New Insight Into the Spawning Behavior of Lake Trout, Salvelinus Namaycush, from a Recovering Population in the Laurentian Great Lakes

Environ Biol Fish DOI 10.1007/s10641-014-0247-6

New insight into the spawning behavior of lake trout, Salvelinus namaycush, from a recovering population in the Laurentian Great Lakes

T. R . B i n d e r & H. T. Thompson & A. M. Muir & S. C. Riley & J. E. Marsden & C. R. Bronte & C. C. Krueger

Received: 3 July 2013 /Accepted: 18 February 2014 # Springer Science+Business Media Dordrecht 2014

Abstract Spawning behavior of lake trout, Salvelinus expand the current conceptual model. Lake trout namaycush, is poorly understood, relative to stream- spawning consisted of at least four distinct behaviors: dwelling salmonines. Underwater video records of hovering, traveling, sinking, and gamete release. spawning in a recovering population from the Hovering is a new courtship behavior that has not been Drummond Island Refuge (Lake Huron) represent the previously described. The apparent concentration of first reported direct observations of lake trout spawning hovering near the margin of the spawning grounds in the Laurentian Great Lakes. These observations pro- suggests that courtship and mate selection might be vide new insight into lake trout spawning behavior and isolated from the spawning act (i.e., traveling, sinking, and gamete release). Moreover, we interpret jockeying for position displayed by males during traveling as a T. R. Binder (*) unique form of male-male competition that likely Great Lakes Fishery Commission and Michigan State evolved in concert with the switch from redd-building University, Hammond Bay Biological Station, 11188 Ray Rd., Millersburg, MI 49759, USA to itinerant spawning in lake trout. Unlike previous e-mail: [email protected] models, which suggested that intra-sexual competition and mate selection do not occur in lake trout, our model H. T. Thompson includes both and is therefore consistent with evolution- United States Geological Survey, Hammond Bay Biological Station, 11188 Ray Rd., ary theory, given that the sex ratio on spawning grounds Millersburg, MI 49759, USA is skewed heavily towards males. The model presented : in this paper is intended as a working hypothesis, and A. M. Muir C. C. Krueger further revision may become necessary as we gain a Great Lakes Fishery Commission, 2100 Commonwealth Blvd. Suite 100, Ann Arbor, MI 48105, more complete understanding of lake trout spawning USA behavior.

S. C. Riley . . Great Lakes Science Center, United States Geological Survey, Keywords Reproductive ecology Itinerant spawning 1451 Green Rd., Ann Arbor, MI 48105, USA Courtship . Male-male competition

J. E. Marsden The Rubenstein School of Environment and Resources, University of Vermont, Introduction 308D Aiken Center, Burlington, VT 05405, USA Lake trout, Salvelinus namaycush, were the apex pred- C. R. Bronte United States Fish and Wildlife Service, ator in the Laurentian Great Lakes, and supported a 2661 Scott Tower Drive, New Franklin, WI 54229, USA valuable commercial fishery until the 1950s. However, Environ Biol Fish after invasion of the upper Great Lakes by predatory sea rocky substrates with clean interstitial spaces where lamprey, Petromyzon marinus, lake trout populations, embryos incubate over winter (Gunn 1995; Marsden already in decline due to expanding commercial harvest et al. 1995). Males mature at younger ages, arrive on (Hile 1949;Hileetal.1951), were lost from all but a few spawning grounds earlier and stay longer, and are gen- regions of lakes Superior (Hansen et al. 1995)and erally present in higher numbers than females (Royce Huron (Eshenroder et al. 1995). Despite intensive sea 1951;Eschmeyer1955; Martin 1957;McCrimmon lamprey control (Smith and Tibbles 1980) and more 1958;DeRoche1969; Peck 1986;Bronteetal.2007; than 50 years of stocking juvenile lake trout, self- Muir et al. 2012b). Females arrive on spawning grounds sustaining populations have only recovered where rem- after males and appear to remain for a shorter duration nant stocks remained after the crash, in Lake Superior than males. However, contrary to reproductive theory, (Hansen 1999;Bronteetal.2003) and in Parry Sound, which predicts that males should compete for females Lake Huron (Reid et al. 2001). In lakes Michigan, Erie when the sex ratio on spawning grounds is skewed and Ontario, rehabilitation has been slow and popula- towards males (Clutton-Brock and Parker 1992; tions continue to rely on stocking (Muir et al. 2012a). Kvarnemo and Ahnesjö 1996), observations of agonis- However, catches of wild lake trout juveniles and adults tic interactions among males are rare (Royce 1951; in annual assessments over the last decade suggest that Esteve et al. 2008;Muiretal.2012b). reproduction is widespread in Lake Huron (Riley et al. Three distinct spawning behaviors have been previ- 2007;Heetal.2012) and increasing in Lake Michigan ously identified from observations of lake trout (Hanson et al. 2013). For example, in the Drummond spawning at a shallow-water (<1 m) site in Kushog Island area of northern Lake Huron, wild fish now Lake, in southern Ontario (Esteve et al. 2008): 1) trav- comprise about 50 % of the adult spawning population eling, 2) sinking, and 3) gamete release. Within the (He et al. 2012), but population density is still below context of mating ritual, these behaviors are expressed historic levels. The recent reproductive success of lake as follows. Courtship begins with traveling, wherein a trout in Lake Huron presents a useful opportunity to female swims rapidly over spawning grounds with one understand the reproductive ecology of lake trout from or more attending males alongside or behind. Males a recovering population in the Great Lakes. quiver next to her and brush and nibble at her vent Compared to stream-spawning salmonines, relatively region. After making several large loops, the female little is known about spawning behavior of lake trout. and attending male(s) stop swimming and sink slowly Direct observations of spawning behavior are rare be- to the substrate. Once on the substrate, the group quivers cause lake trout spawn mainly at night, in deeper water vigorously with jaws agape and release gametes into the than stream-spawning salmonines, and during a logisti- substrate. Following gamete release, which lasts only a cally challenging season for field observations when second or two, the group returns immediately to travel- autumn weather changes to winter. Most information ing and the cycle is repeated (Esteve et al. 2008). Muir comes primarily from studies in small inland lakes et al. (2012b) expanded that conceptual model, based on (Martin 1957;McCrimmon1958;Gunn1995; Esteve observations at Great Bear Lake, Northwest Territories, et al. 2008). Most studies in the Great Lakes described to include splashing and porpoising display courtship, variables that affected timing and location of spawning and a novel display behavior that they termed ‘finning’. activity, and density, origin, and composition of recov- Finning involved two or more lake trout hovering or ering spawning populations, rather than spawning be- moving very slowly just beneath the surface of the havior (e.g., Eschmeyer 1955; Peck 1986; Marsden and water. The name ‘finning’ refers to the fully erect dorsal Krueger 1991; Selgeby et al. 1995;Bronteetal.2002; and adipose fins that conspicuously broke the water Claramunt and Jonas 2005). In the Great Lakes, lake surface. While jumping has been observed in studies trout spawn on shoals, although some historical popu- on other lakes (Merriman 1935; Royce 1951;Marsden lations were adfluvial (Loftus 1958). Spawning occurs and Krueger 1991), finning has not been observed out- mainly in October and November for the lean side of Great Bear Lake. This may indicate greater morphotype, but timing varies with latitude and weather dependence on visual courtship displays in Great Bear (DeRoche 1969; Peck 1986; Scott and Crossman 1998). Lake, a hypothesis supported by a greater degree of Unlike other salmonines, lake trout do not construct sexual dimorphism among lake trout populations in nests (i.e., redds). Lake trout deposit their eggs over Great Bear Lake, relative to more southern lakes (Muir Environ Biol Fish et al. 2012b). Alternatively, an absence of observations of high-quality spawning habitat (i.e., several layers of of finning elsewhere may be an artifact of most cobble substrate with clean interstitial spaces for over- spawning behavior studies being limited to spawning winter egg incubation) on the north-most tip of the east sites shallower than 1 m in depth (Merriman 1935; arm of Horseshoe Reef, a submerged drumlin on the Royce 1951; DeRoche 1969; Esteve et al. 2008). south side of Drummond Island (Fig. 1). The spawning In this paper, we describe the first reported observa- site is located on top of the reef in 3 to 4 m of water, tions of spawning behavior in a recovering population adjacent to a steep slope (~ 50°) where water depth of lake trout (lean morphotype) from the Laurentian increases from 4 to 10 m. An ongoing fine-scale acous- Great Lakes. Our objectives were first, to describe tic telemetry study on adult lake trout has identified this spawning behaviors of lake trout at Drummond Island, site as the most highly-used spawning site within the Lake Huron, in comparison to those observed else- 27 km2 study area, and recovery of fertilized eggs and where. Second, based on our observations in Lake emergent fry at this site in 2011, 2012, and 2013 indi- Huron, we revise the current conceptual framework for cated successful spawning (Binder unpubl. data). lake trout spawning behavior. The revised conceptual framework advances a foundation for development of hypotheses centered on understanding the evolution of Video observations the lake trout spawning strategy, which is unique among salmonines. Behaviors reported herein occurred at the peak of the spawning period, on 22 and 24 October 2012. Diver surveys 6 days earlier on 16 October found few lake Materials and methods trout at the site, although eggs were found in the substrate, which indicated that some spawning had already Study site occurred. Similarly, the number of lake trout on the reef on 27 October was low relative to 24 October. In addi- Lake trout spawning was observed in the Drummond tion, numerous round whitefish (Prosopium Island Refuge, along the south shore of Drummond cylindraceum) were present, presumably foraging on Island, in northern Lake Huron (latitude: 45.32°, longi- lake trout eggs. The length of the spawning period at tude: −83.65°; Fig. 1). The refuge was established in Drummond Island is not known, but some trout were 1985 as part of restoration efforts to prohibit commercial observed to remain on the reef well into November. and recreational fishing for lake trout (Ebener 1998). Watertemperatureonthereefduring22to24October The specific site of these observations was a 40 m2 area ranged from 10.5 to 11.2 °C.

Fig. 1 Map of Lake Huron with boundaries of the Drummond Island Refuge delineated in black. Inset: Bathymetric map of the south shore of Drummond Island, near Scammond Cove. The star indicates the location of Horseshoe Reef (Latitude: 45.931°, Longitude: −83.660°) Environ Biol Fish

Videos of lake trout behavior on the spawning site jumping behavior was seen frequently during the were recorded on two afternoons and one night on 22 spawning period from a boat at the surface. In all three October 2012 and 24 October 2012. Most footage of recorded instances, the lake trout jumped on its own, but spawning behavior was recorded on the afternoon of 22 the sex of these individuals could not be reliably deter- October by divers using a handheld camera (Panasonic mined because dark banding on males was less visible Lumix, model: DMC-FS3) in a watertight case. during day than night. The range of cameras and our Remaining video was recorded using two GoPro (Hero ability to discern behavior during night was limited by 2 outdoor edition) cameras mounted on concrete an- low light, but more lake trout were present on top of the chors. At night, underwater flashlights were added to reef in shallow water at night than day. This observation the concrete mounts, but the viewable range of the is supported by diver observations at the site in 2011 that cameras was less than 2 m, so most fine-scale behavior also indicated a far greater number of lake trout were was observed during the day. present on top of the reef at night, relative to day We recorded and analyzed 4 h 41 min of video; 2 h (T. Binder, pers. obs.). 36 min of afternoon video and 2 h 5 min of nighttime Spawning appeared to begin with a courtship behav- video. Because lake trout behavior extended beyond the ior not previously described in lake trout, which we term viewable range of our cameras and individual lake trout ‘hovering’ (Fig. 2a). In hovering, a female hung nearly were not identifiable, our ability to quantify behavior motionless in the water column near the edge of the reef, was limited to descriptions of the number of times each usually at least 1 m above the substrate. She was flanked behavior was observed. Videos were initially reviewed by usually two males (but on one occasion one and on separately by the first and second authors, who catego- another occasion three), which took up position on rized behaviors based on a three-stage (traveling, sink- either side of her, parallel to one another but below ing, gamete release) conceptual model of spawning and at between 40 and 60° to the long axis of the female. behavior, while noting new behaviors. The video was We observed this behavior 13 times, and angles of males then cropped to exclude periods of inactivity and re- relative to the female were consistent. While in this analyzed by the other authors. position, males moved along the sides and bottom of the female, rubbing, quivering, and occasionally nipping her. In all cases, fish that were observed hovering Results drifted into view, passively moved by wave surge from outside camera view to inside the range of the camera. During 22 to 24 October, divers estimated that at least Therefore, the duration of this courtship behavior is 100 lake trout were present at the Drummond Island site. unknown, but based on our observations, persisted for During the day, lake trout tended to aggregate at the at least several minutes. edge of the reef, swimming mid-column, in about 10 m At some point after hovering, the female began trav- of water. The aggregation appeared to be comprised eling over the substrate with one or more males, either at mostly of male lake trout, based on our acoustic telem- her side or slightly behind (Fig. 2b). In all cases but one, etry data and observations of dark banding along the at least two males were present during traveling. We lateral line that develops in males during the spawning assume that the closest males were the same as those period (Merriman 1935; Martin 1957; Foster 1985). present during hovering, but cannot confirm this be- However, only one to three males attended a female in cause we did not directly observe a transition from a spawning group. Other lake trout swimming within hovering to traveling. The largest traveling group ob- only a few meters seemed to ignore these spawning served contained six males and one female, but males groups. However, on four occasions, a stray male darted beyond the third-closest position to the female remained towards a group during sinking or gamete release, pre- with the group for less than 1 min. While traveling sumably to join in. None of these attempts appeared across the substrate, the female made several course successful because gamete release was usually complete changes, often leading the group in large circles. Fish by the time the stray fish got into position, or the group were in physical contact during traveling, particularly resumed traveling without releasing gametes. Three ob- the female and the two males occupying the positions servations of a lake trout burst swimming towards the directly flanking her. We observed only two cases of surface to jump out of the water were recorded. This overt aggression among males. In both cases, the female Environ Biol Fish

Fig. 2 Screen captures from video of lake trout spawning behav- jockey to occupy positions next to the female. c Bubbles being ior on Horseshoe Reef, in the Drummond Island Refuge, Lake released from the gills of a male lake trout. This behavior may be Huron. a A novel courtship behavior termed ‘hovering’. The related to fine-scale buoyancy control. d A group of lake trout female hangs nearly motionless while two males take position releasing gametes into the substrate. The female is on the outside next to her, parallel to one another, but below and at between 40 of the group, closest to the camera, but is most often in the middle. and 60° to the long axis of the female. Males move along the sides During gamete release, the trout splay their pectoral and pelvic fins and bottom of the female, rubbing, quivering, and nipping at her. b and the dorsal fin is erected. The trout thrust forward as they A female traveling across the substrate with three males. Males release their gametes onto the substrate stopped traveling and one or two males chased another group swam underneath the female while sinking, male for several seconds before all males returned to the which caused her to cease sinking and continue travel- female and traveling continued. In one case, one of the ing. Nine of 16 sinking events resulted in gamete release males nipped the female on the way back to her. The (confirmed visually by the release of a cloud of milt more typical behavior of males during traveling was to from the spawning group; Fig. 2d); three involving one jockey with one another for position adjacent to the male, four involving two males, and two involving three female. When only two males were present, both males males. Each event lasted only about 2 s. During gamete sometimes tried to work their way between the other release, the lake trout continued to quiver with erect male and the female, leaving one side of the female dorsal fins. The fish then arched themselves slightly unoccupied. Males often quivered next to and touched upwards with gonadal pores aligned and released gam- the female while traveling. We also noted five instances etes into the substrate while thrusting forward. (from at least two individuals) of air bubbles being Sometimes, the lake trout (males and females) gaped released from the buccal cavity (Fig. 2c). Males ap- their jaws. After gamete release, the group reformed and peared to release bubbles, but the proximity of fish to traveling continued. We observed a single female sink to one another sometimes prevented definitive assessment. the substrate to release gametes at least five times. During egg deposition, the female stopped swimming and the group sank slowly to the substrate. As the fish sank, they arched their tails slightly downward Discussion and splayed their pelvic and pectoral fins, presumably to stop their forward momentum. Slightly above or touch- The first reported observations of lake trout spawning in ing the substrate, males began quivering next to the the Laurentian Great Lakes were consistent with those female, who responded by also quivering, or by resum- from smaller inland lakes (Royce 1951;Martin1957; ing traveling. On one occasion, a male in the sinking Esteve et al. 2008), and Great Bear Lake (Muir et al. Environ Biol Fish

2012b). However, we observed and described a new females maintained close contact during all stages of courtship behavior called ‘hovering’. Based on our ob- spawning suggests that lake trout in the Great Lakes servations, we propose that lean morphotype lake trout probably depend heavily on tactile cues, or possibly spawning in the Great Lakes is comprised of at least four signals detected by the lateral line (Partridge and distinct behaviors (Fig. 3): 1) hovering, 2) traveling, 3) Pitcher 1980), to coordinate spawning activities. sinking, and 4) gamete release. This model builds upon Curiously, we never observed more than three males that proposed by Esteve et al. (2008), but does not participating in a hovering group. The apparent lack of include ‘finning’, a courtship behavior observed in overt male-male competition differentiates lake trout Great Bear Lake (Muir et al. 2012b). Finning was not from other salmonines (Gunn 1995;Muiretal. observed at our site, possibly because it occurred outside 2012b), and is a mystery because the skewed sex ratio the visual range of our cameras. However, similarities on spawning grounds should stimulate competition between finning and hovering suggest that they may be among males (Clutton-Brock and Parker 1992; analogous behaviors that serve a similar function. Kvarnemo and Ahnesjö 1996). However, based on the Hovering may be initiated soon after a female ap- recent description of two new courtship behaviors (fin- proaches a spawning ground, and appears to be focused ning and hovering) near the margin of spawning along the edge of the reef, in the transition zone between grounds, we hypothesize that mate selection and male- deep and shallow water. The nature of the behavior male competition is more intense than previously suggests that it serves as a way for females to select thought and may be isolated temporally or spatially attending males, but rather than being a visual display, from the actual spawning act, which could explain as suggested for finning by Muir et al. (2012b), it why it has not been observed. Two mechanisms are seemed to be primarily a tactile process. The reason possible. First, a hierarchy may develop among males for this difference is not known, but could be a result on the reefs before females arrive, with dominant males of the longer day length that occurs during spawning in getting preferential access to females for spawning. Great Bear Lake, relative to Lake Huron (Muir et al. Under this scenario, hovering would allow dominant 2012b). Nonetheless, our observation that males and males to present themselves to a female when she

Fig. 3 Aworking model of lake trout spawning behavior based on for a position next to her. When the female chooses a site, she underwater video observation in the Drummond Island Refuge, ceases swimming and the group sinks (3) onto the substrate. On Lake Huron. Spawning begins with a courtship behavior termed the substrate, the trout quiver and release their gametes (4). The ‘hovering’ (1), which occurs mainly near the fringe of a spawning female then resumes traveling and the cycle (2, 3, 4) repeats. Note: ground. After the female selects her mates, she begins traveling (2) In the schematic, the female is depicted at the center of the over a spawning ground in search of appropriate substrate on spawning group which to deposit her eggs, while males follow behind competing Environ Biol Fish arrives at the spawning grounds. Alternatively, mate functions were not obvious. Bubbles released from the selection may occur at the edge of the spawning grounds buccal cavity of lake trout may be a form of communi- and a female could evaluate several suitors before cation among individuals, or may simply be a conse- selecting mates and initiating traveling (similar to quence of physical forces during spawning. lekking in other species). The latter seems more likely Alternatively, bubble release could be related to a need for two reasons. First, lake trout tend to aggregate in for individuals to maintain precise and rapid buoyancy deeper water along reef margins (Merriman 1935; control. This could be important during hovering, and Royce 1951; Marsden and Krueger 1991), rather than during sinking, when lake trout must maintain negative directly on spawning grounds. Second, maintaining buoyancy to sink to the substrate. Similarly, jumping dominance within a hierarchy is energetically expensive could be related to buoyancy, with individuals breaching (Fleming 1996) and usually focuses on acquisition of the surface to fill their swim bladders. It is also possible defendable territories, which is not evident for lake trout that females jump to assist breaking their ovarian mem- (Muir et al. 2012b). brane to release eggs into their body cavity, or jumping Males often quivered alongside a female while trav- could be displacement activity, unrelated to specific eling, but generally seemed more focused on competing objectives (Hinde 1966). The current hypothesis that for space next to the female, sometimes attempting to jumping and splashing at the surface is a form of display displace another male rather than take up an empty courtship (Muir et al. 2012b) was not supported by our position by her side. Esteve et al. (2008)calledtravel- observations because individuals exhibiting this behav- ling courtship, but did not observe females rejecting ior were solitary and did not appear to elicit a response males, which they interpreted as evidence that inter- from other lake trout. Nonetheless, more underwater sexual selection was relaxed in lake trout. Instead, we observations of these behaviors are needed to fully propose that traveling is initiated only after a female has understand their role, if any, in spawning behavior of selected mates, and that male behavior during traveling lake trout. is a form of male-male competition (i.e., the most fit Our results expand understanding of lake trout males are those able to remain immediately adjacent to spawning behavior and provide new insight into a the female for multiple bouts of gamete release). If our spawning strategy that is unique among salmonines. interpretation is correct, then male-male competition in Our revised spawning model includes both mate selec- lake trout is different than in stream-dwelling tion and a unique form of male-male competition that is salmonines, where males in streams viciously chase consistent with evolutionary theory. Behavior during the and nip at each other (Berst et al. 1981; Foote 1990; spawning act seems to be highly conserved among lake Fleming 1996; Esteve 2005). Reproductive success of trout populations (Merriman 1935; Royce 1951; Esteve an individual male will depend in part on his proximity et al. 2008), but differences between the hovering be- to a female at the time of gamete release because fertil- havior in Lake Huron and finning behavior in Great ization success in a multi-male pairing is inversely re- Bear Lake (Muir et al. 2012b) suggest that courtship lated to the time it takes for a sperm to reach an egg behaviors may vary among populations. Further revi- (Mjølnerød et al. 1998). In redd-building salmonines, sions to our conceptual model may be necessary as we like Pacific salmon, males evolved aggressive behaviors develop a more complete understanding of lake trout to isolate a female and redd from competing males spawning behavior. For example, spawning is thought (Berst et al. 1981; Foote 1990; Fleming 1996; Esteve to occur primarily at night; yet we have little information 2005). In contrast, the itinerant spawning strategy of on nighttime behavior. Further, the extent to which lake trout (Esteve et al. 2008) seems to favor males that observed daytime behaviors are representative of night- compete for close proximity to a female while traveling time spawning behavior is unknown. Therefore, the over those that display aggressive behaviors that would model presented in this paper should be viewed as an likely draw them away from a female. This difference evolving hypothesis. Future studies should focus on could also be due to that fact that Pacific salmon are determining the relationship between daytime and semelparous, while lake trout are long-lived and nighttime spawning activity, and on understanding lake iteroparous. trout behavior beyond the spatial and temporal confines We observed two behaviors, bubble release and of the main spawning act. 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