Flower-visiting lizards as key ecological actors for an endemic and critically endangered plant in the Canary Islands





endemic mutualisms, Gallotia galloti, Lotus maculatus, Macaronesia, oceanic islands, pollination effectiveness


Oceanic islands are places where biological assemblages are relatively simple, as compared to the mainland. On islands, however, pollinator assemblages may to be composed of a taxonomically disparate group of organisms (e.g. insects, lizards, and birds), some of them with opportunistic nectar-feeding behaviour. Here we investigated some components of pollination effectiveness of Lotus maculatus (Fabaceae), an endangered Canary Islands endemic. In a flower exclusion experiment, we bagged flowers and compared their subsequent fruit and seed set to that of control flowers. Number of interactions with vertebrate and invertebrate flower visitors was counted and it was recorded whether interactions were legitimate (potentially pollinating) or non-legitimate (nectar robbing). Additionally, we estimated pollen loads on lizards and looked for any relationship between reproductive success of individual plants and number of visits made by the top three flower-visiting species (in terms of both frequency of occurrence at censuses and number of floral visits). Bagged flowers fruited less and with fewer seeds than control flowers. The only observed flower-visiting vertebrate was the Tenerife lizard Gallotia galloti, whose interactions were always legitimate and with around a half of captured individuals carrying pollen grains. The most frequent flower-visiting insect was the honeybee Apis mellifera followed by the solitary bee Lasioglossum arctifrons. The honeybee, however, was only a nectar robber, and the solitary bee was not an effective pollinator, but rather a pollen gatherer. Fruit set by individual plants was positively related only to frequency of visits by the lizard. Thus, the lizard seems to play a key role in the conservation management of L. maculatus.

Author Biography

Aarón González-Castro, Universidad de La Laguna

Tenure track Professor.

Department of Animal Biology, Edaphology and Geology. Area of Zoology.

I am interested on how plant-animal interactions shape island ecosystems and enhance biodiversity maintenance.


Abrahamczyk S (2019) Comparison of the ecology and evolution of plants with a generalist bird pollination system between continents and islands worldwide. Biological Reviews 94:1658-1671. https://doi.org/10.1111/brv.12520 DOI: https://doi.org/10.1111/brv.12520

Anderson M.J. (2001) Permutation tests for univariate or multivariate analysis of variance and regression. Canadian Journal of Fisheries and Aquatic Sciences, 58, 626–639. https://doi.org/10.1139/f01-004 DOI: https://doi.org/10.1139/f01-004

Aplin LM, Farine DR, Morand-Ferron J, Cole EF, Cockburn A, Sheldon BC (2013) Individual personalities predict social behaviour in wild networks of great tits (Parus major). Ecology Letters 16:1365–1372. https://doi.org/10.1111/ele.12181 DOI: https://doi.org/10.1111/ele.12181

Aplin LM, Farine DR, Mann RP, Sheldon BC (2014) Individual-level personality influences social foraging behaviour in wild birds. Proceedings of the Royal Society B 281:20141016. https://doi.org/10.1098/rspb.2014.1016 DOI: https://doi.org/10.1098/rspb.2014.1016

Bates D, Maechler M, Bolker B, Wallker S (2015) Fitting Linear Mixed-Effects Models Using lme4. Journal of Statistical Software 67:1–48 https://doi.org/10.18637/jss.v067.i01 DOI: https://doi.org/10.18637/jss.v067.i01

Benachour K, Louadi K, Terzo M (2007) Rôle des abeilles sauvages et domestiques (Hymenoptera: Apoidea) dans la pollinisation de la fève (Vicia faba L. var. major) (Fabaceae) en région de Constantine (Algérie). Annales de la Société Entomologique de France 43:213–219. https://doi.org/10.1080/00379271.2007.10697513 DOI: https://doi.org/10.1080/00379271.2007.10697513

Breitfeld C (1973) Lotus maculatus, eine bisher unbeschriebne Art von Tenerife. Cuadernos de Botánica Canaria 17:27–31.

Calero A, Santos A (1988) Biología reproductiva de especies amenazadas en la flora canaria. Lagascalia 15 (supplement):661–664.

Carbonari V, Polatto LP, Aives VV (2009) Evaluation of the impact on Pyrostegia venusta (Bignoniaceae) flowers due to nectar robbery by Apis mellifera (Hymenoptera, Apidae). Sociobiology 54:373–382.

Carlquist SJ (1974) Island biology. Columbia University Press, New York. https://doi.org/10.5962/bhl.title.63768 DOI: https://doi.org/10.5962/bhl.title.63768

Dupont YL, Hansen DM, Rasmussen JT, Olesen JM (2004) Evolutionary changes in nectar sugar composition associated with switches between bird and insect pollination: The Canarian bird–flower element revisited. Functional Ecology 18:670–676. https://doi.org/10.1111/j.0269-8463.2004.00891.x DOI: https://doi.org/10.1111/j.0269-8463.2004.00891.x

Elvers I (1977) Flower-visiting lizards on Madeira. Botaniska Notiser 130:231–234.

Esposito F, Costa R, Boieiro M (2021) Foraging behavior and pollen transport by flower visitors of the Madeira Island endemic Echium candicans. Insects 12:488. https://doi.org/10.3390/insects12060488 DOI: https://doi.org/10.3390/insects12060488

Fariña B, Mangani R (2020) Nectarivoría de Tarentola delalandii sobre la planta exótica Hoya kerrii en Tenerife, Islas Canarias. Boletín de la Asociación Herpetológica Española 31:53-54. http://www.herpet-ologica.org/BAHE/31_2/BAHE31-2_240_04_HNat14.pdf

Fox J, Weisberg S (2019) An R Companion to Applied Regression. Third Edition. Thousand Oaks CA.

Fuster F, Kaiser-Bunbury C, Olesen JM, Traveset A (2019) Global patterns of the double mutualism phenomenon. Ecography 42:826-835. https://doi.org/10.1111/ecog.04008 DOI: https://doi.org/10.1111/ecog.04008

García C, Vasconcelos R (2017) The beauty and the beast: Endemic mutualistic interactions promote community-based conservation on Socotra Island (Yemen). Journal for Nature Conservation 35:20–23. https://doi.org/10.1016/j.jnc.2016.11.005 DOI: https://doi.org/10.1016/j.jnc.2016.11.005

Gómez JM (2003) Herbivory reduces the strength of pollinator-mediated selection in the Mediterranean herb Erysimum mediohispanicum: consequences for plant specialization. The American Naturalist 162:242–256. https://doi.org/10.1086/376574 DOI: https://doi.org/10.1086/376574

Gros CL (2001) The effect of introduced honeybees on native bee visitation and fruit set in Dillwynia juniperina (Fabaceae) in a fragmented ecosystem. Biological Conservation 102:89–95. https://doi.org/10.1016/S0006-3207(01)00088-X DOI: https://doi.org/10.1016/S0006-3207(01)00088-X

Hansen DM, Müller CB (2009) Reproductive ecology of the endangered enigmatic Mauritian endemic Roussea simplex (Rousseaceae). International Journal of Plant Sciences 170:42–52. https://doi.org/10.1086/593050 DOI: https://doi.org/10.1086/593050

Heenan, PB (1998) The pollination system and stigmatic cuticle of Clianthus puniceus (Fabaceae). New Zealand Journal of Botany 36:311–314. https://doi.org/10.1080/0028825X.1998.9512571 DOI: https://doi.org/10.1080/0028825X.1998.9512571

Hernández E (1993) La flora vascular de los roques de Anaga (Tenerife, Islas Canarias). Vieraea 22:1–6.

Hernández-Teixidor D, Díaz-Luis N, Medina FM, Nogales M (2020) First record of geckos visiting flowers in the Paleartic Ecozone. Current Zoology 66:447–448. https://doi.org/10.1093/cz/zoz051 DOI: https://doi.org/10.1093/cz/zoz051

Heslop-Harrison J, Heslop-Harrison Y (1983) Pollen-stigma interaction in the Leguminosae: the organization of the stigma in Trifolium pratense. Annals of Botany 51:571–583. https://doi.org/10.1093/oxfordjournals.aob.a086503 DOI: https://doi.org/10.1093/oxfordjournals.aob.a086503

Hind N (2008) 619 Lotus maculatus. Leguminosae-Papilionoideae. Plant in Peril 30. Curtis’s Botanical Magazine 25:146–157. https://doi.org/10.1111/j.1467-8748.2008.00613.x DOI: https://doi.org/10.1111/j.1467-8748.2008.00613.x

Howard SR, Prendergast K, Symonds MRE, Shrestha M, Dyer AG (2021) Spontaneous choices for insect-pollinated flower shapes by wild non-eusocial halictid bees. Journal of Experimental Biology 224:jeb242457. https://doi.org/10.1242/jeb.242457 DOI: https://doi.org/10.1242/jeb.242457

IUCN (2023) The IUCN Red List of Threatened Species. Version 2023-1. https://www.iucnredlist.org. Accessed on 27/02/2024.

Jaca J, Nogales M, Traveset A (2018) Reproductive success of the Canarian Echium simplex (Boraginaceae) mediated by vertebrates and insects. Plant Biology 21:216–226. https://doi.org/10.1111/plb.12926 DOI: https://doi.org/10.1111/plb.12926

Koppetsch T, Sánchez Romero G, Fischer E, Wolfgang B (2020) A new record of nectarivory for Tarentola delalandii (Duméril and Bibron, 1836) pollinating the introduced palm Dypsis lutescens (H. Wendl.) Beentje and J. Dransf. (Arecaceae) on Tenerife, Canary Islands. Herpetology Notes 13:415–419.

Lorite J, Salazar-Mendías C, Pawlak R, Cañadas EM (2021) Assessing effectiveness of exclusion fences in protecting threatened plants. Scientific Reports 11:16124. https://doi.org/10.1038/s41598-021-95739-4 DOI: https://doi.org/10.1038/s41598-021-95739-4

Lundqvist A (1993) The self-incompatibility system in Lotus tenuis (Fabaceae). Heredity 119:59–66. https://doi.org/10.1111/j.1601-5223.1993.00059.x DOI: https://doi.org/10.1111/j.1601-5223.1993.00059.x

Marzol V (2000) El Clima. In: Morales G, Pérez R (eds), Gran Atlas Temático de Canarias. Editorial Interinsular Canaria, Santa Cruz de Tenerife.

McConkey KR, O’Farrill G (2016) Loss of seed dispersal before the loss of seed dispersers. Biological Conservation 201:38–49. https://doi.org/10.1016/j.biocon.2016.06.024 DOI: https://doi.org/10.1016/j.biocon.2016.06.024

Medina FM, Nogales M (2009) A review on the impacts of feral cats (Felis silvestris catus) in the Canary Islands: implications for the conservation of its endangered fauna. Biodiversity and Conservation 18:829–846. https://doi.org/10.1007/s10531-008-9503-4 DOI: https://doi.org/10.1007/s10531-008-9503-4

Ojeda I, Santos-Guerra A (2011) The intersection of conservation and horticulture: bird-pollinated Lotus species from the Canary Islands (Leguminosae). Biodiversity and Conservation 20:3501–3516. https://doi.org/10.1007/s10531-011-0138-5 DOI: https://doi.org/10.1007/s10531-011-0138-5

Ojeda DI, Valido A, Fernández de Castro AG, Ortega-Olivencia A, Fuertes-Aguilar A, Carvalho JA, Santos-Guerra A (2016) Pollinator shifts drive petal epidermal evolution on the Macaronesian Islands bird-flowered species. Biology Letters 12: 20160022. https://doi.org/10.1098/rsbl.2016.0022 DOI: https://doi.org/10.1098/rsbl.2016.0022

Ojeda Alayón, DI (2013) The Macaronesian bird-flowered element as a model system to study the evolution of ornithophilous floral traits. Vieraea 41:73-89. https://doi.org/10.31939/vieraea.2013.41.06 DOI: https://doi.org/10.31939/vieraea.2013.41.06

Olesen JM (1985) The Macaronesian bird-flower element and its relation to bird and bee opportunists. Botanical Journal of the Linnean Society 91:395–414. https://doi.org/10.1111/j.1095-8339.1985.tb01010.x DOI: https://doi.org/10.1111/j.1095-8339.1985.tb01010.x

Olesen JM, Jordano P (2002) Geographic patterns in plant–pollinator mutualistic networks. Ecology 83:2416–2424. https://doi.org/10.1890/0012-9658(2002)083[2416:GPIPPM]2.0.CO;2 DOI: https://doi.org/10.1890/0012-9658(2002)083[2416:GPIPPM]2.0.CO;2

Olesen JM, Valido A (2003) Lizards as pollinators and seed dispersers: an island phenomenon. Trends in Ecology and Evolution 18:177–181. https://doi.org/10.1016/S0169-5347(03)00004-1 DOI: https://doi.org/10.1016/S0169-5347(03)00004-1

Ollerton J (2024) Birds & Flowers: An Intimate 50 million year relationship. Pelagic Publishing, Exeter. https://doi.org/10.53061/FFQO3130 DOI: https://doi.org/10.53061/FFQO3130

Ollerton J, Lack AJ (1998) Relationships between flowering phenology, plant size and reproductive success in Lotus corniculatus (Fabaceae). Plant Ecology 139:35–47. https://doi.org/10.1023/A:1009798320049 DOI: https://doi.org/10.1023/A:1009798320049

Ollerton J, Cranmer L, Stelzer RJ, Sullivan S, Chittka L (2009) Bird pollination of Canary Island endemic plants. Naturwissenschaften 96:221–232. https://doi.org/10.1007/s00114-008-0467-8 DOI: https://doi.org/10.1007/s00114-008-0467-8

Ollerton J, Winfree R, Tarrant S (2011) How many flowering plants are pollinated by animals? Oikos 120:321–326. https://doi.org/10.1111/j.1600-0706.2010.18644.x DOI: https://doi.org/10.1111/j.1600-0706.2010.18644.x

Ortega-Olivencia A, Rodríguez-Riaño T, Pérez-Bote JL, López J, Mayo C, Valtueña FJ, Navarro-Pérez M (2012). Insects, birds and lizards as pollinators of the largest-flowered Scrophularia of Europe and Macaronesia. Annals of Botany 109:153–57. https://doi.org/10.1093/aob/mcr255 DOI: https://doi.org/10.1093/aob/mcr255

Owens SJ (1985) Seed set in Lotus berthelotii Masferrer. Annals of Botany 55:811–814. https://doi.org/10.1093/oxfordjournals.aob.a086960 DOI: https://doi.org/10.1093/oxfordjournals.aob.a086960

Pérez-Cembranos A, Pérez-Mellado V (2014) Local enhancement and social foraging in a non-social insular lizard. Animal Cognition 18:629–637. https://doi.org/10.1007/s10071-014-0831-3 DOI: https://doi.org/10.1007/s10071-014-0831-3

Pérez-Mellado V, Casas JL (1997) Pollination by a lizard in a Mediterranean island. Copeia 1997:593–595. https://doi.org/10.2307/1447565 DOI: https://doi.org/10.2307/1447565

Pérez-Mellado V, Ortega F, Martín-García S, Perera A, Cortázar G (2000) Pollen load and transport by the insular lizard, Podarcis lilfordi (Squamata, Lacertidae) in coastal islets of Menorca (Balearic Islands, Spain). Israel Journal of Zoology 46:193–200. https://doi.org/10.1092/QMY9-PXWF-AG43-RP6F DOI: https://doi.org/10.1092/QMY9-PXWF-AG43-RP6F

Pinho CJ, Santos B, Mata VA, Seguro M, Romeiras MM, Lopes RJ, Vasconcelos R (2018). What is the giant wall gecko having for dinner? Conservation genetics for guiding reserve management in Cabo Verde. Genes 9:599. https://doi.org/10.3390/genes9120599 DOI: https://doi.org/10.3390/genes9120599

Piquet JC, López-Darias M (2021) Invasive snake causes massive reduction of all endemic herpetofauna on Gran Canaria. Proceedings of the Royal Society B 288:20211939. https://doi.org/10.1098/rspb.2021.1939 DOI: https://doi.org/10.1098/rspb.2021.1939

Proctor M, Yeo P, Lack A (1996) The natural history of pollination. Timber Press, Portland, Oregon.

R Core Team (2023) R: A language and environment for statistical computing. R Foundation for Statistical Computing, Vienna, Austria. URL https://www.R-project.org/

Rodríguez Navarro ML, Fariña Trujillo B (2011) On the current presence of Lotus maculatus Breitf. (Fabaceae) in the “roque de Tierra” of Anaga (Tenerife, Canary Islands). Vieraea 39:229–232. https://doi.org/10.31939/vieraea.2011.39.22 DOI: https://doi.org/10.31939/vieraea.2011.39.22

Rodríguez-Riaño T, Ortega-Olivencia A, Devesa Alcaraz JA (2004) Reproductive biology in Cytisus multiflorus (Fabaceae). Annales Botanici Fennici 41:179–188. https://www.annbot.net/PDF/anbf41/anbf41-179.pdf

Rodríguez-Rodríguez MC, Valido A (2008) Opportun-istic nectar-feeding birds are effective pollinators of bird-flowers from Canary Islands: experimental evidence from Isoplexis canariensis (Scrophulariaceae). American Journal of Botany 95:1408–1415. https://doi.org/10.3732/ajb.0800055 DOI: https://doi.org/10.3732/ajb.0800055

Rodríguez-Sambruno C, Narbona E, del Valle JC, Valido A (2024) Bird-flower colour on islands supports the bee-avoidance hypothesis. Functional Ecology 38:600–611. https://doi.org/10.1111/1365-2435.14493 DOI: https://doi.org/10.1111/1365-2435.14493

Romero-Egea V, Robles C, Traveset A, Del Río L, Hervías-Parejo S (2023) Assessing the role of lizards as potential pollinators of an insular plant community and its intraespecific variation. Animals 13:1122. https://doi.org/10.3390/ani13061122 DOI: https://doi.org/10.3390/ani13061122

Signorell A (2023) DescTools: Tools for descriptive statistics. https://CRAN.R-project.org/package=DescTools

Singer RB, Cocucci AA (1999) Pollination mechanism in southern Brazilian orchids which are exclusively or mainly pollinated by halictid bees. Plant Systematics and Evolution 217:101–117. https://doi.org/10.1007/BF00984924 DOI: https://doi.org/10.1007/BF00984924

Siqueira E, Oliveira R, Dotterl S, Cordeiro GD, Alves-dos-Santos I, Mota T, Schlindwein C (2018) Pollination of Machaerium opacum (Fabaceae) by nocturnal and diurnal bees. Arthropod-Plant Interactions 12:633–645. https://doi.org/10.1007/s11829-018-9623-z DOI: https://doi.org/10.1007/s11829-018-9623-z

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

Thompson JN (2005) The geographic mosaic of coevolution. University of Chicago Press, Chicago USA. https://doi.org/10.7208/chicago/9780226118697.001.0001 DOI: https://doi.org/10.7208/chicago/9780226118697.001.0001

Traveset A, Sáez E (1997) Pollination of Euphorbia dendroides by lizards and insects: Spatio-temporal variation in patterns of flower visitation. Oecologia 111:241–248. https://doi.org/10.1007/PL00008816 DOI: https://doi.org/10.1007/PL00008816

Valido A, Dupont YL, Olesen JM (2004) Bird–flower interactions in the Macaronesian islands. Journal of Biogeography 31:1945–1953. https://doi.org/10.1111/j.1365-2699.2004.01116.x DOI: https://doi.org/10.1111/j.1365-2699.2004.01116.x

Valido A, Rodríguez-Rodríguez MC, Jordano P (2019) Honeybees disrupt the structure and functionality of plant-pollinator networks. Scientific Reports 9:4711. https://doi.org/10.1038/s41598-019-41271-5 DOI: https://doi.org/10.1038/s41598-019-41271-5

Valtueña FJ, Rodríguez-Riaño T, Espinosa F, Ortega-Olivencia A (2010) Self- sterility in two Cytisus species (Leguminosae, Papilionidae) due to early-acting inbreeding depression. American Journal of Botany 97:123–135. https://doi.org/10.3732/ajb.0800332 DOI: https://doi.org/10.3732/ajb.0800332

Vogel S, Westerkamp C, Thiel B, Gessner K (1984) Ornithophilie auf den Canarischen Inseln. Plant Systematics and Evolution 146:225–248. https://doi.org/10.1007/BF00989548 DOI: https://doi.org/10.1007/BF00989548



How to Cite

González-Castro, A., & Siverio, F. (2024). Flower-visiting lizards as key ecological actors for an endemic and critically endangered plant in the Canary Islands. Journal of Pollination Ecology, 36, 88–103. https://doi.org/10.26786/1920-7603(2024)777




Similar Articles

<< < 1 2 3 4 5 6 7 8 9 10 > >> 

You may also start an advanced similarity search for this article.