Palm Pollination by Bees, Beetles and Flies: Why Pollinator Taxonomy Does Not Matter. the Case of Hyospathe Elegans (Arecaceae

Plant Species Biology (2001) 16, 165–181

Palm pollination by bees, beetles and ﬂies: Why pollinator taxonomy does not matter. The case of Hyospathe elegans (Arecaceae, Arecoidae, Areceae, Euterpeinae)

CHRISTIAN LISTABARTH Konrad-Lorenz-Institut für vergleichende Verhaltensforschung (KLIVV), Austrian Academy of Sciences, Savoyenstrasse 1A, A–1160 Vienna, Austria

Abstract

The concept of adaptation-based pollination syndromes in which systematically bounded groups of pollinators service a particular host species has been applied to the palms. Except for beetle pollinated species, many palms lack major anthecological adaptations that apparently promote visits of a particular taxonomic group of insects. To address the question whether these palms have evolved insect-specific pollination systems, the interaction of the monoecious, protandrous palm Hyospathe elegans Mart. and visiting insects was studied in Amazonian Peru during an entire flowering period. At least 27 taxa of the orders Coleoptera, Hymenoptera and Diptera were recorded regularly visiting both types of flowers. To test whether flower visitation is taxonomically skewed, two sets of visitor samples from staminate and pistillate flowers were compared. There is no evidence to support the working hypothesis that there is a single optimal pollinator or a systematically bounded group of principal pollinators, based on the frequency of visits or the relative dominance within the visitor spectrum. Visitation rates suggest a mixed-species guild of nectar-feeding insects to be the commonest and most dependable pollinator group, along with an analogous guild of generalist-feeding copollinators. Hyospathe elegans and closely related species of Euterpe and Prestoea show common traits in their interaction with pollinators, such as phenological pattern, flowering behavior and allocation of rewards, and they also share a corresponding feeding guild. Given a preponderance of low taxonomic pollinator specificity in palm reproductive systems, pollination by a mixed-species guild may be widespread and the classification of ‘mellitophilous’ and ‘myophilous’ palms should be reconsidered. Keywords: adaptation, Euterpe, insect–plant interactions, mixed species guild, palms, pollination syndrome, pollinator specificity, Prestoea, temporal dioecism Received 15 October 2000; revision received 5 March 2001; accepted 20 March 2001

Introduction perform pollination services constantly, reliably and effec- tively (Stebbins 1970). Beneficial visitors should move Floral adaptation to attract and reward pollinators is an frequently between flowers of conspecifics, be capable of important issue of reproductive success in animal- travelling the inter-individual distances between plants pollinated plants (Faegri & van der Pijl 1979; Grant 1994; and of transferring large amounts of pollen, and they Waser et al. 1996; Wilson & Thomson 1996). As floral vis- should exploit the resources modestly, leaving the flower itors vary in their benefits to plants, natural selection attractive for further visitors. Emphasis on the adap- should favor floral traits that attract those visitors that tive significance of floral traits in relation to specialized pollinator types launched the concept of pollination Correspondence: Christian Listabarth syndromes. In this concept, flowers are sufficiently Email: [email protected] specialized for pollination by particular animal types for

© 2001 The Society for the Study of Species Biology 166 C. LISTABARTH there to be recognizable convergent suites of floral traits, 1992b, 1996; Bernal & Ervik 1996; Küchmeister et al. 1998), which, together with the presumably specialized pollina- which has also been clearly pointed out by Tomlinson tors, constitute ‘pollination syndromes’ (Percival 1965; (1990). Even so, the focus of many pollination studies in Baker & Hurd 1968; Faegri & van der Pijl 1979). the palms has been the association of a particular species Flowers are clear adaptations to facilitate sexual repro- with one of the syndromes (e.g., Ervik & Bernal 1996; duction. Indeed, there are specialized flowers that show Ervik & Feil 1997). adaptations to a particular mutualist taxon, but there is The Euterpeinae are a neotropical subtribe of the increasing debate on whether floral specialization may be Areceae comprising five monophyletic genera (Hender- entirely explained by adaptations to particular pollinators son & Galeano 1996; Henderson 1999). Euterpe is basal to (references in Herrera 1996; Wilson & Thomson 1996). all other genera of the subtribe. Hyospathe is sister to Simultaneously, there is overwhelming evidence suggest- Neonicholsonia, and to both Prestoea and Oenocarpus. ing that, at the least, insect–plant interactions are taxon- Within this subtribe the genera Euterpe, Prestoea and specific and that in many (if not most) plants, the level Oenocarpus have been extensively studied in regard to of specialization on individual pollinator species is pollination (Henderson & Galeano 1996 and references extremely low (Howe 1984; Roubik 1992; Bronstein 1994; therein; Ervik & Bernal 1996; Ervik & Feil 1997; Thompson 1994; Proctor et al. 1996; Travis 1996; Waser Küchmeister et al. 1997, 1998). There is scant and only et al. 1996). Plant species often employ a variety of polli- anecdotal information on pollination ecology for the com- nating agents from different orders and their pollination mon understorey palm Hyospathe elegans Mart. (Hender- systems are more generalized and dynamic than tradi- son 1986; Skov & Balslev 1989; Ervik & Feil 1997), and tional concepts have suggested (Erhardt 1993; Fishbein & virtually nothing is known about pollination in the mono- Venable 1996; Lippok & Renner 1997; Ollerton & Liede specific genus Neonicholsonia. The most derived genus 1997). In many flowers there is a mismatch of predicted Oenocarpus differs from all other genera in inflorescence and observed pollinators in that a wide array of visitors morphology (Balick 1986; Henderson & Galeano 1996) serve as pollen vectors and the relative contribution to and shows a specialized cantharophilous pollination pollination depends on individual pollination capacity, system that involves pollinator reproduction in the local species composition, reliable abundances and flowers (García 1988; Küchmeister et al. 1998). alternative sources rather than on floral traits of the host There is considerable information on pollination for (Schemske & Horvitz 1984; Herrera 1987; Thompson 1999; species of the genera Euterpe and Prestoea, which rely on Lippok et al. 2000). Additionally, individual pollinator insect pollen vectors and are visited by a large spectrum taxa can vary significantly in their relative contribution to of insects. The conclusions on pollination in each of the pollination of a given plant taxon in both space and time palms differ as to the assignment of systematic groups of (Herrera 1988; Pellmyr & Thompson 1996; Mahy et al. insects that supposedly act as principal pollinators. For 1998). Waser et al. (1996) point out that although behav- example, beetles (and halictid bees) in Euterpe precatoria ioral, morphological, and physiological constraints in Mart., halictid bees (and meliponine bees and small flies) most plant–pollinator associations exist, these constraints in Prestoea decurrens (H. Wendl. ex Burret) H. E. Moore, are rarely strong enough to restrict the interaction to a and syrphid flies (and halictid bees) in Prestoea schultzeana single (or even a few) mutualist species. They conclude (Burret) H. E. Moore, are the alleged vectors with most that ‘generalization in pollination systems appears to be impact on pollination (Ervik & Bernal 1996; Ervik & Feil the rule rather than the exception’ for the majority of 1997; Küchmeister et al. 1997). Despite the range of pollen plants in both temporal and tropical regions. vectors that are considered to be relevant, most conclu- The concept of pollination syndromes has been applied sions on the pollination of Euterpe and Prestoea convey the to the palms (Henderson 1986, 1995). Except for the rather view that systematic groups of insects at the level of fami- uncommon cases of anemophily or the combination of lies and/or orders were intimately associated with these abiotic and biotic pollination (e.g. Read 1975; Anderson palms (Bovi et al. 1994; Ervik & Bernal 1996; Henderson & et al. 1988; Listabarth 1992a), entomophily is generally Galeano 1996; Ervik & Feil 1997). However, there is only recognized to occur in the palms. Henderson (1986) dis- meagre evidence in any of these studies to support the tinguishes three entomophilous pollination syndromes assertion that pollinators are indeed specific, and there is that prevail in palms: (i) cantharophily (beetle pollina- even less indication on how the palms are specialized tion); (ii) mellitophily (bee pollination); and (iii) myophily to attract a particular systematic pollinator group. (fly pollination). However, the palms do not exhibit major This raises the question of what constitutes acceptable morphological specializations of their flowers (Uhl & evidence to demonstrate pollinator specificity in a palm Dransfield 1987) and there is a lack of sufficient evidence species, and whether adaptive specialization on specific for specialization to pollinators of any insect order except pollinator types (in palms that are visited by a diverse for beetles (Syed 1979; Burquez et al. 1987; Listabarth visitor spectrum) may reasonably be expected at all.

Here, I report on the reproductive structures (inflores- Mart., G. cuneata var. gracilis (H. Wendl. ex Spruce) Skov, cences, flowers and fruit) and the reproductive process and juveniles of the subcanopy–canopy species dominate (phenology, anthesis, flower visitors and fruit-set) of the the understorey vegetation. The riverine forest has a tropical palm Hyospathe elegans Mart. in a Peruvian rain much lower canopy and is much less diverse. A few forest. This paper contains the results of a continuous species constitute a relatively open canopy layer, includ- study focusing on the insect visitation to H. elegans in a ing species of Cecropia, Ochroma, Erythrina, and the palms natural population during an entire flowering period. The A. murumuru, Iriartea deltoidea Ruiz & Pav. and Socratea main objective of this study was to determine whether the exorrhiza (Mart.) H. Wendl. Monocot species predo- palm shows particular adaptations to specific insect minate in the understorey (Zingiberaceae, Cyclanthaceae, pollinators, and whether pollinator specialization in this Araceae and Arecaceae). Among palms, Phytelephas interaction can reliably be traced by the visitation pattern macrocarpa Ruiz & Pav., Geonoma cuneata var. gracilis, of these insects by measuring the frequency of occurence Chamaedorea pinnatifrons (Jacq.) Oerst., and H. elegans are for each flower visiting taxon, systematic group of taxa common. (order) and functional unit (guild). In essence: which pollination syndrome, if any, fits for H. elegans? Specifically, Hyospathe elegans I have been studying the degree to which H. elegans flowers attract different suites of insects addressing the Hyospathe is a small genus in the neotropical subtribe following questions: Euterpeinae. In a recent revision based on morphological and biometrical characters, Skov & Balslev (1989) delim- 1. Are flowers generalists in terms of attracting a wide ited two species, H. elegans and Hyospathe macrorhachis disparity of visitors and which visitor taxa habitually Burret, which is narrowly distributed in Eastern Andean visit the inflorescences? Ecuador. Hyospathe elegans ranks among the most widely 2. Do particular insect taxa visit staminate and pistillate distributed neotropical palm species, ranging from phase inflorescences in similar frequencies? Panama throughout tropical South America (Skov & 3. Are pooled insect groups found in similar frequencies Balslev 1989; Henderson et al. 1995). It is a remarkably on both staminate and pistillate inflorescences? variable species with 30 major morphological forms that 4. Which (if any) are the characteristic proportions of differ in habit, size, shape of leaves, and dimensions of pooled visitor groups and do any of these groups have inflorescence and flowers, and different morphological a major impact on pollination? forms occur sympatrically and/or allopatrically within Finally, I will compare the pollination of H. elegans with the species range (Skov & Balslev 1989). In the Peruvian the pollination of closely related species of Euterpe and study site, H. elegans occured in both habitats, the terra Prestoea. firme forest and the riverine forest. Within two 1 ha plots H. elegans was found in clusters of three individuals per ha within a terra firme plot, while eight clusters per ha Materials and methods occured in a plot of the riverine forest. Hyospathe elegans is a slender, cespitose palm, up to 3 m in height. Clones Study site of up to five stems were found in both habitats. The leaves The study was conducted in 1989 in a tropical moist of the individuals of this population were trijugate and broadleaf forest in Western Amazonian Peru, Departa- other morphological traits were consistent within the mento Huánuco, near the junction of the Pachitea and population. Moreover, in terms of habit, flowering phe- Llullapichis Rivers (9°37¢S, 74°56¢W; elevation 260 m) in nology, flowering behavior and insect visitation, the the Ucayali moist forest ecoregion (Dinerstein et al. 1995). palms did not differ between the two habitats, and thus This is an evergreen seasonal forest with a pronounced the data of both forests comprise a single database for this dry season from June to August. More information about study. Hyospathe elegans was collected under no. 12–10589 local settings of the study area, particularly on climate and vouchers are deposited at AAU, NY, USM, WU and vegetation, can be found in Hutterer et al. (1995) and and W. The specimens were identified by A. Henderson Rainer (1995). Hyospathe elegans was studied in two habi- (NY). Palm taxonomy follows Henderson et al. (1995), and tats, the primary terra firme lowland rain forest, and the the species names originally used in the literature are contiguous riverine forest. given in parentheses when mentioned for the first time. Trees in the terra firme forest reach 30–40 m in height, and typical species of palms in the canopy include Data collection and analyses Astrocaryum murumuru Mart., Euterpe precatoria Mart. and Oenocarpus bataua Mart.. Oenocarpus mapora H. Karst. is Two study plots, 1 ha each of both forests, were set up conspicuous in the subcanopy. Geonoma macrostachys by designing a 100 ¥ 100 m plot from a randomly chosen

© 2001 The Society for the Study of Species Biology Plant Species Biology, 16, 165–181 168 C. LISTABARTH individual of H. elegans to the directions east and north. recorded on staminate and pistillate samples, I used a c2 Within these two plots, all individuals were tagged and contingency table, and if this test was not applicable, the all inflorescences produced during the flowering period Fisher’s exact probability test. Comparisons of pooled were checked daily to record flowering status, and to insect groups (orders or guilds) were carried out with the observe flowering behavior and insect visitation. Five absolute numbers of taxonomic units recorded per pooled inflorescences from different, randomly chosen indivi- group and sample. I used two-tailed Mann–Whitney U- duals were studied in detail as follows. To estimate the tests to compare the representation of pooled groups number of flowers per inflorescence, flowerbuds of one from staminate and pistillate samples, and two-tailed basal, central and terminal rachilla (flowering branch) Spearman Rank Correlation (rs) to test for the relationship were counted. The mean number of flowers per rachilla between visitor proportions. was then multiplied by the number of rachillae. To derive information on the intensity of flowering within an individual inflorescence, the flowers reaching anthesis per Results day were counted. To depict flowering intensity of single Inflorescence development and morphology inflorescences, these numbers were transformed to the percentage of flowers starting anthesis per day relative to Stems often produced inflorescences subsequently on the total of flowers per inflorescence. each node. However, between the remains of the previ- To survey flowering traits, and insect visitor behavior, ous year’s inflorescences and the newly produced inflo- activity and abundance, direct observations (14 units of rescence, one or two sterile nodes were found in 54% of 3 h each) were performed at least twice for each of the five the stems that produced inflorescences (N = 12), indicat- inflorescences, for a total of nine units during staminate ing that individual stems do not necessarily flower each anthesis, and five during pistillate anthesis. During the year. One or two subsequent inflorescences were borne pistillate phase, observations were also carried out for 15 per stem and flowering season. The inflorescence buds min each hour (17.00–06.00) during two nights. Total time started to expand approximately 50 days before anthesis, of behavioral observations and insect activity and abun- but remained sheathed by the subtending leafsheath until dance estimates totalled 49 h. 2 weeks before anthesis. They then tended to spread abax- To accumulate a representative sample set of visitors ially and so detached a leaf, which was shed during the (presence/absence data), 54 recording units were carried process. Inflorescences then continued to incline abaxially out on inflorescences of the test population on clear days (up to a 60° angle) and increased slightly in diameter. The during high insect activity (10.00–11.30), documenting all inflorescence bud was enclosed in the then drying pro- insects observed on the inflorescence and flowers during phyll and the first, purplish-brown peduncular bract. A a 15 min period. These records comprise 32 units of obser- mature bud was 35–44 cm long (38.79 ± 2.44 cm; N = 19) vation on staminate phase inflorescences, and 22 units with a diameter of 12–15 mm (13.68 ± 0.86 mm; N = 19). during the pistillate phase, yielding a total of 13.5 h of The inflorescence bud opened in daylight via an abaxial sampling. Insects recorded in these two sample sets were slit of the first peduncular bract and released the inflo- analyzed for relative representations of single-visitor rescence. Immediately, or within the next day, the pro- species or pooled units. The frequency of occurence of phyll and the bract (which has a smooth, shiny white single-visitor taxa is given as the percentage of records for inner surface) were shed. The inflorescence was branched each set of samples. to one order. The peduncle, rachis, rachillae and flower To determine whether H. elegans relies on insect pollen buds were cream or light green colored. Upon release vectors, gauze sleeves (mesh width 1 mm) were placed from the bract, the rachillae began to spread and stiffen, on single rachillae to exclude all insect visitors. These and reached their final positions within the next 3 days. sleeves, however, did not exclude airborne pollen. The Basal rachillae were spread approximately 80° from the rachillae were bagged prior to pistillate anthesis and were inflorescence axis, but this angle decreased continuously left bagged throughout this phase. Other rachillae of the to less than 5° at the apex. same inflorescences served as untreated controls. All The 15–20 spirally arranged rachillae were 18–30 cm flowers from bagged and untreated rachillae were subse- long and bore widely spaced triads throughout, except for quently checked for fruit-set. Pollination success in the very tips that bore paired or single staminate flowers. H. elegans was measured by fruit-set 2 weeks after flower- In five inflorescences, the calculated mean number ing (nonfertilized flowers initially developed, but then of flowers per inflorescence was 4395 ± 589 for stami- aborted during the second week). Production of mature nate flowers and 2072 ± 295 for pistillate flowers. This fruit was counted in these rachillae. results in a mean sex ratio (male : female flowers) of near All average values are presented as the mean ± SD. For 2 : 1 ([2.12 ± 0.02] : 1). The counts of flowers at anthesis comparing the frequency of individual taxonomic units matched these results with only slight differences;

© 2001 The Society for the Study of Species Biology Plant Species Biology, 16, 165–181 PALM POLLINATION BY A MIXED-SPECIES GUILD 169 calculated values ranged from 92% to 107% for the anthesis of an inflorescence lasted from 10 to 14 days (12.1 counted values of staminate flowers, and from 94% to ± 1.2 days; N = 19), followed by a non-sexual phase of 2–6 103% for the pistillate flowers. In two out of 19 inflores- days (3.6 ± 1.0 days; N = 19), and finally the pistillate phase cences (11%), the rachillae bore pairs of pistillate flowers of 3–7 days (5.3 ± 1.0 days; N = 19). During staminate and in their proximal triads. Both pistillate flowers were func- pistillate phases, the number of flowers produced each tional, flowered asynchronously and could develop into day was variable, and highest near the middle of each mature fruit. Therefore, the number of pistillate flowers phase. No major difference in the course of flowering in those inflorescences increased for about 25% and sex between inflorescences was observed (Fig. 2). Notably, ratio decreased to 1.8 : 1. during the central staminate phase a considerable amount The most conspicuous event after bract fall was the of flowers were at anthesis each day, and during the growth of the flower buds. At bract release, one staminate pistillate phase, up to 80% of the pistillate flowers were flower of each triad was always more developed than the receptive simultaneously (longevity of the pistillate other. In staminate flower buds, the pedicel and the bud flowers was approximately 2 days and flowers remained itself increased in length. Flower buds remained cream receptive for that period). This resulted in an extraordi- colored until anthesis. Mature staminate flowers of this nary peak of receptive pistillate flowers over a 3–4 day population were pedicellate, with fused sepals and three period, in which a substantial number of flowers occured free petals, which enclosed a prominent pistillode bearing in anthesis to attract pollinators (Fig. 2). There was no the six stamens. The pistillate flowers increased to twice overlap of sexual phases within any particular inflores- their size from bract release until anthesis, and changed cence, but overlap between inflorescences of a genet color from cream to green. Mature pistillate flowers in this (cluster) occured in as much as 58% (N = 19), of which 32% population were 3 mm in diameter, sessile, with a fused accounted for overlap within a single stem, and 26% calyx and three imbricate green petals, enclosing the pistil within different stems of a cluster. A large percentage before anthesis. (45%) of the intraindividual overlap was minor, that is, it occured during weak flowering intensity of both flowering phases. Flowering phenology Flowering of the population of H. elegans lasted from mid- March until early June. The mean number of flowering inflorescences for each sexual phase is given in Fig. 1 (N = 19 inflorescences from 12 stems in 7 clusters). Flower- ing was highly synchronous within the population and peaked during April and May (wet–dry season transition). Overall flowering (percentage of individuals that produced inflorescences during the flowering period) was 64% (N = 11 clusters) in this population. Inflores- cences were protandrous, and the duration of staminate Mean no. inflorescences per day

Fig. 2 Relative flowering intensity of five randomly chosen Fig. 1 Flowering phenology of Hyospathe elegans. Mean num- inflorescences of Hyospathe elegans. Bars express the percentage ber of staminate () and pistillate () phase inflorescences per of flowers that started anthesis a day. Note that absolute flower- day plotted for the flowering period from March to early June ing intensity during pistillate anthesis would be cumulative, in weekly intervals. The population is represented by seven because the time of receptivity is 2 days. Inflorescences are flowering individuals that produced a total of 19 inflorescences. arranged in decreasing overall duration of their flowering cycles.

Flowering behavior sis, the growth of the young fruit became measurable, and the length of the extremely asymmetric triangular-shaped In 58% (N = 19) of the inflorescences, the onset of stami- fruit was 4 mm. Two weeks after anthesis, fruit were up nate anthesis began the same day after the bract had to 9 mm long, and only 3 mm in diameter. Four-week-old opened. In the other cases, staminate anthesis started the fruit were small, ellipsoid and appeared almost sym- next day. Individual staminate flowers usually opened in metrical except for the basal stigmatic remain. Such fruits the morning between 06.00 and 08.00. Petals spread and were 14–15 mm long and 4–5 mm in diameter. During the bend back, releasing the erect pistillode and the stamens, next 6 weeks, fruit diameter continued to increase, while which are exposed in two planes. Onset of staminate its length decreased slightly until fruit were 12–13 mm anthesis, as defined by dehiscence of the anthers, occured long with a diameter of 6–7 mm, and olive green. Fruits from 07.00 to 10.00. As soon as the petals had spread, the were apparently mature then, and the endosperm pistillode started to produce a clear substance, and its was already hard. However, the fruit did undergo surface appeared shiny. When anthers started to dehisce, another color change to purple and black during the final an intense sweet scent was emitted. Anthers curled up ripening process. This latter phase took another 3 weeks, and appeared head-like at the end of the spread filaments, and was accompanied by the coloring of the inflorescence presenting pollen. Scent production and secretion of the axes (peduncle, rachis and rachillae) to purple. Fruits floral exudate continued during the first hours of anthe- were either harvested (absent the next day) or they sis until noon, but then stopped during the afternoon. In dropped to the ground, but sometimes dried on the late afternoon or early night staminate flowers abscised rachillae (especially late fruit that ripened during the dry from the inflorescence and decayed rapidly. The opening season). of flowers and dehiscence of anthers was seemingly asso- Bagging (exclosure of insect-mediated pollen) of three ciated with weather conditions. On cloudy and especially rachillae each from three inflorescences (N = 9 rachillae) on rainy days, petal opening and anther dehiscence was did not initially influence fruit development, and there delayed 6–8 h. On extremely wet days, although petals was 100% fruit-set after 1 week. During the second week, had opened, the anthers remained closed and the flowers fruit aborted but showed normal fruit development until dropped during the following night without ever having they dropped. The abortion rate was 100% in all bagged been functional. rachillae. Controls (N = 9 rachillae, three untreated When all staminate flowers had finished anthesis, rachillae each from the same three individuals) showed the petals of the pistillate flowers began to spread fruit-set of 100% after the first week, and 0–80% after during the non-sexual phase. Once the petals had com- 2 weeks. Four rachillae did not produce mature fruit at all: pletely opened, the stigmatic lobes protruded within the one aborted all fruits within the second week, and three next 36–48 h, but remained closed. Pistillate anthesis were on an inflorescence that was preyed upon by leaf started when the stigmatic lobes unfolded. Pistillate cutter ants in the third week of fruit development. In the anthesis occured at all times of the day, but most other five rachillae, the output of mature fruit ranged flowers opened stigmatic lobes in the early morning. from 5% to 35%. A liquid film immediately covered stigmas, and the secretion of stigmatic liquid continued during the time of receptivity, although production of this liquid Insect visitation decreased during the second day. During the first day of Visitor spectrum. A broad spectrum of visitors was anthesis, a droplet that covered the free stigmatic lobes attracted to H. elegans, especially from the orders was sometimes formed. About 48 h after stigmas had Hymenoptera, Coleoptera and Diptera (Table 1). The unfolded they changed from hyaline to white, dried com- spectrum of visitors ranged from pollen collecting bees to pletely, and turned brown within the next 12 h. A weak, pollen feeding beetles and flies, tissue feeding beetles, but perceptible scent was produced during pistillate liquid licking bees, wasps, ants, beetles and dipterans. anthesis. Weevils, other beetles, and drosophilid flies were observed to mate but none of these insects was exclusively attracted for mating, nor was oviposition into Postfloral events flowers observed. It is worthwhile to mention the com- Within the first 4 days after anthesis, the pistillate flowers plete absence of parasitic chalcidoid wasps, which para- displayed a conspicuous transformation, but no mea- sitise those insects that reproduce in flowers and are surable growth. Stigmas turned dark brown and the normally found when insect reproduction in flowers pistil changed color to green. When one of the three occurs (Listabarth 1996). Rove beetles and ants preyed carpels had begun to develop, the initially terminally upon other floral visitors. Flower-harvesting leaf cutter positioned stigma moved basally. One week after anthe- ants also visited the inflorescences.

© 2001 The Society for the Study of Species Biology Plant Species Biology, 16, 165–181 PALM POLLINATION BY A MIXED-SPECIES GUILD 171 6 phases 5 Guild 4 of visit 0.001. 3 < P 11). >> Activity cgcgcgcg lcg lcg lcg lcg l gf lfm gf l gf lfm, s gf ns fm, s gf ns prfm, s gf * fm l, (m) nf ** fm l, (m) nf ns fm l, (m) ns –fm gf ns mfm gf ns lfm gf lfm * ** lfm * l gfcg ns lfm nf lfm nf lcg ns nf lfm nf ns lfm nf ns lcg nf ns l gf ns l nf ns l nf ns l nf ns gf ns nf ns nf ns nf *** ns ns * 0.01; *** < harvesting; pr, predation. harvesting; pr, P 2 , common ( 0.05; ** +++ < P Abundance + ++ + ++ + + + + + +++ +++ +++ + + ++ + + + + + + ++ ++ + ++ +++ ++ 1 (%) , few individuals (4–10); ++ 4 of visit 3 Activity cgcgcgcg p (l)cg 0 p (l)cg – p (l)cg –––ns p (l)cg 18 p (l)cgh 64 p (l)fm 27 lfm 23 lfm, s 18 fm, s pr 27 fm, s pr p, t, l, (m)fm p, t, l, (m)fm 50 73 p, t, l, (m)fm 32 82 fm 45 p, t, m 23 fm 0 lfm lfm l 86 fm lcg l, (m)fm l 50 fm – t, l 59 cg 95 lfm 27 lfm 9 lcg 18 p, l 9 l, m – l, m 23 23 l 36 14 32 – 27 77 – ns , single individuals (1–3); + 2 Abundance + ++ ++ ++ + + + + ++ + + +++ +++ +++ + ++ ++ ++ + + + + + ++ +++ +++ +++ +++ +++ Samples from staminate phaseSamples from pistillate phase Samples from Differences 1 78 (%) Frequency Purpose Frequencybetween Purpose Frequency Purpose Hyospathe elegans sp. 6 Atta Visitors of Visitors sp. 1 25 2 spp. 66 sp. 1 69 sp. 88 Sarcophagidae: 5 spp. Sarcophagidae: Percentage of insect occurences in the sample set. of insect occurences Percentage 15 three Counts from min observation units:–, not observed; s, almost sedentary. Activity pattern defined as: cg, come and go; fm, few movements between inflorescences; Observed insect behavior defined as: p, pollen feeding or collecting; l, nectar licking; t, tissue feeding; m, mating; h, flower Guilds defined as: nf, nectar feeding; gf, generalist feeding. ns, non-significant; or significant at * in staminate and pistillate samples are: of taxon-representation Differences Table 1 Trigona 1 2 3 4 5 6 Trigona rufescens Trigona Trigona Plebeia Halictidae sp. 1Halictidae sp. 2 sp. 1Vespidae sp. 2Vespidae Formicoidea: Formicoidea: 8 spp. 28 Staphylinidae: 2 spp. 47 sp. 1Derelomini 75 sp. 2Derelomini 25 sp. 3Derelomini 88 13 Cholus Halticinae sp. 1Halticinae sp. 2 97 100 Cassidinae sp.1 3 spp.Galerucinae: 31 Elateridae: 2 spp. sp. 1Brenthidae 31 Scarabaeidae: 2 spp. 41 Culicidae: 2 spp. 22 91 Nematocera: 4 spp. 19 Phoridae sp. 1Syrphidae: 4 spp. 22 6 small flies (8 spp.) sp. 1Drosophilidae 41 31 Muscidae, Calliphoridae, 100 66 50 63 56

Among other insect orders, there were Orthopteroidea, cially appropriate way, which would have suggested an Homoptera, Lepidoptera: tissue feeding tettigoniid increased aptitude and/or probability of pollen transfer. nymphs and cockroaches (both nocturnal), sucking bugs Usually, small insects (<3 mm) contacted the stigmas with from the Membracidae, Pentatomidae, Miridae and but- their bodies and mouthparts, while larger insects com- terflies from different families, predatory Mantidae and monly contacted stigmas with their mouthparts only, Reduviidae. Thomisid spiders also were occasionally although there were exceptions. observed. These visitors were mainly recorded with Even during the first days after pistillate anthesis had frequency values below 10%. Except for the predatory finished, some visitors arrived at inflorescences that taxa, all of these visitors could be easily put into one of did not offer any reward, among them muscoid flies, the two feeding guilds (defined below). chrysomelid beetles and (rarely) the Trigona bees. Leaf Of the 29 taxonomic units scored for the orders cutter ants harvested staminate flowers in two instances, Hymenoptera, Coleoptera, and Diptera (Table 1), 27 taxo- which did not account for much damage because few ants nomic units (93%) occured on both staminate and pistil- visited the inflorescences on only one day. However, the late inflorescences. The two taxa never found on pistillate ants had a considerable impact on the population as pre- inflorescences were the Atta ants and the predatory rove dispersal seed predators, since fruit of three inflores- beetles, which are not considered along with the other ant cences (16%; N = 19) had been completely removed during taxa in the following analyses, thus 26 taxa remain for the first 4 weeks of fruit development. analysis. To avoid multiple scoring of taxa visiting inflorescences for various purposes, and to achieve a more Male versus female samples. Twenty out of the 26 taxo- general assignment applicable to both types of inflores- nomic units considered here (77%) showed higher fre- cences (if they were differently utilized), only two feeding quency values on staminate inflorescences than on guilds are identified here: (i) generalist feeders; and pistillate ones. However, in only six taxonomic units (ii) exclusive nectar feeders. Bees were ranked as genera- (23%) did the number of records during staminate phase list feeders, since they consumed pollen and nectar. differ significantly from those of the pistillate samples. Mating insects were ranked according to their feeding Another six taxa, most of them beetles and one wasp, resource, because there was no evidence for any of these revealed even higher values of visitation frequency in the insects visiting inflorescences of H. elegans primarily pistillate inflorescences, although these differences were or even exclusively for reproduction. All other taxa could not significant (Table 1). be ranked unambiguously by their foraging behavior Pooling the single taxonomic units to their respec- (Table 1). tive order or feeding guild creates a different picture, however. To test for differences between the represen- Insect activity and behavior. Most beetles, the wasps, the tation of taxa per pooled group in the sets of samples midges (Nematocera), and drosophilid and calyptrate taken during either staminate or pistillate phase, the flies were active during all phases of anthesis, while Mann–Whitney U-test (two tailed, N = 54) was used notably the bees and syrphid flies were rarely observed throughout. The number of taxonomic units represented during very early morning hours and high noon. Activ- in the staminate samples differed significantly from those ity patterns ranged from short visits (‘come and go’) to of pistillate samples for the orders Hymenoptera ‘few movements’ between inflorescences and ‘almost (z = –3.42; P < 0.001), Diptera (z = –3.64; P < 0.001), and the sedentary’ (Table 1). Bees, wasps and the majority of generalist feeding guild (z = –4.17; P < 0.001) in that sta- dipteran visitors foraged in short visits and regularly flew minate inflorescences were visited more frequently. There between the flowers of an inflorescence. Other visitors, was no significant difference in insect representation mainly the drosophilid flies and most beetle taxa, were between the sets of staminate and pistillate samples for less active (‘few movements’), often engaged in feeding the Coleoptera (z = –0.5; not significant), and the nectar and/or mating with infrequent flights even within the feeding guild (z = –1.68; P < 0.1). inflorescence. Finally, the small weevils of the Derelomini were ‘almost sedentary’, since they stayed on the Proportions of visitors. The standardized proportions of rachillae, and even if they dropped with an abscised pooled visitors, that is, the percentage of taxonomic units flower they were observed to return to the same inflores- per order or guild from the total of taxonomic units per cence. Visitation was generally high during fairly fine sample, showed little variation within each set of samples weather conditions (dry and sunny days), and extremely from both staminate and pistillate inflorescences. The poor during rainy days. All insects that were attracted to mean proportions of the 26 taxonomic units pooled pistillate phase inflorescences contacted the receptive to orders and guilds are presented in Fig. 3. The relative stigmas when foraging for floral exudates. There was no contribution of taxonomic units remained virtually con- single insect that handled flowers or stigmas in an espe- stant between single samples in both sets. The fractions

tion of rewards in both types of inflorescences tends to favor visits of mobile insects that gain small amounts of food. Apparently, the flowers neither exercise selective attraction nor limit access to rewards to any particular cat- egory of visitors. Hyospathe elegans attracts a broad spectrum of visitors that visit the flowers regularly for feeding. The rapid sequence of developing inflorescences within an individual stem or cluster may well enhance the continuity of food availability of individuals at fixed places, and anthophilous insects visit the inflorescences repeatedly. Visitation of insects to young infructescences, in which Fig. 3 Mean relative proportions of pooled visitor groups in attraction is lacking and no more reward is offered, is Hyospathe elegans from samples of staminate phase (; N = 32) and pistillate phase (; N = 22) inflorescences. Groups were sound evidence for repeated visitation of already-known pooled to insect orders: H, Hymenoptera; C, Coleoptera; D, food sources. Many visitors observed on H. elegans show Diptera; or to guilds: NF, nectar-feeding guild; GF, general- low host fidelity and are known to service several sym- feeding guild. patric species (Olesen & Balslev 1990; Listabarth 1993; Ervik & Feil 1997). The rotation of mutualists, that is, the opportunistic visitation of various hosts, coupled with of insect orders were positively correlated throughout, temporal specialization, is a commonly observed pattern demonstrating considerable consistency between not only of insect pollinators (Haber & Frankie 1989; samples. The three pairwise rank correlations between Roubik 1989, 1992; Listabarth 1996), but also vertebrate samples for the number of visitor taxa pooled to order pollinator groups (Heithaus et al. 1975; Stiles 1975, 1977; were highly significant in the pistillate samples (rs = 0.571, Sazima et al. 1999). Although the effectiveness of general- N = 22, P < 0.005 [Coleoptera, Hymenoptera]; rs = 0.649, N ist pollinators is thought to be rather low (Faegri & van = 22, P < 0.001 [Coleoptera, Diptera]; rs = 0.773, N = 22, P < der Pijl 1979; but see Herrera 1996; Waser et al. 1996), 0.001 [Hymenoptera, Diptera]), and also in the staminate insect pollen vectors account for pollination of up to 80% samples for Hymenoptera and Diptera (rs = 0.568, N = 32, of the pistillate flowers, since there was no fruit-set when P < 0.001). The two correlations in the staminate samples insect visits were deterred. Thus, insect pollen vectors for the beetles were not significant (rs = 0.104, N = 32, P < are required for sexual reproduction and there is no 0.6 [Coleoptera, Diptera]; rs = 0.332, N = 32, P < 0.07 anemophilous pollen transfer nor agamous fruit-set. [Coleoptera, Hymenoptera]). However, the high overall presence of visitors (Table 1) may explain the reproductive success of H. elegans. Discussion Despite a rather high level of pollination success, the output of mature fruit (seeds) ranged from only 5% to Pollination in Hyospathe elegans 35%. Predispersal seed predation by Atta ants, among Summarizing the floral biology leads to a likely scenario other reasons, probably accounted for the highest losses for how pollination in H. elegans takes place. A high pro- of fruit. portion of individuals in the population, which produced up to four inflorescences each, flower synchronously over Principal pollinators a period of 3 months during the wet–dry transition. As a result, there is a steady availability of flowering individ- The following interpretations are based on the two uals during the whole flowering period (Fig. 1). Inflores- assumptions: (i) that floral specialization of a host plant cences display strongly protandrous flowering (Fig. 2), has evolved under the influence of natural selection with daily pulses of short-lived, diurnal staminate exacted by the presence of a particularly efficient and flowers. The staminate phase is followed by a non- abundant pollinator (group) (Stebbins 1970; Schemske & flowering phase without any functional flowers. The pis- Horvitz 1984; Herrera 1987; Johnson & Steiner 2000); and tillate phase is rather short and highly intense, and indi- (ii) that forager preferences for flowers of a particular sex vidual pistillate flowers are receptive for approximately clearly threaten efficient pollination (Kevan & Baker 1983; 2 days. Usually, the inflorescences of individual stems Goulson 1999). Both the obvious lack of specific floral spe- and/or clusters reach anthesis in sequence, but some cialization and the analysis of visitor samples lead to a minor degree of sexual overlap occurs in more than half rejection of the working hypothesis of a putative depen- of the inflorescences. Both sexes of flowers are scented dence of H. elegans on a particular mutualist taxon. There and provide rewards (pollen and/or nectar). The alloca- is neither direct (foraging, manipulation of flowers, fre-

© 2001 The Society for the Study of Species Biology Plant Species Biology, 16, 165–181 174 C. LISTABARTH quency of visitation) nor indirect (dominance within the Contrary to most individual taxa, the systematically spectrum) evidence to indicate that any single visitor pooled groups revealed significantly higher frequencies taxon, or taxonomic unit performs a particularly efficient of both hymenopteran and dipteran taxa at the staminate pollination service. The questions about pollinator inflorescences. This suggests that the visitation pattern of specalization, formulated at the beginning of this study, systematic groups is less adequate to promote efficient may now be answered specifically. pollination than that of single taxa. Only beetles showed The visitor spectrum of H. elegans is quite diverse and equal representation in staminate and pistillate samples, nearly all visitors of the orders Coleoptera, Hymenoptera which would reflect a proper visitation pattern of these and Diptera habitually visited flowers of either sex (Table visitors as a group. On the other hand, beetles showed the 1). Although in many palms a similarly diverse visitor least mobility, and also rather low values of visitation spectrum is recorded, the staminate inflorescences are frequency for the majority of individual taxa. purported to usually receive visits much more consis- While, within individual samples, the species compo- tently and abundantly than pistillate inflorescences. Visi- sition of pooled groups had a fortuitous character, there tors that almost exclusively occur on staminate flowers were quite similar proportions of hymenopteran and and those that visit both inflorescences, but occur in dipteran taxa across both sets of samples. Beetles repre- higher frequencies and more consistently on staminate sented the major visitor fraction (Fig. 3). However, the inflorescences, are then ruled out as dependable pollina- sampling design had a profound impact upon these tors (e.g., Schmid 1970; Ervik & Bernal 1996; Ervik & Feil results, due to beetle behavior. Beetles did not move 1997). This is quite a rigorous deduction (considering the frequently between inflorescences and they showed usually short sampling periods in the studies), but being sedentary behavior, while many of the Hymenoptera and concerned conceptually with presumably specialized pol- Diptera visited the inflorescences for short foraging bouts. linators, it is a sound conclusion, if it is so. The percep- Thus, the beetles were more likely to be scored during tion of an higher overall presence of insects on staminate sampling. The considerable homogeneity of visitor pro- inflorescences probably pertains to the ‘showiness’ of sta- portions per sample was reflected in the low variance of minate inflorescences and the resulting attraction, or it standardized visitor proportions in both sets of samples, may be a concomitant function of exclusively provided and the positive and significant correlations for the pollen reward in these inflorescences. However, I am not numbers of taxonomic units per order between samples, aware that this phenomenon has ever been measured and except for the beetles in the staminate set. Thus, the quantitated in the palms. Although a similar trend was number of taxonomic units per order and sample also perceived in the field in H. elegans, this was not the depended consistently on overall visitation, which was representative pattern of visitation. Only two predatory probably most influenced by weather conditions. I do not taxa were exclusively recorded in the staminate phase interpret these results to be a fixed pattern of resource par- inflorescences, and from the 26 taxa that visited both titioning among the insects involved, but rather a reflec- types of inflorescences an at least weakly significant tion of factors prone to stochastic variation in response to higher representation in staminate samples was only the biotic environment that characterizes the visitation of found for 23% of these taxa. In general, the bulk of indi- H. elegans by feeding insects. Considerably more data vidual visitor taxa to H. elegans indicates moderate to high would be required to discern patterns. frequencies and consistencies of visits to both types of As a result, none of the insect orders combined flowers. A large majority of these visitors also occured in the traits of a pollinator profile depicted as a pooled group sufficient abundance to be reckoned as dependable polli- of especially dependable and/or prevailing visitors. nators (Table 1). Surprisingly, meliponine bees and However, the same analyses for pooled groups defined as syrphid flies, which are considered ‘good pollinators’ feeding guilds may provide insight in terms of appropri- because of conceptual attributes (such as recruiting ate pollinators on functional grounds, concerning the ability, high flying capacity, large pollen loads) and component ‘frequency of visitation’. Members of both the empiric evidence as repeatedly registered palm pollina- generalist-feeding guild and the nectar-feeding guild tors (Schmid 1970; Kevan & Baker 1983; Henderson 1986; were similarly represented in both sets of samples (Fig. 3). Roubik 1989) were among those visitors of H. elegans that While the presence of taxa from the generalist-feeding visited staminate inflorescences significantly more fre- guild differed in a highly significant manner between sta- quently than pistillate ones. Therefore, I would not espe- minate and pistillate samples, no significant difference for cially favor these taxa as playing a particularly important the nectar-feeding guild was found. This is adequately role in pollination, because this pattern of visitation does explained by the lack of pollen in the pistillate flowers, not promote a reliable pollination service. However, and suggests that the spectrum of visitors was dependent neither does this visitation pattern discredit them as mostly on reward allocation of flowers in both sexes. pollinators completely. In consequence, H. elegans appears to rely on generalist

© 2001 The Society for the Study of Species Biology Plant Species Biology, 16, 165–181 PALM POLLINATION BY A MIXED-SPECIES GUILD 175 pollinators, and the most proper (but not necessarily spe- protandrous palms that flower diurnally show both mel- cialized) insects to effect pollination are members of the litophilous and myophilous characters that are almost the nectar feeding guild, while generalist feeding insects are same (Henderson 1986). Bee pollination is characterized copollinators. This is not consistent with the current asser- by sweet-scented and colored flowers that develop after tion that palm-pollinators may systematically be classi- bract fall, nectar production, protandry, diurnal anthesis fied, since both guilds are composed of a taxonomically of staminate flowers over several days, and short lived mixed set of visitors. The definition of a guild following pistillate anthesis. The syndrome of fly pollination is con- Fauth et al. (1996) is based on resource use (which is sidered to be very much alike, but differs from bee polli- feeding rather than pollination) without regard for nation in that inflorescence development is somewhat taxonomic position, phylogeny and/or geography. Such slower, and it may be more common in understorey a resource-bounded set of species also allows the single species. However, such species sometimes may not be visitor to be replaced by another of the same guild, and pollinated due to the lack of observed fruit-set and low allows operation with stable functional terms within an abundance of dipteran visitors such as Calliphoridae, Syr- unpredictable biotic environment. phidae and Drosophilidae (Henderson 1986). Apart from common floral and flowering traits, many palms (uncluding H. elegans and species of Euterpe and Common traits of the monophyletic genera Euterpe, Prestoea) commonly receive visits from both systematic Hyospathe and Prestoea groups (Diptera and Hymenoptera), and frequently also The reproductive biology of H. elegans corresponds com- from nectar-feeding and generalist-feeding beetles (e.g., prehensively with the sets of floral, flowering and phe- Schmid 1970; Silberbauer-Gottsberger 1973; Henderson nological traits reported so far for species of Euterpe and 1986; Zona 1987; Ratsirarson & Silander 1996; Borchsenius Prestoea (Bannister 1970; Bullock 1981; Bovi et al. 1994; 1997). Therefore, the classification into diffusely charac- Ervik & Bernal 1996; Henderson & Galeano 1996; Ervik & terized pollination syndromes (which are conceptually Feil 1997; Küchmeister et al. 1997). A broad survey of defined through specific adaptations to a higher taxon of flower visitors across these species shows a similar asso- pollinators) is quite uninformative as to the degree of ciation between rewarding flowers with unlimited floral actual visitor specificity in host plants that are morpho- access and a common visitor spectrum at the subfamilial, logically largely unspecialized. Tomlinson (1990) also tribal, and generic level. While only Küchmeister et al. objected to the use of pollination syndromes in the palm (1997) describe ‘general entomophily’ and possible varia- family, because of the basic trimerous pattern of palm tion of pollinators in Euterpe precatoria, most authors con- flowers, and thus the lack of distinctive floral mecha- clude that bees are the principal pollinators of the species nisms. The results of this study suggest that H. elegans has they have studied (Bannister 1970; Bullock 1981; Bovi evolved some minor shifts in floral characteristics that et al. 1994; Ervik & Bernal 1996). Likewise, Ervik and attract and reward a feeding guild of generalist species, coworkers ascribe mellitophily to Prestoea decurrens, which service their hosts as pollen vectors in return. The (Ervik & Bernal 1996) and myophily to P. schultzeana floral characteristics of H. elegans along with those traits (Ervik & Feil 1997), respectively, although they are aware that have been argued to represent adaptations to taxo- that the spectra of visitors of both palms are similar. Ervik nomically bounded sets of pollinators in the species of & Feil (1997) argue that in P. schultzeana, smaller inflores- Euterpe and Prestoea (Table 2) are dicussed below. cence sizes, fewer rachillae and flowers, larger flowers, the presence of scent, later onset of anthesis and its Morphological and floral traits occurence in the understorey (in comparison to P. decurrens) represent adaptations to myophily. However, they Hyospathe elegans has been subject to a monographic finally concluded that ‘such a similarity in fauna (visitor study of morphological and biometrical characters, which spectra of the two species) is likely to facilitate switches turned out to be highly variable even within populations between the two syndromes’. (Skov & Balslev 1989). While this Peruvian population Instead of switching between pollination syndromes, I was homogeneous, and the vegetative morphological would rather reconsider the utility of the terms melit- characters ranged within the means reported in the above tophily and myophily in the palms. For a description of analyses, reproductive characters such as inflorescence specialization to carry meaning, what the organism is spe- length and rachilla number were in the upper range of cialized to use and what it does not use (or cannot use the spectrum. As a result, in the Peruvian H. elegans, the well) because of that specialization must be demonstrated number of flowers per inflorescence was approximately (Thomson et al. 2000). In the palms, the syndromes of six times higher than in an Ecuadorian population. Dif- mellitophily and myophily have remained insufficiently ferences in the numbers of rachillae and flowers in the separated from each other. Most monoecious and same order of magnitude are found across the species of

Table 2 Comparison of ﬂoral and ﬂowering traits between Hyospathe elegans and species of Euterpe and Prestoea

Hyospathe elegans Prestoea schultzeana Prestoea decurrens Euterpe edulis Euterpe precatoria (the present study) (Ervik & Feil 1997) (Ervik & Bernal 1996) (Bovi et al. 1994) (Küchmeister et al. 1997)

Stratum/height Understorey/1–3 m Understorey/2–4 m Subcanopy/5–10 m Subcanopy/5–10 m Canopy/12–20 m No. rachillae 15–20 5–12 36–68 56–58 70–170 No. staminate 4000 4000 27 000 17 000 52 000 ﬂowers Sex ratio 2 : 1 5.5 : 1 2 : 1 3.6 : 1 2 : 1 Scent (sweetish) Strong Strong Weak Weak Strong Rewards Pollen/nectar Pollen/nectar Pollen/nectar Pollen/nectar Pollen/nectar Flowering period 3/peaked 7+/peaked 12?/no data 5/peaked 5.5/peaked (months)/ pattern Flowering Protandrous Protandrous Protandrous Protandrous Protandrous Staminate phase 12 19 18 19 17 duration (days) Sterile phase 4 5 2 5 6 duration (days) Pistillate phase 5 7 7 6 3 duration (days) Staminate anthesis <1 <1 <1 <1 <1 duration (days) Pistillate anthesis 2 2 2 2 2 duration (days) Visitors Coleoptera, Coleoptera, Coleoptera, Coleoptera, Coleoptera, Hymenoptera, Hymenoptera, Hymenoptera, Hymenoptera, Hymenoptera, Diptera, Other Diptera, Other Diptera, Other Diptera, Other Diptera, Other insect Order insect Order insect Order insect Order insect Order

Hyospathe, Euterpe and Prestoea, and tend to depend upon The presence of paired pistillate flowers in the basal palm size (Table 2). Concerning size-dependent traits, triads of H. elegans was probably the most outstanding such as flower size, which could be an adaptation to a par- morphological peculiarity in this population. This feature ticular group of pollinators (Ervik & Feil 1997), a larger slightly influences the ratio of staminate and pistil- radially symmetrical flower would only be an adaptation late flowers (sex ratio) within these inflorescences, but to a size-class of pollinators, but not to one of the visitor appears to be without significant impact on the distribu- orders Coleoptera, Hymenoptera or Diptera in particular. tion of sexual functions. It did not change the sex ratio Many of these insects show an innate preference for radial in this population. A sex ratio of near 2 : 1 is the basic symmetry in flowers, and most studies have also found pattern in the Arecaceae, and is also found in Euterpe and that pollinators in general tend to exert directional selec- Prestoea (Uhl & Dransfield 1987; Henderson & Galeano tion for increasing flower size (Møller & Sorci 1998; 1996). In these genera, sex ratios that differ from near Goulson 1999). Further, as inferred by Wolfe & Krstolic 2 : 1 are mostly caused by the facultative occurence of (1999), flower size in radially symmetrical flowers shows (almost) pure staminate inflorescences (see references in generally more variation than in bilaterally symmetrical Table 2). flowers, which is convincingly explained by stabilizing Colored (mostly brightly white) and sweetly scented selection effected by specialized pollinators that visit flowers, and the presence of nectar, or rewarding liquids, bilaterally symmetrical flowers. Both symmetry and are common in a great quantity of palm species (Uhl & flower size are thus largely indicative of a non-selective Moore 1977; Schmid 1983; Henderson 1986; Knudsen attractant. Finally, as the present data have demonstrated, 1999). Although chemical composition of both the floral size-dependent morphological traits may be a highly vari- exudates in the staminate flowers and stigmatic liquid of able character between populations, and a comparison pistillate flowers was not tested for H. elegans in this across species shows that inflorescence size is often study, it is likely that these liquids also contain sugars related to palm size. Overall, in H. elegans there is no indi- and amino acids, as demonstrated in an exemplary study cation of a size-dependent floral adaptation to any par- of E. precatoria (Küchmeister et al. 1997), and serve as a ticular mutualist taxon. reward. This is also indirectly corroborated by the pres-

© 2001 The Society for the Study of Species Biology Plant Species Biology, 16, 165–181 PALM POLLINATION BY A MIXED-SPECIES GUILD 177 ence of numerous licking and sucking insects from the among the genera of a subtribe (Henderson 1986; Uhl & nectar-feeding guild on both types of inflorescences Dransfield 1987; Listabarth 1992b). Temporal dioecism is (Table 1). Both the presence of nectar and advertisement a derived mating system that promotes outcrossing by colored and scented flowers are also reported for (Cruden 1988), but it is not a device to favor specific species of Euterpe and Prestoea (Table 2), although there pollen vectors. are differences in the quality and intensity of colors and scents between individual species. However, irrespective The enigmatic traits of fly pollination of these differences, all the palms appeal to the same spectrum of feeding visitors, mainly meliponine and halictid From this study, evidence that is associated with the bees, wasps, and a wide array of diverse beetle and syndrome of fly pollination in the palms (Henderson dipteran families. Thus, rewards and advertisements also 1986; Ervik & Feil 1997) is conspicuously controversial. To appear to constitute non-selective traits. begin with, inflorescence development in H. elegans follows the very same and uniform pattern found across the Euterpeinae compared here (including the presum- Flowering traits ably fly pollinated P. schultzeana), of which the majority is In all species compared here, population flowering is syn- thought to be bee pollinated. There is a strong indication chronous and usually there is one peak of flowering, that flies were abundant and consistent visitors of H. although in absolute terms the duration of the flowering elegans (Table 1; Fig. 3), contrary to the view that flies are period differs considerably (Table 2). The flowering generally low-abundance visitors. Finally, data on fruit- sequence within inflorescences follows the same pattern set in H. elegans lends no support to the speculation that across the species compared, and there is little variation understorey species may often fail to be pollinated (as do in the duration of either phase of anthesis (Table 2). several other studies). Although the disproportional pres- Overlap of sexual phases between inflorescences occured ence of myophilous pollination systems in the under- regularly in H. elegans, and has also been reported for storey may occur at a general level, as suggested in the Prestoea acuminata (Willd.) H. E. Moore [as Euterpe globosa few community-wide studies in tropical rainforests in Gaertn. (Bannister 1970)] within inflorescences, and for which this issue has been addressed (Kress & Beach 1994; Euterpe edulis Mart. [as E. espiritosantensis Fernandes (Bovi Momose et al. 1998), an especially high representation of et al. 1994)] between inflorescences. Since in H. elegans the fly-pollinated palm taxa in this stratum is at best ambigu- intensity of flowering peaked markedly during both ous. The majority of palm species occur in the under- sexual phases, minor overlap between the sexual phases storey of tropical rainforests (Uhl & Dransfield 1987; Kahn did not necessarily cause much geitonogamous pollen & de Granville 1992; Henderson 1995), where most palm- transfer. Thus, the overlap of flowering between inflores- pollination studies have been carried out. There is a great cences in otherwise strongly dichogamous palms does not preponderance of beetle-pollinated palm taxa in this necessarily mean that inbreeding by geitonogamy is a fre- stratum (e.g., Listabarth 1992b; Bernal & Ervik 1996; quent event or even a device to compensate for an uncer- Küchmeister et al. 1998). Our ignorance about pollina- tain pollination system. In contrast, minor sexual overlap tion in the majority of canopy palms prevents the finding within individuals may even promote outcrossing by of a statistically testable support for this premature providing regularly available resources. speculation. Pronounced dichogamy, found in many extant palms, has been too strictly associated with a particular pollina- Visitor spectrum tion syndrome (Henderson 1986). Spruce (1869) was the first to comment on this attribute in palms, which he In any of the palm species considered here, characters are called ‘alternation of function’, and associated it with general enough to allow visitation by a large variety of reproductive efforts. Temporal separation of sexual func- insects to effect pollination, despite single floral features tion and gender within a plant (temporal dioecism sensu that may suggest either bee or fly pollination. Waser et al. Cruden & Hermann-Parker [1977]) will not only mean (1996) have pointed out that plants with much more spe- that selfing is avoided, but consequently forces xenoga- cialized characteristics of a particular pollination syn- mous pollen transfer by pollen vectors. However, tempo- drome (than may be attributed to H. elegans) may often ral dioecism has developed several times in the palm depend on animals other than the ones presumed to be family and is not a specific adaptation of H. elegans or the responsible for the majority of pollination. The similarity Euterpeinae. It is found in different expressions (i.e. mod- of the visitor spectra of Hyospathe, Euterpe and Prestoea is erate to highly fine tuned protogyny or protandry, within notable (see references in Table 2), although it is variable and/or between inflorescences and in inflorescences with within the local species composition. The same higher perfect flowers), and different expressions even occur taxa (at the subfamilial and generic level) are repeatedly

© 2001 The Society for the Study of Species Biology Plant Species Biology, 16, 165–181 178 C. LISTABARTH recorded for all those palms, which suggests that the particular interaction by providing an amplified frame insects constitute a feeding guild that also serves as pol- and enlarging the geographic scale, in which the interac- linators to their hosts. Variation in the species composition may be interpreted free from the blur of variable local tion of mutualists or even the partial absence of one of the settings. Very similar floral and flowering specializations partners is a frequent outcome of an interaction. This is are found across the species of Hyospathe, Euterpe and especially true for species with an extremely widespread Prestoea, which may or may not lead to attract specific sys- range (both geographically and altidudinally) and highly tematic groups of pollinators, but in no case are such traits varied environmental conditions across their ranges (e.g. comparable to the massive specializations that have been Bronstein 1994; Thompson 1994; Travis 1996; Renner & used to define pollination syndromes such as melittophily Ricklefs 1998). Variation in mutualists also applies for a and myophily (e.g., Baker & Hurd 1968; Faegri & van der common guild of floral visitors of widely distributed Pijl 1979). Although in the palms a cantharophilous pol- sympatric species (Lippok & Renner 1997; Mahy et al. lination syndrome definitely exists (Henderson 1986; 1998; Listabarth 1999; Dilley et al. 2000). The data of Ervik Listabarth 1992b, 1996; Bernal & Ervik 1996; Küchmeister & Bernal (1996) and Ervik & Feil (1997) are clear evidence et al. 1998), so far there is no major evidence for at least a that this principle similarly pertains to allopatric species similar level of mutual specialization of palms with either that have a rather narrow distribution. The Western bees or flies. A generalist pollination system and pollina- Andean P. decurrens and the Eastern Andean P. schultzeana tion by a feeding mixed-species guild probably applies to differ in terms of their individual visitor species compo- several other palms as well, which have tentatively been sition, but do not show substantial differences in the assigned to mellitophilous or myophilous pollination systematic composition of their overall visitor spectra, syndromes. neither between each other nor among their widely dis- The term ‘generalist pollination system’ as used here tributed sympatric or allopatric relatives. Further corrob- does not impose any evolutionary ranking and does not orative evidence for the plasticity of a common visitor support the idea of general entomophily as an ‘overall spectrum is reported for E. edulis under cultivation in unspecialized process and the primitive condition in an unnatural habitat and biotic environment (Bovi palms’ (Silberbauer-Gottsberger 1990). There is broad evi- et al. 1994). Bovi et al. (1994) found members of most dence that insect pollination evolved in the Jurassic, yet taxonomic units that are identified here for H. elegans the oldest angiospermous fossils are only of early Creta- to be visitors and putative pollinators of E. edulis in ceous age (Pellmyr 1992). The palms are much younger the area of São Paulo State (Brazil), even though this than most of the evolutionary advanced insect taxa that species is native to the biogeographically distinct Atlantic constitute extant pollinator groups (Grimaldi 1999). rainforest of Bahia. Although the chronology of the radiation of the angiosperms is consistent with that of most pollination- Conclusions relevant insect taxa (Grimaldi 1999), this would not necessarily imply that modern anthophilous insects were In addition to the insect visitation pattern, the data on absent in early palm flowers. However, it means that floral and flowering traits do not provide strong evidence specialization to any insect group could have evolved for mutualism between H. elegans and any particular pol- from the very beginning of palm radiation. Further, linator taxon. The protandrous palm H. elegans is tempo- H. elegans shows a generalist pollination system that rally dioecious and consequently requires a pollination employs both phylogenetic old and modern insect taxa system that includes pollen vectors. The pollination with equal significance, and so little can be concluded system of H. elegans is generalist in terms of systematic about early insect pollination in the palms from this or groups of pollinators, but the palm shows specialized similar systems. floral and flowering traits that are critical for the attraction of a guild of feeding insects that effects pollination. Specializations also include continuity of small amounts Acknowledgements of food provided in both sexes to encourage visits of available pollinators that feed on these rewards. My sincerest thanks go to my wife Margarete for her Because observations on the pollination biology of companionship and help during all phases of this tropical plants are often limited to short observation study. I thank A. Henderson, H. Rainer, M. Röser, and periods and a single locality, a comparative view of the D. Roubik for their very helpful comments on earlier pollination biology of host species that comprise a drafts of the manuscript. The research allowance pro- common phylogeny may well contribute to the under- vided from the Peruvian government, and fin- standing of a pollination system. This would allow the ancial support from the Austrian BMWF is gratefully recognition of the type and degree of specialization in a acknowledged.

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