AMZ vol 19 (2021) pp 161-181

Arxius de Miscel·lània Zoològica, 19 (2021): 161–181

Vilca1698–0476 Taco et al.

ISSN:

Seabird temporal composition, abundance and habitat use in Punta La Metalera (Arequipa, Southern Peru) L. M. Vilca Taco, E. Mamani T., C. R. Luque–Fernández

Vilca Taco, L. M., Mamani T., E., Luque–Fernández, C. R., 2021. Seabird temporal composition, abundance and habitat use in Punta La Metalera (Arequipa, Southern Peru). Arxius de Miscel·lània Zoològica, 19: 161–181, Doi: https://doi.org/10.32800/amz.2021.19.0161 Abstract Seabird temporal composition, abundance and habitat use in Punta La Metalera (Arequipa, Southern Peru). Islands, islets, and guano capes provide a unique variety of habitats for seabirds. Their variability determines the structure and dynamics of the community. Studies about the temporal diversity and habitat use of these systems in southern Peru are lacking. The aim of this study was to analyze the abundance, composition, and behavior of seabirds at Punta La Metalera (El Faro) in the province of Islay in the Arequipa region of southern Peru. We recorded a total of 12 species. One of these is endemic to the Peruvian coast (Cinclodes taczanowskii), one is considered in endangered (Spheniscus humboldti), and four have been assigned near threatened status (Phalacrocorax gaimardi, Pelecanus thagus, Sula variegata and Larosterna inca). Some of these birds belong to the guano bird group. Laridae was the most abundant family due to Larosterna inca, which showed the highest number of individuals. Temporal variation showed that species were most abundant in December and January. The habitat was mainly used for resting, preening, and feeding.

However, nesting was also recorded for six species. Based on the little information previously available for this region our findings indicate that Punta La Metalera is an important area for the development and reproduction of some of the species recorded.

Data published through GBIF (Doi: https://doi.org/10.15470/9umyvz) Key words: Diversity, Land–use, Seabird, Behavior, Disturbances, Larosterna inca Resumen Variación temporal de la diversidad, abundancia y uso del hábitat de las aves marinas en Punta La Metalera (Arequipa, al sur de Perú). Los sistemas de islas, islotes y puntas guaneras proporcionan una extraordinaria y amplia variedad de hábitats, única para las aves marinas. Esta variabilidad determina la estructura y dinámica de la comunidad. Hay pocos estudios sobre variación de la diversidad en el tiempo o sobre uso del hábitat por parte de las aves en estos sistemas del sur de Perú. Con este objetivo analizamos estos parámetros en la Punta La Metalera (El Faro) desde octubre de 2019 a marzo de 2020 en un cabo de Islay, Arequipa, al sur de Perú. En total registramos un total de 12 especies,

© [2021] Copyright belongs to the authors, who license the journal Arxius de Miscel·lània Zoològica to publish the paper under a Creative Commons Attribution 4.0 License, which permits its distribution, and reproduction in any medium, provided the original authors and source, the journal Arxius de Miscel·lània Zoològica, are cited.

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incluida una endémica de la costa peruana (Cinclodes taczanowskii), una con estatus de amenazada, Spheniscus humboldti, y otras cuatro con estatus de casi amenazadas (Phalacrocorax gaimardi, Pelecanus thagus, Sula variegata y Larosterna inca) correspondiendo algunas de ellas al grupo de aves guaneras. En cuanto a la abundancia, la familia Laridae fue la más abundante, destacando Larosterna inca con el mayor número de individuos; la fluctuación temporal evidencia una mayor abundancia de especies durante los meses de diciembre y enero. Los principales usos del hábitat fueron el descanso, el arreglo de las plumas con el pico y la alimentación. No obstante, los registros de anidamiento de seis especies también sugieren este uso. Esta área tiene una importancia significativa para el desarrollo de las especies aquí registradas dada la escasa información disponible sobre la costa sur, el tamaño poblacional y la reproducción de algunas de las especies registradas.

Datos publicados en GBIF (Doi: https://doi.org/10.15470/9umyvz) Palabras clave: Diversidad, Uso del suelo, Aves marinas, Comportamiento, Perturbaciones, Larosterna inca Resum Variació temporal de la diversitat, abundància i ús de l'hàbitat dels ocells marins a Punta La Metalera (Arequipa, al sud del Perú). Els sistemes d'illes, illots i puntes guaneres proporcionen una extraordinària i àmplia varietat d'hàbitats, única per als ocells marins. Aquesta variabilitat determina l'estructura i la dinàmica de la comunitat. Hi ha pocs estudis sobre variació de la diversitat en el temps o sobre ús de l'hàbitat per part dels ocells en aquests sistemes del sud del Perú. Amb aquest objectiu vam analitzar aquests paràmetres a la Punta La Metalera (El Faro) des d'octubre de 2019 a març de 2020 en un cap d'Islay, Arequipa, al sud del Perú. En total vam registrar un total de 12 espècies, entre les quals una d'endèmica de la costa peruana (Cinclodes taczanowskii), una amb estatus d'amenaçada, Spheniscus humboldti, i quatre amb estatus de gairebé amenaçades (Phalacrocorax gaimardi, Pelecanus thagus, Sula variegata i Larosterna inca) algunes de les quals pertanyents al grup d'ocells guaners. Pel que fa a l'abundància, la família Laridae va ser la més abundant, amb una presència destacada de Larosterna inca amb el nombre més gran d'individus; la fluctuació temporal evidencia una abundància més gran d'espècies durant els mesos de desembre i gener. Els principals usos de l'hàbitat van ser el descans, l'arranjament de les plomes amb el bec i l'alimentació. Tanmateix, els registres de nidificació de sis espècies també suggereixen aquest ús. Aquesta àrea té una importància significativa per al desenvolupament de les espècies aquí registrades atesa l'escassa informació disponible sobre la costa sud, la grandària poblacional i la reproducció d'algunes de les espècies registrades.

Dades publicades a GBIF (Doi: https://doi.org/10.15470/9umyvz) Paraules clau: Diversitat, Ús del sòl, Ocells marins, Comportament, Pertorbacions, Larosterna inca Rebut: 26/04/2021; Conditional acceptance: 07/06/2021; Final acceptance: 30/07/2021 L. M. Vilca Taco, Enrique Mamani T., Universidad Nacional de San Agustín de Arequipa, c/ San Agustín 108, 04003, Arequipa, Peru.– C. R. Luque Fernández, Departamento Académico de Biología, Facultad de Ciencias Biológicas, Universidad Nacional de San Agustín de Arequipa, c/ Daniel Alcides Carrión s/n., La Pampilla, 04003 Arequipa, Peru and Instituto de Investigación de Ciencia y Gestión Ambiental (ICIGA), Universidad Nacional de San Agustín de Arequipa, c/ San Agustín 108, 04003 Arequipa, Peru.

Corresponding author: C. R. Luque Fernández, Email: cluquef@unsa.edu.pe ORCID ID: L. M. Vilca Taco 0000-0001-7875-6607; E. Mamani T.: 0000-0002-2566-6410; C. R. Luque Fernández: 0000-0001-8050-461X 162

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Introduction The South American Pacific coast is one of the most biologically productive habitats on Earth and its influence on the communities and relationships therein is strong (Flores et al., 2013). In the case of Peru, the coast is bathed by the Peruvian or Humboldt current (Brack and Mendiola, 2000), which together with the extensive areas of coastal upwelling and the dynamics in the processes of nutrients and biogeochemical cycles (Morón, 2000; Graco et al., 2007) has produced the conditions for great biodiversity. This diversity is especially based on the extremely high primary productivity that is reflected in an abundance of zooplankton fish, birds and marine mammals (Chavez et al., 2008; Montecino and Lange, 2009; Cisterna, 2020).

The most important seabird habitats along this coast consist of a system of islands, islets, and guano capes which in many cases host unique bird species (Lara et al., 2008). The study of bird population dynamics in this system is limited, however (Tovar, 1969; Tovar et al., 1987; Goya, 2000; Weimerskirch et al., 2012; Figueroa, 2013; SERNANP, 2016). Besides, these bird populations are under pressure from natural events such as the phenomenon 'El Niño' (Flores et al., 2013), which had severe repercussions. They are also affected by anthropic activities such as the extraction of guano (with the greatest boom occurring in the 19th century) and over fishing which affect the availability of food for many of these birds (Tovar et al., 1987; Apaza and Figari, 1999; Brack and Mendiola, 2000). Additionally, species respond differently to environmental and physiographic factors (Véliz et al., 2002), as monthly variations have shown on one or some specific species (González and Málaga, 1997). As fluctuations can strongly influence a system's functionality they should be monitored.

A vast portion of coastal economic activities are related to the fishing ports and may therefore be linked to the population dynamics within bird communities. The south of Peru houses the country's second largest international port (Matarani), the international terminal port (Tisur in Islay), and many small–scale port infrastructures, such as Punta La Metalera (El Faro). The main activities in Punta La Metalera are tourism, recreation, and the extraction of fish, shellfish, algae and guano. However, information that would help decision–making regarding development plans (Järvinen and Väisänen, 1979; Koskimies, 1989; Bibby et al., 1992) of the urban–rural population and nearby activities for sustainable development is lacking. Such information could provide multiple benefits for biodiversity conservation at a regional scale (Luna–Jorquera et al., 2012). The aim of the present study was to evaluate changes in the bird community at Punta La Metalera on a temporal scale in terms of species composition and richness–abundance, and to characterize habitat use and behavior of the species present in late 2019 and early 2020.

Material and methods Study area The study was conducted in Punta La Metalera in the Islay district of the city of Arequipa, 10 km northeast of Mollendo (–72.111527 ºS, –17.015428 ºW). Punta La Metalera is a cape that has varied landforms: cliffs, shoreline, rocky outcrops with steep slopes and guano– covered surface, and algae vegetation. Its surrounding areas are islets. Moreover, it harbors the IPA (Artesanal Fishing Infrastructure) port. Nearby there are industries such as TISUR (South International Terminal), Diamante, fisheries, and populated areas. A short distance away, at 1.5 km, is the second largest industrial harbor of Peru, Matarani. Punta La Metalera has an area of about 8.21 ha and an average elevation of 21 m.a.s.l.; its topography is rocky with no vegetation. There is a rainy season (June–November) and a dry season (December–May). The rainy season is characterized by fog and sporadic rainfall. The mean

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annual temperature ranges from 15 (June–September) to 29 ºC (November–April). The annual relative humidity ranges from 70 % (January) to 84.23 % (July). The wind direction is predominantly south (S) to southeast (SE) with an average speed of 11 km/h (SENAMHI, 2019). The tidal range varies between 1.5 and to 3 m but is usually about 1 meter. Waves are moderate to high intensity. The sea surface temperature (SST) ranges from 17 to 23 ºC. Before collecting data we surveyed the coast line to determine the characteristics. To minimize recounts we divided the study area into four zones that included a small islet. The four zones included the areas with the highest concentration of birds (fig. 1).

Field surveys We conducted 24 counts from October 2019 to March 2020 using the point count method (Bibby et al., 1992), covering around 700 m of coastline. Counting points were set for the four zones, selected based on accessibility (most of the cape coastline was difficult to access). Six trips were made (one per month). On each trip we conducted three censuses: one between 5:30 a.m. and 9:30 a.m., a second between 12 p.m. and 2.30 p.m., and a third between 3:30 p.m. and 6:00 p.m.). We spent 20 minutes at each point (Bibby et al., 1992), making a total effort of 1,680 minutes (28 hours). We only counted birds that were perched on land or at sea, not those in flight. We did not exclude only coastal birds as our aim was also to look at behavior and habitat use. However, all birds sighted (all species passing through any area) were recorded for richness. At each point, the species present were identified and quantified using Bushnell, Tasco, Nikon, and Galileo binoculars (10 x 50, 12 x 45, and 90 x 80), Fujifilm camera (eight megapixels), field cards, and notes. Before starting the census we waited for five minutes for the birds to adapt to our presence as our arrival caused a slight displacement of some of them, especially those on the edges.

The birds we considered as coastal seabirds were species of the orders Anseriformes, Ciconiiformes, Charadriiformes, Pelecaniformes Suliformes, Podicipediformes, Falconiformes, Passeriformes (Acosta et al., 2013), Sphenisciformes, and Cathartiformes. To identify the species, we used the guides of Jaramillo (2003), Tabini and Paz–Soldán (2007) and Schulenberg et al. (2010). The taxonomic nomenclature was taken from the SACC (Remsen et al., 2020), and the category of species risk was assigned using the IUCN Red List of Threatened Species.

Habitat use and behavior Regarding the use of the territory and behavior, we considered eight categories according to the type of activity developed by the birds during the evaluations (table 1). Additionally, we recorded the interference of anthropic activity considering boats, tourism, guano collection and any other related activity that could be considered to disturb the birds in the evaluation area.

Data analysis We analyzed the temporal fluctuation by comparing months and comparing the mean values for each month of the abundance variation using ANOVA (one way, p < 0.05.). Data normality was previously evaluated using the Shapiro test (Peña–Villalobos et al., 2012) and normalized using the bestNormalize (Peterson, 2020) package in RStudio (RStudio Team, 2020).

The species occurrence frequency (SOF) was analyzed considering six categories (Nores, 1996 cited by Brandolin et al, 2007), which are: (i) very common (0.8–1), (ii) common (0.6–0.8), (iii) frequent (0.4–0.6), (iv) scarce (0.2–0.4), (v) occasional (0.1–0.2), and (vi) accidental (< 0.1). These values were obtained for each species as the number of months in which the species was present, divided by the total number of sampled months. For the species relative abundance (SRA), we considered five categories: (i) abundant (90–100 %),

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–72º 6.687' TISUR

Arequipa

Perú

Islay

Punta La Metalera 8

16 4 9

100

Zone 3

200 m

IPA

5

Zone 2

0

–72º 6.501'

2 3

Pacific Ocean

–72º 6.594'

1

Zone 1

–17º 0.924'

–17º 0.831'

–17º 0.738'

–72º 6.873'

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10 6

7 18

15 11

12

17 13

Zone 4

14

Fig. 1. Sampling zones in Punta La Metalera. Estimated areas for the zones: zone 1 (13,381 m2), zone 2 (6,788 m2), zone 3 (1,870 m2), and zone 4 (6,299 m2): ● observation sites; IPA, Artisanal Fishing Infrastructure; TISUR, South International Terminal.

Fig. 1. Zonas de muestreo en Punta La Metalera. Superficie estimada de las zonas: zona 1 (13.381 m2), zona 2 (6.788 m2), zona 3 (1.870 m2) y zona 4 (6.299 m2): ● puntos de observación; IPA, Infraestructura de pesca artesanal; TISUR, Terminal Internacional Sur.

(ii) common (65–89 %), (iii) moderately common (31–64 %), (iv) uncommon (10–30 %), and (v) rare (1–9 %). These percentages were obtained for each species as the number of individuals of a species divided by the total number of individuals considering all species and multiplied by 100 (Güitrón–López et al., 2018).

The dissimilarity of species abundance between months was calculated using the index of similarity (Bray–Curtis): 1 – (2c/S1 + S2) where S1 and S2 are the number of species in sample months 1 and 2, respectively, and c is the number of species present in both sample months. This dissimilarity was represented with dendrograms using the UPGMA method with PAST v.2.17 (Kusch et al., 2008 cited

by Peña–Villalobos et al., 2012) to establish a similarity relationship between assessment months on species/abundance fluctuations. And finally, habitat use (land–use) was analyzed comparing the birds' behavior s per month, for which we summed up each behavior record.

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Table 1. Ethogram of bird behavior considered at Punta La Metalera (Arequipa, Peru).

Tabla 1. Etograma de los comportamientos considerados en las aves de Punta La Metalera (Arequipa, Perú).

Behavior Definition Reference Preening (P) Any activity of care or attention Hogan–Warburg et al. (1995)

to the animal's body surface; including Mooring et al. (2004)

any cleanliness behavior.

Iannacon et al. (2012) Foraging (F) The spatial search for food resources Castelblanco–Martínez (2010)

and obtaining food.

Sibley (2010) Resting (R) The act of perching or alighting, Quiñonez

and vigilant sleep that allows them and Hernandez (2017)

to be alert to any noise so that they

can escape from any threat.

Copulation (C) Couples mating or attempting to mate, –

where the male mounts the female

from behind.

Nesting (N) The action of nest building, mainly –

with birds carrying materials.

Mating (M) Courtship ceremonies, in which the bird Idárraga (2015)

spreads its feathers by adopting different

positions (enhancing its body parts),

offering food or other gifts to the females.

In addition to these rituals, the male may

interact with the environment to show

physical or individual characteristics

through dancing, singing, or fighting.

Agonistic Aggressive behavior associated with Camerino and Nos (1983) behavior (AB) fighting, including the attack, threat,

escape, and submission.

Non–agonistic Allopreening and crossing beaks.

Camerino and Nos (1983) behavior (NAB) Allopreening refers to grooming or

preening another bird. Crossing beaks i

ndicates that the bird peaks another bird's beak.

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1

2

3

4

5

6

7

8

9

10

11 12

Fig. 2. Bird species recorded from October 2019 to March 2020 in Punta La Metalera: 1, Larus belcheri; 2, Larus dominicanus with breeding plumage; 3, Larosterna inca adult; 4, Pelecanus thagus adult; 5, Cathartes aura; 6, Phalacrocorax gaimardi adult; 7, Phalacrocorax brassilianus adult; 8, Haematopus ater adult; 9, Phalacrocorax bougainvillii adult; 10, Spheniscus humboldtii; 11, Sula variegata adult; 12, Cinclodes taczanowskii adult.

Fig. 2. Especies de aves registradas de octubre de 2019 a marzo de 2020 en Punta La Metalera: 1, Larus belcheri; 2, Larus dominicanus con plumaje de apareamiento; 3, Larosterna inca adulto; 4, Pelecanus thagus adulto; 5, Cathartes aura; 6, Phalacrocorax gaimard adulto; 7, Phalacrocorax brassilianus adulto; 8, Haematopus ater adulto; 9, Phalacrocorax bougainvillii adulto; 10, Spheniscus humboldtii; 11, Sula variegata adulto; 12, Cinclodes taczanowskii adulto.

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B

Similarity

Abundance

Abundance Oct Nov Dec Jan Feb Mar

1.00

83

0.95

1000

0.90

1500

0.85

60 78

0.80

2000

0.75

90 75

0.70

2500

0.65

0.60

3000

Feb Mar Nov Oct Dec Jan

Fig. 3. Plots showing the variation in temporal abundance (A) (mean ± SD), and similarities (B) (Bray–Curtis Similarity Index) between months during 2019–2020 in Punta La Metalera (Arequipa, Peru).

Fig. 3. Gráficos que muestran la variación temporal de la abundancia (A) (media ± SD) y las similitudes (B) (índice de similitud de Bray–Curtis) por meses en el periodo 2019–2020 en Punta La Metalera (Arequipa, Perú).

Results Richness and abundance We recorded a total richness of 12 species (eight families) (fig. 2), ranging from a minimum of nine species (March) to a maximum of 11 species (February and December) during the study months. About 50 % of these species were present in all months sampled (Larosterna inca, Larus belcheri, Sula variegata, Phalacrocorax gaimardi, Cathartes aura, and Haematopus ater), nearly 70 % were present in October, November, and December, and another 70 % were present in January, February, and March. During all the sampled months, the families with the highest richness were Laridae and Phalacrocoracidae, each with three species, followed by Sulidae, Cathartidae, Pelecanidae, Haematopodidae, Furnariidae, and Spheniscidae, each with one species. Species richness was highest in February and March.

Phalacrocoracidae and Laridae were dominant in the number of species, but Phalacrocoracidae was dominant in October, December, and January, and Laridae was dominant in November. Both species were dominant in February and in March.

We recorded a total of 25,364 birds. Over the six months numbers ranged from 500 to 3,000 individuals (appendix 1; see also dataset published through GBIF: Doi: https://doi. org/10.15470/9umyvz). The pattern increased towards the summer; in October 2019 we recorded around 500 individuals but by January 2020 there were 2,700 individuals (fig. 3A).

Abundance decreased approximately 60 %, and around 1,000 individuals were observed in March. Total abundance differed significantly between months (F = 2.33, P = 0.0409) (appendix 2). The Bray–Curtis index of similarity showed three clusters: one composed of February and March with 90 % similarity, another composed of December and January with 83 %, and a third composed of November and October, with 78 % (fig. 3B).

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Abundance

2000

Sula variegata 600

1500

400

1000

200

500 Oct Nov Dec Jan Feb Mar

Abundance

80

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Oct Nov Dec Jan Feb Mar Larus belcheri

Phalacrocorax gaimardi 50

60

40 30

40

20

20 Oct Nov Dec Jan Feb Mar

10

Oct Nov Dec Jan Feb Mar

Fig. 4. Temporal variation in abundance (mean ± SD) of the four most abundant species in Punta La Metalera (Arequipa, Peru).

Fig. 4. Variación temporal de la abundancia (media ± SD) de las cuatro especies más abundantes en Punta La Metalera (Arequipa, Perú).

Temporal variation of bird population Fluctuation analysis of the abundance of the most representative species showed four species: L. inca, S. variegata, P. gaimardi, and L. belcheri, represented 76.06 % of the total number of individuals present, with increased abundance of individuals of these species from January to March (fig. 4). L. inca was the most abundant species between and within the months of evaluation (range of 500–2,000 individuals), showing its dominance and effect on the temporal dynamics of the populations of other species, and reaching its maximum counts with more than 2,000 individuals in January.

Abundance of S. variegata ranged from 50 to 700 individuals increasing towards January and maintaining this until March. Its lowest numbers were in November. P. gaimardi (ranged from 20 to 60 individuals) also presented an increment approaching January but the number of individuals did not vary as significantly as the other species. L. belcheri showed no variation in the pattern of population size. It reached its lowest count in January and highest count in February (60 individuals).

The species that contributed most to the general abundance was L. inca (temporal variation). It contributed over 50 % each month, with the lowest contribution being 60 % in March, and the highest in December with about 75 %. S. variegata contributed between 10 % in November and 25 % in March. P. gaimardi contributed 2–5 %, L. belcheri contributed 1–5 %, and the rest of the species made up between 2 % and 10 % (fig. 5).

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100 %

Abundance %

75 % L. inca S. variegata

50 %

P. gaimardi L. belcheri Other species

25 %

0 % Oct

Nov

Dec

Jan

Feb

Mar

Fig. 5. Contribution of species abundance for each month in Punta La Metalera (Arequipa, Peru).

Fig. 5. Contribución a la abundancia de las especies por meses en Punta La Metalera (Arequipa, Perú).

According to the species occurrence frequency (SOF), all species scored from common to frequent. For the species relative abundance (SRA), all species fitted as rare except for L. inca and S. variegata. The Laridae family was the most common, with L. inca contributing the most (68.05 %). S. variegata (family Sulidae) was very common and contributed 22.41 %.

About the conservation status of the species reported, at least five are in some category. S humboldti is the species that presents the highest criterion, being Vulnerable (VU) according to the IUCN (table 2). C. taczanowski, the endemic species of the Peruvian coast, is a rare species.

Habitat use Birds used their habitat mainly for resting, preening, and foraging. The main behavior was resting. It varied from 36 % in November to 53 % in January. The second most prevalent behavior was preening, between 22 % in December and 36% in February. And foraging was between 9 % and 18 %, in March and October, respectively showing a decreasing trend.

The remaining activities (nesting, mating, and copulation) ranged between 5 % and 12 %.

For copulation, the highest proportion of this activity (9 %) was recorded in November, and for nesting, the highest percentage was observed in December (table 3). We identified six species as active nesters during the study (table 2). Throughout most of the evaluations, L. inca, P. gaimardi, L. belcheri, S. variegata, and C. aura nested in small groups, but C. aura and L. belcheri nested in single (isolated) nests.

Regarding the most abundant species of the evaluation (fig. 6), the inca tern L. inca used the area principally for resting, preening, foraging and courtship (mating and copulation).

We also observed reproduction events, which included nesting protection and parental care.

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Table 2. Species occurrence frequency (SOF), species relative abundance (SRA), conservation status (IUCN) and nesting species in the area (NSA) of species recorded at Punta La Metalera (Arequipa, Peru): * endemic species; IUCN (LC, least concern; NT, near threatened; VU, vulnerable).

Tabla 2. Frecuencia depresencia de especies (SOF), abundancia relativa de especies (SRA), estado de conservación (UICN) y especies nidificantes en el área (NSA) de las especies registradas en Punta La Metalera (Arequipa, Perú): * especie endémica; UICN (LC, preocupación menor; NT, casi amenazado; VU, vulnerable).

Species Common name SOF SOF Category Family Laridae L. inca Inca tern 1 Very common L. belcheri Black–tailed gull 1 Very common L. dominicanus Kelp gull 0.5 Frequent Family Sulidae S. variegata Peruvian booby 1 Very common Family Phalacrocoracidae

SRA SRA Category IUCN 71.04 69.05 Common NT 1.97 Rare LC 0.02 Rare LC 22.41 22.41 Uncommon LC 4.64

NSA

P. gaimardi Red–legged cormorant 1 Very common P. bougainvillii Guanay cormorant 0.83 Very common P. brasilianus Neotropic cormorant 0.83 Very common Family Cathartidae C. aura Turkey vulture 1 Very common Family Pelecanidae P. thagus Peruvian pelican 0.83 Very common Family Haematopodidae H. ater Blackish oystercatcher 1 Very common Family Furnariidae C. taczanowskii* Surf cinclodes 0.5 Frequent Family Spheniscidae S. humboldti Humboldt penguin 0.67 Common

2.63 Rare NT 1.98 Rare NT 0.02 Rare LC 1.54 1.54 Rare LC 0.18 0.18 Rare NT 0.13 0.13 Rare LC 0.05 0.05 Rare LC 0.01 0.01 Rare VU

Yes No No

Yes Yes No Yes

Yes Yes No No No 171

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Table 3. Percentages of behaviors (activities) observed in Punta La Metalera (Arequipa, Peru) from October 2019 to March 2020.

Tabla 3. Porcentaje de los comportamientos observados (actividades) en Punta La Metalera (Arequipa, Perú) de octubre de 2019 a marzo de 2020.

Behavior

October November December January February March

Resting

41.70 %

36.40 %

41.53 %

53.18 %

45.65 %

49.40 %

Preening

34.82 %

29.41 %

22.92 %

21.97 %

34.78 %

35.54 %

Foraging

17.81 %

14.71 %

13.62 %

12.14 %

14.13 %

8.43 %

Mating

0.81 %

5.15 %

4.98 %

7.51 %

2.72 %

5.42 %

Copulation

1.62 %

9.19 %

5.32 %

0.58 %

0.55 %

0.61 %

Nesting

3.24 %

5.14 %

11.63 %

4.62 %

2.17 %

0.60%

In this way, this species was ranked second for nesting. The Peruvian booby S. variegata used the area mainly as a resting and preening zone. The other categories of usage wre uncommon; we observed few attempts of copulation and mating. We had a similar scenario for the red–legged cormorant P. gaimardi. However, compared to the other species, the area represented a significant zone due to the notable percentage (10–20 %) of consecutive nesting events (from October to January). And the black–tailed gull L. belcheri used the area indiscriminately, with resting and foraging behaviors highlighted. For this species, we recorded only a few nesting attempts in December 2019.

The agonistic and non–agonistic behaviors were recorded mainly for L. inca and S. variegata.

Species like L. inca, L. belcheri, and C. aura, which were in groups, exhibited a marked agonistic social behavior. This consisted mainly of aggressive squawking and pecking at nearby species perched on the same rock. Between L. inca and C. taczanowskii we recorded disputes related to food and displacement, especially during nesting months, and increased aggressiveness towards other species located close by. Something similar occurred between S. variegata and L. belcheri, both of which showed very aggressive behaviors. We also occasionally observed aggressive behavior between C. aura and L. belcheri over food.

Finally, among the activities recorded as disturbances for the study area, we identified that the most recurrent disturbance was the presence of people, particularly large groups of local students on educational activities. Furthermore, we observed vehicles, such as motorcycles, very close to the area where the birds were sighted, especially in zone 1. In the sea, we also recorded the presence of tourists in boats, and some small ships. Additionally, local divers used boats for seafood extraction activity, causing stress and dispersing not only the perched birds but even colonies of sea lions. Such activities caused the birds to screech and fly off to another location.

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Larosterna inca

Sula variegata

Phalacrocorax gaimardi

Larus belcheri

Oct Nov Dec Jan Feb Mar Oct Nov Dec Jan Feb Mar 0 %

25 %

50 %

75 %

Copulation Foraging

100 % 0 % Mating Nesting

25 %

50 %

75 %

100 %

Preening Resting

Fig. 6. Behavioral activities of the most abundant bird species present in Punta La Metalera (Arequipa, Peru) from October 2019 to March 2020.

Fig. 6. Actividades comportamentales de las especies de aves más abundantes presentes en Punta La Metalera (Arequipa, Perú) desde octubre de 2019 hasta marzo de 2020.

Discussion Richness and abundance Twelve species of birds belonging to eight families were recorded for Punta La Metalera during the months of evaluation. These birds have not been specifically reported in previous continuous census surveys for the area (Tovar, 1969; Tovar et al., 1987; SERNANP, 2016), and many correspond to endemic species of the Peruvian current (Cisterna, 2020). For the location according to eBird (2021), more species are reported in the lists of this source (49), but many are erroneously listed in the area, corresponding to a nearby locality since some species are found in wetlands such as lagoons. In the case of the other marine capes in Arequipa, such as Lomas, Atico, La Chira and Hornillos, three to eight species have been reported (SERNANP, 2016), although these lists are also conditioned by the fact that during the census in these locations, preference was given to the group of guano birds (S. variegata, P. bouganvillii, P. thagus) due to their economic importance.

About other cape systems, Zeballos (2016) reported a total richness of 18 species in nine families at Punta El Faro in the Peninsula of Illescas in northern Peru, with ten of the species in common with our results. Zeballos also observed that the group of gulls (Laridae) had the highest number of species with three records in common in both the two studies.

Additionally, he mentioned that a specific richness was associated with coastal capes in

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this habitat. It is noteworthy that along the latitudinal gradient throughout the Peruvian coasts, there is a turnover of species, Sula nebouxii, with a greater abundance to the north,

by S. variegata, which is more common to the south (SERNANP, 2016).

The abundance recorded at Punta La Metalera showed that L. inca was the most abundant and most common species (69 %), sharing occurrence frequency values (SOF) with five other species (S. variegata, L. belcheri, P. gaimardi, C. aura, and H. ater). The abundance of L. inca varied from 417 to 2,160 individuals. Although the available information including fluctuations is scarce (Simeone et al., 2003; Figueroa and Stucchi, 2008), a report made by Guillen (1988) during population censuses in 1963 and 1985 on the Peruvian coast showed that the highest abundance was recorded between latitudes 11º and 13º, corresponding to the coastal line from Lima to Pisco, with values fluctuating between 166 to 2,713 individuals. However, the research conducted by Guillen (1988) did not consider the localities of southern Peru in the evaluations; therefore, considering the number of individuals recorded in this study, Punta La Metalera could be a critical location for the establishment of this species. The abundance recorded here could be related to the presence of anchoveta (Engraulis ringens), which is one of the preferred resources for this bird, and which is distributed mainly in cold waters (Calvo, 2016), such as those found essentially in the southern part of Peru.

The second most abundant species, S. variegata (22.41 %) and L. inca were also the most abundant species in the Bahía de Paracas (Ica) (SERNANP, 2016) together with P. bougainvillii, and L. inca. The dynamics of dominance of some of these species could be related to the presence of guano bird species. Moreover, these guano birds cling to the territory because it ecological efficiency and associated characteristics (Vogt and Duffy, 2018).

Temporal composition In general, the composition in this study was very similar (~90 %) to that of other studies, especially those conducted in northern Peru (Figueroa and Stucchi, 2008; Figueroa and Suazo, 2012; Figueroa, 2013) and similar systems in Chile (Simeone et al., 2003). The permanent presence of the four species (L. inca, S. variegata, P. gaimardi, and L. belcheri) in our study showed fluctuations in their populations. This variation in composition, according to Véliz et al. (2002), is related to the study of temporal changes in the communities, which depend mainly on environmental and physiographic factors, where the main effect of the variation is the alteration of the habitat, which causes a change in the distribution and abundance of species according to INE–SEMARNAP (2000).

L. inca was proposed as a potential sea condition indicator species (Calvo, 2016), however, there is limited information on temporal variations. Our results showed that the temporal fluctuation with the highest number of individuals was between December and January. Guillen (1988) reported similar findings in an Asia Island population, where the population size increased from June to December, reaching its maximum value of approximately 1,110. Regarding S. variegata, over 600 individuals were recorded, with topmost numbers being observed during the summer months (December to March). This abundance is a low value for southern Peru compared to other systems reported in the SERNANP master plan for the 2014 census (SERNANP, 2016), where values were over one thousand individuals, similar to Espinosa (2016) in his estimates for the Peruvian coast. Concerning P. gaimardi, there are no reports of abundance or fluctuations in the cape systems on the Peruvian coast. It is noteworthy that this species is very conspicuous and has a broad distribution from the north of Peru to southern Chile. However, Frere and Millones (2020) reported relatively small populations on the Atlantic coast of Argentina. Punta La Metalera could therefore represent a significant site for the species, especially in summer when the number of individuals (20–80) increased due to nesting.

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Habitat use and disturbance Habitat use recorded at Punta La Metalera highlighted resting behavior as the principle activity of the species. This could be related to the territory's relevance for migration, resting, and breeding area in the southern coastal strip. Habitat use records also showed an active breeding area for some species, for example L. inca. Under stable conditions, L. inca can have two clutches per year within a prolonged reproductive period (Murphy, 1936), one in autumn (April–June) and the other in spring (October–December), with high occurrence in May and November (Zavalaga and Paredes, 1997). Our results corroborate this with records of copulation and nesting activities being higher than for the other species from November to December and especially nesting throughout all months. P. gaimardi showed a preference for nesting in cliff areas, this occurring from October to January. Currently, in this coastal region, there are no reports of active nesting areas for this species (Figueroa and Stucchi, 2008).

Regarding agonistic and non–agonistic behavior, we observed that L. inca was rather aggressive with other species, although it has been previously reported that this species tends to show social behavior with species such as cormorants, sea lions and even cetaceans (Harrrison, 1985). This more aggressive social behaviour that we observed could respond to the continuous nesting strategy in the area. Besides the large number of individuals and consequent competition for space this behavior could be related to the fact that they share breeding and nesting seasons with L, belcheri. In addition, L. belcheri is a threat to species such as the Inca tern and boobies as it prey on the eggs and chicks of these and other species (Figueroa and Stucchi, 2008).

We observed that foraging was a primary activity. This is noteworthy because several of these species feed several kilometers inshore. For example, cormorants prefer to feed between 20 km and 60 km from the coast (Espinosa, 2016). The Peruvian booby prefers to feed within the first 10 km from the coastline. This range is related to the anchoveta stocks, as abundance is highest between 0 and 10 km from the coast (Espinosa, 2016). Although L. inca prefers this resource, it also feeds on crustaceans and remains left by other species such as sea lions or by fishing boats.

Perturbations The bird community in the study area was mainly disturbed by human activities related to tourism. As mentioned by Simeone et al. (2003), tourism is a common denominator in this area, partially due to the diversity of animal species in the area and to the proximity of the port of Matarani, both of which are well–known attractions.

Unregulated tourism can affect the richness and abundance of animal communities (Simeone et al., 2003; Ellenberg et al., 2006). Human activities that correspond with this study (Shochat, 2004; Shochat et al., 2006, Garcia et al., 2016; Paredes and Zavalaga, 2001) indicate that inadequate management of organic waste, plastic waste, and resources such as guano, algae, seafood, and fishing, cause moderate stress to the animal communities in the area. According to Ramos (2019), stress decreases the reproductive rate in birds through loss of nests and behavioral changes, and it can also indirectly affect their behavior, physiology, ecology, and quality of life (Ellenberg et al., 2006). It can also affect the timing of the search for food, which in turn could alter nesting and breeding stages (Garcia et al., 2016).

Finally, it is important to mention that these and many other seabird and shorebird communities are under pressure from changes in climate and in the marine system (Apaza and Figari, 1999; Quillfeldt and Masello, 2013). Furthermore, their resources can be markedly reduced due to natural phenomena such as El Niño Southern Oscillation (ENSO) events.

Such phenomena increase bird mortality (Apaza and Figari, 1999; England, 2000; Jaksic and Fariña, 2010) due to desertion of nests or decreased reproduction due to low avai175

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lability of food. We thus consider that Punta La Metalera is a strategic site for continued research as it is a nesting site for a good many species, such as L. inca, that are present in large numbers.

Acknowledgements We are grateful to the Ecology and Conservation Section of the Universidad Nacional de San Agustín de Arequipa for providing us with field equipment. We also thank C. J. Delgado, A. S. Flores, H. S. Leon, B. Y. Luque and C. D. Vega for their useful fieldwork.

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Appendix 1. Abundances of species recorded by month and period in Punta La Metalera (Arequipa, Peru) during 2019–2020. Periods: 1, morning; 2, midday; 3, afternoon.

Apéndice 1. Abundancia de las especies registradas por mes y periodo en Punta La Metalera (Arequipa, Perú) durante el periodo 2019–2020.

Períodos: 1, mañana, 2. mediodía; 3, tarde.

Oct ober

November 3

1

2

3

1

2

3

1

2

3

March

35 26 25

22 22 28

22 3

44

14 6 13

33 7 9

22 31 28

C. taczanowskii

0 0 1

8 1 0

2 1 0

0 0 0

0 0 0

0 0 0

1 1 1

3 3 1

6 3 5

1 0 2

1 0 2

0 1 2

2

February

C. aura

417 493 433

1

January

1

L. inca

3

December

H. ater

2

Month 1

2

3

556 560 810 1,590 1,232 1,534 2,131 987 2,160 1,070 434 612 1,404 515 539

L. belcheri

26 33 21

33 49 43

23 21 29

14 11 11

54 28 32

13 22 37

L. dominicanus

0 0 0

0 0 0

0 0 0

0 0 0

4 0 0

1 0 0

P. thagus

1 19 0

0 0 0

8 5 3

4 20 2

2 0 1

0 0 0

P. bougainvillii

0 0 0

0 0 0

0 0 0

3 500 0

0 0 0

0 0 0

P. brasilianus

1 1 0

0 0 0

0 1 2

0 0 0

0 0 0

0 0 0

P. gaimardi

25 15 30

51 37 42

40 40 43

57 25 81

35 38 33

30 24 34

S. humboldti S. variegata

0 0 0 169 107 239

2 1 0 48 75 115

0 0 0 336 236 310

0 0 1 428 512 718

0 0 0 592 143 314

0 0 0 502 183 662

180

Arxius de Miscel·lània Zoològica, 19 (2021): 161–181

Vilca Taco et al.

Appendix 2. One–way ANOVA for abundance values recorded at Punta La Metalera (Arequipa, Peru).

Apéndice 2. ANOVA de una vía para los valores de abundancia registrados en Punta La Metalera (Arequipa, Perú).

Variation origin

SS

DF

MS

F

P

Between months

11.6

5

2.3115

2.33

0.0409

Residuals Total

820.4 827 0.9921 – 832 832 –

–

181