Skip to main content
Log in

Impact of alien rats and honeybees on the reproductive success of an ornithophilous endemic plant in Canarian thermosclerophyllous woodland relicts

  • Original Paper
  • Published:
Biological Invasions Aims and scope Submit manuscript

Abstract

Islands harbor a considerable portion of global biodiversity and endemic biota, and also are the recipients of the largest proportional numbers of alien invaders. Such invaders may jeopardize the performance of native species, through either their direct or indirect effects. In this study, we investigated the reproductive ecology of the endemic scrambling perennial herb Canarina canariensis in remnants of the former thermosclerophyllous woodland of Tenerife (Canary Islands), assessing how two widespread alien invasive species, the honeybee (Apis mellifera) and the black rat (Rattus rattus), affect its reproductive success. Apis mellifera visits its flowers whereas the black rat consumes both its flowers and fruits. Here, we compared the pollination effectiveness of different animal guilds (vertebrates vs insects) by means of selective exclosures and determined the level of floral herbivory. Three bird species (Phylloscopus canariensis, Cyanistes teneriffae and Sylvia melanocephala), a lizard (Gallotia galloti) and two insects (A. mellifera and the butterfly Gonepteryx cleobule) were the main flower visitors. Phylloscopus canariensis was the most frequent visitor in the early flowering season whereas A. mellifera predominated in the flowers during mid and late flowering periods. Birds increased fruit set, whilst lizards and insects had a negligible effect. Rats consumed about 10% of the flowers and reduced fruit set to one third. Besides contributing little to plant reproduction, A. mellifera might interfere with bird pollination by depleting flowers of nectar. We conclude that both alien species can threaten C. canariensis reproduction and hence population sustainability in the thermosclerophyllous vegetation. Apis mellifera, in particular, may become especially detrimental if apiculture keeps expanding, or if this bee becomes active earlier in the season due to global warming.

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

Access this article

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

Instant access to the full article PDF.

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

Similar content being viewed by others

References

  • Agüero JI, Rollin O, Torretta JP et al (2018) Impactos de la abeja melífera sobre plantas y abejas silvestres en hábitats naturales. Ecosistemas 27:60–69

    Article  Google Scholar 

  • Antonovics J (1968) Evolution in closely adjacent plant populations. V. Evolution of self-fertility. Heredity (Edinb) 23:219–238

    Article  Google Scholar 

  • Arechavaleta M, Rodríguez S, Zurita N, García A (eds) (2010) Lista de especies silvestres de Canarias. Hongos, plantas y animales terrestres 2009. Gobierno de Canarias

  • Ashman T-L, Schoen DJ (1994) How long should flowers live? Nature 371:788–791

    Article  CAS  Google Scholar 

  • Barreno E, Bramwell D, Cabezudo B et al (1984) Listado de plantas endémicas, raras o amenazadas de España. Inf Ambient 3:49–72

    Google Scholar 

  • Bellard C, Rysman J, Leroy B et al (2017) A global picture of biological invasion threat on islands. Nat Ecol Evol 1:1862–1869

    Article  PubMed  Google Scholar 

  • Bertsch A (1983) Nectar production of Epilobium angustifolium L. at different air humidities; nectar sugar in individual flowers and the optimal foraging theory. Oecologia 59:40–48

    Article  CAS  PubMed  Google Scholar 

  • Busch JW, Delph LF (2012) The relative importance of reproductive assurance and automatic selection as hypotheses for the evolution of self-fertilization. Ann Bot 109:553–562

    Article  PubMed  Google Scholar 

  • Cuddihy LW, Stone CP (1990) Alterations of native Hawaiian vegetation. Effects of humans, their activities and introductions. Cooperative National Park Resources Unit., University of Hawaii, Manoa, USA

  • Delgado JD (2000) Selection and treatment of fleshy fruits by the Ship Rat (Rattus rattus L.) in the Canarian laurel forest. Mammalia 64:11–18

    Google Scholar 

  • Delgado J, Arévalo J, Fernández-Palacios J (2001) Road and topography effects on invasion: edge effects in rat foraging patterns in two oceanic island forests (Tenerife, Canary Islands). Ecography (Cop) 24:539–546

    Article  Google Scholar 

  • Dirección General de Ganadería (2006) Panorámica del sector apícola en la comunidad autónoma

  • Donlan CJ, Howald GR, Tershy BR, Croll DA (2003) Evaluating alternative rodenticides for island conservation: roof rat eradication from the San Jorge Islands, Mexico. Biol Conserv 114:29–34

    Article  Google Scholar 

  • Dupont YL, Hansen DM, Olesen JM (2003) Structure of a plant–flower-visitor network in the high-altitude sub-alpine desert of Tenerife, Canary Islands. Ecography (Cop) 26:301–310

    Article  Google Scholar 

  • Dupont YL, Hansen DM, Rasmussen JT, Olesen JM (2004a) Evolutionary changes in nectar sugar composition associated with switches between bird and insect pollination: the Canarian bird-flower element revisited. Funct Ecol 18:670–676

    Article  Google Scholar 

  • Dupont YL, Hansen DM, Valido A, Olesen JM (2004b) Impact of introduced honey bees on native pollination interactions of the endemic Echium wildpretii (Boraginaceae) on Tenerife, Canary Islands. Biol Conserv 118:301–311

    Article  Google Scholar 

  • Ecroyd CE (1996) The ecology of Dactylanthus taylorii and threats to its survival. N Z J Ecol 20:81–100

    Google Scholar 

  • Faegri K, van der Pijl L (1966) The principles of pollination ecology. Pergamon Press, Oxford

    Google Scholar 

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

    Article  Google Scholar 

  • Fernández de Castro AG, Moreno-Saiz JC, Fuertes-Aguilar J (2017) Ornithophily for the nonspecialist: differential pollination efficiency of the Macaronesian island paleoendemic Navaea phoenicea (Malvaceae) by generalist passerines. Am J Bot 104:1556–1568

    Article  PubMed  Google Scholar 

  • Fernández-Palacios JM, Otto R, Delgado JD, et al (2008) Los bosques termófilos de Canarias. Proyecto LIFE04/NAT/ES/000064. Excmo. Cabildo Insular de Tenerife., Santa Cruz de Tenerife

  • Giblin DE (2005) Variation in floral longevity between populations of Campanula rotundifolia (Campanulaceae) in response to fitness accrual rate manipulation. Am J Bot 92:1714–1722

    Article  PubMed  Google Scholar 

  • González-Castro A, Calviño-Cancela M, Nogales M (2015) Comparing seed dispersal effectiveness by frugivores at the community level. Ecology 96:808–818

    Article  PubMed  Google Scholar 

  • Han F, Wallberg A, Webster MT (2012) From where did the Western honeybee (Apis mellifera) originate? Ecol Evol 2:1949–1957

    Article  PubMed  PubMed Central  Google Scholar 

  • Hansen DM, Olesen JM, Jones CG (2002) Trees, birds and bees in Mauritius: exploitative competition between introduced honey bees and endemic nectarivorous birds? J Biogeogr 29:721–734

    Article  Google Scholar 

  • Harper GA, Bunbury N (2015) Invasive rats on tropical islands: their population biology and impacts on native species. Glob Ecol Conserv 3:607–627

    Article  Google Scholar 

  • Hernández MA, Martín A, Nogales M (1999) Breeding success and predation on artificial nests of the endemic pigeons Bolle’s laurel pigeon Columba bollii and white-tailed laurel pigeon Columba junoniae in the laurel forest of Tenerife (Canary Islands). Ibis (Lond 1859) 141:52–59

    Article  Google Scholar 

  • Herrera CM (1985) Determinants of plant–animal coevolution: the case of mutualistic dispersal of seeds by vertebrates. Oikos 44:132–141

    Article  Google Scholar 

  • Hofman CA, Rick TC (2018) Ancient biological invasions and island ecosystems: tracking translocations of wild plants and animals. J Archaeol Res 26:65–115

    Article  Google Scholar 

  • Hohmann H, La Roche F, Ortega G, Barquín J (1993) Bienen. Wespen und Ameisen der Kanarischen Inseln, Übersee-Museum

    Google Scholar 

  • Jensen TS (1985) Seed-seed predator interactions of European beech (Fagus silvatica L.) and forest rodents, Clethrionomys glareolus and Apodemus flavicollis. Oikos 44:149–156

    Article  Google Scholar 

  • Johnson SD, Nicolson SW (2008) Evolutionary associations between nectar properties and specificity in bird pollination systems. Biol Lett 4:49–52

    Article  PubMed  Google Scholar 

  • Jorgensen R, Arathi HS (2013) Floral longevity and autonomous selfing are altered by pollination and water availability in Collinsia heterophylla. Ann Bot 112:821–828

    Article  PubMed  PubMed Central  Google Scholar 

  • Kaiser-Bunbury CN, Traveset A, Hansen DM (2010) Conservation and restoration of plant–animal mutualisms on oceanic islands. Perspect Plant Ecol Evol Syst 12:131–143

    Article  Google Scholar 

  • Kalisz S, Vogler DW, Hanley KM (2004) Context-dependent autonomous self-fertilization yields reproductive assurance and mixed mating. Nature 430:884–887

    Article  CAS  PubMed  Google Scholar 

  • Kier G, Kreft H, Lee TM et al (2009) A global assessment of endemism and species richness across island and mainland regions. Proc Natl Acad Sci USA 106:9322–9327

    Article  PubMed  Google Scholar 

  • Kishimoto-Yamada K, Itioka T (2015) How much have we learned about seasonality in tropical insect abundance since Wolda (1988)? Entomol Sci 18:407–419

    Article  Google Scholar 

  • Kraemer M, Schmitt U (1997) Nectar production patterns and pollination of the Canarian endemic Echium wildpretii Pearson ex Hook. fil. Flora 192:217–221

    Article  Google Scholar 

  • Lloyd DG, Schoen DJ (1992) Self- and cross- fertilization in plants. I. Functional dimensions. Int J Plant Sci 153:358–369

    Article  Google Scholar 

  • Lord JM (1991) Pollination and seed dispersal in Freycinetia baueriana, a dioecious liane that has lost its bat pollinator. New Zeal J Bot 29:83–86

    Article  Google Scholar 

  • Mack RN, Simberloff D, Lonsdale WM et al (2000) Biotic invasions: causes, epidemiology, global consequences and control. Issues Ecol 5:1–12

    Google Scholar 

  • Martin J-L, Thibault J-C, Bretagnolle V (2000) Black rats, island characteristics, and colonial nesting birds in the Mediterranean: consequences of an ancient introduction. Conserv Biol 14:1452–1466

    Article  Google Scholar 

  • Michener CD (1979) Biogeography of bees. Ann Missouri Bot Gard 66:277–347

    Article  Google Scholar 

  • Mooney HA, Cleland EE (2001) The evolutionary impact of invasive species. Proc Natl Acad Sci U S A 98:5446–5451

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Moritz RFA, Härtel S, Neumann P (2005) Global invasions of the western honeybee (Apis mellifera) and the consequences for biodiversity. Écoscience 12:289–301

    Article  Google Scholar 

  • Nogales M, Rodriguez-Luengo JL, Marrero P (2006) Ecological effects and distribution of invasive non-native mammals on the Canary Islands. Mamm Rev 36:49–65

    Article  Google Scholar 

  • Olesen JM (1985) The Macaronesian bird-flower element and its relation to bird and bee opportunists. Bot J Linn Soc 91:395–414

    Article  Google Scholar 

  • Ollerton J, Cranmer L, Stelzer RJ et al (2009) Bird pollination of Canary Island endemic plants. Naturwissenschaften 96:221–232

    Article  CAS  PubMed  Google Scholar 

  • Pacini E, Nepi M, Vesprini JL (2003) Nectar biodiversity: a short review. Plant Syst Evol 238:7–21

    Article  CAS  Google Scholar 

  • Padrón B, Traveset A, Biedenweg T et al (2009) Impact of alien plant invaders on pollination networks in two archipelagos. PLoS ONE 4:e6275

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Pattemore DE, Wilcove DS (2012) Invasive rats and recent colonist birds partially compensate for the loss of endemic New Zealand pollinators. Proc R Soc B Biol Sci 279:1597–1605

    Article  Google Scholar 

  • Price MV, Jenkins SH (1986) Rodents as seed consumers and dispersers. In: Murray DR (ed) Seed dispersal. Academic Press, Cambridge, pp 191–235

    Chapter  Google Scholar 

  • Primack RB (1985) Longevity of individual flowers. Annu Rev 16:15–37

    Google Scholar 

  • Pyšek P, Pergl J, Essl F et al (2017) Naturalized alien flora of the world: species diversity, taxonomic and phylogenetic patterns, geographic distribution and global hotspots of plant invasion. Preslia 89:203–274

    Article  Google Scholar 

  • R Core Team (2018) R: A language and environment for statistical computing. R Core Team, Vienna

    Google Scholar 

  • Rodríguez-Rodríguez MC, Valido A (2011) Consequences of plant-pollinator and floral-herbivore interactions on the reproductive success of the Canary Islands endemic Canarina canariensis (Campanulaceae). Am J Bot 98:1465–1474

    Article  PubMed  Google Scholar 

  • Sanz-Elorza M, Dana E, Sobrino E (2001) Listado de plantas alóctonas invasoras reales y potenciales en España. Lazaroa 22:121–131

    Google Scholar 

  • Sanz-Elorza M, Dana ED, Sobrino E (2005) Aproximación al listado de plantas vasculares alóctonas invasoras reales y potenciales en las islas Canarias. Lazaroa 26:55–66

    Google Scholar 

  • Sax DF, Gaines SD, Brown JH (2002) Species invasions exceed extinctions on islands worldwide: a comparative study of plants and birds. Am Nat 160:766–783

    Article  PubMed  Google Scholar 

  • Shiels AB (2011) Frugivory by introduced black rats (Rattus rattus) promotes dispersal of invasive plant seeds. Biol Invasions 13:781–792

    Article  Google Scholar 

  • Shiels AB, Drake DR (2011) Are introduced rats (Rattus rattus) both seed predators and dispersers in Hawaii? Biol Invasions 13:883–894

    Article  Google Scholar 

  • Shiels AB, Pitt WC, Sugihara RT, Witmer GW (2014) Biology and impacts of Pacific Island invasive species. 11. Rattus rattus, the black rat (Rodentia: Muridae). Pac. Sci 68:145–184

    Article  Google Scholar 

  • Siverio F, Rodríguez-Rodríguez MC (2011) Gallotia caesaris (Caesar´s Lizard), Nectarivory. Herpetol Rev 42:600–602

    Google Scholar 

  • Siverio F, Rodríguez-Rodríguez MC (2012) Gallotia galloti (Canary Lizard), Nectarivory. Herpetol Rev 43:333–334

    Google Scholar 

  • Subdirección General de Productos Ganaderos (2017) El sector apícola en cifras. Principales indicadores económicos. Madrid, Spain

  • Sugihara RT (1997) Abundance and diets of rats in two native Hawaiian forests. Pac Sci 51:189–198

    Google Scholar 

  • Teixido AL, Valladares F (2015) Temperature-limited floral longevity in the large-flowered mediterranean shrub Cistus ladanifer (Cistaceae). Int J Plant Sci 176:131–140

    Article  Google Scholar 

  • Torres C, Galetto L (1998) Patterns and implications of oral nectar secretion, chemical composition, removal effects and standing crop in Mandevilla pentlandiana (Apocynaceae). Society 127:207–223

    Google Scholar 

  • Towns DR, Atkinson IAE, Daugherty CH (2006) Have the harmful effects of introduced rats on islands been exaggerated? Biol Invasions 8:863–891

    Article  Google Scholar 

  • Traveset A, Richardson DM (2006) Biological invasions as disruptors of plant reproductive mutualisms. Trends Ecol Evol 21:208–216

    Article  PubMed  Google Scholar 

  • Traveset A, Richardson DM (2014) Mutualistic interactions and biological invasions. Annu Rev Ecol Evol Syst 45:89–113

    Article  Google Scholar 

  • Traveset A, Nogales M, Alcover JA et al (2009) A review on the effects of alien rodents in the Balearic (western Mediterranean sea) and Canary islands (eastern Atlantic ocean). Biol Invasions 11:1653–1670

    Article  Google Scholar 

  • Trunschke J, Stöcklin J (2017) Plasticity of flower longevity in alpine plants is increased in populations from high elevation compared to low elevation populations. Alp Bot 127:41–51

    Article  Google Scholar 

  • Valido A (1999) Eología de la dispersión de semillas por los lagartos endémicos canarios (g. Universidad de la Laguna, Gallotia

    Google Scholar 

  • Valido A, Olesen JM (2010) Pollination on islands: examples from the Macaronesian archipelagos. In: Serrano ARM, Borges PAV, Boieiro M, Oromí P (eds) Terrestrial arthropods of Macaronesia: Biodiversity, Ecology and Evolution. Sociedad Portuguesa de Entomología, Madrid, pp 249–283

    Google Scholar 

  • Valido A, Dupont YL, Hansen DM (2002) Native birds and insects, and introduced honey bees visiting Echium wildpretii (Boraginaceae) in the Canary Islands. Acta Oecol 23:413–419

    Article  Google Scholar 

  • Valido A, Dupont YL, Olesen JM (2004) Bird–flower interactions in the Macaronesian islands. J Biogeogr 31:1945–1953

    Article  Google Scholar 

  • Valido A, Rodríguez-Rodríguez MC, Jordano P (2011) Interacciones entre plantas y polinizadores en el Parque Nacional del Teide: consecuencias ecológicas de la introducción masiva de la abeja doméstica (Apis mellifera, Apidae). In: Ramírez L, Asensio B (eds) Proyectos de investigación en parques nacionales: 2007–2010, pp 205–232

  • Valido A, Rodríguez-Rodríguez MC, Jordano P (2014) Impacto de la introducción de la abeja doméstica (Apis mellifera, Apidae) en el Parque Nacional del Teide (Tenerife, Islas Canarias). Ecosistemas 23:58–66

    Article  Google Scholar 

  • Valido A, Rodríguez-Rodríguez MC, Jordano P (2019) Honeybees disrupt the structure and functionality of plant-pollinator networks. Sci Rep 9:4711

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Vanbergen AJ, Espíndola A, Aizen MA (2018) Risks to pollinators and pollination from invasive alien species. Nat Ecol Evol 2:16–25

    Article  PubMed  Google Scholar 

  • Vaughton G (1996) Pollination disruption by European honeybees in the Australian bird-pollinated shrub Grevillea barklyana (Proteaceae). Plant Syst Evol 200:89–100

    Article  Google Scholar 

  • Vitousek PM, Loope LL, Stone CP (1987) Introduced species in Hawaii: biological effects and opportunities for ecological research. Trends Ecol Evol 2:224–227

    Article  CAS  PubMed  Google Scholar 

  • Vitousek PM, D’Antonio CM, Loope LL, Westbrooks R (1996) Biological invasions as global environmental change. Am Sci 84:468–478

    Google Scholar 

  • Vogel C, Westerkamp BT, Gessner K (1984) Ornithophilie auf den Canarischen Inseln. Plant Syst Evol 46:225–248

    Article  Google Scholar 

  • Whitfield CW, Behura SK, Berlocher SH et al (2006) Thrice out of Africa: ancient and recent expansions of the honey bee, Apis mellifera. Science 314:642–645

    Article  CAS  PubMed  Google Scholar 

  • Wilcove DS, Rothstein D, Dubow J et al (1998) Quantifying threats to imperiled species in the United States. Bioscience 48:607–615

    Article  Google Scholar 

  • Wildpret W, Martín VE (1997) Laurel forest in the Canary Islands: biodiversity, historical use and conservation. Tropics 6:371–381

    Google Scholar 

  • Wolda H (1988) Insect seasonality: Why? Annu Rev Ecol Syst 19:1–18

    Article  Google Scholar 

  • Worthington EB, Lowe-McConnell R (1994) African lakes reviewed: creation and destruction of biodiversity. Environ Conserv 21:199–213

    Article  Google Scholar 

  • Wyatt R, Broyles SB, Derda GS (1992) Environmental influences on nectar production in milkweeds (Asclepias syriaca and A. exaltata). Am J Bot 79:636–642

    Article  Google Scholar 

  • Yasaka M, Nishiwaki Y, Konno Y (1998) Plasticity of flower longevity in Corydalis ambigua. Ecol Res 13:211–216

    Article  Google Scholar 

  • Zuur AF, Ieno EN, Walker NJ et al (2009) Mixed effect models and extensions in ecology with R. Springer, New York

    Book  Google Scholar 

Download references

Acknowledgements

The authors thank Teobaldo Méndez and Don Manuel for permission to work on their land and the Servicio Administrativo de Medio Ambiente, Excmo. Cabildo Insular de Tenerife for permission (AFF 396/15; No. Sigma: 2015 03468) to work in Teno Rural Park, Tenerife. Julia Jaca was funded by a predoctoral fellowship from the Ministerio de Educación, Cultura y Deporte [FPU13/05880] and by the unemployment benefit from the Ministerio de Trabajo, Migraciones y Seguridad Social; and the study was framed within a project financed by the Ministerio de Economía, Industria y Competitividad [CGL2013-44386-P], granted to Anna Traveset.

Author information

Authors and Affiliations

Authors

Corresponding author

Correspondence to Julia Jaca.

Additional information

Publisher's Note

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

Electronic supplementary material

Rights and permissions

Reprints and permissions

About this article

Check for updates. Verify currency and authenticity via CrossMark

Cite this article

Jaca, J., Rodríguez, N., Nogales, M. et al. Impact of alien rats and honeybees on the reproductive success of an ornithophilous endemic plant in Canarian thermosclerophyllous woodland relicts. Biol Invasions 21, 3203–3219 (2019). https://doi.org/10.1007/s10530-019-02040-7

Download citation

  • Received:

  • Accepted:

  • Published:

  • Issue Date:

  • DOI: https://doi.org/10.1007/s10530-019-02040-7

Keywords

Navigation