching 100%) except for the genus Beilschmie-dia. whose seeds are protected by a stony endocarp(N. T. Wheelwright, unpublished data). As for the'pollinator limitation' and 'community coadapta-tion' hypotheses, I have no data to test the former.and the latter is discredited on a number of grounds(Poole and Rathcke, 1979)..Annual variation in fruit production did not seemobviously related to climatic variability, but moredetailed measurements of the yearly distribution ofrainfall need to be made. I suspect that annualvariation in fruit production results from a com-bination of life-history trade-offs (previous re-productive efforts, vegetative growth: ct. Bull andShine, 1979), responses to climatic variation (Fos-ter. 1982b). and changes in pollinator abundanceand behavior.

their seed or seedling biology suggests unusuallyhigh survival to compensate for low fecundity.Rather, it seems probable that a fraction of thepopulation, located in distinct habitats, may beresponsible for most successful reproduction.Large portions of a forest may be suitable for aplant's growth, but only fragments of the habitat -

or perhaps only other habitats -may support repro-duction as '.veil. Strong winds blow year -roundacross the lower montane rain forest: quite possi-bly, insect pollination and high seed set occur onlyin sheltered coves, even though seeds may be dis-persed and seedlings survive in open areas. Thus.the conspicuous trees that constitute the over-whelming biomass in certain habitats may owetheir presence toa constant rain of propagules fromsome other part of the forest where conditionsfavor reproduction.

The demonstration that individual trees and spe-cies vary from year to year in fruit production raisesthe question of how fruit-eating birds are affected.In temperate zone conifers, supra-annual cycles inreproduction lead to major movements of certainbirds species (Bock and Lepthien. 1976: Svardson.1957) and influence the timing of reproduction inothers (Ligon. 1978). Irruptions may occur as wellin tropical fruit-eating birds. Conceivably, somelife history features of fruit-eatingbirds.suchasthedelay in reproductive maturity typical of many spe-cies, are r:elated to supra-annual cycles of fruitproduction in a manner analogous to seed-eatinginsects (Kraft, 1968). Only long-term studies ofboth trees and birds will determine the effect onbirds of annual variation in fruit production in thetrees on which they depend.

Variance in reproductive success among trees

Several species in this study produced perplexinglyfew fruits over a six-year period. Ocotea sp. RP. acommon canopy tree of the lower montane rainforest, provides one example. I systematically ob-served 12 individuals over the study period andcasually noted fruit production in another dozenindividuals. I estimated that the entire sample of 24trees produced no more than 10.000 fruits over asix-year period. Most trees bore fewer than 1001.4-g fruits each year, despite producing hundredsof thousands of insect-pollinated flowers yearly.This contrasts with O. tonduzii, a species similar inhabitat, stature, and fruit size. Single O. tonduziiindividuals bore up to 100,000 fruits in a season.Because the odds are so minimal that any fruit willbe swallowed, its seed safely dispersed. and theseedling spared being shaded out. destroyed byherbivores, or buried by a treefall. it is hard toimagine that the infecund O. sp. RP individuals inmy sample are actually replacing themselves ordispersing many successful propagules. Nothing in

Conclusion

It is commonplace to note that we need long-termstudies of marked individuals to provide answers tocritical ecological questions. I bother echoing thisappeal in the case of studies of plant reproductionbecause the data are relatively effortlessly ob-tained. Although only a handful of such studieshave been published on tropical. or even temperatezone trees. many researchers doubtless have

34

Literature citedgathered data similar to those presented in thispaper. Annual monitoring of trees bordering one'sstudy site (or one's backyard), if carried out withcareful records over several decades, would beenormously valuable. Phenological observationsneed be neither highly quantitative nor very fre-quent in order to make a contribution, given thatwe have so little information on lifetime patterns ofreproduction in long-lived plants. Records of sim-ple presence or absence of fruits, or, better yet,qualitative indices of fruit production such as thosepresented here, would be useful. The validity ofinfrequent phenological sampling should bechecked against more frequent censuses. Samplingbiases to be aware of when establishing a censustransect include the non-random selection of cen-sus trees (such as trees along a path, or conspic-

uously fruiting trees).Seven years is far from 'long-term,' but the re-

sults of this study illustrate that the period is longenough to show annual variation in fruit produc-tion among individuals and species, and to suggestsupra-annual reproductive periodicity in tropicaltrees.

Acknowledgements

Earlier versions of this paper were improved by thecomments of Alejandro Estrada, Ted Fleming,Charlie Janson, Sarah Sargent, David Snow andMark Witmer. Bob Lawton and John Campbellgraciously supplied meterological information. BillHaber introduced me to the Lauraceae of Mon-teverde. Jim Wolfe conducted most of the phe-nological observations for the year 1981-1982. Iwould like to express appreciation to the entireMonteverde community and to acknowledge sup-port from the Organization for Tropical Studies,Sigma Xi, the National Science Foundation, a Na-tional Academy of Sciences John Henry Grant. aCarr Postdoctoral Fellowship at the University ofFlorida, and the Section of Ecology and Systema-

tics, Cornell University.

Alvim, P. de T. and R. Alvim. 1978. Relation of climate to

growth periodicity in tropical trees. In: Tropical trees as livingsystems (eds. P.B. Tomlinson and M.H. Zimmermann).Cambridge Univ. Press, New York. pp. 445--464.

Augspurger, C.K. 1981. Reproductive synchrony of a tropicalshrub: experimental studies on effects of pollinators and seedpredators on Hybanthus prunifolius (Violaceae). Ecology 62:775-788.

Baker, H.G., K.S. Bawa, G.W. Frankie andP.A. Opler. 1983.Reproductive biology of plants in tl:opical forests. In: Tropi-cal rain forest ecosystems (ed. Golley, F.B.). Elsevier Sci.Publ. Co., New York.

Bock. C.E., and L. W. Lepthien. 1976. Synchronous eruptions

of boreal seed-eating birds. Am. Nat. 110: 559-571.Bull. J.J.. and R. Shine. 1979. Iteroparous animals that skip

opportunities for reproduction. Am. Nat. 114: 296-303.Buttrose, N.S. and E.D. Alexander. 1978. Promotion of floral

initiation in Fuerta avocado by low temperature and shortdaylength. Scientia Hort. 8: 213-217.

Colwell, R. K. 1974. Predictability, constancy, and contigency ofperiodic phenomena. Ecology 55: 1148-1153.

Crome, F.H.J. 1975. The ecology of fruit pigeons in tropicalnorthern Queensland. Aust. Wild. Res. 2: 155-185.

Eis, S., E.H. Garman and L.F. Ebel. 1965. Relation betweencone production and diameter increment of douglas fir(Pseudotsuga menziesii (Mirb.) Franco), grand fir (Abiesgrandis Dougl.), and western white pine (Pinus monticolaDougl.). Can. J. Bot. 43: 1553-1559.

Foster. R.B. 1982a. The seasonal rhythm of fruitfall on BarroColorado Island. In: The ecology of a tropical forest (eds.E.G. Leigh, Jr., et al.), pp. 151-172. Smithsonian InstitutionPress. Washington. D.C.

Foster, R.B. 1982b. Famine on Barro Colorado Island. In: Theecology of a tropical forest (eds. E.G. Leigh. Jr. el al.). pp.201-212. Smithsonian Institution Press. Washington. D.C.

Fournier, L.A. and C. Charpentier. 1975. EI tamano de lamuestra y la frecuencia de las observaciones en el estudio delas caracteristicas fenol6gicas de los arboles tropicales. Tur-rialba 25: 45-48.

Frankie. G. W. 1975. Tropical forest phenology and pollinator-plant coevolution. In: Coevolution of animals and plants(eds. L.E. Gilbert and P.H. Raven). pp. 192-209. Univ.Texas Press. Austin. Texas.

Frankie, G. W ,. H.G. Baker and P .A. Opler. 1974. Compara-tive phenological studies of trees in tropical wet and dryforests in the lowlands of Costa Rica. J. Ecology 62: 881-919.

Gysel. L. W. 1956. Measurements of acorn crops. Forest. Sci. 2:

305-313.Gysel. L. W. 1971. A 100year analysis of beechnut production

and use in Michigan. J. Wildl. Manag. 35: 516-519.Harper, J .L. 1977. Population biology of plants. Academic

Press, New York.

35';

cal wet and dry forests in the lowlands of Costa Rica. J.Ecology 68: 167-188.

Poole. R.W. and B.J. Rathcke. 1979. Regularity. randomnessand aggregation in flowering phenologies. Science 203: ~70-471.

Putz. F.E. 1979. Aseasonality in Malaysian tr~e phenology.Malay. For. 42: 1-24.

Rehfeldt. G.E.. A.R. Stage and R.T. Bingham. 1971. Strobilidevelopment in Western White Pine: periodicity. predictionand association with weather. Forest Sci. 17: 454-461.

Silvertown. J. W. 1980. The evolutionary ecology of mast seed-ing in trees. Bioi. J. Linnaean Soc. 14: 235-250.

Smythe, N. 1970. Relationships between fruiting seasons andseed dispersal methods in a neotropical forest. Am. Nat. 104:25-35.

Snow. B.K. 1970. A field study of the Bearded Bellbird inTrinidad. Ibis 112: 299-329.

Snow. B.K. 1977. Territorial behavior and courtship of the maleThree-wattled Bellbird. Auk. 94: 623-645.

Snow, D. W. 1965. A possible selective factor in the evolution offruiting seasons in a tropical forest. Oikos 15: 274-281.

Snow. D. W .1971. Evolutionary aspects of fruit-eating by birds.Ibis 113: 194-202.

Snow. D.W. 1973. Distribution. ecology and evolution of thebellbirds (Procnias. Cotingidae). Bull. Brit. Mus. (Nat.Hist.) Zoology 25: 1-14.

Stiles. F.G.1977. Coadapted competitors: the flowering seasonsof hummingbird-pollinated plants in a tropical forest. Science198: 1177-1178.

Svardson. G. 1957. The .invasion. type of bird migration. Brit.Birds 50: 314-343.

Thompson. J.N., and M.F. Willson. 1979. Evolution of temper-ate bird/fruit interactions. Evolution 33: 973-982-

Wheelwright, N. T. 1983. Fruits and the ecology of ResplendentQuetzals. Auk 100: 286-301.

Wheelwright, N.T. 1985a. Competition for dispersers. and thetiming of flowering and fruiting in a guild of tropical trees.Oikos 44: 465-477.

Wheelwright, N. T. 1985b. Fruit size. gape width. and the dietsof fruit-eating birds. Ecology 66: 808-818.

Wheelwright, N.T., W.A. Haber. K.G. Murray and C. Guin-don. 1984. Tropical fruit-eating birds and their food plants: asurvey of a Costa Rican lower montane forest. Biotropica 16:

173-192-Wheelwright, N.T. and G.H. Orians. 1982- Seed dispersal by

animals: contrasts with pollen dispersal. problems with termi-nology, and constraints on coevolution. Am. Nat. 119: ~02-

413.

Hilty. S.L. 1980. Flowering and fruiting periodicity in a premon-tane rain forest in Pacific Colombia. Biotropica 12: 292-306.

Holdridge. L. 1967. Life zone ecology. Tropical Science CenterPubl.. San Jose. Costa Rica.

Howe. H.F. 1983. Annual variation in a neotropical seed-dis-persal system. In: The tropical rain forest: ecology and man-agement (eds. S.L. Sutton et af.). pp. 211-227. Blackwell Sci.Publ.. Oxford.

Howe. H.F. andG.F. Estabrook. 1977. On intraspecificcompe-tition for avian dispersers in tropical trees. Am. Nat. III: 817-832.

Janzen. D.H. 1967. Synchronization of sexual reproduction oftrees within the dry season in Central America. Evolution 21:620-637.

Janzen, D.H. 1976. Why bamboos wait so long to flower. Ann.Rev. Ecol. Syst. 7: 347-391.

Janzen. D.H. 1978. Seeding patterns of tropical trees. In: Tropi-cal trees as living systems (eds. P .B. Tomlinson and M.H.Zimmerman) pp. 83-128. Cambridge Univ. Press. NewYork.

Kraft. K.J. 1968. Ecology of the cone moth Laspevresia torll/eta.in Pinus banksiana stands. Annals Ent. Soc. Amer. 61: 1462-1465.

Lawton. R. and V. Dryer. 1980. The vegetation of the Mon-teverde Cloud Forest Reserve. Brenesia 18: 101-116.

Ligon, D.J. 1978. Reproductive interdependence of pinyon jaysand pinyon pines. Ecol. Monogr. 48: 111-126.

McClure. H.E. 1966. Flowering. fruiting. and animals in thecanopy of a tropical rainforest. Malay. For. 29: 182-203.

McKey. D. 1975. The ecology of coevolved seed dispersal sys-tems. In: Coevolution of animals and plants (eds. L.E.Gilbert and P .H. Raven). pp. 159-191. Univ. Texas Press.Austin. Texas.

McNeill. W.M. 1954. Observations on cone and seed productionin plantations of Scots Pine in Scotland. Forest. 27: 122-133.

Medway. L. 1972. Phenology of a tropical rainforest in Malaya.Bioi. J. Linn. Soc. 4: 117-146.

Milton. K.. D.M. Windsor. D.W. Morrison and M.A. Estribi.1982. Fruiting phenologies of two tropical Ficus species. Ecol.63: 752-762.

Monasterio. M. .and G. Sarmiento. 1976. Phenological strat-egies of plant species in the tropical savannah and the semi-deciduous forest of the Venezuelan llanos. J. Biogeogr. 3:

325-356.Opler. P.A.. G. W. Frankie and H.G. Baker. 1976. Rainfall asa

factor in the synchronization. release. and timing of anthesisby tropical trees and shrubs. J. Biogeog. 3: 231-236.

Opler. P.A.. G.W. Frankie and H.G. Baker. 1980. Compara-tive phenological studies of treelet and shrub species in tropi-