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A half-day flowering pattern helps plants sharing pollinators in an oceanic island community

Published online by Cambridge University Press:  08 April 2021

Xiangping Wang
Affiliation:
Key Laboratory of Plant Resources Conservation and Sustainable Utilization, South China Botanical Garden, Chinese Academy of Sciences, Guangzhou, Guangdong, China
Tong Zeng
Affiliation:
Key Laboratory of Plant Resources Conservation and Sustainable Utilization, South China Botanical Garden, Chinese Academy of Sciences, Guangzhou, Guangdong, China
Mingsong Wu
Affiliation:
Key Laboratory of Plant Resources Conservation and Sustainable Utilization, South China Botanical Garden, Chinese Academy of Sciences, Guangzhou, Guangdong, China
Dianxiang Zhang*
Affiliation:
Key Laboratory of Plant Resources Conservation and Sustainable Utilization, South China Botanical Garden, Chinese Academy of Sciences, Guangzhou, Guangdong, China
*
Author for correspondence: *Dianxiang Zhang, Email: [email protected]

Abstract

The temporal pattern of flower opening and closure is a feature of the biology of many plant species, particularly those inhabiting oceanic islands where flowering generally lasts for only a few hours per day. Additionally, flower visitors often seek different floral sources on a timely basis, thus the relative timing of interactions is central to their status in pollination competition, or in the facilitation of pollination among co-flowering plants sharing pollinators. However, few studies have examined the impacts of daily temporal variation in flowering patterns on the pollinator network and competition on a community scale. In order to examine whether the daily pattern of flower opening and closure can impose temporal dynamics on interspecific interactions within a single day, plant–pollinator interaction networks (AM subweb and PM subweb) were quantified, and the relevant interactions between the two subwebs were compared using the Bray–Curtis dissimilarity of visitation frequencies in an oceanic island community (Paracel Islands, South China Sea). The role of species within networks and its variation between two subwebs were assessed by calculating the species-level specialization and species strength of each plant and pollinator species. The quantitative plant–pollinator interaction dissimilarity between morning and afternoon subsets was 0.69, and this value dropped to 0.58 when considering plant species flowering throughout the day. In our study, this dissimilarity between the two subwebs might be explained by the morning peak activity rather than a preference for morning flowers. No significant differences were detected in the species-level specialization and species strength of plants flowering all day from morning to afternoon at the community level. The flower visitation rates of native honeybee Apis cerana were not significantly different between morning and afternoon for most of the whole-day flowering plants. However, plant species only flowering either in the morning or the afternoon differed in the rate of visitation by A. cerana. The analyses of variation in the visitation rates of pollinators shared by plants within a single day in the studied community suggest that daily structuring at a community level and half-day staggered flowering during the morning or afternoon might reduce competitive interactions in oceanic insular habitats.

Type
Research Article
Copyright
© The Author(s), 2021. Published by Cambridge University Press

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References

Abdala-Roberts, L, Parra-Tabla, V and Navarro, J (2007) Is floral longevity influenced by reproductive costs and pollination success in Cohniella ascendens (Orchidaceae)? Annals of Botany 100, 13671371.CrossRefGoogle ScholarPubMed
Aizen, MA and Vázquez, DP (2006) Flowering phenologies of hummingbird plants from the temperate forest of southern South America: is there evidence of competitive displacement? Ecography 29, 357366.CrossRefGoogle Scholar
Armbruster, WS and Herzig, AL (1984) Partitioning and sharing of pollinators by four sympatric species of Dalechampia (Euphorbiaceae) in Panama. Annals of the Missouri Botanical Garden 71, 116.CrossRefGoogle Scholar
Ashman, TL and Schoen, DJ (1994) How long should flowers live? Nature 371, 788.CrossRefGoogle Scholar
Ashton, PS, Givnish, TJ and Appanah, S (1988) Staggered flowering in the Dipterocarpaceae: new insights into floral induction and the evolution of mast fruiting in the aseasonal tropics. American Naturalist 132, 4466.CrossRefGoogle Scholar
Baldock, KC, Memmott, J, Ruiz-Guajardo, JC, Roze, D and Stone, GN (2011) Daily temporal structure in African savanna flower visitation networks and consequences for network sampling. Ecology 92, 687698.CrossRefGoogle ScholarPubMed
Bascompte, J and Jordano, P (2007) Plant–animal mutualistic networks: the architecture of biodiversity. Annual Review of Ecology, Evolution, and Systematics 38, 567593.CrossRefGoogle Scholar
Bascompte, J, Jordano, P and Olesen, JM (2006) Asymmetric coevolutionary networks facilitate biodiversity maintenance. Science 312, 431433.CrossRefGoogle ScholarPubMed
Bernardello, G, Anderson, GJ, Stuessy, TF and Crawford, DJ (2001) A survey of floral traits, breeding systems, floral visitors, and pollination systems of the angiosperms of the Juan Fernández Islands (Chile). Botanical Review 67, 255308.CrossRefGoogle Scholar
Blüthgen, N, Menzel, F and Blüthgen, N (2006) Measuring specialization in species interaction networks. Ecology 6, 112.Google ScholarPubMed
Burkle, LA, Marlin, JC and Knight, TM (2013) Plant-pollinator interactions over 120 years: loss of species, co-occurrence, and function. Science 339, 16111615.CrossRefGoogle ScholarPubMed
Carvalheiro, LG, Biesmeijer, JC, Benadi, G, Fründ, J, Stang, M, Bartomeus, I … and Baldock, KC (2014) The potential for indirect effects between co-flowering plants via shared pollinators depends on resource abundance, accessibility and relatedness. Ecology Letters 17, 13891399.CrossRefGoogle ScholarPubMed
Devaux, C and Lande, R (2010) Selection on variance in flowering time within and among individuals. Evolution: International Journal of Organic Evolution 64, 13111320.Google ScholarPubMed
Development Core Team, R (2016) R: A Language and Environment for Statistical Computing. Vienna: R Foundation for Statistical Computing. Retrieved from https://www.r-project.org/.Google Scholar
Dormann, CF, Gruber, B and Fründ, J (2008) Introducing the bipartite package: analysing ecological networks. R News 8, 811.Google Scholar
Dormann, CF and Strauss, R (2014) A method for detecting modules in quantitative bipartite networks. Methods in Ecology and Evolution 5, 9098.CrossRefGoogle Scholar
Dupont, YL, Hansen, DM and Olesen, JM (2003) Structure of a plant-flower-visitor network in the high-altitude sub-alpine desert of Tenerife, Canary Islands. Ecography 26, 301310.CrossRefGoogle Scholar
Dupont, YL, Padrón, B, Olesen, JM and Petanidou, T (2009) Spatio-temporal variation in the structure of pollination networks. Oikos 118, 12611269.CrossRefGoogle Scholar
Emer, C, Memmott, J, Vaughan, IP, Montoya, D and Tylianakis, JM (2016) Species roles in plant-pollinator communities are conserved across native and alien ranges. Diversity and Distributions 22, 841852.CrossRefGoogle Scholar
Fang, Q and Huang, SQ (2012) Relative stability of core groups in pollination networks in a biodiversity hotspot over four years. PLoS ONE 7, e32663.CrossRefGoogle Scholar
Fang, Q and Huang, SQ (2013) A directed network analysis of heterospecific pollen transfer in a biodiverse community. Ecology 94, 11761185.CrossRefGoogle Scholar
Fang, Q and Huang, SQ (2016) Plant-pollinator interactions in a biodiverse meadow are rather stable and tight for 3 consecutive years. Integrative Zoology 11, 199206.CrossRefGoogle Scholar
Flanagan, RJ, Mitchell, RJ, Knutowski, D and Karron, JD (2009) Interspecific pollinator movements reduce pollen deposition and seed production in Mimulus ringens (Phrymaceae). American Journal of Botany 96, 809815.CrossRefGoogle Scholar
Fründ, J, Dormann, CF and Tscharntke, T (2011) Linné’s floral clock is slow without pollinators-flower closure and plant-pollinator interaction webs. Ecology Letters 14, 896904.CrossRefGoogle ScholarPubMed
Fründ, J, McCann, KS and Williams, NM (2016) Sampling bias is a challenge for quantifying specialization and network structure: lessons from a quantitative niche model. Oikos 125, 502513.CrossRefGoogle Scholar
Funamoto, D (2019) Plant-pollinator interactions in East Asia: a review. Journal of Pollination Ecology 25, 4668.Google Scholar
Gillespie, RG and Roderick, GK (2002) Arthropods on islands: colonization, speciation, and conservation. Annual Review of Entomology 47, 595632.CrossRefGoogle ScholarPubMed
Hoehn, P, Tscharntke, T, Tylianakis, JM and Steffan-Dewenter, I (2008) Functional group diversity of bee pollinators increases crop yield. Proceedings of the Royal Society B: Biological Sciences 275, 22832291.CrossRefGoogle ScholarPubMed
Jordano, P, Bascompte, J and Olesen, JM (2003) Invariant properties in coevolutionary networks of plant-animal interactions. Ecology Letters 6, 6981.CrossRefGoogle Scholar
Jorgensen, R and Arathi, HS (2013) Floral longevity and autonomous selfing are altered by pollination and water availability in Collinsia heterophylla . Annals of Botany 112, 821828.CrossRefGoogle ScholarPubMed
Kaiser-Bunbury, CN and Blüthgen, N (2015) Integrating network ecology with applied conservation: a synthesis and guide to implementation. AoB Plants 7, plv076.CrossRefGoogle Scholar
Kaiser-Bunbury, CN, Memmott, J and Müller, CB (2009) Community structure of pollination webs of Mauritian heathland habitats. Perspectives in Plant Ecology, Evolution and Systematics 11, 241254.CrossRefGoogle Scholar
Kaiser-Bunbury, CN, Muff, S, Memmott, J and Müller, CB (2010) The robustness of pollination networks to the loss of species and interactions: a quantitative approach incorporating pollinator behaviour. Ecology Letters 13, 442452.CrossRefGoogle ScholarPubMed
Lienhard, A, Mirwald, L, Hötzl, T, Kranner, I and Kastberger, G. (2010) Trade-off between foraging activity and infestation by nest parasites in the primitively eusocial bee Halictus scabiosae. Psyche: A Journal of Entomology 2010, 707501.Google Scholar
Maguvu, TE (2018) Effect of different photoperiods on flower opening time in Portulaca umbraticola . The Horticulture Journal 87, 124131.CrossRefGoogle Scholar
Medan, D, Basilio, AM, Devoto, M, Bartoloni, NJ, Torretta, JP and Petanidou, T (2006) Measuring generalization and connectance in temperate, year-long active systems. In Waster NM and Ollerton J (eds), Plant-Pollinator Interactions: From Specialization to Generalization. Chicago, IL: University of Chicago Press, pp. 245259.Google Scholar
Mitchell, RJ, Flanagan, RJ, Brown, BJ, Waser, NM and Karron, JD (2009) New frontiers in competition for pollination. Annals of Botany 103, 14031413.CrossRefGoogle ScholarPubMed
Miyake, T and Yahara, T (1999) Theoretical evaluation of pollen transfer by nocturnal and diurnal pollinators: when should a flower open? Oikos 86, 233240.CrossRefGoogle Scholar
Olesen, JM, Bascompte, J, Elberling, H and Jordano, P (2008) Temporal dynamics in a pollination network. Ecology 89, 15731582.CrossRefGoogle Scholar
Patefield, WM (1981) Algorithm AS 159: An efficient method of generating random R x C tables with given row and column totals. Journal of the Royal Statistical Society: Series C (Applied Statistics) 30, 9197.Google Scholar
Pauw, A (2013) Can pollination niches facilitate plant coexistence? Trends in Ecology and Evolution 28, 3037.CrossRefGoogle ScholarPubMed
Petanidou, T, Kallimanis, AS, Tzanopoulos, J, Sgardelis, SP and Pantis, JD (2008) Long-term observation of a pollination network: fluctuation in species and interactions, relative invariance of network structure and implications for estimates of specialization. Ecology Letters 11, 564575.CrossRefGoogle ScholarPubMed
Sajjad, A, Saeed, S, Ali, M, Khan, FZA, Kwon, YJ and Devoto, M (2017) Effect of temporal data aggregation on the perceived structure of a quantitative plant-floral visitor network. Entomological Research 47, 380387.CrossRefGoogle Scholar
Schwarz, B, Vázquez, DP, CaraDonna, PJ, Knight, TM, Benadi, G, Dormann, CF, … and Fründ, J (2020) Temporal scale-dependence of plant-pollinator networks. Oikos 129, 12891302.CrossRefGoogle Scholar
Souza, CS, Maruyama, PK, Aoki, C, Sigrist, MR, Raizer, J, Gross, CL and de Araujo, AC (2018) Temporal variation in plant-pollinator networks from seasonal tropical environments: higher specialization when resources are scarce. Journal of Ecology 106, 24092420.CrossRefGoogle Scholar
Stone, GN, Gilbert, F, Willmer, P, Potts, S, Semida, F and Zalat, S (1999) Windows of opportunity and the temporal structuring of foraging activity in a desert solitary bee. Ecological Entomology 24, 208221.CrossRefGoogle Scholar
Stuessy, TF, Crawford, DJ, López-Sepúlveda, P and Ruiz, EA. (eds) (2017) Plants of Oceanic Islands: Evolution, Biogeography, and Conservation of the Flora of the Juan Fernández (Robinson Crusoe) Archipelago. Cambridge: Cambridge University Press.CrossRefGoogle Scholar
Taylor, B and Hayes, DE (1980) The tectonic evolution of the South China Basin. In The Tectonic and Geologic Evolution of Southeast Asian Seas and Islands. Geophysics Monograph Series. Washington, D.C.: AGU, vol. 23, pp. 89104.CrossRefGoogle Scholar
Tong, Y, Jian, SG, Chen, Q, Li, YL and Xing, F (2013) Vascular plant diversity of the Paracel Islands, China. Biodiversity Science 21, 364374.Google Scholar
Tong, ZY and Huang, SQ (2018) Safe sites of pollen placement: a conflict of interest between plants and bees? Oecologia 186, 163171.CrossRefGoogle ScholarPubMed
Traveset, A, Heleno, R, Chamorro, S, Vargas, P, McMullen, CK, Castro-Urgal, R, … and Olesen, JM (2013) Invaders of pollination networks in the Galápagos Islands: emergence of novel communities. Proceedings of the Royal Society B: Biological Sciences 280, 20123040.CrossRefGoogle ScholarPubMed
Traveset, A, Tur, C, Trøjelsgaard, K, Heleno, R, Castro-Urgal, R and Olesen, JM (2016) Global patterns of mainland and insular pollination networks. Global Ecology and Biogeography 25, 880890.CrossRefGoogle Scholar
Trøjelsgaard, K and Olesen, JM (2013) Macroecology of pollination networks. Global Ecology and Biogeography 22, 149162.CrossRefGoogle Scholar
van Der Kooi, CJ, Pen, I, Staal, M, Stavenga, DG and Elzenga, JTM (2016) Competition for pollinators and intra-communal spectral dissimilarity of flowers. Plant Biology 18, 5662.CrossRefGoogle ScholarPubMed
van Doorn, WG and Kamdee, C (2014) Flower opening and closure: an update. Journal of Experimental Botany 65, 57495757.CrossRefGoogle ScholarPubMed
van Doorn, WG and van Meeteren, U (2003) Flower opening and closure: a review. Journal of Experimental Botany 54, 18011812.CrossRefGoogle ScholarPubMed
Vázquez, DP, Blüthgen, N, Cagnolo, L and Chacoff, NP (2009) Uniting pattern and process in plant-animal mutualistic networks: a review. Annals of Botany 103, 14451457.CrossRefGoogle ScholarPubMed
Vesprini, JL and Pacini, E (2005) Temperature-dependent floral longevity in two Helleborus species. Plant Systematics and Evolution 252, 6370.CrossRefGoogle Scholar
Vizentin-Bugoni, J, Maruyama, PK, Debastiani, VJ, Duarte, LDS, Dalsgaard, B and Sazima, M (2016) Influences of sampling effort on detected patterns and structuring processes of a Neotropical plant-hummingbird network. Journal of Animal Ecology 85, 262272.CrossRefGoogle ScholarPubMed
Von Hase, A, Cowling, RM and Ellis, AG (2006) Petal movement in cape wildflowers protects pollen from exposure to moisture. Plant Ecology 184, 7587.CrossRefGoogle Scholar
Whittaker, RJ and Fernández-Palacios, JM (2007) Island Biogeography: Ecology, Evolution, and Conservation. Oxford: Oxford University Press.Google Scholar
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