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Reyes-Arriagada, R., L. Hiriart-Bertrand, V. Riquelme, A. Simeone, K. Pütz, B. Lüthi, and A. Raya Rey. 2013. Population trends of a mixed-species colony of Humboldt and Magellanic Penguins in southern Chile after establishing a protected area. Avian Conservation and Ecology 8(2): 13.
Population Trends of a Mixed-Species Colony of Humboldt and Magellanic Penguins in Southern Chile after Establishing a Protected Area
Tendance d’une colonie mixte de Manchots de Humboldt et de Manchots de Magellan dans le sud du Chili à la suite de l’établissement d’une aire protégée
1Instituto de Zoología, Instituto de Ecología y Evolución, Facultad de Ciencias, Universidad Austral de Chile, 2Center for Marine Biodiversity and Conservation, Scripps Institution of Oceanography, University of California San Diego, 3Instituto de Zoología, Facultad de Ciencias, Universidad Austral de Chile, 4Departamento de Ecología y Biodiversidad, Facultad de Ecología y Recursos Naturales, Universidad Andrés Bello, 5Antarctic Research Trust, c/o Zoo Zürich, 6Consejo Nacional de Investigaciones Científicas y Técnicas, CADIC
Worldwide marine protected areas (MPAs) have been designated to protect marine resources, including top predators such as seabirds. There is no conclusive information on whether protected areas can improve population trends of seabirds when these are further exploited as tourist attractions, an activity that has increased in past decades. Humboldt Penguins (Spheniscus humboldti
) and Magellanic Penguins (S. magellanicus
) breed sympatrically on Puñihuil Islets, two small coastal islands off the west coast of Chiloé Island (41° S) in southern Chile that are subject to exploitation for tourism. Our goal was to compare the population size of the mixed colony of Humboldt and Magellanic Penguins before and after protection from unregulated tourism and freely roaming goats in 1997. For this purpose, two censuses were conducted in 2004 and 2008, and the numbers compared with those obtained in 1997 by other authors. The proportion of occupied, unoccupied, and collapsed/flooded burrows changed between years; there were 68% and 34% fewer collapsed burrows in 2004 and 2008, respectively, than in 1997. For the total number of burrows of both species, we counted 48% and 63% more burrows in 2004 and 2008, respectively, than in 1997. We counted 13% more burrows of Humboldt Penguins in 2008 than in 1997, and for Magellanic Penguins, we estimated a 64% increase in burrows in 2008. Presumably, this was as a result of habitat improvement attributable to the exclusion of tourists and the removal of goats from the islets. Although tourist visits to the islets are prohibited, tourism activities around the colonies are prevalent and need to be taken into account to promote appropriate management.
Les aires marines protégées ont été établies à l’échelle mondiale pour protéger les ressources marines, dont les prédateurs au sommet de la chaîne alimentaire comme les oiseaux marins. Rien n’indique de façon concluante que la protection d’aires permet une hausse des populations d’oiseaux marins dans les cas où ces populations représentent toujours une attraction touristique, activité dont la popularité a augmenté au cours des dernières décennies. Les Manchots de Humboldt (Spheniscus humboldti) et les Manchots de Magellan (S. magellanicus) nichent de façon sympatrique sur les îlots Puñihuil, deux petites îles au large de la côte ouest de l’île de Chiloé (41° S.) qui font l’objet de visites touristiques dans le sud du Chili. L’objectif de notre étude était de comparer la taille des deux populations de manchots avant et après l’établissement d’une réglementation touchant le tourisme et les chèvres en liberté en 1997. À cette fin, deux relevés ont été effectués en 2004 et 2008, et les résultats ont été comparés à ceux obtenus en 1997 par d’autres auteurs. La proportion de terriers occupés, non occupés ou effondrés/inondés a varié selon les années; ainsi, il y a eu 68 % et 34 % moins de terriers effondrés en 2004 et 2008, respectivement, qu’en 1997. Pour ce qui est du nombre de terriers des deux espèces, nous avons compté 48 % et 63 % plus de terriers en 2004 et 2008, respectivement, qu’en 1997. Nous avons compté 13 % plus de terriers de Manchots de Humboldt en 2008 par rapport à 1997, et avons observé une hausse de 64 % pour les terriers de Manchots de Magellan en 2008. Nous pouvons présumer que ces hausses résultent de l’amélioration de l’habitat consécutive à l’exclusion des touristes et au retrait des chèvres des îlots. Même si les visites touristiques sont maintenant interdites sur les îlots, l’activité touristique aux abords des colonies a toujours cours et doit être prise en compte si on veut mettre en place une gestion adéquate.
Key words: burrow activity; exclusion; protected area; Spheniscus humboldti; Spheniscus magellanicus; tourism
Historically, marine protected areas (MPAs) have been designated worldwide to protect marine resources, through fisheries management, habitat protection, and conservation of biodiversity (Boersma and Parrish 1999, Hooker and Gerber 2004). This includes top predators such as seabirds, one of the most important indicators of many aspects of the functioning of marine systems at regional and global scales and one of the most threatened groups of birds. At sea, the principal threats are pollution and interaction with fisheries, whereas on land these threats are constituted of alien invasive predators, habitat degradation, and human disturbance (Croxall et al. 2012). It has been suggested that MPAs benefit seabirds, allowing them to improve foraging effort (Louzao et al. 2006, Pichegru et al. 2010) and increasing breeding productivity (Frederiksen et al. 2008). Although the population trends of terrestrial birds have a positive correlation with protected habitats (Donald et al. 2007), there is no conclusive information on whether protected areas can improve population trends of seabirds when these areas are further exploited as tourist attractions. Tourism activities associated with seabird breeding colonies have been developed in several regions and have increased in past decades (Yorio et al. 2001a
). Tourism can result in disturbance to birds when the tourism activity is not controlled or is poorly managed (Carney and Sydeman 1999). These effects include reduced breeding success (Beale and Monaghan 2005), changes in nest distribution patterns (Anderson 1988, Hill and Rosier 1989), size trends in the breeding population (Barnes and Hill 1989), nest predation (Devney and Congdon 2009), loss or deterioration of habitat (Oro 2003, Martínez-Abraín et al. 2004), reduction in foraging activity and exclusion of birds from foraging areas (Velando and Munilla 2011), and changes in behavior (Anderson and Keith 1980, Burger and Gochfeld 1993). Thus, to ensure positive effects, MPAs require that the regulations exclude or restrict human activities that impact negatively on the resource (Frederiksen et al. 2008).
penguin colonies, in particular, are popular tourist destinations in Argentina and Chile (Simeone and Schlatter 1998, Skewgar et al. 2009, Villanueva et al. 2012). Negative effects such as reduced breeding success, lower fledging weights, changes in normal behavior, higher heart rates, lower nest densities, collapsed burrows, and higher levels of stress-induced hormones in penguins in frequently visited sites have been observed for various penguin species (Villanueva et al. 2012). The effect of tourist disturbance can vary from one species to another as in the Humboldt Penguin (Spheniscus humboldti
) and Magellanic Penguin (S. magellanicus
) because Humboldt Penguins are shier and more sensitive to human presence than Magellanic Penguins (Ellenberg et al. 2006). This is because Humboldt Penguins have been hunted by coastal human communities in northern Chile and Peru for more than 11,000 years, whereas Magellanic Penguins in the sparsely populated southern and eastern coasts of South America have never experienced selection pressure of a similar magnitude (Ellenberg et al. 2006 and references therein). Therefore, the effect of protecting areas in mixed-species colonies under exploitation by tourists may exert different responses in these penguin populations.
species, three mixed colonies are known, with the largest reported at Puñihuil Islets, two small coastal islands off the west coast of Chiloé Island (41° S) in southern Chile (Duffy 1987, Wilson et al. 1995, Simeone and Schlatter 1998). The biological relevance of this Humboldt/Magellanic Penguin colony was recognized by its potential for species hybridization, allowing studies of resource partitioning, behavioral interactions, diet comparisons, foraging ecology, and habitat use (Wilson et al. 1995, Simeone and Schlatter 1998, Raya Rey et al. 2013). At the time of its discovery in 1985, no threats were evident for this unique colony, and the site was not officially protected (Duffy 1987).
More than a decade after its discovery, the mixed-species population at Puñihuil was estimated at 561 adult Magellanic and 210 adult Humboldt Penguins. There was serious damage to the nesting burrows from trampling by goats introduced in 1988 and unregulated tourism (Simeone and Schlatter 1998). Trampling and overgrazing by goats alters the structure and composition of plant communities, causing habitat degradation and accelerating soil erosion (McChesney and Tershy 1998, Campbell and Donlan 2005 and references therein), which results in the collapse of breeding burrows of seabirds. In addition to this problem, and according to the local residents, mostly fishermen, these islands are the most accessible known places in Chile where the two penguin species breed, making this a very popular tourist attraction in Chiloé. This has resulted in an unknown number of people visiting the colonies while no regulations or management plans were in place. Regarding their conservation on the Pacific coast, populations of both species have been decreasing as a result of entanglement in artisanal fishing nets and illegal capture for consumption and bait (Simeone et al. 1999, Majluf et al. 2002, Pütz et al. 2011). In Argentina, human disturbance by tourism has been described as one of the main threats to the breeding colonies (Boersma 2009). As a result, the conservation status of these species is classified by Bird Life International as vulnerable for Humboldt Penguins (http://birdlife.org/datazone/speciesfactsheet.php?id=3862
) and near threatened for Magellanic Penguins (http://birdlife.org/datazone/speciesfactsheet.php?id=3863
). There is no information about population trends in the areas where the species occur in sympatry.
In 1999, the colonies became officially protected by the Chilean Forest Service (CONAF). The islets became a “Natural Monument,” subject to some regulations of MPAs (Guarderas et al. 2008). Access to the penguin colony was forbidden as a main restriction, and all the resident goats, of which there were at least six, were removed (Simeone and Schlatter 1998); however, tourist activities continued to occur around the islets through boat trips. Protection was reinforced by a nongovernmental organization, which provided constant surveillance and environmental education to locals. Following these conservation measures, the penguin population was expected to increase in numbers, but differentially between the species, with a greater increase for Magellanic Penguins, the less sensitive and less shy species. Our aim was to verify this expectation and accurately estimate the population sizes of both penguin species on the islets.
The Puñihuil Islets lie in the exposed Pacific Ocean off the Isla Grande de Chiloé (41°55′ S, 74°02′ W). Chico Islet and Grande Islet have areas of 1.54 and 2.65 ha, respectively, and are located 340 m and 700 m offshore, respectively (Fig. 1). Vegetation is composed mostly of understory bamboo (Chusquea
sp.), the bromeliads Fascicularia bicolor
and Greigia sphacelata
, which are in the central part of the islets, and herbaceous vegetation such as Holcus lanatus
and Anthoxantum odoratum
(Simeone and Schlatter 1998). We omitted the largest third islet known as Huiguape (4.45 ha) because of its inaccessibility. Today, there is intense tourist activity from guided boat tours around the islets, mainly during the austral spring and summer (Skewgar et al. 2009). Access ashore to the islets is still forbidden under the Natural Monument regulations. Chico Islet was the only islet with a population of goats until their removal in 1999 (Simeone and Schlatter 1998).
We conducted a complete nest census on both islets from 6 December to 8 December 2004 and again from 20 November to 30 November 2008, when the breeding activities of both species had already begun. At the time of the counts, the contents of the nests of both species ranged from incubating eggs to one to two chicks of up to five weeks, thus ensuring the distinction between an occupied and an unoccupied burrow. The counts were conducted between 1000 and 1600 local time following the methods described by Simeone and Schlatter (1998) from 26 February to 27 February 1997 at the same islets. Because both species were very sensitive to the presence of investigators (Fowler 1999), we counted and checked burrows only once, dividing the total area of every islet into smaller plots distinguished by topographic or vegetation marks and making transects inside to avoid double counting. We inspected each burrow, and its content was assigned to one of three categories according to its activity: (1) occupied burrows, those containing at least one adult with or without eggs, chicks, or their combinations; (2) unoccupied burrows, those with no adults inside and that were empty; and (3) flooded/collapsed burrows or those containing abandoned eggs that were outside of the nest. Because we were interested in the impact over all breeding stages of penguins, we did not distinguish between burrows with breeding pairs and burrows with single penguins. It is important to note that the latter were represented by 4.2% and 3.3% of the total burrow counts in 2008 in Chico and Grande Islets, respectively.
In 2004, nests were additionally categorized according to the substrate as (1) burrow constructed in soil, (2) rocky burrow, or (3) burrow in soil covered by vegetation. We also recorded the nest condition: collapsed or intact. Counts of collapsed burrows allowed the evaluation of the impact of goat removal. We conducted nest inspections with a flashlight and occasionally used a pole to move the bird carefully and determine nest contents. The examination of the burrow usually took a few seconds; thus, damage to the nest and its occupants was minimized.
In 2004 and 2008, we were only able to survey 90% of the total area on Grande Islet because there was an inaccessible dense cover of understory bamboo in the core zone of this islet, i.e., the same scenario as in 1997, resulting in an underestimation of the number of burrows beneath this zone. We compared the proportion of occupied, unoccupied, and collapsed/flooded burrows between 1997, 2004, and 2008.
We used contingency tables with the chi-square test to determine changes in the proportion of burrow count frequencies in different years. To determine changes in the proportion of occupied, unoccupied, and collapsed/flooded burrows, we used a 2 × 3 contingency table, and to determine changes in the proportion of species, we used a 2 × 2 contingency table, excluding hybrids and chicks alone, between 1997 and 2004 and between 2004 and 2008. To determine if the proportion of the substrate used by penguins changed between 1997 and 2004, we used a 2 × 4 contingency table for the observed frequencies of occupied, unoccupied, and collapsed/flooded Humboldt and Magellanic Penguin burrows.
Changes in the number of burrows
The total number of Magellanic and Humboldt Penguin burrows increased significantly on both islands (Table 1). Compared with 1997, the numbers increased by 48% and 63% in 2004 and 2008, respectively. With regard to individual islets, 28% and 60% more burrows were counted on Chico Islet, and 59% and 64% more burrows were counted on Grande Islet (Table 1).
The total number of occupied burrows also increased compared with 1997 levels; we estimated an increase of 55% and 60% in 2004 and 2008, respectively. On Chico Islet, we counted 51% and 82% more burrows for the same time period, and on Grande Islet, the increase was 57% and 48%, respectively (Table 1).
We counted 74% and 93% more unoccupied burrows in 2004 and 2008 compared with 1997. For Chico Islet, the increase was 66% and 110% for the same time period, and for Grande Islet, the increase was 77% and 87%, respectively (Table 1).
The total number of collapsed burrows on both islets decreased by 68% and 34% in 2004 and 2008, respectively, compared with 1997. However, although in 2008 this decrease reached 71% on Chico Islet, the number of collapsed burrows increased by 20% on Grande Islet (Table 1).
Magellanic and Humboldt Penguins after tourist/visitor exclusion and removal of goats
The relative proportion of burrows of the species changed only between 1997 and 2004 on Grande Islet (Table 2). The Magellanic:Humboldt ratio was 4:1, 5:1, and 4:1 in 1997, 2004, and 2008, respectively, on Chico Islet; whereas the ratio on Grande Islet was 4:1 in 1997 and 7:1 in the following years.
Overall, we counted 13% more burrows of Humboldt Penguins in 2008 than in 1997. On Chico and Grande Islets, we estimated 59% more and 12% fewer burrows, respectively, for the same time period (Table 2). For the Magellanic Penguin, we estimated an increase of 64% in burrows in 2008. This increase reached 78% and 57% on Chico Islet and Grande Islet, respectively. Moreover, for both islets in 2008 we recorded 30% fewer burrows with chicks alone and hybrids than in 2004 (Table 2).
In the 1997 and 2004 censuses, both penguin species mainly nested in soil, followed by burrows under bamboo and occasionally under bromeliads (Table 3). For occupied burrows, the proportion of use in the substrate changed significantly on Grande Islet with an increase of the bamboo substrate (χ
² = 11.76, p = < 0.01; Table 3), particularly for Magellanic Penguin burrows. On Chico Islet, the proportion of burrows by type of substrate changed significantly for the number of empty soil burrows (χ
² = 21.69; p = < 0.01), with an increase of 157%; whereas the number of collapsed/flooded soil burrows decreased by 287% in 2004 and 241% in 2008. Similarly, on Grande Islet, empty soil burrows increased by 52%, and collapsed/flooded burrows increased by 22% in 2004 and by 20% in 2008 compared with 1997 (Table 3).
Ecotourism, especially wildlife observation, has been a rapidly growing activity and has resulted in specifically designed activities with benefits to local and regional people and agencies. However, it has been acknowledged that visitation by people interested in the conservation of wildlife can have severe impacts on the wildlife itself (e.g., Boyle and Sampson 1985, Otley 2005). Colonial nesting seabirds are particularly vulnerable to disturbances (Carney and Sydeman 1999), and many wildlife-watching guidelines have been established, with varying success. We report on the recovery of a mixed colony of Humboldt and Magellanic Penguins at Puñihuil Islets, central Chile, following the establishment of guidelines and the removal of alien species from the habitat.
The increase in the total number of burrows after 1997 was assumed to be a direct consequence of the regulations imposed at that time. Compared with 1997, nest numbers for the entire mixed colony for 2004 and 2008 revealed that the increase in number of burrows was more pronounced, but in relative proportions similar, in Magellanic compared with Humboldt Penguins. Significant changes in the proportion of burrows between 1997 and 2004 in favor of Magellanic Penguins may reflect a faster recovery of this species after the regulations became established. This was supported by the fact that the proportion remained similar between 2004 and 2008, thus reflecting a balance in the breeding numbers of the penguin species compared with the numbers without human disturbance and goats. Ellenberg et al. (2006) reported that Humboldt Penguins are more affected by human disturbance than any other penguin species. In addition, Humboldt Penguins are smaller and arrive two to three weeks later in the colony than Magellanic Penguins (Simeone and Schlatter 1998) and are thus restricted in their nest site choices. Despite these disclaimers, it is evident that in species with a critical conservation status, smaller populations and life history affected by human disturbances, as in the case of Humboldt Penguins, the application of conservation measures is a useful tool to enhance their population status.
The magnitude of the total increase in breeding pair numbers was certainly a direct consequence of the conservation measures implied, but other factors may also have contributed to the observed increase. For example, the timing of the censuses has been different. The 1997 study, done almost three months later in the breeding season, included those occupied burrows containing molting adults and not necessarily all breeders, but it also excluded failed breeding attempts of birds that lost their eggs or chicks earlier in the season. However, these two factors positively and negatively influenced our results, and it thus appears that tourist exclusion and goat removal resulted at first in a significant increase in burrow numbers for both species in both colonies between 1997 and 2004, whereas this trend stabilized afterward.
There are a few examples supporting a positive relationship between seabird populations and the establishment of MPAs. For example, in the African Penguin (S. demersus
), the foraging effort decreased after the establishment of an MPA (Pichegru et al. 2010). Other examples include the enhancement of breeding distribution in the Black-footed Albatross (Phoebastria nigripes
; Hyrenbach et al. 2006), a population increase in the Kelp Gull (Larus dominicanus
; Yorio et al. 1998), the protection of breeding adults in Giant Petrels (Macronectes
sp.; Trebilco et al. 2008), and improvements of other aspects of life history, reviewed for marine megafauna by Hooker and Gerber (2004). We have demonstrated that the establishment of an MPA in a seabird colony perturbed by unregulated tourism and introduced goats resulted in an increase in the populations of two penguin species and presumably other seabird species breeding on the islets, e.g., the Red-legged Cormorant (Phalacrocorax gaimardi
) and the Kelp Gull.
Further conservation measures
So far, the long-term impact of regulated tourism on penguin populations has not yet been sufficiently established, mainly because of the lack of population trends described for other Spheniscus
colonies in South America exposed to tourism. However, the increasing number of unoccupied burrows after 1997 may mirror the dynamics between regulated tourism activity and penguin life history. In general, unoccupied burrows may be a result of nest desertion earlier in the breeding season (Yorio et al. 2001a
), but on the other hand, they offer the potential of reoccupancy by penguin recruits in the years to come. Skewgar et al. (2009) acknowledged a report from 2007 in which it was considered that current tourist visitations and logistics appeared sustainable; however, at the same time, the biological impacts of tourist numbers on penguin behavior and ecology were not considered. Taking into account that Spheniscus
species have high intraspecific breeding synchrony (e.g., S. magellanicus
, Yorio et al. 2001b
; S. demersus
, Wolfaardt et al. 2009), the number of unoccupied burrows is unlikely to be a result of temporal differences in the rate of occupancy of breeding burrows used by the penguins. Although there are other factors that may influence population trends in the long term, penguins in general have evolved to cope with oceanographic dynamics that define spatial-temporal variability of resources in the area, e.g., African Penguins (Pichegru et al. 2010). The natural scenario occurs when major events affecting resource availability, such as the El Niño Southern Oscillation, are absent. Therefore, we presume that the current penguin population trends may mirror the impact of ecotourism activities on this mixed-species colony. Although regulations imposed in 1997 have had a measurable effect on breeding pair numbers on the Puñihuil Islets, some threats still remain. To further increase the protection of the islets and their inhabitants, we propose the establishment of the following measures, in line with Skewgar et al. (2009):
- Reduce the number of tourists. An increase in the number of visitors to the islets may cause a decrease in breeding success or long-term physiological changes in penguins (Fowler 1999, Trathan et al. 2008, Lynch et al. 2010). In Puñihuil the number of visitors on touristic boats reached a total of 7000 in 2004 and increased to 20,000 in 2009 (Skewgar et al. 2009).
- Implement ecotourism management. Up until 2010, tourism increased without the application of concurrent control measures, which implies that activities disturbing the colony, such as unregulated touristic boat presence, may also have increased before this date.
- Control pollution increases. As tourism continues to increase, pollution affecting the marine ecosystem will also increase (Hardiman and Burgin 2010, Braun et al. 2012).
- Reduce the mortality of penguins in gill nets. Records indicate that 50 penguins drowned in 2006 (Skewgar et al. 2009) because of a group of Chilean croaker (Cilus gilberti) gill netters who were not participating in ecotourism.
Our data revealed a reduced number of collapsed burrows after nearly eight years of protection of the islets. This is mainly because of the removal of goats from Chico Islet (Simeone and Schlatter 1998). Obviously, islet protection has stimulated penguins to re-excavate collapsed burrows or to build new ones in sites previously affected by trampling. For the different types of substrate, the decrease in collapsed burrows and increase in burrows for both penguin species and for unoccupied burrows was greatest in the soil, mirroring more use of this type of substrate than vegetal or rock substrates because the proportions of the number of burrows in these habitats did not change between 1997 and 2004. Furthermore, collapsed burrows occurred only in the soil in 1997, probably because of the inaccessibility of dense vegetation to goats.
For the mixed-species colony at Puñihuil, the number of collapsed burrows on Grande Islet after 1997 and on both islands after 2004 may be considered as natural burrow collapse, which can result from intense rainfall in the area or from trampling by penguins (Simeone and Schlatter 1998) because goats were not introduced on this islet. These effects can be seen more clearly on Grande Islet where the soil was eroded in the absence of vegetation in a large part of the islet. The tourism activity could have influenced the proportion of occupied burrows between 1997 and 2004, when the increase in burrow numbers was greater in bamboo substrate than in soil, particularly for Magellanic Penguins. Soil burrows were located closer to the coast and were more exposed to boat presence than burrows in the bamboo because this type of substrate was located in the high central part of the islet, away from the coast. This is particularly marked in Humboldt Penguins, for which burrows decreased in soil substrate and increased in the bamboo habitat. Chatwin et al. (2013) reported that boat traffic can have severe effects on breeding or roosting seabirds. Despite some habituation responses, they recommend a minimum distance of 50 m for boats and kayaks around the coastline of sites used for ecotourism.
Additionally, the improved quality of the penguin nesting habitat is relevant because the quality of a site has a direct effect on current and future pair breeding success (Knight and Rogers 2004, Descamps et al. 2009). If the burrow has collapsed or flooded after the breeding season, the chance of mate fidelity will be reduced because fidelity is influenced by the ability to meet again at the nest in the following season (Yorio and Boersma 1994, Knight and Rogers 2004). Secondly, if the current breeding success is low, e.g., burrow collapse by trampling, the probability of pair divorce will be high (Dubois and Cézilly 2002, Setiawan et al. 2005).
Conservation and management
The penguin and seabird colonies at Puñihuil are attracting a significant number of ecotourists, with locals benefiting from this activity, e.g., fishing syndicates and private tour operators (Skewgar et al. 2009). The current activities at Puñihuil appear to be in line with good practices, i.e., those developed in a context of responsibility toward the environment, for the penguin colonies (but see Chatwin et al. 2013); however, there is a need to continue assessing the population trends of penguins and other seabirds. In addition, it is important to consider environmental variables that can affect penguin populations to discriminate between human and natural effects. Despite some regulations, like the local county ordinance that has regulated tourism activity around the islets in Puñihuil since 2009, human activities near the colonies are likely to constitute a source of behavioral and physiological stress for the penguins (Walker et al. 2005, 2008, Ellenberg et al. 2007, Chatwin et al. 2013). These perturbations could be reduced by limiting activities to certain areas of the colonies where birds could habituate to human presence (Fowler 1999). Nevertheless, this management must consider the susceptibility of the birds at critical stages, i.e., incubation and molt, when the energy stores of birds are low and any extra costs may influence their survival rates (Hood et al. 1998). Examples of negative impacts on seabird colonies attributable to poorly managed tourism are abundant (see Carney and Sydeman 1999 for a review), but there are also examples of sustainable coexistence between tourism and seabird conservation, particularly in penguin colonies (e.g., Boersma and Stokes 1995, Holmes 2007, Landau and Splettstoesser 2007, Powell et al. 2008). In this context, the effects of regulations like the ordinance that improved the management of tourism in Puñihuil will be reflected in the penguin populations in the middle and long term.
The second conservation challenge in protected penguin colonies is that protection must be compatible with research activities where the uniqueness of these colonies makes them highly attractive to studies of comparative ecology and potential interactions between the two species of penguins. Indeed, the development of scientific research can be of great value to tourism because the knowledge generated in the colonies could improve the quality of information for visitors, producing a “value-added” experience for tourists if traveling with expert guides. Moreover, the likelihood of success of management plans would also increase with the involvement of representatives from government, private, academic, and nongovernmental organizations. Therefore, after the establishment of a protected area, there is also a need to improve the management of habitats, both animal and human inhabitants, and habits, especially of humans; the latter is a crucial part of conservation planning.
Fieldwork during 2004 was funded by Zoo Landau in der Pfalz, Germany. Fieldwork during 2008 was funded by a research grant from the Antarctic Research Trust. Marcelo Flores and Sabine Dresmman provided valuable help in the field in 2004, and Francisco, Pedro, Pablo, Feña, and Galindo in 2008. The Otway Foundation team was of great help in coordinating logistics at Puñihuil in 2004, and Katja Siemund during 2008. CONAF provided permits to work at Puñihuil in 2004 and 2008. SUBPESCA (Undersecretariat of Chilean Fisheries) provided permits for handling penguins in 2008. Caitlin Scully, Kristina Malizia, and Claire Evans-Serandour improved the English of the manuscript. The manuscript was reviewed and language edited by a native English-speaking scientist. We are very grateful to all of them.
Anderson, D. W. 1988. Dose-response relationship between human disturbance and Brown Pelican breeding success. Wildlife Society Bulletin
Anderson, D. W., and J. O. Keith. 1980. The human influence on seabird nesting success: conservation implications. Biological Conservation
Barnes, A., and G. J. E. Hill. 1989. Census and distribution of Black Noddy Anous minutus
nests on Heron Island, November 1985. Emu
Beale, C. M., and P. Monaghan. 2005. Modeling the effects of limiting the number of visitors on failure rates of seabird nests. Conservation Biology
Boersma, P. D. 2009. The penguin maven. Wildlife Conservation
Boersma, P. D, and J. K. Parrish. 1999. Limiting abuse: marine protected areas, a limited solution. Ecological Economics
Boersma, P. D., and D. L. Stokes. 1995. Conservation: threats to penguin population. Pages 127-139 in
T. D. Williams, editor. The penguins
. Oxford University Press, Oxford, UK.
Boyle, S. A., and F. B. Samson. 1985. Effects of nonconsumptive recreation on wildlife: a review. Wildlife Society Bulletin
Braun, C., O. Mustafa, A. Nordt, S. Pfeiffer, and H.-U. Peter. 2012. Environmental monitoring and management proposals for the Fildes Region, King George Island, Antarctica. Polar Research
Burger, J., and M. Gochfeld. 1993. Tourism and short-term behavioural responses of nesting Masked, Red-footed, and Blue-footed, Boobies in the Galápagos. Environmental Conservation
Campbell, K., and C. J. Donland. 2005. Feral goat eradications on islands. Conservation Biology
Carney, K. M., and W. J. Sydeman. 1999. A review of human disturbance effects on nesting colonial waterbirds. Waterbirds
Chatwin, T. A., R. Joy, and A. E. Burger. 2013. Set-back distances to protect nesting and roosting seabirds off Vancouver Island from boat disturbance. Waterbirds
Croxall, J. P., S. H. M. Butchart, B. Lascelles, A. J. Stattersfield, B. Sullivan, A. Symes, and P. Taylor. 2012. Seabird conservation status, threats and priority actions: a global assessment. Bird Conservation International
Descamps, S., C. Le Bohec, Y. Le Maho, J.-P. Gendner, and M. Gauthier-Clerc. 2009. Relating demographic performance to breeding-site location in the King Penguin. Condor
Devney, C. A., and B. C. Congdon. 2009. Testing the efficacy of a boundary fence at an important tropical seabird breeding colony and key tourist destination. Wildlife Research
Donald, P. F., F. J. Sanderson, I. J. Burfield, S. M. Bierman, R. D. Gregory, and Z. Waliczky. 2007. International conservation policy delivers benefits for birds in Europe. Science
Dubois, F., and F. Cézilly. 2002. Breeding success and mate retention in birds: a meta-analysis. Behavioral Ecology and Sociobiology
Duffy, D. C. 1987. Three thousand kilometers of Chilean penguins. Explorers Journal
Ellenberg, U., T. Mattern, P. J. Seddon, and G. L. Jorquera. 2006. Physiological and reproductive consequences of human disturbance in Humboldt Penguins: the need for species-specific visitor management. Biological Conservation
Ellenberg, U., A. N. Setiawan, A. Cree, D. M. Houston, and P. J. Seddon. 2007. Elevated hormonal stress response and reduced reproductive output in Yellow-eyed Penguins exposed to unregulated tourism. General and Comparative Endocrinology
Fowler, G. S. 1999. Behavioural and hormonal responses of Magellanic Penguins (Spheniscus magellanicus
) to tourism and nest site visitation. Biological Conservation
Frederiksen, M., H. Jensen, F. Daunt, R. A. Mavor, and S. Wanless. 2008. Differential effects of a local industrial sand lance fishery on seabird breeding performance. Ecological Applications
Guarderas, A. P., S. D. Hacker, and J. Lubchenco. 2008. Current status of marine protected areas in Latin America and the Caribbean. Conservation Biology
Hardiman, N., and S. Burgin. 2010. Recreational impacts on the fauna of Australian coastal marine ecosystems. Journal of Environmental Management
Hill, G., and J. Rosier. 1989. Wedge-tailed Shearwaters, White-capped Noddies and tourist development on Heron Island, Great Barrier Marine Park. Journal of Environmental Management
Holmes, N. D. 2007. Comparing King, Gentoo, and Royal Penguin responses to pedestrian visitation. Journal of Wildlife Management
Hood, L. C., P. D. Boersma, and J. C. Wingfield. 1998. The adrenocortical response to stress in incubating Magellanic Penguins (Spheniscus magellanicus
Hooker, S. K., and L. R. Gerber. 2004. Marine reserves as a tool for ecosystem-based management: the potential importance of megafauna. BioScience
Hyrenbach, K. D., C. Keiper, S. G. Allen, D. G. Ainley, and D. J. Anderson. 2006. Use of marine sanctuaries by far-ranging predators: commuting flights to the California Current System by breeding Hawaiian albatrosses. Fisheries Oceanography
Knight, C., and T. Rogers. 2004. Factors influencing fledgling production in Little Penguins (Eudyptula minor
). Wildlife Research
Landau, D., and J. Splettstoesser. 2007. Management of tourism in the marine environment of Antarctica: the IAATO perspective. Tourism in Marine Environments
Louzao, M., K. D. Hyrenbach, J. M. Arcos, P. Abelló, L. G. de Sola, and D. Oro. 2006. Oceanographic habitat of an endangered Mediterranean procellariiform: implications for marine protected areas. Ecological Applications
Lynch, H. J., W. F. Fagan, and R. Naveen. 2010. Population trends and reproductive success at a frequently visited penguin colony on the western Antarctic Peninsula. Polar Biology
Majluf, P., E. A. Babcock, J. C. Riveros, M. A. Schreiber, and W. Alderete. 2002. Catch and bycatch of sea birds and marine mammals in the small-scale fishery of Punta San Juan, Peru. Conservation Biology
Martínez-Abraín, A., B. Sarzo, E. Villuendas, M. A. Bartolomé, E. Mínguez, and D. Oro. 2004. Unforeseen effects of ecosystem restoration on Yellow-legged Gulls in a small western Mediterranean island. Environmental Conservation
McChesney, G. J., and B. R. Tershy. 1998. History and status of introduced mammals and impacts to breeding seabirds on the California Channel and Northwestern Baja California Islands. Colonial Waterbirds
Oro, D. 2003. Managing seabird metapopulations in the Mediterranean: constraints and challenges. Scientia Marina
Otley, H. M. 2005. Nature-based tourism: experiences at the Volunteer Point penguin colony in the Falkland Islands. Marine Ornithology
Pichegru, L., D. Grémillet, R. J. M. Crawford, and P. G. Ryan. 2010. Marine no-take zone rapidly benefits endangered penguin. Biology Letters
Powell, R. B., S. R. Kellert, and S. H. Ham. 2008. Antarctic tourists: ambassadors or consumers? Polar Record
Pütz, K., L. Hiriart-Bertrand, A. Simeone, V. Riquelme, R. Reyes-Arriagada, and B. Lüthi. 2011. Entanglement and drowning of a Magellanic Penguin (Spheniscus magellanicus
) in a gill net recorded by a time-depth recorder in south-central Chile. Waterbirds
Raya Rey, A., K. Pütz, A. Simeone, L. Hiriart-Bertrand, R. Reyes-Arriagada, V. Riquelme, and B. Lüthi. 2013. Comparative foraging behaviour of sympatric Humboldt and Magellanic Penguins reveals species-specific and sex-specific strategies. Emu
Setiawan, A. N., M. Massaro, J. T. Darby, and L. S. Davis. 2005. Mate and territory retention in Yellow-eyed Penguins. Condor
Simeone, A., M. Bernal, and J. Meza. 1999. Incidental mortality of Humboldt Penguins Spheniscus humboldti
in gill nets, central Chile. Marine Ornithology
Simeone, A., and R. P. Schlatter. 1998. Threats to a mixed-species colony of Spheniscus
penguins in southern Chile. Colonial Waterbirds
Skewgar, E., A. Simeone, and P. D. Boersma. 2009. Marine reserve in Chile would benefit penguins and ecotourism. Ocean & Coastal Management
Trathan, P. N., J. Forcada, R. Atkinson, R. H. Downie, and J. R. Shears. 2008. Population assessments of Gentoo Penguins (Pygoscelis papua
) breeding at an important Antarctic tourist site, Goudier Island, Port Lockroy, Palmer Archipelago, Antarctica. Biological Conservation
Trebilco, R., R. Gales, G. B. Baker, A. Terauds, and M. D. Sumner. 2008. At sea movement of Macquarie Island Giant Petrels: relationships with marine protected areas and regional fisheries management organisations. Biological Conservation
Velando, A., and I. Munilla. 2011. Disturbance to a foraging seabird by sea-based tourism: implications for reserve management in marine protected areas. Biological Conservation
Villanueva, C., B. G. Walker, and M. Bertellotti. 2012. A matter of history: effects of tourism on physiology, behaviour and breeding parameters in Magellanic Penguins (Spheniscus magellanicus
) at two colonies in Argentina. Journal of Ornithology
Walker, B. G., P. D. Boersma, and J. C. Wingfield. 2005. Physiological and behavioral differences in Magellanic Penguin chicks in undisturbed and tourist-visited locations of a colony. Conservation Biology
Walker, B. G., J. C. Wingfield, and P. D. Boersma. 2008. Tourism and Magellanic Penguins (Spheniscus magellanicus
): an example of applying field endocrinology to conservation problems. Neotropical Ornithology
Wilson, R. P., D. C. Duffy, M. P. T. Wilson, and B. Araya. 1995. Aspects of the ecology of species replacement in Humboldt and Magellanic Penguins in Chile. Le Gerfaut
Wolfaardt, A. C., L. G. Underhill, and J. Visagie. 2009. Breeding and moult phenology of African Penguins Spheniscus demersus
at Dassen Island. African Journal of Marine Science
Yorio, P., M. Bertellotti, P. Gandini, and E. Frere. 1998. Kelp Gulls Larus dominicanus
breeding on the Argentine coast: population status and relationship with coastal management and conservation. Marine Ornithology
Yorio, P., and P. D. Boersma. 1994. Causes of nest desertion during incubation in the Magellanic Penguin (Spheniscus magellanicus
Yorio, P., E. Frere, P. Gandini, and A. Schiavini. 2001a
. Tourism and recreation at seabird breeding sites in Patagonia, Argentina: current concerns and future prospects. Bird Conservation International
Yorio, P., P. García-Borboroglu, J. Potti, and J. Moreno. 2001b
. Breeding biology of Magellanic Penguins Spheniscus magellanicus
at Golfo San Jorge, Patagonia, Argentina. Marine Ornithology