We initiated a study in 1997 to investigate the impacts of piscivorous colonial waterbirds on the survival of juvenile salmonids ( Oncorhynchus spp.) in the lower Columbia River (Roby et al. 1998; Collis et al. 2002). The study area included the Columbia River from the mouth (river km 0) to the head of the impoundment created by McNary Dam (river km 553). The species of piscivorous waterbirds investigated were California gulls (Larus californicus), ring-billed gulls (L.delawarensis), glaucous-winged/western gulls (L. glaucescens X L. occidentalis), Caspian terns (Sterna caspia), double-crested cormorants (Phalacrocorax auritus), and, more recently, American white pelicans (Pelecanus erythrorhynchos) and California brown pelicans (Pelecanus occidentalis californicus). This study revealed differences in diet composition among the various bird species and colony locations (Collis et al. 2002). Terns, cormorants, and pelicans were strictly piscivorous, whereas the three gull species consumed a diverse array of food types. Gulls nesting at up-river colonies consumed primarily anthropogenic food items (e.g., cherries, potatoes, human refuse).

In general, piscivorous waterbirds nesting in the Columbia River estuary consumed more juvenile salmonids than those nesting up-river. On Rice Island (river km 34), salmonids accounted for 74% of the diet in Caspian terns, 46% in double-crested cormorants, and 11% in glaucous-winged/western gulls (Collis et al. 2002). Juvenile salmonids were especially prevalent in the diets of colonial waterbirds on Rice Island during April and May. By comparison, juvenile salmonids were significantly less prevalent in the diets of cormorants and gulls nesting above The Dalles Dam, although Caspian terns nesting in the John Day and McNary pools also consumed a high proportion of juvenile salmonids. These up-river Caspian tern colonies combined, however, were only about 1/10th the size of the Rice Island tern colony. These results indicated that avian predation on juvenile salmonids is more prevalent in the Columbia River estuary than in the Lower and Middle Columbia River. Furthermore, the high incidence of salmonids in the diets of Caspian terns, cormorants, and gulls nesting on Rice Island suggested that the impact of avian predation on survival of smolts would be reduced by discouraging piscivorous birds from nesting there, while encouraging nesting on East Sand Island and other sites closer to marine foraging areas.

In 1997 and 1998, Caspian terns nesting on Rice Island consumed the highest percentage of juvenile salmonids of those species of piscivorous colonial waterbirds nesting in the Columbia River estuary (Collis et al. 2002). Rice Island , a dredged material disposal site, supported an expanding colony of about 8,500 breeding pairs of terns in 1998 (Collis et al. 2002). This colony was the largest known Caspian tern breeding colony in the world. Using bioenergetics modeling, we estimated that in 1998 this tern colony consumed approximately 13% (95% c.i. = 9.1%–16.9%; Roby et al. 2003) of the estimated 96.6 million out-migrating smolts that reached the estuary during the 1998 migration year. Analysis of over 36,000 smolt PIT tags recovered from the Caspian tern breeding colony on Rice Island revealed that over 13.5% of all PIT-tagged steelhead smolts (O. mykiss) detected migrating in-river through Bonneville Dam were consumed by terns in 1998 (Collis et al. 2001).

The magnitude of predation on juvenile salmonids by Rice Island terns led to management action in 1999 (Roby et al. 2002). A pilot study was conducted to determine whether the Rice Island tern colony could be relocated 26 km closer to the ocean on East Sand Island (river km 8), where it was hoped terns would consume fewer salmonids. Efforts to attract terns to nest on East Sand Island included creation of nesting habitat, use of social attraction techniques, and predator control, with concurrent efforts to discourage terns from nesting on Rice Island. This approach was successful, and in three years all nesting terns shifted from Rice Island to East Sand Island. Juvenile salmonids decreased and marine forage fishes (e.g., Pacific herring [Clupea pallasi], anchovies [Engraulidae], smelt [Osmeridae], and surfperch [Embiotocidae]) increased in the diet of Caspian terns nesting on East Sand Island compared with terns nesting on Rice Island.

Our monitoring of tern management in the Columbia River estuary has continued through the 2005 nesting season. In 2005, the size of the Caspian tern colony on East Sand Island was approximately 8,800 nesting pairs, nearly the same size as the Rice Island tern colony in 1998. Consumption of juvenile salmonids by the East Sand Island tern colony in 2005 was approximately 3.6 million smolts (95% c.i. = 2.0–4.2 million), ca. 9 million fewer smolts consumed compared to 1998, when all terns nested on Rice Island. Caspian terns nesting on East Sand Island continue to rely primarily on marine forage fishes as a food supply, even in 2005 when availability of marine forage fishes declined due to poor ocean conditions.

Although numbers of Caspian terns nesting in the Columbia River estuary have remained stable over the last 8 years, the numbers of double-crested cormorants nesting on East Sand Island have more than doubled during the same period to ca. 12,500 breeding pairs. This colony is now the largest known breeding colony for the species in North America (Anderson et al. 2004). Although juvenile salmonids represented only ca. 5% of the diet of cormorants nesting on East Sand Island in 2004, estimated smolt consumption by the cormorant colony (6.4 million smolts; 95% c.i. = 2.5–10.3 million) was comparable to or greater than that of the East Sand Island tern colony (CBR 2005). This is due mostly to the larger size of the cormorant colony on East Sand Island and the greater food requirements of cormorants relative to terns. The nesting success of the double-crested cormorant colony on East Sand Island in 2005 (1.38 young/breeding pair) was more than three times the nesting success of the East Sand Island Caspian tern colony. The double-crested cormorant colony is expected to continue to expand for the foreseeable future, perhaps posing an increasing risk to survival of juvenile salmonids in the estuary.

The Caspian tern colony on Crescent Island in the mid-Columbia River is the largest of its kind on the Columbia Plateau (Antolos et al. 2004). This colony, which consisted of ca. 476 nesting pairs in 2005, is roughly 1/20th the size of the East Sand Island tern colony in the Columbia River estuary, however. At Crescent Island, salmonid smolts represented about 65% of tern prey items in 2005. Consumption of juvenile salmonids by the Crescent Island tern colony was approximately 440,000 smolts (95% c.i. = 340,000–550,000 smolts) in 2005, compared to about 3.6 million smolts consumed by East Sand Island terns during the same year.

Despite the much smaller numbers of salmonid smolts consumed annually by the Crescent Island tern colony, predation rates on certain salmonid stocks have been unexpectedly high, particularly on some steelhead stocks during years of low river flow (Antolos et al. 2005). For example, PIT tag recoveries on the tern colony in 2004 and 2005 (low flow years) indicate that the predation rate by Crescent Island terns on in-river Snake River steelhead smolts was 34% and 17%, respectively (based on the proportion of PIT-tagged smolts interrogated at Lower Monumental Dam that were subsequently recovered on the Crescent Island tern colony). In-river steelhead smolts from the Snake River were more vulnerable to tern predation than in-river steelhead smolts from the Upper and Middle Columbia River (predation rates between ca. 6% and 4%, based on the proportion of PIT-tagged smolts interrogated at Rock Island Dam that were subsequently recovered on the Crescent Island tern colony in 2004 and 2005). Substantial stock-specific and temporal variability in predation rates were observed in both 2004 and 2005, with predation rates on certain in-river stocks of steelhead ranged from less than one percent to upwards of 30%; an indication that smolt vulnerability to Crescent Island terns changes throughout the nesting season and is not easily characterized by a single point estimate. Furthermore, the higher predation rate on in-river migrants from the Snake River ws offset by the transportation of > 95% of Snake River steelhead smolts past Crescent Island. Conversely, no juvenile salmonids that originated from the Upper Columbia River were transported past Crescent Island, resulting in the entire run being susceptible to predation by Crescent Island terns. Predation rates on salmonids by Crescent Island terns are unlikely to increase appreciably considering habitat constraints on tern colony expansion, limited capacity for increased per capita smolt consumption by terns, and current high transportation rates past Crescent Island for Snake River smolts.

The colony of double-crested cormorants on Foundation Island, near the confluence of the Snake and Columbia rivers and less than 8 Rkm from Crescent Island, is the largest cormorant colony on the mid-Columbia River. This colony consisted of over 315 breeding pairs in 2005, only about 1/40 th the size of the cormorant colony on East Sand Island in the Columbia River estuary. The proportion of juvenile salmonids in the diet of Foundation Island cormorants was much less than that of Crescent Island terns, but the incidence of salmonids in the diet of Foundation Island cormorants was much higher early in the nesting season than during the chick-rearing period. A comparison of PIT tag recovery rates between the Crescent Island tern colony and Foundation Island cormorant colony suggests that the cormorants consumed ca. 1/4 th as many smolts as the terns in 2005. The Foundation Island cormorant colony is growing slowly, however, and the consumption of salmonids, especially early in the season, appears to be increasing. The American white pelican colony on nearby Badger Island is also growing (> 500 pairs in 2005), but based on smolt PIT tag detections on the pelican colony by NOAA Fisheries, this colony is not a source of significant smolt mortality. For example, only 611 smolt PIT tags were recovered on the Badger Island pelican colony in 2005, compared to 16,003 smolt PIT tags and 4,101 smolt PIT tags recovered from the upriver tern and cormorant colonies, respectively.

A system-wide assessment of avian predation using the available data indicates that the most significant impact on survival of juvenile salmonids occurs in the estuary (Ryan et al. in prep). Caspian terns and double-crested cormorants nesting on East Sand Island together consumed ca. 10 million smolts in 2004 (CBR 2005). Additionally, when compared to the impact of avian predation further up-river, avian predation that occurs in the estuary affects juvenile salmonids that have survived freshwater migration to the estuary and presumably have a higher probability of survival compared to those fish that have not yet completed their out-migration. Finally, juvenile salmonids from every ESA-listed stock in the Columbia River Basin are susceptible to predation in the estuary because all surviving fish must migrate in-river through the estuary. For these reasons, management of terns and cormorants nesting on East Sand Island has the greatest potential to benefit ESA-listed salmonids across the Columbia Basin, compared to management of other bird populations. One possible exception is the Caspian tern colony on Crescent Island, where tern management may benefit certain ESA-listed ESUs of steelhead.

Further management of Caspian terns to reduce losses of juvenile salmonids in the estuary is imminent; the Caspian Tern Management Plan for the Columbia River Estuary lists as the management goal the redistribution of approximately two-thirds of the East Sand Island colony to alternative colony sites in Washington, Oregon, and California (USFWS 2005). Management to reduce or limit smolt losses to the expanding double-crested cormorant colony in the estuary and the Caspian tern colony on Crescent Island in the mid-Columbia River are under consideration. Options for management initiatives to reduce the impact of these avian predators on survival of ESA-listed salmonid smolts include partial or complete relocation of these colonies to alternative sites where Columbia Basin salmonids would not constitute a significant proportion of the diet. Colony relocation would likely involve a combination of attraction to the new site using habitat enhancement, social attraction, and nest predator deterrence, coupled with reductions in the availability of suitable nesting habitat at the old colony site. Pilot studies designed to test the feasibility of employing habitat enhancement and social attraction (i.e., decoys, audio playback systems) for relocating nesting cormorants have shown some promise; cormorants were induced to nest at two sites on East Sand Island where they had not previously nested, and one site on Miller Sands Spit where they had not attempted to nest in several years. Restoration, enhancement, or establishment of tern and cormorant colony sites outside the Columbia River estuary would likely benefit Columbia Basin salmonids without negatively affecting protected populations of fish-eating birds. If resource management agencies decide that further management of avian predators (e.g., the East Sand Island cormorant colony, the Crescent Island tern colony) is warranted to increase survival of ESA-listed salmonids, additional research in support of an Environmental Impact Statement will be required.

References

Anderson, C.D., D.D. Roby, and K. Collis. 2004. Conservation implications of the large colony of double-crested cormorants on East Sand Island, Columbia River estuary, Oregon, USA. Waterbirds 27:155-160.

Anderson, C.D., D.D. Roby, and K. Collis. 2004. Conservation implications of the large colony of double-crested cormorants on East Sand Island, Columbia River estuary, Oregon, USA. Waterbirds 27:155-160.

Antolos, M., D.D. Roby, and K. Collis. 2004. Breeding ecology of Caspian terns at colonies on the Columbia Plateau. Northwest Science 787:303-312.

Antolos, M., D.D. Roby, D.E. Lyons, K. Collis, A.F. Evans, M. Hawbecker, and Brad A. Ryan. 2005. Caspian tern predation on juvenile salmonids in the Mid-Columbia River. Transactions of the American Fisheries Society 134:466-480.

CBR ( Columbia Bird Research). 2005. Caspian Tern Research on the Lower Columbia River: 2004 Draft Season Summary. Real Time Research, Bend, Oregon. Available on-line at http://columbiabirdresearch.org/.

Collis, K., D.D. Roby, D.P. Craig, B.A. Ryan, and R.D. Ledgerwood. 2001. Colonial waterbird predation on juvenile salmonids tagged with passive integrated transponders in the Columbia River estuary: vulnerability of different salmonid species, stocks, and rearing types. Transactions of the American Fisheries Society 130:385-396.

Collis, K., D.D. Roby, D.P. Craig, S. Adamany, J. Adkins, and D.E. Lyons. 2002. Colony size and diet composition of piscivorous waterbirds on the lower Columbia River: Implications for losses of juvenile salmonids to avian predation. Transactions of the American Fisheries Society 131:537–550.

Roby, D. D., D. P. Craig, K. Collis, and S. L. Adamany. 1998. Avian predation on juvenile salmonids in the lower Columbia River. 1997 Annual Report of the Oregon Cooperative Fish and Wildlife Research Unit at Oregon State University to Bonneville Power Administration and U.S. Army Corps of Engineers, Portland, Oregon, USA.

Roby, D.D., K. Collis, D.E. Lyons, D.P. Craig, J. Adkins, A.M. Myers, and R.M. Suryan. 2002. Effects of colony relocation on diet and productivity of Caspian terns. Journal of Wildlife Management 66: 662–673.

Roby, D.D., D.E. Lyons, D.P. Craig, K. Collis, and G.H. Visser. 2003. Quantifying the effect of predators on endangered species using a bioenergetics approach: Caspian terns and juvenile salmonids in the Columbia River estuary. Canadian Journal of Zoology 81:250-265.

Ryan, B.A., B.P. Sanford, K. Collis, A.F. Evans, and D.D. Roby. In prep. Predation on juvenile salmonids by colonial waterbirds in the Columbia River basin: System-wide assessment of avian predation based on PIT tag recoveries.

USFWS ( U.S. Fish and Wildlife Service). 2005. Caspian tern management to reduce predation of juvenile salmonids in the Columbia River estuary: Final Environmental Impact Statement, January 2005. Migratory Birds and Habitat Program, Portland OR.