Effect of touristic activities on seabirds’ habitat selection on sandy beaches

The distribution of species at different spatial scales is the result of environmental filters and habitat selection, which is defined by an active choice for environments with optimal conditions within a range of ecological tolerance and by factors that meet species-specific demands for resources (Miller 1942, Jones, 2001, Fauchald, 2009). The selection of feeding habitats is controlled mainly by the trade-off between the availability of resources and antagonistic ecological interactions (Miller 1942, Skórka et al. 2009). According to the optimal foraging theory, behaviours that maximize energy intake and minimize the risk of predation perpetuate more frequently in birds’ populations (Pyke 1984, Skórka et al. 2009). Thus, in a heterogenous landscape, experienced individuals tend to select habitat patches with greater intrinsic quality, i.e., those that offer a higher abundance of resources (Matsumura et al. 2011), although young birds can be unfamiliar with habitat quality (Skórka et al. 2016). However, ideal free distribution theory (IFD) predicts that patches with lower intrinsic quality but with lower population density and competition may be selected because the availability of resources per capita is higher (Fretwell 1969; Matsumura et al. 2011). Patches with lower quality can also be selected when either environmental or human factors inadequately signal a lower risk of predation and a higher availability of food, thus consisting in ecological traps (Sherley et al. 2017).

Seabirds represent model biological groups for the study of movement and habitat selection in marine ecosystems. They are among the most vulnerable groups of marine vertebrates, with metapopulations of more than 150 species currently showing declines globally (Paleczny et al. 2015). The selection of feeding habitats by seabirds is naturally controlled by the abundance of prey (Vilchis et al. 2006, Waggitt et al. 2018) but also comprises a mosaic of abiotic variables (Becker and Beissinger 2003; Meager et al. 2012). Human disturbances also affect the habitat selection of seabirds, especially because human activities are perceived as an additional risk of predation (Frid and Dill 2002). If critical habitats are disturbed to the point of limiting the use of that habitat for feeding and other activities, populations can decline due to losses in individual performance (Mallord et al. 2007).

Sandy beaches are coastal ecosystems that hold metacommunities formed by the association of resident species, mostly invertebrates and transient vertebrates (McLachlan and Defeo 2018). The oceanic limit of this ecosystem includes what is called the surf zone, which is an area where wave energy is dissipated and that is used especially by juvenile fish for shelter and feeding (Lasiak 1986; Olds et al. 2018). Beaches with more gentle hydrodynamics have a greater abundance and richness of practically all biological groups, including fish (Defeo et al. 2017; Olds et al. 2018; Esmaeili et al. 2021). Thus, organisms that prey on invertebrates and fish, such as seabirds, may also select beaches with lower wave action and a gentle swash regime to feed, taking on a bottom-up trophic control (Dugan et al. 2003; Lunardi et al. 2012). Similarly, human disturbances have depleted food resources and driven seabirds away, making the ecosystem inadequate for foraging (Meager et al. 2012).

The aim of this work was to identify the response of seabirds to human disturbances on sandy beaches – in southeastern Brazil. We tested the hypothesis that human disturbances prevent seabirds foraging in sectors impacted by recreational activities, regardless of the physical conditions and food availability.

The sector with the high impact from urbanization and recreational activities in Praia Grande has characteristics that theoretically make it a patch of higher quality for seabird foraging than the other sectors. There, the interface between the surf zone and shoreface is less physically harsh, due to the nearby rocky outcrops, thus presenting a lower wave action and a more gentle swash, for which reason there is a greater availability of food for piscivorous birds such as terns and the brown booby (Costa et al. 2017b). Our results suggest a chronic use of the habitat in sectors with lower resource abundance and further from nesting islands, especially by the brown booby. Thus, the results for this species corroborate the hypothesis that human disturbances regulate the use of the habitat by seabirds at fine scales.

The greater effort to search for prey in patches with less availability of resources and further away from brown booby colonies seem to contradict the optimal foraging theory. Moreover, the increased number of people on the beach showed a linear negative relationship with the foraging activity of the species, evidencing an avoidance behaviour. Similarly, Velando and Munilla (2011) observed that an increase in boat traffic around islands of the Iberian Peninsula resulted in a substantial decrease in the foraging activity of the European shag Phalacrocorax aristotelis (Linnaeus, 1761), excluding individuals from optimal feeding grounds. This higher use of energy may result in decreased body condition among reproductive females and lower success rates among offspring (Graña et al. 2018). Even subtle variations in fecundity and in the success of the offspring can trigger a long-term reduction in the size of populations (Chastel et al. 1995).

The aggregation of individuals in areas with lower availability of resources per capita, though with less human disturbance, may produce a negative density dependence due to the competition in areas with lower carrying capacity. This demands an even greater displacement of birds to other habitat patches that are further away from the colony (Weimerskirch et al. 2007). This displacement that depends on either the density or level of human disturbance into the lower-quality patches is similar to the premise of the ideal free distribution theory (IFD), as proposed by Velando and Munilla (2011). Seabirds are mobile and freely select habitats, which makes them interesting study models for the IFD, especially on beaches that are apparently homogeneous systems. However, studies that measure individual fitness and energetic balance are needed to confirm if the cost-benefit of the selection of areas with different intrinsic qualities is comparable, corroborating the IFD. In addition, the chronic avoidance of urban coastal environments with high food availability can represent a typical ecological trap (a low-quality habitat that animals prefer over other available habitats of higher quality) (Battin 2004).

The implications of seabird species selecting lower quality habitat at a fine scale are, nevertheless, controversial. The species are highly mobile, which could make the choice for feeding grounds that are located a few kilometers away from their nesting islands irrelevant for their body condition (Weimerskirch 1998). Moreover, the availability of fish in the low impact sectors, including in areas other than the surf zone, may be sufficient to meet the caloric needs of the birds and compensate their displacement. However, brown boobies foraging on sandy beaches do not seem to meet their preference for larger pelagic prey (Branco et al. 2005), since the surf zone is inhabited mostly by small juvenile fish (Lasiak 1986). Thus, it is possible that fish from the surf zone near the nesting islands are in fact captured to feed chicks (Lewis et al. 2004). According to Lewis et al. (2004), the distance, frequency, and duration of the displacement of brown boobies in search of food are strong indicators of the age of their offspring. As their young grow, solitary displacement becomes more frequent and long-lasting, due to a perceived lower risk of chick predation (Lewis et al. 2004). Thus, Praia Grande seems to be a decisive habitat for the recruitment success of the brown booby. The search for scarcer food in more distant areas from the colony, induced by human pressure, can therefore result in a cascading loss in body condition among the reproductive pairs responsible for parental care and among their offspring, thus also affecting their future reproductive success (Lewis et al. 2004).

Temporal variation in the use of beaches, near the colony, for seabird feeding can thus be closely linked to periods of nesting, recruitment, and feeding offspring. In tropical regions, the tendency is that metapopulations show a similar contribution of offspring and reproductive adults throughout the year, suppressing possible temporal variations in foraging for this reason. Here we observed that fine-scale temporal variation of habitat selection was related to the wind speed. The higher the wind speed, the lower the number of brown booby individuals foraging on the beach. The brown booby has relatively low wing loading; thus, flight stability and prey detection are hindered by strong winds, leading to lower foraging rates on the beach (Yamamoto et al. 2017). This individual attribute probably makes boobies more susceptible to climate change, since an increase in the frequency and intensity of extreme events has been observed globally (Harley et al. 2006).

Refuting the hypothesis that human disturbances negatively affect the foraging of seabirds on the beach, the kelp gull was generally more abundant in the sector with higher impact from urbanization and recreational activities. This species is known to be synanthropic, tolerating human presence, besides feeding opportunistically on human food subsidies (Duhem et al. 2003; Maciusik et al. 2010). Studies across the globe have observed for decades an increase in the population size of gulls in urban areas due to the higher availability of human food (Goutner 1992; Bosch et al. 1994; Vidal et al. 1998; Spelt et al. 2021). On the other hand, negative effects in fecundity, reproductive success, and behaviour among gulls, which may become reliant on the trophic subsidies from beach visitors, have also been reported (Bosch et al. 1994; Orams 2002; Ramos et al. 2009). Moreover, species that are sensitive to human presence and that coexist with gulls may be competitively excluded from areas with a high availability of human food (Ramos et al. 2009). In the region, feeding seabirds on purpose is considered a relevant tourism activity, with gulls seeking food from visitors’ hands, which also justifies the aggregation of these birds on urban beaches. The socioecological implications of this practice are controversial and need to be better studied, seeking adequate management (Orams 2002; Newsome and Rodger 2008).

The number of kelp gulls foraging on the beach was positively related to the size of the swash. In fact, the high impact sector was characterized by gentler physical conditions, which, added to urbanization, could favour habitat selection in the case of this synanthropic species. The close relationship between biotic systems and physical conditions determines the classical ecological hypothesis and theories of sandy beaches (McLachlan and Defeo 2018). In general, a higher richness of bird communities and size of populations on beaches are attributed to a gentler swash regime, which acts as an environmental filter for habitat harshness (McLachlan and Defeo 2018; Costa et al. 2022b). Under more severe physical conditions, species with low tolerance levels are excluded and, those that establish populations, tend to be less abundant and more sensitive to human disturbances due to the individual energy budget that is directed for survival to the detriment of growth and reproduction (Mclachlan et al. 1993; Defeo et al. 2003; Costa et al. 2022a). These relationships have been tested through observational studies, mainly with sedentary invertebrates, while studies on the active selection of habitats by birds are still incipient (Rangel et al. 2022).

The present study offers an important baseline for investigations on a larger spatial scale regarding the use of beaches and habitat selection by transient species, particularly when beaches are near to seabird breeding islands. Regardless of the limited spatial scale and absence of replicas of urbanization levels, our results have numerous implications for the management and conservation of sandy beaches at local and regional scales. First, birds have a higher conservation appeal than invertebrates (Miralles et al. 2019), which despite these biological groups being more studied and abundant on beaches, does not gain so much interest from the population (Schlacher et al. 2008; Harris et al. 2014). Thus, the choice of priority areas for conservation and beach zoning based on bird habitat selection data, including species that are endangered and considered charismatic, will certainly receive greater support from the general public and decision makers (Maguire et al. 2011). Moreover, controlled ecotourism activities in urban areas, such as birdwatching, can surely contribute to the development of a biocentric behaviour and to the support of local environmental education projects, in addition to enabling opportunities for local economic activities and citizen science (Veríssimo et al. 2009; Fanini et al. 2021). Obviously, activities such as birdwatching and even feeding of synanthropic birds must be supported by previous studies that evaluate their ecological implications on individuals and ecosystems (Newsome and Rodger 2008.

In conclusion, the fine scale habitat selection carried out by the most abundant seabirds in the study area was regulated mainly according to the impact of urbanization and recreational activities. Human disturbance suppresses the brown booby’s use of the habitat patches with more food resources and that are closer to nesting islands. In turn, synanthropic species such as kelp gulls aggregate in areas with greater human presence, benefitting from gentler hydrodynamics. Here we suggest the use of seabirds as study models for the classical hypotheses that determine sandy beach ecology and habitat selection. This recommendation is based on the potential of these birds to support conservation projects and gain community support through environmental education actions, ecotourism, and citizen science. This can be a viable solution for the development of a biocentric perspective on sandy beaches, going beyond the delivery of ecosystem services related exclusively to recreation.