Oecologia (1993) 95:210-219 Oecologia Springer-Verlag 1993 Interaction of a biotic factor (predator presence) and an abiotic factor (low oxygen) as an influence on benthic invertebrate communities Cynthia S. Kolar*, Frank J. Rahel Department of Zoology and Physiology, University of Wyoming, Laramie, WY 82071, USA Received: 23 October 1992 / Accepted: 7 April 1993 Abstract. We examined the response of benthic in- and beetle larvae). Because invertebrates differ in their vertebrates to hypoxia and predation risk in bioassay and ability to withstand hypoxia, episodes of winter hypoxia behavioral experiments. In the bioassay, four in- could have long-lasting effects on benthic invertebrate vertebrate species differed widely in their tolerance of communities either by direct mortality or selective preda- hypoxia. The mayfly, Callibaetis montanus, and the beetle tion on less tolerant taxa. larva, Hydaticus rnodestus, exhibited a low tolerance of hypoxia, the amphipod, Gammarus lacustris, was inter- Key words: Hypoxia - Benthos - Invertebrates Preda- mediate in its response and the caddisfly, Hesperophylax tor-intimidation - Behavior occidentalis, showed high tolerance of hypoxia. In the behavioral experiments, we observed the response of these benthic invertebrates, which differ in locomotor abilities, to vertical oxygen and temperature gradients Episodic disturbance and predation often interact to similar to those in an ice-covered pond. With adequate influence community structure. Typically, this involves oxygen, invertebrates typically remained on the bottom loss or reductions in predators due to severe abiotic substrate. As benthic oxygen declined in the absence of conditions and a subsequent restructuring of the com- fish, all taxa moved above the benthic refuge to areas munity as species previously held in check by predators with higher oxygen concentrations. In the presence of come to dominate the system. In alpine ponds, winter fish mayflies increased activity whereas all other taxa freezing of the water column eliminates amphibians and decreased activity in response to hypoxia. Mayflies and results in a zooplankton community dominated by large amphipods remained in the benthic refuge longer and species: where amphibians persist, small zooplankton endured lower oxygen concentrations whereas the verti- dominate (Dodson 1970). A brief period of unsuitable cal distribution of caddisflies and beetle larvae was not temperature-oxygen conditions during summer stratifi- influenced by the presence of fish. As benthic oxygen cation can cause fish die-offs that in turn cause long-last- declined in the presence of fish, all but the beetle larva ing changes in the phytoplankton community and ulti- reduced activity over all oxygen concentrations com- mately water quality of eutrophic lakes (Vanni et al. pared to when fish were absent. As benthic oxygen con- 1990). Elimination of piscivorous fish by brief periods of tinued to decline, mayflies and amphipods moved above winter anoxia can result in complete transformation of the benthic refuge and were preyed upon by fish. Thus, fish and zooplankton communities as changes in preda- highly mobile taxa unable to tolerate hypoxia (mayflies tor-prey interactions cascade through lower trophic and amphipods) responded behaviorally to declining levels (Tonn and Paszkowski 1986; Carpenter 1988; Hall oxygen concentrations by migrating upward in the water and Ehlinger 1989). column. Taxa that were less mobile (beetle larvae) or Episodes of unfavorable, abiotic conditions can affect hypoxia-tolerant (caddisflies) showed less of a response. community interactions even though organisms may not Taxa most vulnerable to fish predation (mayflies and be directly killed. Behavioral avoidance of unfavorable amphipods) showed a stronger behavioral response to conditions may result in organisms migrating to new predator presence than those less vulnerable (caddisflies environments where they face increased predation or competition (Sousa 1984; Wolf and Kramer 1987). For * Present address: National Fisheries Research Center-Great example, young perch Percaflavescens leave cattail beds Lakes, United States Fish and Wildlife Service, 1451 Green Road, and move into areas with higher predation risk when Ann Arbor, MI 48105, USA dissolved oxygen concentrations in prairie ponds drop Correspondence to: F.J. Rahel during summer nights (Suthers and Gee 1986). Estuarine 211 fish migrate inshore during periods of summer hypoxia Materials and methods even though this may result in exposure to lethal tem- peratures or reduction in reproductive success (Coutant Bioassay : Tolerance of anoxia 1985; Breitburg 1992). Benthic invertebrates may be particularly vulnerable Bioassays were run to rank invertebrates by their ability to with- to interactions between severe abiotic stress and preda- stand hypoxia. Both the bioassay and behavioral experiments used tion. Seasonal or episodic occurrence of low dissolved a flow-through laboratory apparatus to remove the oxygen and chill experimental water to 4 ~ C. The system created vertical temperature oxygen concentrations (hypoxia) in the benthic region is and dissolved oxygen gradients similar to those found during winter common in both marine and freshwater habitats (Green- in shallow ponds with oxygenated, 0 ~ C water under the ice and bank 1945; Rossignal-Strick 1985; Swanson and Parker hypoxic, 4 ~ C water near the bottom substrate (see Fig. 2 in Rahel 1988; Rahel 1990). Shallow lakes having extended and Kolar 1990). The system relied on the temperature-dependent periods of ice-cover are prone to winterkill, i.e. the de- density of water to maintain temperature and dissolved oxygen velopment of low oxygen and associated conditions (e.g. stratification within the experimental chamber and is described elsewhere (Rahe11989). Oxygen was removed by bubbling nitrogen elevated hydrogen sulfide levels) stressful to aquatic or- through the incoming water. ganisms. In extreme cases, the entire water column be- We modified the system described above for the bioassay. After comes anoxic and massive mortality of aquatic organ- water left the oxygen-stripping columns and the chilling tank, it isms results. Often, however, low oxygen is limited to the flowed into a small Plexiglas tank (35 x 22 x 15 cm) placed in a 4 ~ C benthic region and mobile aquatic organisms can avoid water bath. A sodium sulfite solution (20-40 mg/L) dripped into mortality by migrating up in the water column (Nagell this tank to further reduce the dissolved oxygen to about 0.15=k0.05 mg/L 02. Similar concentrations of sodium sulfite did 1977; Magnuson et al. 1985). not alter fish behavior (Kramer and McClure 1982). Wolf and Avoidance of low benthic oxygen by vertical migra- Kramer (i 987) used sodium sulfite to produce hypoxia in a variety tion to the ice-water interface has been observed among of laboratory and field studies with no apparent ill effects. The aquatic invertebrates (Sikorowa 1968; Nagell 1980; Brit- system was set up and allowed to run for 12 h until the dissolved tain and NageU 1981). This strategy works when fish are oxygen concentration equilibrated. Dissolved oxygen concentration absent, but can result in substantial mortality from was measured with a Yellow Springs Instruments Model 57 dis- solved oxygen meter (Yellow Springs Instruments, Anitoch, OH, predation when fish are present (Rahel and Kolar 1990). USA). We collected invertebrates from fishless ponds at the Red Because benthic invertebrates differ in their ability to Buttes Laboratory, about 20 km south of Laramie, WY. All organ- withstand low oxygen concentrations (Jacob et al. 1984; isms were kept in holding tanks at 4 ~ C for 2 weeks prior to use in Davies et al. 1987) and in their vulnerability to fish a 12-h light 12-h dark light regime. Each invertebrate was used only predators (Crowder and Cooper 1982; Morin 1984), once. In the bioassay, invertebrates were subjected to a single low winter hypoxia could alter benthic community com- dissolved oxygen concentration for 48 h. Ten individuals of each invertebrate species were placed in position through both direct mortality and enhanced separate plastic mesh boxes, submerged in anoxic water and ob- vulnerability to predation. Thus, interaction of an abiotic servations on survival were taken every 6 h over a 48 h period. The factor (hypoxia) and a biotic factor (predation) could following invertebrate species were used: the amphipod Garnmarus have important consequences for benthic invertebrate lacustris, the mayfly nymph Callibaetis montanus, the caddisfly larva assemblages in waters that develop dissolved oxygen Hesperophylax occidentalis, and the beetle larva Hydaticus modes- gradients during winter ice-cover. tus. Because these invertebrates become lethargic in anoxia, it was necessary to standardize survival determination. To do this, mesh We examined how various benthic invertebrates bal- boxes were removed from the experimental chambers and placed in ance the conflicting demands of avoiding low benthic normoxic water at every check period. An animal was considered oxygen and fish predation. We exposed benthic in- dead when it did not respond to prodding after 30 s. The mesh boxes vertebrates having different locomotor abilities to hypox- were then replaced in the tank. Two replicate bioassays were run. ia under simulated winter conditions in the presence and We submerged ten individuals of each species in plastic mesh boxes absence offish. The mayfly, Callibaetis montanus, and the