https://orcid.org/0000-0002-0810-749X
Figures
Abstract
Marine subsidies in the extremely arid islands of the northern Gulf of California have been shown to be important enhancing primary productivity and fueling the terrestrial food webs. This effect has been proved in plants, insects, lizards and rodents. The aims of our study were first to determine whether insectivorous lizards from a wide array of islands, including some in the central and southern part of the Gulf, are consuming marine derived products, and secondly to assess its impact on herbivore lizards as well. We hypothesized that the availability and use of marine nutrients for lizards would vary depending on island aridity, island size, and the presence of seabird colonies nearby. To test the hypothesis, we analyzed the isotopic niches of 13 populations of insectivorous lizards (genus Uta) and 9 populations of herbivore iguanas (genera Dipsosarus, Ctenosaura, and Sauromalus) across 16 islands spanning 5 latitude degrees and 350 nautical miles. Our results showed that the proximity of seabird colonies play a key role in reinforcing the presence of marine origin nutrients in both insectivorous and herbivore populations. The ubiquity of seabird colonies on the northern islands combined with higher aridity in the northern part of the Gulf, creates a northward gradient in the importance of marine subsidies for both insectivorous and herbivore lizards, across the Gulf islands. δ13C variation in insectivorous lizards’ tissues was significantly correlated with island aridity/latitude, while the presence of significant seabird colonies nearby was significantly correlated with δ15N variation. The results were less clear in the herbivore group of species. Insectivorous and herbivorous share a large portion (70%) of their isotopic space. The incorporation of the highly enriched 15N to both type of lizards is happening for the two possible ways, the presence of guano, that may be driving plant fertilization, and the direct consumption of insects associated to the birds (or birds’ products, as eggs or corpses); but we could not differentiate between them. The size of the islands was not relevant in our results, possibly due to our sampling design. Additional isotopic analysis of plants and arthropods and in a gradient coast-inland could provide a more comprehensive view of the nutrient flow within these island ecosystems and the effect of the island size.
Citation: Barraza-Soltero IK, Blázquez M, Hernández-Vázquez S, Delgado-Huertas A, Muro-Torres VM (2025) Understanding the influence of marine nutrients on insectivorous and herbivorous reptiles in the Gulf of California islands. PLoS One 20(8): e0329414. https://doi.org/10.1371/journal.pone.0329414
Editor: Hideyuki Doi, University of Hyogo, JAPAN
Received: October 14, 2024; Accepted: July 16, 2025; Published: August 22, 2025
Copyright: © 2025 Barraza-Soltero et al. This is an open access article distributed under the terms of the Creative Commons Attribution License, which permits unrestricted use, distribution, and reproduction in any medium, provided the original author and source are credited.
Data Availability: All relevant data are within the manuscript and its Supporting information files.
Funding: The fieldwork was supported by institutional funds from the Centro de Investigaciones Biológicas del Noroeste [to MCB]. The Mexican government (CONACYT- SECIHTI) provided funding in the form of a scholarship [773264/2020 to IKB-S] and the German Academic Exchange Service (DAAD-Mexico) provided funding in the form of a doctoral grant [57693453 to IKB-S]. The Isotopes analyses were funded by the Ministerio de Ciencia e Innovación through European Regional Development Fund [SUMHAL, LIFEWATCH-2019-09-CSIC-13, POPE 2014-2020 to AD-H].
Competing interests: The authors have declared that no competing interests exist.
Introduction
One of the main questions in behavioral ecology is understanding how species and populations adapt to resource fluctuations in changing environments across their distribution areas. Individual fitness is influenced by inter- or intra-specific interactions but also by climate, habitat heterogeneity, and access to available resources. Some low-productivity, isolated ecosystems, such as arid islands, present unique challenges for animal populations because of the limited habitat heterogeneity, general resource scarcity, and temporally unpredictable variation in resource availability [1–3]
Occasionally, some of those low-productivity systems are surrounded by richer environments such as forests or oceans that, being more productive, provide allochthonous subsidies into the low-productivity systems [4–7]. Examples include “sky islands” such as tepuis or high summits, as well as proper insular ecosystems such as small or arid oceanic islands. Allochthonous marine subsidies entering these arid islands facilitate interaction between oceanic and terrestrial ecosystems by transferring materials, thereby influencing the dynamics of recipient communities [8–10]. Arid islands, islets, and small rocks of the Gulf of California, with their low primary productivity (0–60 gm-2yr-1 dry mass) [11,12] and unique biodiversity [13], offer an ideal setting to study this phenomenon [14–17].
Marine subsidies, which are transported to terrestrial ecosystems through donor-controlled processes (e.g., deposition of macroalgae, detritus, and stranded organisms on shores) or animal-mediated mechanisms (e.g., consumption of marine invertebrates, guano deposition, and remnants from seabird reproductive colonies or roosting places) [8,16], can significantly impact recipient communities. On Gulf of California islands, these subsidies have been linked to increased populations of various species, including invertebrates, lizards, rodents, and plants [4,10,16–18].
Reptiles are the most common vertebrates inhabiting these islands. They have been used as models for exploring long-term isolation, life history, evolution, behavioral change, and expansion of trophic niches to include newly available marine resources [9,10,13,19,20]. The species there, some of them endemic, have the potential to develop plasticity in their feeding behaviors [13,20] and, in some cases, they exhibit convergent responses to environmental resource variations, regardless of phylogenetic relatedness [2,9].
Our study aimed to explore how lizards, whether herbivorous or insectivorous, utilize marine-derived nutrients across multiple islands in the Gulf of California. We hypothesized that the extent of marine components in lizard diets of the same genus would vary depending on factors such as island aridity [7], island size [21], and the presence of significant nearby seabird colonies [17,18]. To test this hypothesis, for insectivorous species we compared the isotopic niches of Uta lizard populations inhabiting the coastal fringes of several Gulf of California islands. For the herbivorous species we compared Dipsosaurus, Ctenosaura or Sauromalus iguana populations inhabiting different islands. This approach was deemed valid because geographic variation in the isotopic niche of generalist predators offers insights into spatial changes in their food webs [22], especially in basal resources fueling trophic webs [23]. We predicted that, despite potential individual variations, meaningful differences in species´ isotopic niches could still be detected across islands, reflecting variations in island aridity, island size, and seabird colony influence [24].
To assess and compare the trophic niches of insectivorous and herbivorous lizards, we employed stable isotope analysis of nitrogen (δ15N) and carbon (δ13C). Stable nitrogen isotopes are a powerful tool for tracing the flow of marine nutrients into terrestrial food webs [25]. Nitrogen isotope values (δ15N) increase predictably with each trophic level. Marine food webs, being generally longer than terrestrial ones, lead to higher δ15N values [26] in marine organisms, and marine-derived resources, such as stranded animals, exhibit elevated δ15N values in consequence. Also, marine algae have higher δ15N values than terrestrial plants. Usually studies consider a trophic discrimination factor (TDF) of approximately 3.4‰ [27,28], due to fractionation processes during protein synthesis and the excretion of lighter isotopes, although the factor could vary more than 9‰ withing a single species and tissue type. We used the generally ~3.4‰ because of the great variation in our samples (species, islands), and to make our results comparable with previously published data. One of the main sources for transferring marine-derived nitrogen onto the islands are seabird colonies. It can be directly through arthropods that feed on seabird by-products, such as faeces, eggs, corpses, and chicks, and hence they become good prey for their reptilian predators [10,29]. The other way is indirectly, because guano (which has a higher proportion of 15N compared to 14N due to the birds’ high trophic position and the preferential volatilization of the lighter isotope [30]) increases the nitrogen content in the soil, from where it is transferred to plant tissue and detritus, which then serves as a food source for detritivores and arthropods [17,18,31]. Variations in carbon isotope signatures (δ13C) between marine and terrestrial organisms also provide insights into long-term dietary patterns, particularly in species with mixed diets. Minimal carbon fractionation, around ~1‰ but also potentially highly variable [28], occurs during digestion and assimilation, resulting in consumer tissues reflecting the δ13C values of their food sources [25,32–34]. In this case, and for the same reasons that we considered in N TDF, we stayed with the traditionally used ~1‰ TDF for C. In terrestrial environments, plants exhibit a range of δ13C values depending on their photosynthetic pathways. C3 plants, the most common type, typically have very negative values (<−28‰) compared with C4 and CAM metabolism plants (−12‰ to −13‰) [33,35]. Marine phytoplankton and coastal algae have intermediate δ13C values (−12‰ to −24‰), while intertidal organisms feeding on algae can exhibit values similar to, or more enriched than C4 plants (−11‰ to −18‰) [10,36]. These distinctions allow for the differentiation of carbon sources incorporated into island-dwelling organisms, indicating whether they originated from marine or terrestrial environments [37].
Overall, we expected higher (less negative) δ13C and higher δ15N values in lizards living near seabird colonies [24], in lizards on smaller islands due to greater exposure to marine nutrients [21], and in lizards from more arid islands due to low primary productivity and the dominance of C4/CAM plants. Finally, we anticipated higher δ15N values in insectivorous lizards compared with herbivorous species, reflecting their higher trophic position.
Materials and methods
Study area
The Gulf of California hosts over 200 islands, islets, and small rocks, spanning 900 km across 7 degrees of latitude. Our study focused on 16 of these islands, covering 650 km and 5 degrees of latitude and encompassing a gradient of sizes, aridity levels, and presence of seabird colonies (Fig 1). Primary productivity on these islands fluctuates significantly across years because rainfall is unpredictable. There can be periods of three or more years without any rainfall. Rainfall events, when they occur, are typically concentrated within a few days, leading to ephemeral blooms of grass (C4 plants) [4]. The islands’ perennial vegetation, while generally scarce, is dominated by drought-tolerant Cactaceae and Agavaceae species, which use crassulacean acid metabolism (CAM). Other plant families present, including Leguminosae, Burseraceae, and Asteraceae, primarily use the C3 photosynthetic pathway [38,39].
The islands are identified with a color pattern following an aridity/latitudinal gradient where red/orange color means more aridity, yellow/green mid-aridity, and blue less aridity. 1: Mejia, 2. Angel de la Guarda, 3: Salsipuedes, 4: Las Animas, 5: San Esteban, 6: San Lorenzo, 7: San Pedro Martir, 8: Tortuga, 9: Coronados, 10: Danzante, 11: La Islita, 12: Las Galeras, 13: Santa Catalina, 14: El Pardito, 15: La Partida, and 16: Espiritu Santo. Map created using the open-source software QGIS [41]. We used two raster vector files from https://www.naturalearthdata.com/. “Land polygons including major islands” large scale data 1:10,000,000 and “Minor islands, islands that are 2 sq. km or less in size” large scale data 1:10,000,000. Derived from 1:250,000 World Vector Shoreline. The coordinates were taken from https://datos.abiertos.inecc.gob.mx/Datos_abiertos_INECC/CGACC/DocumentosRIslasMarias/Eje2_InstrumentosDelTerritorioInsularMexicano/CatalogoInsularDelTerritorioMexicano.pdf.
CAM and C4 carbon fixation are the two photosynthetic pathways well-adapted to arid environments. CAM plants produce more sugar than C3 plants under conditions of high light and temperature, and can fix carbon while their stomata are closed, allowing for better water retention. C4 plants fix carbon during the day and are more efficient than C3 plants, keeping their stomata almost fully closed. However, C4 plants are less nutritious than C3 plants, containing less nitrogen and more fiber, and they are more difficult to digest [40]. The presence of each metabolic pathway can be identified through the carbon isotope analysis of the plant itself or its consumer.
Model species and sampling
The Gulf of California islands host a unique lizard fauna, with many species endemic to one or more islands [13,42,43]. Our study focused on three insectivorous species of the genus Uta: U. palmeri, endemic to San Pedro Martir Island, U. squamata, endemic to Santa Catalina Island, and U. stansburiana, widely distributed across several islands. We also included four herbivorous species of the genus Sauromalus distributed across several islands: S. hispidus, S. varius, S. slevini, and S. obesus (Table 1). Additionally, we included Ctenosaura conspicuosa, an herbivorous species endemic to San Esteban Island, and two species of the genus Dipsosaurus: D. dorsalis and D. catalinensis, the latter being endemic to Santa Catalina Island. While both Dipsosaurus species are primarily herbivorous, they are known to opportunistically consume insects.
We conducted diurnal surveys in all available habitats within 200 meters of the shoreline on each island. We did not collect the GPS data of each precise capture. Lizards were captured using a fishing rod with a thread loop at the end. For each island visit, we collected, when possible, two sets of samples (two populations) representing insectivorous and herbivorous lizards. After each capture, we trimmed approximately 1 cm of the tail tip and preserved the tissue samples in vials with 70% alcohol. This research was carried out under SEMARNAT permits SGPA/DGVS/ −10182/11–07594 7/15–2971/20–05480/21 for handing animals. No organisms were sacrificed for this work.
To characterize the isotopic baseline of primary producers, we collected and analyzed plant samples from Angel de la Guarda Island. This included C3 plants (Larrea tridentata, Datura spp., Euphorbia lomelii, Marina spp, Batis maritima, Lupinus spp. Cucurbita cordata), C4/CAM plants (Stenocereus gummosus, Cylindropuntia cholla, C. imbricata, Pachycereus pringlei, Lophocereus schottii, Stenocereus thurberi, Mammillaria dioica, Opuntia fulgida, Agave spp., Echinocactus platycathus), and marine seaweed (species not determined). We compared the average isotopic values of these plants to the isotopic space occupied by herbivorous lizards. This plant data was complemented with values from the literature [4,10,16,17,23,44] (S1 Table). While we did not collect arthropod samples for direct isotopic analysis, we incorporated data from the literature [4,10,16] on arthropod isotopic signatures from the region to provide context for insectivorous lizard isotopic values (S2 Table).
Fieldwork was conducted between November 2013 and September 2021 (S3 Table). This period included two El Niño events (September 2014 – May 2016), (July 2018 – June 2019) and three La Niña events (July 2016 – January 2017; September 2017 – May 2018; July 2020 – September 2021) [45]. To conduct an exploratory analysis of the effect of those events on our samples, and because of the effect of the ENSO events on the seabird colonies, and on the island vegetation, we assigned a category to each population depending on whether the samples had been taken during neutral season or a period covered by an El Niño or La Niña event (S3 Table) and we then compared the values of δ13C‰ and δ15N‰ of each group using a non-parametric Kruskal-Wallis test. Only populations of U.stansburiana had different average values of δ15N‰ across neutral and El Niño years (K-W chi-squared = 6.226, df = 2, p-value = 0.04; neutral n = 11, average δ15N‰ = 25.3 ± 4.41; Niño n = 35, average δ15N‰ = 19.6 ± 7.86).
Stable isotopes analysis
All stable isotope analyses were carried out at the Stable Isotope Laboratory of the Instituto Andaluz de Ciencias de la Tierra (CSIC-UGR, Granada, Spain). Homogenized lizard tail tips were analyzed for carbon and nitrogen isotopic composition using a Carlo Elba NC1500 elemental analyzer (Milan, Italy) with a Delta Plus XP (ThermoQuest, Bremen, Germany) mass spectrometer (EA-IRMS).
Lipid extraction was not performed, given that lizard tail tips typically exhibit low lipid content [23,46]. This approach is valid when the lipid content is under 10%, indicated by a C:N ratio value around 4 [47], and only one of our samples per group had a C:N ratio > 5 (6.8) (S3 Table). Stable isotope values are presented as δ values per mil, calculated using the formula; δ = (Rsample/Rstandard – 1) * 1000, where R represents the ratio of heavy to light isotopes (13C/12C for δ13C and 15N/14N for δ15N).
Commercial CO2 and N2 served as internal standards for carbon and nitrogen analyses, respectively. For carbon, we used two internal standards of −30.63‰ and −11.65‰ (Vienna Pee Dee Belemnite; V-PDB), analyzed every ten samples. For nitrogen, we used two internal standards of −1.02‰ and +16.01‰ (AIR). The calculated precision, after correction for daily mass spectrometer drift, based on standards systematically analyzed across analytical batches was better than ±0.1‰ for both δ13C and δ15N.
Isotopic niche metrics
We analyzed isotopic niches for insectivorous and herbivorous lizard populations separately. For each island population with at least five samples, we estimated isotopic niches using Bayesian Analysis of Standard Ellipses with the SIBER package in R [48,49]. We calculated the Standard Ellipse area (SEAc) with 95% of the data. Additionally, to obtain basic summary statistics of each population, we calculated Layman metrics [50]. They include total area of the convex hull with 100% of the data (TA), Carbon range (CR), Nitrogen range (NR), mean distance to centroid (CD), and mean nearest neighbor distance (MNND). These measures allow us to compare the populations.
To evaluate the impact of seabird colonies on the insectivorous, we grouped the 65 tail-tip samples into two categories: islands with significant seabird presence and islands without, disregarding aridity/latitude and island size. We then calculated isotopic niche metrics for each group
We also used the “Ellipse Overlap” function within SIBER to quantify shared isotopic space between island populations and between insectivores and herbivores.
Statistical analysis
To assess aridity and latitude relationships among the islands, we calculated the aridity index (AI) for each island using data from the Mexican Insular Territory layer [51] and WorldClim bioclimatic variables: Annual Precipitation and Mean Annual Temperature spanning the period of 1970−2000 [52]. We used these data because specific climate data for the Gulf of California islands were unavailable. Despite the existence of numerous aridity indices, we chose the Köppen aridity index for its recognized accuracy in reflecting arid climates in North America [53,54], and because it collects the rainfall data for long periods, which would include Enso events, that we noticed could be important for the δ15N levels of insectivorous populations (see model species and sampling). The data were processed using the Geographic Information System software QGIS 3.16.13 [41], applying Köppen’s formula for aridity: AIKöppen = MAP/ MAT + 33, where MAP denotes Mean Annual Precipitation, MAT denotes Mean Annual Temperature, and 33 is a constant. AI values equal to or greater than 0.32 indicate less arid conditions, values between 0.21–0.31 indicate moderate aridity, and values at or below 0.20 denote hyper-aridity. Subsequently, we explored correlations between latitude, MAT, MAP, and AI using Spearman correlation.
Seabird colony presence was determined based on the literature [2,10,17,18,29] and on field observations over the years. Because it has been proved that the impact of the colony’s decays spatially and temporary [24], we categorized its presence as positive only when colonies (nests or perches) were evident on at least 25% of the island (for which we made a coastal survey by boat) or were close (less than 1 km) to our sampling area; otherwise, any seabird colony presence was categorized as “absence”. While we recognize the significant effects of guano on soil fertility and biogeochemistry, we lacked information on historical seabird colonies, except for very evident and current colonies on Isla Rasa, San Lorenzo and San Pedro Martir which we considered as with birds [55–58]. Given this limitation and the short lifespan of lizards, we excluded historical seabird data from our analysis.
We used Linear Mixed-Effects Models (LME) with response variables (y) being carbon and nitrogen values and independent variables being aridity index, island size, and the presence/absence of significant seabird colonies. We did not have the precise location of each lizard, and because we visited three of the islands more than once (S3 Table), we included the island as a random effect in order to avoid pseudoreplication (δ13C or δ15N ~ aridity index+ island size + presence/absence of significant seabird colonies, random = ~ 1 | island ID). Separate models were used for insectivorous lizards (n = 65) and herbivorous lizards (n = 44). All analyses were performed in R version 4.4.2 (2024-10-31) -- “Pile of Leaves”, using the package “nlme” with the “lme” function [59].
Results
We found significant negative correlations between Latitude and Mean Annual Temperature (MAT) (Spearman r = −0.62, p = 2.6e-09), Mean Annual Precipitation (MAP) (Spearman, r = −0.95, p < 2.2e-16), and the aridity index (AI) (Spearman, r = −0.95, p < 2.6e-16). These results indicate that northern islands in the Gulf of California tend to be cooler, drier, and more arid than the southern islands.
Insectivorous lizards
We analyzed 65 tail-tip samples from insectivorous lizards (Table 1). As predicted, lizards on more arid islands rely more on marine-derived nutrients and had significantly less negative δ13C, while on islands with presence of sea birds’ colonies, we found lizard tissues containing significantly higher values of δ15N (Table 2). The size of the islands was not significantly correlated with the isotopic variation in the lizard´s tissues. The correlation between the variables was similar in both models C and N (aridity/size correlation 0.24, 0.26; sea birds presence/aridity correlation 0.46, 0.47 and presence of seabirds/size correlation 0.28, 0.30).
The isotopic spaces of Uta stansburiana populations generally followed a latitudinal (aridity) gradient with more influence of marine nutrients on the northern (more arid) islands with two exceptions (Fig 2). First, the population from El Pardito Island showed less negative isotopic C (−13.27 ± 1.3‰) than other islands at its latitude. Second, the population from Las Galeras Island in the middle of the Gulf exhibited the least negative δ13C values (−11.51 ± 1.22‰) of all.
The color pattern of each island corresponds to the latitudinal gradient shown in Fig 1.
The lizards from these two islands have also high δ15N values (24.28 ± 1.55‰, 38.22 ± 1.30‰) indicating strong influence of marine nutrients. El Pardito is tiny and the only habited island on the Gulf, the fishermen living there leave fish entrails quite regularly on the shoreline. Las Galeras support a large yellow-footed seagull colony (Larus livens) present across almost the entire flat part of the island, where the lizards live and forage (personal obs) [60] and its vegetation is comprised only of cactus (CAM).
Uta populations living close to seabird colonies on islands of the northern part of the Gulf also had elevated δ15N values (Table 1, Fig 1). Salsipuedes’ population (northern non-bird island) also had elevated δ15N values.
The carbon range value (CR) was wide on the population from Salsipuedes Island, and on the population from Coronados in the middle Gulf, and narrower on the islands with sea bird colonies. The minimum range corresponded to the less arid sampled island, Espiritu Santo (Table 3), on the southern part of the Gulf.
Las Animas and Salsipuedes, on the north, and Tortuga in the middle of the Gulf, had the widest nitrogen range values (NR) (Table 3). Individuals from these populations had also disperse position within the isotopic space (MNND) suggesting variability in their diets. Populations from La Partida and Danzante Islands, had the narrowest nitrogen range values, suggesting less isotopic diversity in their diets.
Importance of seabird colonies
As expected, overall insectivorous lizards from islands with seabird colonies showed less negative δ13C and higher δ15N values compared with insectivorous lizards from islands without seabird colonies (Fig 3). Lizards from islands with seabird colonies occupied smaller areas in the isotopic space (smaller TA and SEABc), and had narrower carbon range (CR values) (Table 4). The NR was quite similar and also MNND, indicating the same dispersion in the isotopic space and from the centroid (CD). Ellipse overlap analysis revealed that the two groups shared 50.33% of the isotopic space, suggesting considerable overlap in dietary sources.
Red triangles represent the population of lizards living in islands with presence of significant seabird colonies and black circles represent populations living on islands without significant seabird colonies.
Herbivorous lizards
We analyzed 44 tail-tip samples from iguanas of the genera Sauromalus, Ctenosaura, and Dipsosaurus (Table 1). We did not find an effect of aridity, the presence of seabird colonies or islands size on the isotopic variation of the tail tissues on the herbivorous lizards either in C or N (Table 5). The correlation between the variables was similar in both models C and N (aridity/size correlation 0.16, 0.23; sea birds presence/aridity correlation −0.15, −0.10 and seabirds presence/size correlation 0.13, 0.14).
Although for herbivorous lizards we did not detect an effect of the aridity on the whole, we noticed some differences between populations. For instance, it seems more a prevalence of CAM/C4 plants in the diet Sauromalus from Mejia Island (δ13C average −19.2 ‰), and Ctenosaura and Sauromalus iguanas from arid San Esteban Island`s (with δ13C average of −16.76, and −17.1‰), compared to a diet more towards C3 plants on iguanas from less arid Coronados Island’s, Dipsosarus and Sauromalus (δ13C average of −23.70 and −21‰ respectively) or Espiritu Santo Sauromalus (δ13C average of −21.23‰). Individual Sauromalus iguanas from Mejia and San Esteban should have more variation in their diets because they showed broader carbon range values (CR) than Sauromalus from Coronados (Table 6).
There are two Dipsosaurus populations with less negative values of δ13C from less arid islands. One is the population from the inlet, la Islita, very close to Coronados, (δ13C values −17.1 ‰) and with the same aridity index but almost barren. They were probably feeding on the few Cactaceae (CAM/C4 plants) present there. The other, is a single individual of D. catalinensis endemic to Santa Catalina Island. Its tissues had levels δ13C corresponding also to a diet based on C4/CAM plants (−14.59‰).
Our results also highlight the importance of the sea birds’ colonies for the iguanas to be able to incorporate marine nutrients into their tissues. For example, la Islita was the only island sampled for herbivores with a large sea bird colony, in this case of yellow-footed seagull (L. livens), and some nests of blue heron A. herodias [60]. Dipsosaurus there had very high levels of δ15N (average = 30.4‰). We found also strong marine influence on the diet of Mejia Island’s Sauromalus individuals (δ15N average = 31.55‰). Here our results are probably due to the fishermen activity on the shores of this island. On the other side Sauromalus from Espiritu Santo, with no marine influence had lower δ15N levels (average = 7.67‰).
We only collected one individual of S. hispidus from Angel de la Guarda Island, found perched on a Pachycormus discolor tree (C3 plant). Its δ13C and δ15N values were closer to those of the iguanas from the southern islands. Angel de la Guarda is a massive island with scarce vegetation; its aridity index is higher than the southern islands, and lower than the smaller islands on the north, but this value has in any event to be treated with care because it was only one individual feeding on a C3 plant.
The isotope niche metrics indicated that the Dipsosaurus dorsalis population from La Islita Island had a diet with minimal isotopic variation, exhibiting the narrowest carbon (CR) and nitrogen range (NR) values of all the iguanas along with small distance to centroide and individuals packed on the isotopic space (Table 6).
S. hispidus from Mejia had narrower NR than S. varius from San Esteban and both less broad than S. slevini from Coronados Island in the south. Also, the individuals from Coronados and San Esteban, were more disperse on the isotopic space than Sauromalus from Mejia (Table 6). The small CR in Coronados Sauromalus along with its lower δ15N values suggest a diet more focused on C3 plants.
Isotopic niche of insectivorous vs herbivorous lizards
Insectivorous and herbivorous lizards share a wide (0.694) overlap in isotopic niches (Fig 5). Insectivorous lizards displayed less negative values for C and higher values for N, consistent with their higher position in the trophic web.
The color pattern of each island corresponds to the latitudinal gradient shown in Fig 1. Circles represent species of the Sauromalus genus, while triangles represent Dipsosaurus dorsalis.
Insectivorous lizards are denoted by red squares and herbivorous lizards by green triangles.
Analysis of isotopic niche metrics revealed that insectivorous lizards had a carbon range value almost twice that of herbivorous lizards. The NR was similar but herbivorous lizards, had a larger TA and Standard Ellipse Area. This larger ellipse resulted from the two groups with different nitrogen values from islands with and without seabird colonies (Fig 4). Both groups exhibited similar diversity and packing metrics (Table 7).
Discussion
Since the pioneering studies conducted by the Polis group in the 1900s, the importance of allochthonous subsidies to the arid islands of the northern part of the Gulf of California has been well documented, particularly for insect, spider, and rodent populations [5–8]. Posterior research has further confirmed that insectivorous lizard populations, as well as cardon forests and other vegetation, also rely heavily on these marine subsidies, especially those derived from guano deposits [10,12,17]. The primary objective of our study was to assess whether the importance of the marine subsidies extends to all the islands, including those less arid in the southern region, and to evaluate their impact on herbivores lizards as well. Our first result was that insectivorous lizards from all the sampled islands were able to incorporate marine-derived nutrients into their diets.
The δ13C variation in each population was significantly associated with the degree of aridity of the islands where they live. The carbon (δ 13C) values were less negative on the northern (more arid) islands and overall, the δ13C values recorded for Uta lizards in this study (−11.78 to −20.00‰) are similar to those reported for the same species on the northern Gulf of California islands (−13.09 to −18.99‰) [10]. Both values are consistent with a diet based on insects feeding on C4/ CAM plants. When insectivorous lizards are consuming insects that feed on Cactaceae or other C4/ CAM metabolism plants, and because the low TFD, their tissues will reflect the C signature of the insects and the plant [23,61]. That could mean that the aridity gradient on δ 13C values is reflecting a prevalence of this type of vegetation towards the northern islands. But it is interesting that the δ13C values in our study remain less negative than those found for Uta stansburiana in the Chihuahuan Desert (−19 to −22), a highly arid region at a similar latitude but subject to entirely continental conditions [40]. Also, lizards from Atacama Desert, in the southern hemisphere, lizards from Namibia Desert, or insectivorous skins from Australian desert have more negative δ13C values that our insular Uta lizards although they feed on C4/CAM plants [62–64]. We might then suppose it must be additional marine elements in the diet of the insular lizards besides the prevalence of C4/CAM plants. It has been demonstrated on the Upper Gulf islands, that Uta lizards are significantly more abundant on the shorelines of the islands than in the interior, regardless the size of the island or if the islands have sea birds’ colonies or not [10]. The coastal fringe can support higher numbers of lizards because it has more food coming from the sea (insects, amphipods or crustaceans feeding on algae or in stranded carrion, like in Rasa Island where Uta feeding grounds are the drying sand flats at low tide, obs. pers). The authors report that aprox 40% of the coastal Uta lizards’ food contains arthropods who have been feeding on algae [10]. This is remarkable, because our lizards came precisely from the coast of the islands, and that may be the additional element for our samples to have less negative δ13C than others in continental deserts. In other island lizards, from temperate regions like Azores [65] or in coastal areas like South Puget Sound on the Pacific Coast of North America, [66] it has been probed that there is indeed an influence of marine nutrients in lizards diets on the shore that decrease towards lizards living inside the island or the forest. This was evident on the Uta numbers registered by [10] on the very arid and very poor productive northern islands of the sea of Cortes, but only in terms of abundance. They were more than four times abundant on the coast in the islands with sea bird colonies and until nine more times abundant in islands without sea bird colonies. But it will be interesting to test it in terms of isotopic δ13C and δ15N values.
The range of δ13C was slightly broader on the arid islands of the north, and was narrower on lizards from sea bird islands. It was minimum on the southern island of Espiritu Santo (CR = 0.2). On Salsipuedes, an arid northern island without seabirds, we found the population spread out in the isotopic space with wide ranges or C and N (Table 3). It could reflect some individuals feeding on the insects living of shore debris, and others feeding on insects feeding on plants.
The δ15N in insectivorous as expected, was significantly higher on populations close to seabird colonies, despite the aridity/latitude or the size of the island. Previous studies have highlighted the importance of seabirds in incorporating marine nutrients into terrestrial food webs, primarily through guano which enriches the soil with nitrogen [10]. Studies of seabird-island soils report δ 15N values ranging from 28.26 to 35.64‰ [12,17,18,36]. This nitrogen enrichment enhances plant productivity and rises up the food web, supporting populations of animals consuming detritus, plants, and seeds, [17,18,29,31]. Additionally, seabird colonies themselves provide a good habitat for arthropods and other scavengers feeding on seabird by-products, such as faeces, feathers, eggs, and carcasses, all of which insectivorous lizards may consume [6,10,16,29,67]. Although we could not distinguish between these two sources, our results strongly support the importance of seabird colonies as a primary marine nutrient source for arthropod populations [4,10,16] and insectivorous lizards along the entire range of the Gulf islands (S2 Table, S1 Fig), mainly regarding nitrogen isotopes. Areas near seabird colonies may act as nutrient-rich hotspots, offering a higher availability of insects [24], which likely leads to more generalized lizard diets, as observed in Uta palmeri from San Pedro Mártir Island [2]. We have commonly observed insectivorous lizards (e.g., Uta, Urosaurus, or Aspidoscelis) around the nests of terns, seagulls, boobies, or brown pelicans, even outside the birds’ breeding season. This may be because these nests, even when empty, offer shade and protection. Another example is U. stansburiana lizards on Las Galeras Island, they have year-round access to guano-derived nutrients, which results in high δ15N values.
The nitrogen range on the tissues of our insectivorous lizard samples (10.68 to 38.22‰) exceeds those reported previously for the northern islands [10], probably because our study included samples from southern islands as well, where some arthropods might feed on plants growing on less subsidized ground, although lizards from islands with or without sea bird colonies shared 50% of the isotopic space, meaning that the marine nutrients are present in both south and northern islands.
So, the presence of seabird`s colonies and the aridity index, which correlates with the south-north latitudinal gradient, were the two factors contributing to the presence of marine nutrients in the tissues of coastal Uta stansburiana lizards, and not the size of the islands along the Gulf of California.
Rainfall on these islands is generally scarce, with some years experiencing no rain at all. When rainfall does occur, it is typically associated with late summer (August-October) Pacific hurricanes in the southern and central Gulf or with cooler months (November- February) on the Upper Gulf islands [19,45]. However, these patterns can vary during El Niño/La Niña events. Although neither the frequency nor the intensity of hurricanes is clearly associated with El Niño/La Niña, El Niño years tend to show a mild positive rainfall anomaly along the southern Gulf coast of the Baja California Peninsula [68]. In the northern islands, during dry years, arthropod composition primarily relies on kelp, carrion, and parasitic flies [69] with presumably δ 13 C values less negative and δ 15N high values. After rainfall, there is a pulse of C4 plant production and seasonal growth of C3 plants [40], leading to an increase in herbivorous arthropods that consume both C3 and C4 plants [7] (more negative δ 13 C values). Rainfall also mobilizes nutrients and increases guano availability, making nitrogen (15N) more available.
During El Niño events, however, rising sea surface temperatures deplete the surface waters of plankton and fish. As a result, seabird breeding colonies typically decline, or may not occur at all on certain islands in those years [55,70]. Our data partially support this pattern as Uta samples from El Niño years had lower δ 15N values, but no differences in δ 13C values. Additionally, alongside this complex scenario, failures in nesting on traditional rookeries have been linked to global warming and overfishing in the Gulf [55–58]. Given these uncertainties, within the scope of this study we could not make predictions regarding El Niño/La Niña events. We focused instead on the aridity index, which accounts for total annual precipitation over long periods including both El Niño and La Niña years.
For herbivorous lizards any of the tested variables had significant effect on the isotopic variation. The δ13C values recorded for iguanas in this study (−16.76 to −23.70‰) were more negative that in insectivorous while δ 15N values (2.01 to 31.55‰), were not very different. While the importance of marine subsidies for herbivores on these islands has not been previously studied, the diet of giant Sauromalus (S. varius and S. hipidus) was studied on 1988 in several islands, including Mejia and San Esteban [71]. According to this study the chuckwallas are quite selective, choosing only 24% of the flora species of the islands, preferring shrubs as a food-base through the year when the annuals are not available, and choosing very actively forbs when appeared; cactus representing only 7% of their diet. In total they feed on 42 species of plants from 25 families. S. hispidus in Mejia (δ13C values −19.2‰), chooses ten species, it prefers flowers and leaves of Perytile emoryi, a forb with C3 metabolism, when available in the summer, and Amaranthus palmeri (C4) (leaves and seeds) in autumn and spring; The only registered Cactaceae (C4) was Opuntia fulgida in the autumn. The diet of S. varius endemic to San Esteban (δ13C values −17.1) included 22 species from 12 families, the majority of them C3, although cactus (C4) fruits and flowers represented 13%. On iguanas from these northern arid islands CR is wider (and more negative δ13C values), that on less arid southern Coronados or Espiritu Santo, these results suggest that they might prefer C3 plants when available, because generally C3 plants are more nutritive and easier to digest than C4/CAM, [40]. But we consider the results of this study only a first approach because there are many factors that could be important in the isotopic values, i.e., in a recent study in land iguanas on Galapagos [61] authors find isotopic niche differences between sympatric species and sexes due to their choice of food, mediated by their body size, and the productivity (NDVI) of their microhabitat.
The presence of significant seabird colonies directly increases nitrogen values in the soil, which are then reflected in the δ15N values of the plants and on ultimacy on the iguanas’ tissues (S1 Table, S2 Fig). Old, mineralized guano likely serves as a primary agent fertilizing the soil and plants, enriching isotopic signatures across the ecosystem [17,18,72,73], C3 and C4 plants on bird islands had significantly greater δ15N values than plants with the same photosynthetic pathway in both coastal and inland habitats [10]. Additionally, in the northern islands, characterized by extreme aridity, previous studies have shown that allochthonous nutrients support primary productivity and plant growth rates [5,8,17,18,74]. Thus, even in areas with sparse vegetation, the plants consumed by iguanas are likely to be enriched with marine nutrients, particularly nitrogen, this point has been demonstrated in Caribbean iguanas. There subsidized island support more abundant populations and also of bigger size animals [75]. The populations from southern islands with no seabird colonies showed lower δ15N values. The only island where we sampled iguanas and hosted an important sea bird colony is La Islita. There Dipsosaurus dorsalis was very abundant and its diet exhibited high δ15N values, the lowest packing metric values, and values of δ13C around −17‰, consistent with CAM metabolism of the Cactaceae living on the island. S hispidus from Mejia had also unexpectedly high δ15N values (31.55‰), much higher than those at the top of the food chain in Baja California sharks, where δ15N values range from +12.3‰ to +18 ‰ [76] and are comparable to la Islita's Dipsosaurus. Despite Mejia is not hosting big seabird colonies, organic matter mineralization on the island may be causing 15N enrichment in plants. Several factors may be behind this mineralization as fishermen activity leaving carcass on the shore (pers. observation), or other elements like, i.e., ocean spray [77].
The lack of island size effect on the isotopic values of lizards was surprising, given the range of island sizes in our study. Small islands have larger coastline perimeters, offering more shoreline area accessible for lizards, and some studies have suggested that ocean spray might influence terrestrial nutrients, and lizards from coastal areas had significantly greater δ15N values relative to populations in unsubsidized areas [10]. However, our sampling design, which collected samples approximately 100–200 m from the shore, may have overlooked the effect of island size. The Subsidized Island Biogeography Hypothesis [21] and other studies suggest that size can affect the impact of marine subsidy effects on animal populations, increasing species richness [21,78], population density [16,79] population abundance [10], and nitrogen enrichment [14]. Future studies with more precise sampling designs along transects from the coastline to the interior of different islands would provide better insights into the relationship between island size and marine subsidies in all lizard diets.
Finally, we expected a larger difference in isotopic values between insectivorous and herbivorous lizards and higher δ 15N values in insectivorous lizards. However, despite their distinct trophic positions, both groups shared a significant portion (almost 70%) of the isotopic space across the sampled islands. Both lizard groups showed relatively low variation in carbon isotopes, with less variation observed in iguanas, but they showed greater variation in nitrogen isotopes. This variation is likely to be due to differences in nitrogen sources between islands with and without significant seabird colonies (Figs 3 and 4) regardless of aridity.
This suggests that both lizard groups incorporate marine subsidies into their diets to a substantial degree. These findings are consistent with Obrist’s study [14], which emphasizes that the primary mechanism for marine nutrient transfer within island food webs is plant fertilization, rather than direct consumption of marine subsidies.
Conclusion
Our hypothesis was that the size of the island, its degree of aridity or the presence of seabird colonies will be related to the amount of the marine food available for the lizards.
Overall, our study provides evidence for the role played by marine subsidies in the diets of both insectivorous and herbivorous lizards across the islands in the Gulf of California. We found higher nitrogen values and less negative carbon values in lizards inhabiting islands with significant seabird colonies and with hyper-arid conditions, regardless of the lizards’ foraging strategies. The ubiquity of seabird colonies combined with higher aridity in the northern part of the Gulf, creates a northward gradient in the importance of marine subsidies for both insectivorous and herbivorous lizards, across the Gulf islands as a whole.
We could not find a relationship with the size of the islands, but we suspect the design of our sampling was not adequate for it. Future research could focus on more detailed sampling along coastal-inland transects to better understand the spatial distribution of marine subsidies on islands of varying sizes. Additional isotopic analysis of plants and arthropods could provide a more comprehensive view of the nutrient flow within these island ecosystems.
Supporting information
S1 Fig. Isotopic values of insectivorous lizards and average isotopic data of arthropods.
δ13C and δ15N values of insectivorous lizards (Uta stansburiana) from islands of the Gulf of California. The color pattern of each island corresponds to the aridity/latitudinal gradient shown in Figure 1. Averages and standard deviations of spiders (circles), scorpions (squares), carrion insects (triangles), and seabird ectoparasites (rhombus) data from Anderson and Polis (1998) (purple), herbivore insects (downward triangles), detritivores (dodecagons), predator insects (stars), and littoral invertebrates (hexagons) data from Stapp and Polis (2003) (pink), arthropods (crosses) data Barrett et al. (2005) (orange) are shown. Empty symbols represent habitats with the presence of seabirds, filled symbols represent non-seabird habitats, and dashed-line figures represent mainland. For more details regarding arthropods species or locality, see S2 Table.
https://doi.org/10.1371/journal.pone.0329414.s001
(TIF)
S2 Fig. Isotopic values of herbivorous lizards and average isotopic data of plants.
δ13C and δ15N values of herbivorous iguanas from Mejia, San Esteban, Coronados and La Islita Islands. The color pattern of each island corresponds to the aridity/latitudinal gradient shown in Figure 1. Circles represent species of the Sauromalus genus, while squares represent Dipsosaurus dorsalis. Averages and standard deviations of C3 (circles), C4 (squares), and CAM (triangles) plants, as well as algae (rhombus) collected during our surveys (dark green), algae data from Anderson and Polis (1998) (purple), C3, C4/CAM plants, and algae data from Stapp and Polis (2003) (pink), C3, C4 plants, and algae data from Barrett et al. (2005) (orange), and C3, C4, and CAM plants data from Delibes et al. (2015) (black) are shown. Empty symbols represent habitats with the presence of seabirds, filled symbols represent non-seabird habitats, and dashed-line figures represent mainland. For more details regarding plant species or locality, see S1 Table.
https://doi.org/10.1371/journal.pone.0329414.s002
(TIF)
S1 Table. Average isotopic data of C3, C4, and CAM plants from our study and literature.
Average and standard deviation of δ13C and δ15N of C3, C4, and CAM plants, as well as marine algae collected for this study on Angel de la Guarda Island. Average and standard deviation of δ13C and δ15N of C3, C4, and CAM plants, as well as marine algae found in the literature from some islands and coastal areas of the Gulf of California, as well as the Baja California Peninsula (mainland).
https://doi.org/10.1371/journal.pone.0329414.s003
(DOCX)
S2 Table. Average isotopic data of arthropods from the literature.
Average and standard deviation of δ13C and δ15N of terrestrial and littoral arthropods found in the literature from some islands and coastal areas of the Gulf of California, as well as the Baja California Peninsula (mainland).
https://doi.org/10.1371/journal.pone.0329414.s004
(DOCX)
S3 Table. Raw isotopic data of insular lizards used in this study.
δ13C ‰ and δ15N ‰ of tail-tissues of insectivorous and herbivorous lizards from different islands of the Gulf of California. Sampling year and C:N ratios are shown per individual. In shade the sampling period that could reflect effects of El Niño event.
https://doi.org/10.1371/journal.pone.0329414.s005
(DOCX)
Acknowledgments
We extend our gratitude to the people of the Star of the Sea boat for their support over the years in the islands. The first author (IKBS) thanks the Secretaría de Ciencia, Humanidades, Tecnología e Innovación (SECIHTI-Mexico, before CONAHCYT) for the master and current doctoral scholarship. Special thanks to Rodrigo Ayala and Abelino Cota for their invaluable assistance in the field, and to M. Delibes for providing insightful comments on an earlier draft of this manuscript. Nicola Holt, reviewed the English edition. This research was carried out under SEMARNAT permits SGPA/DGVS/ −10182/11–07594 7/15–2971/20–05480/21.
References
- 1. Rosenzweig ML. Net primary productivity of terrestrial communities: prediction from climatological data. Am Nat. 1968;102(923):67–74.
- 2. Hews DK. Food resources affect female distribution and male mating opportunities in the iguanian lizard Uta palmeri. Animal Behav. 1993;46(2):279–91.
- 3. Polis GA, Hurd SD, Jackson CT, Sanchez-Piñero F. Multifactor population limitation: variable spatial and temporal control of spiders on Gulf of California islands. Ecology. 1998;79(2):490–502.
- 4. Anderson WB, Polis GA. Marine subsidies of island communities in the Gulf of California: evidence from stable carbon and nitrogen isotopes. Oikos. 1998;81(1):75.
- 5. Polis GA, Hurd SD. Linking marine and terrestrial food webs: allochthonous input from the ocean supports high secondary productivity on small islands and coastal land communities. Am Nat. 1996;147(3):396–423.
- 6. Anderson WB, Wait DA, Stapp P. Resources from another place and time: responses to pulses in a spatially subsidized system. Ecology. 2008;89(3):660–70. pmid:18459330
- 7. Polis GA, Anderson WB, Holt RD. Toward an integration of landscape and food web ecology: the dynamics of spatially subsidized food webs. Ann Rev Ecol Syst. 1997;28(1):289–316.
- 8. Spiller DA, Piovia-Scorr J, Wright AN, Yang LH, Takimoto G, Schoener TW, et al. Marine subsidies have multiple effects on coastal food webs. Ecology. 2010;91(5):1424–34. pmid:20503874
- 9. Kenny HV, Wright AN, Piovia-Scott J, Yang LH, Spiller DA, Schoener TW. Marine subsidies change short-term foraging activity and habitat utilization of terrestrial lizards. Ecol Evol. 2017;7(24):10701–9. pmid:29299250
- 10. Barrett K, Anderson WB, Wait DA, Grismer LL, Polis GA, Rose MD. Marine subsidies alter the diet and abundance of insular and coastal lizard populations. Oikos. 2005;109(1):145–53.
- 11.
Anderson WB, Wait DA. Allochthonous nutrient and food inputs: consequences for temporal stability. In: Polis GA, Power ME, Huxel GR, eds. Food webs at the landscape scale. University of Chicago Press; 2004: 82–114.
- 12. Wait DA, Aubrey DP, Anderson WB. Seabird guano influences on desert islands: soil chemistry and herbaceous species richness and productivity. J Arid Environ. 2005;60(4):681–95.
- 13.
Case TJ. Reptiles: ecology. In Cody ML, Ezcurra E, eds. A new island biogeography of the Sea of Cortés. Oxford University Press; 2002: 221–70.
- 14. Obrist DS, Hanly PJ, Brown NEM, Ernst CM, Wickham SB, Fitzpatrick OT, et al. Biogeographic features mediate marine subsidies to island food webs. Ecosphere. 2022;13(7).
- 15. Blázquez MC, Arnaud G, Ortiz-Avila V, Ortega-Rubio A, Delibes M. Stable isotope analyses suggest Mus musculus occupies the place of the “possibly extinct” Peromyscus guardia in Angel de la Guarda Island, (Mexico). Mamm Res. 2018;64(1):121–5.
- 16. Stapp P, Polis GA. Marine resources subsidize insular rodent populations in the Gulf of California, Mexico. Oecologia. 2003;134(4):496–504. pmid:12647121
- 17. Wilder BT, Becker AT, Dettman DL. Marine subsidies produce cactus forests on desert islands. Sci Rep. 2022;12(1):17110. pmid:36224217
- 18. Anderson WB, Polis GA. Nutrient fluxes from water to land: seabirds affect plant nutrient status on Gulf of California islands. Oecologia. 1999;118(3):324–32. pmid:28307276
- 19.
Murphy RW, Aguirre-León G. Non-avian reptiles: origin and evolution. In: Case TJ, Cody ML, Ezcurra E, eds. A new island biogeography of the Sea of Cortés. Oxford University Press; 2002: 181–220.
- 20. Runemark A, Sagonas K, Svensson EI. Ecological explanations to island gigantism: dietary niche divergence, predation, and size in an endemic lizard. Ecology. 2015;96(8):2077–92. pmid:26405734
- 21. Anderson WB, Wait DA. Subsidized island biogeography hypothesis: another new twist on an old theory. Ecology Letters. 2001;4(4):289–91.
- 22. Bearhop S, Adams CE, Waldron S, Fuller RA, Macleod JH. Determining trophic niche width: a novel approach using stable isotope analysis. J Anim Ecol. 2004;73(5):1007–12.
- 23. Delibes M, Blazquez MC, Fedriani JM, Granados A, Soriano L, Delgado A. Isotopic niche variation in a higher trophic level ectotherm: highlighting the role of succulent plants in desert food webs. PLoS One. 2015;10(5):e0126814. pmid:25973609
- 24. Caut S, Angulo E, Pisanu B, Ruffino L, Faulquier L, Lorvelec O, et al. Seabird modulations of isotopic nitrogen on islands. PLoS One. 2012;7(6):e39125. pmid:22723945
- 25. Kelly JF. Stable isotopes of carbon and nitrogen in the study of avian and mammalian trophic ecology. Can J Zool. 2000;78(1):1–27.
- 26. Potapov AM, Brose U, Scheu S, Tiunov AV. Trophic position of consumers and size structure of food webs across aquatic and terrestrial ecosystems. Am Nat. 2019;194(6):823–39. pmid:31738104
- 27. Post DM. Using stable isotopes to estimate trophic position: models, methods, and assumptions. Ecology. 2002;83(3):703–18.
- 28. Stephens RB, Shipley ON, Moll RJ. Meta‐analysis and critical review of trophic discrimination factors (Δ13C and Δ15N): Importance of tissue, trophic level and diet source. Functional Ecol. 2023;37(9):2535–48.
- 29. Sanchez-Pinero F, Polis GA. Bottom-up dynamics of allochthonous input: direct and indirect effects of seabirds on islands. Ecology. 2000;81(11):3117.
- 30. Mizutani H, Kabaya Y, Wada E. Ammonia volatilization and high 15N/14N ratio in a penguin rookery in Antarctica. Geochem J. 1985;19(6):323–7.
- 31. Wainright SC, Haney JC, Kerr C, Golovkin AN, Flint MV. Utilization of nitrogen derived from seabird guano by terrestrial and marine plants at St. Paul, Pribilof Islands, Bering Sea, Alaska. Marine Biol. 1998;131(1):63–71.
- 32. Schoeninger MJ, DeNiro MJ. Nitrogen and carbon isotopic composition of bone collagen from marine and terrestrial animals. Geochimica et Cosmochimica Acta. 1984;48(4):625–39.
- 33. Peterson BJ, Fry B. Stable isotopes in ecosystem studies. Annu Rev Ecol Syst. 1987;18:293–320.
- 34. Lapiedra O, Morales N, Yang LH, Fernández-Bellon D, Michaelides SN, Giery ST, et al. Predator-driven behavioural shifts in a common lizard shape resource-flow from marine to terrestrial ecosystems. Ecol Lett. 2024;27(1):e14335. pmid:37972585
- 35. Newsome SD, Clementz MT, Koch PL. Using stable isotope biogeochemistry to study marine mammal ecology. Marine Mammal Sci. 2010.
- 36. Stapp P, Polis GA, Sánchez Piñero F. Stable isotopes reveal strong marine and El Niño effects on island food webs. Nature. 1999;401(6752):467–9.
- 37. Lattanzio M, Miles D. Stable carbon and nitrogen isotope discrimination and turnover in a small-bodied insectivorous lizard. Isotopes Environ Health Stud. 2016;52(6):673–81. pmid:26999652
- 38.
Cody ML, Rebman J, Moran R, Thompson HJ. Plants. In: Case TJ, Cody ML, Ezcurra E, eds. A new island biogeography of the Sea of Cortés. Oxford University Press; 2002: 63–108.
- 39. Drennan PM, Nobel PS. Responses of CAM species to increasing atmospheric CO2 concentrations. Plant Cell Environ. 2000;23(8):767–81.
- 40. Warne RW, Pershall AD, Wolf BO. Linking precipitation and C3-C4 plant production to resource dynamics in higher-trophic-level consumers. Ecology. 2010;91(6):1628–38. doi: https://doi.org/10.1890/08-1471.1 pmid:20583705
- 41.
QGIS Development Team. QGIS Geographic Information System. 2020. http://qgis.org
- 42.
Blázquez MC, Vázquez P, Ortega-Rubio A. Status of the phylogeography, taxonomy and conservation of the reptiles of the Gulf of California Islands. In: Ortega A, ed. Mexican natural resources management and biodiversity conservation. Springer International Publishing; 2018: 285–304. doi: https://doi.org/10.1007/978-3-319-90584-6_13
- 43.
Grismer LL. Amphibians and reptiles of Baja California, including its Pacific islands and the islands in the Sea of Cortés. University of California Press; 2002.
- 44.
Soto-Jimenez MF, Velázquez-Ochoa R, Izaguirre MJ. Analysis of the variation of stable carbon isotopes in macroalgae communities from shallow marine habitats in the Gulf of California ecoregion. Authorea Preprints. 2022.
- 45.
National Oceanic and Atmospheric Administration (NOAA). Oceanic Niño Index (ONI) [Internet]. https://origin.cpc.ncep.noaa.gov/products/analysis_monitoring/ensostuff/ONI_v5.php
- 46. Lin Z-H, Ji X. Partial tail loss has no severe effects on energy stores and locomotor performance in a lacertid lizard, Takydromus septentrionalis. J Comp Physiol B. 2005;175(8):567–73. pmid:16133493
- 47. Post DM, Layman CA, Arrington DA, Takimoto G, Quattrochi J, Montaña CG. Getting to the fat of the matter: models, methods and assumptions for dealing with lipids in stable isotope analyses. Oecologia. 2007;152(1):179–89. pmid:17225157
- 48. Jackson AL, Inger R, Parnell AC, Bearhop S. Comparing isotopic niche widths among and within communities: SIBER - Stable Isotope Bayesian Ellipses in R. J Anim Ecol. 2011;80(3):595–602. pmid:21401589
- 49.
R Core Team. R: A language and environment for statistical computing. Vienna, Austria: R Foundation for Statistical Computing; 2022.
- 50. Layman CA, Arrington DA, Montaña CG, Post DM. Can stable isotope ratios provide for community-wide measures of trophic structure? Ecology. 2007;88(1):42–8. pmid:17489452
- 51.
Conjunto de datos del Territorio Insular Mexicano. México: Instituto Nacional de Estadística y Geografía; 2013.
- 52. Fick SE, Hijmans RJ. WorldClim 2: new 1‐km spatial resolution climate surfaces for global land areas. Intl J Climatol. 2017;37(12):4302–15.
- 53.
Köppen WP. Die Klimate der Erde: Grundriss der Klimakunde. Walter de Gruyter & Company; 1923.
- 54. Quan C, Han S, Utescher T, Zhang C, Liu YS. Validation of temperature–precipitation-based aridity index: paleoclimatic implications. Palaeogeogr Palaeoclimatol Palaeoecol. 2013;386:86–95.
- 55. Bowen T, Velarde E, Anderson DW, Marlett SA. Federico Craveri and changes in nesting seabirds on Isla Rasa, Gulf of California, since 1856. Southwestern Nat. 2015:1–5.
- 56. Velarde E, Ezcurra E, Cisneros-Mata MA, Lavín MF. Seabird ecology, El Niño anomalies, and prediction of sardine fisheries in the Gulf of California. Ecol Appl. 2004;14(1):607–15.
- 57. Velarde E, Ezcurra E, Horn MH, Patton RT. Warm oceanographic anomalies and fishing pressure drive seabird nesting north. Sci Adv. 2015;1(5):e1400210. pmid:26601193
- 58. Anderson DW, Godínez-Reyes CR, Velarde E, Avalos-Tellez R, Ramírez-Delgado D, Moreno-Prado H, et al. Brown Pelicans, Pelecanus occidentalis californicus (Aves: Pelecanidae): Five decades with ENSO, dynamic nesting, and contemporary breeding status in the Gulf of California. Cienc Mar. 2017;43(1):1–34.
- 59.
Pinheiro J, Bates D, R Core Team. nlme: linear and nonlinear mixed effects models. 2025.
- 60.
Huerta-Hernández V. Descripción de las aves en islotes del Parque Nacional Bahía de Loreto, Baja California Sur. Zacatecas, México: Universidad Autónoma de Zacatecas “Francisco García Salinas”; 2018.
- 61. Gargano M, Colosimo G, Gratton P, Marta S, Brilli M, Giustini F, et al. Nitrogen and carbon stable isotope analysis sheds light on trophic competition between two syntopic land iguana species from Galápagos. Sci Rep. 2022;12(1):16897. pmid:36207376
- 62. Lobos G, Tapia G, Alzamora A, Rojas O. Distribución, densidad y nicho isotópico en reptiles y mamíferos del desierto absoluto de Atacama; con registro de saurofagia entre reptiles. Gayana (Concepc). 2020;84(2):118–28.
- 63. Murray IW, Lease HM, Hetem RS, Mitchell D, Fuller A, Woodborne S. Stable isotope analysis of diet confirms niche separation of two sympatric species of Namib Desert lizard. Integr Zool. 2016;11(1):60–75. pmid:26817923
- 64. Grundler MR, Pianka ER, Pelegrin N, Cowan MA, Rabosky DL. Stable isotope ecology of a hyper-diverse community of scincid lizards from arid Australia. PLoS One. 2017;12(2):e0172879. pmid:28245270
- 65. Neves V, Rund D, Pinho CJ, Vasconcelos R, Bustamante P, Quillfeldt P. Diet of the exotic Madeiran wall lizard: first insights into trophic interactions in an Atlantic seabird sanctuary. Herpetozoa. 2022;35:107–13.
- 66. Ebersole A, Bunker ME, Weiss SL, Fox-Dobbs K. Inter- and intrapopulation resource use variation of marine subsidized western fence lizards. Oecologia. 2024;204(1):1–11. pmid:38244058
- 67. Markwell TJ, Daugherty CH. Invertebrate and lizard abundance is greater on seabird-inhabited islands than on seabird-free islands in the Marlborough Sounds, New Zealand. Ecoscience. 2002;9(3):293–9.
- 68.
Osorio Ayala FL. Evaluación de los efectos del ENSO sobre las lluvias de Baja California Sur, con énfasis en ciudades costeras y cuencas hidrológicas. Centro Investigaciones Biológicas del Noroeste (CIBNOR); 2015.
- 69. Wright AN, Yang LH, Piovia-Scott J, Spiller DA, Schoener TW. Consumer responses to experimental pulsed subsidies in isolated versus connected habitats. Am Nat. 2020;196(3):369–81. pmid:32813995
- 70. Velarde E, Ezcurra E. Are seabirds’ life history traits maladaptive under present oceanographic variability? The case of Heermann’s Gull (Larus heermanni). Condor. 2018;120(2):388–401.
- 71. Sylber CK. Feeding habits of the lizards Sauromalus varius and S. hispidus in the Gulf of California. J Herpetol. 1988;22(4):413.
- 72. Mizutani H, Wada E. Nitrogen and carbon isotope ratios in seabird rookeries and their ecological implications. Ecology. 1988;69(2):340–9.
- 73. Menegotto A, Rangel TF, Schrader J, Weigelt P, Kreft H. A global test of the subsidized island biogeography hypothesis. Glob Ecol Biogeogr. 2019;29(2):320–30.
- 74. Ellis JC. Marine birds on land: a review of plant biomass, species richness, and community composition in seabird colonies. Plant Ecol. 2005;181(2):227–41.
- 75. Richardson KM, Iverson JB, Kurle CM. Marine subsidies likely cause gigantism of iguanas in the Bahamas. Oecologia. 2019;189(4):1005–15. doi: https://doi.org/10.1007/s00442-019-04366-4 pmid:30850885
- 76. Sánchez-Latorre C, Galván-Magaña F, Elorriaga-Verplancken FR, Tripp-Valdez A, González-Armas R, Piñón-Gimate A, et al. Trophic ecology during the ontogenetic development of the Pelagic Thresher Shark Alopias pelagicus in Baja California Sur, Mexico. Diversity. 2023;15(10):1057.
- 77.
Smith V, Froneman PW. Nutrient dynamics in the vicinity of the Prince Edward Islands. In: Chown Sl, Froneman PW, eds. The prince edward islands: land-sea interactions in a changing ecosystem. SUN MeDIA; 2008: 165–79. doi: https://doi.org/10.18820/9781928357063/07
- 78. Barrett K, Wait DA, Anderson WB. Small island biogeography in the Gulf of California: lizards, the subsidized island biogeography hypothesis, and the small island effect. J Biogeogr. 2003;30(10):1575–81.
- 79. Polis GA, Hurd SD. Extraordinarily high spider densities on islands: flow of energy from the marine to terrestrial food webs and the absence of predation. Proc Natl Acad Sci U S A. 1995;92(10):4382–6. pmid:7753815