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Small size does not restrain frugivory and seed dispersal across the evolutionary radiation of Galápagos lava lizards
Abstract and Figures
Frugivory in lizards is often assumed to be constrained by body size; only large individuals are considered 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 archipelago scale across closely related species. All nine lava lizards (Microlophus spp.) were studied on the eleven largest Galápagos 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 Galápagos. Most seeds (91%) showed no external structural damage. Seedling emergence time (44 vs. 118 days) and percentage (20% vs. 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 suitable recruitment conditions. We concluded that lizards are important seed dispersers throughout the year and across the whole archipelago, regardless of body size.
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... Therefore, it is not expected that these animals have relevant roles in plant reproduction through seed dispersal and pollination. This perception has changed greatly in recent decades, revealing more flexible trophic behaviors of lizards with important implications for the communities in which they are integrated . 2 of 12 The interactions of lizards with flowers have been documented in continental environments [3, but mostly on islands [1,5,9,. The low richness of species and, therefore, fewer interspecific competitors, parasites and predators, may explain the high densities reached by lizards on islands, due to the density compensation phenomenon . ...
... (Figure 3). (6), Lobularia maritima (7), Silene vulgaris (8), Cistus monspeliensis (9) and Cistus heterophyllus (10); and pollen grains visible over a lizard (11). (6), Lobularia maritima (7), Silene vulgaris (8), Cistus monspeliensis (9) and Cistus heterophyllus (10); and pollen grains visible over a lizard (11). ...
The role of lizards as potential pollinators on islands has been documented for either one or a few plants in different parts of the world, but it has never been assessed for an entire plant community. Here, we quantified interaction rate by lizards and evaluated intraspecific differences in the use of flowers on Cabrera Gran (Cabrera archipelago, Balearic Islands) by means of visual observations, automated cameras and the analysis of pollen grain samples. Overall, we recorded interactions of the Balearic wall lizard (Podarcis lilfordi) with flowers of 44 plant species, 72.7% of which were unknown to date. Although florivory occurs in some of these species (35%), the majority of visits were legitimate (65%); in addition, we found intraspecific differences in the interactions related to the sex and age of lizards. Our findings support the role of Balearic wall lizards as potential pollinators across the entire plant community, and their contribution to particular plant species, for instance the endangered Cistus heterophyllus carthaginensis. This study also documents the first record of another sympatric lizard (Tarentola mauritanica) visiting flowers and contributes to the few existing records of flower interactions involving geckos in the Paleartic ecozone.
... barringtonensis on Santa Fe island), on the main Galápagos Islands. Studies on plant-animal interactions at an archipelago scale (despite being scarce) are essential to identify key ecological links and drivers of functional shifts in insular biodiversity (Traveset et al. 2015;Heinen et al. 2018;Hervías-Parejo et al. 2018). ...
... At least on some oceanic islands with depauperate pollinator faunas, lizards have been reported to contribute to pollination success (Olesen & Valido 2003;Fuster & Traveset 2019). If effective transfer of pollen onto stigmas results in pollination, M. habellii on Marchena and M. pacificus on Pinta would act as both pollinators and seed dispersers of Cordia leucophlyctis and Bursera graveolens, respectively (see Hervías-Parejo et al. 2018). In other words, we hypothesize that these lizard species could fit into the concept of double mutualism, similar to that already described between some Galápagos birds and plants (Olesen et al. 2018). ...
Lizards have been reported as important pollinators on several oceanic islands. Here we evaluate the potential role of Galápagos lava lizards (Microlophus spp.) as pollinators across their radiation. During three years, we sampled pollen transport by nine lava lizard species on the 10 islands where they are present, including seven single‐island endemics. Overall, only 25 of 296 individuals sampled (8.4%) transported pollen of 10 plant species, the most common being Prosopis juliflora, Exodeconus miersii, Sesuvium sp. and Cordia leucophlyctis. At least eight of these plant species were native, and none were confirmed as introduced to the archipelago. Despite the low overall proportion of individuals carrying pollen, this was observed in seven of the nine lizard species, and on eight of the ten main islands (Española, Fernandina, Floreana, Isabela, Marchena, Pinta, Santa Cruz and Santiago), suggesting that this is a widespread interaction. The results reported here support the potential role of lava lizards as pollinators across their radiation, although they may represent a relatively modest contribution when compared with birds and insects. However, we cannot discard that lizards may be ecologically significant for particular plant species and ecosystems given the specific climatic condition and functional diversity of each island. This article is protected by copyright. All rights reserved.
... This lizard is an opportunistic omnivore that travels freely across the island and establishes temporary territories during the breeding season (February-April). Mating may occur yearround given the appropriate environmental conditions (Troya 2012;Lewbart et al. 2017;Moore et al. 2017; but see Hervías-Parejo et al. 2019). Males exhibit a color pattern of dark browns and grays punctuated by a white lateral stripe running the length of the torso on each side. ...
Intrasexual selection through male competition favoring larger male body size is the preferred explanation for the evolution andmaintenance of male-biased sexual size dimorphism among polygynous species. Although sexual selection has been well studied in some groups oflizards, sexual selection in the nine species of lava lizards (Microlophus spp.) of the Gala ́pagos has received little attention. The purpose of thisresearch was to test the importance of male body size in the context of sexual selection by both sexes. Using three different sizes of robotic modelscapable of emulating the appearance and display patterns of male San Crist ́obal Lava Lizards (M. bivittatus), we analyzed the responses that themodels elicited among free-ranging lizards of the same sex (confrontation) and opposite sex (courtship). Results showed that body size of bothmale lizards and robotic antagonists influenced the number of displays performed by males. Male body size positively influenced the number ofaggressive responses, scaling with the size of the opponent. The model representing larger lizards received higher display counts from males. Bodysize of robotic models, but not female lizards, influenced the number of displays performed by females. Females responded the most to the smalland large models. Display intensity was not affected by any of the variables considered for either sex. Results from this study support thehypothesis that male-biased sexual size dimorphism in M. bivittatus is driven at least in part by both intrasexual and intersexual selection favoringlarger male body size.
... Colonisation and establishment of many plants is mediated by generalist seed dispersers. In the Canary Islands and Madeira, such a function is widely performed by frugivorous lizards (Sadek, 1981;Valido and Nogales, 1994;Nogales et al., 2016;Pinho et al., 2018), following a pattern common in many islands worldwide (Hervías-Parejo et al., 2019;Valido and Olesen, 2019). Lizard-plant interactions result in a relatively short-distance dispersal pattern of seed distribution, with the lizard Gallotia stehlini dispersing seeds over almost 100 m on Gran Canaria (Pérez-Méndez et al., 2016). ...
Research in Macaronesia has led to substantial advances in ecology, evolution and conservation biology. We review the scientific developments achieved in this region, and outline promising research avenues enhancing conservation. Some of these discoveries indicate that the Macaronesian flora and fauna is composed of rather young lineages, not Tertiary relicts, predominantly of European origin. Macaronesia also seems to be an important source region for back-colonization of continental fringe regions on both sides of the Atlantic. This group of archipelagos (Azores, Madeira, Selvagens, Canary Islands, and Cabo Verde) has been crucial to learn about the particularities of macroecological patterns and interaction networks on islands, providing evidence for the development of the General Dynamic Model of oceanic island biogeography and subsequent updates. However, in addition to exceptionally high richness of endemic species, Macaronesia is also home to a growing number of threatened species, along with invasive alien plants and animals. Several innovative conservation and management actions are in place to protect its biodiversity from these and other drivers of global change. The Macaronesian Islands are a well-suited field of study for island ecology and evolution research, mostly due to its special geological layout with 40 islands grouped within five archipelagos differing in geological age, climate and isolation. A large amount of data is now available for several groups of organisms on and around many of these islands. However, continued efforts should be made towards compiling new information on their biodiversity, to pursue various fruitful research avenues and develop appropriate conservation management tools.
... However, in other plant species, especially those possessing drupe-or berry-type fleshy fruits, higher percentages of germination of lizard-ingested seeds have been reported regularly . Several studies, including ours, have found that the digestive tracts of lizards could enhance seed germination . Our results showed that a DRT of 0-70 h could directly promote the germination rate of C. spinosa seeds, and, although statistical analysis showed no significant difference between other gut-passed seeds and the control group, the germination rates after DRTs of 72-120 h (9.28%) and 120-360 h (8.84%) were higher than those of the control group (2.92%). ...
Seed dispersal is a key component of the interactions between plants and animals. There is little research on the effects of lizard seed dispersal, which is more common on islands than elsewhere. In this study, the effects of the passage of Capparis spinosa seeds through Tera-toscincus roborowskii lizard digestive tracts on the seed coats, water uptake rates and germination rates were investigated. In addition, the spatial patterns of fecal deposition by lizards in various microhabitats were assessed. Our results showed that the mean retention time (MRT) of mealworms was significantly longer than that of C. spinosa seeds in both adult and juvenile lizards. The defecation rate of C. spinosa tended to be lower than that of mealworms, which might be beneficial for seed dispersal. It was determined that the longer MRT of C. spinosa seeds enhanced the permeability of the seed coats, which promoted fast water uptake, broke seed dormancy and increased the seed germination rate. Furthermore, the seeds that passed through the digestive tracts of lizards were deposited in favorable germination microhabitats. By enhancing seed germination and depositing intact and viable seeds in safe potential recruitment sites, the lizard T. roborowskii acts, at least qualitatively, as an effective disperser of C. spinosa.
... In this respect, several studies have shown that small arthropod-eating lizards do consume fruit if their favorite arthropod food is scarce. This is most often observed on islands (e.g., Patterson, 1928;Vinson and Vinson, 1969;Schoener et al., 1982;Cheke, 1984;Whitaker, 1987;Pérez-Mellado and Corti, 1993;Valido and Nogales, 1994;Wotton, 2002;Hare et al., 2016;Wotton et al., 2016;Melzer et al., 2017;Parejo et al., 2018), where arthropods might be in short supply, but also in arthropod-poor habitats on mainland, such as high mountains and deserts (e.g., Fuentes, 1976;Mautz and Lopez-Forment, 1978;Hódar et al., 1996;Whiting and Greeff, 1997;Kiefer and Sazima, 2002;Espinoza et al., 2004;Valdecantos et al., 2012). By feeding from at least two trophic levels, these lizards become omnivorous. ...
Birds and mammals are the only vertebrates which receive comprehensive attention in studies of dispersal of fleshy-fruited plant species. However, recently the importance of fleshy fruit in the diet of lizards (order Squamata: suborder Sauria), and their role as seed dispersers have been recognized in a number of studies, especially in studies from arthropod-poor habitats, such as oceanic islands. Here, we revisit the evidence of fruit-eating lizards on a global scale in order to test if fruit consumption is more common on islands than expected by chance. We constructed a database of 470 lizard species (from a global count of 6,515 species), that have been reported to consume fleshy fruits. This set of lizards belong to 27 families with Scincidae (N = 78 species), Gekkonidae (69), and Dactyloidae (55) having more frugivorous species than other lizard families. We found that 62.4% of these lizards inhabit islands, whereas only one third (35.3%) of all lizard species inhabit islands. These values support the presence of an “insular phenomenon,” however; we also tested if this biogeographical pattern might be driven by body size and evolutionary history of lizards. Thus, we looked for any phylogenetic signals in the distributions of lizard body size, island-presence, and frugivory and calculated phylogenetically corrected correlations among the three variables on a global subset of 2,417 lizard species for which we had detailed phylogenetic information. Both lizard body size and island-presence were weakly influenced by phylogeny; whereas, frugivory was not. In addition, we found that (1) body size and frugivory were weakly positively correlated; (2) body size and island-presence were uncorrelated; and (3) island-presence and frugivory were strongly positively correlated. Thus, we conclude that the main driver of frugivory on islands is the specific island environment and not lizard body size per se. Islands are said to be poor in arthropods and predators, and this may force/allow island lizards to forage for additional food sources, such as fleshy fruits. We also suggest that modern lizards as well as their ancestors may potentially play an important role to many plants as seed dispersers. However, we do not known how tight the correlation is between frugivory and seed dispersal. Thus, lizards repeatedly inspire us to ask new ecological and evolutionary questions.
Plant-lizard interactions are still poorly studied, despite lizards are known to interact with flowering plants in many parts of the world. They are commonly reported on islands although the number of documented interactions has also increased in mainland, mostly in isolated environments. In this study, we first performed a global review to explore whether lizard-flower and lizard double mutualistic interactions in continents occur in environments similar to those of islands. Then, we aimed at explaining the factors driving the current distribution of such interactions worldwide. To do this, we considered four environmental factors (latitude, altitude, rainfall and temperature), and phylogeny and body size of lizards that may influence flower visitation. Furthermore, we investigated for the first time the functional role (legitimate visit vs florivory) of lizards in plant reproduction and the conditions under which each type of interaction occurs. Finally, we explored the factors influencing the distribution of lizard double mutualisms wordwide. We recorded a total of 452 lizard-flower interactions (c. 3.4% and 0.1% of the extant lizard and plant species, respectively). Lizard-flower interactions were more frequently recorded on islands (79%) regardless of phylogeny and lizard body size, whereas in mainland the number of interactions increased with altitud. Our analyses also revealed that only 20% of all interactions confirmed pollination effectiveness and a strong association of the type of interaction with environmental factors and species traits. Regarding the distribution of lizard double mutualisms, we found a positive effect of island and rainfall, but a decrease in their occurrence with latitude, altitude, temperature and body size. We predict that mutualistic plant-lizard interactions will be increasingly documented, especially in isolated environments (both on islands and continents), which will help us to better understand the biological patterns of this phenomenon and the mechanisms underlying them.
Island faunas can be characterized by gigantism in small animals and dwarfism in large animals, but the extent to which this so-called ‘island rule’ provides a general explanation for evolutionary trajectories on islands remains contentious. Here we use a phylogenetic meta-analysis to assess patterns and drivers of body size evolution across a global sample of paired island–mainland populations of terrestrial vertebrates. We show that ‘island rule’ effects are widespread in mammals, birds and reptiles, but less evident in amphibians, which mostly tend towards gigantism. We also found that the magnitude of insular dwarfism and gigantism is mediated by climate as well as island size and isolation, with more pronounced effects in smaller, more remote islands for mammals and reptiles. We conclude that the island rule is pervasive across vertebrates, but that the implications for body size evolution are nuanced and depend on an array of context-dependent ecological pressures and environmental conditions.
Living lizards exploit almost all terrestrial ecosystems where they play the roles of both predator and prey in complex food webs. Bels et al. (Biomechanics of feeding in Vertebrates, 197–240, 1994) and Schwenk (Feeding: form, function and evolution in Tetrapod Vertebrates, 459–485, 2000) provided first detailed overviews about the anatomical and functional traits of the feeding stages and phases of the feeding cycle in these tetrapods. Here, we synthesize recent literature in order to provide discussion of the evolution of their feeding behavior from capture to swallowing.
Significance How eating animals affect the evolution of fruit-producing plants is still poorly understood. This is important because large vertebrates are being overhunted in ecosystems around the world, which might force plants to alter phenotypes in response to the loss of these animals. I used a natural experiment in which many of the same plant lineages in a large and megadiverse tropical archipelago have been exposed to very different suites of vertebrates on different islands. Statistical analysis that accounts for species’ shared evolutionary histories revealed that average fruit sizes across more than 400 plant species were positively related to the diversity and size of the fruit-eating birds and mammals in each area. Fruit color, however, was not affected by the vertebrate assemblage.
The accelerating rate of vertebrate extinctions and population declines threatens to disrupt important ecological interactions, altering key ecosystem processes such as animal seed dispersal. The study of highly specialized mutualistic interactions is crucial to predict the consequences of population declines and extinctions. Islands offer unique opportunities to study highly specialized interactions, as they often have naturally depauperated faunas and are experiencing high rates of human-driven extinctions. In this study, we assess the effect of seed dispersal on seedling recruitment of Ephedra fragilis (Ephedraceae) on a Mediterranean island ecosystem. We used field data and stochastic simulation modeling to estimate seed fate and recruitment patterns of this pioneer shrub typical of arid and semiarid areas, andto estimate the dependence of recruitment on the lizard Podarcis lilfordi (Lacertidae), its only known seed disperser. Ephedra fragilis recruitment highly depended on lizards: lizards produced 3.8 times more newly-emerged seedlings than non-dispersed seeds and no seedlings from undispersed seeds survived the study period. Seed dispersal by lizards was mostly to open sites, which was key for the increased success observed, while undispersed seeds, falling under mother plants, suffered higher predation and lower seedling emergence andsurvival. The ability of this pioneer shrub to get established in open ground is crucial for vegetation colonization and restoration, especially on degraded lands affected by desertification, where they act as nurse plants for other species. Lizards are key in this process, which has important consequences for community structure and ecosystem functioning.
Seed dispersal and seedling recruitment are crucial phases in the life cycle of all spermatophyte plants. The net contribution of seed dispersers to plant establishment is known as seed dispersal effectiveness (SDE) and is defined as the product of a quantitative (number of seeds dispersed) and a qualitative (probability of recruitment) component. In Galápagos, we studied the direct contribution to SDE (number of seeds dispersed and effect on seedling emergence) provided by the five island groups of frugivores (giant tortoises, lizards, medium-sized passerine birds, small non-finch passerine birds and finches) in the two main habitats in this archipelago: the lowland and the highland zones, and found 16 vertebrate species dispersing 58 plant species. Data on frequency of occurrence of seeds in droppings and number of seeds dispersed per unit area produced contrasting patterns of seed dispersal. Based on the former, giant tortoises and medium-sized passerines were the most important seed dispersers. However, based on the latter, small non-finch passerines were the most important dispersers, followed by finches and medium-sized passerines. The effect of disperser gut passage on seedling emergence varied greatly depending on both, the disperser and the plant species. Although the contribution to SDE provided by different disperser guilds changed across plant species, medium-sized passerines (e.g. mockingbirds) provided a higher contribution to SDE than lava lizards in ten out of 16 plant species analysed, whereas lava lizards provided a higher contribution to SDE than birds in fiveplant species. While both the quantitative and qualitative components addressed are important, our data suggests that the former is a better predictor of SDE in the Galápagos archipelago. This article is protected by copyright. All rights reserved.
Insular species are predicted to broaden their niches, in response to having fewer competitors. They can thus exploit a greater proportion of the resource spectrum. In turn, broader niches are hypothesized to facilitate (or be a consequence of) increased population densities. (2) We tested whether insular lizards have broader dietary niches than mainland species, how it relates to competitor and predator richness, and the nature of the relationship between population density and dietary niche breadth. (3) We collected population density and dietary niche breadth data for 36 insular and 59 mainland lizard species, and estimated competitor and predator richness at the localities where diet data were collected. We estimated dietary niche shift by comparing island species to their mainland relatives. We controlled for phylogenetic relatedness, body mass, and the size of the plots over which densities were estimated. (4) We found that island and mainland species had similar niche breadths. Dietary niche breadth was unrelated to competitor and predator richness, on both islands and the mainland. Population density was unrelated to dietary niche breadth across island and mainland populations. (5) Our results indicate that dietary generalism is not an effective way of increasing population density nor is it result of lower competitive pressure. A lower variety of resources on islands may prevent insular animals from increasing their niche breadths even in the face of few competitors. This article is protected by copyright. All rights reserved.
Capsule: The diet of Yellow-legged Gulls Larus michahellis on an oceanic island, surrounded by deep waters without a wide shelf, was mainly composed of terrestrial invertebrates. Aims: To study the trophic ecology of Yellow-legged Gulls on an island surrounded by deep waters, to quantify the importance of terrestrial prey items and their availability, and to evaluate the relative importance of nutritional values of terrestrial and marine resources. Methods: Diet was monitored for one year. We assessed the relative contribution of the main prey items and their macronutrients through the study of pellets and faeces. Results: Terrestrial invertebrates were the most frequently consumed prey items (frequency of occurrence (FO) 67%), followed by marine fish (Osteichthyes FO 33%). Coleoptera and Orthoptera were the most consumed terrestrial invertebrates and provided a high nutritional value. The rate of consumption of terrestrial invertebrates varied in synchrony with the breeding season, being higher in spring, indicating their potential importance for reproduction. Conclusion: It is unusual that terrestrial invertebrates constitute a large proportion of the diet of large gulls, but they seemed to cover their trophic energy requirements during the reproductive period.
Seed dispersal is a vital step for plant reproduction and long-term vegetation dynamics, and many plants rely on animals for this process. Large animals are disproportionally important dispersers, however they tend to be under a higher extinction risk worldwide. There is compelling evidence that the global biodiversity crisis is leading to the deterioration of several ecosystem functions, including that of seed dispersal. However, there is virtually no information on how large-scale refaunation efforts can reinstate seed dispersal. We evaluated the effectiveness of a 62 km(2) wildlife sanctuary, aimed at recovering large mammals' populations in the Gorongosa National Park (Mozambique), in restoring seed dispersal interactions. The sanctuary provided a unique natural experiment to test the effect of large-mammals' refaunation on this key ecosystem function. The results reveal a higher diversity of dispersers inside the sanctuary that translates into a more diverse, larger and more complex seed-dispersal network. The higher number and diversity of seeds dispersed inside the sanctuary was explained mostly by the greater disperser's abundance, rather than by their identity. Overall, the seed dispersal network inside the sanctuary was less specialized (>H2') and there was a greater overlap on the plant species dispersed by all animals. Both networks were significantly modular and anti-nested. Our findings suggest that conservation efforts aimed at recovering large mammals populations are reinstating not only those target species, but also their functional roles in the ecosystems, specifically restoring seed dispersal networks in Gorongosa. This article is protected by copyright. All rights reserved.
Capsule: The diet of Yellow-legged Gulls Larus michahellis on an oceanic island, surrounded by deep waters without a wide shelf, was mainly composed of terrestrial invertebrates.Aims: To study the trophic ecology of Yellow-legged Gulls on an island surrounded by deep waters, to quantify the importance of terrestrial prey items and their availability, and to evaluate the relative importance of nutritional values of terrestrial and marine resources.Methods: Diet was monitored for one year. We assessed the relative contribution of the main prey items and their macronutrients through the study of pellets and faeces.Results: Terrestrial invertebrates were the most frequently consumed prey items (frequency of occurrence (FO) 67%), followed by marine fish (Osteichthyes FO 33%). Coleoptera and Orthoptera were the most consumed terrestrial invertebrates and provided a high nutritional value. The rate of consumption of terrestrial invertebrates varied in synchrony with the breeding season, being higher in spring, indicating their potential importance for reproduction.Conclusion: It is unusual that terrestrial invertebrates constitute a large proportion of the diet of large gulls, but they seemed to cover their trophic energy requirements during the reproductive period.
Seed dispersal, together with pollination, are two key services provided by animals to plants. On oceanic islands, where strong isolation limits the arrival of medium and large sized mammals (Gorman 1979), tortoises, iguanas or lizards often undertake an important ecological role as dispersers (Olesen & Valido 2003). Furthermore, the reported niche expansion or interaction release of island vertebrates, which tend to occupy underexplored ecological niches and adopt super-generalized diets, magnifies the ecological importance of insular native fauna (MacArthur et al. 1972; Cox & Ricklefs 1977; Traveset et al. 2015). This article is protected by copyright. All rights reserved.