Hawkmoth pollination in Cereus peruvianus, a columnar cactus from southeastern Brazil

Flora (1995) 190 339-343 ©by Gustav Fischer Verlag Jena

Hawkmoth pollination in Cereus peruvianus, a columnar cactus from southeastern Brazil WESLEY R. SILVA and MARLIES SAZIMA* Departamento& de Zoologia e de Botanica, Universidade Estadual de Campinas, 13083-970 Campinas, Sao Paulo, Brasil

* Corresponding author: Prof. Dr. Marlies Sazima, Departamento de Botanica, Caixa Postal 6109, Universidade Estadual de Campinas, 13083-970 Campinas, Sao Paulo, Brasil. Accepted: January 25, 1995

Summary Pollination by hawkmoths ( Sphingidae) is described for Cereus peruvianus ( Cactaceae) in southeastern Brazil. The flower presents a dish to bowl-shaped perianth with whitish tepals and a long floral tube. The stamens, arranged like a brush, produce abundant pollen and the long, tube-like style ends in a multi-lobed stigma. Start of anthesis is crepuscular. Anthesis lasts one night. Only little nectar is produced, with ca. 27% sugar concentration. Odour is weak, sweetish and persists throughout the night. Handpollination tests indicate that seed production is dependent on cross-pollination. Honeybees, scarabid beetles, and hawkmoths were observed visiting the flowers, but only the latter seem to be effective pollinators. The sphingids, Agrius cingulatus and Manduca rustica, showed similar visiting behavior, which consisted of hovering, alighting on the perianth, and partially introducing the body into the nectar chamber. Both floral attributes and the morphological/behavioral characteristics of sphingids point to an adaptive trend toward sphingophily in C. peruvianus. This trend is also reflected in the flowering season, which matches the main peak of activity for sphingids at the study areas, and in the "steady state" flowering pattern, which promotes cross-pollination visits by these insects. Key words: Cactaceae, Cereus peruvianus, Sphingidae, pollination, sphingophily, southeastern Brazil

Introduction

Material and methods

The Cactaceae is a family with about 2000 species widespread in most xeric habitats from North to South America (BRITTON & RosE 1963, WILLIS 1973). Although their flowers are variable in many features such as color, size, displacement of sexual structures and diurnal or nocturnal anthesis, most species exhibit flowers with animal-pollinated syndromes (PoRSCH 1939). Several groups of invertebrates and vertebrates have been reported to visit flowers of cacti species, such as bees (GRANT & GRANT 1979a), beetles (GRANT & CONNELL 1979), hawkmoths (HABER 1983), doves and bats (ALCORN et al. 1961, DoBAT & PEIKERT-HOLLE 1985). Here we report on hawkmoth pollination in Cereus peruvianus MILLER 1768 and comment on some of its sphingophilous characteristics.

Field observations were made on the northern slope of the Serra do Japi, Sao Pau1o (ca. 23° 12' S; 46° 57' W, 800 m alt.), during the rainy season (September-March) from 1980 to 1982. There C. peruvianus commonly grows on rocky outcrops in the forest and deforested areas. A detailed description of this region is found in MoRELLATO (1992). Additional observations were carried out at the Esta~ao Ecologica do Taim, RS, extreme South Brazil (32° 50'S; 52° 26' W, 5 malt.), in January 1981, where many plants can be found growing on sandy soil in small forest tracts surrounded by grassland. Floral events and the behavior of visitors were registered from evening to midnight, sometimes until dawn. Sugar concentrations in nectar were measured with an Atago N1 (0-32%) pocket refractometer and FLORA (1995) 190

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nectar volume was estimated with micro-pipettes. The plant breeding system was investigated through hand pollination tests similar to those described in SAZIMA (1977).

Results and discussion

The flowers At the study sites C. peruvianus plants reach the height of 7 m and occur in rocky habitats. The flowering period extends from late September to early January, with a peak in October. Some larger plants also bloom in January- February. Each individual plant bears up to 1000 flowers per blooming season and each flower is open for one night. The number of flowers open per night is about 5 to 15, but larger individuals can open up to 50 flowers at the peak of the flowering period. The actinomorphic flower has a dish- to bowl-shaped perianth (200 mm in diameter) with whitish tepals (Fig. 1), and its floral tube is green and very long (150 mm). The stamens are numerous (over 500) and the anthers dehisce longitudinally exposing the dry and abundant pollen. A long tube-like style bears a 12-14 lobed stigma, which outstrips the anthers in about 20 mm. Both male and female organs are whitish to creamy. As a whole, these features fit the general morphological patterns described for sphingophilous flowers (BAKER 1961. F AEGRI & VAN DER PIJL

1980).

Anthesis begins at sunset and one hour later the flower is completely open. By that time, both pollen and nectar are available, and the stigma is laterally or upwardly displaced. Subsequently, the style begins to descend slowly, placing the stigma in a central position about 6 hours later. At this occasion, the stigmatic surface is perceptibly wet and by dawn the stigma is downwardly placed. Only small amount of nectar is produced along the nectar chamber (Fig. 2), averaging 110,3 Jll (sd = 42,1; N = 6), which is less than that produced by some other sphingophilous flowers (HEINRICH & RAVEN 1972), but similar to that found in Acanthocereus pentagonus and Hylocereus costaricensis (HABER & FRANKIE 1989). Sugar concentration in nectar averaged 27,7°/o (sd = 3,7; N = 12), which matches the values obtained for other sphingophilous flowers (BAKER 1978, PYKE & WASER 1981, HABER & FRANKIE 1989). Nevertheless, the average values reported by ScoGIN (1985) were slightly lower (21 o/o for C. peruvianus and 22°/o for other 21 species of sphingophilous cacti). 340

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Fig. 1. The flower of Cereus peruvianus showing the stigma outstriping the anthers (picture taken about 24:00 h). Fig. 2. A sagital cut of the floral tube exposing the nectar chamber. Nectar droplets of different sizes are scattered on the wall and on the style surface.

A weak odour of fresh vegetables, like cauliflower, is produced by the tepals at the beginning of an thesis and persists throughout the night. This kind of scent agrees with the scent patterns attributed to sphingophilous cactus flowers (PORSCH 1939), although strong sweet fragrances are expected to be more common within this syndrome (BAKER 1961, HABER & FRANKIE 1989). The hand pollination tests showed that C. peruvianus depends mainly upon crosspollination, since successful fruit production between treatments was 70°/o for xenogamy versus 7 ,5°/o for autogamy (chi square= 32,91; p < 0,0001; N =40).

The visitors Hawkmoths, beetles and honeybees were the visitors most commonly observed on C. peruvianus flowers at both study sites. The hawkmoths Agrius cingulatus and M anduca rustica ( Sphingidae) visited the flowers regularly throughout the blooming period. Both moths are common at the study sites and have morphological and behavioral traits adapted to perform efficient cross-spollination, such as fur-like scales, a long proboscis (110-120mm) and a "trapline" foraging mode (BAKER 1973, LINHART & MENDENHALL 1977). Sphingid visits occured 1-8 hours after start of anthesis. The hawkmoth approached the flower and introduced the extended proboscis into the nectar chamber, while hovering at variable distances in front of the flower (hovering visit, Fig. 3). Sometimes the hawkmoth alighted on the perianth and inserted the proboscis into the nectar chamber (alighting visit), or moved forward to the entrance of the nectar chamber and introduced part of the body into the chamber (penetration visit, Fig. 4). In the latter, the hawkmoth was in full contact with reproductive organs. Several hawkmoths captured during their foraging activities had pollen grains attached mainly to their proboscis, head and belly. The visits to each flower were short (2-5 s) in the hovering, or long (up to 180 s) in the penetration visits, and the hawkmoths frequently visited flowers of different individuals. Similar pattern of visiting behavior was reported for the hawkmoth M anduca rustic a on flowers of Hylocereus costaricensis (HABER 1983). Honeybee, Apis mellifera, usually visited the flowers late afternoon, even before anthesis, displacing some tepals in order to reach the anthers. In most flowers heavily visited by bees, the pollen was readily depleted at the beginning of the anthesis. During pollen gathering the bees rarely touched the stigma. Although regular pollinators of other cacti species (GRANT & GRANT 1979a), these bees acted mainly as pollen thieves (see INOUYE 1980 for terminology) in C. peruvianus. The scarabid beetle Cyclocephala melanocephala (ca. 12 mm long) visited some flowers at dusk, remaining there up to 2 days after anthesis. The beetles were never seen flying from flower to flower and rarely touched the stigma. Apparently they ate small floral parts while remaining deep within the flowers, as is typical for this species (D' ARAino E SILVA et al. 1968). Beetles seem not to be important pollen vectors for most cacti species (see GRANT & HURD 1979). Although pollen-eating and nectarivorous glossophagine bats such as Anoura caudifer occur at the Serra do J a pi (MARINHO-FILHO & SAZIMA 1989),

Fig. 3. The hawkmoth M anduca rustic a hovers in front of the flower of C. peruvianus (hovering visit). Note the extended proboscis being introduced in the perianth. Fig. 4. The hawkmoth Agrius cingulatus with the body partially introduced in the floral tube (penetration visit). Only the wing tips are visible.

none were observed visiting these cactus flowers. Bats probably are discouraged from visiting long-tubed sphingophilous flowers, being attracted instead to flowers with more accessible and copious nectar (DOBAT & PEIKERT-HOLLE 1985).

Adaptive trends to sphingophily The great number of species of night-blooming cacti sharing the sphingophilous syndrome contrasts sharply with the lack of information on floral biology FLORA (1995) 190

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for most of them. The similar C. jamacaru from northeastern Brazil, with same floral attributes, has been reported to be visited by hawkmoths (SoHRENS 1924 apud PORSCH 1939), and HABER & FRANKIE (1989) presented data on hawkmoth pollination for Acanthocereus pentagonus and Hylocereus costaricensis in Costa Rica. GRANT & GRANT (1979 b), although not reporting well documented cases, comment on the role of hawkmoths as potential pollinators of several nocturnal tubular-flowered cacti in southwestern North America. In C. peruvianus the long hypanthium increases the distance between the reproductive organs and the nectar source, excluding visits of smaller shorttongued hawkmoths, a feature which can represent a major trend toward specialization within sphingophily. Supporting this idea, the two sphingophilous cacti with long-tubed flowers observed by HABER & FRANKIE (1989) in Costa Rica were visited only by a few long-tongued species presented in the overall hawkmoth community (A. cingulatus and M. rustica were among the five hawkmoth species with the longest average tongue length). The tight dependence of C. peruvianus upon a small group of pollinators requires a well-adjusted phenological mechanism by the plant, since hawkmoths have a markedly seasonal activity pattern in many tropical habitats (LAROCA & MIELKE 1975, HABER & FRANKIE 1989). As a presumable adaptation to this seasonal pollinator availability, at the Serra do Japi C. peruvianus displays its flowers during the main peak of activity of these sphingids (K. S. BROWN Jr., pers. com.). The flowering pattern of C. peruvianus approaches the "steady state" of GENTRY (1974). This strategy generally promotes selection for more specialized and constant pollinators, which often set daily feeding routes encompassing several individuals of a plant species. This foraging behavior, known as "trap lining", is characteristic for many hawkmoth species (JANZEN 1971, LINHART & MENDENHALL 1977), and enables these insects to be efficient pollinators of C. peruvianus and other cacti species with similar floral patterns along their distributional range.

Acknowledgements We thank I. SAZIMA and K. SYLVIUS for helpful comments on the manuscript. W. UIEDA and V. S. UIEDA assisted the fieldwork. The sphingids were identified by K. S. BROWN Jr. and the scarabid beetles by S. VANIM. Our gratitude to all of them. M. S. thanks CNPq for financial support (grant 300993/79); W.R.S. the Programa PG-EcologiajUNICAMP. 342

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LINHART, Y. S., & MENDENHALL, J. A. (1977): Pollen dispersal by hawkmoths in a Lindenia rivalis BENTH. population in Belize. Biotropica 9: 143. MARINHO-FILHO, J. S., & SAZIMA, I (1989): Activity patterns of six phyllostomid bat species in southeastern Brazil. Rev. Bras. Bioi. 49: 777-782. MORELLATO, L. P. C. (org.) (1992): Hist6ria natural da Serra do Japi. Campinas. PoRSCH, 0. (1939): Das Bestiiubungsleben der Kakteenbliite, II. Jahrb., 81-142.

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Buchbesprechung

FEOLI, E., & 0RL6CI, L. (Herausg.): Computer assisted vegetation analysis (Handbook of vegetation science 11) Dordrecht: Kluver Academic Publishers 1991-498 S., 152 Abb., 131 Tabellen, hart gebunden, 425,00 Dfl., 235,00 US$, 142,00 UK£. ISBN 0-7923-1126-4 Das vorliegende Buch ist gleichzeitig der 11. Band der Reihe der ,Handbiicher der Vegetationsanalyse". Es bietet eine Zusammenstellung wichtiger Originalarbeiten auf dem Gebiet der numerischen Vegetationsanalyse. Meist handelt es sich urn Beitriige, die in den letzten Jahren in der Zeitschrift Coenosis erschienen. FEOLI und 0RL6CI fiigten in dieser Obersicht zweiundvierzig separate Artikel zur Anwendung mathematischer und statistischer Methoden zusammen und lieferten damit einen aktuellen AbriB iiber die seit Anfang der 70er Jahre durch die Internationale Vereinigung fiir Vegetationskunde angeregten Aktivitiiten auf diesem Gebiet. Die Herausgeber bemiihen sich, vier Grundgedanken zu vermitteln, die ihrer Meinung nach zukiinftig bei der Vegetationsanalyse starker zu beriicksichtigen sind: 1. Die Vegetation ist als unscharfes (,Fuzzy"-)System aufzufassen. 2. Die Vegetation ist nicht ausschlieBlich anhand der vorkommenden Arten zu beschreiben, sondern auch mit Hilfe von okologischen Indikatormerkmalen. 3. Bei der Aufnahme der Vegetation sollte man sich schrittweise, unter Riickkopplung zu einer flexiblen Datenanalyse, den fiir denjeweiligen MaBstab sinnvollsten AufnahmegroBen und -modi niihern. 4. Beobachtete Muster sollten unabhiingig von den Restriktionen traditioneller Statistik mit den Mustern hypothetischer Oberlegungen verglichen werden. Beim

Testen solcher Hypothesen sollten auch neue Wege gefunden werden. Der einfiihrende Artikel der Herausgeber kommentiert zusammenfassend die verschiedenen Klassifikations- und vor allem Ordinationsmethoden in ihrer prinzipiellen Vorgehensweise sowie ihrer Geschichte und gibt zahlreiche Literaturverweise. Er umreiBt zudem grundsiitzliche Fragen bei der okologischen Interpretation vegetationskundlicher Daten. Der Grundtenor, Biologie und Okologie der einzelnen Arten in ihrer Komplexitiit auch bei numerischen Analysen verstiirkt Beachtung zu schenken, sowie die Datenanalyse mit der Datengrundlage in einem iterativen ProzeB abzugleichen, erscheint besonders wichtig. Die konsequente Umsetzung dieses Prinzips verbietet das ,schnell 'mal durchrechnen" und zwingt zum intensiven Beschiiftigen mit den Anspriichen der Arten. Ein sicheres Gefiihl fiir die okologischen Zusammenhiinge beim Bearbeiter verbessert die Interpretationsergebnisse, insbesondere wenn jeder Vegetationstyp als unscharfes System (fuzzy set) betrachtet wird. Leider wird der Diskussion der biologisch-okologischen Bedeutung von Berechnungsergebnissen in den Spezialbeitriigen dieses Buches nur geringer Raum eingeriiumt. Im ersten Kapitel finden sich grundsiitzliche Oberlegungen zur Aufnahmemethodik. Insbesondere wird die Fliichenauswahl diskutiert, werden Anwendungsbeispiele gezeigt, unzuliissige Methoden kommentiert und eine Reihe alternativer Vorgehensweisen vorgestellt. Aufnahmestrukturen und -inhalte werden auf numerische Auswertbarkeit gepriift. Letztere setzt nutzbare Dateistrukturen voraus. Der mogliche Aufbau einer relationalen Datenbank wird im zweiten Kapitel beschrieben. Im dritten Kapitel steht die Nutzung von IndikatormerkFLORA (1995) 190

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