Effect of seed passage through vertebrate frugivores ...imedea.uib-csic.es/icg/ecol_terr/all pdfs/1998_Traveset_PPES_review… · Effect of seed passage through vertebrate frugivores’

Perspectives in Plant Ecology,Evolution and Systematics

Vol. 1/2, pp. 151–190© Gustav Fischer Verlag, 1998

Effect of seed passage through vertebratefrugivores’ guts on germination: a reviewAnna Traveset

Institut Mediterrani d’Estudis Avançats (CSIC-UIB), Ctra. de Valldemossa km 7’5, 07071-Palma de Mal-lorca, Spain; email: [email protected]

Abstract

The capacity of seeds to germinate after ingestion by frugivores is important for thepopulation dynamics of some plant species and significant for the evolution of plant-frugivore interactions. In this paper the effects of different vertebrates on seed germi-nation of nearly 200 plant species are reviewed, searching for patterns that predictthe circumstances in which germination of seeds is enhanced, inhibited, or unaffectedby the passage through the digestive tract of a seed disperser. It was found that seeddispersers commonly have an effect on the germinability of seeds, or on the rate ofgermination, or both, in about 50% of the plants they consume, although the diversityof animal species tested so far is still rather low (42 bird species, 28 non-flying mam-mals, 10–15 bats, 12 reptiles, 2 fishes). Enhancement of germination occurred abouttwice as often as inhibition.

In spite of the morphological and physiological differences in their digestive tracts,the different animal groups tested have similar effects on seed germination, althoughnon-flying mammals tend to influence germination slightly more often than the othergroups. Data on fishes are still too scarce for any generalization. Seed retention timein the dispersers’ digestive tract is one factor affecting germination, and helps to ex-plain the variation in seed responses observed among plant species, and even withina species. However other factors are also important; for example, the type of food in-gested along with the fruits may affect germination through its influence on chemicalor mechanical abrasion of the seed coat. Seed traits such as coat structure or thick-ness may themselves be responsible for some of the variation in seed retentiontimes. Seeds of different sizes, which usually have different transit times through fru-givores, and seeds of either fleshy or dry fruits, show often similar germination re-sponse to gut passage.

Seeds of different plants species differ strongly in their germination response afteringestion, even by the same frugivore species. Congeneric plants often show little con-sistency in their response. Even within a species variation is found which can be re-lated to factors such as the environmental conditions under which germination takesplace, seed morphology, seed age, and the season when the seeds are produced.

The effect of gut passage on germination differs between tropical and temperatezones. Seed germination of both shrubs and trees (data on herbaceous species arestill scarce) in the temperate zone is more frequently enhanced than in the tropics.This result supports the hypothesis that enhanced germination may be more advanta-geous in unpredictable or less constant environments. Significant differences in frugi-vore-mediated germination are also found among different life forms. In both tropicaland temperate zones, trees appear to be consistently more affected than shrubs orherbs. This might be due to an overall higher thickness of the seed coats, or to ahigher frequency of seed-coat dormancy in tree species.

The influence of frugivory upon the population dynamics of a species has to beevaluated relative to other factors that influence germination and seedling recruitment

Introduction

In recent decades, there have been manystudies of ecological and evolutionary as-pects of frugivory and seed dispersal by ani-mals, covering a range of latitudes and differ-ent habitats (e.g. Howe & Smallwood 1982;Janzen 1983; Estrada & Fleming 1986; Jor-dano 1992; Willson 1992; Fleming & Estrada1993). However, the germination capacity ofseeds after passing through the digestivetracts of an animal is one of those aspectsthat has received relatively little attention, al-though it is important to understand the evo-lution of plant-frugivore interactions. For ex-ample, the hypothesis that plants exert somekind of control over seed shadows producedby frugivores, by specific laxative and/or con-stipative chemicals in the fruit pulp which af-fect seed retention time in the dispersers’guts, has only recently been examined (Mur-ray et al. 1994; Cipollini & Levey 1997; Wahajet al., in press).

Germination enhancement, i.e. an in-creased rate of germination or a higher finalpercentage germination or both, has beenlooked upon as one of the principal advan-tages of seed ingestion by frugivorous ani-mals (Krefting & Roe 1949; van der Pijl1982). However, the available data are oftenequivocal, and the number of animal speciestested is small, especially in certain groupssuch as reptiles or fishes. In addition, there isoften great variation in seed responses withina genus or even within the same plantspecies. Whether germination enhancementrepresents an advantage to a plant, and thusmay be regarded as adaptive, probably de-pends on many factors, including the type ofhabitat where the seeds are deposited andthe time of germination. Unless an increasein plant fitness can be shown, it is difficult tosupport the claim that germination enhance-ment is advantageous.

Few generalizations have been made asto how frequently and under what circum-stances germination is influenced by fru-

152 A. Traveset

givory, or how consistently the same frugi-vore affects seeds of different plant species(but see Lieberman & Lieberman 1986). Thegoal of this article is to review studies of dif-ferent groups of frugivores (birds, mammals,reptiles and fishes) in the search for patternsthat allow to assess the ecological and evolu-tionary importance of this aspect of plant-fru-givore interactions. In particular, the followingquestions are addressed:1. Do animal seed dispersers usually en-

hance the germination of the seeds theyingest? Frugivores can enhance germina-tion in two ways: (a) by cleaning the seedsof pulp, which may contain germination in-hibitors or be a potential source of infec-tion by fungal or other pathogens, and/or(b) by having an abrasive effect on theseed coat, making it more rapidly perme-able to water and gases.

2. Do different taxonomic groups of frugi-vores (differing in the morphology andphysiology of their digestive tracts) affectseed germination differently? This couldarise because of factors such as differ-ences in the retention time of seeds in thegut, or from the presence of grit in gizzards(in some bird species, for example), whichmay have a mechanical and/or chemicaleffect on the seed coat.

3. Do seeds of different plant species re-spond similarly to ingestion by the samefrugivore species? We might expect thatthe germination of closely related species,belonging to the same genus for instance,would be similarly affected by the samespecies of vertebrate. If not, what factorshelp to explain the differences (e.g. seedcoat structure and thickness)?

4. Is there an interaction between seed sizeand the effect of a frugivore upon germina-tion? For example, if small seeds are re-tained for a longer period within the ani-mal’s digestive tract than large seeds, assuggested in a number of studies, we may

at a particular site. Whether seed ingestion by dispersers is really advantageous to aplant (as has commonly been assumed) can only be assessed if we also determinethe fate of the ingested seeds under natural conditions, and compare it to the fate ofseeds that have not been ingested.

Key words: frugivory, seed dispersal, seed ingestion, germination patterns

Effect of vertebrate frugivores on seed germination 153

hypothesize that germination enhance-ment tends to decrease as seed size in-creases.

5. Do seeds of fleshy fruits and dry fruits re-spond similarly to frugivores’ ingestion?

6. Are there any differences between seedresponses in the tropics and the temper-ate zones? If the effect of seed ingestionby frugivores on germination is adaptive inunpredictable or less constant environ-ments, as Izhaki & Safriel (1990) suggest,we might expect that seeds in the temper-ate zones would be affected more oftenthan seeds in the tropics.

7. Do seeds of plants with different life formsdiffer in their response to ingestion by fru-givores? If, for instance, trees have seed-coat dormancy more frequently thanshrubs and herbs, a germination enhance-ment after ingestion might be more com-mon in trees. Likewise, possible differ-ences in seed traits such as coat thick-ness, among different life forms might welltranslate into differences in the effect thatfrugivores have on seed germination.

8. Related to 7, do seed responses to frugi-vores’ ingestion vary between habitats(e.g. grasslands, shrublands and wood-lands)?

9. How important is seed ingestion by frugi-vores for plant recruitment relative to otherfactors?

About 80 papers dealing with the effect ofseed passage through vertebrate frugivoresare reviewed here. They cover 182 plant

species belonging to 68 families, and 94–99frugivore species belonging to 47 families(Table 1). A complete list of the plants and an-imals examined as well as a summary abouthow passage through the gut affects germi-nation is given in the Appendix. The few con-trolled experiments performed prior to 1949are mentioned in Krefting & Roe (1949) butare not included here as it was not possible toreexamine most of the data. These authorssuggest that those data are often misleadingdue to small sample sizes and inadequatecontrols, and are thus not strictly comparableto later work. For example, it is not alwaysclear whether ingested and control seedscame from the same plant population or thesame individuals. Some other studies that ex-amined the effect of seed passage throughfrugivores on germination have been re-viewed but are not included in the Appendix(Alexandre 1978; Yan 1993; Wrangham et al.1994), either because no information is avail-able concerning samples sizes or the statisti-cal tests performed, or because the authorsdo not say what kind of control was used inthe comparison with ingested seeds.

In most studies, only the total percentageof seeds that germinated after a given periodof time, often a few months, was measured.In less than half of the studies (see Table 1),both percentage of germination and germina-tion rate are given, i.e. the time elapsed untilthe first germination and/or the time elapseduntil 50% of the seeds have germinated. Insome studies, the term germination rate is er-roneously used as a synonym of the percent-

Table 1. Number of studies which showed enhancement, inhibition or a neutral effect on the two main char-acteristics of germination, i.e. percent germination and germination rate, after gut passage by differentgroups of vertebrate frugivores. For all plant species tested, ingested seeds have been compared with con-trols (uningested seeds). Based on data from the Appendix.

Frugivores Effect on No. studies Plant species Enhancement Inhibition Neutral(no. species/ germination (families) N (%) N (%) N (%)families)

Birds (42/19) percentage 153 80 (38) 55 (36) 25 (16) 73 (48)rate 103 42 (41) 15 (14) 46 (45)

Non-flying percentage 95 73 (40) 37 (39) 18 (19) 40 (42)mammals (28/18) rate 46 14 (30) 6 (13) 26 (57)

Bats (10–15/2) percentage 24 21 (16) 6 (25) 2 (8) 16 (67)rate 17 0 (0) 5 (29) 12 (71)

Reptiles (12/6) percentage 43 41 (23) 12 (28) 7 (16) 24 (56)rate 19 9 (47) 3 (16) 7 (37)

Fishes (2/2) percentage 2 2 (2) 2 (100) 0 0

age of germination. It is important to discrimi-nate between these two components of ger-mination performance, as they have quite dif-ferent ecological consequences. The differ-ences in germination rates between ingestedand control seeds are often a few days,sometimes several weeks, and rarely a fewmonths. Such differences are not examinedin this review since their implications arecompletely unknown for the species exam-ined.

The majority of germination experimentswere carried out in the laboratory, usually inPetri dishes under controlled conditions oflight, humidity and temperature; others wereperformed in glasshouses, and a very few in-vestigated seed germination in potting soilplaced in the natural habitat where the plantsare usually found. In most experiments,depulped seeds were used as a control, i.e.manually cleaned from pulp. Thus, moststudies did not test the effect that frugivoreshave in separating the pulp from the seeds,but rather the possible abrasive (scarifying)effect that ingestion by vertebrates has onseed coats (integuments). Intact fruits (freshfruits with seeds inside) were used as con-trols in only eleven studies, eight of whichtook manually depulped seeds as additionalcontrols.

The experimental data show that seed in-gestion by dispersers may either increase ordecrease the germinability of seeds. How-ever, the large majority of studies did not ex-amine the viability of the seeds that failed togerminate. Thus, it is unknown whether theremaining seeds could potentially germinate,or had died, or were already dead before theexperiment began. The age of seeds mustalso be considered in any germination exper-iment, as it determines the degree of ger-minability in many species, and especiallythose that only remain viable for a short pe-riod. In most studies freshly collected seedswere used.

How common is enhanced germination due to passagethrough disperser guts?

About half of the data come from experimentswith fruits consumed by birds, mostly passer-ines, and especially Turdus merula, T. migra-torius and Pycnonotus barbatus (cf. Appen-

154 A. Traveset

dix). The data suggest that birds have noconsistent effect on percent germination:studies in which there was no effect on germi-nation percentage are almost as frequent asthose in which a significant effect (either pos-itive or negative) occurred (Table 1). In 36%of cases germination was increased while itwas reduced in only 16% of cases. On theother hand, birds had a significant effect onthe rate of germination slightly more often (in55% of all studies, and disregarding whetheror not they had an effect on the final percentgermination), accelerating the germination ofingested seeds much more commonly(40.5%) than delaying it (14.5%).

Non-flying mammals influence seed ger-mination in 58% of all studies. Like birds, theyenhanced germination (increasing both per-cent and rate of germination) more than twiceas often as they inhibited it. However, in 57%of cases, the seed germination rate was notsignificantly affected by passage through thegut. Most data within this group of frugivorescome from experiments performed with eitherprimates or bears (see Appendix). Seed pas-sage through the guts of primates either in-creased percent germination or had no effecton it in a similar number of cases (38% and36%, respectively), and decreased it in 26%;they accelerated germination in 34% ofcases, delayed it in 14%, but in more thanhalf of cases (52%) had no effect on the rateof germination. The two species of frugivo-rous bears, in contrast, had no effect on thepercent seed germination of most plantspecies, increasing it in only 29% of casesand decreasing it in none. Similarly, a neutraleffect of seed passage through bears wasfound in all nine cases in which the rate ofgermination was examined.

The germination of most seed species in-gested by frugivorous bats of the two familiesPteropodidae and Phyllostomidae was not in-fluenced by gut passage (Table 1). Neitherthe percentage nor the rate of germinationwas affected in the majority of studies (67%and 71% of the cases, respectively). In aquarter of cases, the percent germinationwas increased, but there were no cases ofaccelerated gemination. In contrast, delays ingermination were observed in 29% of cases,but decreases in percent germination only in8%.

Fewer data have been published (in aboutten papers) on the effects of reptiles on ger-mination, turtles being more commonly


tested than lizards. The pattern that emergesfrom the 41 plant species is that percent ger-mination is mostly (56% of cases) unaffectedby seed ingestion by reptiles; when there wasan effect it was more usually positive (28%)than negative (16%). In contrast, reptilesseems to modify the rate of germination inmost cases (63%), accelerating it more often(47%) than delaying it (16%; Table 1). For theplant Neochamalaea pulverulenta (Cneo-raceae), whose fruit are consumed by thelacertid Gallotia galloti in the Canary Islands,seed germination was very low during thefirst year after planting, apparently due to in-hibition by the reptile (Valido & Nogales1994). Three years later, however, the totalpercentage of germination of treated andcontrol seeds did not differ significantly(Valido & Nogales, pers. comm.). This sug-gests that, at least for some plants, apparentdifferences in the final percentage germina-tion between control and ingested seeds de-pend on the duration of the germination ex-periment.

To my knowledge, the effect of fishes onseed germination has been tested with onlytwo aquatic plants, both of which showed anincrease in percent germination after inges-tion by a cichlid and a cyprinid (Agami &Waisel 1988). More data on this group of ver-tebrates are needed, both from temperatezones and the tropics. In some tropical re-gions, especially in the Amazon and in RíoNegro, large numbers of frugivore fisheshave been reported (Gottsberger 1978; Goul-ding et al. 1988).

Overall, seed dispersers appear to influ-ence both the percentage and the rate of ger-mination in a large fraction of plant speciesconsumed (c. 52% and 50% of the studies,respectively). From these results, it seemsthat non-flying mammals have an effect onseed germination more frequently than othertaxonomic groups, although the variability isquite high within each group of frugivores(see next section). Considering all disperserstogether, the percentage germination is in-creased more often (35%) than reduced(17%), and an acceleration of germinationafter seed ingestion is more common (35% ofthe cases) than a delay (16%). Germinationis either enhanced or inhibited in a wide vari-ety of plant species belonging to differentfamilies (see Appendix). The seeds of suchplants vary widely in size, shape and coatthickness. Therefore, by looking at seed traits

alone, it is not possible to predict whethergermination will be affected after ingestion bya particular frugivore or not. It is possible thatinhibition occurs in some species becausethe seeds are not completely mature when in-gested. For example, Figueiredo & Longatti(1997) found that howler monkeys (Alouattafusca ssp. fusca), which eat both mature andinmature fruits of Miconia cinnamomifolia, in-hibited germination, whereas marmosets(Callithrix penicillata), which feed only on ma-ture fruits, did not.

A significant part of the variation in germi-nation after ingestion appears to be related toplant species. This is consistent with the con-clusions of Lieberman & Lieberman (1986),who also found that the effects of individualanimal species are highly idiosyncratic andunpredictable from one plant species to thenext. Using a total of 52 plant–animal combi-nations, these authors found that the majorityof plants (73%) revealed no significant differ-ences between ingested and uningestedseeds, and concluded that “germination en-hancement (and concomitant dependenceupon ingestion) was neither inevitable noreven common”.

How consistently does thesame plant species respond toingestion by different frugivores?

For a given plant species, the outcome ofseed passage through a digestive tract maydepend on the animal species that consumesit. The way in which seeds are ‘treated’ in thefrugivore’s gut is actually one of the compo-nents of dispersal quality that determine theeffectiveness of a seed disperser (Schupp1993). A rather long retention time in the ver-tebrate guts, for instance, and thus a pro-longed exposure to digestive fluids, may re-sult in the removal of much of the protectivemesocarp and thus damage to the seed em-bryo, especially in seeds with soft seed coats(e.g. Gardener et al. 1993; Murphy et al.1993). Likewise, an excessive mechanicalgrinding in a bird’s gizzard may be detrimen-tal, increasing the possibility of embryo desic-cation and pathogenic attack. Since the di-gestive systems of frugivores such as mam-mals, birds and reptiles differ greatly, bothmorphologically and physiologically (e.g.

King 1996), it is scarcely surprising if thereare differences in their influence upon germi-nation.

Morphological and physiologicaltraits of frugivores that can affectseed treatment

Just as the teeth of herbivorous mammalsare modified in various ways, to crush, grindor shred plant matter, so also may the chemi-cal environment of the digestive tract be mod-ified to extract nutrients in an effective way,usually harbouring symbiotic bacteria andprotozoa which can digest the structural poly-mers of the cell wall through fermentation.Ruminant artiodactyls (e.g. cows, deer, pec-caries) have a refined stomach fermentationwhich takes place in the two compartments,rumen and reticulum, near the oesophagus(foregut fermentation). In contrast, hindgutfermentation (found in horses, rhinoceros,tapirs, for instance) takes place in the cae-cum, a much less complicated structure thatallows a faster digestion (King 1996). Gutpassage time for a ruminant such as a cow isusually 70–90 hours (Gardener et al. 1993),whereas food is processed in about 48 hoursby a horse (Sibly 1981). Seeds of Enterolo-bium cyclocarpum, however, can be retainedin horse guts for up to two months, and alarge fraction will them be digested (Janzen1982). Likewise, seeds of Trewia ingested byrhinoceros show peak passage times of64–88 h, but ranging widely from 46 h to 172 h (Dinerstein & Wemmer 1988). Frugivo-rous bats also exhibit special modifications totheir digestive tract: the oesophagous leadsinto a cardiac vestibule and the stomach is anelongated tube with a large, strongly-devel-oped caecum (Jordano 1992). Transit timesreported for bats are quite fast, ranging from22 to 144 min (Laska 1990).

Jordano (1992) reviewed specific modifi-cations of the digestive systems in frugivo-rous birds: (a) the crop and/or the proven-triculus may be extremely reduced, or evenabsent in some species; (b) the gizzard mayhave thin, non-muscular walls; (c) the simpli-fied gizzard is often in a lateral position, andthus the oesophagus is tightly connected withthe duodenum; and (d) the intestine is shortrelative to body size. In strongly frugivorousbirds, seeds are processed much morerapidly than pulp, presumably to maximizegut capacity for digestible pulp. Regurgitation

156 A. Traveset

of seeds by passerine birds is very rapid,often within 5–20 min, while defaecatedseeds are retained for much longer, usually0.3–1.5 h (Sorensen 1981, 1984; Herrera1984; Jordano 1992). Data for pigeons showgut passage times ranging from 55 to 140min (Clout & Tilley 1992).

In herbivorous reptiles, the small and largeintestines tend to be shorter and less coiledthan in mammals and birds (King 1996); as aresult, the rate of nutrient absorption is muchgreater in mammals and birds, which alsohave a much higher metabolic rate than rep-tiles. At the distal part of the large intestinethere is usually a caecum, a prominent struc-ture that can absorb nutrients and thathouses symbiotic micro-organisms which fer-ment cell wall polymers. For lizards, in partic-ular, the large intestine is much longer andthe small intestine much shorter in herbivo-rous species than in their carnivorous coun-terparts (King 1996). Herbivorous lizardshave long gut passage times (several days)compared to small herbivorous mammals(less than 10 h; Karasov et al. 1986), presum-ably because reptiles do not chew their food,and thus take more time to digest it. However,it is possible that some of them break up foodmechanically in the stomach, as suggestedby observations on Galápagos tortoises (Tes-tudo elephantopus ssp. porteri), which pro-duce faecal pellets containing sand, graveland small pieces of wood (Rick & Bowman1961), and on Sauromalus which ingestssand and gravel along with its food (Sylber1988). Seed retention time in Galápagos tortoises ranges from 12 to 20 days (Rick &Bowman 1961), although much shorterranges (24–48 h) are reported for turtles ofthe genus Rhinoclemmys (Moll & Jansen1995). Geckos of the genus Hoplodactylustake 36–72 hours to defaecate seeds, beingfaster when temperatures are higher and theanimals are more active (Whitaker 1987).

Studies performed with fishes show thatonly hard seeds pass through the intestinesintact and that these can be retained in the di-gestive tracts for up to 65 hours (Agami &Waisel 1988). The mandibles of commoncarps (Cyprinus carpio), a species used insome tests, usually crush the seed coats ofspecies such as Najas marina and Ruppiamaritima completely, digesting the seed con-tents. Apparently, many other fish speciesconsume some seeds but disperse and ex-crete the remainder (Agami & Waisel 1988).


Other factors that determine the timeof seed passage within a frugivore

Food retention time within a digestive tract isnot determined only by the intrinsic morpho-logical and physiological traits of the particu-lar animal. Factors such as nutritional levels(especially fat composition) of the diet, con-sistency, hardness, water content or amountof food are known to affect directly the speedat which a meal moves through the gut (e.g.Demment & van Soest 1985; Clench & Math-ias 1992; Gardener et al. 1993). Mean gutpassage time (GPT) can also vary dependingon the amount of food consumed; for exam-ple, it has been found to decrease with an in-creasing number of fruits ingested (Murphy etal. 1993). In frugivorous birds, GPT tends tobe short in order to increase the ingestionrate (Levey 1991), at the cost of a low diges-tive efficiency (Karasov & Levey 1990). TheGPT can also change through the feedingseason and even during the day, being shortin the early morning as energy reserves arereplenished, and in the late afternoon, pre-sumably so as to build up sufficient energy forthe night (Murphy et al. 1993).

Seed retention time within the same frugi-vore species can vary significantly depend-ing on the fruit ingested, with high individualvariability. Barnea et al. (1991) reportedgreat variation in GPT in birds for 12 plantspecies, with values ranging from 9 to 33 minfor bulbuls, and from 13 to 74 min for black-birds. The size and weight of a seed usuallydetermines the speed at which it passesthrough the digestive tract of a bird, largeand heavy seeds being defaecated morequickly than small and light seeds (Garber1986; Levey & Grajal 1991; Gardener et al.1993). Seed size may also determinewhether it will be defaecated or regurgitated,thus also affecting the time the seeds arekept in the digestive tract; this may translateinto different germination patterns (Clergeau1992; Izhaki et al. 1995). The texture of thefruit pulp is another trait that may influenceseed retention time, as reported by Levey(1986), who found that seeds of fruits with avery firm texture were retained longer thanthose of watery fruits.

The effect of seed retention time in verte-brate guts on germination success can alsodiffer among species of frugivores and plants.Barnea et al. (1991) found that blackbirds(Turdus merula), in general, show a stronger

enhancing effect on germination than bulbuls(Pycnonotus xanthopygos) because of thelonger retention time. Not all plants re-sponded equally, however; for example, verydifferent retention times (a few minutes to 24h) of Solanum luteum seeds in the two birdspecies had no effect on germination suc-cess (Barnea et al. 1992). In contrast, Mur-phy et al. (1993) found that spiny-cheekedhoneyeaters (Acanthagenys rufogularis) re-tained the seeds of grey mistletoe, Amyemaquandang, for much longer in their guts thanmistletoebirds (Dicaeum hirundinaceum; 40min vs. 13 min), which translated into lowerseedling establishment after ingestion byhoneyeaters. Apparently, the more gentletreatment in the guts of the specialized dis-perser was more beneficial to the seeds. Anegative effect of seed retention time on ger-mination success has also been reported forGalápagos tortoises (Rick & Bowman 1961),and for herbivorous mammals (Janzen et al.1985).

Levey & Grajal (1991) proposed that rapidseed processing, e.g. by many frugivorousbirds, has influenced the evolution of pulpcomposition and seed-packaging, with a se-lection for nutrients that are rapidly assimi-lated, e.g. simple sugars and free amino-acids. In large-seeded fruits, which are oftenrich in lipids, this may be different as seedsare processed more rapidly and indepen-dently of pulp (Levey & Grajal 1991). Murrayet al. (1994) have argued that the pulp ofsome fleshy fruits contains “laxative” chemi-cals that shorten seed retention time in theguts, thus reducing seed mortality. Theyfound that, although percentage germinationof Witheringia solanacea seeds was in-creased by passage through the gut of thebird Myadestes melanops, the germinationsuccess decreased with increasing timespent in the gut. While a mild abrasion proba-bly enhances water imbibition or the percep-tion of germination cues, a longer exposureto abrasion in the gut may be excessive andcause premature germination. However, Wit-mer (1996) has given an alternative explana-tion for the results of Murray et al. (1994),which concerns how nutrient concentration infood influences the digestive function of fru-givorous birds. He found that for at least threespecies of birds (Turdus migratorius, Hyloci-chla mustelina, Bombycilla cedrorum) seedpassage rates increased as sugar concentra-tion in their diet declined. This result is not

true for all species; for example, starlings(Sturnus vulgaris) showed similar gut reten-tion times regardless of the diet composition(insects vs fruits), whereas American robins(Turdus migratorius) showed a decrease inretention time when their diet was changedfrom insects to fruit (Levey & Karasov 1994).Recently, Cipollini & Levey (1997) have hy-pothesized that specific secondary metabo-lites found in the fruit pulp alter seed pas-sage rates, either slowing them down (i.e.having a “constipating” effect on animals) oraccelerating them (i.e. a “laxative” effects).Wahaj et al. (in press) show that glycoalka-loids in ripe fruits of Solanum can increase ordecrease retention time and thereby influ-ence seed deposition patterns (e.g. numberof defaecations with seeds, number of seedsper defaecation, and presumably also dis-persal distance). Future studies may shedmore light on this subject, and allow us to de-termine whether the fruit chemicals that ap-parently influence the seed passage rate incertain frugivores have an adaptive functionor not.

Patterns associated with differenttypes of frugivore

Of the 34 plant species that were tested withmore than one animal species of differentclasses or orders, 17 showed a consistent re-sponse to passage through the gut (Table 2).In 12 plant species the comparison was ei-ther between birds and bats or between birdsand non-flying mammals. In at least two plantspecies, even though response to ingestionwas consistent, one frugivore had a signifi-cantly stronger effect than the other. In Spon-dias purpurea seeds ingested by white-taileddeer (Odocoileus virginianus) germinated ina greater percentage than those ingested bythe iguana Ctenosaura pectinata (Mandujanoet al. 1994). Likewise, the germination ofseeds of Plocama pendula ingested either bya lacertid or by birds did not differ from thecontrol, yet a larger fraction of seeds ingestedby the lizard germinated compared to thoseconsumed by birds (Valido & Nogales, un-publ. data).

For the remaining plant species testedwith frugivores belonging to different orders,there were significant differences in seedgermination depending on the animal thathad ingested the seeds (Table 3). The most

158 A. Traveset

common comparisons were between birdsand either non-flying mammals (ten plantspecies), bats (six plant species), or reptiles(four plant species); some species weretested with more than two groups. Thelonger seed retention times in mammalscompared to those in birds might explain theenhancement of germination (either percent-age or rate of germination, or both) in only sixcases: Azaridachta indica, Carissa edulis,Cornus stolonifera, Prunus virginiana, Prem-na quadrifolia and Securinega virosa. Atleast three species (Byrsocarpus coccineus,Clausena anisata and Plocama pendula)seem to be negatively affected by the longerretention times within mammalian guts. Inthe case of P. pendula, rabbits have a nega-tive effect on germination compared to birds.However, seed retention time is unlikely tobe the reason, since lizards, although theyhave even longer retention times than rab-bits, have a neutral effect on germination.When both birds and bats were tested withthe same plant species, it was observed thatbats had no effect on germination in threecases (Carissa edulis, Ficus luschnathianaand Morus nigra), enhanced germination inAzadirachta indica and Ficus microcarpa,and inhibited it in Clausena anisata com-pared to birds (Table 3). Reptiles had eitherno effect on seed germination tested againstbirds (with Sambucus canadensis, Plocamapendula and Lycium intricatum), and againstmammals (with Diospyros consolatae and P.pendula), or inhibited germination (Morusalba and L. intricatum), while birds enhancedit (Table 3). Finally, in the three plant speciesin which non-flying mammals were com-pared with bats (Securinega virosa, Azadira-chta indica and Premna quadrifolia), the non-flying mammals enhanced germination whilebats had no effect.

Significant differences in seed responsescan also be observed in frugivores belongingto the same order, usually birds, since theseare the most commonly studied group (Table3). This suggests that seed retention timealone cannot explain the high variabilityfound in seed responses to avian ingestion.The differences in the effect of two primatespecies on Miconia cinnamomifolia can alsonot be attributed to differences in seed reten-tion time in their guts but, as already noted, tothe consumption of immature fruits by howlermonkeys but not by marmosets (Figueiredo &Longatti 1997).


Table 2. Plant species tested with vertebrate frugivores belonging to different orders which show a consis-tent seed germination response to ingestion: enhancement (+), inhibition (–), or neutral (0). The first sym-bol refers to total percent germination and the second one to germination rate.

Plant species Frugivores Effect on germination Reference––––––––––––––––––––––percent rate

Carissa edulis 1 sp. of bird 0 0 Lieberman & Lieberman (1986)1 sp. of bat 0 0

Clausena anisata 1 sp. of bird – – Lieberman & Lieberman (1986)1 sp. of bat – – Lieberman & Lieberman (1986)1 sp. of primate – – Lieberman & Lieberman (1986)

Ehretia cymosa 2 spp. of birds 0 0 Lieberman & Lieberman (1986)2 spp. of bats 0 0 Lieberman & Lieberman (1986)

Ficus carica 1 sp. of bird 0 .† Lisci & Pacini (1994)1 sp. of bat 0 0

Ficus microcarpa 1 sp. of bird + + Guerrero & Figueiredo (1997)Unid. spp. of bats + . Figueiredo et al. (1995)

Flacourtia flavescens 2 spp. of birds – – Lieberman & Lieberman (1986)1 sp. of primate – – Lieberman & Lieberman (1986)1 sp. of bat – – Lieberman & Lieberman (1986)

Najas marina 1 sp. of bird + + Agami & Waisel (1988)2 spp. of fish + . Agami & Waisel (1986)

Oplopanax horridus 2 spp. of birds 0 0 Traveset & Willson (1997)2 spp. of bears 0 0 Traveset & Willson (1997)

Premna quadrifolia 1 sp. of bat 0 0 Lieberman & Lieberman (1986)1 sp. of bird 0 0 Lieberman & Lieberman (1986)

Prunus serotina 1 sp. of bird + . Krefting & Roe (1949)Unid. spp. of birds + . Smith (1975)1 sp. of turtle + . Braun & Brooks (1987)

Ribes bracteosum 2 spp. of birds 0 0 Traveset & Willson (1997)2 spp. of bears 0 0 Traveset & Willson (1997)

Rubus procerus 1 sp. of bird 0 . Brunner et al. (1976)1 sp. of fox 0 . Brunner et al. (1976)

Rubus spectabilis 2 spp. of birds 0 + Traveset & Willson (1997)2 spp. of bears 0 + Traveset & Willson (1997)

Securinega virosa 3 spp. of birds 0 0 Lieberman & Lieberman (1986)2 spp. of bats 0 0 Lieberman & Lieberman (1986)

Spondias purpurea 1 sp. of deer + . Mandujano et al. (1994)1 sp. of iguana + . Mandujano et al. (1994)

Spreptopus amplexifolius 2 spp. of birds 0 0 Traveset & Willson (1997)2 spp. of bears 0 0 Traveset & Willson (1997)

Vaccinium alaskaense, 2 spp. of birds 0 0 Traveset & Willson (1997)V. ovalifolium 2 spp. of bears 0 0 Traveset & Willson (1997)

† No results.

160 A. Traveset

Table 3. Plant species tested with frugivore species belonging to the same or different orders whichshowed an inconsistent seed germination response to ingestion: enhancement (+), inhibition (–), or neutral(0). The first symbol refers to total percent germination and the second one to germination rate.


Azadirachta indica 2 spp. of birds 0 + Lieberman & Lieberman (1986)1 sp. of bird + + Lieberman & Lieberman (1986)1 sp. of primate + + Lieberman et al. (1979)1 sp. of primate + 0 Lieberman & Lieberman (1986)1 sp. of bat 0 0 Lieberman & Lieberman (1986)1 sp. of bat + – Lieberman & Lieberman (1986)

Byrsocarpus coccineus 3 spp. of birds 0 0 Lieberman & Lieberman (1986)1 sp. of primate – – Lieberman & Lieberman (1986)

Capparis erythrocarpos 1 sp. of bird 0 0 Lieberman & Lieberman (1986)2 spp. of birds 0 + Lieberman & Lieberman (1986)1 sp. of primate 0 + Lieberman & Lieberman (1986)

Carissa edulis 1 sp. of bird – – Lieberman & Lieberman (1986)1 sp. of bird 0 0 Lieberman & Lieberman (1986)1 sp. of bat 0 0 Lieberman & Lieberman (1986)

Clausena anisata 1 sp. of bird 0 – Lieberman & Lieberman (1986)1 sp. of bird – – Lieberman & Lieberman (1986)1 sp. of primate – – Lieberman & Lieberman (1986)1 sp. of bat – – Lieberman & Lieberman (1986)

Cornus racemosa 2 spp. of birds – .† Krefting & Roe (1949)Unid. spp. of birds + . Smith (1975)

Cornus stolonifera 2 spp. of birds – . Krefting & Roe (1949)1 sp. of bear + . Rogers & Applegate (1983)

Diospyros consolatae 1 sp. of primate + . Engel (1997)1 sp. of snake 0 . Engel (1997)

Ficus luschnathiana 1 sp. of bird + . Figueiredo & Perin (1995)1 sp. of bat 0 . Figueiredo & Perin (1995)

Ficus microcarpa Unid. spp. of birds 0 . Figueiredo et al. (1995)1 sp. of bird + + Guerrero & Figueiredo (1997)Unid. spp. of bats + . Figueiredo et al. (1995)

Juniperus virginiana 3 spp. of birds – . Livingston (1972)2 spp. of bird + . Holthuijzen & Sharik (1985)

Lonicera tatarica 1 sp. of bird + . Krefting & Roe (1949)1 sp. of bird 0 . Krefting & Roe (1949)

Lycium intricatum 1 sp. of bird + + Nogales et al. (1998)1 sp. of lizard 0 0 Valido & Nogales (1994)1 sp. of lizard – – Nogales et al. (1998)

Miconia cinnamomifolia 1 sp. of primate – . Figueiredo & Longatti (1997)1 sp. of primate 0 . Figueiredo & Longatti (1997)


Morus alba 1 sp. of bird + . Krefting & Roe (1949)1 sp. of turtle – . Braun & Brooks (1987)

Morus nigra 2 spp. of birds + + Barnea et al. (1991)1 sp. of bat 0 0 Izhaki et al. (1995)

Neochamaelea pulverulenta 1 sp. of lizard – + Valido & Nogales (1994)1 sp. of lizard + + Valido & Nogales (unpubl.)

Plocama pendula 2 spp. of birds 0 + Valido & Nogales (unpubl.)1 sp. of rabbit – – Nogales et al. (1995)1 sp. of lizard 0 0 Valido & Nogales (unpubl.)

Premna quadrifolia 1 sp. of bird 0 0 Lieberman & Lieberman (1986)1 sp. of primate 0 + Lieberman & Lieberman (1986)1 sp. of bat 0 0 Lieberman & Lieberman (1986)

Prunus virginiana 1 sp. of bird – . Krefting & Roe (1949)1 sp. of bear + . Rogers & Applegate (1983)

Rosa sp. 1 sp. of bird – . Krefting & Roe (1949)1 sp. of bird + . Krefting & Roe (1949)

Rubus sp. 1 sp. of bird 0 . Krefting & Roe (1949)2 spp. of birds + . Krefting & Roe (1949)

Rubia tenuifolia 5 spp. of birds 0 – Izhaki & Safriel (1990)2 spp. of birds‡ 0 + Barnea et al. (1991)

Smilax aspera 1 sp. of bird + 0 Izhaki & Safriel (1990)2 spp. of birds 0 0 Izhaki & Safriel (1990)

Solanum nigrum 2 spp. of birds 0 . Barnea et al. (1990)0 0 Mas & Traveset (unpubl.)

2 spp. of birds + + Clergeau (1992)

Rhamnus palaestinus 1 sp. of bird + + Izhaki & Safriel (1990)+ – Barnea et al. (1991)

1 sp. of bird + 0 Barnea et al. (1991)4 spp. of birds 0 0 Izhaki & Safriel (1990)

Sambucus canadensis 1 sp. of bird – . Krefting & Roe (1949)2 spp. of birds + . Krefting & Roe (1949)1 sp. of turtle 0 . Braun & Brooks (1987)

Sambucus racemosa 2 spp. of birds 0 . Traveset & Willson (1997)1 sp. of bear 0 0 Traveset & Willson (1997)

Securinega virosa 3 spp. of birds 0 0 Lieberman & Lieberman (1986)1 sp. of primate + + Lieberman & Lieberman (1986)2 spp. of bats 0 0 Lieberman & Lieberman (1986)

† No results.‡ One of these species is the same as used by Izhaki & Safriel (1990).

Table 3. (continued).


In short, the great variation observed inthe effect of seed ingestion on germination,even when comparing congeneric frugivores,suggests that differences in retention time (atleast within a limited range of hours or days)is not the only important factor. For mostspecies, an effect on germination is not asso-ciated, either positively or negatively, with thetime that seeds remain in the digestive tractof dispersers. Other factors, such as the typeof food ingested along with the fruits (withvariable acidity, water content, etc.), mayeven be more relevant in determining the ex-tent to which the seeds are mechanicallyand/or chemically abraded.

Responses of different seedspecies ingested by the samefrugivores

A particular animal species can have signifi-cantly different effects on seed germinationdepending on a variety of traits (seed size,coat thickness, sculpture, etc.) which are in-trinsic to the plants it consumes. Many stud-ies show that pulp (aril) removal may be suffi-cient to enhance germination, as germinationinhibitors present in these tissues are elimi-nated (e.g. Evenari 1949; Mayer & Poljakoff-Mayber 1975; McDiarmid et al. 1977; Izhaki &Safriel 1990; Barnea et al. 1991; Clergeau1992; Bustamante et al. 1993; Lisci & Pacini1994) and the possibility of microbial or fun-gal attack is reduced (Ng 1983; Jackson et al.1988). At least three studies confirm that, inaddition, some frugivores enhance germina-tion by abrading the seed coats (Izhaki &Safriel 1990; Barnea et al. 1991; Clergeau1992).

For other species, the ingestion implies achemical or mechanical abrasion of the seedcoat that may or may not enhance germina-tion, depending on the extent to which seedsare abraded. For a long time it has been as-sumed that the fruits of some plants, espe-cially those believed to have “coevolved” withtheir animal dispersers, obligatorily need tobe ingested by them for seeds to germinate(the case of the dodo and the tambalacoquetree from Mauritius Island is probably themost famous example; Temple 1977). Never-theless, evidence that contradicts this as-sumption is accumulating (e.g. Witmer &Cheke 1991). In some species, there is cor-

162 A. Traveset

relative evidence for a dramatic reduction inplant populations, associated with extinctionor decline of a specific disperser (e.g. Temple1977; Janzen & Martin 1982; Given 1995;Traveset 1995). However, little evidence ex-ists that such reduction has been due to therequirement for seed ingestion by a particularfrugivore. Probably the reduction in plantpopulation densities is more related to thelimited dispersal of seeds, with the conse-quence of higher seed/seedling mortality dueto predators and pathogens. Nonetheless,there are a few cases where ingestion seemsto be essential; for example, Rick & Bowman(1961) reported that the only natural way ofbreaking seed dormancy in the native Galá-pagos tomatoes (Lycopersicon esculentumvar. minor) was through ingestion by gianttortoises.

Different seed coat sculptures, which maybe found even in closely related speciessuch as Solanum luteum and S. nigrum(Barnea et al. 1990), or different seed coatthickness (Gardener et al. 1993) can some-times account for the different effects of a fru-givore on germination. Amongst congenericplant species, seed responses to ingestionshow a great variability (see Appendix). Thegenera Rubus, Ficus, Vaccinium, Solanumand Vitis have been most often studied (al-though data of at least three species alsoexist for Cornus, Juniperus, Prunus, Acaciaand Sambucus); none of them shows a con-sistent result response to ingestion, evenwhen the frugivores belong to the sameorder. The results for the ten species ofRubus tested so far show that seed germina-tion may be: (a) enhanced (in three speciestested with several frugivores includingbears and birds), (b) inhibited (in threespecies ingested by either rodents or birds),and (c) unaffected (in the other four speciesingested by foxes, turtles or birds). Within thegenus Ficus, the effect of seed passagethrough various vertebrates (primates, batsand birds) has been examined in ninespecies, the results being a consistent ger-mination enhancement in five of them, andvariable in four (F. carica, F. glabrata, F. insip-ida and F. microcarpa). Of the Vacciniumspecies studied, seeds were unaffected byfrugivore ingestion (by bears, turtles or birds)in three species, but germination was inhib-ited in two (ingested by either rodents orbirds) and enhanced in one (ingested bymartens). In the case of Solanum, seeds of


two of six species are enhanced by mam-mals, three are not affected by either birds ora mammal, and the sixth (S. nigrum) is eitherenhanced or not affected, depending on thespecies of bird used in the test. Finally, whiletwo species of Vitis are not affected by inges-tion by a species of turtle, the germination ofanother species is enhanced after passingthrough the same reptile, and a fourth (V. ri-paria) is either enhanced or inhibited de-pending on the bird consuming it.

Even the same plant species can responddifferently to the same frugivore, dependingon factors such as environmental conditions,plant population and/or seed age. Seeds ofSolanum luteum, for instance, were differ-ently influenced by avian ingestion in summerand in winter, suggesting that seeds with dif-ferent qualities of seed coats are produced bythe same plant throughout the year (Barneaet al. 1990); the seed coat might be thicker insummer than in winter in order to withstanddesiccation. Similar findings have been re-ported by Howe (1986) and by Agami &Waisel (1988). Lombardi & Motta (1995)show different results for Rhipsalis bacciferaseeds ingested by birds according to theplant population which produced the seeds.Salomonson (1978) found that six-month-oldseeds of Juniperus monosperma were unaf-fected by avian ingestion but the germinationof one-year-old seeds was inhibited by thesame bird species. These variable seed re-sponses may partly the contradictory resultsfound by different authors working on thesame plant and testing it with the samespecies of frugivore. Examples of such incon-sistencies include: (1) germination of Rubiaangustifolia was found to be either acceler-ated (Barnea et al. 1991) or delayed (Izhaki &Safriel 1990) after seeds were fed to black-birds; (2) the seeds of Solanum nigrum wereunaffected by blackbirds (Barnea et al. 1990;Mas & Traveset, unpubl. data), althoughClergeau (1992) reports that their germina-tion is enhanced by this species; and (3) thepercentage of germination of Aralia nudi-caulis seeds was either not affected (Krefting& Roe 1949) or enhanced (Rogers & Apple-gate 1983) by black bears. There are otherfactors, however, which might also explainthe equivocal results. Krefting & Roe (1949)found that, depending on the treatment ap-plied to break seed dormancy, the responseto seed ingestion by frugivores can vary sig-nificantly. Rogers & Applegate (1983) also

obtained different results in their experimentswhen they compared seeds placed in the re-frigerator with seeds not refrigerated prior tothe germination tests. The conditions underwhich such germination tests are performedmay also affect the results. Bustamante et al.(1992) found a significant effect of seed pas-sage through foxes on germination in the lab-oratory but not in the field, where germinationvaried depending on habitats. Similar resultswere found by Figueiredo et al. (1995) work-ing with Ficus microcarpa. Likewise, Figuei-redo & Perin (1995) found a significant effectof ingestion by bats on germination underlaboratory conditions but not in the field; theyattributed this to factors such as variation intemperature, chemical characteristics of thesoil, and soil-borne pathogens that kill theembryos. Other conditions, such as theamount of illumination per day or the degreeof humidity, might also be a source of varia-tion in seed responses.

The same plant species may also be af-fected differently by the same frugivore ifseeds are polymorphic. This has beenshown in at least two studies, where the ef-fect of frugivores on seed germination wasstudied comparing different fruit colourmorphs. In one species, Rhagodia paraboli-ca, seeds of the white morph show a greaterresponse to passage through silvereyes’(Zosterops lateralis) guts than the red or theyellow morph (Willson & O’Dowd 1989). Inanother species, Rubus spectabilis, seeds ofthe orange morph showed a slight shift ingermination patterns compared to the redmorph after passing through the digestivetract of birds (Traveset & Willson 1998), andalso through an invertebrate seed disperser,the banana slug Ariolimax columbianus(Gervais et al. 1998). Differences in re-sponses of the two type of seeds to ingestiondo not seem to be attributable to differencesin seed coats, as both morphs are equallythick and have a similar coat structure. In avariety of species, mainly Compositae,Chenopodiaceae and Gramineae, the germi-nation of seeds from the same parent plant iscorrelated with their position in the inflores-cence. These species usually produce twotypes of seeds, which differ in size, shapeand germinability. In Bidens pilosa, for in-stance, Forsyth & Brown (1982) found thatthe smaller ray seeds have a higher degreeof dormancy than the larger disk seeds pro-duced by the plant.

Does the effect of frugivores ongermination vary with seedsize and with the type of fruit?As mentioned above, the size of a seed maydetermine the time it remains in an animal’sdigestive tract (Levey & Grajal 1991; Izhaki etal. 1995) and, ultimately, the degree to whichits coat is mechanically and/or chemicallyabraded. In order to test the hypothesis thatthe germination of large seeds is less af-fected by ingestion than that of small seeds,the species in the compiled data set weresorted into three groups (small seeds: thosein which the largest dimension (l.d.) was < 5 mm; medium seeds: l.d. 5–10 mm; andlarge seeds: l.d. > 10 mm) and examined fordifferences in germination. Even though sam-ple sizes for the medium and large categoriesare much lower than for the small one (Table4), results showed no significant associationbetween seed size and either effect on germi-nation percentage (chi-square test of inde-pendence; χ2 = 4.8, P > 0.05) or on the rate of

164 A. Traveset

germination (χ2 = 3.0, P > 0.05). This result isin accordance with the finding that seed re-tention time in the digestive tract often has noeffect on germination; smaller seeds whichtend to be longer in the digestive tract are notnecessarily more often affected than largeones. Seed size, however, as well as seed re-tention time in the frugivore guts, are impor-tant for some species in determining theirgermination success.

If the texture of the fruit pulp influencesseed retention time, as reported by Levey(1986), we might find some differences inseed responses to ingestion between fleshyand dry fruits. To test this, the data set was di-vided into fleshy and dry fruits and the effectsof frugivores on seed germination examined.Fleshy fruits have been tested much moreoften than dry ones (by a factor of ten), but nosignificant differences were found betweenthe two categories (Table 5), either in the fru-givore’s effect on percentage of germination(χ2 = 3.7, P > 0.05), or on germination rate(χ2 = 1.2, P > 0.05). Although dry fruits have

Table 4. Number and percentage (in brackets) of study cases (not species, as some are tested in severalstudies) for three seed size categories where germination was enhanced, inhibited or not affected by pas-sage through frugivore‘s guts. Both components of germination performance (percentage and rate germi-nation) are given. Only species for which seed size was known (see Appendix) were included.

Seed size Enhancement Inhibition Neutral effect–––––––––––––––––––––– –––––––––––––––––––––– ––––––––––––––––––––––––percent rate percent rate percent rate

Small 72 45 37 16 100 58(<5 mm) 34) (38) (18) (13) (48) (49)

Medium 17 6 6 5 20 11(5–10 mm) (40) (27) (14) (23) (46) (50)

Large 14 8 1 1 16 9(>10 mm) (45) (44) (3) (6) (52) (50)

Table 5. Number and proportion (in brackets) of study cases for each fruit type category that are en-hanced, inhibited or not affected by passage through frugivore‘s guts. Both components of germinationperformance (percentage of germination and germination rate) are given.

Fruit type Enhancement Inhibition Neutral effect–––––––––––––––––––––– –––––––––––––––––––––– ––––––––––––––––––––––––percent rate percent rate percent rate

Dry fruits 15 5 4 4 10 7(52) (31) (14) (25) (34) (44)

Fleshy fruits 99 60 48 25 145 84(34) (35) (16) (15) (50) (50)


been tested most frequently with non-flyingmammals and fleshy fruits with birds, the ef-fect of each of these groups of frugivores onseed germination is found to be similar forboth type of fruits.

Influences of region, life formand habitat on the effect of frugivores on seed germination

The effect that ingestion by frugivores hasboth on the percentage germination and onthe speed of germination differs significantlybetween tropical and temperate zones (χ2 =7.1 and χ2 = 6.2, P < 0.05, respectively), ger-mination enhancement being more frequentlyin the temperate zone (Fig. 1). To determine ifsuch differences can be attributed to the un-equal representation of life forms of thespecies studied (mostly trees in the tropicsand mostly shrubs in the temperate zone), Itested the possibility that different plant lifeforms vary in their seed responses to pas-sage through frugivores. The species in thedata set were divided into three categories:herbs, shrubs, and trees. The percentage ofgermination of ingested seeds appeared tobe more frequently increased in tree speciesthan in either herbs or shrubs (χ2 = 22.0, P <0.01); the effect on germination rate, in con-trast, did not differ among life forms (χ2 = 7.3,P > 0.05). The germination of most herbs andshrubs was not significantly affected afterpassing through an animal’s digestive tract,although shrubs were more frequently inhib-ited than either herbs or trees. Such differ-ences among life forms were consistent inthe two regions (Fig. 1): both percentage andspeed of germination were enhanced morefrequently in trees than in the other life formsin the temperate zones (χ2 = 24.2 and χ2 =16.0, P < 0.01, respectively) and in the trop-ics (χ2 = 10.6 and χ2 = 19.0, P < 0.01, respec-tively). Therefore, the greater frequency ofgermination enhancement after gut passagein the temperate zone compared to the trop-ics is not due to the different frequency ofplant life forms tested in the two zones. Thedifferent distribution of seed sizes (seeabove) between tropical and temperatezones (a greater proportion of large seeds inthe tropics) is also not responsible for the dif-ference, as all seed sizes were found to re-

spond similarly to ingestion by frugivores inboth regions.

In order to know if the differences betweentropics and temperate zones were consistentamong life forms, the analyses were per-formed for each of the three categories.While no differences in the effect on seedgermination performance were observed be-tween tropical and temperate herbs (χ2 = 0.74

Fig. 1. Proportion of studies for each life form andregion that showed enhancement, inhibition or aneutral effect on (a) percent and (b) rate of germi-nation after seeds have passed through frugivoreguts.

Eff

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and χ2 = 1.3, P > 0.05, for percentage andrate of germination, respectively), shrubs andtrees were more frequently affected in thetemperate zones. Seed germination of tem-perate shrubs was accelerated much moreoften than that of tropical shrubs (χ2 = 9.8, P <0.01), although the majority of shrubs in bothregions were unaffected by passage through

166 A. Traveset

frugivores, and the final percentage of germi-nation is also similar (χ2 = 3.1, P > 0.05). Tem-perate trees, on the other hand, showed amore frequent enhancement in both com-ponents of seed germination performance (χ2 = 17.1 and χ2 = 7.1, P < 0.01, respectively)than tropical trees; moreover, while in thetropics most tree seeds are unaffected in ei-ther their germination potential or rate, in thetemperate zones the opposite occurs (Fig. 1).

These results, therefore, support two ofthe hypotheses presented in the Introduction:(1) that an effect of seed passage through thedispersers’ guts might be more adaptive inless constant environments, such as thoseusually found in temperate regions, and (2)that trees are more likely to be affected thanother life forms (perhaps due to a larger fre-quency of species with seed-coat dormancy).The effect of seed ingestion by frugivores ongermination appears also to be influenced bythe habitat where the plant species is mostcommon (Fig. 2). A germination enhance-ment of seeds passed through vertebrate fru-givores occurs more commonly in grasslandsthan in the other two habitats (χ2 = 10.0 andχ2 = 11.6, P < 0.05, for percentage and rate ofgermination, respectively; Fig. 2). In bothshrublands and woodlands, most of thespecies show a neutral effect of seed inges-tion, although a much larger fraction ofspecies of shrublands are inhibited comparedto species of woodlands. In analyses for eachregion separately, significant differences areonly found when the percentage of seed ger-mination is compared and only in the temper-ate zone (χ2 = 11.1, P < 0.05; Fig. 2). The pos-sibility exists, however, that the “grassland”results are biased due to the much smallersample size of species tested compared tothose of the other two habitats. The reasonfor the greater proportion of shrublandspecies that show an inhibition effect in theirgermination when ingested compared towoodland species, especially in the temper-ate zone, is unknown.

Other ways in which frugivoresinfluence establishment success

Besides having the potential to affect per-centage and rate of germination of the seedsthey ingest, vertebrate frugivores can deter-mine germination success and seedling es-

Fig. 2. Proportion of studies for each type of habitatand region that showed enhancement, inhibition ora neutral effect on (a) percent and (b) rate of germi-nation after seeds have passed through frugivoreguts.

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tablishment in various other ways. These in-clude: (1) the site and microsite where theyregurgitate or defaecate seeds; (2) the timewhen seed ingestion and dispersal takesplace, (3) how clean of pulp (or aril) theyleave the seeds; (4) the amount of seeds de-faecated in a dropping, (5) the diversity ofseed species found in a defaecation; (6) thefrugivore’s selection for particular fruit traitswithin a species (fruit size – which may becorrelated with seed size in certain speciesand, thus, with germination – level of seed in-festation by insects); and (7) the plant nutri-ent content of the frugivore’s faeces, whichmay be important, especially for seedling es-tablishment and growth.

(1) The environmental conditions of themicrohabitat where seeds are “released” maybe crucial for successful establishment. Nu-merous studies have shown the effects ofdistance from the parent plant, the type ofhabitat where the seeds are deposited, theprobability of seed predation by animals, orseedling survival to herbivores or pathogens.Likewise, many studies have demonstratedthe effects of competition for nutrients in siteswhere seedlings are found in great densities.Hence, a frugivore may enhance the germi-nation of seeds by passing them through itsdigestive tract but this enhancement may beinsignificant if the animal is inefficient as aseed disperser and regurgitates or defae-cates most seeds at high densities under theparent plant, or in places (e.g. within caves, inintertidal zones, on rocky outcrops) where thenecessary conditions (light, temperature, hu-midity, nutrient availability) for germinationand/or growth of that plant are not found (e.g.Bustamante et al. 1992). By defaecatingseeds free of pulp, frugivores may enhancegermination, but simultaneously may in-crease seed predation by rodents, as foundby Bustamante et al. (1993). Chemical traitsof the soil where seeds are deposited arealso known to affect seed germination, modi-fying osmotic pressure (e.g. Evenari 1949;Mayer & Poljakoff-Mayber 1975; Debussche1985) and even affecting metabolic pro-cesses secondarily related to flower and fruitpigments (Chenery 1948; Horowitz 1976). Ina recent study on Rubus spectabilis, someunknown (physical or chemical) soil traitswere shown to affect the germination be-haviour of the two seed morphs of thisspecies (Traveset & Willson 1998). More-over, soil-borne pathogens can kill the em-

bryo (e.g. Titus et al. 1990). More informationis needed to find out which soil componentsand pathogens affect seed germination ingeneral. In future studies on the effect on ger-mination of seed passage through verte-brates, it is important to realize that the re-sults of the experiments may vary signifi-cantly, depending on the type of soil in whichthe seeds are planted. Also, as already men-tioned, the outcome of tests performed inPetri dishes is not always the same as that oftests performed by planting the seeds in‘more natural’ conditions.

(2) The time in the season when a fruit isconsumed and dispersed may be crucial forgermination and seedling establishment. Thismay be especially important for plant specieswith long fruiting periods that can encompassa whole season. A seed that is dispersedearly in the season may have a higher orlower probability of establishment than a laterdispersed seed depending on the environ-mental conditions, both physical (water avail-ability, temperature, etc.) and biological (seedpredators, pathogens, etc.) prevalent at themoment of dispersal. Seed predation, for in-stance, can either be smaller (Schupp 1988)or greater (Traveset 1990) for early dispersedseeds than for seeds dispersed late in theseason. Earlier seedlings may also out-compete the next emerging ones (Loiselle1990).

(3) The pulp that remains around theseeds once these leave the digestive tract ofthe frugivore may still contain germination in-hibitors. Seeds that are regurgitated, espe-cially by birds, are usually completely clean-ed; in contrast, it is not unusual to find moreor less pulp still attached to seeds which havebeen defaecated, and in some cases, most oreven all apparently intact pulp is expelledwith the seeds (e.g. in the dung of bears,fruits of blueberries, Vaccinium, may survivealmost entire and with all seeds inside; pers.obs.). Therefore, if defaecated seeds are stillpartially or totally surrounded by pulp, andsuch pulp still contains active germination in-hibitors after passing through the vertebrate’sguts, the possible enhancing effect of the fru-givore on germination may be masked. Evenif the defaecated pulp does not contain anygermination inhibitor, it can become infestedwith fungi or bacteria which may prevent ger-mination (Witmer & Cheke 1991; Crossland &Vander Kloet 1996). This should be taken intoaccount when designing the seed germina-

tion experiments in future studies, especiallyif plant species are investigated whose seedsare not completely depulped during inges-tion; in these cases, the suitable controlsmight be seeds extracted from uningestedfruits but with some pulp still attached tothem, and not the absolutely clean, usuallyrinsed, seeds often used.

(4) The number of seeds defaecated in adropping is also relevant to the future estab-lishment success of a plant. Barnea et al.(1992) reported that the number of seeds in adefaecation is inversely correlated with ger-mination success, suggesting that the mech-anism might operate at the seed level (e.g.autotoxicity). They found that for multi-seeded fruits, birds reduce the number ofseeds per group and that this enhances ger-mination. However, this was only found inPetri dishes and needs to be confirmed innatural conditions. The presence of a largequantity of seeds in a dropping can also influ-ence both post-dispersal seed predation (e.g.Janzen 1982, 1986; Schupp 1988; Traveset1990; Willson & Whelan 1990; Hulme 1994;Bermejo et al. 1998) and intra- and inter-specific competition for resources amongseedlings (e.g. Loiselle 1990). The impor-tance of seed predation can vary (Hulme1998) depending on factors such as the habi-tat in which the droppings have been left(within the forest, in a gap, below plants or faraway from them, etc.), the time when seedshave been dropped, the predator species (ro-dents, insects, birds), seed density, and eventhe amount of dung; these findings seem tobe true for all vertebrate seed disperserspecies. Seedling competition, in contrast, ispresumably much more important in drop-pings left by big mammals, such as bears,cattle, elephants and primates, than in scatsof reptiles, bats or birds. In droppings of bigmammals, we can easily find several thou-sand seeds (especially small seeds such asthose of Vaccinium) whereas in scats, thenumber of seeds rarely reaches several hun-dreds and low densities are usual. Indeed,the laxative chemicals (Murray et al. 1994) orsecondary metabolites (Cipollini & Levey1997) present in the pulp of some fruits mightserve not only to decrease seed retentiontime in the guts of dispersers but also tocause frugivores to defaecate more often sothat lower numbers of seeds are expelled together, thus decreasing seedling competi-tion.

168 A. Traveset

(5) As pointed out above, animal seeddispersers may affect plant fitness by de-positing seeds in different densities, but theycan also affect it by defaecating seeds in dif-ferent species combinations. This was de-monstrated by Loiselle (1990), who showedthat seed composition in bird droppings de-termined the survival of certain species.Using different seed combinations in pairwisegrowth experiments, she found that someplant species were competitively superior toothers. At least in the case of frugivorousbirds, most species consume a variety offruits in a short period of time with the resultthat seed mixtures are commonly observed inbird droppings, both in the tropics and in thetemperate zones. The composition of seedsin droppings, however, varies among frugi-vore groups, for instance between birds thatswallow whole fruits and birds that mandibu-late them (Loiselle 1990, and referencestherein). The composition can also vary dur-ing the season, being more diverse whenbirds are more dependent on fruit (White &Stiles 1990). Certain species combinations indroppings are more common than others, asfrugivores do not choose fruits randomly, andthis has direct consequences for plant estab-lishment. If a plant species is always outcom-peted by others in the droppings, we mightexpect that birds that swallow entire fruits areattracted, as they probably deposit seeds inmonocultures (Loiselle 1990). More experi-mental data on intra- and interspecificseedling competition in droppings of birds aswell as of mammals and reptiles are required.The fate of seeds and seedlings in such de-faecations may actually be crucial for off-spring survival, and for the composition ofplant communities (Loiselle 1990, and refer-ences therein).

(6) Frugivores are known to select theirfood on the basis of different traits such assize, shape, colour, accessibility, nutrientcomposition, presence of insect larvae insidethe fruits, etc. Such fruit selection is anotherfactor that can influence seed germinationpatterns. By choosing large fruits (eitherwithin a species or among species), for ex-ample, a frugivore may ingest larger seeds,which in turn may be competitively superior tosmaller seeds (possibly because the largerseed may be more viable or have higher ger-mination rates, e.g. Banovetz & Scheiner1994). Similarly, a frugivore’s preferencesconcerning nutritional (e.g. for simple sugars;


Martínez del Río et al. 1989) and water con-tent in the pulp could also influence seed pas-sage rates, and ultimately determine whetherseeds are abraded or not and thus whethergermination is enhanced, inhibited or unaf-fected. The presence of insect larvae withinfruits may either foster or inhibit selection ofinfested fruits (Traveset et al. 1995, and ref-erences therein) with consequences for seedgermination success. A frugivore thatchooses berries containing attacked seeds,even if not all of them are killed, is obviouslydispersing some inviable seeds; thus germi-nation success will be lower than with an-other frugivore that rejects the infested fruitsand defaecates a larger proportion of viableseeds. Seeds attacked by insects, even if thelarvae have not killed the embryo, presum-ably are less likely to survive the passagethrough a vertebrate gut. However, seeds ofAcacia infested, but not killed, by bruchidbeetles actually showed enhanced germina-tion after passing through the gut of abrowser where the insect larvae died (Halevy1974; Lamprey et al. 1974; Coe & Coe 1987).More data from other species will allow us todetermine how frequently this occurs.

(7) Depending on the other materials in-gested with the fruits, the composition of thefaeces will change, and so will the potentialeffect on seedling establishment. Many frugi-vores consume a mixed diet, which results ina variable composition of their excrement.This is evident in birds, which excrete rela-tively high amounts of white urates when eat-ing invertebrates, and watery material oftencolored with fruit pigments when eating fruits.In carnivorous mammals that seasonally con-sume high volumes of fruits (Herrera 1989;Willson 1993), such variation in compositionis even more evident, and a single defaeca-tion may contain bones, feathers, leaves,stems, roots and seeds. Little experimentaldata exist on the effect of such dung compo-sition on seed germination and seedlinggrowth, though a few studies show that sucheffect is significant for some species (Archer& Pyke 1991; Jones et al. 1991; Quinn et al.1994; Malo & Suárez 1995; Traveset et al.,unpubl.) but not for others (Izhaki & Ne’eman1997). The type of substrate in which seedsgerminate has also been shown to influencethe effect of seed passage through frugi-vores’ guts on germination. Quinn et al.(1994) found that cattle increased both per-centage and rate of seed germination, but

that this effect was obscured by the temporalinhibition produced by the substrate in whichseeds were planted, consisting of soil anddung. Fresh dung often kills or suppressesvegetation, but once this dung has partiallydecomposed, it represents a more favorablemicrohabitat, as it has a greater capacity ofhumidity and nutrients. Seedlings grow betterin such microhabitats, even though germina-tion has been temporally inhibited.

Are differences in seed germination rates adaptive?

In environments with unpredictable climaticconditions, selection is expected to favourthose species that show asynchronous ger-mination, as the risk of seedling mortality isspread over a longer time (Harper 1977).Variation in temporal patterns of germinationof uningested seeds can often be foundamong individuals and among populationswithin a species (e.g. Lieberman et al. 1979;Zimmerman & Weis 1984; Miller et al. 1994).According to Izhaki & Safriel (1990) andIzhaki et al. (1995), when fruits are consumedby a variety of seed dispersers, such varia-tion in germination patterns may becomeeven more pronounced. These authors inter-pret asynchronous germination as an adapta-tion of the species they study to easternMediterranean habitats where rainfall pat-terns are rather unpredictable. Such an ex-planation, however, is not valid for other envi-ronments where climatic conditions are morepredictable, such as rainforests of temperatezones (Traveset & Willson 1997).

A variety of frugivore species modify thelength of seed dormancy, but not necessarilyincreasing the final germination percentage.That an early germination and establishmentmay represent an advantage for a particularspecies has been shown in a number of stud-ies (e.g. Ross & Harper 1972; Halevy 1974;Weaver & Cavers 1979; Cook 1980; Gar-wood 1983, 1986; Zimmerman & Weis 1984;Waller 1985). A difference in germination timeof only a few days may lead to differences inseedling fates (growth rate, probability ofdeath), later seedlings being at a disadvan-tage (Symonides 1977). According to Cook(1980), differences in mortality risks in Violablanda may even persist for several years.Selection, however, does not always favour

prompt high germination (Janzen 1981) and,in fact, the probability of predation, orpathogen attack, might be greater for earlythan for late seedlings (Traveset 1990), de-pending on the time of season, etc. Also, forexample, a large number of species (e.g.many shrubs and trees in the Northern Hemi-sphere; Burrows 1994) have developedmechanisms for delaying seed germinationover winter. If passage of these seedsthrough frugivores breaks this inherent dor-mancy, seeds will germinate under un-favourable conditions. We would thus expectthat selection acts on these species to pre-clude any enhancement effect on germina-tion rate after seeds are ingested by dis-persers. Probably seed passage through afrugivore’s guts only breaks seed-coat dor-mancy (so-called functional dormancy), andnot the physiological (internal or embryologi-cal) dormancy. If this proves true, differencesin germination time between ingested anduningested seeds will only be a matter ofdays or weeks (this was found in mostspecies studied so far). Whether dispersersbenefit the plant by advancing seed germina-tion time, even by a few days, will depend ulti-mately on each species and on the quality ofthe conditions for establishment provided bythe prevailing environment.

Further research on germination patternsof uningested (fresh) seeds compared withthose of seeds ingested by their natural dis-persers is required for more species of thesame community, to improve our knowledgeabout establishment success in the field. Wealso need more information on the type ofseed dormancy of the plant species tested,on how often and in what cases frugivorescan break inherent seed dormancy, andabout the consequences for fate of seedsand seedlings.

Concluding remarks

In addition to moving seeds from the parentplant to sites that can be suitable for recruit-ment and seedling growth, frugivore seeddispersers have the capacity to modify thegermination patterns of many plants by vary-ing the potential germinability of seeds, therate of germination, or both. They can en-hance germination by abrading the seedcoats, which become more rapidly permeableto gases and water, or just by removing the

170 A. Traveset

pulp (or other structures that may containgermination inhibitors) in their digestivetracts. Frugivores can also inhibit seed germi-nation by reducing the number of seeds thatare able to germinate, probably by excessiveabrasion, or by delaying their time of germi-nation (the mechanism for this is unknown).Presumably, this inhibitory effect must occuronly rarely if the frugivore is to be an effectivedisperser of the plant, and if the plant-animalinteraction has evolved over a long time. Onthe other hand, seed passage through frugi-vores’ guts can have no effect on germina-tion; in such cases frugivores only act as dis-seminators of the seeds.

If the plants and frugivores tested so farare representative of what happens in nature,it can be concluded that overall they signifi-cantly influence the germination patterns ofnearly half the species they consume, en-hancing germination – increasing either thegerminability of seeds or the speed of germi-nation – twice as often as they inhibit it. Thedifferent groups of frugivores tested, regard-less of the morphological and physiologicaldifferences in their digestive tracts, have sim-ilar effects, although non-flying mammalstend to influence germination patterns of theseeds slightly more often than other groups.The effect of a particular frugivore species islargely unpredictable, varying from one plantto the next and presumably depending onseed traits, intrinsic to the plant species.These traits may determine the extent ofseed coat abrasion in the digestive tract. Inturn, only about half of the plant speciestested, belonging to many different families,show a consistent response to seed passagethrough the guts of different frugivores. Con-generic plants also show little consistency intheir seed responses to ingestion. Even thesame plant species can be found to responddifferently to the same frugivore, dependingon factors such as environmental conditionsunder which germination takes place, theplant population, the individual plant, theseed morph, seed age, or even time of theseason when seeds are produced.

Seed retention time in frugivore guts is asignificant factor influencing the degree ofabrasion in some species, but is certainly notthe only one. Despite the possible advantagethat a long retention time may have in termsof seed dispersal, the time seeds remainwithin the digestive tract of dispersers is notassociated for most species with a particular


effect on germination; indeed, factors like thetype of food ingested may actually be moreimportant. Seeds of different sizes, whichusually have different transit times throughfrugivores, and seeds of either fleshy or dryfruits show similar responses to gut passage.Seed coat thickness might perhaps be amore important factor determining whethergermination patterns will be affected by seedingestion; presumably seeds with a thick coatmight be less abraded than seeds with a thinone, although this also depends on the timespent within the anaerobic conditions of thedigestive tract. Species having seed-coatdormancy might also be more affected thanthose which do not. So far, however, we donot have the necessary information to testsuch possibilities.

The hypothesis that an effect of seed pas-sage through the dispersers’ guts might bemore adaptive in unpredictable or less con-stant environments, such as those in temper-ate regions, appears to be confirmed. Exceptfor herbaceous species, for which little dataexist yet, seed germination of both shrubs andtrees in the temperate zones is more fre-quentlly enhanced after passage through frugi-vores than in the tropics. This finding is consis-tent with the idea that germination enhance-ment is especially advantageous in habitatslike those found in the eastern Mediterranean,where the risk of seed mortality needs to bespread with time, as climatic conditions, mainlyrain, are rather unpredictable (Izhaki & Safriel1990; Barnea et al. 1991; Izhaki et al. 1995).Likewise, trees are found to be more often af-fected than shrubs or herbs. This may reflect agenerally greater coat thickness in tree seeds,or a higher frequency of seed-coat dormancyin tree species. Future studies may help to elu-cidate these assumptions.

Whether germination enhancement in aparticular species, regardless of life form,habitat or region, translates into an advan-tage for the plant can only be determined bystudying the fate of ingested seeds and com-pare it with that of uningested ones. Thatsuch enhancement increases plant fitnessdepends on many factors: for example, onthe particular plant species and on whether itforms a seed bank, and on the environmentalconditions (temperature, rain, nutrient avail-ability, intra- and interspecific competition,herbivory, pathogen attack, etc.) prevalent inthe population or in the community at the timeof seed emergence.

Finally, the importance of this aspect ofplant-frugivore interactions, namely the roleof seed dispersers as “modifiers” of germina-tion patterns, can only be assessed whenevaluated together with other factors (e.g.site where seeds are deposited, time whenthey are dispersed, quantity and diversity ofseeds in a defaecation, frugivores’ selectionfor particular fruit traits, quality of nutrientconditions where seeds are found) that alsocan influence germination and establishmentsuccess.

Acknowledgements

I would like to express my gratitude to several peo-ple that have helped me in different ways duringthe elaboration of this review: Doug Levey, RodolfoAntônio de Figueiredo and Ido Izhaki for sendingme some of their papers; Alfredo Valido andManolo Nogales, for sharing their unpublished re-sults; the librarian, Marta Macías, for being so effi-cient in supplying some references; Tonyo Alcoverand Joan Rita, for telling me the family names, notgiven in a large number of papers, of some animaland plant species listed in the Appendix; Peter Ed-wards, Carlos Herrera, Ido Izhaki, Johannes Koll-mann, Mary Willson, and two anonymous review-ers for their valuable comments on earlier versionsof the manuscript; and Rol for his patience and en-couragement.

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Received 29 November 1997Revised version accepted 16 June 1998

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idae

++

Cob

o &

And

reu

(198

8)D

SH

STe

mp

CE

CR

OP

IAC

EA

EC

ecro

pia

sp.

Rhi

nocl

emm

ys fu

nere

aE

myd

idae

0M

oll &

Jan

sen

(199

5)F

ST

WTr

op

CN

EO

RA

CE

AE

Neo

cham

aele

a pu

lver

ulen

taG

allo

tia g

allo

tiLa

cert

idae

– +

Val

ido

& N

ogal

es (

1994

)F

MS

STe

mp

Neo

cham

aele

a pu

lver

ulen

taG

allo

tia s

tehl

ini

Lace

rtid

ae+

+V

alid

o &

Nog

ales

(un

publ

.)

FM

SS

Tem

p

CO

MP

OS

ITA

EH

ypoc

haer

is g

labr

aTe

stud

o gr

aeca

Test

udin

idae

– –

Cob

o &

And

reu

(198

8)D

SH

STe

mp

CO

NV

OLV

ULA

CE

AE

Ipom

oea

trifi

daR

hino

clem

mys

fune

rea

Em

ydid

ae0

Mol

l & J

anse

n (1

995)

DS

HW

Trop

EB

EN

AC

EA

ED

iosp

yros

con

sola

tae

Naj

as n

igric

ollis

Naj

idae

0E

ngel

(19

97)

FM

TW

Trop

ER

ICA

CE

AE

Gay

luss

acia

bac

cata

Terr

apen

e ca

rolin

aTe

stud

inid

ae0

Bra

un &

Bro

oks

(198

7)F

SS

WTe

mp

Vac

cini

um v

acill

ans

Terr

apen

e ca

rolin

aTe

stud

inid

ae0

Bra

un &

Bro

oks

(198

7)F

SS

WTe

mp

GR

AM

INE

AE

Briz

a m

axim

aTe

stud

o gr

aeca

Test

udin

idae

00C

obo

& A

ndre

u (1

988)

DS

HS

Tem

p

LEG

UM

INO

SA

EO

rnith

opus

sat

ivus

Test

udo

grae

caTe

stud

inid

ae–

0C

obo

& A

ndre

u (1

988)

DS

HS

Tem

p

MO

RA

CE

AE

Fic

us g

labr

ata

Rhi

nocl

emm

ys fu

nere

aE

myd

idae

0M

oll &

Jan

sen

(199

5)F

ST

WTr

opM

orus

alb

aTe

rrap

ene

caro

lina

Test

udin

idae

–B

raun

& B

rook

s (1

987)

FS

TW

Tem

p

PH

YT

OLA

CC

AC

EA

EP

hyto

lacc

a am

eric

ana

Terr

apen

e ca

rolin

aTe

stud

inid

ae+

Bra

un &

Bro

oks

(198

7)F

SH

WTe

mp

PO

LYG

ON

AC

EA

ER

umex

buc

epha

loph

orus

Test

udo

grae

caTe

stud

inid

ae–

–C

obo

& A

ndre

u (1

988)

DS

HS

Tem

p

RO

SA

CE

AE

Duc

hesn

ea in

dica

Terr

apen

e ca

rolin

aTe

stud

inid

ae0

Bra

un &

Bro

oks

(198

7)F

SH

WTe

mp

Fra

garia

virg

inia

naTe

rrap

ene

caro

lina

Test

udin

idae

0B

raun

& B

rook

s (1

987)

FS

HW

Tem

pP

runu

s se

rotin

aTe

rrap

ene

caro

lina

Test

udin

idae

+B

raun

& B

rook

s (1

987)

FM

TW

Tem

pR

ubus

pho

enic

olas

ius

Terr

apen

e ca

rolin

aTe

stud

inid

ae0

Bra

un &

Bro

oks

(198

7)F

SS

WTe

mp

Rub

us s

p.Te

rrap

ene

caro

lina

Test

udin

idae

0B

raun

& B

rook

s (1

987)

FS

SW

Tem

p

RU

BIA

CE

AE

Far

amea

sue

rren

sis

Rhi

nocl

emm

ys a

nnul

ata

Em

ydid

ae0

Mol

l & J

anse

n (1

995)

FM

?T

WTr

opN

erte

ra g

rana

dens

isLi

olae

mus

pic

tus

Trop

idur

idae

++

Will

son

et a

l.(1

996)

FS

HW

Tem

pP

loca

ma

pend

ula

Gal

lotia

gal

loti

Lace

rtid

ae00

Val

ido

& N

ogal

es (

unpu

bl.)

F

SS

STe

mp

Rel

boni

um h

ypoc

arpi

umLi

olae

mus

pic

tus

Trop

idur

idae

00W

illso

n et

al.

(199

6)F

SH

WTe

mp

Rub

ia fr

utic

osa

Gal

lotia

gal

loti

Lace

rtid

ae–

0V

alid

o &

Nog

ales

(19

94)

FS

SS

Tem

p

SA

NTA

LAC

EA

EK

unke

liella

ret

amoi

des

Gal

lotia

gal

loti

Lace

rtid

ae+

+V

alid

o &

Nog

ales

(un

publ

.)

FS

SS

Tem

p

SO

LAN

AC

EA

ELy

cium

intr

icat

umG

allo

tia a

tlant

ica

Lace

rtid

ae–

–N

ogal

es e

t al.

(199

8)F

SS

STe

mp

Lyci

um in

tric

atum

Gal

lotia

gal

loti

Lace

rtid

ae00

Val

ido

& N

ogal

es (

1994

)F

SS

STe

mp

Lyco

pers

icon

esc

ulen

tum

Test

udo

elep

hant

opus

Test

udin

idae

++

Ric

k &

Bow

man

(19

61)

FS

HS

Trop

Sol

anum

och

race

o-R

hino

clem

mys

ann

ulat

aE

myd

idae

0M

oll &

Jan

sen

(199

5)F

SS

WTr

opfe

rrug

ineu

mS

olan

um s

ipar

unoi

des

Rhi

nocl

emm

ys a

nnul

ata

Em

ydid

ae0

Mol

l & J

anse

n (1

995)

FS

SW

Trop

With

ania

aris

tata

Gal

lotia

gal

loti

Lace

rtid

ae+

+V

alid

o &

Nog

ales

(19

94)

FS

SS

Tem

p

VIT

AC

EA

EV

itis

aest

ival

isTe

rrap

ene

caro

lina

Test

udin

idae

+B

raun

& B

rook

s (1

987)

FM

SW

Tem

pV

itis

rotu

ndifo

liaTe

rrap

ene

caro

lina

Test

udin

idae

0B

raun

& B

rook

s (1

987)

FM

SW

Tem

pV

itis

vulp

ina

Terr

apen

e ca

rolin

aTe

stud

inid

ae0

Bra

un &

Bro

oks

(198

7)F

MS

WTe

mp

Bir

ds

AN

AC

AR

DIA

CE

AE

φP

ista

cia

pala

estin

aP

hoen

icur

us p

hoen

icur

usM

usci

capi

dae

++

Izha

ki &

Saf

riel (

1990

)F

ST

WTe

mp

φP

ista

cia

pala

estin

aTu

rdus

mer

ula

Mus

cica

pida

e+

+Iz

haki

& S

afrie

l (19

90)

FS

TW

Tem

pφ

Pis

taci

a pa

laes

tina

Pyc

nono

tus

barb

atus

Pyc

nono

tidae

++

Izha

ki &

Saf

riel (

1990

)F

ST

WTe

mp

178 A. Traveset

Ap

pen

dix

. (co

ntin

ued)

.

Pla

nt s

pec

ies

Dis

per

ser

spec

ies

Dis

per

ser

Eff

ect

Ref

eren

ceF

ruit

See

dL

ife

Hab

itat

Zo

ne

(FA

MIL

Y)

fam

ilyty

pe

size

form


φP

ista

cia

pala

estin

aS

ylvi

a at

ricap

illa

Syl

viid

ae+

+Iz

haki

& S

afrie

l (19

90)

FS

TW

Tem

pφ

Pis

taci

a pa

laes

tina

Syl

via

curr

uca

Syl

viid

ae+

+Iz

haki

& S

afrie

l (19

90)

FS

TW

Tem

pφ

Pis

taci

a pa

laes

tina

Syl

via

hort

ensi

sS

ylvi

idae

++

Izha

ki &

Saf

riel (

1990

)F

ST

WTe

mp

Rhu

s gl

abra

Col

inus

virg

inia

nus

Pha

sian

idae

+K

refti

ng &

Roe

(19

49)

FS

TW

Tem

pTo

xico

dend

ron

vern

ixC

olin

us v

irgin

ianu

sP

hasi

anid

ae+

Kre

fting

& R

oe (

1949

)F

ST

WTe

mp

Toxi

code

ndro

n ve

rnix

Pha

sian

us c

olch

icus

P

hasi

anid

ae+

Kre

fting

& R

oe (

1949

)F

ST

WTe

mp

ssp.

torq

uatu

s

AP

OC

YN

AC

EA

EC

aris

sa e

dulis

Pyc

nono

tus

barb

atus

Pyc

nono

tidae

00Li

eber

man

& L

iebe

rman

(19

86)

FS

?S

TS

WTr

opC

aris

sa e

dulis

Lam

prot

orni

s sp

.S

turn

idae

– –

Lieb

erm

an &

Lie

berm

an (

1986

)F

S?

ST

SW

Trop

φS

tem

mad

enia

don

nell-

smith

iiV

ireo

flavo

virid

isV

ireon

idae

0 –

McD

iarm

id e

t al.

(197

7)D

MT

WTr

op

AR

AC

EA

Eφ

Aru

m h

ygro

philu

mTu

rdus

mer

ula

Mus

cica

pida

e0

–B

arne

a et

al.

(199

1)F

SH

WTe

mp

AR

ALI

AC

EA

Eφ

Hed

era

helix

Uni

dent

ified

pas

serin

es00

Deb

ussc

he (

1985

)F

MS

STe

mp

φHed

era

helix

T. m

erul

a, S

turn

us v

ulga

risM

usci

capi

dae,

00

Cle

rgea

u (1

992)

FM

SW

Tem

pS

turn

idae

Opl

opan

ax h

orrid

usIx

oreu

s na

eviu

sM

usci

capi

dae

00Tr

aves

et &

Will

son

(199

7)

FM

SW

Tem

pO

plop

anax

hor

ridus

Turd

us m

igra

toriu

sM

usci

capi

dae

00Tr

aves

et &

Will

son

(199

7)

FM

SW

Tem

p

BO

RA

GIN

AC

EA

EE

hret

ia c

ymos

aP

oice

phal

us s

eneg

alus

Psi

ttaci

dae

00Li

eber

man

& L

iebe

rman

(19

86)

FS

ST

STr

opE

hret

ia c

ymos

aLa

mpr

otor

nis

sp.

Stu

rnid

ae00

Lieb

erm

an &

Lie

berm

an (

1986

) F

SS

TS

Trop

CA

CTA

CE

AE

Rhi

psal

is b

acci

fera

Turd

us le

ucom

elas

Mus

cica

pida

e+

, –Lo

mba

rdi &

Mot

ta (

1995

)F

SS

W?

Trop

diffe

rent

res

ults

in tw

opo

pula

tions

Rhi

psal

is p

unic

eo-d

iscu

sTu

rdus

leuc

omel

asM

usci

capi

dae

+Lo

mba

rdi &

Mot

ta (

1995

)F

SS

W?

Trop

CA

PP

AR

AC

EA

EC

appa

ris e

ryth

roca

rpos

Poi

ceph

alus

sen

egal

usP

sitta

cida

e00

Lieb

erm

an &

Lie

berm

an (

1986

)F

S?

SS

WTr

opC

appa

ris e

ryth

roca

rpos

Pyc

nono

tus

barb

atus

Pyc

nono

tidae

0+Li

eber

man

& L

iebe

rman

(19

86)

FS

?S

SW

Trop

Cap

paris

ery

thro

carp

osLa

mpr

otor

nis

sp.

Stu

rnid

ae0+

Lieb

erm

an &

Lie

berm

an (

1986

)F

S?

SS

WTr

op

CA

PR

IFO

LIA

CE

AE

Loni

cera

tata

rica

Dum

etel

la c

arol

inen

sis

Mim

idae

0K

refti

ng &

Roe

(19

49)

FS

SW

Tem

pLo

nice

ra ta

taric

aTu

rdus

mig

rato

rius

Mus

cica

pida

e+

Kre

fting

& R

oe (

1949

),

FS

SW

Tem

pin

cons

iste

nt a

mon

g pr

e-se

ed tr

eatm

ents

Sam

bucu

s ca

nade

nsis

Dum

etel

la c

arol

inen

sis

Mim

idae

+K

refti

ng &

Roe

(19

49)

FS

ST

WTe

mp

Sam

bucu

s ca

nade

nsis

Turd

us m

igra

toriu

sM

usci

capi

dae

+K

refti

ng &

Roe

(19

49)

FS

ST

WTe

mp

Sam

bucu

s ca

nade

nsis

Pha

sian

us c

olch

icus

P

hasi

anid

ae–

Kre

fting

& R

oe (

1949

)F

SS

TW

Tem

pss

p. to

rqua

tus

φS

ambu

cus

nigr

aT.

mer

ula,

Mus

cica

pida

e,

– +

Cle

rgea

u (1

992)

FS

SW

Tem

pS

turn

us v

ulga

risS

turn

idae

Sam

bucu

s ra

cem

osa

Ixor

eus

naev

ius

Mus

cica

pida

e0+

Trav

eset

& W

illso

n (1

997)

F

SS

WTe

mp

Sam

bucu

s ra

cem

osa

Turd

us m

igra

toriu

sM

usci

capi

dae

0+Tr

aves

et &

Will

son

(199

7)

FS

SW

Tem

p

CH

EN

OP

OD

IAC

EA

ER

hago

dia

para

bolic

aZ

oste

rops

late

ralis

Zos

tero

pida

e+

+W

illso

n &

O’D

owd

(198

9)

FS

SW

Tem

p

CO

NN

AR

AC

EA

EB

yrso

carp

us c

occi

neus

Poi

ceph

alus

sen

egal

usP

sitta

cida

e00

Lieb

erm

an &

Lie

berm

an (

1986

)F

M?

SS

Trop

Byr

soca

rpus

coc

cine

usP

ycno

notu

s ba

rbat

usP

ycno

notid

ae00

Lieb

erm

an &

Lie

berm

an (

1986

)F

M?

SS

Trop

Byr

soca

rpus

coc

cine

usLa

mpr

otor

nis

sp.

Stu

rnid

ae00

Lieb

erm

an &

Lie

berm

an (

1986

)F

M?

SS

Trop

CO

RN

AC

EA

EC

ornu

s ra

cem

osa

Uni

dent

ified

pas

serin

es+

Sm

ith (

1975

)F

SS

WTe

mp

Cor

nus

race

mos

aC

olin

us v

irgin

ianu

sP

hasi

anid

ae–

Kre

fting

& R

oe (

1949

)F

SS

WTe

mp

Cor

nus

race

mos

aP

hasi

anus

col

chic

us

Pha

sian

idae

–K

refti

ng &

Roe

(19

49)

FS

SW

Tem

pss

p. to

rqua

tus

Cor

nus

stol

onife

raC

olin

us v

irgin

ianu

sP

hasi

anid

ae–

Kre

fting

& R

oe (

1949

),

FS

TW

Tem

pin

cons

iste

nt a

mon

g pr

e-se

ed tr

eatm

ents

Cor

nus

stol

onife

raP

hasi

anus

col

chic

us

Pha

sian

idae

–K

refti

ng &

Roe

(19

49),

F

ST

WTe

mp

ssp.

torq

uatu

sin

cons

iste

nt a

mon

g pr

e-se

ed tr

eatm

ents

CU

PR

ES

SA

CE

AE

Juni

peru

s m

onos

perm

aM

yade

stes

tow

nsen

diM

usci

capi

dae

00S

alom

onso

n (1

978)

, F

SS

TW

Tem

pin

cons

iste

nt r

esul

tsam

ong

seed

age

sJu

nipe

rus

virg

inia

naB

omby

cilla

ced

roru

m,

Bom

byci

llida

e,+

Hol

thui

jzen

& S

harik

(19

85)

FS

TG

Tem

pD

endr

oica

cor

onat

aE

mbe

rizid

aeJu

nipe

rus

virg

inia

naC

yano

citta

cris

tata

Cor

vida

e–

Livi

ngst

on (

1972

)F

ST

GTe

mp

Juni

peru

s vi

rgin

iana

Loph

orty

x ca

lifor

nica

Pha

sian

idae

–Li

ving

ston

(19

72)

FS

TG

Tem

pJu

nipe

rus

virg

inia

naS

turn

us v

ulga

risS

turn

idae

–Li

ving

ston

(19

72)

FS

TG

Tem

p

180 A. Traveset

Ap

pen

dix

. (co

ntin

ued)

.

Pla

nt s

pec

ies

Dis

per

ser

spec

ies

Dis

per

ser

Eff

ect

Ref

eren

ceF

ruit

See

dL

ife

Hab

itat

Zo

ne

(FA

MIL

Y)

fam

ilyty

pe

size

form


EP

HE

DR

AC

EA

Eφ

Eph

edra

cam

pylo

poda

Turd

us m

erul

aM

usci

capi

dae

00B

arne

a et

al.

(199

1)F

SS

WTe

mp

φE

phed

ra c

ampy

lopo

daP

ycno

notu

s xa

ntho

pygo

sP

ycno

notid

ae00

Bar

nea

et a

l.(1

991)

FS

SW

Tem

p

ER

ICA

CE

AE

Vac

cini

um a

lask

aens

e,Ix

oreu

s na

eviu

sM

usci

capi

dae

00Tr

aves

et &

Will

son

(199

7)

FS

SW

Tem

pV

. ova

lifol

ium

Vac

cini

um a

lask

aens

e,Tu

rdus

mig

rato

rius

Mus

cica

pida

e00

Trav

eset

& W

illso

n (1

997)

F

SS

WTe

mp

V. o

valif

oliu

mV

acci

nium

ang

ustif

oliu

mTu

rdus

mig

rato

rius

Mus

cica

pida

e–

0C

ross

land

& V

ande

r Klo

et (

1996

)F

SS

STe

mp

EU

PH

OR

BIA

CE

AE

Sec

urin

ega

viro

saP

oice

phal

us s

eneg

alus

Psi

ttaci

dae

00Li

eber

man

& L

iebe

rman

(19

86)

FS

SS

Trop

Sec

urin

ega

viro

saP

ycno

notu

s ba

rbat

usP

ycno

notid

ae00

Lieb

erm

an &

Lie

berm

an (

1986

)F

SS

STr

opS

ecur

ineg

a vi

rosa

Lam

prot

orni

s sp

.S

turn

idae

00Li

eber

man

& L

iebe

rman

(19

86)

FS

SS

Trop

FLA

CO

UR

TIA

CE

AE

Cas

earia

cor

ymbo

saM

elan

erpe

s au

rifro

nsP

icid

ae00

How

e &

Van

de K

erkh

ove

(197

9)

DM

TW

Trop

Cas

earia

cor

ymbo

saM

yiod

ynas

tes

mac

ulat

usTy

rann

idae

00H

owe

& V

ande

Ker

khov

e (1

979)

DM

TW

Trop

Cas

earia

cor

ymbo

saV

ireo

flavo

virid

isV

ireon

idae

00H

owe

& V

ande

Ker

khov

e (1

979)

D

MT

WTr

opF

laco

urtia

flav

esce

nsP

ycno

notu

s ba

rbat

usP

ycno

notid

ae–

–Li

eber

man

& L

iebe

rman

(19

86)

FM

SS

WTr

opF

laco

urtia

flav

esce

nsLa

mpr

otor

nis

sp.

Stu

rnid

ae–

–Li

eber

man

& L

iebe

rman

(19

86)

FM

SS

WTr

op

LAU

RA

CE

AE

Lind

era

benz

oin

Turd

us m

igra

toriu

sM

usci

capi

dae

0C

ipol

lini (

unpu

bl.)

FM

SW

Tem

pC

ipol

lini &

Lev

ey (

1997

)LE

GU

MIN

OS

AE

Aca

cia

cycl

ops

Uni

dent

ified

pas

serin

es+

Gly

phis

et a

l.(1

981)

DM

SS

Trop

LILI

AC

EA

EA

spar

agus

acu

tifol

ius

Uni

dent

ified

pas

serin

es00

Deb

ussc

he (

1985

)F

SH

STe

mp

φA

spar

agus

aph

yllu

sE

ritha

cus

rube

cula

Mus

cica

pida

e00

Bar

nea

et a

l.(1

991)

Fs

HW

Tem

pφ

Asp

arag

us a

phyl

lus

Turd

us m

erul

aM

usci

capi

dae

00B

arne

a et

al.

(199

1)F

sH

WTe

mp

Str

epto

pus

ampl

exifo

lius

Ixor

eus

naev

ius

Mus

cica

pida

e00

Trav

eset

& W

illso

n (1

997)

F

SH

WTe

mp

Str

epto

pus

ampl

exifo

lius

Turd

us m

igra

toriu

sM

usci

capi

dae

00Tr

aves

et &

Will

son

(199

7)

SH

WTe

mp

MA

GN

OLI

AC

EA

EM

iche

lia c

ham

paca

Ters

ina

virid

isF

ringi

llida

e+

+F

igue

iredo

(19

97)

DL

TC

Trop

ME

LAS

TO

MA

TAC

EA

EC

lidem

ia d

ensi

flora

Pip

ra m

enta

lisTy

rann

idae

++

Elli

son

et a

l.(1

993)

FS

TW

Trop

Clid

emia

pur

pure

o-vi

olac

eaA

rrem

on a

uran

tirro

stris

Em

beriz

idae

++

Leve

y (1

986)

FS

S?

WTr

opC

onos

tegi

a su

bcru

stul

ata

Pip

ra m

enta

lisTy

rann

idae

00E

lliso

n et

al.

(199

3)F

ST

WTr

op

Mic

onia

affi

nis

Pip

ra m

enta

lisTy

rann

idae

– +

Elli

son

et a

l. (1

993)

FS

TW

Trop

Mic

onia

sim

plex

Pip

ra m

enta

lisTy

rann

idae

+ –

Elli

son

et a

l.(1

993)

FS

TW

Trop

Oss

aea

mac

roph

ylla

Pip

ra m

enta

lisTy

rann

idae

+ –

Elli

son

et a

l.(1

993)

FS

TW

Trop

ME

LIA

CE

AE

Aza

dira

chta

indi

caP

oice

phal

us s

eneg

alus

Psi

ttaci

dae

0+Li

eber

man

& L

iebe

rman

(19

86)

FL

TS

GTr

opA

zadi

rach

ta in

dica

Pyc

nono

tus

barb

atus

Pyc

nono

tidae

++

Lieb

erm

an &

Lie

berm

an (

1986

)F

LT

SG

Trop

Aza

dira

chta

indi

caLa

mpr

otor

nis

sp.

Stu

rnid

ae0+

Lieb

erm

an &

Lie

berm

an (

1986

)F

LT

SG

Trop

MO

RA

CE

AE

Fic

us b

enga

lens

isA

crid

othe

res

tris

tis,

Stu

rnid

ae+

+M

idya

& B

rahm

acha

ry (

1991

)F

ST

WTr

opA

. fus

cus

φF

icus

car

ica

Syl

via

borin

Syl

viid

ae0

Lisc

i & P

acin

i (19

94)

FS

TC

Tem

pF

icus

lusc

hnat

hian

aTu

rdus

leuc

omel

asM

usci

capi

dae

+F

igue

iredo

& P

erin

(19

95)

FS

TW

Trop

φF

icus

mic

roca

rpa

Uni

dent

ified

spe

cies

0F

igue

iredo

et a

l. (1

995)

FS

TC

Trop

Fic

us m

icro

carp

aTu

rdus

ruf

iven

tris

Mus

cica

pida

e+

+G

uerr

ero

& F

igue

iredo

(19

97)

FS

TC

Trop

Mor

us a

lba

Turd

us m

igra

toriu

sM

usci

capi

dae

+K

refti

ng &

Roe

(19

49)

FS

TC

Tem

pM

orus

nig

raTu

rdus

mer

ula

Mus

cica

pida

e+

+B

arne

a et

al.

(199

1, 1

992)

F

ST

CTe

mp

Mor

us n

igra

Pyc

nono

tus

xant

hopy

gos

Pyc

nono

tidae

++

Bar

nea

et a

l.(1

991,

199

2)

FS

TC

Tem

p

MY

RTA

CE

AE

φM

yrtu

s co

mm

unis

Turd

us m

erul

aM

usci

capi

dae

0+B

arne

a et

al.

(199

1)F

SS

WTe

mp

φM

yrtu

s co

mm

unis

Pyc

nono

tus

xant

hopy

gos

Pyc

nono

tidae

0+B

arne

a et

al.

(199

1)F

SS

WTe

mp

NA

JAD

AC

EA

EN

ajas

mar

ina

Ana

s pl

atyr

hync

hos

Ana

tidae

++

Aga

mi &

Wai

sel (

1986

)D

SH

ATe

mp

PO

DO

CA

RP

AC

EA

EP

rum

nopi

tys

ferr

ugin

eaH

emip

haga

C

olum

bida

e00

Clo

ut &

Till

ey (

1992

)F

LT

WTe

mp

nova

esee

land

iae

RH

AM

NA

CE

AE

φR

ham

nus

alat

ernu

sTu

rdus

mer

ula

Mus

cica

pida

e+

+B

arne

a et

al.

(199

1)F

SS

TS

WTe

mp

φR

ham

nus

alat

ernu

sP

ycno

notu

s xa

ntho

pygo

sP

ycno

notid

ae+

+B

arne

a et

al.

(199

1)F

SS

TS

WTe

mp

φR

ham

nus

pala

estin

usTu

rdus

mer

ula

Mus

cica

pida

e+

+Iz

haki

& S

afrie

l (19

90)

FS

SS

Tem

p+

–B

arne

a et

al.

(199

1)R

ham

nus

pala

estin

usP

ycno

notu

s ba

rbat

usP

ycno

notid

ae00

Izha

ki &

Saf

riel (

1990

)F

SS

STe

mp

φR

ham

nus

pala

estin

usP

ycno

notu

s xa

ntho

pygo

sP

ycno

notid

ae+

0B

arne

a et

al.

(199

1)F

SS

STe

mp

182 A. Traveset

Ap

pen

dix

. (co

ntin

ued)

.

Pla

nt s

pec

ies

Dis

per

ser

spec

ies

Dis

per

ser

Eff

ect

Ref

eren

ceF

ruit

See

dL

ife

Hab

itat

Zo

ne

(FA

MIL

Y)

fam

ilyty

pe

size

form


Rha

mnu

s pa

laes

tinus

Syl

via

atric

apill

aS

ylvi

idae

00Iz

haki

& S

afrie

l (19

90)

FS

SS

Tem

pR

ham

nus

pala

estin

usS

ylvi

a cu

rruc

aS

ylvi

idae

00Iz

haki

& S

afrie

l (19

90)

FS

SS

Tem

pR

ham

nus

pala

estin

usS

ylvi

a ho

rten

sis

Syl

viid

ae00

Izha

ki &

Saf

riel (

1990

)F

SS

STe

mp

RO

SA

CE

AE

Pru

nus

sero

tina

Uni

dent

ified

pas

serin

es+

Sm

ith (

1975

)F

MT

WTe

mp

Pru

nus

sero

tina

Turd

us m

igra

toriu

sM

usci

capi

dae

+K

refti

ng &

Roe

(19

49)

FM

TW

Tem

pP

runu

s vi

rgin

iana

Pha

sian

us c

olch

icus

P

hasi

anid

ae–

Kre

fting

& R

oe (

1949

)F

MT

WTe

mp

ssp.

torq

uatu

sP

yrac

anth

a co

ccin

eaU

nide

ntifi

ed p

asse

rines

0+D

ebus

sche

(19

85)

FS

SS

Tem

pR

osa

blan

daC

olin

us v

irgin

ianu

sP

hasi

anid

ae–

Kre

fting

& R

oe (

1949

),F

SS

SW

Tem

pin

cons

iste

nt a

mon

g pr

e-se

ed tr

eatm

ents

Ros

a bl

anda

Pha

sian

us c

olch

icus

P

hasi

anid

ae–

Kre

fting

& R

oe (

1949

),

FS

SS

WTe

mp

ssp.

torq

uatu

sin

cons

iste

nt a

mon

g pr

e-se

ed tr

eatm

ents

Ros

a sp

.P

edio

cete

s ph

asia

nellu

sP

hasi

anid

ae–

Kre

fting

& R

oe (

1949

)F

SS

SW

Tem

pR

osa

sp.

Pha

sian

us c

olch

icus

P

hasi

anid

ae+

Kre

fting

& R

oe (

1949

)F

SS

SW

Tem

pss

p. to

rqua

tus

φR

ubus

frut

icos

usTu

rdus

mer

ula,

Mus

cica

pida

e,00

Cle

rgea

u (1

992)

FS

SG

Tem

pS

turn

us v

ulga

risS

turn

idae

Rub

us o

ccid

enta

lisB

omby

cilla

ced

roru

mB

omby

cilli

dae

–K

refti

ng &

Roe

(19

49),

F

SS

SW

Tem

pin

cons

iste

nt a

mon

g pr

e-se

ed tr

eatm

ents

Rub

us p

roce

rus

Dro

mai

us n

ovae

holla

ndia

eC

asua

riida

e0

Bru

nner

et a

l. (1

976)

FS

SS

WTe

mp

Rub

us s

anct

usTu

rdus

mer

ula

Mus

cica

pida

e–

0B

arne

a et

al.

(199

1)F

SS

STe

mp

Rub

us s

anct

usP

ycno

notu

s xa

ntho

pygo

sP

ycno

notid

ae–

0B

arne

a et

al.

(199

1)F

SS

STe

mp

Rub

us s

p.B

omby

cilla

ced

roru

mB

omby

cilli

dae

0K

refti

ng &

Roe

(19

49)

FS

SS

WTe

mp

Rub

us s

p.D

umet

ella

car

olin

ensi

sM

imid

ae+

Kre

fting

& R

oe (

1949

)F

SS

SW

Tem

pR

ubus

sp.

Turd

us m

igra

toriu

sM

usci

capi

dae

+K

refti

ng &

Roe

(19

49)

FS

SS

WTe

mp

Rub

us s

pect

abili

sIx

oreu

s na

eviu

sM

usci

capi

dae

0+Tr

aves

et &

Will

son

(199

7)

FS

SW

Tem

pR

ubus

spe

ctab

ilis

Turd

us m

igra

toriu

sM

usci

capi

dae

0+Tr

aves

et &

Will

son

(199

7)

FS

SW

Tem

p

RU

BIA

CE

AE

Plo

cam

a pe

ndul

aS

ylvi

a m

elan

ocep

hala

, S

ylvi

idae

0+V

alid

o &

Nog

ales

(un

publ

.)F

SS

STe

mp

S. c

onsp

icill

ata

Rub

ia te

nuifo

liaTu

rdus

mer

ula

Mus

cica

pida

e0

–Iz

haki

& S

afrie

l (19

90)

FS

HW

Tem

pφ

Rub

ia te

nuifo

liaTu

rdus

mer

ula

Mus

cica

pida

e0+

Bar

nea

et a

l.(1

991)

FS

HW

Tem

pR

ubia

tenu

ifolia

Pyc

nono

tus

barb

atus

Pyc

nono

tidae

0 –

Izha

ki &

Saf

riel (

1990

)F

SH

WTe

mp

φR

ubia

tenu

ifolia

Pyc

nono

tus

xant

hopy

gos

Pyc

nono

tidae

0+B

arne

a et

al.

(199

1)F

SH

WTe

mp

Rub

ia te

nuifo

liaS

ylvi

a at

ricap

illa

Syl

viid

ae0

–Iz

haki

& S

afrie

l (19

90)

FS

HW

Tem

pR

ubia

tenu

ifolia

Syl

via

curr

uca

Syl

viid

ae0

–Iz

haki

& S

afrie

l (19

90)

FS

HW

Tem

pR

ubia

tenu

ifolia

Syl

via

hort

ensi

sS

ylvi

idae

0 –

Izha

ki &

Saf

riel (

1990

)F

SH

WTe

mp

RU

TAC

EA

EC

laus

ena

anis

ata

Pyc

nono

tus

barb

atus

Pyc

nono

tidae

0 –

Lieb

erm

an &

Lie

berm

an (

1986

)F

M?

SS

Trop

Cla

usen

a an

isat

aLa

mpr

otor

nis

sp.

Stu

rnid

ae–

–Li

eber

man

& L

iebe

rman

(19

86)

FM

?S

STr

op

SA

NTA

LAC

EA

EO

syris

alb

aTu

rdus

mer

ula

Mus

cica

pida

e+

+Iz

haki

& S

afrie

l (19

90)

FM

SW

Tem

pO

syris

alb

aP

ycno

notu

s ba

rbat

usP

ycno

notid

ae+

+Iz

haki

& S

afrie

l (19

90)

FM

SW

Tem

p

SA

XIF

RA

GA

CE

AE

Rib

es b

ract

eosu

mIx

oreu

s na

eviu

sM

usci

capi

dae

00Tr

aves

et &

Will

son

(199

7)

FS

SW

Tem

pR

ibes

bra

cteo

sum

Turd

us m

igra

toriu

sM

usci

capi

dae

00Tr

aves

et &

Will

son

(199

7)

FS

SW

Tem

pR

ibes

mis

sour

iens

eB

omby

cilla

ced

roru

mB

omby

cilli

dae

+K

refti

ng &

Roe

(19

49)

FS

SW

Tem

pR

ibes

mis

sour

iens

eD

umet

ella

car

olin

ensi

sM

imid

ae+

Kre

fting

& R

oe (

1949

)F

SS

WTe

mp

SM

ILA

CA

CE

AE

φS

mila

x as

pera

Turd

us m

erul

aM

usci

capi

dae

+0

Izha

ki &

Saf

riel (

1990

)F

SS

SW

Tem

pφ

Sm

ilax

aspe

raTu

rdus

phi

lom

elos

Mus

cica

pida

e00

Izha

ki &

Saf

riel (

1990

)F

SS

SW

Tem

pφ

Sm

ilax

aspe

raP

ycno

notu

s ba

rbat

usP

ycno

notid

ae00

Izha

ki &

Saf

riel (

1990

)F

SS

SW

Tem

p

SO

LAN

AC

EA

ELy

cium

intr

icat

umLa

nius

exc

ubito

rLa

niid

ae+

+N

ogal

es e

t al.

(unp

ubl.)

F

SS

STe

mp

Sol

anum

dul

cam

ara

Uni

dent

ified

pas

serin

es0

Sm

ith (

1975

)F

SH

WTe

mp

Sol

anum

lute

umTu

rdus

mer

ula

Mus

cica

pida

e+

Bar

nea

et a

l.(1

990)

,F

SH

CTe

mp

++

Mas

& T

rave

set (

unpu

bl.)

Sol

anum

lute

umP

ycno

notu

s xa

ntho

pygo

sP

ycno

notid

ae+

Bar

nea

et a

l.(1

990)

FS

HC

Tem

pS

olan

um lu

teum

Syl

via

mel

anoc

epha

laS

ylvi

idae

++

Mas

& T

rave

set (

unpu

bl.)

FS

HC

Tem

pφ

Sol

anum

nig

rum

Turd

us m

erul

a,M

usci

capi

dae,

+

+C

lerg

eau

(199

2)F

SH

CTe

mp

Stu

rnus

vul

garis

Stu

rnid

aeS

olan

um n

igru

mTu

rdus

mer

ula

Mus

cica

pida

e0

Bar

nea

et a

l. (1

990)

,F

SH

CTe

mp

00M

as &

Tra

vese

t (un

publ

.)S

olan

um n

igru

mP

ycno

notu

s xa

ntho

pygo

sP

ycno

notid

ae0

Bar

nea

et a

l. (1

990)

FS

HC

Tem

pS

olan

um n

igru

mS

ylvi

a m

elan

ocep

hala

Syl

viid

ae00

Mas

& T

rave

set (

unpu

bl.)

FS

HC

Tem

pW

ither

ingi

a so

lana

ceae

Mya

dest

es m

elan

ops

Mus

cica

pida

e+

Mur

ray

et a

l. (1

994)

FS

?S

WTr

op

UR

TIC

AC

EA

EU

rera

car

acas

ana

Arr

emon

aur

antir

rost

risE

mbe

rizid

ae0

Leve

y (1

986)

, onl

yF

SS

?W

Trop

viab

ility

test

ed

184 A. Traveset

Ap

pen

dix

. (co

ntin

ued)

.

Pla

nt s

pec

ies

Dis

per

ser

spec

ies

Dis

per

ser

Eff

ect

Ref

eren

ceF

ruit

See

dL

ife

Hab

itat

Zo

ne

(FA

MIL

Y)

fam

ilyty

pe

size

form


VE

RB

EN

AC

EA

EP

rem

na q

uadr

ifolia

Lam

prot

orni

ssp

.S

turn

idae

00Li

eber

man

& L

iebe

rman

(19

86)

FS

SS

WTr

op

VIT

AC

EA

EV

itis

ripar

iaU

nide

ntifi

ed p

asse

rines

+S

mith

(19

75)

FM

SC

Tem

pV

itis

ripar

iaC

olin

us v

irgin

ianu

sP

hasi

anid

ae–

Kre

fting

& R

oe (

1949

)F

SS

CTe

mp

Viti

s rip

aria

Pha

sian

us c

olch

icus

P

hasi

anid

ae–

Kre

fting

& R

oe (

1949

)F

SS

CTe

mp

ssp.

torq

uatu

s

ZY

GO

PH

YLL

AC

EA

EN

itrar

ia b

illar

dier

iD

rom

aius

nov

aeho

lland

iae

Cas

uarii

dae

++

Nob

le (

1975

)F

?S

?Te

mp

Fly

ing

mam

mal

s (b

ats)

AP

OC

YN

AC

EA

EC

aris

sa e

dulis

Epo

mop

horu

s ga

mbi

anus

Pte

ropo

dida

e00

Lieb

erm

an &

Lie

berm

an (

1986

)F

S?

ST

SW

Trop

BO

RA

GIN

AC

EA

EE

hret

ia c

ymos

aE

idol

on h

elvu

mP

tero

podi

dae

00Li

eber

man

& L

iebe

rman

(19

86)

FS

ST

STr

opE

hret

ia c

ymos

aE

pom

opho

rus

gam

bian

usP

tero

podi

dae

00Li

eber

man

& L

iebe

rman

(19

86)

FS

ST

STr

op

CE

CR

OP

IAC

EA

EC

ecro

pia

pelta

taC

arol

lia p

ersp

icill

ata

Phy

llost

omid

ae+

Fle

min

g (1

988)

FS

TW

Trop

ELA

EO

CA

RP

AC

EA

EM

untin

gia

cala

bura

Car

ollia

per

spic

illat

aP

hyllo

stom

idae

0F

lem

ing

(198

8)F

ST

WTr

op

ER

ICA

CE

AE

Arb

utus

and

rach

neR

ouse

tus

aegy

ptia

cus

Pte

ropo

dida

e0-

Izha

ki e

t al.

(199

5)F

ST

WTe

mp

EU

PH

OR

BIA

CE

AE

Sec

urin

ega

viro

saE

idol

on h

elvu

mP

tero

podi

dae

00Li

eber

man

& L

iebe

rman

(19

86)

FS

SS

GTr

opS

ecur

ineg

a vi

rosa

Epo

mop

horu

s ga

mbi

anus

Pte

ropo

dida

e00

Lieb

erm

an &

Lie

berm

an (

1986

)F

SS

SG

Trop

FLA

CO

UR

TIA

CE

AE

Fla

cour

tia fl

aves

cens

Epo

mop

horu

s ga

mbi

anus

Pte

ropo

dida

e–

–Li

eber

man

& L

iebe

rman

(19

86)

FM

SS

WTr

op

LEG

UM

INO

SA

EC

erat

onia

sili

qua

Rou

setu

s ae

gypt

iacu

sP

tero

podi

dae

00Iz

haki

et a

l.(1

995)

DL

TC

Tem

p

ME

LIA

CE

AE

Aza

dira

chta

indi

caE

idol

on h

elvu

mP

tero

podi

dae

00Li

eber

man

& L

iebe

rman

(19

86)

FL

TS

Trop

Aza

dira

chta

indi

caE

pom

opho

rus

gam

bian

usP

tero

podi

dae

+ –

Lieb

erm

an &

Lie

berm

an (

1986

)F

LT

STr

op

MO

RA

CE

AE

Chl

orop

hora

tinc

toria

Car

ollia

per

spic

illat

aP

hyllo

stom

idae

0F

lem

ing

(198

8)F

ST

WTr

opF

icus

car

ica

Rou

setu

s ae

gypt

iacu

sP

tero

podi

dae

00Iz

haki

et a

l. (1

995)

FS

TC

Tem

pF

icus

chr

ysol

epis

5–10

spe

cies

Pte

ropo

dida

e+

0U

tzur

rum

& H

eide

man

(19

91)

FS

TW

Trop

Fic

us lu

schn

athi

ana

Pla

tyrr

hinu

s lin

eatu

sP

hyllo

stom

idae

0F

igue

iredo

& P

erin

(19

95)

FS

TC

Trop

Fic

us m

icro

carp

aU

nide

nfiti

ed s

peci

esP

hyllo

stom

idae

+F

igue

iredo

et a

l. (1

995)

,F

ST

WTr

opin

labo

rato

ry n

ot fi

eld

Mor

us n

igra

Rou

setu

s ae

gypt

iacu

sP

tero

podi

dae

00Iz

haki

et a

l.(1

995)

FS

TC

Tem

p

PIP

ER

AC

EA

EP

iper

am

alag

oC

arol

lia p

ersp

icill

ata

Phy

llost

omid

ae0

Fle

min

g (1

988)

FS

ST

WTr

op

RH

AM

NA

CE

AE

Ziz

yphu

s sp

ina-

chris

tiR

ouse

tus

aegy

ptia

cus

Pte

ropo

dida

e00

Izha

ki e

t al.

(199

5)F

LT

STe

mp

RO

SA

CE

AE

Erio

botr

ya ja

poni

caR

ouse

tus

aegy

ptia

cus

Pte

ropo

dida

e+

0Iz

haki

et a

l.(1

995)

FL

TC

Tem

p

RU

TAC

EA

EC

laus

ena

anis

ata

Epo

mop

horu

s ga

mbi

anus

Pte

ropo

dida

e–

–Li

eber

man

& L

iebe

rman

(19

86)

FM

?S

STr

op

SO

LAN

AC

EA

ES

olan

um h

azen

iiC

arol

lia p

ersp

icill

ata

Phy

llost

omid

ae+

Fle

min

g (1

988)

FS

?S

G?

Trop

VE

RB

EN

AC

EA

EP

rem

na q

uadr

ifolia

Epo

mop

horu

s ga

mbi

anus

Pte

ropo

dida

e00

Lieb

erm

an &

Lie

berm

an (

1986

)F

SS

SW

Trop

No

n-f

lyin

g m

amm

als

AN

AC

AR

DIA

CE

AE

Pse

udos

pond

ias

mic

roca

rpa

Pan

trog

lody

tes

Pon

gida

e0

Taka

saki

(19

83)

FL

TW

Trop

Scl

eroc

arya

caf

fra

Loxo

dont

a af

rican

aE

leph

antid

ae+

Lew

is (

1987

)F

LT

WTr

opS

pond

ias

purp

urea

Odo

coile

us v

irgin

ianu

sC

ervi

dae

0M

andu

jano

et a

l. (1

994)

FL

TW

Trop

AN

NO

NA

CE

AE

Rol

linia

jim

enez

iiA

loua

tta p

allia

taC

ebid

ae0

Est

rada

& C

oate

s-F

?T

WTr

opE

stra

da (

1986

)

186 A. Traveset

Ap

pen

dix

. (co

ntin

ued)

.

Pla

nt s

pec

ies

Dis

per

ser

spec

ies

Dis

per

ser

Eff

ect

Ref

eren

ceF

ruit

See

dL

ife

Hab

itat

Zo

ne

(FA

MIL

Y)

fam

ilyty

pe

size

form


AR

ALI

AC

EA

EA

ralia

nud

icau

lisU

rsus

am

eric

anus

Urs

idae

0K

refti

ng &

Roe

(19

49)

FS

HW

Tem

pφ

Ara

lia n

udic

aulis

Urs

us a

mer

ican

usU

rsid

ae+

Rog

ers

& A

pple

gate

(19

83)

FS

HW

Tem

pO

plop

anax

hor

ridus

Urs

us a

mer

ican

usU

rsid

ae00

Trav

eset

& W

illso

n (1

997)

F

MS

WTe

mp

Opl

opan

ax h

orrid

usU

rsus

arc

tos

Urs

idae

00Tr

aves

et &

Will

son

(199

7)

FM

SW

Tem

p

BA

LAN

ITA

CE

AE

Bal

anite

s w

ilson

iana

Loxo

dont

a af

rican

aE

leph

antid

ae+

Lieb

erm

an e

t al.

(198

7)F

LT

WTr

op

BIG

NO

NIA

CE

AE

Cre

scen

tia a

lata

Equ

us c

abal

lus

Equ

idae

0Ja

nzen

& M

artin

(19

82)

FM

TG

Trop

BO

RA

GIN

AC

EA

EC

ordi

a lo

mat

olob

aA

loua

tta s

enic

ulus

Ceb

idae

00Ju

lliot

(19

96)

FS

TW

Trop

CA

PP

AR

AC

EA

EC

appa

ris e

ryth

roca

rpos

Ery

thro

cebu

s pa

tas

Cer

copi

thec

idae

0+Li

eber

man

& L

iebe

rman

(19

86)

FS

?S

SW

Trop

CA

PR

IFO

LIA

CE

AE

Sam

bucu

s ra

cem

osa

Urs

us a

mer

ican

usU

rsid

ae00

Trav

eset

& W

illso

n (1

997)

F

SS

WTe

mp

CE

CR

OP

IAC

EA

EC

ecro

pia

obtu

saA

loua

tta s

enic

ulus

Ceb

idae

– 0

Julli

ot (

1996

)F

ST

WTr

opC

ecro

pia

obtu

sifo

liaA

loua

tta p

allia

taC

ebid

ae+

Est

rada

& C

oate

s-E

stra

da (1

986)

FS

TW

Trop

CE

LAS

TR

AC

EA

EG

oupi

a gl

abra

Alo

uatta

sen

icul

usC

ebid

ae+

+Ju

lliot

(19

96)

F?

?W

Trop

CH

RY

SO

BA

LAN

AC

EA

ELi

cani

a m

embr

anac

eae

Alo

uatta

sen

icul

usC

ebid

ae00

Julli

ot (

1996

)F

?T

WTr

opP

arin

ari e

xcel

saLo

xodo

nta

afric

ana

Ele

phan

tidae

0Li

eber

man

et a

l.(1

987)

FL

TW

Trop

CIS

TAC

EA

EC

istu

s la

dani

fer

Cer

vus

elap

hus

Cer

vida

e+

Mal

o &

Suá

rez

(199

6)D

SS

STe

mp

CO

NN

AR

AC

EA

EB

yrso

carp

us c

occi

neus

Ery

thro

cebu

s pa

tas

Cer

copi

thec

idae

– –

Lieb

erm

an &

Lie

berm

an (

1986

)D

M?

SS

Trop

CO

RN

AC

EA

Eφ

Cor

nus

rugo

saU

rsus

am

eric

anus

Urs

idae

0R

oger

s &

App

lega

te (

1983

) F

SS

WTe

mp

φC

ornu

s st

olon

ifera

Urs

us a

mer

ican

usU

rsid

ae+

Rog

ers

& A

pple

gate

(19

83)

FS

TW

Tem

p

CU

PR

ES

SA

CE

AE

Juni

peru

s ph

oeni

cea

Ory

ctol

agus

cun

icul

usLe

porid

ae–

–M

uñoz

Rei

noso

(19

93)

FS

SS

Tem

p

CY

CLA

NT

HA

CE

AE

Ludo

via

lanc

ifolia

Alo

uatta

sen

icul

usC

ebid

ae0

–Ju

lliot

(19

96)

FS

HW

Trop

EB

EN

AC

EA

ED

iosp

yros

con

sola

tae

Oto

lem

ur g

arne

ttiG

alag

onid

ae+

Eng

el (

1997

)F

MT

WTr

opD

iosp

yros

mes

pilif

orm

isP

apio

anu

bis

Cer

copi

thec

idae

0+Li

eber

man

et a

l.(1

979)

FL

TS

WTr

opD

iosp

yros

sp.

Loxo

dont

a af

rican

aE

leph

antid

ae+

Lieb

erm

an e

t al.

(198

7)F

LT

WTr

op

ER

ICA

CE

AE

Vac

cini

um o

valif

oliu

mM

arte

s am

eric

ana

Mus

telid

ae0

Hic

key

et a

l. (in

pre

ss)

FS

SW

Tem

pV

acci

nium

ala

skae

nse

Mar

tes

amer

ican

aM

uste

lidae

+H

icke

y et

al.

(in p

ress

),

FS

SW

Tem

pon

ly in

old

gro

wth

V

acci

nium

ala

skae

nse,

Urs

us a

mer

ican

usU

rsid

ae00

Trav

eset

& W

illso

n (1

997)

F

SS

WTe

mp

V. o

valif

oliu

mV

acci

nium

ala

skae

nse,

Urs

us a

rcto

sU

rsid

ae00

Trav

eset

& W

illso

n (1

997)

F

SS

WTe

mp

V. o

valif

oliu

mV

acci

nium

sp.

Per

omys

cus

man

icul

atus

Mur

idae

–K

refti

ng &

Roe

(19

49)

FS

SW

Tem

pV

acci

nium

sp.

Eut

amia

s m

inim

usS

ciur

idae

–K

refti

ng &

Roe

(19

49)

FS

SW

Tem

pV

acci

nium

sp.

Tam

ias

stria

tus

Sci

urid

ae–

Kre

fting

& R

oe (

1949

)F

SS

WTe

mp

φ V

acci

nium

spp

.U

rsus

am

eric

anus

Urs

idae

0R

oger

s &

App

lega

te (

1983

) F

SS

WTe

mp

EU

PH

OR

BIA

CE

AE

Dry

pete

s va

riabi

lisA

loua

tta s

enic

ulus

Ceb

idae

00Ju

lliot

(19

96)

F?

?W

Trop

Sec

urin

ega

viro

saE

ryth

roce

bus

pata

sC

erco

pith

ecid

ae+

+Li

eber

man

& L

iebe

rman

(19

86)

FS

SS

GTr

opS

ecur

ineg

a vi

rosa

Pap

io a

nubi

sC

erco

pith

ecid

ae+

+Li

eber

man

et a

l.(1

979)

FS

SS

GTr

opTr

ewia

nud

iflor

aR

hino

cero

s un

icor

nis

Rhi

noce

ront

idae

00D

iner

stei

n &

Wem

mer

(19

88)

FM

TW

Trop

FLA

CO

UR

TIA

CE

AE

Fla

cour

tia fl

aves

cens

Ery

thro

cebu

s pa

tas

Cer

copi

thec

idae

– –

Lieb

erm

an &

Lie

berm

an (

1986

)F

MS

SW

Trop

LAU

RA

CE

AE

φ C

rypt

ocar

ya a

lba

Dus

icyo

n cu

lpae

usC

anid

ae+

+B

usta

man

te e

t al.

(199

2, 1

993)

FL

TW

Tem

p

LEG

UM

INO

SA

EA

caci

a ca

ven

Bos

taur

us

Bov

idae

, +

Gut

iérr

ez &

Arm

esto

(19

81)

DM

ST

GTe

mp

Equ

us c

abal

lus

Equ

idae

Aca

cia

radd

iana

Gaz

elle

dor

cas

Bov

idae

++

Hal

evy

(197

4)D

MS

TG

Tem

pE

nter

olob

ium

cyc

loca

rpum

Equ

us c

abal

lus

Equ

idae

0Ja

nzen

(19

81)

DL

TG

Trop

Ent

erol

obiu

m c

yclo

carp

umH

omo

sapi

ens

Hom

inid

ae0

Hun

ter

(198

9)D

LT

GTr

opR

etam

a ra

etam

Lepu

s ss

p.Le

porid

ae00

Izha

ki &

Ne’

eman

(19

97)

DM

SG

Tem

p

188 A. Traveset

Ap

pen

dix

. (co

ntin

ued)

.

Pla

nt s

pec

ies

Dis

per

ser

spec

ies

Dis

per

ser

Eff

ect

Ref

eren

ceF

ruit

See

dL

ife

Hab

itat

Zo

ne

(FA

MIL

Y)

fam

ilyty

pe

size

form


LILI

AC

EA

ES

trep

topu

s am

plex

ifoliu

sU

rsus

am

eric

anus

Urs

idae

00Tr

aves

et &

Will

son

(199

7)

FS

HW

Tem

pS

trep

topu

s am

plex

ifoliu

sU

rsus

arc

tos

Urs

idae

00Tr

aves

et &

Will

son

(199

7)

FS

HW

Tem

p

ME

LAS

TO

MA

TAC

EA

EM

icon

ia c

inna

mom

ifolia

Cal

lithr

ix p

enic

illat

aC

allit

hric

idae

0F

igue

iredo

& L

onga

tti (

1997

) F

ST

WTr

opM

icon

ia c

inna

mom

ifolia

Alo

uatta

fusc

a ss

p. fu

sca

Ceb

idae

–F

igue

iredo

& L

onga

tti (

1997

) F

ST

WTr

opM

ourir

i cra

ssifo

liaA

loua

tta s

enic

ulus

Ceb

idae

+0

Julli

ot (

1996

)F

ST

WTr

op

ME

LIA

CE

AE

Aza

dira

chta

indi

caE

ryth

roce

bus

pata

sC

erco

pith

ecid

ae+

0Li

eber

man

& L

iebe

rman

(19

86)

FL

TS

GTr

opA

zadi

rach

ta in

dica

Pap

io a

nubi

s C

erco

pith

ecid

ae+

+Li

eber

man

et a

l. (1

979)

FL

TS

GTr

op

MO

RA

CE

AE

Bag

assa

gui

anen

sis

Alo

uatta

sen

icul

usC

ebid

ae+

0Ju

lliot

(19

96)

F?

TW

Trop

Bro

sim

um a

licas

trum

Alo

uatta

pal

liata

Ceb

idae

0E

stra

da &

Coa

tes-

Est

rada

(198

6)F

LT

WTr

opF

icus

eno

rmis

Alo

uatta

fusc

aC

ebid

ae+

Fig

ueire

do (

1993

)F

ST

WTr

opF

icus

insi

pida

ssp

. sca

bra

Alo

uatta

sen

icul

usC

ebid

ae–

0Ju

lliot

(19

96)

FS

TW

Trop

Fic

us s

p.A

loua

tta p

allia

taC

ebid

ae+

Est

rada

& C

oate

s-E

stra

da (1

986)

FS

TW

Trop

Myr

iant

hus

hols

tiiP

an tr

oglo

dyte

sP

ongi

dae

+Ta

kasa

ki (

1983

)F

LT

WTr

op

MY

RIS

TIC

AC

EA

EP

ycna

nthu

s an

gole

nsis

Loxo

dont

a af

rican

aE

leph

antid

ae+

Lieb

erm

an e

t al.

(198

7)D

LT

WTr

opP

ycna

nthu

s an

gole

nsis

Pan

trog

lody

tes

Pon

gida

e+

Taka

saki

(19

83)

DL

TW

Trop

Viro

la m

iche

liiA

loua

tta s

enic

ulus

Ceb

idae

00Ju

lliot

(19

96)

FL

TW

Trop

OLA

CA

CE

AE

Min

quar

tia g

uian

ensi

sA

loua

tta s

enic

ulus

Ceb

idae

– 0

Julli

ot (

1996

)F

??

WTr

op

PA

ND

AC

EA

EP

anda

ole

osa

Loxo

dont

a af

rican

aE

leph

antid

ae0

Lieb

erm

an e

t al.

(198

7)F

LT

WTr

op

PO

AC

EA

EB

uchl

oe d

acty

loid

esB

os ta

urus

B

ovid

ae+

+Q

uinn

et a

l.(1

994)

DS

HG

Tem

p

PO

LYG

ALA

CE

AE

Mou

tabe

a gu

iane

nsis

Alo

uatta

sen

icul

usC

ebid

ae–

0Ju

lliot

(19

96)

F?

?W

Trop

QU

INA

CE

AE

Qui

ina

obov

ata

Alo

uatta

sen

icul

usC

ebid

ae+

+Ju

lliot

(19

96)

F?

TW

Trop

RO

SA

CE

AE

Am

elan

chie

r sp

.U

rsus

am

eric

anus

Urs

idae

+R

oger

s &

App

lega

te (

1983

) F

SS

TW

Tem

pC

rata

egus

mon

ogyn

aTr

icho

suru

s vu

lpec

ula

Pot

oroi

dae

0B

ass

(199

0), o

nly

viab

ility

test

edF

MS

WTe

mp

Pru

nus

penn

sylv

anic

usU

rsus

am

eric

anus

Urs

idae

0R

oger

s &

App

lega

te (

1983

) F

MT

WTe

mp

Pru

nus

virg

inia

naU

rsus

am

eric

anus

Urs

idae

+R

oger

s &

App

lega

te (

1983

) F

MT

WTe

mp

Rub

us id

aeus

Per

omys

cus

man

icul

atus

Mur

idae

–K

refti

ng &

Roe

(19

49)

FS

SW

Tem

pR

ubus

idae

usE

utam

ias

min

imus

Sci

urid

ae–

Kre

fting

& R

oe (

1949

)F

SS

WTe

mp

Rub

us id

aeus

Tam

ias

stria

tus

Sci

urid

ae–

Kre

fting

& R

oe (

1949

)F

SS

WTe

mp

Rub

us p

roce

rus

Vul

pes

vulp

esC

anid

ae0

Bru

nner

et a

l. (1

976)

FS

SS

WTe

mp

Rub

us s

pect

abili

sU

rsus

am

eric

anus

Urs

idae

0+Tr

aves

et &

Will

son

(199

7)

FS

SW

Tem

pR

ubus

spe

ctab

ilis

Urs

us a

rcto

sU

rsid

ae0+

Trav

eset

& W

illso

n (1

997)

F

SS

WTe

mp

Rub

us s

trig

osus

Urs

us a

mer

ican

usU

rsid

ae+

Rog

ers

& A

pple

gate

(19

83)

FS

SW

Tem

p

RU

BIA

CE

AE

Nau

clea

latif

olia

Pap

io a

nubi

sC

erco

pith

ecid

ae+

+Li

eber

man

et a

l. (1

979)

FS

ST

GTr

opP

loca

ma

pend

ula

Ory

ctol

agus

cun

icul

usLe

porid

ae–

–N

ogal

es e

t al.

(199

5)F

SS

STe

mp

Psy

chot

riacf

.car

thag

inen

sis

Alo

uatta

sen

icul

usC

ebid

ae–

0Ju

lliot

(19

96)

FS

?S

?W

Trop

RU

TAC

EA

EC

laus

ena

anis

ata

Ery

thro

cebu

s pa

tas

Cer

copi

thec

idae

– –

Lieb

erm

an &

Lie

berm

an (

1986

)F

M?

SS

Trop

SA

PO

TAC

EA

EC

hrys

ophy

llum

luce

ntifo

lium

Alo

uatta

sen

icul

usC

ebid

ae00

Julli

ot (

1996

)F

LT

WTr

opC

hrys

ophy

llum

prie

urii

Alo

uatta

sen

icul

usC

ebid

ae–

0Ju

lliot

(19

96)

FL

TW

Trop

SA

XIF

RA

GA

CE

AE

Rib

es b

ract

eosu

mU

rsus

am

eric

anus

Urs

idae

00Tr

aves

et &

Will

son

(199

7)

FS

SW

Tem

pR

ibes

bra

cteo

sum

Urs

us a

rcto

sU

rsid

ae00

Trav

eset

& W

illso

n (1

997)

F

SS

WTe

mp

SO

LAN

AC

EA

ES

olan

um ly

coca

rpum

Chr

ysoc

yon

brac

hyur

usC

anid

ae+

Lom

bard

i & M

otta

(19

93)

FM

SS

Trop

Sol

anum

sp.

Alo

uatta

sen

icul

usC

ebid

ae00

Julli

ot (

1996

)F

S?

?W

Trop

UM

BE

LLIF

ER

AE

Her

acle

um la

natu

mU

rsus

arc

tos

Urs

idae

+A

pple

gate

et a

l.(1

979)

DM

HW

Tem

p

VE

RB

EN

AC

EA

EP

rem

na q

uadr

ifolia

Ery

thro

cebu

s pa

tas

Cer

copi

thec

idae

0+Li

eber

man

& L

iebe

rman

(19

86)

FS

SS

WTr

op

190 A. Traveset

Ap

pen

dix

. (co

ntin

ued)

.

Pla

nt s

pec

ies

Dis

per

ser

spec

ies

Dis

per

ser

Eff

ect

Ref

eren

ceF

ruit

See

dL

ife

Hab

itat

Zo

ne

(FA

MIL

Y)

fam

ilyty

pe

size

form

Documents

Effect of seed passage through vertebrate frugivores ...imedea.uib-csic.es/icg/ecol_terr/all pdfs/1998_Traveset_PPES_review… · Effect of seed passage through vertebrate frugivores’