Previous work on the medium ground finch suggests that divergence of the morphs has recently diminished at sites adjacent to a human settlement (Hendry et al., 2006 ). It has been hypothesized that the apparent recent fusion of beak‐size distributions of the morphs, from bimodal to unimodal, was due to the introduction and ready availability of human foods, which might be flattening the adaptive landscape and thereby reducing selection against intermediate forms (De León et al., 2011 ; Hendry et al., 2006 ). A critical test of this hypothesis would involve asking whether niche segregation and feeding preferences actually differ between urban and non‐urban contexts. In the present paper, we offer such a test, by conducting feeding observations and field experiments on coexisting ground finch species at sites that span different degrees of urbanization.

In the adaptive radiation of Darwin's finches, beak morphology has diversified as a consequence of adaptation to different ecological resources. For instance, in the ground finches, divergent beak sizes and shapes are considered adaptations to exploit different seed types (Supporting Information Figure S1 ), presumably corresponding to different peaks on their adaptive landscape (Abbott, Abbott, & Grant, 1977 ; Bowman, 1961 ; Grant & Grant, 2008 ; Lack, 1947 ; Schluter & Grant, 1984 ). Specifically, the small, medium, and large ground finches ( Geospiza fuliginosa, G. fortis, and G. magnirostris ) feed on small/soft, medium, and large/hard seeds, respectively, and accordingly have evolved small, medium, and large beaks. The closely related cactus finch ( Geospiza scandens) specializes on the nectar, pollen, and seeds of Opuntia cacti and has evolved an elongated beak (Supporting Information Figure S1 ). Resource partitioning has also promoted intra‐specific adaptive divergence within the medium ground finch, where two beak‐size morphs on Santa Cruz Island have diverged significantly in ecological (De León et al., 2014, 2012 ), morphological (Hendry et al., 2006 ; Hendry, Huber, León, Herrel, & Podos, 2009 ; Huber, Leon, Hendry, Bermingham, & Podos, 2007 ), and genetic attributes (Chaves et al., 2016 ; De León, Bermingham, Podos, & Hendry, 2010 ; Huber et al., 2007 ). Resource partitioning has also been associated with morphological divergence between highland and lowland populations of the small ground finches on Santa Cruz Island (Kleindorfer, Chapman, Winkler, & Sulloway, 2006 ; Sulloway & Kleindorfer, 2013 ). Studies on the continuum of intra‐ to inter‐specific divergence in the ground finches can help reveal the processes underlying adaptive divergence and how it might be influenced by urbanization.

The process of divergence via niche segregation can be conceptualized as the splitting of populations along a “rugged” adaptive landscape—a surface relating the mean fitness of populations or species to mean trait values, with “ruggedness” arising from distinct alternative fitness peaks that correspond to different ecological resources (Simpson, 1953 ; Svensson & Calsbeek, 2012 ). As such, alterations to resource availability and resource distributions are viewed as affecting the shape of adaptive landscapes underlying diversification (De León et al., 2011 ; Hendry et al., 2006 ). Alterations to adaptive landscapes can be particularly drastic in the case of human disturbances such as urbanization, where large swathes of natural environments—and the resources they contain—are altered by many factors, including infrastructure development, the introduction of exotic species, and human food availability (Alberti, 2015 ; Aronson et al., 2014 ; Gaston, 2010 ; Gotanda, Hendry, & Svensson, 2017 ; McKinney, 2002, 2006 ; Penick, Savage, & Dunn, 2015 ). However, despite the rapid increase in urbanization worldwide (Grimm et al., 2008 ; Seto, Sánchez‐Rodríguez, & Fragkias, 2010 ; Wigginton, Fahrenkamp‐Uppenbrink, Wible, & Malakoff, 2016 ), and accumulating evidence that some species can adapt accordingly (Donihue & Lambert, 2014 ; Johnson & Munshi‐South, 2017 ; Kettlewell, 1955 ; Littleford‐Colquhoun, Clemente, Whiting, Ortiz‐Barrientos, & Frère, 2017 ; Lowry, Lill, & Wong, 2013 ; Slabbekoorn & Peet, 2003 ; Winchell, Reynolds, Prado‐Irwin, Puente‐Rolón, & Revell, 2016 ), the exploitation of human‐introduced ecological resources has not yet been linked to the alteration of specific ecological niches or adaptive landscapes that drive diversification in nature. Here, we explore such links in Darwin's ground finches ( Geospiza spp.) across sites with different degrees of urbanization on Santa Cruz Island, Galápagos, Ecuador. Specifically, we ask the following: (a) Has the availability of novel human foods in urban areas altered finch diets?; and, if so, (b) Do finches in urban environments prefer human foods over natural foods?; (c) Do finches in urban areas respond differently to the presence of people?; and (d) What are the consequences of finches' use of human foods for the persistence of ecological differences underlying the finch adaptive radiation?

One of the hallmarks of adaptive radiation is niche segregation, whereby closely related populations or species evolve to specialize on distinct ecological resources (Grant, 1999 ; Lack, 1947 ; Schluter, 2000 ; Simpson, 1953 ). Niche segregation is thought to emerge principally from competition for shared ecological resources (Gause, 1934 ; Hardin, 1960 ; Macarthur & Levins, 1967 ; Roughgarden, 1976 ; Schoener, 1968 ) and is determined jointly by the availability of ecological resources and the ability of consumer populations to exploit those resources. Accordingly, variation in resource distributions can facilitate niche segregation between populations or species in a given environment (De León, Podos, Gardezi, Herrel, & Hendry, 2014 ; Levine & HilleRisLambers, 2009 ; Pianka, 1973 ; Schoener, 1974 ; Tilman, 1982 ). Niche segregation can also be favored by additional factors, including behavioral flexibility or phenotypic plasticity, whereby individuals explore novel resources within shared environments (Boogert, Monceau, & Lefebvre, 2010 ; Ducatez, Clavel, & Lefebvre, 2015 ; Inouye, 1978 ; Nicolakakis, Sol, & Lefebvre, 2003 ; Sol, González‐Lagos, Moreira, Maspons, & Lapiedra, 2014 ; Wright, Eberhard, Hobson, Avery, & Russello, 2010 ) or by genetically based phenotypic variability, whereby individuals with different trait values exploit and diverge into resources to which they are best adapted (Bolnick & Paull, 2009 ; Bolnick, Svanbäck, Araújo, & Persson, 2007 ; De León, Rolshausen, Bermingham, Podos, & Hendry, 2012 ).

2 METHODS

2.1 Field sites Sampling and experiments took place between January and March of 2014 and 2015 at four sites on Santa Cruz Island, Galápagos, Ecuador (Figure 1). All four sites are located within the low‐elevation arid zone of the island (Wiggins & Porter, 1971) and differed in their degrees of urbanization as well as human‐associated activities (i.e., the tendency of people to feed finches; see Table 1 for details). The foraging ecology and food preferences of finches are likely to differ in transition or high‐elevation sites, and therefore, responses to urbanization may also differ in these zones. Figure 1 Open in figure viewer PowerPoint Finches feeding on human foods at urban sites. Panels show a female medium ground finch eating dry rice from a feeder (a). Study sites on Santa Cruz Island, Galápagos, Ecuador, with urban (black dots) sites, non‐urban sites (gray dots), and roads (lines) designed for vehicular traffic (b). Santa Rosa and Bellavista were not included in our study, but are shown here for illustrative purpose only. A group of small ground finches feeding crumbs off a plate at restaurant in Puerto Ayora (c). Photo credit: L. F. De León Table 1. Level of urbanization and human behavior at each study site on Santa Cruz Island, Galápagos, Ecuador Site Urbanization level Annual visitors Tendency of feeding Human contact El Garrapatero Non‐urban Only scientists visit this site No human feeding; low human density Minimal contact with humans, except for scientists and park rangers El Garrapatero Beach Non‐urban tourist 38,542 Regular human feeding; low human density Humans visit beach for the day and bring snacks/picnics as there are no shops Academy Bay Intermediate urban 78,555 Little human feeding, but finches feed opportunistically on food scraps, and are likely to be intentionally fed on occasions; high human density Humans visit research center and are advised not to feed the finches, but finches are often within close proximity to large groups of people Puerto Ayora Urban 158,339 Regular human feeding; high human density Humans in city generate food scraps on an hourly basis The first site, El Garrapatero (EG; “non‐urban” site; 0°41'16.6"S 90°13'19.4"W), is located 1–2 km inland of the island's eastern coast and is about 10 km from the nearest major human settlement (Bellavista, Figure 1). Introduced plant species and human foods are rare at this site (De León et al., 2011), although human activity has increased since 2009 due to the paving of a road that provides access to the coast. On a typical day, dozens of vehicles now pass through the site. Browsing by feral goats and donkeys was historically common at EG, but eradication efforts led by the Galápagos National Park (Phillips, Wiedenfeld, & Snell, 2012) have resulted in decreased grazing disturbance. Surveys at this site were performed in an area of ~0.5 km2 eastward from EG road. The second site, EG Beach (“non‐urban tourist” site; 0°41'39.9"S 90°13'15.8"W), hereafter referred to as “EG Beach,” is located on the eastern shore of the island adjacent to the first site (Figure 1). The number of visitors to this site has increased markedly due to the newly paved road, which provides direct access to the beach. Although this site supports no permanent human presence, infrastructure has expanded over the past 6 years to include a gravel parking lot, cobblestone paths, a ranger outpost, and an overnight camping ground. Typically, 5–20 tourists a day (although sometimes many more) visit the beach to swim, kayak, picnic, and observe wildlife. We included this site to help disentangle two urban factors: the large‐scale alteration of habitats (absent here) versus the occasional to regular presence of humans themselves (present here). The third site, Academy Bay (AB; “intermediate urban” site; 0°44'31.6"S 90°18'15.3"W), is situated on the south coast of the island and is contiguous with the town of Puerto Ayora (PA). Human influences at AB include wide cobblestone and dirt paths, a high abundance of exotic plant species, and the presence of human foods associated mainly with concessions for tourists visiting the Charles Darwin Research Station (CDRS), as well as a few local residents and dorms. Finches at this site are regularly observed consuming human foods (Figure 1) and drinking freshwater from tortoise pens and broken pipes (De León et al., 2011). Surveys at this site were performed in an area of ~0.5 km2 encompassing trails from the public entrance of the Galápagos National Park eastward to a cliff behind the animal facilities of the CDRS and did not include the beach areas bordering the CDRS. The fourth site, PA (“urban” site; 0°44'34.8"S 90°18'43.4"W), is the largest human settlement on Galápagos with over 12,000 inhabitants (Instituto Nacional de Estadística y Censos). Puerto Ayora also receives many more tourists than other islands in the Archipelago, with ~218,365, and 241,800 recorded visitors in 2016 and 2017, respectively (Dirección del Parque Nacional Galápagos & Observatorio de Turismo de Galápagos, 2016, 2017). At this site, we have seen finches feeding on a wide variety of introduced plant species and human foods (Figure 1), including bread, potato chips, ice‐cream cones, rice, and beans (De León et al., 2011). Surveys at this site were performed in an area of ~1.0 km2 encompassing the fire station, the farmer's market, the cemetery, the public dock, and the entrance to the trail to Tortuga Bay. Given the complex ways in which finches could interact with humans on Santa Cruz Island (Table 1), we cannot consider our four sampling sites as representing a simple urbanization gradient. We rather consider them as four discrete sites that vary independently in both the degree of urbanization (as given by human infrastructure and population density) and the potential for human interaction with finches (a function of both the number and behavior of tourists). Regarding human interaction with finches, reports from the Galapagos National Park indicate that the number of visitors to the Galápagos is high during the entire year, with two inter‐annual peaks: the first between July and September, and the second in March (Dirección del Parque Nacional Galápagos & Observatorio de Turismo de Galápagos, 2016, 2017 ). Thus, our sampling period (January–March) occurred just before the onset of the second largest peak in the number of visitors. Although we did not quantify food availability in the current study, finches in urban areas are likely to enjoy a surplus of human foods throughout the year. However, we do not expect that this supply was any higher during our sampling period. Further studies will be necessary, however, to better understand how finch preferences for human foods might respond to temporal variation in the availability of both natural and human foods.

2.2 Feeding observations Our first goal was to quantify the diets at our study sites of the four Geospiza species (G. fortis, G. fuliginosa, G. scandens, and G. magnirostris). Toward this end, we employed a point observation method (De León et al., 2014, 2011, 2012 ). Briefly, during morning or afternoon hours, we walked along predetermined transects and used binoculars to identify birds (to the species level) and, if possible, the food items on which they were feeding. At three of our sites, we surveyed along a total of 74 transects covering a linear distance of 30.74 km: EG (n = 22, mean length = 436.80 m), AB (n = 22, 476.75 m), and PA (n = 30, 353.84 m). No feeding observations or estimations of bird density were performed at EG Beach because this site is represented by an open sandy beach with little natural vegetation. Transect courses were determined randomly at the beginning of each walk, but they were limited to a series of preexisting trails that facilitated access to sites with dense vegetation (EG and AB). In the town of PA, transects were determined by following both large and small streets through the middle and around the town, including surrounding neighborhoods (Miraflores and El Edén). Observations in this area included finches found on the streets, sidewalks, and restaurant areas, as well as on the natural vegetation of parks, gardens, and roadsides. Food items included specific plant species and plant parts (i.e., seeds, fruits, leaves, or flowers) as well as different types of human foods. We also recorded the category “ground,” when birds were feeding on the ground, but the exact food items could not be identified owing to their small size. After a feeding event was recorded, we moved immediately onto the next individual to avoid pseudoreplication. Our data therefore represent counts of discrete observations of individual birds feeding on particular food items (De León et al., 2014, 2012 ). Finally, we generated rarefaction curves to visualize how the cumulative numbers of food items observed varied in relation to our sampling efforts at each site.

2.3 Bird density Our second goal was to estimate variation in bird density across sites. For this task, we used bird count data for our focal species from our feeding observation transects, given that we recorded all birds within 30 m at each side of the observer, whether they were feeding or not. We then used these values to estimate the number of individuals per unit area (Emlen, 1977). Two factors could have affected our estimates of bird density. The first is bird detectability at sites with dense vegetation, such as EG and AB, in contrast to the more open urban site (PA). And second, combining feeding observations and bird count along the same transect might not be as accurate as surveys dedicated to bird counts alone. However, our main goal here was to estimate relative differences in bird abundance between urban and non‐urban environments, rather than providing a precise value of bird density at each site. In addition, to reduce autocorrelation effects and to improve detectability we recorded only one feeding event per individual (see above), and only within 30 m of the observer. These types of observations were also facilitated by the fact that Darwin's finches are tame and can be easily observed at short distances with little interference (De León et al., 2014; Grant, 1999).

2.4 Finch response to food cues To test whether and how finches across our study sites respond to the presence of people, we developed a “finch–human interaction” experiment. We recorded finch responses to two different human stimuli: a visual stimulus (an experimenter standing or sitting still and quietly in an open space) and an audiovisual stimulus (an experimenter standing or sitting still and noisily rustling a bag of potato chips, generating a “crinkle” sound typically associated with packaged human foods). Including this second stimulus was inspired by observations of finches approaching humans opening and/or handling packaged foods. The stimuli were presented sequentially and in the same spot, with the visual stimulus first (5 min) and the audiovisual stimulus second (five more minutes). During stimulus presentation, we recorded the number, species, and sex of all birds that approached within 1.5 m of the experimenter, including birds that perched above the experimenter. Presentation locations within our sites were selected haphazardly and were conducted at least 100 m apart from each other during a given day. Data for this experiment were collected at all four sites: EG (non‐urban, n = 22), EG beach (non‐urban tourist, n = 37), AB (intermediate urban, n = 14), and PA (urban, n = 30).

2.5 Feeding preference experiment To quantify finch feeding preferences, and whether and how they varied with the degree of urbanization, we performed replicate “cafeteria” experiments, in which finches were presented with a choice of human and native food items. We constructed cardboard feeding trays (30 cm × 30 cm) with nine sections (3 × 3 grid pattern) into which food could be placed. A rock was placed in the center section of each tray as an anchor. Each tray was stocked with 2.5 g of each of six natural or human foods commonly observed previously (De León et al., 2014, 2011, 2012 ). To control for any potential biases associated with the location of food on the tray, food items were placed randomly in six of the eight available sections of the tray. Human food items included uncooked white rice, potato chips, and coconut cookies, the latter two of which we crumbled into small pieces to mimic the size and shape commonly seen in urban sites. For natural native foods, we included fruits from Cryptocarpus pyriformis, Tournefortia psilostachya, and Scutia spicata. We choose these three plant species because they occur commonly at each of our sites and are eaten frequently by all ground finches, regardless of their beak size (De León et al., 2014). Furthermore, they all produce small and soft seeds, and therefore are comparable to human foods in terms hardness, and are unlikely to impose functional constraints on finch feeding. We did not include additional soft food items such as insect larvae in our experiments because their most important contribution to finch diet is limited to the onset of the rainy season (De León et al., 2014); thus, they represent a less stable food resource for finches when compared with other natural and human foods items. The tray was placed on the ground, and observers moved at least 10 m away or concealed themselves at least 5 m away to record feeding activity. We did not present empty trays in our trials because we were interested in finch preference for different types of foods rather than finches' reactions to the presence of food in general. Trial sites were selected haphazardly, and no trials were conducted within 100 m of each other during the same day. Trays were left out for a maximum of 20 min if no finch approached. If a finch approached and fed from the tray, a timer was started and observations recorded for 10 min from the first finch feeding. We recorded the total number of finches that approached, perched on, and/or fed at the tray, and their species identity. At the end of each trial, trays were collected and the food that remained in each section re‐weighed. We performed trials at all four sites: EG (n = 34), EG beach (n = 40), AB (n = 31), and PA (n = 46). Overall, our experiments were not designed to disentangle the mechanisms underlying natural feeding preferences in Darwin's finches, but rather to test whether or not Darwin finches show preferences for human foods over natural foods in both urban environments and non‐urban environments.