- Email: [email protected]
Stable isotope evidence for Turkey Vulture reliance on food subsidies from the sea
Ecological Indicators 63 (2016) 332–336
Contents lists available at ScienceDirect
Ecological Indicators journal homepage: www.elsevier.com/locate/ecolind
Short Communication
Stable isotope evidence for Turkey Vulture reliance on food subsidies from the sea Ma Carmen Blázquez a,∗ , Miguel Delibes-Mateos b,c , J. Mario Vargas d , Arsenio Granados e , Antonio Delgado e , Miguel Delibes f a
Centro Investigaciones Biológicas Noroeste, Avda. Politécnico Nacional 195, 23096 La Paz, B.C.S., Mexico CIBIO/InBIO, Universidade do Porto, Campus de Vairão, 4485-661 Vairão, Portugal c Instituto de Estudios Sociales Avanzados (IESA-CSIC), Campo Santo de los Mártires 7, 14004 Córdoba, Spain d Department of Biología Animal, Facultad de Ciencias, Universidad de Málaga, 29071 Málaga, Spain e Instituto Andaluz de Ciencias de la Tierra, CSIC-UGR, Avda. de las Palmeras 4, 18100 Armilla, Granada, Spain f Department of Conservation Biology, Estación Biológica de Do˜ nana, CSIC, Avda. Américo Vespucio s/n., 41092 Seville, Spain b
a r t i c l e
i n f o
Article history: Received 27 October 2015 Received in revised form 11 December 2015 Accepted 13 December 2015 Keywords: Baja California Cathartes aura Isotopic niche Marine subsidies Stranded carcasses
a b s t r a c t Turkey Vulture (Cathartes aura) reliance on marine subsidies in coastal Baja California peninsula was quantitatively assessed by analyzing carbon and nitrogen stable isotope ratios in its feathers. Feathers were collected in two separate roosts in a small farm, a small fishing village and an uninhabited beach. We compared among them the isotopic niches of the four populations and also with those of Yellowfooted Seagull (Larus livens), Brown Pelican (Pelecanus occidentalis) and Orange-throated Whiptail lizard (Aspidoscelis hyperythra), used as reference for sympatric marine and terrestrial species. The importance of nutrients of marine origin varied among local close subpopulations, suggesting some spatial segregation. Dominant individuals would be established near predictable sources of food (human settlements), having a mixed terrestrial–marine diet influenced by local human activities (isotopic signature of feathers also indicated the role of human-fed cattle as vulture food). Subordinate individuals would be relegated to wandering along the beaches searching for washed up food, having a diet almost exclusively marine. © 2015 Elsevier Ltd. All rights reserved.
1. Introduction Contiguous ecosystems exchange nutrients, energy and organisms, usually referred to as resource subsidies. These subsidies can substantially influence population dynamics, interactions, trophic pathways and other aspects of the recipient food webs (Polis et al., 1997). Often it is assumed that the roles of ecosystem crossing resources vary in function of their productivity, more productive systems being mainly donors and poorer ones being recipients. The Gulf of California with its islands and surrounding lands makes a good example of this resources asymmetry, as very low terrestrial productivity contrasts with the highly productive sea (Maulf, 1983). Probably because of this, the area has been scenario of several pioneering studies showing the effects of marine subsidies on terrestrial consumers at species (e.g. Coyote, Canis latrans; Rose and Polis, 1998), guild (e.g. spiders; Polis and Hurd, 1995) and community levels (e.g. algae, arthropods and lizards; Barrett et al., 2005).
∗ Corresponding author. Tel.: +52 6121238441. E-mail address: [email protected] (M.C. Blázquez). http://dx.doi.org/10.1016/j.ecolind.2015.12.015 1470-160X/© 2015 Elsevier Ltd. All rights reserved.
To the best of our knowledge, the use of marine subsidies by terrestrial bird species has been scarcely assessed anywhere in the world, with some exceptions (e.g. Hobson and Sealy, 1991). The Turkey Vulture (Cathartes aura) is the most widespread of all Neotropical vultures, ranging from south Canada to Tierra del Fuego in Chile and Argentina. Its diet includes dung and refuse, some fruits, small animals actively hunted and mainly carrion, which it can locate through olfaction (Houston, 1994). We suspect marine food is important in the diet of Turkey Vultures living by the coast in subtropical Baja California peninsula, as individuals eating from discarded remains near fishermen’s camps or from stranded carcasses at the beach are frequently detected (Fig. S1.B and C). However, this prediction has not been evaluated until now. We will prove that stable isotope ratios of carbon (13 C/12 C) and nitrogen (15 N/14 N) in Turkey Vulture feathers can indicate the quantitative importance for the species of marine resources at four sites of Baja California (Mexico). Supplementary Fig. S1 can be found, in the online version, at http://dx.doi.org/10.1016/j.ecolind.2015.12.015. The isotopic composition of body tissues reflects the materials used to build them. Classical pioneering studies proved that marine
M.C. Blázquez et al. / Ecological Indicators 63 (2016) 332–336
resources are enriched in heavier nitrogen and in heavier carbon (when terrestrial C3 biomass is dominant), which allows using carbon and nitrogen stable isotopes for dietary analyses focusing on the relative importance of terrestrial and marine food sources (Schoeninger and De Niro, 1984). Also, differences in the role of some kinds of terrestrial resources, including human-fed livestock, could be detected, because plants using different photosynthetic metabolic ways (C3 , C4 and Crassulacean Acid Metabolism, CAM) generate distinct ı13 C signatures (Bender, 1971). As feathers are metabolically inert tissue, their isotopic values indicate what the bird consumed at the time the feather was growing (Inger and Bearhop, 2008). Turkey Vulture feathers grown while its owner was consuming marine food should be enriched in heavier nitrogen and (in C3 based food-webs) heavier carbon, having rather similar isotopic signatures to feathers of sympatric marine birds. On the other hand, feathers grown when the bird was consuming mainly terrestrial foods should be depleted in heavier nitrogen and (in a lesser degree) carbon, their isotopic signatures resembling those of tissues of sympatric high-level trophic terrestrial consumers. We expect a mixed terrestrial-marine diet for coastal Turkey Vulture residents in Baja California. To test this prediction we compared the isotopic niche of Turkey Vulture with those of two typically marine birds, the Yellow-footed Seagull (Larus livens) and the Brown Pelican (Pelecanus occidentalis), and a terrestrial highlevel trophic consumer, the arthropodivorous Orange-throated Whiptail (Aspidoscelis hyperythra). Additionally, we also predict a reduced intrapopulation variation in the Turkey Vulture isotopic niche, as it is a mobile bird and our sampling sites were nearby. 2. Materials and methods 2.1. Study area Baja California peninsula is a volcanic fringe of land at the Western side of North America, running from north-west to south-east 1300 km long and, on average, about 100 km wide. Our study area at the Gulf of California coast, characterized by soft hills, dry sandy pebbly riverbeds, and scattered oasis with palm trees, is arid and hot, with uncertain precipitations from August to October, and practically without rain in other months of the year. The Turkey Vulture is the most abundant raptor species in southern Baja California, especially near villages, in agricultural areas and by the coast. Feathers were collected on October 2011, before the arrival to the area of potential wintering individuals, at three localities (and four sites) on the Gulf coast of southern Baja California. From north to south, these were: (A) Los Dolores (25◦ 4 34 N, 110◦ 51 32 W): A palm oasis, with a traditional cattle farm (about 400 cows and goats), owned by one family. Some feathers (n = 11) were taken under a vulture roost on high palms (Washingtonia robusta, Phoenix dactylifera) by the beach (site Dolores 1). More feathers (n = 33) were taken under another roost on giant cacti (Cardon, Pachycereus pringlei), about 1 km inland, by an open-air abattoir (site Dolores 2) (see Fig. S1.E). (B) San Evaristo (24◦ 54 25 N, 110◦ 42 14 W): A small fishermen’s village (about 80 inhabitants), 27 km south of Los Dolores. Feathers (n = 14) were collected under a metal lighthouse where vultures roost at night. (C) Punta Arenas (24◦ 53 17 N, 110◦ 41 28 W): An uninhabited beach with sand dunes, 5 km south of San Evaristo. Feathers (n = 12) were collected around a marine turtle carcass that was being eaten by several Turkey Vultures.
333
Seagull and pelican feathers (n = 17 and 23, respectively) were also collected on October 2011 at distinct communal roosting places in San Evaristo and Nopoló (24◦ 59 49 N, 110◦ 45 32 W). For comparison, we used isotopic data of tail tissue of whiptail lizards (n = 13) live-captured in 2009 at Presa de Ihuazil (24◦ 56 49 N, 111◦ 24 25 W; for details, see Delibes et al., 2015). This location is at the same latitude as A, B and C but 52 km inland. 2.2. Sample collection and analyses We collected equally downy, small and large contour feathers. From large feathers, we cut a transversal fringe of about 1 cm of the tail tip, in order to select a fraction grown in a few days, removing potential within-feather variation (Grecian et al., 2015). Before analysis, feathers were cleaned of surface contaminants using warm water (50 ◦ C) in an ultrasonic cleaner for 5 min and dried at room temperature for 24 h. Isotope measurements were carried out at the Stable Isotope Laboratory of the Instituto Andaluz de Ciencias de la Tierra (CSIC-UGR, Granada, Spain), using a Carlo Elba NC1500 (Milan, Italy) elemental analyzer on line with a Delta Plus XL (ThermoQuest, Bremen, Germany) mass spectrometer (EAIRMS). Isotopic ratios of carbon and nitrogen are presented as ı values, where ı = (Rsample /Rstandard − 1) × 1000, being R = 13 C/12 C for ı13 C values, and R = 15 N/14 N for ı15 N values. Commercial CO2 and N2 were used as internal standards for C and N isotopic analyses. For C, two internal standards of −30.63‰ and −11.65‰ (Vienna Pee Dee Belemnite; VPDB) were analyzed every 10 samples. For N, two internal standards of −1.02‰ and +16.01‰ (AIR) were used. Precision calculated, after correction of the mass spectrometer daily drift from standards systematically interspersed in analytical batches, was better than ±0.1‰ for both ı13 C and ı15 N. Most results are presented through isotopic niche quantitative metrics developed by Layman et al. (2007), adapted to population level by including the ı13 C and ı15 N values of all samples in each population. We first analyzed all Turkey Vulture together in order to obtain an estimation of the overall isotopic niche of the species in the area and compare it with those of the other species. We then analyzed separately the Turkey Vulture niches at each site. Calculations were made in R using the SIAR package (Jackson et al., 2011). For each species or population we calculated: (1) Mean and low and upper 95% confidence limits of ı13 C and ı15 N. In this case, differences among means of species and populations were also analyzed through GLM-Anova tests. (2) Carbon range (CR) and nitrogen range (NR), corresponding to the distance between the two feathers (for whiptails, the two individuals) with the lowest and the highest ı13 C and ı15 N values within each population; they estimate the total carbon and nitrogen range exploited by each population and its relative position in the ı13 C–ı15 N space. (3) Total area (TA) of the convex hull encompassing all points, as a measure of population niche width. This estimator is very dependent on sample size. Because of this we also calculated: (4) Bayesian Standard Ellipse Area (SEAb), bootstrapping data (n = 10,000). Standard ellipse (SEA) contains about 40% of the points and estimates the mean core population niche, being to bivariate data as standard deviation is to univariate data (Jackson et al., 2012). SEAb allows comparisons among populations differing in sample size. Mean areas and the low and upper 95% credible limits are shown. (5) Mean distance to centroid (CD), calculated as the mean Euclidean distance of each sample of a population to the ı13 C–ı15 N centroid for that population, as an estimator of the population isotopic diversity.
334
M.C. Blázquez et al. / Ecological Indicators 63 (2016) 332–336
Table 1 Stable isotope niche metrics for the total Turkey Vulture sample (Cathartes ALL), each Turkey Vulture separate population (DOL1 = Los Dolores 1, DOL2 = Los Dolores 2, EVA = San Evaristo, PAR = Punta Arenas), Yellow-footed gull (Larus livens), Brown pelican (Pelecanus occidentalis) and Orange-throated whiptail (Aspidoscelis hyperythra). TA = total area of convex hull; SEAb = Bayesian standard ellipse area; MC = Mean ı13 C; SD = standard deviation; CR = ı13 C range; MN = mean ı15 N; NR = ı15 N range; CR = mean distance to centroid; n = bivariate sample size. Sp./population
TA
SEAb (95% limits)
MC (SD)
CR (min,max)
MN (SD)
NR (min,max)
CD
n
Cathartes ALL Cathartes DOL1 Cathartes DOL2 Cathartes EVA Cathartes PAR Larus Pelecanus Aspidoscelis
41.8 11.2 25.5 16.7 5.36 5.01 4.74 19.3
12.95 (12.91–12.98) 6.18 (6.15–6.22) 10.65 (10.62–10.70) 8.83 (8.78–8.87) 3.35 (3.33–3.37) 2.31 (2.30–2.33) 2.19 (2.18–2.20) 7.65 (7.61–7.69)
−16.11 (1.48) −17.14 (0.83) −16.34 (1.49) −16.44 (1.38) −14.54 (0.93) −14.88 (1.08) −15.07 (0.55) −17.03 (1.72)
5.75 (−18.99,−13.24) 3.15 (−18.76,−15.61) 4.94 (−18.85,−14.01) 4.24 (−18.99,−14.75) 2.82 (−16.06,−13.24) 3.35 (−16.57,−13.22) 2.08 (−16.10,−14.02) 6.29 (−20.73,−14.44)
16.17 (3.34) 15.72 (2.32) 14.58 (2.33) 16.61 (3.53) 20.69 (1.12) 21.25 (0.58) 19.92 (1.10) 12.09 (1.43)
10.80 (11.11,21.88) 6.57 (12.32,18.89) 7.59 (11.11,18.90) 9.80 (12.08,21.88) 4.16 (17.51,21.67) 2.17 (20.06,22.23) 3.78 (18.02,21.80) 4.66 (9.79,14.45)
3.26 2.14 2.50 3.44 1.18 1.06 1.11 1.92
70 11 33 14 12 17 23 13
3. Results The average values of ı13 C and ı15 N differed among species (F(3,119) = 10.17, F(3,119) = 42.73, respectively; P < 0.001). Post hoc tests showed significant differences among ı13 C values of Turkey Vulture and whiptail compared to pelican and seagull. However, in ı15 N values there were three groups: Turkey Vulture alone, whiptail alone and seagull and pelican together. As expected, the overall Turkey Vulture isotopic niche was much wider than those of seagull and pelican in all considered metrics. The niche of whiptail was intermediate in width among those of Turkey Vulture and marine birds (Table 1). The overlap
(similarity) among the core niches of the four species was quite small (but it must be taken into account that standard ellipse includes only about 40% of the points). The Turkey Vulture core niche slightly overlapped those of whiptail and pelican, which in turn slightly overlapped that of seagull (Fig. 1A). Besides niche width, the greater differences in the isotopic niche of the four species were related to the average values and the range of ı15 N (Table 1 and Fig. 1A). Mean ı15 N was lowest in the whiptail, followed by the Turkey Vulture, the pelican and the seagull. Simultaneously, NR was much greater in the Turkey Vulture than in the other species. In addition, mean ı13 C values were more negative in the whiptail, followed by Turkey Vulture, pelican and seagull. These results indicate, as expected, a terrestrial diet in the whiptail, a marine diet in the pelican and the seagull, and a diet in-between marine and terrestrial in the Turkey Vulture. Contrary to our expectations, the isotopic profiles of Turkey Vulture feathers seemed to be different among the four studied sites (for ı13 C, F(3,66) = 8.714; for ı15 N, F(3,66) = 18.18; P < 0.001 in both cases; see also Table 1 and Fig. 1B), despite they were separated less than 33 km. Post hoc tests showed significant differences among feathers of Punta Arenas and those of the other sites, both for ı13 C (P < 0.002) and ı15 N (P < 0.001) average values. Also, vultures of Punta Arenas had the smallest isotopic niche, with most of its metrics very similar to those of pelican and seagull. On the other hand, the vulture populations of Los Dolores 1, Los Dolores 2 and San Evaristo had partially overlapping, but otherwise different, isotopic niches (Fig. 1B), although their ı13 C and ı15 N means did not differ statistically. In San Evaristo, both MN and NR values were higher. In Los Dolores 1 (by the beach), ı13 C and ı15 N values were smaller. In Los Dolores 2 (by the abattoir) there were a larger proportion of feathers with simultaneously less negative values of ı13 C and low values of ı15 N. The core niche of the Turkey Vulture population of San Evaristo overlapped the other three populations, while Los Dolores 1 and Los Dolores 2 overlapped between them and Punta Arenas only overlapped San Evaristo (Fig. 1B).
4. Discussion
Fig. 1. Stable isotope standard ellipses in the ı13 C–ı15 N space of: (A) Turkey Vulture (Cathartes), Yellow-legged Seagull (Larus), Brown Pelican (Pelecanus) and Orangethroated Whiptail (Aspidoscelis). (B) The four Turkey Vulture populations. A standard ellipse contains about 40% of the points and represents the mean core niche of a population.
The isotopic ranges of carbon and especially nitrogen in feathers of Turkey Vultures confirmed that they relied heavily on marine subsidies, at least in some populations, as previously showed for Pleistocene California condors (Gymnogyps californianus) by Chamberlain et al. (2005). Surprisingly, we found important differences in stable isotopes content among feathers of the four study sites despite their geographic proximity, suggesting some local specialization. Feathers collected in Punta Arenas indicated a Turkey Vulture isotope niche similar to those of the seagull and pelican of neighboring areas, suggesting these vultures exploit almost exclusively marine resources.
M.C. Blázquez et al. / Ecological Indicators 63 (2016) 332–336
The nitrogen range and the distance to centroid in Turkey Vulture feathers of San Evaristo were the highest in our samples, and also CR and SEAb were large, indicating high intrapopulation diversity. The two poles of the San Evaristo standard ellipse pointed to the areas of pelican and whiptail lizard, respectively (Fig. 1A), indicating some feathers were built from marine food, some others from terrestrial food, and maybe some ones from mixed food. As San Evaristo is an isolated fishing village, we can speculate that most of the marine food consumed by Turkey Vultures was made from human discards and fishery waste (Fig. S1.C). Thus, the species would play a role recycling organic waste products similar to that described for another small vulture, Neophron percnopterus, in Socotra Island (Gangoso et al., 2013). Vulture pellets collected in San Evaristo contained reptile scales and hairs of mammals (cattle, Lepus sp., Canis sp.). These resources and human refuse likely constitute the bulk of the Turkey Vultures’ terrestrial food at the area (Fig. S1.D). The diet of Turkey Vulture at Los Dolores 1 and Los Dolores 2, was clearly less biased toward marine resources, as indicated by the nearby position of their ellipses to that of the whiptail. This can be explained by the scarcer marine subsidies provided by humans at Los Dolores, where inhabitants are ranchers. However, a noticeable difference did appear when comparing Los Dolores 1 and Los Dolores 2, despite being separated by scarcely 1 km. Many feathers at Los Dolores 2 were strikingly enriched in 13 C, suggesting a terrestrial, but different, source of food. The more feasible explanation is that terrestrial resources contributing to feathers from Los Dolores 2 (abattoir roost) included remains of human-fed cows and goats, whose food was supplemented by corn and sorghum, which are C4 plants (Chamberlain et al., 2005). The isotope niches of our reference species deserve some discussion. Seagulls are potential garbage eaters, but our results indicated they relied exclusively on marine resources at the area. Besides, their feathers seemed consistently enriched in 15 N with respect to those of pelicans, suggesting a higher relative trophiclevel (Post, 2002), probably because gulls consume remains of predator fish discarded by fishermen, while pelicans are mainly active hunters of low trophic-level pelagic fish. Regarding the whiptail, a lizard consuming a variety of arthropods, its isotopic niche revealed the importance of C4 -CAM plants fueling the terrestrial food-webs at Baja California deserts (Delibes et al., 2015). The number of individual vultures contributing feathers is unknown (i.e. one individual could contribute more than one feather). However, as the isotopic composition of feathers was associated with the food ingested when they were growing, each one should be considered a separate sample (Jaeger et al., 2009). Besides, our Turkey Vultures were residents at the area and their molt is slow along one year (Chandler et al., 2010), so their feathers were grown at place and at different yearly moments. We consider that, despite this and other potential criticisms, our results are clear enough to allow a definite reading. To conclude, stable isotope analysis clearly indicated that marine subsidies are important resources for coastal Turkey Vultures in Baja California, surely contributing to their abundance in the area. Also, the importance of nutrients of marine origin varied among local subpopulations, suggesting some spatial segregation. We speculate that dominant individuals would be established all around the year near predictable sources of food (e.g. human settlements: cattle ranches, villages, fishermen camps. . .), having a mixed terrestrial-marine diet highly influenced by the type of local human activities. Meanwhile, subordinate individuals would be relegated to wandering along the beaches searching for washed up food, having a diet almost exclusively marine. This type of habitat segregation among conspecific Turkey Vultures has been previously described elsewhere (Kirk and Houston, 1995). On the other
335
hand the fine discrimination among feathers’ isotopic signatures from close sites allow us speculate that Turkey Vultures could be used as good indicators for the environmental/ecological change in the food web mediated by human activities in arid and coastal areas. Acknowledgments We thank our expedition partners for permanent support. Dr. J.A. Donázar and Dr. K. Hobson made accurate comments on the early stages of this manuscript, C. Swann reviewed the English and S. Conradi gave edition support. M. Delibes-Mateos is currently funded by Consejería de Economía, Innovación, Ciencia y Empleo of Junta de Andalucía, and the European Union’s Seventh Framework Programme for research, technological development and demonstration under grant agreement 267226. All applicable institutional and/or national guidelines for the care and use of animals were followed. References Barrett, K., Anderson, W.B., Wait, D.A., Grismer, L.L., Polis, G.A., Rose, M.D., 2005. Marine subsidies alter the diet and abundance of insular and coastal lizard populations. Oikos 109, 145–153, http://dx.doi.org/10.1111/j.0030-1299.2005. 13728.x. Bender, M.M., 1971. Variations in the 13 C/12 C ratios of plants in relation to the pathway of photosynthetic carbon dioxide fixation. Phytochemistry 10, 1239–1244. Chamberlain, C.P., Waldbauer, J.R., Fox-Dobbs, K., Newsome, S.D., Koch, P.L., Smith, D.R., Church, M.E., Chamberlain, S.D., Sorenson, K.J., Risebrough, R., 2005. Pleistocene to recent dietary shifts in California condors. Proc. Natl. Acad. Sci. U.S.A. 102, 16707–16711, http://dx.doi.org/10.1073/pnas.0508529102. Chandler, R.M., Pyle, P., Flannery, M.E., Long, D.J., Howell, S.N.G., 2010. Flight feather molt of Turkey Vultures. Wilson J. Ornithol. 122, 354–360, http://dx.doi.org/10. 1676/09-094.1. Delibes, M., Blázquez, M.C., Fedriani, J.M., Granados, A., Soriano, L., Delgado, A., 2015. Isotopic niche variation in a higher trophic level ectotherm: highlighting the role of succulent plants in desert food webs. PLOS ONE 10, e0126814, http://dx.doi. org/10.1371/journal.pone.0126814. Gangoso, L., Agudo, R., Anadón, J.D., De la Riva, M., Suleyman, A.S., Porter, R., Donázar, J.A., 2013. Reinventing mutualism between humans and wild fauna: Insights from vultures as ecosystem services providers. Conserv. Lett. 6, 172–179, http:// dx.doi.org/10.1111/j.1755-263X.2012.00289.x. Grecian, W.J., McGill, R.A.R., Phillips, R.A., Ryan, P.G., Furness, R.W., 2015. Quantifying variation in ı13 C and ı15 N isotopes within and between feathers and individuals: Is one sample enough? Mar. Biol. 162, 733–741, http://dx.doi.org/10.1007/ s00227-015-2618-8. Hobson, K.A., Sealy, S.G., 1991. Marine protein contributions to the diet of Northern Saw-whet Owls on the Queen Charlotte Islands: a stable-isotope approach. Auk 108, 437–440. Houston, D.C., 1994. Family Cathartidae (New World Vultures). In: Hoyo, J., Elliot, A., J.S. (Eds.), Handbook of the Birds of the World, vol. 2. New World Vultures to Guineafowl, Lynx Edicions, Barcelona, pp. 24–41. Inger, R., Bearhop, S., 2008. Applications of stable isotope analysis to studies of avian ecology. Ibis (Lond. 1859) 150, 447–461. Jackson, A.L., Inger, R., Parnell, A.C., Bearhop, S., 2011. Comparing isotopic niche widths among and within communities: SIBER – stable isotope Bayesian ellipses in R. J. Anim. Ecol. 80, 595–602, http://dx.doi.org/10.1111/j.1365-2656.2011. 01806.x. Jackson, M.C., Donohue, I., Jackson, A.L., Britton, J.R., Harper, D.M., Grey, J., 2012. Population-level metrics of trophic structure based on stable isotopes and their application to invasion ecology. PLoS ONE 7, 1–12, http://dx.doi.org/10.1371/ journal.pone.0031757. Jaeger, A., Blanchard, P., Richard, P., Cherel, Y., 2009. Using carbon and nitrogen isotopic values of body feathers to infer inter- and intra-individual variations of seabird feeding ecology during moult. Mar. Biol. 156, 1233–1240, http://dx.doi. org/10.1007/s00227-009-1165-6. Kirk, D.A., Houston, D.C., 1995. Social dominance in migrant and resident turkey vultures at carcasses: evidence for a despotic distribution? Behav. Ecol. Sociobiol. 36, 323–332, http://dx.doi.org/10.1007/s002650050154. ˜ C.G., Post, D.M., 2007. Can stable isotope Layman, C.A., Arrington, D.A., Montana, ratios provide for community-wide measures of trophic structure? Ecology 88, 42–48, http://dx.doi.org/10.1890/0012-9658(2007)88[42:CSIRPF]2.0.CO;2. Maulf, L.Y., 1983. The physical oceanography. In: Case, T.J., Cody, M.L. (Eds.), Island Biogeography in the Sea of Cortez. University of California Press, Los Angeles, pp. 26–45. Polis, G.A., Anderson, W.B., Holt, R.D., 1997. Towards an integration of landscape and food web ecology: the dynamics of spatially subsidized food webs. Annu. Rev. Ecol. Syst. 28, 289–316, http://dx.doi.org/10.1146/annurev.ecolsys.28.1.289.
336
M.C. Blázquez et al. / Ecological Indicators 63 (2016) 332–336
Polis, G.A., Hurd, S.D., 1995. 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. 92, 4382–4386, http://dx.doi.org/10.1073/pnas.92. 10.4382. Post, D.M., 2002. Using stable isotopes to estimate trophic position: models, methods, and assumptions. Ecology 83, 703–718, http://dx.doi.org/10.2307/3071875.
Rose, M.D., Polis, G.A., 1998. The distribution and abundance of coyotes: the effects of allochthonous food subsidies from the sea. Ecology 79, 998–1007, http://dx. doi.org/10.1890/0012-9658(1998)079[0998:TDAAOC]2.0.CO;2. Schoeninger, M.J., De Niro, M.J., 1984. Nitrogen and carbon isotopic composition of bone-collagen from marine and terrestrial animals. Geochim. Cosmochim. Acta 48, 625–639.
Contents lists available at ScienceDirect
Ecological Indicators journal homepage: www.elsevier.com/locate/ecolind
Short Communication
Stable isotope evidence for Turkey Vulture reliance on food subsidies from the sea Ma Carmen Blázquez a,∗ , Miguel Delibes-Mateos b,c , J. Mario Vargas d , Arsenio Granados e , Antonio Delgado e , Miguel Delibes f a
Centro Investigaciones Biológicas Noroeste, Avda. Politécnico Nacional 195, 23096 La Paz, B.C.S., Mexico CIBIO/InBIO, Universidade do Porto, Campus de Vairão, 4485-661 Vairão, Portugal c Instituto de Estudios Sociales Avanzados (IESA-CSIC), Campo Santo de los Mártires 7, 14004 Córdoba, Spain d Department of Biología Animal, Facultad de Ciencias, Universidad de Málaga, 29071 Málaga, Spain e Instituto Andaluz de Ciencias de la Tierra, CSIC-UGR, Avda. de las Palmeras 4, 18100 Armilla, Granada, Spain f Department of Conservation Biology, Estación Biológica de Do˜ nana, CSIC, Avda. Américo Vespucio s/n., 41092 Seville, Spain b
a r t i c l e
i n f o
Article history: Received 27 October 2015 Received in revised form 11 December 2015 Accepted 13 December 2015 Keywords: Baja California Cathartes aura Isotopic niche Marine subsidies Stranded carcasses
a b s t r a c t Turkey Vulture (Cathartes aura) reliance on marine subsidies in coastal Baja California peninsula was quantitatively assessed by analyzing carbon and nitrogen stable isotope ratios in its feathers. Feathers were collected in two separate roosts in a small farm, a small fishing village and an uninhabited beach. We compared among them the isotopic niches of the four populations and also with those of Yellowfooted Seagull (Larus livens), Brown Pelican (Pelecanus occidentalis) and Orange-throated Whiptail lizard (Aspidoscelis hyperythra), used as reference for sympatric marine and terrestrial species. The importance of nutrients of marine origin varied among local close subpopulations, suggesting some spatial segregation. Dominant individuals would be established near predictable sources of food (human settlements), having a mixed terrestrial–marine diet influenced by local human activities (isotopic signature of feathers also indicated the role of human-fed cattle as vulture food). Subordinate individuals would be relegated to wandering along the beaches searching for washed up food, having a diet almost exclusively marine. © 2015 Elsevier Ltd. All rights reserved.
1. Introduction Contiguous ecosystems exchange nutrients, energy and organisms, usually referred to as resource subsidies. These subsidies can substantially influence population dynamics, interactions, trophic pathways and other aspects of the recipient food webs (Polis et al., 1997). Often it is assumed that the roles of ecosystem crossing resources vary in function of their productivity, more productive systems being mainly donors and poorer ones being recipients. The Gulf of California with its islands and surrounding lands makes a good example of this resources asymmetry, as very low terrestrial productivity contrasts with the highly productive sea (Maulf, 1983). Probably because of this, the area has been scenario of several pioneering studies showing the effects of marine subsidies on terrestrial consumers at species (e.g. Coyote, Canis latrans; Rose and Polis, 1998), guild (e.g. spiders; Polis and Hurd, 1995) and community levels (e.g. algae, arthropods and lizards; Barrett et al., 2005).
∗ Corresponding author. Tel.: +52 6121238441. E-mail address: [email protected] (M.C. Blázquez). http://dx.doi.org/10.1016/j.ecolind.2015.12.015 1470-160X/© 2015 Elsevier Ltd. All rights reserved.
To the best of our knowledge, the use of marine subsidies by terrestrial bird species has been scarcely assessed anywhere in the world, with some exceptions (e.g. Hobson and Sealy, 1991). The Turkey Vulture (Cathartes aura) is the most widespread of all Neotropical vultures, ranging from south Canada to Tierra del Fuego in Chile and Argentina. Its diet includes dung and refuse, some fruits, small animals actively hunted and mainly carrion, which it can locate through olfaction (Houston, 1994). We suspect marine food is important in the diet of Turkey Vultures living by the coast in subtropical Baja California peninsula, as individuals eating from discarded remains near fishermen’s camps or from stranded carcasses at the beach are frequently detected (Fig. S1.B and C). However, this prediction has not been evaluated until now. We will prove that stable isotope ratios of carbon (13 C/12 C) and nitrogen (15 N/14 N) in Turkey Vulture feathers can indicate the quantitative importance for the species of marine resources at four sites of Baja California (Mexico). Supplementary Fig. S1 can be found, in the online version, at http://dx.doi.org/10.1016/j.ecolind.2015.12.015. The isotopic composition of body tissues reflects the materials used to build them. Classical pioneering studies proved that marine
M.C. Blázquez et al. / Ecological Indicators 63 (2016) 332–336
resources are enriched in heavier nitrogen and in heavier carbon (when terrestrial C3 biomass is dominant), which allows using carbon and nitrogen stable isotopes for dietary analyses focusing on the relative importance of terrestrial and marine food sources (Schoeninger and De Niro, 1984). Also, differences in the role of some kinds of terrestrial resources, including human-fed livestock, could be detected, because plants using different photosynthetic metabolic ways (C3 , C4 and Crassulacean Acid Metabolism, CAM) generate distinct ı13 C signatures (Bender, 1971). As feathers are metabolically inert tissue, their isotopic values indicate what the bird consumed at the time the feather was growing (Inger and Bearhop, 2008). Turkey Vulture feathers grown while its owner was consuming marine food should be enriched in heavier nitrogen and (in C3 based food-webs) heavier carbon, having rather similar isotopic signatures to feathers of sympatric marine birds. On the other hand, feathers grown when the bird was consuming mainly terrestrial foods should be depleted in heavier nitrogen and (in a lesser degree) carbon, their isotopic signatures resembling those of tissues of sympatric high-level trophic terrestrial consumers. We expect a mixed terrestrial-marine diet for coastal Turkey Vulture residents in Baja California. To test this prediction we compared the isotopic niche of Turkey Vulture with those of two typically marine birds, the Yellow-footed Seagull (Larus livens) and the Brown Pelican (Pelecanus occidentalis), and a terrestrial highlevel trophic consumer, the arthropodivorous Orange-throated Whiptail (Aspidoscelis hyperythra). Additionally, we also predict a reduced intrapopulation variation in the Turkey Vulture isotopic niche, as it is a mobile bird and our sampling sites were nearby. 2. Materials and methods 2.1. Study area Baja California peninsula is a volcanic fringe of land at the Western side of North America, running from north-west to south-east 1300 km long and, on average, about 100 km wide. Our study area at the Gulf of California coast, characterized by soft hills, dry sandy pebbly riverbeds, and scattered oasis with palm trees, is arid and hot, with uncertain precipitations from August to October, and practically without rain in other months of the year. The Turkey Vulture is the most abundant raptor species in southern Baja California, especially near villages, in agricultural areas and by the coast. Feathers were collected on October 2011, before the arrival to the area of potential wintering individuals, at three localities (and four sites) on the Gulf coast of southern Baja California. From north to south, these were: (A) Los Dolores (25◦ 4 34 N, 110◦ 51 32 W): A palm oasis, with a traditional cattle farm (about 400 cows and goats), owned by one family. Some feathers (n = 11) were taken under a vulture roost on high palms (Washingtonia robusta, Phoenix dactylifera) by the beach (site Dolores 1). More feathers (n = 33) were taken under another roost on giant cacti (Cardon, Pachycereus pringlei), about 1 km inland, by an open-air abattoir (site Dolores 2) (see Fig. S1.E). (B) San Evaristo (24◦ 54 25 N, 110◦ 42 14 W): A small fishermen’s village (about 80 inhabitants), 27 km south of Los Dolores. Feathers (n = 14) were collected under a metal lighthouse where vultures roost at night. (C) Punta Arenas (24◦ 53 17 N, 110◦ 41 28 W): An uninhabited beach with sand dunes, 5 km south of San Evaristo. Feathers (n = 12) were collected around a marine turtle carcass that was being eaten by several Turkey Vultures.
333
Seagull and pelican feathers (n = 17 and 23, respectively) were also collected on October 2011 at distinct communal roosting places in San Evaristo and Nopoló (24◦ 59 49 N, 110◦ 45 32 W). For comparison, we used isotopic data of tail tissue of whiptail lizards (n = 13) live-captured in 2009 at Presa de Ihuazil (24◦ 56 49 N, 111◦ 24 25 W; for details, see Delibes et al., 2015). This location is at the same latitude as A, B and C but 52 km inland. 2.2. Sample collection and analyses We collected equally downy, small and large contour feathers. From large feathers, we cut a transversal fringe of about 1 cm of the tail tip, in order to select a fraction grown in a few days, removing potential within-feather variation (Grecian et al., 2015). Before analysis, feathers were cleaned of surface contaminants using warm water (50 ◦ C) in an ultrasonic cleaner for 5 min and dried at room temperature for 24 h. Isotope measurements were carried out at the Stable Isotope Laboratory of the Instituto Andaluz de Ciencias de la Tierra (CSIC-UGR, Granada, Spain), using a Carlo Elba NC1500 (Milan, Italy) elemental analyzer on line with a Delta Plus XL (ThermoQuest, Bremen, Germany) mass spectrometer (EAIRMS). Isotopic ratios of carbon and nitrogen are presented as ı values, where ı = (Rsample /Rstandard − 1) × 1000, being R = 13 C/12 C for ı13 C values, and R = 15 N/14 N for ı15 N values. Commercial CO2 and N2 were used as internal standards for C and N isotopic analyses. For C, two internal standards of −30.63‰ and −11.65‰ (Vienna Pee Dee Belemnite; VPDB) were analyzed every 10 samples. For N, two internal standards of −1.02‰ and +16.01‰ (AIR) were used. Precision calculated, after correction of the mass spectrometer daily drift from standards systematically interspersed in analytical batches, was better than ±0.1‰ for both ı13 C and ı15 N. Most results are presented through isotopic niche quantitative metrics developed by Layman et al. (2007), adapted to population level by including the ı13 C and ı15 N values of all samples in each population. We first analyzed all Turkey Vulture together in order to obtain an estimation of the overall isotopic niche of the species in the area and compare it with those of the other species. We then analyzed separately the Turkey Vulture niches at each site. Calculations were made in R using the SIAR package (Jackson et al., 2011). For each species or population we calculated: (1) Mean and low and upper 95% confidence limits of ı13 C and ı15 N. In this case, differences among means of species and populations were also analyzed through GLM-Anova tests. (2) Carbon range (CR) and nitrogen range (NR), corresponding to the distance between the two feathers (for whiptails, the two individuals) with the lowest and the highest ı13 C and ı15 N values within each population; they estimate the total carbon and nitrogen range exploited by each population and its relative position in the ı13 C–ı15 N space. (3) Total area (TA) of the convex hull encompassing all points, as a measure of population niche width. This estimator is very dependent on sample size. Because of this we also calculated: (4) Bayesian Standard Ellipse Area (SEAb), bootstrapping data (n = 10,000). Standard ellipse (SEA) contains about 40% of the points and estimates the mean core population niche, being to bivariate data as standard deviation is to univariate data (Jackson et al., 2012). SEAb allows comparisons among populations differing in sample size. Mean areas and the low and upper 95% credible limits are shown. (5) Mean distance to centroid (CD), calculated as the mean Euclidean distance of each sample of a population to the ı13 C–ı15 N centroid for that population, as an estimator of the population isotopic diversity.
334
M.C. Blázquez et al. / Ecological Indicators 63 (2016) 332–336
Table 1 Stable isotope niche metrics for the total Turkey Vulture sample (Cathartes ALL), each Turkey Vulture separate population (DOL1 = Los Dolores 1, DOL2 = Los Dolores 2, EVA = San Evaristo, PAR = Punta Arenas), Yellow-footed gull (Larus livens), Brown pelican (Pelecanus occidentalis) and Orange-throated whiptail (Aspidoscelis hyperythra). TA = total area of convex hull; SEAb = Bayesian standard ellipse area; MC = Mean ı13 C; SD = standard deviation; CR = ı13 C range; MN = mean ı15 N; NR = ı15 N range; CR = mean distance to centroid; n = bivariate sample size. Sp./population
TA
SEAb (95% limits)
MC (SD)
CR (min,max)
MN (SD)
NR (min,max)
CD
n
Cathartes ALL Cathartes DOL1 Cathartes DOL2 Cathartes EVA Cathartes PAR Larus Pelecanus Aspidoscelis
41.8 11.2 25.5 16.7 5.36 5.01 4.74 19.3
12.95 (12.91–12.98) 6.18 (6.15–6.22) 10.65 (10.62–10.70) 8.83 (8.78–8.87) 3.35 (3.33–3.37) 2.31 (2.30–2.33) 2.19 (2.18–2.20) 7.65 (7.61–7.69)
−16.11 (1.48) −17.14 (0.83) −16.34 (1.49) −16.44 (1.38) −14.54 (0.93) −14.88 (1.08) −15.07 (0.55) −17.03 (1.72)
5.75 (−18.99,−13.24) 3.15 (−18.76,−15.61) 4.94 (−18.85,−14.01) 4.24 (−18.99,−14.75) 2.82 (−16.06,−13.24) 3.35 (−16.57,−13.22) 2.08 (−16.10,−14.02) 6.29 (−20.73,−14.44)
16.17 (3.34) 15.72 (2.32) 14.58 (2.33) 16.61 (3.53) 20.69 (1.12) 21.25 (0.58) 19.92 (1.10) 12.09 (1.43)
10.80 (11.11,21.88) 6.57 (12.32,18.89) 7.59 (11.11,18.90) 9.80 (12.08,21.88) 4.16 (17.51,21.67) 2.17 (20.06,22.23) 3.78 (18.02,21.80) 4.66 (9.79,14.45)
3.26 2.14 2.50 3.44 1.18 1.06 1.11 1.92
70 11 33 14 12 17 23 13
3. Results The average values of ı13 C and ı15 N differed among species (F(3,119) = 10.17, F(3,119) = 42.73, respectively; P < 0.001). Post hoc tests showed significant differences among ı13 C values of Turkey Vulture and whiptail compared to pelican and seagull. However, in ı15 N values there were three groups: Turkey Vulture alone, whiptail alone and seagull and pelican together. As expected, the overall Turkey Vulture isotopic niche was much wider than those of seagull and pelican in all considered metrics. The niche of whiptail was intermediate in width among those of Turkey Vulture and marine birds (Table 1). The overlap
(similarity) among the core niches of the four species was quite small (but it must be taken into account that standard ellipse includes only about 40% of the points). The Turkey Vulture core niche slightly overlapped those of whiptail and pelican, which in turn slightly overlapped that of seagull (Fig. 1A). Besides niche width, the greater differences in the isotopic niche of the four species were related to the average values and the range of ı15 N (Table 1 and Fig. 1A). Mean ı15 N was lowest in the whiptail, followed by the Turkey Vulture, the pelican and the seagull. Simultaneously, NR was much greater in the Turkey Vulture than in the other species. In addition, mean ı13 C values were more negative in the whiptail, followed by Turkey Vulture, pelican and seagull. These results indicate, as expected, a terrestrial diet in the whiptail, a marine diet in the pelican and the seagull, and a diet in-between marine and terrestrial in the Turkey Vulture. Contrary to our expectations, the isotopic profiles of Turkey Vulture feathers seemed to be different among the four studied sites (for ı13 C, F(3,66) = 8.714; for ı15 N, F(3,66) = 18.18; P < 0.001 in both cases; see also Table 1 and Fig. 1B), despite they were separated less than 33 km. Post hoc tests showed significant differences among feathers of Punta Arenas and those of the other sites, both for ı13 C (P < 0.002) and ı15 N (P < 0.001) average values. Also, vultures of Punta Arenas had the smallest isotopic niche, with most of its metrics very similar to those of pelican and seagull. On the other hand, the vulture populations of Los Dolores 1, Los Dolores 2 and San Evaristo had partially overlapping, but otherwise different, isotopic niches (Fig. 1B), although their ı13 C and ı15 N means did not differ statistically. In San Evaristo, both MN and NR values were higher. In Los Dolores 1 (by the beach), ı13 C and ı15 N values were smaller. In Los Dolores 2 (by the abattoir) there were a larger proportion of feathers with simultaneously less negative values of ı13 C and low values of ı15 N. The core niche of the Turkey Vulture population of San Evaristo overlapped the other three populations, while Los Dolores 1 and Los Dolores 2 overlapped between them and Punta Arenas only overlapped San Evaristo (Fig. 1B).
4. Discussion
Fig. 1. Stable isotope standard ellipses in the ı13 C–ı15 N space of: (A) Turkey Vulture (Cathartes), Yellow-legged Seagull (Larus), Brown Pelican (Pelecanus) and Orangethroated Whiptail (Aspidoscelis). (B) The four Turkey Vulture populations. A standard ellipse contains about 40% of the points and represents the mean core niche of a population.
The isotopic ranges of carbon and especially nitrogen in feathers of Turkey Vultures confirmed that they relied heavily on marine subsidies, at least in some populations, as previously showed for Pleistocene California condors (Gymnogyps californianus) by Chamberlain et al. (2005). Surprisingly, we found important differences in stable isotopes content among feathers of the four study sites despite their geographic proximity, suggesting some local specialization. Feathers collected in Punta Arenas indicated a Turkey Vulture isotope niche similar to those of the seagull and pelican of neighboring areas, suggesting these vultures exploit almost exclusively marine resources.
M.C. Blázquez et al. / Ecological Indicators 63 (2016) 332–336
The nitrogen range and the distance to centroid in Turkey Vulture feathers of San Evaristo were the highest in our samples, and also CR and SEAb were large, indicating high intrapopulation diversity. The two poles of the San Evaristo standard ellipse pointed to the areas of pelican and whiptail lizard, respectively (Fig. 1A), indicating some feathers were built from marine food, some others from terrestrial food, and maybe some ones from mixed food. As San Evaristo is an isolated fishing village, we can speculate that most of the marine food consumed by Turkey Vultures was made from human discards and fishery waste (Fig. S1.C). Thus, the species would play a role recycling organic waste products similar to that described for another small vulture, Neophron percnopterus, in Socotra Island (Gangoso et al., 2013). Vulture pellets collected in San Evaristo contained reptile scales and hairs of mammals (cattle, Lepus sp., Canis sp.). These resources and human refuse likely constitute the bulk of the Turkey Vultures’ terrestrial food at the area (Fig. S1.D). The diet of Turkey Vulture at Los Dolores 1 and Los Dolores 2, was clearly less biased toward marine resources, as indicated by the nearby position of their ellipses to that of the whiptail. This can be explained by the scarcer marine subsidies provided by humans at Los Dolores, where inhabitants are ranchers. However, a noticeable difference did appear when comparing Los Dolores 1 and Los Dolores 2, despite being separated by scarcely 1 km. Many feathers at Los Dolores 2 were strikingly enriched in 13 C, suggesting a terrestrial, but different, source of food. The more feasible explanation is that terrestrial resources contributing to feathers from Los Dolores 2 (abattoir roost) included remains of human-fed cows and goats, whose food was supplemented by corn and sorghum, which are C4 plants (Chamberlain et al., 2005). The isotope niches of our reference species deserve some discussion. Seagulls are potential garbage eaters, but our results indicated they relied exclusively on marine resources at the area. Besides, their feathers seemed consistently enriched in 15 N with respect to those of pelicans, suggesting a higher relative trophiclevel (Post, 2002), probably because gulls consume remains of predator fish discarded by fishermen, while pelicans are mainly active hunters of low trophic-level pelagic fish. Regarding the whiptail, a lizard consuming a variety of arthropods, its isotopic niche revealed the importance of C4 -CAM plants fueling the terrestrial food-webs at Baja California deserts (Delibes et al., 2015). The number of individual vultures contributing feathers is unknown (i.e. one individual could contribute more than one feather). However, as the isotopic composition of feathers was associated with the food ingested when they were growing, each one should be considered a separate sample (Jaeger et al., 2009). Besides, our Turkey Vultures were residents at the area and their molt is slow along one year (Chandler et al., 2010), so their feathers were grown at place and at different yearly moments. We consider that, despite this and other potential criticisms, our results are clear enough to allow a definite reading. To conclude, stable isotope analysis clearly indicated that marine subsidies are important resources for coastal Turkey Vultures in Baja California, surely contributing to their abundance in the area. Also, the importance of nutrients of marine origin varied among local subpopulations, suggesting some spatial segregation. We speculate that dominant individuals would be established all around the year near predictable sources of food (e.g. human settlements: cattle ranches, villages, fishermen camps. . .), having a mixed terrestrial-marine diet highly influenced by the type of local human activities. Meanwhile, subordinate individuals would be relegated to wandering along the beaches searching for washed up food, having a diet almost exclusively marine. This type of habitat segregation among conspecific Turkey Vultures has been previously described elsewhere (Kirk and Houston, 1995). On the other
335
hand the fine discrimination among feathers’ isotopic signatures from close sites allow us speculate that Turkey Vultures could be used as good indicators for the environmental/ecological change in the food web mediated by human activities in arid and coastal areas. Acknowledgments We thank our expedition partners for permanent support. Dr. J.A. Donázar and Dr. K. Hobson made accurate comments on the early stages of this manuscript, C. Swann reviewed the English and S. Conradi gave edition support. M. Delibes-Mateos is currently funded by Consejería de Economía, Innovación, Ciencia y Empleo of Junta de Andalucía, and the European Union’s Seventh Framework Programme for research, technological development and demonstration under grant agreement 267226. All applicable institutional and/or national guidelines for the care and use of animals were followed. References Barrett, K., Anderson, W.B., Wait, D.A., Grismer, L.L., Polis, G.A., Rose, M.D., 2005. Marine subsidies alter the diet and abundance of insular and coastal lizard populations. Oikos 109, 145–153, http://dx.doi.org/10.1111/j.0030-1299.2005. 13728.x. Bender, M.M., 1971. Variations in the 13 C/12 C ratios of plants in relation to the pathway of photosynthetic carbon dioxide fixation. Phytochemistry 10, 1239–1244. Chamberlain, C.P., Waldbauer, J.R., Fox-Dobbs, K., Newsome, S.D., Koch, P.L., Smith, D.R., Church, M.E., Chamberlain, S.D., Sorenson, K.J., Risebrough, R., 2005. Pleistocene to recent dietary shifts in California condors. Proc. Natl. Acad. Sci. U.S.A. 102, 16707–16711, http://dx.doi.org/10.1073/pnas.0508529102. Chandler, R.M., Pyle, P., Flannery, M.E., Long, D.J., Howell, S.N.G., 2010. Flight feather molt of Turkey Vultures. Wilson J. Ornithol. 122, 354–360, http://dx.doi.org/10. 1676/09-094.1. Delibes, M., Blázquez, M.C., Fedriani, J.M., Granados, A., Soriano, L., Delgado, A., 2015. Isotopic niche variation in a higher trophic level ectotherm: highlighting the role of succulent plants in desert food webs. PLOS ONE 10, e0126814, http://dx.doi. org/10.1371/journal.pone.0126814. Gangoso, L., Agudo, R., Anadón, J.D., De la Riva, M., Suleyman, A.S., Porter, R., Donázar, J.A., 2013. Reinventing mutualism between humans and wild fauna: Insights from vultures as ecosystem services providers. Conserv. Lett. 6, 172–179, http:// dx.doi.org/10.1111/j.1755-263X.2012.00289.x. Grecian, W.J., McGill, R.A.R., Phillips, R.A., Ryan, P.G., Furness, R.W., 2015. Quantifying variation in ı13 C and ı15 N isotopes within and between feathers and individuals: Is one sample enough? Mar. Biol. 162, 733–741, http://dx.doi.org/10.1007/ s00227-015-2618-8. Hobson, K.A., Sealy, S.G., 1991. Marine protein contributions to the diet of Northern Saw-whet Owls on the Queen Charlotte Islands: a stable-isotope approach. Auk 108, 437–440. Houston, D.C., 1994. Family Cathartidae (New World Vultures). In: Hoyo, J., Elliot, A., J.S. (Eds.), Handbook of the Birds of the World, vol. 2. New World Vultures to Guineafowl, Lynx Edicions, Barcelona, pp. 24–41. Inger, R., Bearhop, S., 2008. Applications of stable isotope analysis to studies of avian ecology. Ibis (Lond. 1859) 150, 447–461. Jackson, A.L., Inger, R., Parnell, A.C., Bearhop, S., 2011. Comparing isotopic niche widths among and within communities: SIBER – stable isotope Bayesian ellipses in R. J. Anim. Ecol. 80, 595–602, http://dx.doi.org/10.1111/j.1365-2656.2011. 01806.x. Jackson, M.C., Donohue, I., Jackson, A.L., Britton, J.R., Harper, D.M., Grey, J., 2012. Population-level metrics of trophic structure based on stable isotopes and their application to invasion ecology. PLoS ONE 7, 1–12, http://dx.doi.org/10.1371/ journal.pone.0031757. Jaeger, A., Blanchard, P., Richard, P., Cherel, Y., 2009. Using carbon and nitrogen isotopic values of body feathers to infer inter- and intra-individual variations of seabird feeding ecology during moult. Mar. Biol. 156, 1233–1240, http://dx.doi. org/10.1007/s00227-009-1165-6. Kirk, D.A., Houston, D.C., 1995. Social dominance in migrant and resident turkey vultures at carcasses: evidence for a despotic distribution? Behav. Ecol. Sociobiol. 36, 323–332, http://dx.doi.org/10.1007/s002650050154. ˜ C.G., Post, D.M., 2007. Can stable isotope Layman, C.A., Arrington, D.A., Montana, ratios provide for community-wide measures of trophic structure? Ecology 88, 42–48, http://dx.doi.org/10.1890/0012-9658(2007)88[42:CSIRPF]2.0.CO;2. Maulf, L.Y., 1983. The physical oceanography. In: Case, T.J., Cody, M.L. (Eds.), Island Biogeography in the Sea of Cortez. University of California Press, Los Angeles, pp. 26–45. Polis, G.A., Anderson, W.B., Holt, R.D., 1997. Towards an integration of landscape and food web ecology: the dynamics of spatially subsidized food webs. Annu. Rev. Ecol. Syst. 28, 289–316, http://dx.doi.org/10.1146/annurev.ecolsys.28.1.289.
336
M.C. Blázquez et al. / Ecological Indicators 63 (2016) 332–336
Polis, G.A., Hurd, S.D., 1995. 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. 92, 4382–4386, http://dx.doi.org/10.1073/pnas.92. 10.4382. Post, D.M., 2002. Using stable isotopes to estimate trophic position: models, methods, and assumptions. Ecology 83, 703–718, http://dx.doi.org/10.2307/3071875.
Rose, M.D., Polis, G.A., 1998. The distribution and abundance of coyotes: the effects of allochthonous food subsidies from the sea. Ecology 79, 998–1007, http://dx. doi.org/10.1890/0012-9658(1998)079[0998:TDAAOC]2.0.CO;2. Schoeninger, M.J., De Niro, M.J., 1984. Nitrogen and carbon isotopic composition of bone-collagen from marine and terrestrial animals. Geochim. Cosmochim. Acta 48, 625–639.