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(Cactaceae): Evidence for a Mixed Pollination Syndrome

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(Cactaceae): Evidence for a Mixed Pollination Syndrome Flora 205 (2010) 757–763 Contents lists available at ScienceDirect Flora journal homepage: www.elsevier.de/flora Floral biology of Echinopsis chiloensis ssp. chiloensis (Cactaceae): Evidence for a mixed pollination syndrome Helmut E. Walter The EXSIS Project: Cactaceae Ex situ & In situ Conservation, Casilla 561, Rancagua, VI, Región, Chile article info abstract Article history: In this study the flower biology of Echinopsis chiloensis ssp. chiloensis, a columnar cactus occurring in Received 17 September 2009 Central Chile, is investigated, in particular its pollination syndrome, its visitors, their frequencies and Accepted 4 December 2009 behaviors and their pollination efficiencies. As statements on floral anthesis of this species are contradic- tory, this study also intended to elucidate both its beginning and duration. A pollinator exclusion study Keywords: of a total of 162 flowers from 12 plants was conducted at one of the two study sites. Fruit and seed Chile production as well as seed viability were documented to evaluate pollinator efficiencies. Columnar cacti Anthesis proved to be nocturnal and diurnal, its duration and beginning was inversely proportional to Floral anthesis Hawkmoths maximum day temperatures. The experiment revealed that nocturnal and diurnal pollinator guilds both Pollination biology contributed to fruit set and that nocturnal pollination was more efficient. Yet, the efficiency of each of the Pollinator exclusion members of the three pollinator guilds was limited for different reasons such as scarcity, unpredictability or specific pollination behaviors. Although E. chiloensis has nocturnal flowers, various floral traits where found to differ from the clas- sical hawkmoth pollination syndrome, suggesting a shift from the specialized nocturnal to a more open pollination syndrome, thus adding to fruit set when hawkmoths are locally or temporarily scarce. © 2010 Elsevier GmbH. All rights reserved. Introduction Friedrich and G.D. Rowley ssp. pasacana (F.A.C. Weber ex Rüm- pler) G. Navarro (Badano and Schlumpberger, 2001; De Viana et The tall Chilean columnar Echinopsis chiloensis ssp. chiloensis al., 2001; Schlumpberger and Badano, 2005), Cereus peruvianus (L.) (Colla) H. Friedrich and G. D. Rowley (in the following abbreviated Miller (Silva and Sazima, 1995) and on the four Venezuelan species as E. chiloensis) occurs between the latitudes of 36◦ S and 30◦ S and Stenocereus griseus (Haworth) Buxbaum, P. moritzianus, Subpilo- is one of the most prominent plants in Central Chile. Its southerly cereus repandus (Linnaeus) Backeberg and Subpilocereus horrispinus habitats lie within the dry spiniferous matorrals and sclerophyl- (Backeberg) Backeberg (Nassar et al., 1997). Both specialized and lous woodlands characterized by a Mediterranean pluvio-seasonal mixed pollination syndromes have been described for columnar bioclimate with average annual precipitations between 250 and cacti in the Americas. Specializations for bat- (Nassar et al., 1997; 800 mm, while the northerly populations growing in the arid Valiente-Banuet et al., 1996), hummingbird- (Valiente-Banuet et desertic matorrals with a xeric-oceanic bioclimate receive average al., 1996), hawkmoth- (Fleming and Holland, 1998; Silva and rainfall between 70 and 200 mm (Luebert and Pliscoff, 2006). Sazima, 1995; Valiente-Banuet et al., 1996) or bee pollination The flowers of columnar cacti are mostly hermaphroditic (Valiente-Banuet et al., 2002) have been reported, but also mixed (Gibson and Nobel, 1986) and xenogamous, though a consider- pollination by bats, diurnal insects and hummingbirds (Sahley, able number of individuals from a population of Weberbauerocereus 1996; Valiente-Banuet et al., 2002), and by bats and hummingbirds weberbaueri (K. Schumann ex Vaupel) Backeberg was reported to be (Dar et al., 2006). Finally, evidence for a mixed pollination by hawk- autogamous (Sahley, 1996), and Nassar et al. (1997) reported par- moths, hummingbirds and diurnal insects has been documented for tial self-compatibility for Pilosocereus moritzianus (Otto ex Pfeiffer) E. atacamensis ssp. pasacana (Schlumpberger and Badano, 2005). Byles and G.D. Rowley. Flower morphology and the duration of floral anthesis in E. Only a few studies on the pollination biology of South Amer- atacamensis ssp. pasacana and E. chiloensis are similar, and Johow ican columnar cacti have been published so far: the studies on (1921) reported visits from the Giant Hummingbird (Patagona W. weberbaueri (Sahley, 1996), Echinopsis atacamensis (Philippi) H. gigas) to flowers of Cereus litoralis Johow (E. chiloensis ssp. litoralis (Johow) Lowry). And, as most columnar cacti in extratropical regions were assumed to have a mixed pollination syndrome (Nassar et al., 1997), a mixed pollination with different portions E-mail address: [email protected]. 0367-2530/$ – see front matter © 2010 Elsevier GmbH. All rights reserved. doi:10.1016/j.flora.2009.12.038 758 H.E. Walter / Flora 205 (2010) 757–763 from Sphingidae, hummingbirds and diurnal insects was hypothe- bag that was closed at the pericarpel with a wire before the begin- sized for E. chiloensis in the present study. To test this hypothesis, ning of anthesis. The bag was removed at 06:30 h in the morning a pollinator exclusion experiment was conducted at Site 1 of the to allow diurnal pollination. The other portion of flowers was left studied sites and diurnal and nocturnal visitors were recorded. uncovered from the beginning of anthesis at dusk, remaining acces- Published statements on the beginning and duration of the flo- sible to nocturnal pollinators, but the following morning at 06:30 h ral anthesis of E. chiloensis have been contradictory, incomplete they were covered with a bag as described above to avoid pollina- or vague in the past (Anderson, 2001; Eggli and Nyffeler, 2000; tion by diurnal pollinators. Care was taken that at any given period Hunt, 2006; Ritter, 1980). To settle the question, the beginning and 4–6 flowers from at least four individuals were left open synchron- duration of anthesis was documented for the flowers at Site 1. ically. In the middle of January 2009, all mature fruits in the three groups were counted separately to evaluate pollination efficiencies. Materials and methods Apart from the six tagged flowers that had been used for hand- cross-pollination, all flowers at Site 2 were left unmanipulated The species thus serving as an external control group. The plants were num- bered and all the flowers appearing during the observation period E. chiloensis is a tall columnar cactus (3–6 m) mainly branch- were counted. After the observation period, the number of success- ing from near the base. It occurs between the latitudes of 30◦30 ful fruit initiations was counted to evaluate pollination efficiency S (Quebrada Choros) and 36◦ S (Maule Valley), mainly at inland under natural conditions. Successful fruit initiation was defined as ≥ habitats from 150 to 1200 m in the southerly and up to 1800 m maturing fruits 2.5 cm with remnants of the abscised perianth. in the northerly range of its distribution; its habitat preferences In mid January 2009, five mature fruits from five different plants are mainly dry north-facing hill sides with a low spiniferous vege- were collected to estimate seed production and compare it to the tation (typically Acacia caven, Puya coerulea or Colliguaja odorifera seed production of the different groups at Site 1. No fruit parasites and other low shrubs; Luebert and Pliscoff, 2006) but also dry river were observed at either site during the observation period. Fruit set valleys and alluvial deposits. among the nocturnal, diurnal, natural and control treatments was analyzed by one-way ANOVA. Study sites and observation periods Hand cross-pollination at Site 2 For this study, two adjacent sites in different habitats were cho- Six flowers from different plants were tagged and cross- sen. Both are located in the Central Chilean Valley in the Region of pollinated by hand at three different times during the duration of Bernardo O’ Higgins, Prov. Cachapoal, 34◦ S. Rainfall occurs exclu- anthesis – shortly after anthesis at dusk, in the morning and shortly sively during autumn, winter and spring (April to November) and before the end of anthesis around midday – to be able to compare amounts to 450-500 mm per annum (Luebert and Pliscoff, 2006). their fruit production with the ones in the other groups. The flowers Absolute minimum temperatures may fall to −5 ◦C in the early were bagged during these intervals to exclude natural pollination. morning hours in June and July, while summers are long, hot and In mid-January 2009 the resulting fruits were counted. dry. Site 1 is located on the valley floor (18 individuals in an area of about 2000 m2, 520 m above sea level), Site 2 is located at a dis- Hand self-pollination at Site 1 tance of some 700 m north of Site 1, on the north-facing side of a hill (36 individuals in an area of about 3000 m2, 610 m above sea To test E. chiloensis ssp. chiloensis for xenogamy, six flowers from level). The pollinator exclusion study was performed at Site 1 only, different plants were tagged and hand self-pollinated at three dif- while all the flowers at Site 2 were left unmanipulated to study nat- ferent times of the day as described above. ural pollination efficiency and to serve as an external control group. The study period was from the beginning of the flowering period in Seed number and quality early November to peak flower production at the end of November 2008 at Site 1, and from mid November to early December at Site In mid January 2009, five mature fruits from each group at Site 2, respectively. Temperatures were measured during the complete 1 and the same number of mature fruits from non-manipulated observation period; minimum night temperatures varied from 9 ◦C flowers at Site 2 were harvested immediately after their equato- at the beginning to 15◦ C at the end of the study period, while day’s rial splitting to avoid losses caused by foraging ants.
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