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Small Size Does Not Restrain Frugivory and Seed Dispersal Across the Evolutionary Radiation of Gala´ Pagos Lava Lizards

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Small Size Does Not Restrain Frugivory and Seed Dispersal Across the Evolutionary Radiation of Gala´ Pagos Lava Lizards Downloaded from https://academic.oup.com/cz/advance-article-abstract/doi/10.1093/cz/zoy066/5069192 by Departamento de Matemática da Fac. Ciências e Tecnologia Universidade Coimbra user on 13 September 2018 Current Zoology, 2018, 1–9 doi: 10.1093/cz/zoy066 Advance Access Publication Date: 10 August 2018 Article Article Small size does not restrain frugivory and seed dispersal across the evolutionary radiation of Gala´ pagos lava lizards a, b a Sandra HERVI´AS-PAREJO *, Ruben HELENO , Beatriz RUMEU , c c d a Beatriz GUZMAN , Pablo VARGAS , Jens M. OLESEN , Anna TRAVESET , e f g Carlos VERA , Edgar BENAVIDES , and Manuel NOGALES aInstitut Mediterrani d’Estudis Avanc¸ats (CSIC-UIB), Global Change Research Group, Mallorca, Balearic Islands, Spain, bCentre for Functional Ecology, Department of Life Sciences, University of Coimbra, Portugal, cReal Jardı´n Bota´nico (CSIC-RJB), Madrid, Spain, dDepartment of Bioscience, Aarhus University, Denmark, eGala´pagos National Park, Puerto Ayora, Santa Cruz, Gala´pagos, Ecuador, fDepartment of Ecology and Evolutionary Biology, Yale University, USA and gInstituto de Productos Naturales y Agrobiologı´a (CSIC-IPNA), Island Ecology and Evolution Research Group, Canary Islands, Spain. *Address correspondence to Sandra Hervı´as-Parejo. E-mail: [email protected] Handling editor: Xiang Ji Received on 25 June 2018; accepted on 6 August 2018 Abstract Frugivory in lizards is often assumed to be constrained by body size; only large individuals are con- sidered capable of consuming fruits, with the potential of acting as seed dispersers. However, only one previous study has tested the correlation of frugivory with body and head size at an archipel- ago scale across closely related species. All nine lava lizards (Microlophus spp.) were studied on the eleven largest Gala´ pagos islands from 2010 to 2016 to investigate whether frugivory is related to body and head size. We also tested whether fruit abundance influences fruit consumption and explored the effect of seed ingestion on seedling emergence time and percentage. Our results showed that across islands, lava lizards varied considerably in size (64–102 mm in mean snout– vent length) and level of frugivory (1–23%, i.e., percentage of droppings with seeds). However, level of frugivory was only weakly affected by size as fruit consumption was also common among small lizards. Lava lizards consumed fruits throughout the year and factors other than fruit abundance may be more important drivers of fruit selection (e.g., fruit size, energy content of pulp). From 2,530 droppings, 1,714 seeds of at least 61 plant species were identified, 76% of the species being native to the Gala´ pagos. Most seeds (91%) showed no external structural damage. Seedling emer- gence time (44 versus 118 days) and percentage (20% versus 12%) were enhanced for lizard- ingested seeds compared to control (uningested) fruits. De-pulping by lizards (i.e., removal of pulp with potential germination inhibitors) might increase the chances that at least some seeds find suit- able recruitment conditions. We concluded that lizards are important seed dispersers throughout the year and across the whole archipelago, regardless of body size. Key words: Microlophus, oceanic islands, plant–animal interactions, seed disperser size, seed dispersal effectiveness, seedling emergence VC The Author(s) (2018). Published by Oxford University Press. 1 This is an Open Access article distributed under the terms of the Creative Commons Attribution Non-Commercial License (http://creativecommons.org/licenses/by-nc/4.0/), which permits non-commercial re-use, distribution, and reproduction in any medium, provided the original work is properly cited. For commercial re-use, please contact [email protected] Downloaded from https://academic.oup.com/cz/advance-article-abstract/doi/10.1093/cz/zoy066/5069192 by Departamento de Matemática da Fac. Ciências e Tecnologia Universidade Coimbra user on 13 September 2018 2 Current Zoology, 2018, Vol. 0, No. 0 Lizards of different evolutionary lineages consume fruits on a regu- lar basis (Olesen and Valido 2003; Traveset et al. 2016; Neghme et al. 2017), but the ecological and evolutionary drivers of such habit in these animals remain poorly understood. Body size has been considered a strong correlate of frugivory in lizards (Van Damme 1999; Herrel et al. 2004a). It is often assumed that large body and head size is required for lizards to efficiently process plant material (Pough 1973; Cooper Jr and Vitt 2002). Large lizards have more di- verse prey-size range than smaller ones and are better adapted to coping with more generalist diets including plant material (Meiri 2008). Frugivory by lizards is particularly common on islands. Insular liz- ards are more likely to consume fruits, since population densities tend to be higher whereas interspecific competition and predator pressure tend to be lower than on the mainland (Olesen and Valido 2003; Novosolov et al. 2018). This either allows or forces insular lizards to expand their trophic niche and explore novel food resources such as Figure 1. Distribution of the nine species of lava lizards across the Gala´ pagos fruits (i.e., undergoing an “interaction release”, sensu Traveset et al. archipelago and location of the sites sampled on each island. Fernandina: 1– Cabo Douglas, 2–Cabo Hammond; Isabela: 3–Punta Albemarle, 4–Playa 2015). However, it is not clear whether such interaction release in liz- Tortuga Negra, 5–Bahı´a Elizabeth; Pinta: 6–*Barrancos, 7–Playa del Muerto; ards occurs regardless of their body sizes, especially on tropical islands Marchena: 8–Playa Negra; Santiago: 9–Bahı´a James, 10–Bahı´a Ladilla; where these animals are active year-round and have continuous access Pinzo´ n: 11–Bahı´a de Pinzo´ n; Santa Cruz: 12–Garrapatero, 13–Tortuga Bay; to fruit (Nogales et al. 2016). Specifically, only one study explored Floreana: 14–*Punta Cormorant, 15–Puerto Velazco Ibarra; Santa Fe: 16– variation in lizard frugivory within a clade of closely related species Bahı´a de Santa Fe; San Cristo´ bal: 17–Punta Carola; Espanola:~ 18–Playa showing a strong correlation between body size and frugivory (Anolis Manzanillo, 19–*Punta Cevallos. Sites marked with an asterisk were not included in the analysis of frugivory and body size due to a lack of biometric species in Jamaica; Herrel et al. 2004a). data. The Gala´pagos islands host nine species of lava lizards (Microlophus spp., Tropiduridae). They constitute a remarkable ver- tebrate island radiation with only one species per island including Materials and Methods seven single-island endemics (Benavides et al. 2009). Evolutionary radiations like this are valuable systems in our efforts to understand Study site whether species interactions, including their food preferences, are This study was carried out on all main Gala´pagos islands (n ¼ 11; the cause or the consequence of habitat-dependent shifts of morpho- Figure 1) with lava lizards (Table 1). Sampling was conducted in the logical features (Calsbeek and Irschick 2007). Lava lizards are very arid zone (c. 0–300 m a.s.l.) where lizards are common (Tanner and common in the arid lowland of the Gala´pagos (Tanner and Perry Perry 2007). This zone is the largest (c. 60% of total land area) and 2007), where access to animal prey (arthropods) and water is often most biodiverse of the archipelago (Gue´zou et al. 2010). This habi- limited (Schluter 1984). Lizards on three Gala´pagos islands (Santa tat is dominated by evergreen drought-tolerant shrubs, e.g., Croton Cruz, San Cristo´ bal, Pinta) are known to consume fruits (Schluter scouleri, and fleshy-fruited species such as Opuntia spp., Cordia leu- 1984; Heleno et al. 2013). However, we do not know if this is a gen- cophlyctis, C. lutea, Lantana peduncularis, Tournefortia psilosta- eral pattern across both the entire lizard radiation and the archipel- chya and Scutia spicata. The arid zone becomes increasingly dry ago. Variation in frugivory in relation to lizard size, and if there are during the cold/dry season (June to December), until the first rains. seasonal differences in frugivory also remain unexplored. The latter Rainfall is extremely unpredictable spatially, varying considerably could be expected since fruit availability has seasonal variations, among islands (Trueman and d’Ozouville 2010). Arthropod abun- and it is important to know whether fruit abundance is a driver of dance and activity and fruit production are highest in the hot/wet fruit selection (Pe´rez-Mellado and Corti 1993). season (January–May) (Schluter 1984; Heleno et al. 2013). Many frugivores provide a highly valuable ecosystem service that may impact long-term vegetation dynamics due to their role as Lizard body and head size potential seed dispersers (Howe and Westley 1988; Traveset et al. Between 2014 and 2015, ca. 30 adult individuals (15 males and 15 2013). Frugivores can reduce germination time by both removing females whenever possible), from each island were captured by hand fruit pulp, which often contains chemical inhibitors, and weakening with noose poles. Snout–vent length (hereafter SVL), gape width physical barriers to germination, e.g. scarification (Traveset et al. (horizontal distance between commissural points), and skull length 2008). Nevertheless, the effect of disperser gut passage on germin- (rear of parietal bone to tip of upper jaw) were all measured using a ation varies depending on both animal and plant identity (Wotton digital calliper (precision 0.01 mm). This was normally performed 2002; Nogales et al. 2017). Therefore, germination trials are needed by one observer (MN) in order to minimise potential biases. After to evaluate the viability of seeds after gut passage and the effect on measuring lizards, they were immediately released at the same place germination time, in order to understand the ecological role of liz- where they were captured. ards towards plants. Differences in body size (SVL) and head size (gape width and Our aims were to assess at an archipelago level, whether (1) fru- skull length) among islands were tested using Kruskall-Wallis analy- givory is related to body and head size; and whether (2) lizards con- ses followed by Dunn’s post-hoc tests.
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