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Australian Journal of Botany Australian Journal of Botany Society
Southern hemisphere botanical ecosystems
RESEARCH ARTICLE

Pollination unpredictability and ovule number in a South-Andean Proteaceae along a rainfall gradient

Vanina Ruth Chalcoff A B and Marcelo Adrián Aizen A
+ Author Affiliations
- Author Affiliations

A Laboratorio Ecotono, INIBIOMA (CONICET – UNCO), Quintral 1250, 8400, Bariloche, Río Negro, Argentina.

B Corresponding author. Email: vchalcoff@gmail.com

Australian Journal of Botany 64(1) 8-14 https://doi.org/10.1071/BT15016
Submitted: 20 January 2015  Accepted: 10 October 2015   Published: 5 February 2016

Abstract

Pollen limitation occurs frequently in plant populations and, as result, many ovules are wasted. One possible adaptive explanation posits that ovule overproduction represents a ‘bet-hedging’ strategy against pollination inefficiency. This hypothesis is supported by comparative evidence showing that unpredictability in pollen receipt is positively associated with an increasing number of ovules per flower across species. Yet, this proposition has not been tested at the intraspecific level, where natural selection operates. Here, we evaluated the relationship between pollination unpredictability, considering both pollination quantity and quality, and number of ovules per flower, across 16 populations of the south-Andean generalist treelet Embothrium coccineum J.R.Forster and G.Forst from north-western Patagonia, which occurs along a west–east gradient of decreasing rainfall. Despite sizable variation in mean number of ovules per flower, we found no increase in ovule production with increasing pollination unpredictability across populations. Instead, we found that mean number of ovules per flower decreased with decreasing rainfall. Therefore, in this species, there was no support for the proposal that ovule overproduction represents a bet-hedging strategy against unpredictable pollen receipt. Rather, the number of ovules per flower seems to be conditioned primarily by resource availability.

Additional keywords: among-population variation, ovule number per flower, resource availability.


References

Aizen MA, Harder LD (2007) Expanding the limits of the pollen-limitation concept: effects of pollen quantity and quality. Ecology 88, 271–281.
Expanding the limits of the pollen-limitation concept: effects of pollen quantity and quality.Crossref | GoogleScholarGoogle Scholar | 17479745PubMed |

Alonso C, Herrera CM, Ashman T-L (2012) A piece of the puzzle: a method for comparing pollination quality and quantity across multiple species and reproductive events. New Phytologist 193, 532–542.
A piece of the puzzle: a method for comparing pollination quality and quantity across multiple species and reproductive events.Crossref | GoogleScholarGoogle Scholar | 22007922PubMed |

Ashman T-L, Knight TM, Steets JA, Amarasekare P, Burd M, Campbell DR, Dudash MR, Johnston MO, Mazer SJ, Mitchell RJ, Morgan MT, Wilson WG (2004) Pollen limitation of plant reproduction: ecological and evolutionary causes and consequences. Ecology 85, 2408–2421.
Pollen limitation of plant reproduction: ecological and evolutionary causes and consequences.Crossref | GoogleScholarGoogle Scholar |

Burd M (1994) Bateman’s principle and plant reproduction: the role of pollen limitation in fruit and seed set. Botanical Review 60, 83–139.
Bateman’s principle and plant reproduction: the role of pollen limitation in fruit and seed set.Crossref | GoogleScholarGoogle Scholar |

Burd M (1995) Ovule packaging in stochastic pollination and fertilization environments. Evolution 49, 100–109.
Ovule packaging in stochastic pollination and fertilization environments.Crossref | GoogleScholarGoogle Scholar | http://www.jstor.org/stable/2410296.

Burd M (2008) The Haig–Westoby model revisited. American Naturalist 171, 400–404.
The Haig–Westoby model revisited.Crossref | GoogleScholarGoogle Scholar | 18217857PubMed | http://www.jstor.org/stable/10.1086/527499

Burd M, Ashman T-L, Campbell DR, Dudash MR, Johnston MO, Knight TM, Mazer SJ, Mitchell RJ, Steets JA, Vamosi JC (2009) Ovule number per flower in a world of unpredictable pollination. American Journal of Botany 96, 1159–1167.
Ovule number per flower in a world of unpredictable pollination.Crossref | GoogleScholarGoogle Scholar | 21628266PubMed | http://www.amjbot.org/cgi/content/abstract/96/6/1159

Calvo RN, Horvitz CC (1990) Pollinator limitation, cost of reproduction, and fitness in plants: a transition-matrix demographic approach. American Naturalist 136, 499–516.
Pollinator limitation, cost of reproduction, and fitness in plants: a transition-matrix demographic approach.Crossref | GoogleScholarGoogle Scholar |

Chalcoff VR (2008) Variación geográfica en los rasgos florales de Embothrium coccineum (Proteaceae) y su relación con los ensambles de polinizadores a ambos lados de los Andes australes. PhD Thesis, Universidad Nacional del Comahue, San Carlos de Bariloche, Argentina.

Chalcoff VR, Ezcurra C, Aizen MA (2008) Uncoupled geographical variation between leaves and flowers in a South-Andean Proteaceae. Annals of Botany 102, 79–91.
Uncoupled geographical variation between leaves and flowers in a South-Andean Proteaceae.Crossref | GoogleScholarGoogle Scholar | 18436551PubMed |

Chalcoff VR, Aizen MA, Ezcurra C (2012) Erosion of a pollination mutualism along an environmental gradient in a south Andean treelet, Embothrium coccineum (Proteaceae). Oikos 121, 471–480.
Erosion of a pollination mutualism along an environmental gradient in a south Andean treelet, Embothrium coccineum (Proteaceae).Crossref | GoogleScholarGoogle Scholar |

Cruden RW (1977) Pollen-ovule ratios: a conservative indicator of breeding systems in flowering plants. Evolution 31, 32–46.
Pollen-ovule ratios: a conservative indicator of breeding systems in flowering plants.Crossref | GoogleScholarGoogle Scholar | http://www.jstor.org/stable/2407542

Cruden RW (2000) Pollen grains: why so many? (Eds A Dafni, M Hesse, E Pacini) Plant Systematics and Evolution 222, 143–165. 10.1007/978-3-7091-6306-1.

Devoto M, Montaldo NH, Medan D (2006) Mixed hummingbird–long-proboscid-fly pollination in ‘ornithophilous’ Embothrium coccineum (Proteaceae) along a rainfall gradient in Patagonia, Argentina. Austral Ecology 31, 512–519.
Mixed hummingbird–long-proboscid-fly pollination in ‘ornithophilous’ Embothrium coccineum (Proteaceae) along a rainfall gradient in Patagonia, Argentina.Crossref | GoogleScholarGoogle Scholar |

Diniz-Filho JAF, Bini LM, Hawkins BA (2003) Spatial autocorrelation and red herrings in geographical ecology. Global Ecology and Biogeography 12, 53–64.
Spatial autocorrelation and red herrings in geographical ecology.Crossref | GoogleScholarGoogle Scholar |

Dray S, Dufour AB (2007) The ade4 package: implementing the duality diagram for ecologists. Journal of Statistical Software 22, 1–20.
The ade4 package: implementing the duality diagram for ecologists.Crossref | GoogleScholarGoogle Scholar |

Dudley SA (1996) Differing selection on plant physiological traits in response to environmental water availability: a test of adaptive hypotheses. Evolution 50, 92–102.
Differing selection on plant physiological traits in response to environmental water availability: a test of adaptive hypotheses.Crossref | GoogleScholarGoogle Scholar | http://www.jstor.org/stable/2410783

Endler JA (1986) ‘Natural selection in the wild.’ (Princeton University Press: Princeton, NJ)

Faegri K, van der Pijl L (1979) ‘The principles of pollination ecology.’ (Pergamon Press: New York)

Fuss AM, Sedgley M (1991) Pollen tube growth and seed set of Banksia coccinea R.Br. (Proteaceae). Annals of Botany 68, 377–384. http://aob.oxfordjournals.org/content/68/4/377.short

Garibaldi LA, Steffan-Dewenter I, Kremen C, Morales JM, Bommarco R, Cunningham SA, Carvalheiro LG, Chacoff NP, Dudenhöffer JH, Greenleaf SS, Holzschuh A, Isaacs R, Krewenka K, Mandelik Y, Mayfield MM, Morandin LA, Potts SG, Ricketts TH, Szentgyörgyi H, Viana BF, Westphal C, Winfree R, Klein AM (2011) Stability of pollination services decreases with isolation from natural areas despite honey bee visits. Ecology Letters 14, 1062–1072.
Stability of pollination services decreases with isolation from natural areas despite honey bee visits.Crossref | GoogleScholarGoogle Scholar | 21806746PubMed |

Gelman A, Hill J (2007) ‘Data analysis using regression and multilevel/hierarchical models.’ (Cambridge University Press: New York)

Haig D, Westoby M (1988) On limits to seed production. American Naturalist 131, 757–759.
On limits to seed production.Crossref | GoogleScholarGoogle Scholar | http://www.jstor.org/stable/2461676

Harder LD, Routley MB (2006) Pollen and ovule fates and reproductive performance by flowering plants. ‘Ecology & Evolution of Flowers’. (Eds LD Harder, SCH Barret) pp. 61–80. (Oxford University Press: New York)

Herrera CM (1988) Variation in mutualisms: the spatio-temporal mosaic of a pollinator assemblage. Biological Journal of the Linnean Society. Linnean Society of London 35, 95–125.
Variation in mutualisms: the spatio-temporal mosaic of a pollinator assemblage.Crossref | GoogleScholarGoogle Scholar |

Herrera CM (2009) ‘Multiplicity in unity. Plant subindividual variation and interactions with animals.’ (University of Chicago Press: Chicago, IL)

Hijmans RJ, Cameron SE, Parra JL, Jones PG, Jarvis A (2005) Very high resolution interpolated climate surfaces for global land areas. International Journal of Climatology 25, 1965–1978.
Very high resolution interpolated climate surfaces for global land areas.Crossref | GoogleScholarGoogle Scholar |

Martin FW (1959) Staining and observing pollen tubes in the style by means of fluorescence. Biotechnic & Histochemistry 34, 125–128.
Staining and observing pollen tubes in the style by means of fluorescence.Crossref | GoogleScholarGoogle Scholar | 1:STN:280:DyaG1M%2FovV2jtQ%3D%3D&md5=c311ee88c1cae5bb43a6e0811f266fd7CAS |

Medan D, Zarlavsky G, Bartoloni NJ (2013) Plant reproduction in the high-Andean puna: Kentrothamnus weddellianus (Rhamnaceae: Colletieae). Plant Systematics and Evolution 299, 841–851.
Plant reproduction in the high-Andean puna: Kentrothamnus weddellianus (Rhamnaceae: Colletieae).Crossref | GoogleScholarGoogle Scholar |

Rovere AE, Chalcoff VR (2010) Embothrium coccineum J.R.Forst. et G.Forst. Kurtziana 35, 23–33.

Schreiber SJ, Rosenheim JA, Williams NM, Harder LD (2015) Evolutionary and ecological consequences of multiscale variation in pollen receipt for seed production. American Naturalist 185, E14–E29.
Evolutionary and ecological consequences of multiscale variation in pollen receipt for seed production.Crossref | GoogleScholarGoogle Scholar | 25560562PubMed |

Sleumer HO (1984) Proteaceae. ‘Flora Patagónica’. (Ed. MN Correa) pp. 20–28. (INTA: Buenos Aires, Argentina)

Smith-Ramírez C, Armesto JJ (1998) Nectarivoría y polinización por aves en Embothriun coccineum (Proteaceae) en el bosque templado del sur de Chile. Revista Chilena de Historia Natural 71, 53–65.

Smith-Ramírez C, Armesto JJ (2003) Foraging behaviour of bird pollinators on Embothrium coccineum (Proteaceae) trees in forest fragments and pastures in southern Chile. Austral Ecology 28, 53–60.
Foraging behaviour of bird pollinators on Embothrium coccineum (Proteaceae) trees in forest fragments and pastures in southern Chile.Crossref | GoogleScholarGoogle Scholar |

Smith-Ramírez C, Martinez P, Nuñez M, González C, Armesto JJ (2005) Diversity, flower visitation frecuency and generalism of pollinators in temperate rain forests of Chiloé Islan, Chile. Botanical Journal of the Linnean Society 147, 399–416.
Diversity, flower visitation frecuency and generalism of pollinators in temperate rain forests of Chiloé Islan, Chile.Crossref | GoogleScholarGoogle Scholar |

Sokal RR, Rohlf FJ (1995) ‘Biometry: the principles and practices of statistics in biological research.’ (Ed. WH Freeman) (Freeman Company: New York)

Stebbins GL (1970) Adaptive radiation of reproductive characteristics in angiosperms, I: pollination pechanisms. Annual Review of Ecology and Systematics 1, 307–326.
Adaptive radiation of reproductive characteristics in angiosperms, I: pollination pechanisms.Crossref | GoogleScholarGoogle Scholar |

Strauss SY, Whittall JB (2006) Non-pollinator agents of selection on floral traits. ‘Ecology & Evolution of Flowers’. (Eds LD Harder, SCH Barret) pp. 120–139. (Oxford University Press: New York)