Susceptibility of Juvenile Steelhead to Avian Predation: the Influence of Individual Fish Characteristics and River Conditions

Identification of the factors that influence susceptibility to predation can aid in developing management strategies to recover fish populations of conservation concern. Predator–prey relationships can be influenced by numerous factors, including prey condition, prey size, and environmental conditions. We investigated these factors by using juvenile steelhead Oncorhynchus mykiss from the Snake River (Pacific Northwest, USA), a distinct population segment that is listed as threatened under the U.S. Endangered Species Act. During 2007–2009, steelhead smolts (n = 25,909) were captured, examined for external condition characteristics (e.g., body injuries, descaling, external signs of disease, fin damage, and ectoparasite infestations), marked with passive integrated transponder (PIT) tags, and released to continue their out-migration. Recoveries of PIT tags on a downstream colony of Caspian terns Hydroprogne caspia (n = 913 tags) indicated that steelhead susceptibility to Caspian tern predation increased significantly with decreases in steelhead external condition, decreased water discharge, and decreased water clarity. Susceptibility to Caspian tern predation also increased with increasing steelhead fork length up to 202 mm but then decreased for longer steelhead. Recoveries of PIT tags on a downstream colony of double-crested cormorants Phalacrocorax auritus (n = 493 tags) indicated that steelhead susceptibility to double-crested cormorant predation increased significantly with declining external condition of steelhead, and that steelhead of hatchery origin were more susceptible than their wild counterparts. Results indicate that steelhead susceptibility to avian predation is dependent on fish condition and length and is influenced by river conditions and rearing environment. Predation is a key ecological process influencing the size of fish populations and the composition of fish communities (Sih 1987). Predator–prey relationships are often influenced by numerous factors, including prey condition (see review by Mesa *Corresponding author: [email protected] 1Present address: Real Time Research, Inc., 52 Southwest Roosevelt Avenue, Bend, Oregon 97702, USA. Received February 23, 2012; accepted July 18, 2012 Published online October 15, 2012 et al. 1994), prey size (see review by Sogard 1997), and environmental factors (Gregory 1993; Mesa 1994; Mesa and Warren 1997; Gregory and Levings 1998; De Robertis et al. 2003). An understanding of how these factors influence predator–prey 1586 D ow nl oa de d by [ O re go n St at e U ni ve rs ity ] at 1 3: 32 1 8 M ar ch 2 01 3 JUVENILE STEELHEAD SUSCEPTIBILITY TO AVIAN PREDATION 1587 relationships has important implications for fitness at both the individual and population levels and also provides valuable information regarding the efficacy of top-down ecosystem management (i.e., predator management). The theory that predators disproportionately prey on individuals that are in substandard condition (e.g., weak, sick, stressed, or inexperienced; sensu Temple 1987) is widely accepted and has been well supported in fish predation studies (see review by Mesa et al. 1994). The occurrence and magnitude of conditiondependent predation may vary as a function of predator foraging strategy. In theory, predators that chase their prey should be more likely to disproportionately take individuals in poorer condition compared to predators that ambush their prey (Estes and Goddard 1967; Schaller 1968). Studies evaluating predator–prey interactions and the efficacy of predator management, however, rarely consider the influence of prey condition and predator foraging strategies (Mesa et al. 1994). For instance, the success of predator management efforts to increase prey populations would be diminished if the prey would have died from other causes (e.g., disease, competition, or other predators) regardless of the predation event (Errington 1956; Temple 1987). Thus, the degree to which the mortality caused by predation is compensatory is a primary consideration for programs that seek to restore prey populations through predator management. Within populations of Pacific salmon Oncorhynchus spp., increased susceptibility to predation by piscivorous fish and birds has been attributed to differences in fish behavior, condition, size, rearing, and environmental conditions (Gregory and Levings 1998; Mesa et al. 1998; Collis et al. 2002; Schreck et al. 2006; Kennedy et al. 2007). Environmental conditions experienced by juvenile salmonids during out-migration (e.g., water flow, turbidity, or factors associated with migration timing) are known to increase stress, reduce fish performance, and increase susceptibility to predation (Raymond 1979; Gregory and Levings 1998; Budy et al. 2002; Schreck et al. 2006). The external condition (e.g., body injuries, descaling, external signs of disease, fin damage, and ectoparasite infestations) of out-migrating juvenile steelhead O. mykiss has been linked to internal fish condition and to survival during out-migration (Hostetter et al. 2011). Although some studies have suggested that the condition of smolts influences their susceptibility to avian predation (Schreck et al. 2006; Kennedy et al. 2007), no direct link between external fish condition and susceptibility to avian predation has been documented in the wild. Predator foraging strategy can play an important role in determining which factors influence prey susceptibility to predation (Estes and Goddard 1967; Schaller 1968; Temple 1987). In the Columbia River basin, Caspian terns Hydroprogne caspia and double-crested cormorants Phalacrocorax auritus are responsible for the majority of the avian predation mortalities among smolts (Collis et al. 2002; Evans et al. 2012), but the two waterbird species employ very different foraging behaviors. Double-crested cormorants are pursuit divers that actively hunt their prey underwater (Hatch 1999), whereas Caspian terns are plunge divers that capture (i.e., ambush) their prey at or near the water surface (Cuthbert and Wires 1999). In addition to foraging behavior, these predators also differ in size, gape width, and foraging range from the breeding colony (Cuthbert and Wires 1999; Hatch 1999), suggesting that factors influencing the susceptibility of juvenile salmonids to avian predation may differ between the two predator species. Avian predation on salmonid smolts has been identified as one of several factors limiting recovery of salmonid evolutionarily significant units (ESUs) and steelhead distinct population segments (Waples 1991) within the Columbia River basin that are listed as threatened or endangered under the U.S. Endangered Species Act (ESA; Roby et al. 2003; Lyons 2010). Management efforts to reduce the impact of avian predation on survival of juvenile salmonids within the Columbia River estuary are currently being implemented (Roby et al. 2002; USFWS 2006). However, knowledge of how individual fish characteristics and environmental factors influence the susceptibility of juvenile salmonids to avian predation is extremely limited. In the present study, we tested three hypotheses regarding the predator–prey relationship between piscivorous birds (e.g., Caspian terns and double-crested cormorants) and anadromous salmonids (e.g., steelhead) in the Columbia River basin. Hypothesis 1 was that the probability of a smolt being consumed by an avian predator is influenced by both individual fish characteristics (e.g., size, rearing type [hatchery versus wild], and external condition) and environmental factors (e.g., turbidity and water discharge rate). Hypothesis 2 was that avian predation on salmonid smolts is condition dependent, such that the probability of a smolt being consumed by an avian predator increases with declining external condition of the smolt. Hypothesis 3 was that factors influencing smolt susceptibility to avian predation will vary with the species of avian predator. Snake River steelhead were selected for this study because prior research suggested that among salmonids in the mid-Columbia River, steelhead smolts were the most susceptible to avian predation (Antolos et al. 2005). In addition, data describing the impact of avian predation are needed to evaluate recovery options for Snake River steelhead, which are listed as threatened under the ESA (Good et al. 2005).