Proc. Natl. Acad. Sci. USA Vol. 80, pp. 4766-4769, August 1983 Ecology Ornitholimnology: Effects of grazing by the Andean flamingo (Phoenicoparrus andinus) (predation/Surirella/lacustrine microbenthos) STUART H. HURLBERT AND CECILY C. Y. CHANG Department of Biology, San Diego State University, San Diego, California 92182 Communicated by G. Evelyn Hutchinson, May 6, 1983 ABSTRACT Experimental exclusion of the Andean flamingo (Phoenicoparrus andinus) from shallow water areas of a salt lake in the Bolivian Andes caused large increases in the biomass of mi- croorganisms inhabiting the surface sediments, especially a large diatom (Surirella wetzeli), amebas, ciliates, and nematodes. This is a conservative demonstration of the influences that water birds in general exert on the structure of aquatic ecosystems. Of the -8,900 species of birds in the world roughly 9% feed entirely or predominantly on aquatic organisms. Their diets range over the entire spectrum of available foods, from fish to in- vertebrates, from vascular plants to microscopic algae. The more abundant of these birds may strongly affect the dynamics of their prey populations and, indirectly, the dynamics of entire aquatic ecosystems. However, few experimental studies of these interactions have been attempted (1-4), and we scarcely have an inkling of how the structure and functioning of any aquatic ecosystem would be altered by the disappearance of one or more of the bird spe- cies feeding in it. In this report we document the strong influence exerted by the Andean flamingo (Phoenicoparrus andinus) on lacustrine microbenthos, the assemblage of microscopic organisms in- habiting the surface sediments of a lake bottom. P. andinus is a.common inhabitant of numerous shallow, mostly saline lakes of the altiplano region of the central Andes of South America (5-7). Two otherflamingos, James' (Phoenicoparrusjamesi) and the Chilean (Phoenicopterus chilensis), also occur abundantly on many of these same lakes. Other flamingo species are dom- inant components of salt lake and coastal lagoon ecosystems in Africa and Eurasia, and the fossil record indicates that, in the past, still other flamingos occupied similar environments in North America and Australia (8-10). The role that flamingos play in the functioning of these lake ecosystems is thus of general in- terest. We suspect that this role is great in consequence of flamingos' high feeding rates and the large size of their feeding FIG. 1. Location of study site in Laguna Puripica Chico, Bolivia, flocks. and arrangement of control (F = flamingos) and exclosure (NF = no flamingos) areas. STUDY AREA AND METHODS To test this suspicion we conducted an exclosure experiment more numerous than the other two species; this pattern was during January and February 1979 in Laguna Puripica Chico, maintained throughout our study (Table 1). On earlier visits we a small (1.0 km2), shallow (maximal depth, ca. 50 cm), slightly had found even larger numbers of flamingos here. Approxi- saline (8.2 g/liter), high-altitude (4,393 m) lake in the desertic mately 3,000 (66% P. jamesi, 29% P. andinus, and 5% P. chi- altiplano of the southwesternmost tip (22031' S, 67°30' W) of lensis) were observed on the lake in December 1975 (6) and Bolivia; this is one of several lakes scattered around the margin about 5,700 (65% P.jamesi, 33% P. andinus, and 2% P. chilensis) of a salt-encrusted basin called Salar de Chalviri (Fig. 1). On in November 1977 (7). By way of comparison, the lesser flamin- visits in late December 1978 and early January 1979 we found go (Phoeniconais minor) occurs on some African lakes at 10 times flamingos to be abundant on this lake and P. andinus to be much these densities (11). On January 2 we selected a mudflat that was being used as a P. but not the other The publication costs of this article were defrayed in part bypage charge feeding ground by andinus by species. payment. This article must therefore be hereby marked "advertise- ment" in accordance with 18 U.S.C. §1734 solely to indicate this fact. Abbreviations: F, flamingo(s); NF, no flamingo(s). 4766 Downloaded by guest on September 28, 2021 Ecology: Hurlbert and Chang Proc. Natl. Acad. Sci. USA 80 (1983) 4767 Table 1. Effects of the Andean flamingo (P. andinus) on the microbenthos of Laguna Puripica Chico, Bolivia Sampling date Taxon or feature January 3a January 19b February 4 February 24c Time since exclosures established, days 1 17 31 51 Water depth, cm 0-1 2-4 9-11 3-5 Number of flamingos on lake P. andinus 654 716 1,159 1,000 P.jamesi 81 9 0 12 P. chilensis 29 75 68 30 F NF F NF F NF F NF Individuals, no. per mm2 of sediment surface Diatoms, totald 4,117 2,895 890 859 1,816 631 7,538 12,112 Surirella wetzelie 32 30 37 54 27 12 52 156* Navicula spp.' 3,764 2,733 795 761 1,613 594 7,077 10,631 Amphora spp. 17 33 0.3 0.8 0.0 0.7 280 553 Nitzschia spp. 78 58 12 13 46 5 76.5 330 Protozoa, total 4.0 5.9 6.7 31.2+ 2.8 7.6 4.7 52.2t Amebasg 2.8 1.8 6.4 29.2 2.5 6.5 2.8 43.8t Ciliatesh 1.6 4.0 0.6 2.0 0.1 1.0 1.4 9.0O Nematodes' 0.59 0.66 0.82 0.44 0.30 1.31 0.50 1.96X Biomass, tug per mm2 of sediment surface Blue-green algae, totali 0.146 0.103 0.027 0.360 0.009 0.140 1.54 3.16 Diatoms, totald 17.5 13.7 15.3 25.7 12.8 6.1 30.9 73.3+ Surirella wetzelie 13.0 10.0 13.8 23.3 10.1 4.8 20.0 58.0T Navicula spp.f 2.48 2.20 0.69 1.22 1.02 9.56 3.77 7.58* Amphora spp. 0.20 0.19 0.005 0.015 0.00 0.01 2.8 3.5 Nitzschia spp. 0.19 0.24 0.04 0.03 0.12 0.001 0.19 0.91 Protozoa, total 0.80 2.24 0.61 3.62t 0.24 1.66 1.36 8.98T Amebasg 0.20 0.13 0.48 2.20t 0.18 0.49 0.21 3.29t Ciliatesh 0.62 2.10 0.23 1.32t 0.04 1.16 1.15 5.28+ Nematodes' 0.15 0.48 0.48 0.14 0.14 0.22 0.26 1.05T Total microbenthos 18.7 16.2 16.5 30.1 13.3 8.1 35.1 86.2t Tabulated values for the microbenthos are "hybrid" means, each the arithmetic mean of: (i) the median of and (ii) the arithmetic mean of the 4 or 10 replicate values. Statistical significance of each difference between NF and F areas was assessed by the Mann-Whitney U test and is denoted, by symbols above the NF means, as follows: no symbol, P > 0.10; *, 0.10 - P > 0.05; t, 0.05 > P > 0.01; and T, P < 0.01. a Census data are for January 4. bCensus data are for January 31; values do not include 150 flamingos unidentified to species. CCensus data are for February 18; values do not include 200 flamingos unidentified to species. dThirteen genera of diatoms were encountered, the great majority contributing negligibly to total diatom abundance. eAveraged 135 ,um in length. An individual that size has volume of -373,000 ,m3 and occupies about 9,100 /Im2 of sediment surface. fAt least 10 species were present, but 3 small (mean valve lengths, 10-30 ,um), chain-forming (chain ranging up to at least 250 ,um in length) species strongly dominated both numerically and in terms of biomass. An undetermined species, usually contracted into an approximate spherical shape about 30 ,um in diameter. hFour undetermined hypotrich and holotrich species, ranging approximately from 40 to 130 ,um in length. 'Taxonomic study of 7 specimens found two genera to be represented: Ethmolaimus and Monohystera (E. M. Noffsinger, personal communication). Mean length for all 131 nematodes measured was 793 ,um (range: 147-3,330 ,tm). Includes only filamentous genera (Lyngbya, Oscillatoria, Schizothrix, and Anabaena); unicellular forms probably were present but contributed negligibly to total blue-green biomass. This was located about 70 m off the eastern shore, had a thin region of each area and combined to vield a single composite film of water over it, and consisted of 10-15 cm of soft sedi- sample for that area. The only locations avoided in our sampling ments overlying a firm sandy bottom. In a row along this flat were where the sediment was covered bv excrement or had a and spaced at about 15-m intervals from each other, we fenced deep depression (fresh flamingo track) in it. The larger more off four 4 x 3 m experimental (NF) areas, thereby excluding active organisms-e.g., nematodes-mav have been under- flamingos from them. Each fence consisted of four stakes pro- represented by this sampling method. Samples were preserved jecting about 1.2 m above the water, with two strands of nvlon in 5% formaldehyde and analvzed on return to San Diego. An twine connecting them. A total of 10 control (F) areas, two be- amount of sample equivalent to 0.015, 0.094, 0.17, or 3.5 mm2 tween each pair of NF areas and two at both ends of the row, of bottom sediment (depending on the taxon) was examined un- were delimited by imaginary lines (Fig.