Peces Presas del Gaviotín chico (Sternula lorata), en costas del norte de Chile

Fish Prey of the Peruvian Tern (Sternula lorata), in northern coasts of Chile

Yerko A. Vilina, Beatriz Munizaga, Alvaro Neira-Soto & Frederic Toro

Facultad de Medicina Veterinaria, Universidad Santo Tomás, Santiago, Chile. E-mail: [email protected]

SUMMARY KEYWORDS .- Chile, Humboldt Current Peruvian tern, Sternula lorata,

INTRODUCTION Terns (Laridae, Sternine) form one of the bird groups most frequently used as environment indicators of marine ecosystems. One of the most studied aspects is for its trophic ecology. Foraging strategies are considered opportunistic - generalists (Aygen & Emslie 2006), which is reflected in studies describing more than 23 families of prey species (Jaquemet et al., 2008). Given that resources partition is frequent (Ashmole 1968, Rock et al. 2007), both prey species, such as their size and the feeding areas they use. There are some studies that compare their feeding ecology in different geographic locations (Jaquemet et al. 2008). Others considered seasonal changes in the diet, by correlating the change in the supply of prey to offspring regarding their ontogeny. Aygen & Emslie (2006) studied the diet of the juvenile Royal tern (Sterna maxima) on the East Coast of the United States, concluding that there are variations in the delivery of the species, as well as in the size of prey along the breeding season, prevailing smaller sizes at the beginning of the breeding season, and being displaced by larger classes at the end of the this breeding season.

Ramos (2000) recorded significant differences in the supply of prey chickens while studying Roseate tern in Aride Island, Seychelles, both between years and between seasons, finding that the species main prey is preserved with respect to secondary ones, in addition to be a correlation between the increase in the capture rate and the amount of food offered to the young terns (Aygen & Emslie 2006, Braby et al. 2011). As to the difference between the diet held by chickens in comparison to their parents, Lachlan et al. (2009), state that there are significant differences in the diversity and size of species offered to the chickens in comparison to their parents, with arrangements of size and/or prey species throughout the chicken ontogeny. Ashmole (1968) studied populations of five species of sympatric terns in Chritsman island, in the central Pacific, analyzing ecological segregation processes, associating differences in body size and terns peaks relative to the size of the prey. Something similar to the study of Rock et al. (2007) who compared the diet of two tern species that share the same nesting site but foraging different areas.

Many species in this group are considered to be threatened due to various factors, which are mainly anthropic, such as the loss and pollution of their habitats, the anthropic disturbance of their nesting sites, the introduction of non-native species, the eggs harvest, etc. In a global level, among all threatened species, it is the Chinese small tern, Sterna bernsteini, the one species under critical danger (CR) while fumarel terns, Sterna albostriata, and small terns, Sternula lorata, are classified as endangered species (EN) (IUCN/Birdlife International 2013).

The Peruvian tern, (Sternula lorata), is endemic to the Humboldt Current, which is distributed from the Gulf of Guayaquil in Ecuador, to the coasts of Antofagasta in Chile (Murphy 1936). This species would be living off the coast of Peru and northern Chile, while it would be a visitor in the center of Northern Ecuador during the breeding season rest (Chapman 1926, Harrison 1985, del Hoyo et al. 1996). Peruvian tern, have coastal habits, sometimes associated to the El Niño-Southern Oscillation (ENSO). Adult and subadult specimens have been observed in foraging activities at a distance of 25-200 km from the coast towards the sea (Mackiernan et al. 2001).

Their nesting habitat corresponds to coastal plains or dunes which go over two kms into the continent, where the specimens form colonies or can nesting solitarily (Del Hoyo et al., 1996). According Vilina (1998) and subsequent studies by this author, their breeding may occur between the months of August and January, in Chile.

Peruvian tern preys mainly on the coast; however, there are reports suggesting that their habits would not be strictly coastal and pelagic during El Niño-Southern Oscillation (Zavalaga et al. 2008). This tern species would feed mainly on small fish, and a small crustacean of the genus Euphasia type, being anchovy (Engraulis ringens) an important item in their diet (Murphy 1936). In Peru, Zavalaga et al. (2008) mentioned mackerels (Odonthestes regia regia), the mote sculpin, (Normanichthys crockery); and atlantic saury scombroides as food items in the nutrition of small terns.

MATERIALS AND METHODS The study area corresponds to the northern coast of Chile, from the north of Arica (18 ° 28'S - 70 ° 18'W) at the border of Chile and Peru to Mejillones (23 ° 10'S - 70 ° 25' W) in the south of Antofagasta, covering an area of approximately 650 km of coastline. Since the northern part of this area is not accessible by land, it is not well studied. This zone is part of the coast of the Atacama Desert, where rainfall is null or very little; however, it is more abundant in north of this area. The vegetation is almost nonexistent; and Peruvian tern nesting sites consist of coastal plains; which were prospected on foot and from a vehicle.

Between September and January of 2008 to early 2014, 14 coastal sites recorded as Peruvian tern nesting (Figure 1) were prospected; in seven of them, we and /or the keepers of the Foundation for Sustainability of Peruvian tern collected fish (n = 63) who had been abandoned by adult terns in colonies, or which had been regurgitated by chick in our presence. After the collection, they were identified in the laboratory according to the species level. These fish were probably caught by terns either during courtship or to feed the chick.

The prospected colonies were: southern Arica Airport, Pozo Toyo, southern Iquique Airport, Caramucho, Quinteros, Patillo, southern Puerto Patache Huanillo - Ike Ike, Playa Arenosa, Chipana, Cobija, Michilla, Guala Guala and Mejillones.

Figure 1. Breeding colonies or sighting sites of Peruvian tern in the northern coast of Chile.

For morphometric estimates of prey fish, a standard length was considered, as well as the maximum width and length of head. Because not all individuals were in good condition, the ranges were estimated based on a sample subset, from which a standard length could be taken (n = 58). The measurements were obtained with a bore known as calliper and an accuracy of +/- 1.0 mm.

RESULTS In the seven sites where samples were obtained, a total of 63 fish corresponding to four species belonging to four families were collected, all of them relatively small. We considered 58 of these specimens; given the conservation condition of the samples. The prey species (pictures 1, 2, 3, 4) were South pacific saury (Scomberesox saurus scombroides) (n = 29), Mote sculpins (Normanichthys crockery) (n = 12), Peruvian silversides (Odonthestes regia) (n = 9) and Paloma pompano (Trachinotus paitensis) (n = 8). The predominant prey species was short-beaked garfish, and Guala Guala was the place where the greatest amount of individuals (n = 11) were collected. Short-Beaked Garfish was also the most frequently recorded species (6/7 sites). However the species covering a greater latitudinal range was the mote sculpin; registered at both ends of the study area (Table 1). The fish obtained from what chicks regurgitated, and were found inside the colony. Short- beaked garfish were identified four times and silversides were identified twice. Guala Species Arica Pozo Toyo Chipana Michilla Guala Hornitos Mejillones

South Pacific saury 1 5 1 11 7 5 Mote sculpin 4 1 2 5 Peruvian Silverside 5 2 1 1 Paloma pompano 1 5 1 1 10 1 13 3 12 8 12

Note: The mote sculpin specimen from Pozo Toyo was not considered in morphometry, since it was incomplete. Table 1. Prey species per register site in the study area.

Among the 58 prey species measured, South pacific saury was the biggest one (97.05±12,07mm), followed by Mote sculpin (n=12), (75.3± 12,73mm), Peruvian silverside (n=9) (74.80±19, 69 mm) and Paloma pompano (n=8), being this species the one with the average smallest sizes (54.10±8,53mm) (Table 2). The widest total rank (head-tail) in all the captured prey species varied from 41, 0 to 128,6mm.

Total Minimum Maximun Species N° of samples Length Length Length Head Length

South pacific saury 29 97,0 81,0 128,6 25,8 Mote sculpins 12 75,3 42,0 90,1 20,5 Peruvian Silverside 9 74,8 57,0 123,2 16,4 Paloma Pompano 8 54,1 41,0 60,9 14,2

Table 2. Morphometric sizes of the prey species found in integral conditions, and which could be measured. As for the size ranges of the preys found inside the breeding colonies of Peruvian tern, Fig. 2 shows that most of the dams presented an intermediate size range, between 70 and 100 mm total length (60%). There is no bias and their distribution approaches the Normal distribution.

Figure 2. Number of fish according to size rank.

DISCUSSION AND CONCLUSIONS

This is the first report on the diet of small terns on the Chilean coast. During the breeding season the Peruvian tern captured at least four species of fish to feed their chick or to use them during courtship and the establishment of couples. The information we provide is a significant advance in understanding the feeding ecology of Peruvian tern in Chile, as anchovy and a small crustaceans of the genus Euphasia were previously mentioned only as potential preys (Murphy 1936, Goodall et al., 1951). When it comes to Perú, Zavalaga et al. (2008) indicated three of the four fish species recorded during this study as prey, except butterfish, which was collected by us at four sites, including the colony of Arica, at the northern border with Peru. It is important to highlight the fact that the recorded species show coastal habits in their juvenile forms, as well as in the case of short-beaked garfish; therefore their capture might be occurring in this habitat. Considering the size range of the prey fish collected, it is likely that all these species are part of the food item of the chicks during the breeding in the colony, as the largest species regurgitated by the young specimens was the short beaked garfish. However, this should be confirmed by other methods.

According to our field recordings, Peruvian tern only occasionally foraging near the coast where breeding colonies are; generally they must prey far from the coast or far away from nesting colonies. Therefore, their regular foraging areas are not well established. They co-exists with at least two species of terns which are observed with relative frequency: the elegant tern, Sterna elegans, a sort of summer visitor coming from California and the Inca tern Larosterna, a resident species: The diet of both species and the potential interactions of competition for prey are unknown in this area.

It is noticeable the fact that anchovy is absent in the diet, since some authors mention it as one of the main preys, but without providing further information (Murphy 1936, Guerra-Correa 2003). We have not recorded evidence of krill consumption (Euphausia spp), which is mentioned by Murphy (1936). The diet of Peruvian tern studied in the area was similar to that reported by Zavalaga et al. (2008) in the coast of Peru; and similar to the sizes recorded for other species of small terns, California least tern, Least Tern (Elliot et al. 2007) little tern, Sterna albifrons in Portugal (Catry et al. 2006), and the Damara tern, Sterna balaenarum in Namibia (Braby et al. 2011). In the winter ground, in northern Ecuador, Hasse & Ahlman (pers. comm.) recorded these terns feeding actively on the coast, between May and October, but also in indoor artificial pools. However, their diet is unknown. Therefore, it is possible that the diet of adults and juveniles is different in the breeding areas and the winter ground. This study is an advance in the knowledge of the trophic ecology of this species, which is in serious risk due to various anthropogenic factors. It is necessary to establish Peruvian tern diet; both in the case of adults and chicks, their interannual changes, as well as the various colonies the offspring during ontogeny. Indirectly, it could be attempted to quantify the offer in their foraging during the reproduction of the species.

ACKNOWLEDGEMENTS To Valeria Sabaj, Franco Cruz, Paola Sáez, Jorge Gibbons, Hernán Cofré, Carlos Garín and Juan Capella for their support on the field. To Jürgen Rottmann and the rangers in the Foundation for the Sustainability of Small Tern, which provided the fund for this study.

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