© 2004 by ICES/CIEM International Council for the Exploration of the Sea/Conseil International pour l'Exploration de la Mer
Seabird distribution on the Humboldt Current in northern Chile in relation to hydrography, productivity, and fisheries
a Forschungs- und Technologiezentrum Westküste Hafentörn, D-25761 Büsum, Germany
b Departamento de Biología Marina, Universidad Católica del Norte Larrondo 1281, Coquimbo, Chile
*Correspondence to T. Weichler; fax: +49 (0)4834 604 199. e-mail: weichler{at}ftz-west.uni-kiel.de.
Factors affecting seabird distribution in the Humboldt Current upwelling system in northern Chile were studied in January 1999 using ship transect counts. Of 24 species recorded, the Peruvian booby (Sula variegata), the kelp gull (Larus dominicanus) and the Humboldt penguin (Spheniscus humboldti) were the most abundant. Species composition varied among different areas of the system and distribution patterns differed substantially among eight of the more abundant species. Most species showed links to variation in environmental factors (trawler distribution, SST and chlorophyll concentration). Principal component analysis identified a feeding-flock factor as the most important one for explaining observed distribution patterns. One-third of all birds recorded were associated in feeding flocks and 3% of all individuals were directly attending fishing vessels.
Keywords: Chile, distribution, feeding flock, fisheries, hydrography, seabirds, upwelling
Received 3 December 2002; accepted 11 July 2003.
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Introduction |
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 Top Introduction Materials and methodsResultsDiscussionReferences |
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The upwelling system of the Humboldt Current on the west coast of South America is one of the most productive marine ecosystems of the world and supports large stocks of fish, seabirds and marine mammals (Arntz and Fahrbach, 1991). Well-known seabirds of the area are the so-called guano birds: the guanay cormorant, Peruvian booby and Chilean pelican (see Table 1 for scientific bird names). They breed along the coast and on adjacent islands. All three species are endemic to the Humboldt Current (del Hoyo et al., 1992). Their principal prey are pelagic, schooling fishes, chiefly anchovies (Engraulis ringens) and sardines (Sardinops sagax; Arntz and Fahrbach, 1991). Other endemic seabird species are the Humboldt penguin, Peruvian diving-petrel, grey gull and Inca tern.
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The Humboldt Current area is characterized by a strong periodic but irregular climate variation, the El Niño Southern Oscillation (ENSO). In extreme cases, warm surface water forces the schooling fishes to move to greater depths and/or areas farther away from the coast where nutrients are consistently available. Often, these species are then only available in sufficient quantity outside the foraging ranges of incubating and chick-rearing seabirds (Arntz and Fahrbach, 1991). Food availability to seabirds is affected also by another "environmental" variable, the commercial fishery. Especially the anchovy fishery has been intensive over many decades, with landings in 1999 amounting to approximately 8 and 2 million t for Peru (Ministerio de Pesquería de Peru, 2000) and Chile (SERNAPESCA, 1999), respectively.
The distributions of seabirds at sea in relation to hydrography, fisheries and other factors have been investigated in many areas of the world over the past two decades. However, relatively few studies have been conducted around South America. Comprehensive quantitative data have been presented for Pacific equatorial waters by Ribic et al. (1997), for the Panama Bight by Spear and Ainley (1999), and for the Beagle Channel in southern Argentina by Raya Rey and Schiavini (2000). For Chilean waters, only classic, qualitative studies are available so far (Murphy, 1936; Jehl, 1973).
To examine how the endemic as well as other seabird species utilize the rich waters of the Humboldt Current, we studied their distribution and abundance in northern Chile during the breeding season in relation to environmental factors such as hydrography and fishing activity.
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Materials and methods |
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TopIntroductionMaterials and methodsResultsDiscussionReferences |
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Eight cruises on the RV "Stella Maris II" (Universidad Católica del Norte, Coquimbo) were carried out in the Humboldt Current upwelling system of northern Chile between 29°08'30''S and 30°11'S ("Coquimbo area"; Figure 1) between 12 and 29 January 1999. Seabird distribution was studied using transect counts following the method described by Tasker et al. (1984) and Webb and Durinck (1992). All seabirds on the water surface up to 300 m from the ship's track were counted directly while flying birds were counted using the "snapshot" method. In principle, bird records were summed over 10 min intervals (Tasker et al., 1984), but intervals often deviated from the norm because of arrival at stations or changes in vessel course. In addition to their mere numbers, typical behaviour such as attending fishing trawlers or being involved in a feeding flock was recorded too. Hydrographic parameters (temperature, salinity and sometimes also chlorophyll) were measured at 51 stations at depths of 10, 20, 30 and 50 m on the same cruises (Figure 1b). During counting, all trawlers within a radius of 5 km were recorded to analyse whether seabird distribution was influenced by their presence by providing a direct food resource in the form of discards at sea. Such effects might be more widespread than suggested by those birds directly attending fishing vessels. Transects extended up to 53 km from the coast covering a total area of 470 km2 within the 300 m band. To relate seabird densities to environmental parameters, a principal component analysis (PCA) was carried out based on 46 sections of the cruise tracks. Each section comprised a hydrographic station approximately midway and 10 min intervals in two opposite directions (with a minimum of 4 km and a maximum of 8 km in either direction from the station). Only the commoner species with numbers sighted exceeding 1% of all individuals counted (Table 1) were included in the analysis. Density by species and seven environmental variables were included in the analysis: (1) water depth (Anon., 1999), (2) distance to nearest land, (3) number of trawlers within a radius of 5 km, (4) sea surface temperature, sea surface temperature minus water temperature in (5) 10 m and (6) 30 m, and (7) the difference between temperature at 10 and 50 m depth. Salinity was excluded, because it was virtually constant throughout the study area. Although the number and distribution of chlorophyll measurements obtained were insufficient for inclusion in statistical analyses, the data did provide a general distribution pattern from which inferences could be made in relation to the distribution of seabirds. Only principal components with eigenvalues >1 were included in the model, and axes were varimax-rotated to facilitate interpretation (Backhaus et al., 1996).
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Seabird assemblages were analysed using cluster analysis. Species densities were selected as variables and counting intervals (7–19 min), derived from the original 10 min intervals (see above), were selected as cases. Only species seen in at least five counting intervals were included, an arbitrary choice that allowed covering a wide spectrum of species while ignoring species with few occurrences. Data were standardized by z-transformation. Following recommendations of Backhaus et al. (1996), we used the Ward method with Euclidean distance as similarity coefficient.
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Results |
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TopIntroductionMaterials and methodsResultsDiscussionReferences |
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A total of 24 species was recorded with the Peruvian booby, Humboldt penguin and kelp gull being the most abundant (Table 1). The distribution patterns differed substantially among eight of the more abundant species (Figure 2). Most species showed apparent links to variation in environmental factors, particularly to trawler distribution (Figure 2g, h), centres of upwelling of cold water (Figure 2d–f) and chlorophyll concentrations (Figure 2b, c).
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The proportion of divers (Peruvian booby, Humboldt penguin, and Peruvian diving-petrel) decreased significantly as a function of distance to the coast (Spearman rank correlation rs=–0.279, p<0.01, n=87 grid cells). Also, the proportion of surface-feeding birds (white-chinned petrel, Juan-Fernandez petrel, Antarctic prion, kelp gull, and Franklin's gull) and of diving birds (see above) differed significantly among three classes of distances to the coast (0–10 km, 10–30 km, 30–53.4 km;
=206; df=2, p<0.001), with the former being relatively more numerous further offshore and the latter more numerous closer to the coast. Analysis of environmental variables and seabird density by PCA revealed that six components explained 78% of the variance in all variables (Table 2). A feeding-flock factor including Peruvian booby, Humboldt penguin, guanay cormorant and grey gull was identified as the most important factor, followed by a hydrographic factor and a factor reflecting the distance to the coast and depth (Table 3).
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Cluster analysis revealed two main clusters (Figure 3). One consisted of Humboldt penguins, guanay cormorants, Peruvian boobies, and grey gulls (forming the typical feeding-flock species) and the other one of species that were to a much lesser extent or not at all engaged in feeding flocks and did not show this behaviour (Table 4).
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Seven species were found to directly attend fishing trawlers. The highest percentage of individuals following trawlers was observed for Chilean pelican (53%), followed by Buller's albatross (17%), Franklin's gull (9%), Kelp gull (8%), white-chinned petrel (5%), Peruvian booby (1%) and Antarctic prion (1%). Overall, 3% of all seabirds observed were attending fishing vessels.
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Discussion |
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TopIntroductionMaterials and methodsResultsDiscussionReferences |
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Many of the species observed showed distinct distribution patterns and the PCA indicates that these are related to various environmental factors. However, the interpretation of these relationships is not straightforward, because ultimately distribution of different seabirds is expected to reflect the availability of their preferred prey and the question is how these prey are affected by the environment.
The distribution of sea surface temperatures indicates a major upwelling area in the southern part of the Coquimbo area, where Juan-Fernandez petrels (Figure 2e), Antarctic prions (Figure 2f) and white-chinned petrels (Figure 2d) were also concentrated. These species showed similar distribution patterns and were grouped closely in both cluster analysis and PCA. We can only speculate about the reasons for the association between their distribution and cold surface waters. Their common feeding technique offers one possible explanation. All three species search for food at or close to the sea surface. White-chinned petrels feed on a variety of prey items including crustaceans (mainly Euphausids), pelagic fish, squid, salps (Jackson, 1988; Croxall et al., 1995; Catard et al., 2000) and have been observed behind fishing vessels (Warham, 1996; Yorio and Caille, 1999). Literature on the feeding behaviour of the other two species is scarce, but Antarctic prions feed also on Euphausids and small fish (Prince, 1980; del Hoyo et al., 1992) and Juan-Fernandez petrels probably feed on squid and fish (del Hoyo et al., 1992).
Upwelling is supposed to enhance nutrient availability and consequently phytoplankton production. Unfortunately, chlorophyll could not be measured at all stations and therefore this index of primary production had to be excluded from the PCA. Nevertheless, the available information suggests some association between the distribution of Humboldt penguin (Figure 2b), kelp gull (Figure 2g), and Franklin's gull (Figure 2h) and the integrated chlorophyll values over the upper 50 m of the water column. Phytoplankton is the main prey of pelagic schooling fishes such as anchovies and sardines (Rojas de Mendiola 1980; Arntz and Fahrbach, 1991; Arrizaga et al., 1993), which are favourite prey of the Humboldt penguin (Wilson and Wilson, 1988), the Peruvian booby (Tovar et al., 1988; Jahncke and Goya, 1998; Jahncke and Zileri, 1998) and the Neotropical cormorant (Tovar and Guillén, 1989).
The Peruvian diving-petrel (Figure 2c) had two distribution centres in the Coquimbo area, one with low densities in the upwelling area to the south and one with high densities situated directly south of Isla Choros. The upwelling area appears to be too far away to be exploited effectively by breeding birds from the colony on Isla Choros (Figure 4) and we presume that the birds seen there were non-breeding individuals.
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Interestingly, a chlorophyll maximum existed at 10 m depth just south of Isla Choros, presumably caused by upwelled water from the northern focus advected southward (Acuña et al., 1989). The Peruvian diving-petrels were observed in the direction of this maximum. Because this species dives deep for food (average maximum dive depth 31 m; Zavalaga and Jahncke, 1997), a food source at a depth of 10 m can be easily utilized. None of the other species showed such high densities near the isle. Thus, the food supply around Isla Choros appears to be fundamentally different from the central and southern parts of the Coquimbo area. The Peruvian diving-petrel feeds mainly on planktonic invertebrates with Euphausia mucronata as the main prey (Jahncke et al., 1999). In contrast, fish-eating seabirds were only observed in low densities in the area around Isla Choros, even though quite a few breed there.
Studies in other parts of the world, such as the North Sea, have shown that fishing activities may have a considerable influence on seabirds. Particularly discards are an additional, easily accessible food resource for many species (Camphuysen et al., 1995; Garthe et al., 1996) and spatial and temporal differences in availability of discards affect their distribution (Garthe, 1997). During this study, we observed seven seabird species attending fishing vessels. In addition, during two trips on the commercial trawler "Don Antonio" (1–2 and 4 February 1999, respectively), we observed large numbers of kelp gulls (maximum 600), Franklin's gulls (840), grey gulls (310), Peruvian boobies (400) and Inca terns (310) feeding behind the vessel. Other authors have also observed kelp gulls behind fishing vessels (Abrams, 1983; Ryan and Moloney, 1988; Bertelotti and Yorio, 2000) and Franklin's gulls are known to feed partly on discards (del Hoyo et al., 1996). These two species, Franklin's gull (Figure 2h) and kelp gull (Figure 2g), showed nearly the same distribution pattern in the transect study as the presence of fishing vessels. Yet, fishing activities do not seem to have a strong influence on the distribution of seabirds and proportions of ship-followers were remarkably low compared to many other oceans.
In conclusion, the distribution of seabirds in the Humboldt Current system of northern Chile can be related to major abiotic and biotic factors. A prominent feature was the presence of feeding flocks comprising different species and accounting for one-third of all birds recorded during transect counts. Surface feeders and shallow divers such as the Juan-Fernandez petrel and Antarctic prion occurred relatively far offshore whereas deep divers such as the Humboldt penguin and Peruvian diving-petrel were most frequently observed in inshore waters, suggesting changes in predominant feeding mode as a function of distance to the coast.
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Acknowledgements |
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The project was funded by the Volkswagen-Stiftung ("Effects of the marine environment on at-sea distribution, feeding ecology, reproduction and energetics of seabirds in northern Chile", Az. I/74 573). G. Cubillos, V. Dierschke, and T. Ponce helped with the ornithological fieldwork. M. Castro, P. Lagos, and R. Villablanca of Universidad Católica del Nor collaborated with the oceanographic sampling. The fish plant "San José" permitted us to work on board one of their vessels. The crews of "Stella Maris II" and "Don Antonio" made our stay at sea very pleasant. L. DiSalvo improved our English. N. Daan, G.L. Hunt Jr. and M.L. Tasker critically reviewed our manuscript.
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