Skip to main content

Advertisement

SpringerLink
Log in

Forest connectivity boosts pollen flow among populations of the oil-producing Nierembergia linariifolia

  • Research Article
  • Published:
Landscape Ecology Aims and scope Submit manuscript

Abstract

Context

The process of forest fragmentation determines landscapes with isolated forest patches immersed in a distinct matrix. This process may hinder pollinator movement throughout the landscape, which may negatively impact on pollen flow among native plant populations.

Objectives

We evaluated the effect of the loss of forest connectivity on pollen dispersal by specialized native bees in the oil-producing and self-incompatible Nierembergia linariifolia.

Methods

We estimated pollen flow between plants of N. linariifolia at an agroecosystem with remnant forest of central Argentina. Six plant populations (source populations) were treated with fluorescent dyes as pollen analogues, and stigmata of recipient plants were collected to seek for dye particles. Dye deposition rate was assessed for plants that were connected through remnant forest to a source population or unconnected by a crop matrix, and at increasing distances to a source population.

Results

Deposition rate per plant was higher in connected than in unconnected plants, and decreased with increasing distances to a source population in an exponential fashion. Most of the dispersal events between connected plants occurred at the vicinity of a source population. Long dispersal events (up to 1259 m) were recorded between plants located at neighbouring forest patches separated by an agricultural matrix.

Conclusions

Landscape connectivity through forest remnants is key to enhance pollen flow between self-incompatible plants such as N. linariifolia. Besides, the evidence of pollen dispersal through the agricultural matrix pinpoints the essential role of native pollinators in maintaining pollen flow among unconnected plant populations in fragmented landscapes.

This is a preview of subscription content, log in via an institution to check access.

Access this article

Log in via an institution

Price excludes VAT (USA)
Tax calculation will be finalised during checkout.

Instant access to the full article PDF.

Institutional subscriptions

Fig. 1
Fig. 2
Fig. 3
Fig. 4
Fig. 5
Fig. 6
Fig. 7

Similar content being viewed by others

Data availability

The data that supports the findings of this study is available at the Dryad Digital Repository (https://doi.org/10.5061/dryad.08kprr55c).

Code availability

Not applicable.

References

  • Adler LS, Irwin RE (2006) Comparison of pollen transfer dynamics by multiple floral visitors: experiments with pollen and fluorescent dye. Ann Bot-Lond 97(1):141–150

    Article  Google Scholar 

  • Aguiar CML (2003) Flower visits of Centris bees (Hymenoptera: Apidae) in an area of caatinga (Bahia, Brazil). Stud Neotrop Fauna Environ 38(1):41–45

    Article  Google Scholar 

  • Aguilar R, Galetto L (2004) Effects of forest fragmentation on male and female reproductive success in Cestrum parqui(Solanaceae). Oecologia 138(4):513–520.

  • Aguilar R, Ashworth L, Galetto L, Aizen MA (2006) Plant reproductive susceptibility to habitat fragmentation: review and synthesis through a meta-analysis. Ecol Lett 9(8):968–980

    Article  PubMed  Google Scholar 

  • Aguilar R, Quesada M, Ashworth L, Herrerias-Diego Y, Lobo J (2008) Genetic consequences of habitat fragmentation in plant populations: Susceptible signals in plant traits and methodological approaches. Mol Ecol 17(24):5177–5188

  • Aguilar R, Calviño A, Ashworth L, Aguirre-Acosta N, Carbone LM, Albrieu-Llinás G, Nolasco M, Ghilardi A, Cagnolo L (2018) Unprecedented plant species loss after a decade in fragmented subtropical Chaco Serrano forests. Plos One 13(11): e0206738

  • Aizen MA, Ashworth L, Galetto L (2002) Reproductive success in fragmented habitats: do compatibility systems and pollination specialization matter? J Veg Sci 13(6):885–892

    Article  Google Scholar 

  • Aquino DS, Amela García MT (2019) Pollen dispersal in a population of Passiflora caerulea: spatial components and ecological implications. Plant Ecol 220(9):845–860

    Article  Google Scholar 

  • Austerlitz F, Dick CW, Dutech C, Klein EK, Oddou-Muratorio S, Smouse PE, Sork VL (2004) Using genetic markers to estimate the pollen dispersal curve. Mol Ecol 13(4):937–954

    Article  PubMed  Google Scholar 

  • Bates D, Maechle M, Bolker B, Walker S (2015) Fitting linear mixed-effects models using lme4. J Stat Softw 67(1):1–48

    Article  Google Scholar 

  • Beekman M, Ratnieks FLW (2000) Long-range foraging by the honey-bee Apis mellifera L. Funct Ecol 14(4):490–496

    Article  Google Scholar 

  • Buchmann SL (1987) The ecology of oil flowers and their bees. Annu Rev Ecol Syst 18:343–369

    Article  Google Scholar 

  • Buschi CA, Pomilio AB (1987) Pyrrole-3-carbamdine: a lethal principle from Nierembergia hippomanica. Phytochemistry 26(3):863–865

    Article  CAS  Google Scholar 

  • Cabido M, Zeballos SR, Zak M, Carranza ML, Giorgis MA, Cantero JJ, Acosta ATR (2018) Native woody vegetation in central Argentina: classification of Chaco and Espinal forests. Appl Veg Sci 21(2):298–311

    Article  Google Scholar 

  • Cáceres DM (2015) Accumulation by dispossession and socio-environmental conflicts caused by the expansion of agribusiness in Argentina. J Agrar Change 15(1):116–147

    Article  Google Scholar 

  • Cocucci AA (1984) Polinizacion en Nierembergia hippomanica (Solanaceae). Kurtziana 17:31–47

    Google Scholar 

  • Cocucci AA (1991) Pollination biology of Nierembergia (Solanaceae). Plant Syst Evol 174(1):17–35

    Article  Google Scholar 

  • Cocucci AA, Hunziker AT (1995) Estudios sobre Solanaceae. XLI. Nierembergia linariaefolia y N. pulchella: sus sinónimos y variedades. Darwiniana 33(1):33–42

    Google Scholar 

  • Cagnolo L, Cabido M, Valladares G (2006) Plant species richness in the Chaco Serrano Woodland from central Argentina: Ecological traits and habitat fragmentation effects. Biol Conserv 132(4):510–519

  • Cosacov A, Nattero J, Cocucci AA (2008) Variation of pollinator assemblages and pollen limitation in a locally specialized system: the oil-producing Nierembergia linariifolia (Solanaceae). Ann Bot-Lond 102(5):723–734

    Article  Google Scholar 

  • Cranmer L, McCollin D, Ollerton J (2012) Landscape structure influences pollinator movements and directly affects plant reproductive success. Oikos 121(4):562–568

    Article  Google Scholar 

  • Cunningham SA (2000) Depressed pollination in habitat fragments causes low fruit set. P R Soc B-Biol Sci 267(1448):1149–1152

    Article  CAS  Google Scholar 

  • Danner N, Härtel S, Steffan-Dewenter I (2014) Maize pollen foraging by honey bees in relation to crop area and landscape context. Basic Appl Ecol 15(8):677–684

    Article  Google Scholar 

  • Defries RS, Foley JA, Asner GP (2004) Land-use choice : balancing human needs and ecosystem function. Front Ecol Environ 2(5):249–257

    Article  Google Scholar 

  • Díaz S, Demissew S, Carabias J, Joly C, Lonsdale M, Ash N et al (2015) The IPBES conceptual framework: connecting nature and people. Curr Opin Environ Sustain 14:1–16

    Article  Google Scholar 

  • Fahrig L (2003) Effects of habitat fragmentation on biodiversity. Annu Rev Ecol Syst 34(1):487–515

    Article  Google Scholar 

  • Fenster CB, Armbruster WS, Wilson P, Dudash MR, Thomson JD (2004) Pollination syndromes and floral specialization. Annu Rev Ecol Evol Syst 35:375–403

    Article  Google Scholar 

  • Ferreira PA, Boscolo D, Viana BF (2013) What do we know about the effects of landscape changes on plant-pollinator interaction networks? Ecol Indic 31:35–40

  • Ferreira F, Torres C, Bracamonte E, Galetto L (2017) Effects of herbicide glyphosate on non-target plant native species form Chaco forests from Argentina. Ecotox Environ Saf 144:360–368

    Article  CAS  Google Scholar 

  • Foley JA, DeFries R, Asner GP, Barford C, Bonan G, Carpenter SR et al (2005) Global consequences of land use. Science 309(5734):570–574

    Article  CAS  PubMed  Google Scholar 

  • Franzén M, Larsson M, Nilsson SG (2009) Small local population sizes and high habitat patch fidelity in a specialised solitary bee. J Insect Conserv 13(1):89–95

    Article  Google Scholar 

  • Galetto L, Aizen MA, Arizmendi MC, Freitas BM, Garibaldi LA, Giannini TC et al (2022) Risks and opportunities associated with pollinators’ conservation and management of pollination services in Latin America. Ecol Austral 32:055–076

    Article  Google Scholar 

  • Garibaldi LA, Steffan-Dewenter I, Kremen C, Morales JM, Bommarco R, Cunningham SA et al (2011) Stability of pollination services decreases with isolation from natural areas despite honey bee visits. Ecol Lett 14(10):1062–1072

    Article  PubMed  Google Scholar 

  • Gathmann A, Tscharntke T (2002) Foraging ranges of solitary bees. J Anim Ecol 71(5):757–764

    Article  Google Scholar 

  • Gonçalves L, Silva CI, Buschini MLT (2012) Collection of pollen grains by Centris (Hemisiella) tarsata Smith (Apidae: Centridini): is C. tarsata an oligolectic or polylectic species? Zool Stud 51(2):195–203

    Google Scholar 

  • Green RE, Cornell SJ, Scharlemann JPW, Balmford A (2005) Farming and the fate of wild nature. Science 307(5709):550–555

    Article  CAS  PubMed  Google Scholar 

  • Greenleaf SS, Williams NM, Winfree R, Kremen C (2007) Bee foraging ranges and their relationship to body size. Oecologia 153(3):589–596

    Article  PubMed  Google Scholar 

  • Hadley AS, Betts MG (2012) The effects of landscape fragmentation on pollination dynamics: absence of evidence not evidence of absence. Biol Rev 87(3):526–544

    Article  PubMed  Google Scholar 

  • Hansen MC, Potapov PV, Moore R, Hancher M, Turubanova SA, Tyukavina A et al (2013) High-resolution global maps of 21st-century forest cover change. Science 342(6160):850–853

    Article  CAS  PubMed  Google Scholar 

  • Harrison XA (2014) Using observation-level random effects to model overdispersion in count data in ecology and evolution. PeerJ 2:e616

    Article  PubMed  PubMed Central  Google Scholar 

  • Hartig F (2020) DHARMa: residual diagnostics for hierarchical (Multi-Level/Mixed) regression models. R package version 0.3.3.0. https://CRAN.R-project.org/package=DHARMa

  • Hofmann MM, Fleischmann A, Renner SS (2020) Foraging distances in six species of solitary bees with body lengths of 6 to 15 mm, inferred from individual tagging, suggest 150 m-rule-of-thumb for flower strip distances. J Hymenop Res 77:105

    Article  Google Scholar 

  • Holzschuh A, Dormann CF, Tscharntke T, Steffan-Dewenter I (2011) Expansion of mass-flowering crops leads to transient pollinator dilution and reduced wild plant pollination. Proc R Soc B-Biol Sci 278(1723):3444–3451

    Article  Google Scholar 

  • Holzschuh A, Dainese M, González-Varo JP, Mudri-Stojnić S, Riedinger V, Rundlöf M et al (2016) Mass-flowering crops dilute pollinator abundance in agricultural landscapes across Europe. Ecol Lett 19(10):1228–1236

    Article  PubMed  PubMed Central  Google Scholar 

  • Hoyos LE, Cingolani AM, Zak MR, Vaieretti MV, Gorla DE, Cabido MR (2012) Deforestation and precipitation patterns in the arid Chaco forests of central Argentina. Appl Veg Sci 16(2):260–271

    Article  Google Scholar 

  • IPBES (2016) The assessment report of the Intergovernmental Science-Policy Platform on Biodiversity and Ecosystem Services on pollinators, pollination and food production. Secretariat of the Intergovernmental Science-Policy Platform on Biodiversity and Ecosystem Services, Bonn, Germany

  • Janzen DH (1971) Euglossine bees as long-distance pollinators of tropical plants. Science 171(3967):203–205

    Article  CAS  PubMed  Google Scholar 

  • Jules ES, Shahani P (2003) A broader ecological context to habitat fragmentation: why matrix habitat is more important than we thought. J Veg Sci 14(3):459–464

    Article  Google Scholar 

  • Kapyla M (1978) Foraging distance of a small solitary bee, Chelostoma maxillosum (Hymenoptera, Megachilidae). Ann Entomol Fenn 35:63–64

    Google Scholar 

  • Kennedy CM, Lonsdorf E, Neel MC, Williams NM, Ricketts TH, Winfree R et al (2013) A global quantitative synthesis of local and landscape effects on wild bee pollinators in agroecosystems. Ecol Lett 16(5):584–599

    Article  PubMed  Google Scholar 

  • Kormann U, Scherber C, Tscharntke T, Klein N, Larbig M, Valente JJ, Hadley AS, Betts MG (2016) Corridors restore animal-mediated pollination in fragmented tropical forest landscapes. P R Soc B-Biol Sci 283(1823):20152347

    Google Scholar 

  • LanderTA BDH, Harris SA (2010) Fragmented but not isolated: contribution of single trees, small patches and long-distance pollen flow to genetic connectivity for Gomortega keule, an endangered Chilean tree. Biol Conserv 143(11):2583–2590

    Article  Google Scholar 

  • Leimu R, Vergeer P, Angeloni F, Ouborg NJ (2010) Habitat fragmentation, climate change, and inbreeding in plants. Ann NY Acad Sci 1195:84–98

    Article  PubMed  Google Scholar 

  • Lienert J (2004) Habitat fragmentation effects of fitness of plant populations: a review. J Nat Conserv 12(1):53–72

    Article  Google Scholar 

  • Lüdecke D (2018) ggeffects: tidy data frames of marginal effects from regression models. J Open Sour Softw 3(26):772

    Article  Google Scholar 

  • Malerbo-Souza DT, da Silva TG, de Andrade MO, de Farias LR, Medeiros NMG (2018) Factors affecting the foraging behavior of bees in different maize hybrids. Revista Brasileira De Ciências Agrárias 13(3):1–8

    Article  Google Scholar 

  • Maubecin CC, Rocamundi N, Palombo N, Aguirre LA, Cocucci AA, Sérsic AN (2021) Teasing out the functional groups of oil-collecting bees in the light of the pollination of Nierembergia flowers. Arthropod-Plant Inte 15(5):809–819

    Article  Google Scholar 

  • Mayer C, Van Rossum F, Jacquemart AL (2012) Evaluating pollen flow indicators for an insect-pollinated plant species. Basic Appl Ecol 13(8):690–697

    Article  Google Scholar 

  • Menz MHM, Phillips RD, Winfree R, Kremen C, Aizen MA, Johnson SD, Dixon KW (2011) Reconnecting plants and pollinators: challenges in the restoration of pollination mutualisms. Trends Plant Sci 16(1):4–12

    Article  CAS  PubMed  Google Scholar 

  • Minnaar C, Anderson B (2019) Using quantum dots as pollen labels to track the fates of individual pollen grains. Methods Ecol Evol 10(5):604–614

    Article  Google Scholar 

  • Musicante M (2013) Fragmentación del hábitat y su efecto sobre comunidades de polinizadores y antófilos (Hymenoptera: Aculeata) en el Bosque Chaqueño Serrano. PhD Thesis. Fac. Cs. Ex., F. y Naturales, UNC. Córdoba, Argentina

  • Odini A, Rivero R, Correa FR, Mendez C (1995) Intoxicación por Nierembergia hippomanica en bovinos y ovinos. Veterinaria (montevideo) 31(127):3–8

    Google Scholar 

  • Ottewell K, Grey E, Castillo F, Karubian J (2012) The pollen dispersal kernel and mating system of an insect-pollinated tropical palm Oenocarpus Bataua. Heredity 109(6):332–339

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • R Core Team (2020) R: a language and environment for statistical computing. R Foundation for Statistical Computing, Vienna, Austria. https://www.R-project.org/

  • Rasmussen C, Olesen JM (2000) Oil flowers and oil-collecting bees. Scand Assoc Pollinat Ecol Honours Knut Faegri 39:23–31

    Google Scholar 

  • Stanley DA, Stout JC (2014) Pollinator sharing between mass-flowering oilseed rape and co-flowering wild plants: implications for wild plant pollination. Plant Ecol 215(3):315–325

    Article  Google Scholar 

  • Thomson JD, Eisenhart KS (2003) Rescue of stranded pollen grains by secondary transfer. Plant Spec Biol 18(2–3):67–74

    Article  Google Scholar 

  • Torino F, Colque Caro LA, Martinez OG, Micheloud JF (2017) Intoxicación experimental con Nierembergia linariifolia var. linariifolia en cabras. FAVE-Sección Ciencias Veterinarias 16(2):66–69

    Article  Google Scholar 

  • Townsend PA, Levey DJ (2010) An experimental test of whether habitat corridors affect pollen transfer. Ecology 86(2):466–475

    Article  Google Scholar 

  • Vallejos M, Volante JN, Mosciaro MJ, Vale LM, Bustamante ML, Paruelo JM (2015) Transformation dynamics of the natural cover in the Dry Chaco ecoregion: a plot level geo-database from 1976 to 2012. J Arid Environ 123:3–11

    Article  Google Scholar 

  • Van Rossum F (2010) Reproductive success and pollen dispersal in urban populations of an insect-pollinated hay-meadow herb. Perspect Plant Ecol 12(1):21–29

    Article  Google Scholar 

  • Van Rossum F, Triest L (2010) Pollen dispersal in an insect-pollinated wet meadow herb along an urban river. Landsc Urban Plan 95(4):201–208

    Article  Google Scholar 

  • Van Rossum F, Triest L (2012) Stepping-stone populations in linear landscape elements increase pollen dispersal between urban forest fragments. Plant Ecol Evol 145(3):332–340

    Article  Google Scholar 

  • Van Geert A, Van Rossum F, Triest L (2010) Do linear landscape elements in farmland act as biological corridors for pollen dispersal? J Ecol 98(1):178–187

    Article  Google Scholar 

  • Van Geert A, Triest L, Van Rossum F (2014) Does the surrounding matrix influence corridor effectiveness for pollen dispersal in farmland? Perspect Plant Ecol 16(4):180–189

    Article  Google Scholar 

  • Van Rossum F, Stiers I, Van Geert A, Triest L, Hardy OJ (2011) Fluorescent dye particles as pollen analogues for measuring pollen dispersal in an insect-pollinated forest herb. Oecologia 165(3):663–674

    Article  PubMed  Google Scholar 

  • Van Rossum F, Vereecken NJ, Brédat E, Michez D (2012) Pollen dispersal and fruit production in Vaccinium oxycoccos and comparison with its sympatric congener V. uliginosum. Plant Biol 15(2):344–352

    Article  PubMed  Google Scholar 

  • Van Rossum F, Leprince N, Mayer C, Raabová J, Hans G, Jacquemart AL (2015) What influences pollen dispersal in the clonal distylous Menyanthes trifoliata (Menyanthaceae)? Plant Ecol Evol 148(2):199–212

    Article  Google Scholar 

  • Volpe NL, Robinson WD, Frey SJK, Hadley AS, Betts MG (2016) Tropical forest fragmentation limits movements, but not occurrence of a generalist pollinator species. PLoS ONE 11(12):1–13

    Article  CAS  Google Scholar 

  • Wanderley AM, dos Santos EKR, Galetto L, Benko-Iseppon AM, Machado ICS (2020) Pollen flow within and among isolated populations of two rare, self-compatible plant species from inselbergs of Northeast Brazil. Plant Ecol 221(4):229–240

    Article  Google Scholar 

  • Wickham H (2016) ggplot2: elegant graphics for data analysis. Springer-Verlag, Cham

    Book  Google Scholar 

  • Young HJ (2002) Diurnal and nocturnal pollination of Silene alba (Caryophyllaceae). Am J Bot 89(3):433–440

    Article  PubMed  Google Scholar 

  • Zak MR, Cabido M, Cáceres D, Díaz S (2008) What drives accelerated land cover change in central Argentina? Synergistic consequences of climatic, socioeconomic, and technological factors. Environ Manag 42(2):181–189

    Article  Google Scholar 

  • Zuur A, Ieno E, Walker N, Saveliev A, Smith G (2009) Mixed effect models and extensions in ecology with R. Springer, New York

    Book  Google Scholar 

Download references

Acknowledgements

We thank anonymous reviewers for useful suggestions and comments, Consejo Nacional de Investigaciones Científicas y Técnicas (CONICET), Secretaría de Ciencia y Tecnología de la Universidad Nacional de Córdoba (UNC) and FONCYT for financial support. We thank the landowners for the access to the fields.

Funding

Foncyt, PICT-2015-0538. “Efectos de la biodiversidad sobre el funcionamiento de agro-ecosistemas: evaluación experimental a distintas escalas espaciales”. Proyecto Consolidar SECYT (UNC), Res. 411/18. 2018-2021. “Fragmentación de bosque y pérdida de biodiversidad por el cambio en el uso del suelo: evaluación de umbrales genéticos y ecológicos en agroecosistemas".

Author information

Authors and Affiliations

  1. Instituto Multidisciplinario de Biología Vegetal, FCEFyN (CONICET-Universidad Nacional de Córdoba), Vélez Sarsfield 1611, CC 495, Córdoba, Argentina

    Pablo Y. Huais, Gabriel Grilli & Leonardo Galetto

  2. Departamento de Matemática, Facultad de Ciencias Exactas, Físicas y Naturales, Universidad Nacional de Córdoba, Córdoba, Argentina

    Pablo Y. Huais

  3. Departamento de Diversidad Biológica y Ecología, Facultad de Ciencias Exactas, Físicas y Naturales, Universidad Nacional de Córdoba, Córdoba, Argentina

    Leonardo Galetto

Authors
  1. Pablo Y. Huais
    View author publications

    You can also search for this author in PubMed Google Scholar

  2. Gabriel Grilli
    View author publications

    You can also search for this author in PubMed Google Scholar

  3. Leonardo Galetto
    View author publications

    You can also search for this author in PubMed Google Scholar

Contributions

PYH conceived the initial idea. PYH, GG and LG planned the experiment. PYH and GG performed the experiment. All authors discussed the results and contributed to the final manuscript.

Corresponding author

Correspondence to Pablo Y. Huais.

Ethics declarations

Conflict of interest

Not applicable.

Ethical approval

Not applicable.

Consent to participate

Not applicable.

Consent for publication

Not applicable.

Additional information

Publisher's Note

Springer Nature remains neutral with regard to jurisdictional claims in published maps and institutional affiliations.

Rights and permissions

Reprints and permissions

About this article

Check for updates. Verify currency and authenticity via CrossMark

Cite this article

Huais, P.Y., Grilli, G. & Galetto, L. Forest connectivity boosts pollen flow among populations of the oil-producing Nierembergia linariifolia. Landsc Ecol 37, 2435–2450 (2022). https://doi.org/10.1007/s10980-022-01483-z

Download citation

  • Received:

  • Accepted:

  • Published:

  • Issue Date:

  • DOI: https://doi.org/10.1007/s10980-022-01483-z

Keywords

Search

Navigation