Jan 3, 1996 - cases of American Myrtaceae-Colletidae interaction have been reported: Eugenia sahmensis D. Sm. (Frankie et al. 1983) and Siphoneugenia ...
BIOTROPICA 29(2): 162-168
1997
Pollination Biology of Myrrhinium atropurpureum (Myrtaceae): Sweet, Fleshy Petals Attract Frugivorous Birds' G. German Roitman, Norbert0 H. Montaldo, and Diego Medan
Laboratorios de Botanica "L. R. Parodi", Facultad de Agronomia de la Universidad de Buenos Aires, Av. San Martin 4453, RA-1417 Buenos Aires, Argentina
ABSTRACT hlyrrhinium atropurpureurn has unusual floral characteristics: sweet, juicy petals, long vivid stamens, and absence of nectar and odor. This uncommon syndrome is morphologically and anatomically described. Floral phenology is also described, and censuses of flower visitors are provided. The main pollinators are frugivorous passerine birds, which are attracted by the petals. This type of floral reward is v e v uncommon and seems to be restricted, in South America, to Myrrhinium, &&a (Myrtaceae) and Calreohria (Scrophulariaceae). The possible origin of the pollination mechanism is discussed.
RESUMEN Myrrhinium atropurpureum posee caracteres florales inusuales: pttalos dulces y carnosos, estambres exertos y vistosos, y ausrncia dr nktar y perfume. Este poco comhn sindrome floral es descrito morfol6gica y anat6micamente. Se describe la fenologia floral y se censaron 10s visitantes a las flores. Los principales polinizadores son aves frugivoras, que son atraidas por 10s pkalos. Este tip0 de recompensa floral es infrecuente y parece estar restringido, en Sudamtrica, a Myrrhinium, Feioa (Myrtaceae) y Cakeohria (Scrophulariaceae). Se discute el posible origen de este mecanismo de pol inizaci6n.
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ugord: bird; yesby petah; Jower anatomy; Myrtaceae; omitbopbib;pollination.
MYRRHINIUM SCHOTT(MYRTACEAE) is a monotypic genus ranging from Ecuador to Perh and from Brazil to northern Argentina (McVaugh 1968, Landrum 1986). Myrrbinium atropurpureum Schott. var. ortandrum Bentham [= M. loranthoides (Hook. et Arn.) Burr.] is a 3-8 m high tree, inhabiting tropical and subtropical forests in Colombia, Ecuador, Perk, Brazil, Uruguay, and Argentina (Landrum 1986). In Argentina, M . atropurpureum occurs in two disjunct areas (Legrand 1941, Digilio & Legname 1966), reaching 32'40's in riparian gallery forests along the Parani and Uruguay Rivers. Myrrbinium atropurpureum has distinctive floral characteristics. The flowers are grouped in brush-like inflorescences, with long red stamens, and odorless (which suggest ornithophily); however, they secrete no nectar. Published descriptions uniformly report M . atropurpureum petals as concave and red, pink to purplish (Landrum 1986). We observed drastic changes in shape and color of petals during anthesis (they became grey and fleshy), presumably associated with their consumpReceived 10 June 1995; revision accepted 3 January 1996
tion by birds. Reports on pollination by flowereating birds are apparently scarce (Faegri & van der Pijl 1971, Proctor & Ye0 1973, Cox 1983). In this paper we explore the role of birds in the pollination of Myrrhinium atropurpureum, and report on morphological and anatomical changes experienced by petals.
MATERIALS AND METHODS PLANTMATERIALS AND STUDY SITES.-A natural population (ca. 15 individuals) located at the El Palmar National Park, Entre Nos Province, Argentina, (31"55'S, 58'10%') was studied 20-24 September 1992. The population occurred along the El Palmar Creek, in the ecotone between the subtropical gallery forest and the xerophyllous scrub. Vouchers are kept at the herbarium of the Facultad de Agronomia, Universidad de Buenos Aires (BAA). Additionally, an individual of M. atropurpureum cultivated at the Lucien Hauman Botanical Garden (Facultad de Agronomia, Universidad de Buenos Aires, 34'40'S, 58"30'W), was monitored during the flowering seasons of 1991, 1992, and 1995.
I
PoLLINATom.-visitors
162
were censused during three
Pollination of Myrrhinium
163
TABLE 1. Abunahnce andfied categoy of thefiwer visitors to M. atropurpureum. Observed at site Species
Family
1
Birds Pitangus sulphuram Ekaenia parvirostriir Mimus saturninus Turdus r u j v e n d p ) Turdus amaurochalinur Paruka pitiayumi Strphanophoncc diadnnam Thraupis sayaca Thraupu bonariensis Saltator aurantirosdp) Zonotrichia capensis Poospiza kateraldp~ I c t m cayanensis Molothncc badiur
Tyrannidae Tyrannidae Mimidae Turdidae Turdidae Parulidae Thraupidae Thraupidae Thraupidae Emberizidae Emberizidae Emberizidae Icteridae Icteridae
X X X X X X X X X X X X*
Insects Apis mellifa Palpaah sp.
Apidae Syrphidae
X X
2 X
X*
Visitor abundance
111 I1 I1 I1 n-a
IFE IFE IFE FIE FIE IE FIE FIE FIE SE SE SE IFE IFE
I1 I
PE PE
n-a n-a
I X X
Feeding category
111
I1 I I1 I1 I
Observation sites: 1. El Palmar 2. Buenos Aires. Vistor abundance: I: Rare, less than 3 observations during census period; 11: scarce, between 3 to 6 observations; 111: common, more than 6 observations; n-a: non available data. Feeding categories: SE: seed eaters; IFE: invertebrate-fruit eaters; FIE; fruit-invertebrate eaters; IE: invertebrate eaters; P E pollen eaters. (PI Species upon which pollen of M. atropurpureum was detected in 1 or more individuals (see text). * Observed by J. Veiga (pers. comm.).
days (1-6 hours per day) for five individuals at the El Palmar site, casual observations were performed on the cultivated specimen. Bird and insect activity was observed and avian visitors were captured with mist nets. Pollen was removed from visitors’ bodies by rubbing on them pieces of glycerin-gelatin, which was then compared with Myrrhinium pollen. MORPHOLOGY AND PHENOLOGY.-FiftY flowFLORAL ers (25 per year) of the specimen at Buenos Aires were observed periodically to describe phenology and changes in flower morphology. Color changes were described according to Kornerup and Wanscher (1984). Sugar concentrations (weighdweight percentages) were measured with a temperature-compensated hand refractometer in three bulk samples of 50 crushed petals. Water content of 100 petals was also determined. Both parameters were obtained at two stages of petal development. Stigmas were checked for receptivity at different flower stages (N = 30) using H z 0 2 (Kearns & Inouye 1993). Pollen-ovule ratios (Cruden 1977) were calculated for 30 flowers.
ANATOMICALossERvATIoNs.-FAA-fixed flower buds and anthetic flowers with petals showing dif-
ferent degrees of swelling were embedded in paraffin and serially cut at 10 p n with a rotary microtome. Additional flowers were critical-point dried and viewed with a Jeol JSM-I1 SEM. Sections (25 p,m thick) from petals at maximal swelling were obtained with a freeze microtome. Photomicrographs of petal transections were digitized, and cross-sectional areas of a minimum of 10 cells per photograph were recorded using MeasurementTV (Updegraff 1989).
RESULTS FLOWERVISITATION.-FlOWCT visitors and their abundance are listed in Table 1. Visitors can be grouped in four feeding behavior categories (adapted from Moermond & Denslow 1985 and Howe 1986): (a) seed eaters (SE), that occasionally eat fruits (Emberizidae); (b) invertebrate (rarely vertebrate, e.g., Pitangw) and fruit eaters (IFE) (Tyrannidae, Icteridae, and Mimidae); (c) fruit-invertebrate eaters (FIE) (Turdidae and Thraupidae), where fruits are a very important source of energy; and (d) invertebrate eaters (IE) (Parulidae). Parukz pitiuyumi, however, may also feed on leaf corpuscles of Cecropia (Moraceae) (Sick 1986), and visits
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TABLE 2.
Feeding behaviour of avian visitors to M. atropurpureum at El Palmar site.
Birds species
Mean number Mean of petals permremoved anence Numper branch at a ber of Num(mean single ob- ber of number of branch served visiting branches) (min.) plants birds
Poospiza lateralis 6.2 (2) 7 (3) Saltator aurantirostris Turdus arnaurorhalinus 21.2 (6) Turdus rufiventris 17.2 (5) 4 (2) Zonotrirhia rapensis
0.4 1.0 2.5 1.5 0.2
1 2
3 3 1
4 7 5 8 4
flowers of Pisonia zapallo (Nyctaginaceae) (R. Fraga, pers. comm.) and Eucalyptw (Belton, 1985), probably eating nectar. Also, Icterw cayanensis, as many Icteridae, is quite nectarivorus and visits flowers of trees such as Tabebuia (Bignoniaceae) (R. Fraga, pers. comm.) and climbers such as Combretum juticosurn (Combretaceae) (G.G. Roitman, pers. obs.). All species of visiting birds perched in the flowering branches, moved from one branch to another and removed the sugary petals. Individual activity (petal removal rates, intra- and inter-plant movements) of the more common visitors are listed in Table 2. Their approaches were from above and in most cases their heads and breasts contacted both stigma and anthers. It was unlikely that birds, no matter their size, would remove petals without touching the anthers, as flowers are grouped in a brush-like inflorescence so they cannot easily be approached laterally or from below. The presence of pollen on Turdus rufiventris and Poospiza lateralis was detected by direct observation. Additionally, one individual of Saltator aurantirostrisfrom El Palmar and another of Turdw rufiventris from the Botanical Garden, both captured, showed (after rub-
TABLE 3.
bing on them pieces of glycerin-gelatin) pollen of M. atropurpureum in bill and feathers. Two insect species were observed trying to collect pollen of M. atropurpureum (Table 1). Both visited flowers during pollen presentation. They did not show any interest in petals but removed pollen from the anthers. Palpada sp., the only native insect, fed on pollen in flight, and the common bee walked among flowers and crept on filaments to reach the anthers with difficulty. In both cases little pollen transport, if any, was expected to occur. We performed no nocturnal observations. Therefore, the possibility that bats visit the flowers cannot be rejected. Although colors and morphology are consistent with hawkmoth pollination, lack of nectar and odor probably rules out Sphingidae. PHENOLOGY AND MoRPHoLoGY.-F~owering FLORAL of M. atropurpureurn extended from late August to late October. Flowers were borne upright on horizontal branches produced the previous years. Flowers were grouped in 3-7-flowered dichasia, which were either solitary or aggregated (2-8 inflorescences) on short shoots. Inflorescences on older branches become more complex, compact and brush-like. In each dichasium the central flower opened 3 2 1 days before the two lateral ones which were synchronous. The flowers were odorless and produced no nectar. They passed through several stages during anthesis, involving strong changes in shape and color of petals (Table 3 and Fig. la). Pollen presentation started at stage 3-petals flat, red-when the sugar concentration was 4 t 1 percent w/w and the water content was 74 percent; and continued through stage 5. Each flower had 4-8 stamens with a filament 15 mm long, the style was 12-20 mm long, the distance between anthers and stigma was 4-8 mm. Each anther contained ca. 8000 pollen grains. Petals were usually removed at stage P p e t a l s biconvex, gray-when sugar concentration reached to 13.16 t 3.48 per-
Changes undergone bfiwers of M. atropurpureum during anthesis.
Stage
Colour of petals (codes after Mean duration Pollen Kornerup & Wanscher 1984) (days) presentation ~
1. Flower opening, stamens unrolling 2. Petals attain maximal area, concave 3. Petals flat to somewhat convex 4. Petals attain maximal thickness, biconvex 5. Petals senescent 6. Petals dropped
Dark red, 11D7 Red, 11E8 Red-violet, 11D3 Gray, 8C1 Dark violet, 15F7
1.4 2.4 1.1 1.2 0.4
X X X
~~~
Pollination of Myrrhinium
165
FIGURE 1 . M. atropurpureum. (a) floral development from flower bud (far left) through stages 1 to 6. L c , SEM of partial transections of a stage 2 petal (b) and a stage 4 petal (c) at their regions of maximal thickness. Abaxial epidermis to the left side. For definitions of developmental stages see text. Bar = 6.7 mm (a); = 100 p,m (b and c).
cent and the water content was 84.8 percent. In rare cases the petals were left untouched by visitors, became dark violet, tended to detach and eventually dropped. The stigma was receptive in coincidence with pollen presentation. Mean pollen-ovule ratio was 8203 5 853, which suggests obligate xenogamy. Preliminary data indicate that the cultivated individual is self-infertile. the bud stage, just prior to PETALANAToMY.-h anthesis (stage I), the petals were ca. 235 km thick. In cross-section, they showed a small-celled adaxial epidermis, a 8-10 layers thick mesophyll made up of rounded, isodiametric cells which left many intercellular spaces, a more or less continuous hypodermis, and an abaxial epidermis with reinforced outer walls. Dark contents occurred in (a) cells associated with vascular strands and (b) spherical, apparently lysigenous, subepidermal cavities. At stage 2 (Fig. Ib) petals became ca. 500 km thick, and the mesophyll cells increased its mean Cross-Sectional Area (CSA) from 580 pm2 (bud stage) to 1840 pm2, also showing incipient radial expansion (CSA may reasonably be assumed to be proportional to cell volume). At stage 4 (Fig. lc) petals
greatly increased in thickness, reaching ca. 1100 p m due to a predominantly radial expansion of mesophyll cells. Expansion was stronger in the midplane of the petals (where the cells reached ca. 3190 pm2 of CSA) than it was at both sides. From bud stage to stage 4 petal thickness increased by a factor of 4.7, and the CSA of mesophyll cells did so by a factor of 5.5. In conclusion, growth of mesophyll cells, with its associated change in cell shape from rounded to radially extended, seems to account clearly for the observed petal swelling.
DISCUSSION ORNITHorHIw.-Animals play very important roles as pollinators and dispersers of many tropical species (Kress & Stone 1993). Passerine pollination has been considered a very common interaction in the Old World (Faegri & van der Pijl 1971), but in the Neotropics the importance of birds other than hummingbirds as pollinators has been stressed only recently. At least 12 species of Eythrina (Fabaceae) show adaptations to pollination by perching birds (Steiner 1979). The orchard oriole (Zcttrus spurius) is considered the most effective pollinator
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Roitrnan. Montaldo and Medan
of E. &ca (Morton 1979) and E. olivae is visited by orioles (Toledo & Hernandez 1979). Combretum fiuticosum (Combretaceae) produces brushtype inflorescences visited by perching birds (Bernardello et al. 1994). In the Myrtaceae, bird pollination is common in Australian species of Eucalyptus, Callistenaton and Calothamnw, which are visited by nectar-consuming Meliphagidae (Armstrong 1979). However, in the species of Eucalyptus introduced to America, nectar is used by hummingbirds (Trochilidae) (e.g., Carpenter 1976, Montaldo 1984). Ornithophily is scarcely represented in the American Myrtaceae, Feijoa sellowiana (= Acca sellowiana) being the unique case known to us. Like Myrrhinium, Feijoa produces no nectar, a reward considered by Stiles (1981) as the only one regularly offered to birds. Feijoa produces pollen in numerous stamens and has fleshy, sweet petals, being visited by pollen-eating insects and birds which feed on petals (Popenoe 1920, Sick 1986). Stewart (1986) and Stewart and Craig (1989) showed that birds are more important than insects as pollinators of Feijoa under culture in New &aland, U.S.A. and Japan. In Myrrhinium atropurpureum the reduction in the number of stamens (and consequently in the amount of pollen offered) seems a further step towards ornithophdy, because fleshy petals are the sole reward. The virtual absence of visits by native insects (only one individual of Palpada sp. was observed during the censuses) tends to support the hypothesis. When comparing Feijoa with Myrrhinium, it is interesting that the morphological advancement in the structure of the androecium (McVaugh 1968) seems paralleled by an increasing specialization toward ornithophily, a trend already stressed by Armstrong (1979) for Myrtaceae. FLORAL TRUTS.--PI~~~Shave evolved traits that enable them to influence directly the behavior and movements of both pollinators and dispersers. One of the traits that usually involve animal learning is floral color changes (Weiss 1991). In most cases (ca. 220 genera of 74 families of flowering plants) insects learn to distinguish and visit pre-change flowers where the reward is available, instead of post-change flowers that increase the plant’s attractiveness to pollinators at a distance (Weiss 1991). In Myrrhinium, post-change flowers (with gray petals) present the reward, while pre-change flowers (with dark red petals) from the same dichasium may increase the attractiveness. In contrast to floral color changes, color signals may be used in ornitochorous interactions to indicate which fruits are
ripe (post-change) and ready for dispersal OJGrllson & Melampy 1983). Petal changes in Myrrhinium seem to work this way. The presence of a bicolored display enhances avian visits in Prunw serotina and Phytohcca americana (Willson & Melampy 1983). The water and sugar contents of Myrrhinium petals (ca. 80% and 14%, respectively) are coincident with those of general low-value food offered to birds by plants: fruits (Moermond & Denslow 1985, Herrera 1987) and nectar (Dafni 1994).
MWINIUM SYNDRoME.-The structure Of inflorescences, their position on the branches, and the floral traits (vivid color, exerted stamens) of M. atropurpureum point to ornithophily. However, two features deviate from the typical syndrome: there is no nectar, and the floral reward consists of fleshy petals. Moreover, the most important visitors are fruit and seed-eating birds. The number of avian visitors observed in this study (14 native species) allow us to conclude that the birds are important for M. atropurpureum pollination. Those birds belong to seven different families with a great variation in feeding behavior (see Table 1). Therefore, the Myrrhinium-bird interaction seems to be an unspecialized one and, like most cases of pollination and seed dispersal by animals, it would be the outcome of diffuse coevolution Uanxn 1980, Jordano 1987). The Myrrhinium syndrome contrasts with the highly coevolved oligotropic ornithophilous systems frequently found in the Neotropics, but is comparable to several paleotropical allotropic species reviewed below. FOOD BODIES AS FLORAL wwm.-Simpson and Neff (1 98 1) reviewed floral rewards other than pollen and nectar. Flower tissues are sometimes offered as food to adult visitors. Beetles and other insects consume different floral and extra-floral parts while pollinating species of Nymphaea (Nymphaeaceae), Bactris (Palmae), and orchids (Simpson & Neff 1981). Apart from Feijoa, there are few examples of this unusual type of pollination, in which birds and bats are rewarded with parts of flowers or associated structures. Freycinetia &nicuhris (Pandanaceae) from Asia provides fleshy, sugary bracts surrounding the flowers. These are eaten particularly by bulbuls (Pycnonotidae), which act as pollinators (Proctor & Ye0 1973). Cox (1983) showed that the bird-pollinated E arborea from Hawaii was once visited by the endemic (now extinct or endangered) species Psittirostra psittacea, Loxiodes kona and Corvw tropicus, and in recent years by Zosteropsjaponica, the introduced white-eye. In Sa-
Pollinationof Myrrhinium
moa, E reineckie is visited by birds and also bats which feed on fleshy bracts (Cox 1990). E insignis offers sweet, white bracts and Bassia (Sapotaceae) a very sweet and easily detached corolla, both being visited by bats (Pteropinae) (Faegri & van der Pijl 1971). Recently, Sersic and Cocucci (1996) found that one species of Cakeohria offers food bodies to birds. Boerhgiodendron (Araliaceae) from Malaysia attracts pigeons by means of fruit imitations, which consist of sterile flowers between the normal ones (Faegri & van der Pijl 1971). The last authors speculate that pollination by birds is a development from destructive eating of flowers, perhaps by fruiteating birds, and that only a few examples remain. Although chiropterophily is not unusual in the study area (G. G. Roitman, pers. obs.), the absence of odor and the vivid colors of Myrrhinium flowers make it unlikely that bats visit them.
EVOLUTION.-HOW has this particular SYNDROME mode of pollination developed in South American Myrtaceae?A possible explanation can be found in the biogeography of the Myrtaceae and that of their main pollinators. The family Colletidae (Hymenoptera) is considered the most primitive among bees, and Euryglossinae the most primitive subfamily. Members of this subfamily can be found in dry warm zones of Australia and are restricted to collect pollen, principally, from flowers of Myrtaceae (Michener 1965). The early isolation of Australia, at the end of the Eocene, produced a close interaction between Colletidae and Myrtaceae, and was responsible for the great diversity of forms present in both families. Australia and South America were never in contact but were joined by Antarctica. The effectiveness of Antarctica as a faunal bridge was limited in the early Tertiary to forms able to tolerate cool temperate climates (Michener 1979). There are no Euryglossinae out of Australia and,
167
coincidentally, the Myrtaceae are poorly diversified elsewhere, except in South America. In tropical and subtropical regions of Central and South America, the Myrtaceae are pollinated mainly by Apidae and Anthophoridae (ProenGa & Gibbs 1994). Only two cases of American Myrtaceae-Colletidae interaction have been reported: Eugenia sahmensis D. Sm. (Frankie et al. 1983) and Siphoneugenia densilfEora Berg. (Proenp & Gibbs 1994), both of them are visited by PtiLogossa species. In most zoophilous species pollen and nectar are the primary floral rewards, but selection has promoted the use of several alternative rewards by many species. Simpson and Neff (198 1) concluded that selection favored the elaboration of a different reward either to capture a segment of the pollination community not used by other plants or to achieve greater constancy of pollination. These changes usually promote a one-to-one relationship a n d o r a more expensive reward. However, in both Feyoa and Myrrhinium, the relationship is still diffuse (many bird species visit them) and the reward quality has not been increased (as compared to nectar or fruit). Nevertheless, the production of “fruitlike” petals enables these plants to attract a new kind of pollinator (birds) different from those prevalent in most Myrtaceae (bees). It is possible that the lack of the primitive hymenopteran pollinators could have been a selective force leading to the evolution of bird pollination in South American Myrtaceae.
ACKNOWLEDGMENTS We are grateful to J. J. Valla for encouraging us to study Myrrbinium and for his constructive criticism of an earlier draft, and R. Fraga, G. E. Schatz, and an anonymous reviewer for their comments on the manuscript. The Direccibn de Parques Nacionales, Argentina allowed us to work in the Parque Nacional El Palmar.
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