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1 Seabird diets provide early warning of sardine fishery declines in the Gulf of California Enriqueta Velarde 1, Exequiel Ezcurra 2 and Daniel W. Anderson 3 1 Instituto de Ciencias Marinas y Pesquerías, Universidad Veracruzana, Boca del Río, Veracruz 94290, Mexico 2 Department of Botany and Plant Sciences, University of California, Riverside (UCR), Riverside, CA 92521, USA 3 Department of Wildlife, Fish, & Conservation Biology, University of California, Davis; Davis, CA 95616, USA Supplementary information THE STUDY AREA The most important concentrations of seabirds in the Gulf of California occur in the Midriff area (Fig. 1). Anderson et al. 1 estimated approximately 43,350 pairs of California Brown Pelicans (Pelecanus occidentalis californicus) in the Gulf of California, from a total of about 70,680 pairs in all of western Mexico and including the Southern California Bight islands. Most of the world's population (close to 95%) of Heermann's Gulls (Larus heermanni; about 130,000 pairs) and Elegant Terns (Thalasseus elegans; ca. 90,000 pairs) nest alongside the largest western North American population of Royal Terns (Thalasseus maximus) on the tiny, flat Isla Rasa Isla San Pedro Mártir, the most oceanic of the islands in the Gulf of California, contains some 110,000 pairs of Blue-footed Boobies (Sula nebouxii) and another 74,000 pairs of Brown Boobies (Sula leucogaster) and shelters at least six other species of breeding seabirds 5. Isla Partida supports the largest 1

2 populations of both Black and Least Storm Petrels (Oceanodroma melania and O. microsoma), numbering ca. 50,000 and 500,000 individuals, respectively 6. The Gulf of California is one of the most productive marine ecosystems in the world 7. Around 36% of all cetacean species can be found here 2. Small pelagic fisheries constitute up to 40% of the total national landings of Mexico, and the Gulf of California provides over 70% of these landings, the most important species being the Pacific Sardine (Sardinops sagax), and secondarily the Northern Anchovy (Engraulis mordax), Pacific Mackerel (Scomber japonicus), and other species in smaller proportions 8,9. The total sardine catch in the Gulf of California rose exponentially between 1970 and 1989, after which the fishery collapsed in the fishing seasons 10. Since then, reductions in fishing effort by the fleet have partially recovered the fishery, although landings have now become increasingly oscillatory with total catches ranging from 50 to 500 thousand tons on a 6 year cycle (Fig. 2). Furthermore, the tight relationship between effort and catch, and hence the high predictability of landings typical of the years previous to 1992, was lost after the collapse 4. REFERENCES 1. Anderson, D. W., Henny, C. J., Godínez-Reyes, C., Gress, F., Palacios, E. L., Santos del Prado, K. & Bredy, J. Size of the California Brown Pelican metapopulation during a non-el Niño year. USGS Open-File Report , U.S. Geological Survey, Reston, Virginia, USA (2007) 2. Velarde, E. & Anderson, D. W. Conservation and management of seabird islands in the Gulf of California: setbacks and successes. Pages in D. N. Nettleship, J. Burger, and M. Gochfeld, editors. Seabirds on islands: threats, case studies and action plans. Technical Publication Number 1. International Council for Bird Preservation, Cambridge, UK. (1994) 2

3 3. Velarde, E., Tordesillas, M. S., Vieyra, L. & Esquivel, R. Seabirds as indicators of important fish populations in the Gulf of California. California Cooperative Oceanic Fisheries Investigation Report 35, (1994) 4. Velarde, E., Ezcurra, E., Cisneros-Mata, M. A. & Lavín, M. F. Seabird ecology, El Niño anomalies, and prediction of sardine fisheries in the Gulf of California. Ecological Applications 14, (2004) 5. Tershy, B.R. & Breese, D. The birds of San Pedro Martír Island, Gulf of California, Mexico. Western Birds 28, (1997) 6. Anderson, D. W. The Seabirds. Pages in T. J. Case, and M. L. Cody, editors. Island biogeography in the Sea of Cortéz. University of California Press, Berkeley, Califorina, USA (1983) 7. Álvarez-Borrego, S. Physical Oceanography. Pages in T. J. Case, M. L. Cody, and E. Ezcurra, editors. A new island biogeography in the Sea of Cortés. Oxford University Press, Oxford, UK (2002) 8. Cisneros-Mata, M. A., Montemayor-López, G. & Nevárez-Martínez, M. O. Modeling deterministic effects of age structure, density dependence, environmental forcing and fishing in the population dynamics of the Pacific sardine (Sardinops sagax caeruleus) stock of the Gulf of California. California Cooperative Oceanic Fisheries Investigation Report 37, (1996) 9. Sánchez-Velasco, L., Shirasago, B., Cisneros-Mata, M. A. & Ávalos-García, C. Spatial distribution of small pelagic fish larvae in the Gulf of California and its relation to the El Niño Journal of Plankton Research 22, (2000) 3

4 10. Cisneros-Mata, M. A., Nevárez-Martínez, M. O. & Hammann, M. G. The rise and fall of the Pacific sardine, Sardinops sagax caeruleus Girard, in the Gulf of Californa, México. California Cooperative Oceanic Fisheries Investigation Report 36, (1995) 4

5 Table SI-1. Above the main diagonal: Correlation coefficients between the proportion of Pacific Sardine and Northern Anchovy in the diet for the three seabird species (Brown Pelican: P.o.; Heerman s Gull: L.h.; Elegant tern: T.e.. Below the diagonal: Significances (P) of the correlation coefficients under the null hypothesis of no correlation. % sardine in the diet % anchovy in the diet P.o. L.h. T.e. P.o. L.h. T.e. % sardine in the diet % anchovy in the diet P.o L.h T.e < P.o L.h < T.e <

6 Table SI-2. Time-lag effect on the correlations between the proportion of a given fish species in the seabirds diet and CPUE for the same species. In the case of Elegant Terns and Heermann's Gulls, the correlation between sardines and anchovies in their diet was highest with CPUEs of the following season (the lagged values), indicating that their diets can contribute to predict the fishery s success. Brown Pelican diets, in contrast, had higher correlations with CPUEs of the same season in which the diets were estimated. Pacific Sardines Northern Anchovies unlagged lagged unlagged lagged Elegant Terns Heermann's Gulls Brown Pelicans

7 Table SI-3. Coefficients of variation (cv) of the main two dietary elements (Pacific Sardines and Northern Anchovies) of the three seabird species compared to the coefficients of variation of the fleet s CPUEs. Variation in sardine consumption by seabirds is significantly higher (P < 0.05 according to an F-test) than cv in sardine CPUE, while the cv in anchovy consumption by seabirds is significantly lower than the cv of the fleet s CPUE. coefficients of variation Pacific Sardines Northern Anchovies Elegant Terns diets Heermann's Gull diets Brown Pelicans diets Fleet CPUE

8 Table SI-4. Multiple regression ANOVA parameters (coeff. of determination, r 2 ; F-values, and significances, P) of proportion of Pacific Sardine and Northern Anchovy in the diet of the three seabird species as predictors of CPUE for the industrial fleet in the Midriff region. Pacific Sardine Northern Anchovy Predictor partial r 2 F P partial r 2 F P Elegant Tern diet SOI n.s. Heermann s Gull diet SOI n.s. 8

9 Table SI-5. Sampling effort: The values in each cell show the number of birds whose regurgitations were analyzed to determine the species diet. The last row shows the number of years during which diets were studied for each species. Dashes indicate years during which regurgitations were not studied for a particular seabird species. Year Elegant Tern Heerman s Gull Brown Pelican

10 years sampled