DOI: 10.13102/sociobiology.v60i3.306-316Sociobiology 60(3): 306-316 (2013) Open access journal: http://periodicos.uefs.br/ojs/index.php/sociobiology ISSN: 0361-6525 Interactions of the Cerrado Palms Butia paraguayensis and Syagrus petraea with Parasitic and Pollinating Insects I Silberbauer-Gottsberger¹, SA Vanin2, G Gottsberger¹ Introduction Palms are prominent, characteristic and abundant com- ponents of most tropical and subtropical landscapes. They are known to attract and to shelter many insects (Lepesmé, 1947, Howard et al., 2001). Therefore, palms are also hotspots of insect abundance and diversity in any vegetation type. Re- sponsible for this are, among others, the commonly large inflorescences and infructescences, which carry many flowers and fruits and thus provide abundant food for insects in form of pollen, nectar and tissue. The other reason for insect richness on palms are the many possibilities for them to hide between the hard or woody leaf bases and the large inflorescence structures, which themselves have an extended Abstract The two cerrado palms Butia paraguayensis and Syagrus petraea were studied with regard to parasitizing and pollinating insects that visit their reproductive organs. At the study site in Botucatu, São Paulo State, both species occurred together, while at the study site in Indianópolis, Minas Gerais state, only S. petraea was growing. Bees of the subfamily Meliponinae and Halictinae were the main pollinators of B. paraguayensis and several beetles and flies were additional pollinators. The visiting beetles divided up in more exclusive parasites, such as the weevils Tripusus leiospathae and Petalochilus lineolatus, and the Colydiidae Bitoma palmarum, which bored and oviposited the closed spathe and whose larvae fed on the flower buds, as well as species of the weevil Micro- strates, which bred in staminate flowers. Differently, the curculionids Anchylorhynchus bicolor, Parisoschoenus sp., Dialomia sp., and species of Mystrops (Nitidulididae) behaved as parasites and pollinators. On the other hand, S. petraea shows more evident adaptations for pollination by beetles. This species has Trigona spinipes as prominent bee pollinator, but otherwise beetles dominated as visitors, being them either parasites, pollinators or both. Although several identical beetle genera occur on both palms, at the species level they are different, as for example Anchylorhynchus camposi on S. petraea. At the two distant study sites of S. petraea in Botucatu and Indianópolis, several species, especially of the parasitic insects, are identical, indicating that parasitism is a stronger bond than pollination in this species which is characterized by a generalist pollination mode. Sociobiology An international journal on social insects 1 - Universität Ulm, Ulm, Germany. 2 - University of São Paulo - USP, São Paulo, Brazil. reSeArCH ArTICle - BeeS Article History edited by Helena M. Torezan-Silingardi, UFU, Brazil received 01 July 2013 Initial acceptance 26 July 2013 Final acceptance 12 August 2013 Key words Anchylorhynchus, Microstrates, Hustachea, Phytotribus, Mystrops, Meliponinae, Halictinae Corresponding author Ilse Silberbauer-Gottsberger Botanischer Garten und Herbarium Universität Ulm, Hans-Krebs-Weg 89081 Ulm, Germany e-Mail: ilse.silberbauer@uni-ulm.de developmental time and thus provide ample possibilities for insects to oviposit and breeding. One of the early Brazilian pioneers working on palms and their insects was Gregorio Bondar, who noted that a considerable entomological fauna of Hemiptera, Lepidoptera and Coleoptera has evolved on the native palms of Brazil, some of them damaging or destroying leaves, flowers and fruits. Bondar (1964) elaborated that of Coleoptera, especially Hispinae (Chrysomelidae) and Curculionidae have segregated on American palms a large number of genera and species. “Each genus of native palms, and at times, each species, has its own entomological fauna, and by means of the insects collected, one can determine the genus and species of the palm.” (Bondar, 1964). Palms are mainly pollinated by insects (Henderson, Sociobiology 60(3): 306-316 (2013) 307 1986) and many palm species are visited jointly by an array of different insects, which are of varying importance in pollination. However, often a predominance of one group of insects as pollinators can be observed (Silberbauer-Gottsberger, 1990, Gottsberger & Silberbauer-Gottsberger, 2006b). Certain mor- phological and physiological differentiation patterns of flow- ers or inflorescences and scent emissions are correlated with this predominance of pollinators. Palms are frequently asso- ciated with beetles, which may take advantage of different vegetative and floral organs for mating and reproduction. Several of these beetles are involved in pollination. They may act as additional, predominant or exclusive pollinators. In the World Checklist of Palms by Govaerts and Dransfield (2005), 2364 species in 190 genera are accepted. Sixty-seven genera and 550 species are said to occur naturally in the Americas (Henderson et al., 1995), and of these, 210 species are native to Brazil (Lorenzi et al., 2004). Based on the last mentioned authors, 20 species are native to the Central Brazilian cerrado sensu lato vegetation (see Gottsberger & Sil- berbauer-Gottsberger, 2006a). The distribution of the cerrado species among its six genera is the following: Acanthococos (1 species), Allagoptera (2 spp.), Astrocaryum (1 sp.), Attalea (4 spp.), Butia (4 spp.) and Syagrus (8 spp.) (Lorenzi et al., 2004). In this paper we compare two cerrado palms, Butia paraguayensis and Syagrus petraea, with respect to the insects visiting and feeding on still closed and already opened inflo- rescences, flower buds and open flowers, as well as immature and mature fruits. In a previous paper a detailed account of the phenology, the growth and duration of the inflorescences and infructescences, of anthesis, and the morphology and functioning of extrafloral nectaries of Butia (under the old, now invalid name B. leiospatha) was given (Silberbauer- Gottsberger, 1973). It was also mentioned that principally bees, beetles and flies were the visitors and pollinators of this species, but most insects at that time were not identified to genera and species and observations on their behavior have been scarce. Also S. petraea (under the synonym S. loefgrenii) was already shortly mentioned as being pollinated by bees and beetles (Silberbauer-Gottsberger, 1990), again without being able at that time to provide details about visitors and their importance as pollinators and parasites. One aspect of the present paper was to distinguish for both species between insects which are flower visitors without being pollinators and others which are effective pollinators. Another aspect was to verify, by direct obser- vation and, additionally, by information from the literature, the level of parasitism of certain insect species; which one is an exclusive harmful floral parasite, destroying floral tis- sue without contributing to pollination and which one is a parasite and an effective pollinator at the same time? At one study site, in the state of São Paulo, both studied species occurred sympatrically, which provided the opportu- nity to verify similarities and differences in the attracted para- sitic and pollinating insects. In another study site in the state of Minas Gerais, only S. petraea occurred. Since the open, unspecialized palm flowers often have a generalist pollination system (Gottsberger & Silberbauer- Gottsberger, 2006b), we hypothesized that in distant sites of the same palm species, the parasitic insects, living inside and nourishing themselves of floral or fruit tissue, should be more specific than the pollinating insects which mainly collect and feed only on pollen and nectar. Material and methods The two species studied have a quite vast distribution. Butia paraguayensis (Barb. Rodr.) L.H. Bailey is distributed from the Brazilian states of Minas Gerais, Mato Grosso do Sul, São Paulo, Paraná and Rio Grande do Sul, to Paraguay, Argentina, and northern Uruguay. This species occurs mainly in cerrado s.l. vegetation on sandy soils, at 500-900 m eleva- tion (Henderson et al., 1995, Lorenzi et al., 2004). Syagrus petraea (Mart.) Becc. has an even more northern distribution, occurring from the Brazilian states Pará, Maranhão, Piauí, Ba- hia, Minas Gerais, Tocantins, Goiás, Rondônia, Mato Grosso, Mato Grosso do Sul, and São Paulo, to eastern Bolivia and eastern Paraguay. Also this species grows mainly in cerrado s.l. vegetation, however, apparently in more open physiogno- mies than B. paraguayensis (pers. observation), on sandy to red clayey soils, but also in open, semideciduous forests on stony soils, at 600-1000 m elevation (Henderson et al., 1995, Lorenzi et al., 2004). There were principally two study sites for the two spe- cies, one was in the municipality of Botucatu in São Paulo state, where both species occurred together, and the other was in the municipality of Indianópolis, Minas Gerais, where only S. petraea occurred. The climate of the Botucatu region (city coordinates 22°53´9´´S, 48°26´42´´W, alt. 756 to 920 m) is characterized by an average yearly precipitation of about 1300 mm. The seasonal distribution of precipitation indicates that 37% of the total annual rainfall occurs in spring, 44% in summer, 10% in autumn and only 9% in winter, that is, a warm rainy season from October to March alternates with a cooler dry season from April to September (Tubelis et al., 1975). The daily temperature means throughout the year ranged from about 16 to 25°C, with the lowest in July and the highest in February. The yearly average temperature is about 21°C. The exact place of the Botucatu study site, Treze de Maio, where both species occurred, about 8 km northwest of the city of Botucatu, consisted of a mixture of several, more closed and more open, cerrado s.l. physiognomies and lies at 650 m alt. The other study site of S. petraea was close to Indianópolis (city coordinates 19°2´20´´S, 47°55´1´´W, alt. c. 800 m) at Fazenda Bela Taanda and neighboring fazendas. The temperatures in the more northern Indianópolis site are somewhat higher than in Botucatu. In B. paraguayensis in Botucatu, 20 flowering individu- I Silberbauer-Gottsberger, SA Vanin, G Gottsberger - Interactions between Cerrado Palms and Insects308 als were marked in 1970/1971. These individuals served for studying the phenology, the duration of flowering of stami- nate and pistillate flowers, the fruit development and ripening, as well as the approach to and the behavior of insects at the inflorescences and infructescences. To verify the duration of development during the colder and drier versus the warmer and more humid periods of the year, inflorescence buds were weekly measured (length and circumference) from a length of 30 cm on until their opening. Visitors were partly observed and collected during blocks of 30 minutes at different times of the day to obtain a more equilibrated picture of occurrence of insects on this palm during whole days. Additional and com- plementing observations on this species occurred in the years 1977, 1980, 1983, 1989, 1990, 2007 and 2009. For studies of S. petraea in Botucatu in 1980, 1981, 1983, 1985 and 1990, 35 flowering individuals were selected and investigated at the same site as for B. paraguayensis. At the other site in Indianópolis, similar comparative studies of S. petraea were done on 26 flowering individuals in 1983, 1985 and 1990. Voucher specimens of both species are deposited in the herbaria Botucatu (BOTU), Brasília (B) and Ulm (ULM). The insects collected at the palms are deposited in the insect collection of Sergio Vanin at the Department of Zoology, Uni- versity of São Paulo (USP), in São Paulo, and in the private collection of the authors in Ulm. Results Flowering and anthesis Adult individuals of Butia paraguayensis in Botucatu are erect palms and can attain a maximum stem height of 1.5 to 2 m (Gottsberger & Silberbauer-Gottsberger, 2006b); indi- viduals become already sexually mature having a stem height of only half a meter. On the other hand, Syagrus petraea is a so-called “acaulous” short palm. It has subterranean ramified stems. The apical part of the shoot, were the leaves and in- florescences are formed, emerges from the soil in an inclined position and may grow to a height of 20-40 cm (Gottsberger & Silberbauer-Gottsberger, 2006b). When growing in a larger population of ca. 30-50 plants, both species are flowering and fruiting practically year-round. The flowers are unisexual and the inflorescences are monoecious. The pistillate flowers together with staminate ones are arranged in triads more at the basal part of the rachil- lae (inflorescence ramification of the first order), while stam- inate flowers alone occupy the apical part. There are about 30-40 rachillae with about ten times more staminate than pis- tillate flowers. Flower number is variable and apparently de- pends on the size of the inflorescence. One inflorescence of B. paraguayensis can carry about 1200-2500 staminate and 120- 200 pistillate flowers. S. petraea has smaller and less ramified inflorescences (up to 8 rachillae) and with about five times more staminate than pistillate flowers. One inflorescence can carry about 150-250 staminate and 30-50 pistillate flowers. Some inflorescences at the Indianópolis site had only stami- nate flowers. We detected a considerable seasonal difference in the rate of reproductive organ development in B. paraguayensis. Development of inflorescences, flowers and fruits was faster during the warm rainy season than during the cool dry season. In 30 cm long inflorescence buds, the time until spathe open- ing decreased from June to December, this is from mid-dry season to mid-rainy season. Also from September onwards, there was an increase in the number of inflorescences pro- duced by an individual. Flowering and fruiting time also ac- celerated. For example, inflorescences which opened in June, July or August took 111 days (on average) to produce ripe fruits, those which opened in September and October took 93 and those in November and December only 57 days. The inflorescences of each individual of B. paraguay- ensis and S. petraea developed one after the other. Only very rarely are staminate and pistillate flowers, either within or be- tween inflorescences of the same plant, simultaneously in a functional stage. For this reason, these palms are mostly func- tionally dioecious. Anthesis in both species begins in the morning with the longitudinal splitting of the woody peduncular bract, the spathe, which can be up to 80 cm long in B. paraguayensis and ca. 20 cm long in S. petraea. With the opening of the spathe the inflorescence is released. The rachillae are spread. The staminate flowers are functioning first, viz. the inflorescence is protandrous. In Butia about 1/3 of staminate flowers open at the first day, while this was 1/10 in Syagrus petraea. In both species the staminate phase of an inflorescence lasts for about fifteen days (or even longer in the dry season), while one individual flower lasts for one or two days only. Only after the last staminate flower has withered, followed by a non-flowering interval of 10 to 15 days, the pistillate flowers become receptive. In Butia the stigmas are spread apart, while in Syagrus they keep together. All the pistillate flowers in Butia enter their receptive phase within two to three days, in S. petraea within 5 to 7 days, while an individual pistillate flower may be receptive for one or two days only. In the population of Butia there existed individuals with grayish purple staminate and pistillate flowers, and others with yellow flowers. The flowers emit a faint, pleasant, sweet scent. The flowers of S. petraea are pale yellow, the pistillate ones turning to orange yellow when sexually active. Both sexes emit a similar odor, which is faint and straw-like during the day, gradually becoming stronger in the afternoon, as well as gaining spermatic- and mushroom-like notes; this stronger odor persists overnight. Staminate flowers in both species have a reduced, sexually non-functional, central gynoeceum, known as pistillode. Nectar is produced by septal nectaries in both staminate and pistillate flowers, less abundant in S. petraea than in B. paraguayensis. Sociobiology 60(3): 306-316 (2013) 309 Insects visiting Butia paraguayensis The insects observed visiting the reproductive organs of B. paraguayensis, from unopened inflorescences to ripe fruits, belong to 6 orders. The more frequent visitors were of the orders Hymenoptera, Diptera and Coleoptera, while the Hemiptera, Orthoptera and the enigmatic order Strepsiptera were less represented (Table 1). More than 45 different insect species, representing 15 families were found visiting the re- productive organs of B. paraguayensis. The most common insects visiting both staminate and pistillate flowers, and thus being the effective pollinators, were bees, especially Meliponinae, but also Halictidae and Apinae. Trigona hyalinata and T. spinipes were frequent and about twice as abundant at staminate than at pistillate flow- ers, whereas the more rare Paratrigona lineata lineata and the introduced Apis mellifera sometimes visited the pistil- late flowers more frequently. Other bee species that visited both the staminate and pistillate flowers were Ceratalictus theius, and Chloralictus cf. opacus. Bee species of the genera Augochlora, Augochlorella, and Augochloropsis were seen at staminate and sometimes also more frequently on pistillate flowers and therefore are also effective pollinators. A further, not identified Chloralictus species was seen Order, family, subfamily, tribe Genus, species Inflor. bud Flowers Fruits staminate pistillate unripe ripe COLEOPTERA Corylophidae indet. + Colydiidae Bitoma palmarum +/op? +/pf Chrysomelidae Galucerinae indet. +/pf/nf +/nf Curculionidae Anthonominae Anthonomini Anthonomus sp. 2 + Baridinae indet. +/op? ++/pf Centrinini sp. 2 ++ Centrinaspis sp. +/pf Dialomia sp. 1 + Revena rubiginosa + +/op Madarini Angelocentris schubarti ++/pf/nf +/nf/op? Tripusus leiospathae +/op? +++/pf Parisoschoenus sp. +/pf +/op? Microstrates rufus +/pf/op? Microstrates sp. nov. ++/pf/op? Gen. 1 + Erirhininae Derelomini Anchylorhynchus bicolor +++/pf +/mop Molytinae Conotrachelini Conotrachelus sp. 6 + Petalochilinae Petalochilus lineolatus + Nitidulidae Mystrops palmarum +/pf/op? + Mystrops sp. 2 ++/pnf Mystrops sp. 4 ++/pnf ++ Mystrops sp. 6 ++/pnf Scarabaeidae Rutelinae Antichira capucina group +/ff Scarabaeinae Ateuchus sp. +/op Silvanidae Silvanus sp. 1 ++/pf Tenebrionidae Alleculinae Prostenus cyaneus +/pf Table 1. Insects on reproductive organs of Butia paraguayensis in Botucatu, SP. +++ very frequent, ++ frequent, + rare, pc pollen collecting, pf pollen feeding, nf nectar feeding, pnf pollen and nectar feeding, ff fruit feeding, m mating, op ovipositing. I Silberbauer-Gottsberger, SA Vanin, G Gottsberger - Interactions between Cerrado Palms and Insects310 only on staminate flowers. In staminate flowers, bees princi- pally collected pollen, but fed also a little on nectar, whereas in pistillate ones only nectar was available for them. Addi- tionally, several fly, wasp and ant species visited both types of flowers and therefore at least the flies and wasps have to be considered effective pollinators as well. At our study site in Botucatu, the two Trigona species were very abundant and ag- gressive, and other bees, even the often dominant Apis mellifera, as well as occasionally also wasps and flies were attacked and chased away by them. A recently opened inflorescence was often inhabited and visited by many species and individuals of beetles. Some- times we counted up to ten species of beetles in one inflores- cence represented by more than 40 individuals. Half of them were often made up by very small beetles, different species of Mystrops (Nitidulidae) and Microstrates (Curculionidae) or by the somewhat larger (8 mm) weevil Anchylorhynchus bicolor. The numerous individuals of Mystrops and Micros- trates species were mostly feeding on pollen, sometimes took profit also of the nectar, also oviposited in the stamens and visited pistillate flowers only sporadically, thus not being of great importance in pollination. The frequent Derelomini weevil Anchylorhynchus bicolor (sometimes represented by up to 20 individuals in one inflorescence) also fed on pollen and on nectar but visited the pistillate flowers more frequently and were also pollinating. These beetles were always present in the inflorescences, hidden at the base of the spathe, when either staminate or pistillate flowers were active, respectively. They left the inflorescences in the “inactive” interval phase. However, besides pollinating, they parasitized the pistillate flowers after mating and ovipositing the ovary. The larvae developed inside the gynoeceum and were eating the ovule. The destroyed flowers fell to the ground, where the beetles continued their development to pupae and adults. About 30 to 50% of the pistillate flowers were attacked and did not de- velop to fruits. The more rare visitors of the pistillate flowers, Angelocentris schubartii and Parisoschoenus sp., were also pollinators and we suspect them to parasitize the pistillate flowers too. In the open inflorescences of Butia, in some years, Anchylorhynchus bicolor was represented by two morphs. There was a common form of one color (gray-magenta) and another one with black longitudinal stripes. In another year an additional third black morph with one yellowish line sur- rounding the wings appeared. In 19 inflorescences in the DIPTERA 3 spp. (Muscidae, Calliphoridae) +/nf +/nf HEMIPTERA Cydnidae indet. +/nf + Coreidae indet. +/nf HYMENOPTERA Apidae Apinae Apis mellifera +/pc +/nf Meliponinae Trigonini Paratrigona lineata lineata +/pc/nf +/nf Trigona hyalinata +++/pc/nf, ++/nf Trigona spinipes +++/pc/nf ++/nf Halictidae Halictinae Augochlorini Augochlora sp. +/pc ++/nf Augochlorella michaelis +/pc Aurochloropsis aurifluens +/pc Aurochloropsis cleopatra +/pc Ceratalictus theius +/nf ++/nf Lasioglossini Chloralictus cf. opacus ++/nf Chloralictus sp. 1 +/nf Formicidae several spp. indet. +/nf +/nf Vespidae indet. +/nf +/nf ORTHOPTERA Proscopiidae + STREPSIPTERA indet. + Table 1. [Continued]. Insects on reproductive organs of Butia paraguayensis in Botucatu, SP. +++ very frequent, ++ frequent, + rare, pc pollen collecting, pf pollen feeding, nf nectar feeding, pnf pollen and nectar feeding, ff fruit feeding, m mating, op ovipositing. Sociobiology 60(3): 306-316 (2013) 311 staminate stage, 109 individuals of the one colored morph, 42 striped ones and only one of the dark morphs were counted. In ten inflorescences in pistillate phase, 8 one colored, eleven striped individuals and one dark individual were present. The Microstrates species oviposited in the stamens and their larvae fed on the anthers; they were only occasion- ally seen to visit the pistillate flowers. At midday the pollen became powdery, thus pollination by wind apparently occurs as well. Before opening, the inflorescence bud often was para- sitized by the small Colydiidae Bitoma palmarum (2 mm long), the weevil Tripusus leiospathae (3.5 mm long and with a 2.5 mm long proboscis), and a not identified further weevil of the subfamily Baridinae (5.5 mm long with a 1.2 mm long proboscis). They made holes into the bud spathe and layed their eggs into the spathe. These holes were always closed by the plant by a resinous substance. Bitoma larvae devel- oped in the spathe tissue, while Tripusus and the Baridinae larvae probably fed on staminate flower buds in the interior of the inflorescence. When the inflorescence bud had recently opened, beetle larvae were present in between the flowers, and often had destroyed and eaten many of them. Unfortu- nately, we could not rear the larvae to adults. As these species were never seen on pistillate flowers, they are probably no Order, family, subfamily, tribe Genus, species Botucatu Flowers Indianópolis Flowersstaminate pistillate staminate pistillate COLEOPTERA Chrysomelidae Cassidinae indet. + Hispinae Imatidium sp. + Cleridae indet. + Cucujidae indet. + Colydiidae Bitoma palmarum +/pf ++ Curculionidae Baridinae Baridini Cryptobaris sulcata + Centrinini Dialomia sp. 1 + Ladustes speciosus + Palmocentrinus cf. lucidulus + + Madarini Hustachea campestris +++ ++/tf +++/op? +++ Microstrates cocos-campestris +++ Microstrates sp. nov. +++/pf + +++/pf/op? + Parisoschoenus plagiatus + Cryptorhynchinae Cryptorhynchini Coelosternus sp. 1 + Erirhininae Derelomini Anchylorhynchus camposi +++/pf ++ +++/pf +++/nf/m/op Phytotribus sp. 1 +/pf ++/pf/m/op + Phytotribus sp. 2 +/pf + Molytinae Hilobiini Heilus sp. 1 + Nitidulidae Mystrops sp. 3 +/pnf/op +/nf Mystrops sp. 5 +/pnf +/nf +/pnf/op +/nf Silvanidae Silvanus sp. 2 + + +/pnf +/nf DIPTERA indet. +/nf Phoridae indet. +/nf +/nf HYMENOPTERA Apidae Apinae Apis mellifera +/pc Meliponinae Trigonini Trigonisca pseudogreaffii + Paratrigona lineata lineata +/pc + Trigona spinipes ++/pc +/search +++/pc +/search Halictidae Augochlorini indet. +/pc Formicidae indet. +/nf +/nf BLATTODEA indet. + Table 2. Insects on reproductive organs of Syagrus petraea in Botucatu, SP and Indianópolis, MG. +++ very frequent, ++ frequent, + rare, pc pollen collecting, pf pollen feeding, nf nectar feeding, pnf pollen and nectar feeding, tf tissue feeding, m mating , op ovipositing, search searching on the flower. I Silberbauer-Gottsberger, SA Vanin, G Gottsberger - Interactions between Cerrado Palms and Insects312 pollinators. Also the maiority of the other insects found in the inflorescence visited only the staminate flowers. Many of the observed insects just crawled around or were sitting on the flowers and it was not possible to obtain informations about their behavior or their specific importance for the plant. Not only flowers but also young and ripe fruits of Butia were parasitized. One parasite was the weevil Revena rubiginosa which oviposited in very young fruits. The large green rutelid beetle Antichira capucina was seen to feed on ripe fruits of Butia. Under the palm individuals holes in the soil were seen. When digged out, the scarabaeid Ateuchus sp. was detected sitting on ripe fruits of Butia. It was even pos- sible to observe once an individual of Ateuchus rolling a ripe fruit about half a meter away from the palm, digging a hole of about 10 cm depth and than burying a fruit. In some of the holes we found larvae eating the fleshy part of the fruit. The seed inside the hard shell of the inner fruit layer remained intact. Insects visiting Syagrus petraea About 30 insect species (from 13 families and 4 orders) were observed and collected on the comparatively smaller in- florescences of S. petraea, at the two study sites in Botucatu and Indianópolis together (Table 2). The recently opened in- florescences sometimes sheltered up to hundred individuals of beetles, most of them belonging to small Mystrops and Micro- strates species, followed by Anchylorhynchus camposi, Hus- tachea campestris, 2 species of Phytotribus and one Silvanus sp., which all visited staminate and pistillate flowers. They are all pollinators. The other beetle species visited the staminate and/or pistillate flowers only sporadically and were of no real importance in pollination. Many of the species were already active, even copu- lating, in the early morning at 5:30 AM, changing the inflo- rescences also during the day, and increasing their activity in the evening hours. They fed on pollen, on the small amounts of nectar and on flower tissue at the base of the petals of the staminate flowers and on the margins of petals of the pistillate ones. Mystrops, Microstrates and Phytotribus copulated on the staminate flowers and oviposited them. At different sub- populations and in different years the damage caused by these beetles at staminate flowers could vary from zero to 90%. Of 100 dropped staminate flowers from seven inflorescences counted in September 1990 in Indianópolis, 44% were dam- aged. In many of these damaged flowers 1.2 mm long larvae were found. In these so infected flowers mostly the anthers were eaten, but also the petals showed gnawing marks on the nutritious tissues. Anchylorhynchus camposi copulated on the pistillate flowers and oviposited the ovary. This species was present only in inflorescences with sexually active flowers and left the inflorescence during the interval between the staminate and pistillate phases. Hustachea campestris was seen on stami- nate and pistillate flowers, but no copulation or oviposition was detected. Although the spathe of the bud was sometimes damaged, we were unable to detect which one of the insects was responsible for entering the interior of the inflorescence buds. From the morning on, Meliponinae bees, mainly Trig- ona and Paratrigona, frequently collected pollen and also visited the pistillate flowers, where they seemed to search for something but were leaving them soon. However, the bees only visited the flowers from 7:00 AM to 3:00 PM. Diptera and Formicidae were seen on staminate and pistillate flowers in very small numbers. Discussion Butia paraguayensis and Syagrus petraea are visited by numerous insects, mainly bees and beetles, which play dif- ferent roles during the development of the inflorescence buds, the flowers and fruits. There are nearly exclusive parasitic beetles, which oviposit and destroy the tissue of the young spathe, as well as staminate flowers and unripe fruits. A second group of insects are parasites and pollinators, and a third group are pure pollinators which only feed on pollen and/or nectar. There is also a forth group of insects, which only visit the staminate flowers, nourishing themselves from pollen and nectar. Examples of pure parasites in B. paraguayensis are the weevils Tripusus leiospathae (the former name of this palm was Cocos leiospatha!) and an unidentified Baridinae, which bores the spathe and the larvae feed inside the closed inflo- rescence on staminate flowers. As in nearly all Baridinae, the larvae after dropping of the flowers complete their develop- ment in the soil (Costa Lima, 1956). The Colydiidae Bitoma palmarum supposedly develops inside the spathe tissue; we found the adult beetle in newly opened inflorescences. Bondar described this beetle as predator of Attalea funifera and Cocos nucifera (Costa Lima, 1953). Also the weevil Petalochilus li- neolatus may develop in the interior of the closed spathe. Oth- er species of this genus are mentioned to develop in the inner spathes of the palms of the genera Diplothemium, Attalea and Syagrus (Vaurie, 1954). The larvae of the two Microstrates (Curculionidae) species develop in the interior of staminate flower buds, eating anthers and pollen. They complete their development in the fallen flowers at the ground. This was also observed by Bondar for Microstrates ypsilon on Syagrus coronata and Cocos nucifera, and other species, among them Butia eriospatha parasitized by M. hatschbachi, and Syagrus flexuosa (syn. Cocos campestris) parasitized by M. cocos- campestris (Bondar, 1941, Costa Lima, 1956). Revena rubigi- nosa, which was seen to oviposit young fruits may also be an exclusive parasite. Another species, R. vagans, was described by Bondar to bore the young fruits of Syagrus vagans, and the growing larva was eating and destroying the whole interior (Lepesmé, 1947). Sociobiology 60(3): 306-316 (2013) 313 One prominent and frequent beetle that is a parasite of the pistillate flowers and at the same time causes pollination in B. paraguayensis is Anchylorhynchus bicolor (Curculionidae, Derelomini). As this beetle feeds on pollen and passes over several pistillate flowers before ovipositing, it is a relatively effective pollinator. There are many species of Anchylorhyn- chus associated quite specifically with palms (Bondar, 1943, Vaurie, 1954). Angelocentris schubarti and Parisoschoenus sp. also visit staminate and pistillate flowers and seem to para- sitize the pistillate ones. Parisoschoenus obesulus is a pest on Cocos nucifera, parasitizing the ovary (Sánchez & Nakano, 2003, Moura et al., 2009). One unidentified Dialomia species was found on stam- inate flowers, but it may belong to the group of parasitic and pollinating insects as well. Larvae of Dialomia polyphaga feed on petals and anthers and adult females may lay their eggs in pistillate flowers of palms (Lepesmé, 1947). The nitid- ulid Mystrops species which feed on pollen and nectar appar- ently parasitize the staminate flower buds. Following Bondar (1940), in Mystrops palmarum the larval stage takes 5 to 6 days in the staminate buds and the pupae need 4 to 6 days for their development. The whole cycle of the beetle does not exceed 12 days. Hymenoptera and Diptera are non-parasitic pollina- tors and are the most abundant and effective ones in B. para- guayensis. The scarab Ateuchus functions as a short distance disperser of the fruit. It rolls the ripe fruits a short distance away from the mother individuals and digs holes to bring the fruit underground to oviposit there. The intact fruit is in the right depth for germinating and at the same time it is protected from fire. The visitor spectrum of S. petraea is different from B. paraguayensis. Beetles are the most abundant visitors of the inflorescences and flowers, while Hymenoptera and Diptera are less prominent. This species shows adaptations for beetle pollination. The specific floral scent, especially in the after- noon and evening attracts beetles. Some of them are nourished by nutritious tissues on the petals of both the staminate and pistillate flowers. As the flowers produce very low amounts of nectar, they are not that attractive as B. paraguayensis for nectar-imbibing insects such as bees and flies. The only insect species which S. petraea were found to share with B. paraguayensis are the bees Trigona spinipes, Paratrigona lineata, and the beetles Bitoma palmarum, Di- alomia sp. 1 and Microstrates sp. nov. These species showed on S. petraea about the same behavior as on B. paraguayen- sis, with exception of the new Microstrates species. In both palm species Microstrates sp. nov. developed in the staminate flowers, but visited the pistillate ones only in S. petraea, be- ing a pollinator for this species. Otherwise, only the genera of beetles are the same at the two palm species as, for instance, Anchylorhynchus, Parisoschoenus, Microstrates, Mystrops and Silvanus, but the species are different ones. The set of species in S. petraea are Anchylorhynchus camposi, Parisoschoenus plagiatus, Microstrates cocos- campestris, Mystrops sp. 3, sp. 5, and Silvanus sp. 2., while Anchylorhynchus bicolor, Parisoschoenus sp., Microstrates rufus, Mystrops palmarum, Mystrops sp. 2, sp. 4, sp. 6, and Silvanus sp. 1 occur in Butia paraguayensis. One of the im- portant pollinating beetles of S. petraea, Hustachea campes- tris, did not occur on B. paraguayensis. Hustachea species appear to parasite staminate flowers; Bondar provided a draw- ing of H. bondari, shown in Lepesmé (1947), piercing and ovipositing the petals of a staminate bud of a palm, with the subsequent development of the larva in its interior. The two Phytotribus species also only occurred on S. petraea. Species 1 was found at the two sites, ovipositing the staminate flow- ers in Indianópolis, whereas species 2 occurred only at the Botucatu site. There are differences in S. petraea with regard to the occurrence of several beetle and bee species at the Botucatu and Indianópolis sites. But the parasitic species Anchylo- rhynchus camposi, Phytotribus sp. 1, Microstrates sp. nov., Hustachea campestris, Mystrops sp. 5, and Bitoma palmarum were found on flowers at both sites. Anchylorhynchus camposi was found by Bondar (1941) also on flowers of Syagrus flexuosa. Apparently, there are beetles that have a more restrict occurrence on a small group of palms. To this group certainly belongs the weevil genus Anchylorhynchus, visiting the two palm species treated in this paper, and Petalochilus, which was found only on B. paraguayensis. After the revision of Anchylorhynchus by Bondar (1943), Voss (1943) and Vaurie (1954), 16 species of this genus were recognized and five in Petalochilus (Vaurie, 1954). Bondar stated that all species of Anchylorhynchus develop in palms and as far as verified they breed in flowers of the former genus Cocos, which is now sub- divided in the monotypic genus Cocos, as well as the genera Butia and Syagrus. Butia is a monophyletic genus of nine species confined to cooler, drier areas in southern Brazil, Paraguay, Uruguay and Argentina. Recently, Martel et al. (2013) verified raphid- containing idioplasts in all Butia staminate flower petals sam- pled, which do not occur in the most closely related genus Jubaea, further supporting the cohesive monophyly of Butia. Syagrus with its 31 species in its present concept apparently is polyphyletic and occurs from Venezuela southwards to Argentina with many species in the Brazilian cerrados and campos rupestris (Dransfield et al., 2008). Butia paraguay- ensis and B. yatay are said to be closely related species and being perhaps not distinct from each other (Henderson et al., 1995); at least the beetle breeding on them, in both cases Anchylorhynchus bicolor, eventually confirms that the two species are identical. For Syagrus, at present recognized as being polyphyletic, future studies may show the whole di- mension of the association with Anchylorhynchus. It has to be seen after the circumscription of a cohesive monophyletic Syagrus, which one of the species still has associations with Anchylorhynchus. Meanwhile, besides occurring on species I Silberbauer-Gottsberger, SA Vanin, G Gottsberger - Interactions between Cerrado Palms and Insects314 of Butia and Syagrus, Anchylorhynchus species were detected also on species of Oenocarpus in Central Amazonia (Küch- meister, 1997) and in the Colombian Andes (Núnez-Avellane- da and Rojas-Robles, 2008). On the other side, there are beetles which associate with a multitude of palm genera. Notorious are the genera Mystrops (present also on B. paraguayensis and S. petraea) and Phyllotrox, but also, Celetes, Hustachea, Andranthobius, Dialomia and others (see e.g., Schmid, 1970, Uhl and Moore, 1977, Beach, 1984, Búrquez et al., 1987, Barfod et al., 1987, Anderson et al., 1988, Scariot & Lleras, 1991, Bernal & Er- vik, 1996, Ervik & Feil, 1997, Küchmeister, 1997, Küch- meister et al., 1997, Listabart, 1999, Voeks, 2002, Henderson, 2002). Several of these beetle genera might have numerous (but badly known or undescribed) species which are more or less specific to one or a few palm species. We are beginning to understand that even close-by standing different species of palms often share few visitors and no pollinators because dif- ferences in floral scent composition may cause isolation (e.g., Ervik et al., 1999, Knudsen et al., 2001, Núñez et al., 2005). In many cases palms are parasitized by beetles which afterwards function as pollinators. We then can even say that these palms are breeding their own pollinators. This is an el- egant way to make those palms more or less independent for pollination from their surroundings and at the same time this breeding of pollinators shapes the specificity of the beetles for “their” palm species. The nocturnal, thermogenic Attalea microcarpa, studied by Küchmeister (1997) in Manaus, pro- vides a most elegant example of a palm breeding its own pol- linators. This palm is visited by more than 30 species of Co- leoptera, Hymenoptera, Lepidoptera, Diptera and others, but species of staphylinid beetles, Mystrops (Nitidulidae), Groa- tus, Celetes, Phyllotrox and Belopoeus (all Curculionidae) are the main pollinators. They are attracted in enormously large numbers (up to 60,000 estimated individuals per inflores- cence) during the evening hours by the strongly heated stami- nate inflorescences which have a fruit- and yeast-like scent emission. The beetles´ activity after entering the semi-closed staminate flowers was pollen eating and oviposition. The lar- vae develop in the anthers and nourish themselves from pol- len grains and anther tissue. Fast growing hyphae of a fungus envolve the totality of the staminate flowers and prevent their dropping to the ground. The fungus holds the withered and loose staminate flowers at the inflorescence, which gives the larvae of the beetles´ time to finish their development in a flushwater-free space above the ground in the heavily raining environment of the palm. The emerging beetles transport pol- len grains and fungus spores to other inflorescences. The pis- tillate flowers also are heating, they emit a similar scent as the staminate ones and attract the same beetle species that visit the staminate inflorescences, however in much lower number. In A. microcarpa three organisms or groups of organisms, the palm and its flowers, the beetles and finally a fungus work together to make parasitism and at the same time pollination effective processes. Not only in A. microcarpa but in all palms observed up to now, parasitism by flower beetles is more or less in balance with the number of flowers and inflorescences formed. There always remain enough intact flowers within a palm population to guarantee successful pollination and reproduction. The two studied cerrado palms, B. paraguayensis and S. petraea, are visited by insects which are non-pollinators or only occasional pollinators, besides others which are regu- lar and effective pollinators and at the same time parasites. Several of these parasites are effective pollinators. Also these two palms breed several of its pollinating beetle species. Our data confirmed that the parasitic beetles of S. petraea found in Botucatu and Indianópolis, two sites about 400 km distant from each other, are more constant visitors than the non- parasitic ones. Acknowledgements This study was supported by the German Research Council (DFG). The first and last author thank the authorities of their former university in Botucatu for support during the years of their employment (1968-1981). 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