The endangered Galápagos sea lion Zalophus wollebaeki is one of the Galápagos Archipelago's most visible and beloved endemic species. This highly social marine predator uses sandy beaches and rocky outcroppings throughout the Archipelago as haul-out sites, places where individuals rest, breed and care for their young. Often, sea lions choose haul-out sites that overlap with the Galápagos' rapidly growing human settlements, leading to conflict between humans and sea lions. During the day, sea lions compete for space on the beaches with sunbathers, tourists, children and dogs often leading to sea lions chasing humans out of their territory. Sea lions often sleep on fishing boats, creating conflicts with fisherman who see them as threats to their livelihood. At night, sea lions are frequently disturbed by bright lights and music from restaurants and bars.

A crucial question for the conservation and management of this endangered species is: how does living in such close quarters with a rapidly growing human population affect Galápagos sea lions? The species declined from an estimated 40 000 individuals to 16 000 individuals between 1978 and 2001, with little evidence of recovery since 2001 (Trillmich 1979, Trillmich et al. 1991, Alava and Salazar 2006, Riofrío-Lazo et al. 2017). At the same time, the permanent human population of the Galápagos has grown from fewer than 5000 people in 1974 (Epler 2007) to over 25 000 people in 2015 (INEC 2015), and well over 30 000 today. Tourism, too, brings an increasing number of people to the islands each year. In 2015, over 220 000 people visited the Galápagos for cruises or land-based tours (Izurieta 2017), and over 250 000 visited in 2018. Given the fragility of the sea lion population, it is important to understand any threats that humans pose to this species.

Some human threats to sea lions are well-documented. The proportion of recorded sea lion deaths and injuries attributed to humans in one portion of the Archipelago (the island of San Cristóbal) rose dramatically between 2008 and 2012 (Denkinger et al. 2014, 2015). Sea lion pup mortality is also much higher in colonies that live near human settlements than it is in colonies that live on islands uninhabited by humans, perhaps because infectious diseases have been transmitted from domestic animals to sea lions (Denkinger et al. 2017). But such studies only consider deaths and injuries that are directly caused by human activity (e.g. intentional killing of sea lions, injuries caused by dog attacks or fishing equipment). Much less is known about how exposure to humans may indirectly affect the well-being of sea lions – by altering their behavior, stress levels or reproductive habits.

Researchers have documented such indirect effects of exposure to humans in other sea lion species, usually by observing sea lions' behavioral reactions to being approached by researchers or tourists, either on foot or by boat. Some species, such as the Steller sea lion Eumetopias jubatus, react dramatically to human approach. Individuals resting at haul-out sites make agitated calls and often retreat into the water when researchers approach them (Lewis 1987, Kucey 2005). Such disturbances – if they occur frequently – may reduce the amount of time that individual sea lions spend resting on land to recover from hunting, or affect the quality of care that mothers provide to their pups (Kovacs and Innes 1990, Jansen et al. 2015).

Other sea lion species appear more resilient to human presence, at least in the short term. Holcomb et al. (2009) conducted an approach study of California sea lions Zalophus californianus hauled-out on an uninhabited island in the Gulf of California and observed little to no behavioral responses (but see French et al. 2011). A study of Australian sea lions Neophoca cinerea on two different islands (one that allows public beach access and one that does not) found small but measurable differences in the frequency of aggressive behavioral reactions from sea lions toward tourists across the two sites (Osterrieder et al. 2016). Given this variation in behavioral responses across species, assessments of how sea lions react to humans should be done on a species-by-species basis (Kucey and Trites 2006). Although Galápagos sea lions are generally believed to be less reactive to humans than other sea lion species, this has not been empirically tested. Species-specific assessments are especially important for Galápagos sea lions because many of them they have closer contact with humans than do members of other sea lion species.

Prior attempts at environmental management in the Galápagos have avoided actively involving the local community in designing management protocols, instead often imposing protocols on the community without explanation (Weisberg et al. 2020). As a result, the local community often views environmental management protocols as annoying disturbances in their daily lives and do not take them entirely seriously. Citizen science offers a powerful opportunity to involve the local community conservation efforts. Community Science, a type of citizen science characterized by the local community being involved in data collection with the goal of affecting policy or decision-making (Bonney et al. 2016), is likely to be especially effective in promoting deep engagement with Galapagueños. A potential side benefit of this project is that the participating students may feel more motivated to engage in conservation as a result of learning more about the endangered species.

In order to understand how living alongside humans affects the behavior of Galápagos sea lions, we conducted a Community Science study on one of the largest breeding colonies in the Galápagos – known as El Malecón – which has seven haul-out sites in and around Puerto Baquerizo Moreno, a town of 8000 people on San Cristóbal Island. We and a team of 28 local high school students observed sea lions at four of these haul-out sites. All these sites are in or adjacent to Puerto Baquerizo Moreno's urban zone, but the types and amount of human activity varies from site to site.

We expected that if exposure to humans affects the behavior of Galápagos sea lions, then we would observe variation in sea lion behavior across the four sites. In particular, we expected that if human disturbances are stressful for sea lions, then this stress would manifest itself in more aggressive sea lion behavior, both toward humans and toward one another, at haul-out sites occupied by greater numbers of people. At the same time, mammals living in areas with lots of human visitors often decrease their ‘antipredator’ responses to humans (Neuhaus and Mainini 1998, Magle et al. 2005), so we also considered the possibility that sea lions would be less reactive to human approach at haul-out sites occupied by more people.

We also recorded sea lion group size (the number of neighboring sea lions resting near any given individual) and predicted that large numbers of people at a site would cause sea lions to crowd together in larger groups than at sites with fewer people. Finally, we observed instances of calling, growling, barking and challenging. Three of these behaviors (growling, barking and challenging) are aggressive behaviors. We predicted that at sites with more people, we would observe more of these aggressive behaviors directed towards both humans and other sea lions.

Methods

Study sites and setup

Twice per week, between June and December of 2017 and 2018, we and a group of Community Scientists conducted observations. These Community Scientists were International Baccalaureate students at the UAE-San Cristóbal school who participated in Project LAVA, an initiative led by the Galápagos Education and Research Alliance (Weisberg et al. 2020). A team of graduate and undergraduate students from the University of Pennsylvania spent six weeks at the beginning of each field season training the community scientists and ensuring their mastery of the observation protocol. The participation of these community scientists (12 students in 2017 and 18 students in 2018) allowed us to observe Galápagos sea lion behavior for six full months each field season. Typically, behavioral observations of this species range from only two weeks to three months per field season (Wolf and Trillmich 2007).

In 2017, we conducted observations on three beaches (Fig. 1): Playa Mann (0°53′44″S, 89°36′33″V ∼2350 m²), Playa de Oro (0°53′59S, 89°36′34″ ∼1800 m²) and Playa Zona Naval (0°54′07′S, 89°36′51″V ∼2450 m²). In 2018, we added a fourth beach, Playa de los Marinos (0°54′09″S, 89°36′47″V, ∼3550 m²). During each of our observations, we counted the number of people at each site. We used the average number of people at each site over the course of both field seasons as a proxy for each site's level of human disturbance. We acknowledge that the sites likely varied in other ways besides the level of human disturbance, but we feel that our approach is a good first step in exploring whether sea lion exhibit behavioral differences across different sites and a similar measure of human disturbance has been used to study Australian sea lions living on Carnac Island (Orsini et al. 2006) and in a comparison of Australian sea lions on Carnac Island and Seal Island (Osterrieder et al. 2016).

Figure 1.

Map of Puerto Baquerizo Moreno showing the four El Malecón colony haul-out sites included in this study.

Playa Mann is a beach that locals and tourists use for recreation year-round. It is by far the most human-disturbed of all El Malécon's haul-out sites. Naturalist guides bring groups of tourists here for swimming and sunning, and there are multiple food vendors, as well as outdoor showers, on the beach itself. It is common to observe visitors violating Galápagos National Park rules by approaching sea lions to less than 2 m to tease or photograph them. Playa de los Marinos is primarily used by fishermen for repairing boats. It is visited occasionally by tourists and locals, but sea lions hauled out see fewer humans than they do at Playa Mann. Playa de Oro is a launching site for kayaks and paddleboards adjacent to several busy hotels and restaurants. There is frequent foot traffic on a boardwalk running by the beach, but humans rarely spend time working, relaxing or playing on the beach itself. Zona Naval is inside a navy base and is rarely visited by locals or tourists. Due to its proximity to the navy base, this is the colony's least human-disturbed haul-out site. A road runs along the beach, but is set back several meters, and the foot and vehicle traffic along the road is infrequent compared to the traffic along the waterfront outside of the navy base.

We assigned numbers to all sea lions hauled out at a site and then assigned 4–5 of the numbered sea lions to each observer. If there were more sea lions than five times the number of observers (5–10 depending on the site), we preferentially chose to include sea lions that were easiest to approach (e.g. those basking on sand rather than on rocks). Once we had chosen the focal individuals (25–50 per observation, depending on the number of observers) for the observation and assigned specific sea lions to each observer, the observation protocol proceeded in three parts: an approach assay, a survey of age, sex and group size, and finally, a 15-min behavioral observation period.

Results

Behavioral observations

We recorded 422 calls across 2017 and 2018 (Table 3). Site, age and sex were significant, but group size was not (calls ∼ site + age + sex, random = date, family = quasi-Poisson; Supplementary material Appendix l Table A3). Post hoc tests revealed that sea lions called significantly fewer times on Playa Zona Naval than Playa de Oro. Females called more often than males. Pups called more than juveniles and there was no difference in the number of calls between pups and adults or juveniles and adults.

We recorded a total of 1311 growls (Table 3). Group size, age and sex were significant, but site was not (growls ∼ group size + age + sex, random = date, family = quasi-Poisson; Supplementary material Appendix l Table A3). Post hoc tests revealed that adult sea lions growled significantly more than pups or juveniles. There was no difference in the number of growls between pups and juveniles. Female sea lions growled more than males. The relationship between the number of growls and group size was positive, suggesting that sea lions growled more often when in larger groups.

Table 1.

A summary of likelihood ratio tests evaluating the significance of fixed effects in GLMMs on the results for approach assay reactions.

Table 2.

A summary of GLM results on group size.

We recorded a total of 216 challenges (Table 3). Group size was significant, but site, age and sex were not (challenges ∼ group size, random = date, family = quasi-Poisson; Supplementary material Appendix l Table A3). The relationship between group size and the number of challenges was positive, suggesting sea lions challenged more often when in larger groups.

We recorded 203 total barks (Table 3). Because typically only adult male sea lions bark, we did not include age or sex in the GLMs. We found that site and group size were significant (barks ∼ site + group size, random = date, family = quasi-Poisson; Supplementary material Appendix l Table A3). Post hoc tests revealed that sea lions barked more often on Playa de Oro than Playa Zona Naval. The relationship between group size and the number of barks was negative, suggesting that sea lions barked more often when in smaller groups.

We observed a total of 226 aggressive behaviors (barks, growls and challenges, Table 3) directed towards humans. Group size, age and sex were significant, but site was not (aggression towards humans ∼ group size + age + sex, random = date, family = quasi-Poisson; Supplementary material Appendix l Table A3). Post hoc tests revealed that both male and female sea lions were more aggressive towards humans than sea lions of unknown sex, but there was no difference between male and female sea lions. Adult sea lions were more aggressive towards humans than either juveniles or pups but there was no difference between juveniles and pups. The relationship between the number of aggressive acts towards humans and group size was negative, suggesting that sea lions were more aggressive towards humans when in smaller groups.

We observed a total of 1501 aggressive behaviors directed towards other sea lions (Table 3). We found that age and group size were significant but sex and site were not (aggression towards sea lions ∼ group size + age, random = date, family = quasi-Poisson; Supplementary material Appendix l Table A3). Post hoc tests revealed that adult sea lions were more aggressive towards other sea lions than either juveniles or pups but there was no difference between juveniles and pups. The relationship between aggression between sea lions and group size was positive, suggesting that sea lions were more aggressive towards other sea lions when in larger groups.

Discussion

Conservation of endangered animal populations requires an understanding of the effects of anthropogenic activity on health and survival. Here, we used a Community Science approach to compare Galápagos sea lion vocalizations, group size and reaction to human approach across four different haul-out sites which varied in their levels of human disturbance. We found that sea lions were less reactive to human approach on Playa Mann, the beach most disturbed by humans (Table 1, Fig. 2). We also found differences in group size across our study sites, but the differences did not track human disturbance (Table 2). Instead, group sizes were largest on the least disturbed beach and the most disturbed beach. Finally, we did not find variation across sites in the number of aggressive behaviors (growls, barks and challenges) directed towards either humans or other sea lions, but we did find that sea lion aggression towards humans decreased with group size, while aggression towards other sea lions increased with group size (Table 3).

Table 3.

A summary of recorded behaviors across sites, ages and sexes.

Unlike other pinniped species (Lovasz et al. 2008, Osterrieder et al. 2016), Galápagos sea lions responded least aggressively to human approach at the most disturbed haul-out site. One interpretation of this result is that sea lions who choose haul-out sites where there are large numbers of people become acclimated to the presence of people as a result of their site choice, making them less likely to react in an aggressive or agitated way when directly approached by a human. This study did not identify and track particular individual sea lions, but previous research on site fidelity has found that Galápagos sea lions do consistently return to the same haul-out sites (Wolf and Trillmich 2007), which would provide the occasion for acclimation. This finding is consistent with a recent meta-analysis which found that across mammals, birds and lizards, populations that live among humans are more tolerant of human presence than populations that do not (Samia et al. 2015). If Galápagos sea lions are indeed acclimating to human disturbance, this may have both positive and negative consequences. Acclimation can prevent or lessen stress due to human disturbance. But acclimation can also increase conflicts between humans and sea lions. Sea lions who are very comfortable around humans are more likely to occupy fishing boats, public parks and walkways, and waterfront businesses.

Figure 2.

Stacked bar plots showing the percentage of approach assay scores across sites (A), ages (B) and sexes (C).

Another possibility is that sea lions with a low tolerance for human presence simply avoid spending time at sites where there are large numbers of people. This is a concern because Galápagos sea lions exhibit long-term and fine-scale site fidelity. Females, in particular, develop preferences for particular spatial areas within haul-out sites. They return to these fine-scale sites year after year, and even appear to transmit preferences for specific sites to their daughters, which may also be a mechanism for transmitting social connections (Wolf and Trillmich 2007). Human disturbance may interfere with this transmission of haul-out site preferences. A daughter who is less tolerant of humans than her mother is, for example, may choose a haul-out site where there are fewer people, even if that means leaving her mother's preferred site and the social connections that come with it.

Our data does not allow us to discriminate between these two explanations – acclimation or low tolerance for human presence. But in a recent study of Galápagos sea lions on the uninhabited islet Caamaño, DeRango et al. (2019) found inter-individual differences in Galápagos sea lion pups' reactions to human approach. Their data suggests that tolerance for human presence varies among individual sea lions, and that these differences in tolerance emerge early in life and remain stable over time. These differences may well affect individual haul-out site choices later in life.

Our second main finding was that aggression towards humans decreases with group size, while aggression between sea lions (the number of growls, barks or challenges) increases with group size. The levels of aggression towards humans or other sea lions were not different across sites and therefore not likely directly linked to human disturbances at the haul-out sites. It is, however, possible that human activity not quantified by this study affects individual haul-out site choices and, by extension, group size at a site.

Although we did not attempt to quantify stress levels, increased aggression, either between sea lions or toward humans, can increase stress levels. Elevated stress levels are energetically taxing and can impair immune function (Eskesen et al. 2009). Aggression related to group size is, therefore, a concern, especially if group size is affected by competition over limited space due to a growing human population. This finding underscores the importance of protecting current haul-out sites and increasing the available space for sea lions to rest so that individuals can avoid crowding together. Indeed, Galápagos sea lions will readily use artificial floating platforms as resting places (Montero-Serra et al. 2014).

These results are relevant for future initiatives aimed at understanding and reducing the effect of anthropogenic activity on Galápagos sea lions. In addition to protecting existing haul-out sites and increasing possible resting areas, we suggest attempting to reduce the interactions between the human and sea lion populations. It is likely that most beach visitors are not aware they are potentially disturbing the sea lions. Signs and other educational material could be mounted near beaches, especially the most crowded areas, to improve awareness. Future studies might track individuals with the goal of determining whether sea lions are actually acclimating to human disturbance, or if sea lions with a low tolerance for humans simply avoid crowded beaches. Additionally, future studies should quantify stress levels across beaches with varying levels of human disturbance and across sea lions resting in groups of varying size. We hope that our Community Science approach will lead to more engagement with the local community, including involvement of Galapagueños in future environmental management decisions. Although the local communities are the biggest source of stress on the islands, they are also positioned to be the most effective protectors.