¹Biology Department, Algoma University Queen St. East, Sault Ste. Marie, ON, P6A 2G4

²Biology Department, Condordia University, 7141 Sherbrooke St. West, Montreal, Quebec, H4B 1R6

³USGS, Great Lakes Science Center, Hammond Bay Biological Station, 11188 Ray Road, Millersburg MI 49759

⁴Fisheries and Oceans Canada, 1 Canal Dr., Sault Ste. Marie, ON P6A 6W4

December 2012

ABSTRACT:

Sea lamprey, an ectoparasitic pest, invaded the upper Great Lakes in the early 20th century and caused extensive economic damage to a broad variety of native fish populations. We conducted an experimental proof-ofconcept study aimed at investigating whether sea lamprey show an avoidance response to a variety of natural chemical stimuli. If successful, these repellents could contribute to a new alternative control method to be added to the range of control techniques already in use by the Great Lakes Fishery Commission. Our objectives were to investigate (1) whether sea lamprey show avoidance of damaged conspecific cues, damaged heterospecific cues, and direct predator cues, (2) whether this is a general response to injured heterospecific fish or a specific response to injured sea lamprey, (3) determine the length of avoidance response and presence of habituation, and (4) determine whether the response is sex specific and whether it differs between day and -night. During three nighttime and two daytime experiments, ten replicate groups of 10 individual migratory sea lamprey, separated by sex, were exposed to one of the following eleven stimuli (the number of stimuli varied by experiment): distilled water (control), extracts prepared from common white sucker (Catostomus commersonii), suckermouth armoured catfish (Pterygoplichthys pardalis) (heterospecific stimuli), migratory sea lamprey, decayed migratory sea lamprey, sea lamprey ammocoete (conspecific stimuli); two varieties of phenyl-ethyl-amine (free-base and HCl salt) solution, northern water snake (Nerodia sipedon sipedon) washing, human saliva (direct predator cues), and a migratory sea lamprey extract and human saliva combination. Sea lamprey showed a strong nocturnal avoidance response to several injured conspecific cues (injured migratory lamprey, decayed migratory lamprey) as well as direct predator cues, like human saliva (mammalian predator cue) and phenyl-ethyl-amine (a chemical present in the urine of a large number of mammalian carnivores) as well as a combination of injured conspecific cue and direct predator cue (migratory sea lamprey plus human saliva). Interestingly, northern water snake washings, a known predator of lamprey, induced a strong preference response. Further, sea lamprey demonstrated indirectly the ability to associate danger with the alarm cues released from injured sympatric fish species, like the common white sucker. Sea lamprey showed a very weak to no response to tissue extract from P. pardalis, providing support for the above responses being specific, rather than general to any injured fish. The strong avoidance response at night to the stimuli mentioned above lasted for 20 minutes after a 20 minute exposure, and could be induced after experimental subjects being exposed 4 times and 8 times (except human saliva), respectively, to the same stimulus type the previous day. This finding supported the prediction that these stimuli function as alarm cues, because sea lamprey do not habituate to them for up to approx. 24 hours after being exposed to them repeatedly. Northern water snake washing was ignored by sea lamprey after repeated exposure to it. The avoidance responses and the lack of habituation were consistently shown both by all lamprey as well as the moving complement of the experimental “population” in the 4x and the 8x pre-exposure nighttime experiments, presumably because increasingly larger proportion of the experimental subjects were mobile at night, as the migratory season progressed. Daytime experiments performed at low water temperatures early in the migratory season and at high water temperatures later in the season indicated a reduced avoidance response as compared to nighttime findings, with avoidance being shown only by moving animals, but not by resting or hiding individuals. Higher daytime water temperatures resulted in a higher proportion of animals being active; moving sea lamprey strongly avoided injured ammocoete alarm cues at low water temperatures (out of seven experimental stimuli), while migratory sea lamprey alarm cues and PEA (out of six experimental stimuli) induced strong avoidance responses at high water temperatures. There was some evidence for a stronger avoidance response by females as compared to males to some stimuli; however, sex differences in avoidance response to repellents need further research. The above findings raise the realistic possibility of using the above repellents for efficient behavioural manipulation of sea lamprey populations in the wild at night and during the day at high water temperatures, but probably not during the day at water temperatures below 10oC, due to response by a smaller proportion of the population to a reduced number of cues during the day. Further research should explore the effect of alarm cue concentration on the strength of avoidance, as well as the efficiency of application of the above stimuli in the wild, where sea lamprey of both sexes migrate in streams that are variable in size, temperature, microhabitat type and flow conditions.