Frugivores and Fruit Syndromes: Differences in Patterns at the Genus

OIKOS66: 472-482. Copenhagen1993

Frugivoresand fruit syndromes:differences in patternsat the genus and specieslevel

Kathleen E. Fischer and Colin A. Chapman

Fischer, K. E. and Chapman,C. A. 1993. Frugivoresand fruit syndromes:differences in patternsat the genus and species level. - Oikos 66: 472-482.

Comparativestudies have suggestedthat fruit traits,such as color, size, and protection, have evolved as covaryingcharacter complexes ("dispersalsyndromes") in responseto selectionby frugivorousdispersers. However, many comparative studies of disperser-specificsyndromes have used species as samplingunits, a methodwhich implicitlyassumes that charactercomplexes evolve de novo in each species. This approachoverestimates the numberof times a charactercomplex has evolved because covariationthat resultsfrom commonancestry (plesiomorphy) is confounded with covariationacross independentlineages (convergence).We compileddata on fleshy fruittraits from five regionalfloras to test the hypothesisthat fruittraits form charactercomplexes which covary independently of phylogeny(i.e. acrosslineages). Our results suggest that such charactercomplexes are rare, and that analyses of covariationamong these charactercomplexes are extremely sensitive to the in- vestigator'schoice of samplingunit. When syndromesderived from observationsof the foragingbehavior of frugivoresare analyzedusing species as samplingunits, our data show significantassociations among traits at four out of five locations. In contrast,when genera are used as samplingunits, there is no significantassociation amongtraits at any of the sites. Theoriesof coevolutionbetween fruits and frugivores have proposedthat fruit morphologyis a responseto selective pressuresexerted by frugivorousbirds and mammals.If these frugivoreshave shaped fruit morphology into dispersal-relatedcharacter complexes or syndromes,then traitsassociated with a syndromeshould be absent or much reducedin frequencyin regions lacking that guild of dispersers.To test this prediction,we examinedthe flora of New Guinea, which lacks primatesand other diurnalmammalian frugivores, and found no difference in the frequencyof traitsassociated with dispersalby diurnalmammals.

K. E. Fischer and C. A. Chapman, The Biological Laboratories,and Peabody Museum,Harvard Univ., Cambridge,MA 02138, USA.

Most tropical rainforest trees produce fruits that are studies have produced little empirical support for tight consumed by animals and are thought to rely on frugi- coevolutionary relationships between plants and their vores for seed dispersal (Frankie et al. 1974, Howe seed dispersers (Howe and Smallwood 1982, Wheel- 1986, Dowsett-Lemaire 1988). Comparative studies wright and Orians 1982, Herrera 1984, 1985, 1986, (Ridley 1930, Turcek 1963, van der Pijl 1969, Snow Howe 1984). These findings have been attributed to 1981, Janson 1983, Knight and Siegfried 1983, Pratt and factors which limit the potential for mutualistic coevolu- Stiles 1985, Wheelwright and Janson 1985, Herrera tion between plants and their animal dispersers, in- 1986, Howe 1986, Dowsett-Lemaire 1988) have sug- cluding: asymmetries in the relationship between plants gested that fruit traits, such as color, size, and protec- and their dispersers, inequalities in the evolutionary life tion, have evolved as covarying character complexes spans of plant and animal taxa, differences in gener- ("dispersal syndromes") in response to selection by fru- ation lengths of plants and their dispersers, extensive givorous dispersers (Table 1). However, seed dispersal gene flow between plant populations, weak selective

Accepted 8 May 1992 ? OIKOS

472 OIKOS 66:3 (1993) Table 1. Bird and mammal fruit syndromes based on observations of frugivore foraging behavior derived from the literature. Note: 1) the variability in syndromes ascribed to the same disperser guild in different geographic regions, 2) the variability in the extent to which syndromes are subdivided by disperser guilds (e.g. mammal vs arboreal mammal), and 3) the variability in the composition of guilds in different regions (e.g. bird vs mammal in Peru, in contrast to birds and monkeys in Gabon and Malawi).

Bird fruit syndromes

Site/Type Size* Form Color Protection Source

Peru < 14 mm not given red, black, mixed, none Janson 1983 blue, white, purple Gabon <5g berry, drupe, purple, red thin or dehiscent Gauthier-Hion et al. capsule 1985 Costa Rica not given juicy, persistent bright not given Wheelwright et al. 1984 Montane New t = 11.6 figs, capsule and mixed, white, none or dehiscent Beehler 1982 Guinea range 3-28 drupe green, pink, yellow, red, purple, orange Southern Africa "small" pod, capsule, red, black dehiscent or none Knight and Siegfried drupe, berry 1983 Malawi "small" - 3-50 ml m berries, drupes, black, green, none, dehiscent, Dowsett-Lemaire capsules orange, red, protected 1988 yellow, blue, brown, white, purple Highly frugivorous large, > 10 mm aril, drupe blue, black dehiscent, Howe 1986, Howe long unprotected and Westley 1988 Partly frugivorous < 10 mm long aril, berry drupe black, blue, not given Howe 1986, Howe orange, red, white and Westley 1988 Generalized "small" berry, drupe, none given none Snow 1981 frugivores capsule, aril Specialized "large" berry, drupe, none given none or dehiscent Snow 1981 frugivores capsule, aril

Mammal fruit syndromes

Site/Type Size* Form Color Protection Source

Peru > 14 mm none given brown, green, present Janson 1983 white, yellow Gabon 5-50 g berry, drupe, bright red, orange, not significant Gauthier-Hion et al. capsule yellow 1985 Southern Africa "large" pod, capsule, yellow, green not given Knight and Siegfried drupe, berry 1983 Malawi "variable" x = 15 berry, drupe, red, none, Dowsett- Lemaire - purple, green, protected, range 4-100 capsule orange, brown, dehiscent 1988 yellow, white Arboreal "large" aril, compound green, brown, often dehiscent Howe 1986, Howe orange, white, and Westley 1988 yellow Aerial "large" various green, yellow not given Howe 1986, Howe and Westley 1988 Hoarding none given nuts brown thick walls, Howe and Westley indehiscent 1988 Terrestrial none given nuts, pods or green, brown indehiscent Howe and Westley capsules 1988 * width in mm, unless noted otherwise.

OIKOS 66:3 (1993) 473 pressures on dispersers, ecological variables outside the iability and may underestimate the number of evolu- control of the parent plant (e.g. influence of other fruit- tionary transitions between character states. In addi- ing plants, numbers and kinds of seeds in feces), unpre- tion, a lack of accurate phylogenies for the taxa in dictability of germination sites, secondary dispersal sub- question renders comparative analyses insensitive to the sequent to deposition by the primary disperser, morph- direction and sequence of character transformation ological similarities among dispersers, and lack of (Donoghue 1989). evolutionary plasticity in fruit traits (Wheelwright and Because we lack accurate phylogenies for the plants Orians 1982, Howe 1984, Herrera 1985, 1986, Loiselle in question, we treated genera as monophyletic groups 1990). In addition, fruit traits may represent a response and assumed that each character complex represented to other selection pressures or may perform more than in the genus evolved no more than once within that one function. For example, it has been suggested that genus. For example, given a genus containing five spe- green fruits reduce the energetic costs of reproduction cies with unprotected red fruits and two species with through photosynthesis (Wheelwright and Janson 1985, unprotected black fruits, each complex (unprotected- Cipollini and Levey 1991) or that red fruit colors pro- red and unprotected-black) would be counted as having vide protection from arthropod predators through cryp- evolved once. sis (Willson and Thompson 1982). Genera may be more appropriate sampling units than The objectives of this study are to examine the degree species or higher taxa (e.g. families) for attempting to to which plants have evolved predictable, disperser- identify coevolved dispersal syndromes because 1) gen- specific syndromes and to determine the consequences era are more likely to be monophyletic than higher taxa; of using different taxa as sampling units when analyzing 2) use of genera as sampling units prevents speciose taxa comparative data to test for the existence of dispersal from dominating the analyses; 3) traits shared among syndromes. If syndromes have evolved in response to species within a genus are likely to be the result of selection by frugivorous dispersal agents then 1) con- common descent rather than convergence (see also Jan- vergent evolution should produce character complexes son 1983). Our assumption, that each character com- that covary across lineages among plants that share plex evolved only once within a genus is based on the dispersers and 2) regions that lack a particular group of premise that within a monophyletic clade the most dispersal agents (e.g. diurnal mammals) should show a likely evolutionary pathway is that which minimizes the low frequency of traits associated with dispersal by that number of transitions (i.e. that evolution tends toward guild. We first assess these predictions by testing the parsimony). Use of genera as sampling units is not a hypothesis that fruit traits covary across taxa. To do this panacea: because genera are related to one another, we examine the effects of using species and genera as assuming that traits evolve de novo within genera and sampling units: if syndromes are the result of conver- that genera are independent within families can over- gent evolution, patterns should persist whether genera estimate the number of times each character complex or species are used as sampling units. Second, in order evolved; however, analyses using genera as sampling to make our statistical tests more stringent, we use two units inflate estimates of the number of evolutionary "consensus" color syndromes (consensus definitions of events far less than does the use of species as sampling bird and mammal fruit colors derived from the litera- units. ture; see Table 1), to determine whether size and pro- To illustrate this point, let N be the number of genera tection covary with these color syndromes as predicted per character complex within a family, and let P be the by observations of frugivores' foraging behavior. Fi- number of species per character complex within a ge- nally, we test the specific prediction that character com- nus. Using genera as sampling units will inflate the plexes associated with a given frugivore guild should number of evolutionary events within a family by a decrease in frequency when that guild is absent. maximum of N for the family's plesiomorphic character Choosing the appropriate taxonomic level for analysis complex and by a maximum of N-1 for each derived poses the problem of what to consider an independent character complex. Analyses of the same family using evolutionary event (Huey 1987, Pagel and Harvey 1988, species as the sampling units will inflate the number of 1989, Gittleman and Kot 1990). Many comparative evolutionary events by (N)(P) for the plesiomorphic studies present analyses that use species as sampling character complex and (N-1)(P) for each derived char- units, a method which implicitly assumes that the character complex within the family. For example, given a acter complexes in question evolved independently in family with five genera, each of which has four species each species of a given clade. It is unlikely that all that produce brown-husked fruits, the most parsimo- species within a genus are independent with respect to nious assumption is that brown-husked fruits evolved fruit morphology, and therefore analyses using species once and the remaining species inherited this condition as sampling units are likely to inflate estimates of the as a plesiomorphic trait. If fruits with brown husks are number of times a particular character complex the family's ancestral condition (plesiomorphic), then evolved. Without accurate phylogenies, use of higher use of genera as sampling units overestimates the num- taxa becomes problematic because including polyphy- ber of evolutionary events by a maximum of N, i.e. 5. letic taxa in analyses overestimates within-taxon var- Alternatively, if brown-husked fruits are derived (syn-

474 OIKOS 66:3 (1993) apomorphic) with respect to the family's ancestral fruit, flora of New Guinea. New Guinea offers an ideal test of then we have overestimated the number of times brown this prediction because it lacks diurnal mammalian fru- husks have evolved by a maximum of N-1 or 4. The givores; although it has frugivorous birds, bats, rodents, same analysis, performed using species rather than gen- and marsupials, the bats, rodents, and marsupials are era as sampling units, could inflate the estimates of the nocturnal (Lee and Cockburn 1985, Fischer pers. obs.). number of times brown husks evolved by a maximum of In addition, there are a number of historical and bioge- (N)(P), i.e. 20, in the plesiomorphic case and by a ographical reasons that we would not expect to find maximum of (N-1)(P) or 16 in the derived case. Thus, fruits adapted for diurnal mammalian dispersal in New while each analysis risks inflating estimates of the num- Guinea. ber of times a character complex has evolved, the use of New Guinea's biota is derived from two geographic genera reduces by a factor of P the maximum potential regions: West Malesia (Borneo, Malaya and the lands of error. the Sunda continental shelf west of Wallace's line) and In contrast, our assumption that evolution tends to- Sahul (Australia and adjacent islands) (Gressitt 1982a). ward parsimony may underestimate the number of evo- The majority of plants (van Balgooy 1976, Walker and lutionary events within the genus (i.e. at the species Hope 1982), invertebrates (Main 1982, Evans 1982, level). If character complexes are repeatedly derived Gressitt 1982b), reptiles, amphibians (Zweifel and Tyler within genera, then the assumption of parsimony is false 1982), and birds (Mayr 1988) in New Guinea originated and will cause an underestimation of the number of in West Malesia, while most of the mammals are de- times a character complex has evolved. For example, rived from Sahul (Gressitt 1982a). Geologic evidence suppose that a genus contains four species with blue- (A and the bicentric distribution of some important floristic and B) and green-husked (C and D) fruits. Assuming elements in Malesia suggest that many Malesian plant that blue-husked fruits are derived with respect to the species reached New Guinea before the collision of genus, the most parsimonious sequence would be that Australia with the Sundaic island arcs during the Mio- blue-husked fruits evolved once in A and were inherited cene (Audley-Charles 1987). Indeed, there is palyn- by (plesiomorphic for) B (i.e. A -> B). Similarly, if ological evidence for land connections between Austra- green-husked fruits were derived with respect to the lia-New Guinea and Asia as far back as the mid-Creta- genus, the most parsimonious scheme would be if green ceous (Truswell et al. 1987). Thus, a large number of husks evolved once in C and were subsequently inher- plant taxa were likely to be established in both regions ited by D (i.e. C > D). In contrast, if we knew the before the arrival of many of the extant mammalian phylogeny was C -> B, and A -> D, then green-husked species at either site. In New Guinea, the plant taxa that fruits would have evolved twice, once in C, and once predate the arrival of diurnal mammalian frugivores in from the blue-husked condition in D. Likewise, blue- Sunda should be adapted to bird, bat, marsupial, or husked fruits would have evolved twice, once in A, and wind dispersal. once from the green-husked condition in B. In this case Second, it is unlikely that Sundaic plants with fruits the effect of our assumption of parsimony would be to adapted for non-volant mammalian dispersal have colo- underestimate the number of times green-husked and nized New Guinea because of the persistent oceanic blue-husked fruits had evolved. barriers between New Guinea and the Sunda shelf. The The effects of these two potential sources of error, major land masses reached positions close to those they assuming that genera are independent and assuming currently occupy approximately 15 million years ago that evolution is parsimonious, are in opposite direc- (Whitmore 1987). Although sea levels fluctuated con- tions. Overestimating the number of times that a char- siderably during the Plio-Pleistocene, substantial bar- acter complex has evolved will mimic syndromes of riers to dispersal between Sundaland and New Guinea correlated characters, whereas underestimating the persisted. It is probable that most plant taxa that reach- number of evolutionary events may obscure syndromes. ed New Guinea during this period did so with volant In the best of all possible worlds the potential inflation dispersers (i.e. birds, bats, and wind). Thus, in New caused by the first assumption would exactly offset the Guinea we expect that character complexes associated potential under-estimation caused by the second. Al- with dispersal by diurnal mammalian frugivores should though it is unlikely that these factors will balance one be under-represented relative to those character com- another perfectly, there is no reason to believe that the plexes associated with bird and bat dispersal. two assumptions, taken together, consistently bias our results. In contrast, analyses using species as sampling units employ the least parsimonious assumptions and increase the risk of overestimating the number of times Methods that a character complex has evolved by a factor of P. Our second prediction was that regions lacking a Data on fruit size, color, and structural protection were guild of dispersal agents (e.g. diurnal mammals) should collected from the published literature and floras: show a low frequency of traits associated with dispersal Guiana (van Roosmalen 1985); Malaya (Whitmore by that guild. To test this prediction we examined the 1972, 1973, Ng 1978); New Guinea (Womersley 1978,

OIKOS 66:3 (1993) 475 Table2. Foreach site we list the total numberof genera,the meannumber of characterstates found within a genus,the proportion of generawith either protectedor unprotectedfruits, the proportionof generawith both protectedand unprotectedfruits, the proportionof generawith fruitsof only one color, the proportionof generawith fruitsin two color categories,the proportionof generawith fruitsin three color categories,the proportionof generawith fruitsin four color categories,and the proportionof generawith fruitsin five color categories. Guiana Uganda Malaya New Guinea Panama

No. of Genera 132 24 64 35 59 Mean characterstates/genus 2.6 2.4 2.3 2.5 2.7 Genera w/1 protectionstate 92.1% 100% 87.8% 77.8% 86.7% Genera w/2 protectionstates 7.9% 0% 12.2% 22.2% 13.3% Genera w/1 color 11.2% 10% 34.1% 22.2% 30.0% Genera w/2 colors 36.0% 50% 24.4% 50.0% 30.0% Genera w/3 colors 39.3% 3% 24.4% 16.7% 20.0% Generaw/4 colors 11.2% 10% 14.6% 5.6% 20.0% Genera w/5 colors 2.2% 0% 2.4% 5.6% 0%

Henty 1981, Johns 1987); Panama (Croat 1978, Chap- these analyses, fruit colors were consolidated into two man pers. obs.) and Uganda (Hamilton 1981 and Chap- categories corresponding to a consensus definition of man pers. obs.). Fruits were classified as structurally bird (red, pink, blue, black and purple) and mammal protected if the exocarp was greater than 3 mm thick or (orange, yellow, green, brown) color syndromes (Table described as thick, leathery, coriaceous, or woody. 1). The data were then analyzed using G-tests to deter- Fruits with spines, stinging hairs or other forms of me- mine whether color (bird or mammal) and protection chanical defense were also considered to be protected. were associated among the tabulated taxa within each Only non-dehiscent, fleshy fruits were considered since geographic location. This analysis was performed twice, botanists do not employ uniform criteria in describing once with genera as the sampling units, and once with dehiscent fruit. Color was assigned based on descrip- species as the sampling units. If sample sizes were less tions of ripe material only. If more than one color was than 50, G-tests were adjusted for small sample size listed for a ripe fruit (e.g. red or black when ripe) the using Williams' correction (Sokal and Rohlf 1981). species was listed in both color categories. If more than These data are not without shortcomings. Floristic one color was present on ripe individual fruits, then the accounts of fruit color and size are usually based on field fruit was classified as having mixed colors and was ex- data; however, fruit construction is often analysed using cluded from our analysis. Fruit size was based on pub- herbarium specimens which differ in their state of pres- lished measures of the diameter of fresh, ripe speci- ervation and the extent to which relevant characters mens. When a range of values was given, the mean for such as husk thickness are preserved. Nonetheless, the range was used. these problems are unlikely to act in a consistent fashion The color and protection state of fruit in each species that would bias our results. within a genus was tabulated and each unique occur- Because inferential statistics are techniques designed rence was scored. Each color and each category of primarily to reject a false null hypothesis, rather than to protection is considered a character state; color and confirm it or to test its reliability, it is important to protection, together, form a character complex. When a determine the statistical power of a test if confirmation genus contained species with different character states, of a null hypothesis is required (Cohen 1988). Power each character complex was scored as evolving once tests are often used to determine the ability of a given within that genus. Thus, if a genus contained species statistical test to detect type II error or the probability producing brown, husked fruits and species producing of failing to reject a false null hypothesis. For statistical orange, husked fruits, the character complexes orange- tests where the null hypothesis is of particular interest, husked and brown-husked were each scored as having power analyses should be used to ensure that the power evolved once within that genus. Analyses performed of the test (1-D) is as large as possible and I3is minimized with species as sampling units employed the same pro- (Sokal and Rohlf 1981). The larger 1-(3, the smaller the cedures. probability that one has failed to reject a false null The mean size of fruits in each character complex was hypothesis. The power of a test is determined, in part, determined for each region. The mean size of fruits by the size of the difference or the "effect size" one within each genus was also determined and ANOVA wishes to detect. Effect size is the difference between was used to compare the generic means of the character the distribution posited by the null hypothesis (in our complexes within regions. analyses, no association between character states) and We used G-tests to determine whether color and pro- that posited by the alternative hypothesis (i.e. reliability tection were associated among the tabulated genera and of retaining some association between character states). species within each geographic location. Following As the effect size to be detected becomes smaller, the

476 OIKOS 66:3 (1993) 60 60- N 30

NEWGUINEA UGANDA 30 30 LU ~ X Z20 w 20 C, *10 RED ORANGE / I .-E -- RED ORANGE BROWN RED ORANGE BROWN a BLUE GREEN d BLUE GREEN

60 UJ Lm N N 30 _ O- GUIANA $ 30 ru u 20 Co $I 10 d?

RED ORANGE BROWN RED ORANGE BROWN b BLUE GREEN e BLUE GREEN

60 N 30

MALAYA 30 % rU 3 20 Fig. 1. The proportionof genera containingspecies in each charactercomplex for the five regions.These proportionsmay sumto morethan 100because genera may have species in more than one charactercomplex. The mean diasporesize (in mm) RED ORANGE BROWN for each charactercomplex is given above the histogram.Solid bars indicate protected complexes; hatched indicate unpro- c BLUE GREEN tected complexes.

OIKOS 66:3 (1993) 477 Table3. Resultsfor each of the analyses.Analyses are subdividedby region,by how the color of fruitswas categorized(colors or consensussyndromes), and by the taxon used as the samplingunit (species or genus). Valuesfor the G-test, P-values,and the power (1-1) of each comparisonare provided. Location Category Samplingunit G-value P-value 1-B-value

Uganda colors species (N=81) 12.99* <0.025 0.83 genus (N=24) 1.17 >0.50 0.19 syndrome species (N=81) 2.92 >0.05 0.37 genus (N=24) 0.73 >0.10 <0.17 Malaya colors species (N=411) 63.41* <<0.001 0.90 genus (N=64) 1.45 >0.50 0.61 syndrome species (N=411) 29.35** <<0.001 >0.99 genus (N=64) 0.12 >0.50 0.12 New Guinea colors species (N=136) 26.18** <0.001 0.98 genus (N=35) 9.32 >0.05 0.29 syndrome species (N=136) 13.10** <0.001 0.93 genus-(N=35) 1.14 >0.10 <0.22 Guiana colors species (N=570) 51.73** <<0.001 >0.99 genus (N=132) 15.49** <0.005 0.98 syndrome species (N=570) 45.93** <<0.001 >0.99 genus (N=132) 2.73 >0.05 0.47 Panama colors species (N=176) 9.33 >0.05 0.71 genus (N=59) 1.44 >0.50 0.49 syndrome species (N=176) 6.61** <0.01 0.76 genus (N=59) 0.41 >0.50 0.12 *significant at p<0.05. **significantat p<0.01.

power of the test declines and discriminating between significant associations between character states at four null and alternative hypotheses becomes more difficult. out of five locations. In contrast, when genera are used In other words the power of a test decays rapidly as the as sampling units, there is no significant association predictions of the alternative and null hypotheses con- between character states at any of the sites (Table 3). verge, a consequence of the roughly inverse relationship Thus, our first prediction, that if syndromes exist char- between type I and type II error. acter states should covary independently of phylogeny, appears not to be supported. Our results also suggest that analyses of association among character states are extremely sensitive to the choice of sampling unit. Our second prediction was that if existing frugivores Results have shaped fruit morphology into dispersal-related character complexes or syndromes, then traits associ- On average each genus contained two to three character ated with a syndrome should be absent or much reduced complexes (mean across sites = 2.50), indicating flex- in frequency in regions lacking that guild of dispersers. ibility within genera (i.e. at the species level) in the To test this prediction, we examined the flora of New expression of these traits (Table 2). Most species were Guinea, which lacks diurnal mammalian frugivores. monomorphic for color; however there was consider- To determine whether character complexes associ- able variation in color among species within a genus (x ated with diurnal mammalian dispersal were underrep- = 2.56 colors per genus). Similarly, the size of fruits resented in New Guinea, we first determined which within a character complex tended to be quite variable fruit traits are associated with consumption by diurnal (Fig. 1); size often ranged several hundred millimeters mammalian frugivores. The variety of syndromes de- within a single character complex. In contrast, protec- scribed in past studies makes it difficult to determine tion appeared to be less variable than color or size: on traits consistently associated with diurnal mammalian average 11.1% of the genera at each site contained both dispersal. For instance, Gautier-Hion et al. (1985) and protected and unprotected fruit species. Dowsett-Lemaire (1988) unite birds and primates in a When species were used as sampling units, our analy- single dispersal syndrome, whereas other studies (re- ses indicated that color and protection were associated viewed by Howe 1986) have described separate bird and in all locations except Panama (Table 3). In contrast, mammal syndromes. The consensus syndrome used when genera were used as sampling units, color and here is based on Howe's (1986) review, which indicates protection were not associated in any location except that fruits consumed by diurnal mammals generally tend Guiana (Table 3). When consensus syndromes are ana- to be large, mechanically protected, and green, brown, lyzed using species as sampling units, our data show orange, or yellow in color.

478 OIKOS 66:3 (1993) The proportion of genera with these traits in New of years. Fleshy diaspores have evolved multiple times, Guinea did not differ from the proportion of genera in a variety of ecological circumstances (Wing and Tiff- with these traits in the four locations with diurnal mam- ney 1987, Herrera 1989). For some traits, however, it malian frugivores (Fig. 1). It has been suggested that seems likely that a succession of frugivore lineages has primates are usually more capable of handling fruits encountered morphologically similar fruits. This sug- with indehiscent husks than avian frugivores (Howe gests that persistence of some fruit characters depends 1986). We therefore contrasted the number of genera more on the persistence of plant taxa than on the per- with protected and unprotected fruits at all locations to sistence of specific dispersers (Tiffney 1986) and that test the prediction that New Guinea should have fewer some aspects of fruit morphology are exapted (sensu protected fruits than areas with primate frugivores. This Gould and Vrba 1982) to their current dispersers. prediction was not upheld (protection was not signif- Whether or not fruit traits are the result of coevolu- icantly associated with location, (G = 3.03, df = 4, tion, it is likely that plant - frugivore interactions do p>0.50, P = 0.06)). In fact, contraryto prediction, influence the fitness of both interactants. Both macro- New Guinea had the highest proportion of protected evolutionary and microevolutionary consequences of fruits of any location. To test this prediction more rigor- plant - frugivore interaction have been explored (e.g. ously, we performed a pair-wise comparison of genera Herrera 1989, Janson 1992). For instance, Janson found in both New Guinea and Malaya (N = 22 gen- (1992) has proposed that macroevolutionary patterns of era). There was no significant difference between the change in fruit morphology may be influenced by plant- proportion of protected fruits between the two sites frugivore interactions. His analysis of transitions among (Gadj = 4.47, df = 4, p > 0.10, [3 = 0.68). The power of fruit characters, using a Markov model to estimate tran- the first comparison (New Guinea vs the other four sition probabilities, indicates that transitions from un- locations) is sufficient (1-13 = 0.94) that we can retain husked to husked forms are more likely than the reci- the first null hypothesis with relative confidence. Given procal transition. Janson suggests that this may be the G-value and the low power of the second test we can partly due to differences in the foraging behavior of neither accept nor reject the hypothesis that the propor- birds and mammals. Mammals feed on both husked and tion of protected fruits differs in New Guinea and Ma- unhusked fruits, whereas birds feed almost exclusively laya; however, it is important to recall that the low on unhusked fruits (Janson 1983). This, he suggests, power of the second test is, in part, a function of the provides a selection pressure favouring the transition small sample size (N = 22). from unhusked to husked, while a reciprocal selection pressure associated with avian dispersal is never applied to husked fruits. Although Herrera (1989) has shown that plant genera Discussion with fleshy diaspores are no more speciose than those without fleshy diaspores, our analysis suggests that Dispersal syndromes have been compiled based on ob- when only genera with fleshy diaspores are considered servations of frugivores' foraging behavior and diet. some character complexes are more speciose than These syndromes may reflect frugivores' fruit prefer- others (Table 3). In our sample this effect appears to be ences; however, our results suggest that, with respect to the result of including speciose genera within which fruit the traits considered, the evidence garnered thus far is morphology varies little. The radiation of these speciose inadequate to infer that these traits evolved in response genera may or may not be related to seed dispersal, but to selective pressures exerted by frugivores. To propose this result raises the questions of 1) whether some kinds that coevolution between frugivores and fruiting plants of biotic dispersal affect speciation and/or extinction has led to the evolution of fruit character complexes we rates, and 2) if they exist, how the effects are generated. must be able to demonstrate that there have been reci- To pursue these questions we must first determine procal evolutionary changes in the interactants (Janzen whether speciose complexes are actually associated with 1980). Although incomplete, data from the fossil record particular guilds of dispersers, as our analysis of consen- demonstrate that dispersal syndromes persist longer sus syndromes suggests. than dispersers (Tiffney 1986, Herrera 1989). Work which relates the effects of plant - frugivore Gymnosperms have produced fleshy diaspores that interactions to the fitness of the interactants can also are functionally analogous to fruits since at least the offer insights into the evolution of dispersal syndromes. Carboniferous (Herrera 1989). Fleshy angiosperm fruits In several studies (e.g. Becker and Wong 1985, Howe of modern aspect (e.g. drupes) first appear in the Late 1986, Dinerstein and Wemmer 1988, Herrera 1988, Cretaceous (Friis and Crepet 1987), and many modern Murray 1988, Chapman 1989, Loiselle 1990) the influ- families are well established by the early to middle ence of frugivores on the germination and survival of Eocene (e.g. Burseraceae, Anacardiaceae, Annona- seedlings has been examined; such studies relate dis- ceae, Lauraceae, Menispermaceae) (Collinson and persal directly to components of plant fitness. Likewise, Hooker 1987). This implies that aspects of fruit mor- studies which relate the effects of differences in mor- have phology remained relatively constant for millions phology, physiology, and behavior of plants and frugi-

OIKOS 66:3 (1993) 479 vores to components of the fitness of the interactants attempts to determine the effects of biotic dispersal on suggest which traits are currently under selection (e.g. micro- and macroevolutionary processes (e.g. Herrera Herrera 1982, 1984, Levey 1986, Vasquez-Yanez and 1989, Janson 1992). Orozco-Segovia 1986, Murray 1987). Before evaluating data on fruit syndromes, research- Convergence also offers evidence of past selective ers should examine the extent to which species and pressures. For example, the convergence of morphology genera can be treated as independent units for the pur- and physiology among distantly related taxa of folivores poses of analysis. The current study uses a method has been adduced as evidence that functional consid- which is likely to underestimate the number of evolu- erations associated with leaf-eating have exerted strong tionary events at the species level, and to overestimate selective pressures on dentition, gut morphology, and the number of evolutionary events at the genus level. A physiology (e.g. Grand 1978, Kay and Hylander 1978, more satisfying resolution of this problem will be pos- Hume 1982). In this study we used data from floristic sible as phylogenies are better understood (Donoghue accounts to examine plant taxa from various families 1989). Reconstruction of phylogenetic lineages should and geographic regions for convergence in several dis- allow an analysis of the temporal sequence of character persal-related traits (protection, color, and size). Simi- transformation in a limited number of plant groups lar studies that examine convergence among fruiting across a range of geographically and ecologically dis- plants and frugivores may offer insights into the selec- junct sites. This approach could address specific ques- tive pressures which have shaped the morphology, phys- tions concerning the evolution of fruit traits in response iology, and behavior of the interactants (Howe and to selection pressures exerted by frugivorous dispersal Westley 1988). Polymorphic taxa offer a particularly agents. Such studies would also facilitate a more com- useful group (e.g. Herrera 1989). For example, one plete understanding of the influence of phylogeny. Until approach would be to examine the dispersal of poly- phylogenetic information is available, there are a num- morphic plant species in sites with and without key ber of methods that estimate phylogenetic effects (Huey disperser groups. Because polymorphic species are 1987, Pagel and Harvey 1988, Bell 1989, Gittleman and known to have the genetic potential for convergent Kot 1990) and these should be used to avoid conflating evolution of a given trait, a priori predictions can be adaptation with ancestry. tested by comparing population-level responses to re- Finally, although our analyses suggest that the fruit gions with different dispersers. traits examined here are fortuitously compatible exapta- To determine the range of characteristics that influ- tions rather than the results of coevolution (see Janzen ence plant - frugivore interactions, future research 1980), the results offered here cannot refute the hy- should attempt to quantify the variety of fruit character- pothesis of coevolution between frugivores and their istics encountered by dispersers and the variety of dis- food plants. When genera are used as sampling units, persers typical for a given syndrome or character-com- only our analysis of Guiana has sufficient power to plex. Second, we should continue to extend our analy- reliably confirm the null hypothesis that color and pro- ses of fruit syndromes to include a wider range of fruit tection are not associated. For all other analyses effect traits, such as nutrient content, secondary compounds, sizes are very small, hence the power required to con- crop size, temporal and spatial dispersion, and spatial firm the null hypothesis can only be achieved with very display of fruits (e.g. Tomback 1983, Manzur and large (N > 1000) sample sizes. These very small effect Courtney 1984, Moermond et al. 1986, Herrera 1987, sizes indicate that the observed distributions differ little Levey 1988, Loiselle and Blake 1989). These traits from those posited by the null hypothesis in most cases. could be more important than color and protection in The effect size required to establish biological signif- determining frugivore food preferences (Willson et al. icance (i.e. to be worth detecting) is beyond the scope 1990). Third, future studies might consider including of conventional inferential statistics. Rather than rely- experiments that evaluate correlative field observa- ing on statistical methods to determine whether a test is tions. For example, our results suggest that blue and red sufficiently powerful to detect the observed effect size, unprotected fruits are generally more speciose than biologists should establish a priori hypotheses about the other character complexes. This corresponds with syn- magnitude of the effect expected on biological grounds dromes derived from observations of bird foraging be- and use these as criteria for the power required of a test. havior (e.g. Howe and Westley 1988); however, in color preference experiments three species of North Amer- Acknowledgements- We wouldlike to thankboth L. Chapman ican frugivorous birds showed no tendency to favour red and E. McKenziefor help in all stages of preparationof this The Herbariumand the Arnold Arboretum or black and only a weak to manuscript. Grey tendency reject yellow LibraryStaff providedinvaluable assistance in the et al. It would be to know collecting (Willson 1990). interesting if data. P. Ashton, S. Austad, L. Chapman,R. Cook, C. Her- birds are consuming blue and red fruits in proportion to rera, A. Gautier-Hion,D. Holmes, C. Janson, T. Laman,S. their abundance relative to other colors, and whether Lewis, C. Lindell,E. McKenzie,M. Pagel, J. Phelan,and Hal red and blue fruit colors are correlated with other char- Stern providedhelpful commentson this paper. Portionsof this researchwere a Jacob K. Javits acteristics that do influence fruit supportedby scholarship, choice in birds (Will- Sheldon Fellowshipand WennerGren PredoctoralGrant to son and Whelan 1990). Finally, we should continue K.F., and NationalGeographic and USAID grantsto C.A.C.

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