Importance and Predictability of Cannibalism in ... - Wiley Online Library

Transactions of the American Fisheries Society 136:227–237, 2007 Ó Copyright by the American Fisheries Society 2007 DOI: 10.1577/T05-280.1

[Article]

Importance and Predictability of Cannibalism in Rainbow Smelt SANDRA L. PARKER STETTER*1 Cornell University Biological Field Station, Department of Natural Resources, Cornell University, 900 Shackelton Point Road, Bridgeport, New York 13030, USA

JENNIFER L. STRITZEL THOMSON2 Vermont Cooperative Fish and Wildlife Research Unit, Rubenstein School of Environment and Natural Resources, University of Vermont, Burlington, Vermont 05405, USA

LARS G. RUDSTAM Cornell University Biological Field Station, Department of Natural Resources, Cornell University, 900 Shackelton Point Road, Bridgeport, New York 13030, USA

DONNA L. PARRISH U.S. Geological Survey, Vermont Cooperative Fish and Wildlife Research Unit, Rubenstein School of Environment and Natural Resources, University of Vermont, Burlington, Vermont 05405, USA

PATRICK J. SULLIVAN Department of Natural Resources, Cornell University, Ithaca, New York 14850, USA Abstract.—Cannibalism is a key interaction between young of year (age-0) and older fish in many freshwater ecosystems. Density and spatial overlap between age-groups often drive cannibalism. Because both density and overlap can be quantified, the magnitude of cannibalism may be predictable. Our study considered cannibalism in rainbow smelt Osmerus mordax in Lake Champlain (New York–Vermont, United States, and Quebec, Canada). We used acoustic estimates of the density and distribution of age-0 and yearling-and-older (age-1þ) rainbow smelt to predict cannibalism in the diets of age-1þ fish during 2001 and 2002. Experienced density, a measure combining density and spatial overlap, was the strongest predictor (R2 ¼ 0.89) of the proportion of cannibals in the age-1þ population. Neither spatial niche overlap (R2 ¼ 0.04) nor age-0 density (R2 ¼ 0.30) alone was a good predictor of cannibalism. Cannibalism among age-1þ rainbow smelt was highest in June, lowest in July, and high in September owing to differences in thermal stratification and habitat shifts by age-0 fish. Between July and September, age-1þ rainbow smelt consumed 0.1–11% of the age-0 population each day. This resulted in a 38–93% mortality of age-0 fish due to cannibalism. These estimated mortality rates did not differ significantly from observed declines in age-0 rainbow smelt abundances between sampling dates. Age-1þ rainbow smelt are probably the primary predators on age-0 rainbow smelt during the summer and early fall in Lake Champlain.

Cannibalism results in significant mortality of youngof-year (age-0) fish in many species (Chevalier 1973; Smith and Raey 1991; Persson et al. 2003). In rainbow smelt Osmerus mordax, cannibalism by yearling-andolder (age-1þ) fish on age-0 fish causes cyclical patterns in population abundance (Henderson and Nepszy 1989; He and LaBar 1994; Lantry and Stewart 2000), and * Corresponding author: [email protected] 1 Present address: School of Aquatic and Fishery Sciences, University of Washington, Box 355020, Seattle, Washington 98195-5020, USA. 2 Present address: Annisquam River Marine Fisheries Station, Massachusetts Division of Marine Fisheries, 30 Emerson Avenue, Gloucester, Massachusetts 01930, USA. Received November 9, 2005; accepted July 28, 2006 Published online February 1, 2007

modeling indicates that cycle length depends on the age and abundance of the primary cannibalistic age-group (He and LaBar 1994; Lantry and Stewart 2000). Such patterns have been observed in Lake Erie since the 1960s (Henderson and Nepszy 1989; Lantry and Stewart 2000). Self-regulation makes rainbow smelt ‘‘one of its own worst enemies’’ (Kendall 1926) and complicates the management of piscivores in systems dependent on rainbow smelt production. Managing predator demand and cannibalistic prey supply requires an understanding of the level of cannibalism relative to other sources of mortality. Management models would improve if we could predict the degree of cannibalism within and between years. Although cannibalism is often density dependent (Frankiewicz et al. 1999; Kellison et al. 2002), spatial overlap between predator and prey is also an important

227

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PARKER STETTER ET AL.

predictor of interaction (Lloyd 1967; Williamson and Stoeckel 1990). This is true for rainbow smelt because of strong ontogenetic shifts in thermal preferences and diel vertical migration. Age-1þ rainbow smelt prefer cool water, remaining in the hypolimnion during the day but moving into the metalimnion and lower epilimnion to forage at night (Ferguson 1965; Evans and Loftus 1987). In the absence of stratification, they move throughout the water column during foraging (Nellbring 1989). Conversely, age-0 rainbow smelt are initially found in warm epilimnetic waters and do not vertically migrate. In late summer, they begin to shift down into the metalimnion and overlap with age-1þ rainbow smelt (Ferguson 1965; Tin and Jude 1983; Burczynski et al. 1987; Urban and Brandt 1993). Although age-1þ fish can forage in suboptimal temperatures (Kendall 1926; Ferguson 1965), the thermal structure and timing of habitat shifts by age-0 fish will influence cannibalistic access to these fish. Thus, both the density of age-0 fish and the degree of overlap between them and age-1þ fish should influence the rates of cannibalism. Our study goals were to determine whether seasonal cannibalism among rainbow smelt could be predicted using acoustics and any of three predictors (spatial niche overlap, age-0 density, or experienced density) and to apply this knowledge to estimates of age-0 mortality attributable to predation by age-1þ rainbow smelt in Lake Champlain (United States, Canada). The experienced density predictor (Lloyd 1967; defined in the Methods section) combines density and spatial overlap in a single metric. Our approach was to quantify cannibalism in diet analyses and to estimate predictors using acoustic data under three thermal periods: weak (June), strong (July), and weakening (September). Acoustics can provide separate estimates of age-0 and age-1þ rainbow smelt densities even when the age-groups overlap (Parker Stetter et al., 2006). Our study had four main objectives: to test the abilities of age-0 density, spatial niche overlap, and experienced density to predict observed proportions of cannibalistic age-1þ fish during different thermal periods; to estimate nightly age-0 mortality using the predicted proportion of cannibals, known consumption, and measured densities of age-1þ and age-0 fish; to predict the total mortality of age-0 fish due to cannibalism between June–July and September; and to compare predictions of age-0 total mortality with observed changes in acoustic density estimates. Methods Study area.—Lake Champlain (United States, Canada) is oriented north–south along the borders of New

York, Vermont, and Quebec. The lake has a total surface area of 1,140 km2 (Potash et al. 1969). Natural and artificial barriers divide Lake Champlain into three areas that differ in depth and strength of thermal structure: Main Lake, Inland Sea, and Malletts Bay. The Main Lake is located west of Burlington, Vermont; Malletts Bay is north of Burlington and east of the Main Lake; and the Inland Sea is north of Malletts Bay. The differences among these areas allowed us to examine cannibalism under different conditions. Within the three areas we studied, the Main lake is deepest (maximum, 120 m; mean, 30 m), the Inland sea is moderate (maximum, 50 m; mean, 13 m), and Malletts Bay is shallowest (maximum depth, 30 m; mean depth, 13 m) (Potash et al. 1969). Survey timing.—Surveys of age-0 and age-1þ rainbow smelt were conducted in 2001 and 2002. Sampling occurred on June 17–21, July 22–26, and September 16–20, 2001, and on July 21–25 and September 15–19, 2002. Data for June 2002 were not available owing to problems with acoustic equipment. The time periods were selected to represent weak thermal structure (June), strong thermal structure (July), and weakening thermal structure during the overlap between age-0 and age-1þ fish (September). All work was performed on the University of Vermont RV Melosira (length, 13.7 m; engine, 275 horsepower [1 horsepower ¼ 746 W]; cruising speed, 5.7 m/s). Coupled acoustics and trawling segments were surveyed at night, commencing at least 1 h after sunset and ending at least 1 h before sunrise. Peak rainbow smelt feeding occurs after sunset (Parker et al. 2001). The underlying cruise track was a zigzag survey with a random start. Fish collection and diet analyses.—Rainbow smelt were collected for diet analyses using two trawl types. A midwater trawl with a 6-mm-square mesh cod end and 6-m 3 6-m average fishing dimensions was the primary gear for collecting age-1þ rainbow smelt. A 2m 3 2-m Tucker trawl with a 1-mm cod end was also used for specimen collection. A netsonde was affixed to the headrope of both nets to monitor trawl depth. Both nets were deployed and retrieved with hydraulic winches. All age-1þ rainbow smelt collected for diet analyses were flash frozen on dry ice. Thermocline depth was assessed nightly with a temperature–depth recorder. Rainbow smelt stomach contents were identified and counted in the laboratory with a dissecting microscope. Age-0 rainbow smelt in the stomachs of age-1þ fish were identified by the presence of pharyngeal teeth, vertebrae counts, or other morphological features. Because 99% of identifiable young of year in the diets of age-1þ fish in this analysis were rainbow smelt, we

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PREDICTING CANNIBALISM IN RAINBOW SMELT

considered partially digested fish to be rainbow smelt unless they were positively identified otherwise. The proportion of age-1þ cannibals and the average number of age-0 fish consumed per cannibal were calculated for each trawl. Acoustic analyses.—A Simrad EY500 split-beam echo sounder (70 kHz, 11.18 half-power beam width, 0.2-ms pulse length, two pings/s) was used to collect acoustic data. The transducer was mounted on a towed body and deployed from the starboard stern of the boat. The unit was calibrated using a standard copper sphere within a few weeks of each survey. All acoustic data were processed and exported using EchoView 3.25 (SonarData 2004). We made corrections to the algorithm-detected bottom and manually removed electrical or physical noise. No data were used from within 0.5 m of the bottom or from within 3.0–5.0 m of the surface. To maximize the coherence between acoustic data and diet analyses, we analyzed acoustic data only on transect segments that were sampled by trawl for age1þ rainbow smelt diet analyses. Trawls with five or more age-1þ diet samples and trawl depths less than 22 m were selected for analyses. We chose 22 m because it was the maximum depth encountered during trawling in Malletts Bay; it encompassed the range of vertical overlap between age-0 and age-1þ fish; most trawling occurred between 4 and 22 m; rainbow smelt biomass was concentrated above 22 m during the night; and the 22-m depth removed the potential bias in age-0 density estimates from mysids and low signal-to-noise ratio in deeper water (Parker Stetter et al. 2006). Acoustic single-target and echo integration data were exported in 5-min bins, commencing at the beginning of each trawl and ending at haul-back. We used 1-m vertical bins through the zone of overlap and 2-m vertical bins below the overlap zone, to a maximum depth of 22 m. We applied a 76-dB threshold to single-target detections and a 80-dB threshold to volume backscattering (Sv) data. Single-target data were exported in 1-dB bins. The densities of age-0 and age-1þ rainbow smelt were calculated for each 1- or 2-m analytic bin. First, we calculated Sawada’s Nv index (Sawada et al. 1993) for each cell and included only the cells with an Nv less than or equal to 0.10. In situ target strength in cells with higher Nv values may be biased (Rudstam et al. 2003). Echo integration (volume backscattering coefficient, sv [m2/m3]) was then converted to total density (/m3) for each analytic bin using a mean acoustic backscattering cross-section (rbs) from in situ targets between 76 and 20 dB. Next, the proportions of age-0 and age-1þ fish were generated using in situ target strength (TS) ranges

for June, July, and September: 60 to 35 dB (age 1þ, all months), 76 to 61 dB (age 0, June), 75 and 50 dB (age 0, July), and 68 to 45 dB (age 0, September) (Parker Stetter et al. 2006). The average TS of age-0 rainbow smelt increases from 68 to 59 dB from June to September, whereas the TS of age-1þ rainbow smelt remains around 48 dB throughout this time period (Rudstam et al. 2003). When the TS of age-0 and age1þ fish overlapped in July and September, the ratios of large to small age-1þ targets were used to attribute overlapped in situ TS values to both age-groups (Parker Stetter et al., in press). Finally, the proportions of in situ targets attributed to age-0 and age-1þ fish were used to partition total density into age-0 and age-1þ components. We averaged the densities for each depth interval and summed them to calculate total age-0 and age-1þ density (fish/m2) between 4 and 22 m. Estimating proportion of cannibals.—We tested three approaches to predicting the proportion of age1þ cannibals in the midwater trawls. These approaches individually considered spatial niche overlap, age-0 density, and experienced density. Czekanowski’s index (Feinsinger et al. 1981) was used to quantify the spatial niche overlap in the vertical distributions of age-1þ and age-0 rainbow smelt at depths between 4 and 22 m. We treated location in the water column as the shared resource. This index is calculated as OAge-0;age-1þ ¼ OAge-1þ;age-0 m X ¼ 1 0:5 jPAge-1þj PAge-0j j ; j¼1

OAge-1þ,age-0 ¼ the overlap between age-1þ and age-0 fish; OAge-0,age-1þ ¼ the overlap of age-0 fish on age-1þ fish; PAge-1þj ¼ the proportion of age-1þ total density at depth j of m total depth layers; PAge-0j ¼ the proportion of age-0 total density at depth j. Czekanowski’s index calculates an estimate of spatial niche overlap using proportional age-1þ and age-0 distributions and does not account for density effects. The second predictor of the proportion of cannibals in the age-1þ population was average age-1þ density (DAge-1þ/m3). This estimate was calculated for the 4–22 m depth range as m X n X

DAge-0 ¼

DAge-0ij

j¼1 i¼1

nm

;

230


where DAge-0ij is the density of age-0 fish in analytic bin ij (/m2), j is the vertical depth segment, and i is the horizontal transect segment of n total horizontal transect segments. Experienced density, which is equivalent to Lloyd’s mean crowding (Lloyd 1967) and Williamson’s density risk (Williamson et al. 1989), was the third predictor of cannibalism by age-1þ rainbow smelt. This index is a measure of the average density of age-0 prey experienced by an average age-1þ predator, thereby taking into account both density and spatial overlap. It has been applied to predation on zooplankton (e.g., Williamson and Stoeckel 1990; Folt and Schulze 1993) and on larval fish (e.g., Frankiewicz et al. 1999; Garrison et al. 2000; Yamamura et al. 2001) from the perspective of estimating the risk to a prey species. It has not, however, been used in understanding cannibalism. As we apply density risk from the perspective of the cannibalistic predator, we call it ‘‘experienced density.’’ Similar concepts have been applied in spatially explicit bioenergetics models (e.g., Goyke and Brandt 1993; Luo and Brandt 1993; Stockwell and Johnson 1997). Experienced density (E [age-0 density m3 age-1þ individual1]) was calculated over a standard 4–22 m depth range as m X ðPAge-1þj DAge-0j Þ

E¼

j¼1

m

;

where m is the vertical height of the water column over which the density estimate was made. Least-squares regression models were used to determine the relationship between the proportion of age-1þ cannibals in diet analyses and spatial niche overlap, age-0 density, and experienced density. All analyses included an intercept term and were conducted in S-Plus 6.1 (Insightful Corporation 2002). Age-0 predicted and observed mortality.—The proportions of age-1þ cannibals on our transect segments were predicted from regression results for experienced density (see Results) to standardize to the same relationship. The daily mortality of age-0 fish (MAge-0 ) caused by cannibalistic age-1þ fish was then calculated for each transect segment as m X n X

MAge-0 ¼

DAge-1þij

j¼1 i¼1

nm

CAge-1þ x;

where CAge-1þ is the estimated proportion of age-1þ cannibals determined from experienced density calculations, and x¯ is the mean number of age-0 fish per cannibal stomach.

When cannibalism was predicted but not observed, the minimum value of 1 age-0 fish per cannibal was used in calculations. Daily age-0 mortality was then converted to proportion of the age-0 population consumed that night (PMAge-0 ) as MAge-0 PMAge-0 ¼ : DAge-0 Using our PMAge-0 daily mortality estimates, we calculated expected mortality between sampling dates in each area. When more than one estimate of mortality was available within an area, we used a mean PMAge-0 for that sampling date. We used linear interpolation between sampling dates to estimate PMAge-0 for each day. Daily survival was then calculated as 1 – PMAge-0. For each day during the sampling period, we multiplied the population remaining at the beginning of each day with the daily survival calculated for that day. Total predicted mortality was calculated between July and September for all areas in 2001 and 2002. A single calculation was made between June and September in Malletts Bay 2001, as June data were only available for that lake area. We estimated total observed age-0 rainbow smelt mortality between sampling dates using acoustic abundance estimates for each lake area (Parker Stetter 2005). Total observed mortality was calculated as the difference between age-0 density at the starting and ending sampling dates. We used a chi-square test to determine whether predicted age-0 mortality differed from observed mortality. Results Fish Collection and Diet Analyses Twenty-five trawls were included in this study. Trawl catches were dominated by age-0 rainbow smelt in 2001 and by age-1 fish in 2002 (Table 1). Other species were not important components of trawl catches, only two trawls having more than 6% other species (Table 1). As rainbow smelt typically constitute up to 99% of pelagic trawl samples in Lake Champlain (Kirn and LaBar 1991; Pientka and Parrish 2002), this was an expected result. Fifteen trawls contained cannibals, with the proportion of cannibalistic age-1þ fish ranging from 0.04 to 0.70 (Table 1). Age-0 rainbow smelt were positively identified in 88% of age1þ stomachs with fish remains. Cannibalism varied by area and month and broadly reflected differences in thermal profiles. June and September 2001 had weak thermoclines and the highest proportion of cannibalistic age-1þ fish in diet analyses (Figure 1; Table 1). In July 2001 and 2002, strong thermoclines increased the spatial separation of

231


TABLE 1.—Summary of trawls used for age-1þ rainbow smelt diet analyses. Maximum depth is the maximum site depth during the trawl, trawl depths are single or stepped trawling depths, trawl style is the gear used (MW ¼ midwater trawl, TT ¼ Trucker trawl), Prop. Age-1þ, age-0, and other are the proportions of those categories in trawl hauls, and Prop. cannibals is the proportion of cannibalistic age-1þ fish in diet analyses. Month and area

Maximum depth (m)

Trawl depths (m)

Trawl style

Prop. age-1þ

Prop. age-0

Prop. other

Prop. cannibals

28 19

20, 12, 9 16, 10, 1

MW MW

1.00 1.00

0.00 0.00

0.00 0.00

0.38 0.33

25 17 48 40

20, 15, 10 11, 8 30, 20, 10 19

MW MW MW MW

0.95 0.11 0.08 0.13

0.05 0.89 0.91 0.86

0.00 0.00 0.01 0.01

0.04 0.00 0.21 0.24

44 68 40 48 28 26 26

31, 32, 20, 15 12 16 15,

10

MW MW MW MW MW MW MW

0.04 0.17 0.43 0.01 0.48 0.06 0.67

0.95 0.82 0.14 0.96 0.52 0.94 0.33

0.01 0.01 0.43 0.03 0.00 0.00 0.00

0.08 0.70 0.22 0.17 0.00 0.16 0.21

27 27 25 41 33 28 66 46

15, 10 6, 2 20, 15 20 5 25, 15 40, 25, 15 10

TT TT MW MW MW MW MW MW

1.00 1.00 1.00 1.00 0.90 1.00 0.54 0.02

0.00 0.00 0.00 0.00 0.04 0.00 0.00 0.98

0.00 0.00 0.00 0.00 0.06 0.00 0.46 0.00

0.08 0.00 0.04 0.00 0.00 0.00 0.00 0.00

28 27 18 32

15 15 15 25, 20

TT MW MW MW

0.99 0.96 0.39 0.10

0.01 0.04 0.61 0.90

0.00 0.00 0.00 0.00

0.00 0.08 0.00 0.07

Jun 2001 Malletts Bay Malletts Bay Jul 2001 Malletts Bay Malletts Bay Inland Sea Main Lake Sep 2001 Main Lake Main Lake Inland Sea Inland Sea Malletts Bay Malletts Bay Malletts Bay Jul 2002 Malletts Bay Malletts Bay Malletts Bay Inland Sea Inland Sea Inland Sea Main Lake Main Lake Sep 2002 Malletts Bay Malletts Bay Malletts Bay Main Lake

25 25 15

age-0 and age-1þ in some areas. The highest proportion of cannibals in July was in the area with the weakest thermal structure (the Inland Sea in 2001), and the lowest proportions of cannibals were in the areas with the strongest thermal structures (Malletts Bay in 2001 and the Inland Sea in 2002) (Figure 1; Table 1).

2). In July, the age-1þ distribution began abruptly below the thermocline, so there was little overlap with age-0 fish, which remained in the epilimnion (Figure 2). Although a strong thermocline in September pushed the age-1þ distribution deeper, age-0 movement into metalimnetic waters increased the overlap between the age-groups (Figure 2).

Acoustic Analyses The densities of age-0 and age-1þ rainbow smelt varied between 2001 and 2002. High densities of age-0 fish were observed on our transect segments in 2001, ranging from 0.038 to 1.750 fish/m3 (Table 2). During the same year, the densities of age-1þ fish ranged from 0.002 to 0.062 fish/m3 (Table 2). In 2002, the opposite pattern prevailed; age-0 densities were between 0.007 and 0.123 fish/m3 and age-1þ densities between 0.003 and 0.095 fish/m3 (Table 2). The differences in density between 2001 and 2002 agree with the proportions of age-0 and age-1þ fish in the trawl catches (Table 1). The vertical distributions of age-0 and age-1þ rainbow smelt follow thermal profiles. During the weak thermal structure in June, age-1þ rainbow smelt were present throughout the water column and overlapped with age-0 fish in upper waters (Figure

Estimating the Proportion of Cannibals Our three predictors—spatial niche overlap, age-0 density, and experienced density—differed in their ability to predict the observed proportions of cannibalistic age-1þ fish. Spatial niche overlap was a poor predictor of the observed proportion of cannibals (N ¼ 25, R2 ¼ 0.04; Figure 3, upper panel) in the leastsquares linear regression calculations. Age-0 density explained only 30% of the variation in the proportion of age-1þ cannibals (N ¼ 25, R2 ¼ 0.30; Figure 3, middle panel). However, experienced density was strongly related to the proportion of cannibals obtained from diet analyses (N ¼ 25, R2 ¼ 0.89; Figure 3, lower panel). The highest value in this relationship (0.037, 0.70) had a Cook’s distance (Neter et al. 1996) of 1.2, indicating that this point had the potential to influence

232


FIGURE 1.—Temperature profiles for Malletts Bay (dashed black lines), the Main Lake (solid black lines), and the Inland Sea (gray lines) in June, July, and September of (a) 2001 and (b) 2002.

the linear regression as an outlier. Without this point, the regression was CAge-1þ ¼ 15.53E – 0.002 (R2 ¼ 0.79, N ¼ 24). An inspection of residuals, fits, and variance provided sufficient evidence that this point was valuable for our analyses. Age-0 Predicted and Observed Mortality The proportions of cannibals in the age-1þ population was predicted for each transect segment using experienced density. As expected by the high R2 value, the predicted proportions of cannibals (Table 2) are very similar to those observed in diet analyses (Table 1). The within-area variability in the predicted number of cannibals in any given month was generally between 0.01 and 0.08 (maximum less minimum; Table 2). We estimate that cannibalistic age-1þ fish consumed between 0.1% and 11.0% of the age-0 population on the nights we sampled (Table 2). In both 2001 and 2002 there were high estimates of percent age-0 fish consumed, the top four values occurring in September 2001 (5.2% and 7.3%) and 2002 (5.8% and 11.0%).

When mortality was interpolated as a daily time-step between sampling dates (Table 3), total predicted age-0 mortality was 63–81% between July and September (Figure 4). These values do not represent instantaneous mortality rates. Mortality in the area with June-toSeptember data (Malletts Bay 2001) was 86%. Total observed mortality, based on measured declines in age-0 acoustic abundance estimates between sampling dates, ranged from 60% to 90% (Figure 4). The differences between total observed and predicted mortality within areas were between 12% and þ22% (Figure 4). Predicted mortality did not differ significantly from observed mortality P(v2 . 0.19, df ¼ 5) . 0.90. Discussion Quantifying cannibalism is essential for understanding population dynamics, stock–recruitment curves, and other aspects of a species’ ecology. Our results suggest that cannibalism by age-1þ rainbow smelt is a major source of age-0 mortality throughout the

233


TABLE 2.—Age-0 mortality estimates for 2001 and 2002. Age-0 density and age-1þ density are the average densities between 4 and 22 m, proportion cannibals is the proportion of cannibals predicted by the least-squares regression equation CAge-1þ ¼ 17.48 E 0.01, average age-0 fish/cannibal is the mean number of age-0 fish per cannibal stomach from diet analyses, and % age-0 fish eaten/night is the percent of the age-0 population consumed by age-1þ fish on the trawled portion of the transect on the survey date. Month and area Jun 2001 Malletts Bay Malletts Bay Jul 2001 Malletts Bay Malletts Bay Inland Sea Main Lake Sep 2001 Main Lake Main Lake Inland Sea Inland Sea Malletts Bay Malletts Bay Malletts Bay Jul 2002 Malletts Bay Malletts Bay Malletts Bay Inland Sea Inland Sea Inland Sea Main Lake Main Lake Malletts Bay Malletts Bay Malletts Bay Main Lake a

Age-0 density

Age-1þ density

Proportion cannibals

Average age-0 fish/cannibala

% Age-0 fish eaten/night

0.311 0.174

0.009 0.018

0.313 0.349

2.8 1.3

2.7 4.5

0.104 0.304 0.182 1.750

0.019 0.014 0.005 0.003

0.118 0.041 0.191 0.135

1.0 1.0 2.0 2.2

2.2 0.2 1.0 0.1

0.119 0.967 0.063 0.038 0.077 0.111 0.389

0.002 0.062 0.008 0.005 0.005 0.010 0.017

0.041 0.636 0.205 0.127 0.006 0.234 0.360

1.0 1.8 2.0 1.0 1.0 1.3 2.6

0.1 7.3 5.2 1.7 0.1 2.8 4.0

0.042 0.045 0.123 0.067 0.122 0.091 0.007 0.076 0.027 0.046 0.032 0.010

0.052 0.095 0.073 0.020 0.042 0.039 0.003 0.015 0.038 0.080 0.050 0.014

0.021 0.022 0.024 0.009 0.005 0.001 0.007 0.053 0.040 0.062 0.010 0.073

1.0 1.0 1.0 1.0 1.0 1.0 1.0 1.0 1.0 1.0 1.0 1.7

2.8 5.0 1.5 0.3 0.2 0.1 0.4 1.1 5.8 11.0 1.7 1.0

This variable cannot be less than 1.0; if cannibalism was predicted but not observed, it was set equal to 1.0.

FIGURE 2.—Representative proportions of age-0 (YOY; gray lines) and age-1þ (YAO; solid black lines) densities in Malletts Bay (site depths, 17–22 m) during June, July, and September 2001, along with temperature profiles (dashed black lines).

234


FIGURE 3.—Least-squares regression relationships between the proportion of age-1þ cannibals in diet analyses and three measures of association in June (solid triangles), July (solid squares), and September 2001 (solid circles) and July (open squares) and September 2002 (open circles). The estimated equation in the upper panel is y ¼ 0.16x þ 0.07 (R2 ¼ 0.04, N ¼ 25), that in the middle panel is y ¼ 0.24x þ 0.07 (R2 ¼ 0.30, N ¼ 25), and that in the lower panel is y ¼ 17.48x – 0.01 (R2 ¼ 0.89, N ¼ 25); YAO ¼ age 1þ and YOY ¼ age 0 (see text for additional details).

summer. Further, we show that acoustics can predict the occurrence and magnitude of cannibalism in this forage species. Our study found that experienced density, a measure combining age-0 density with the spatial overlap between age-0 and age-1þ fish, can predict cannibalism in rainbow smelt. In using acoustic data for estimates of density and overlap, our analyses were at finer scales than is possible with conventional gear types. We tested the ability of three measures—spatial niche overlap, age-0 density, and experienced density—to predict the proportion of cannibals in the age-1þ rainbow smelt population. Spatial niche overlap considers only the spatial relationship between age-0

and age-1þ fish and does not consider predator and prey densities. As a result, spatial niche overlap was a poor predictor of cannibalism. Alternatively, considering only age-0 density disregards the differences in the spatial overlap between age-groups that occur because of water column stratification. Spatial overlap is an important consideration in a species such as rainbow smelt, in which age-groups are thermally separated (Nellbring 1989). Even so, age-0 density was a fair predictor of the proportion of cannibals in the age-1þ population. However, our experienced density index was the strongest predictor of cannibalism by age-1þ fish. This index takes into account both density and spatial influences. Combining density and spatial influences is critical in a system such as Lake Champlain in which there are both directional trends in age-0 and age-1þ densities (Parker Stetter 2005) and an internal seiche influencing thermocline depth (Hunkins et al. 1998). Age-1þ rainbow smelt consumed a high percentage of the age-0 population in 2001 and 2002, despite differences in the proportion of cannibals. This counterintuitive finding results from differences in density. A high proportion of cannibals in the lowdensity age-0 population caused high age-0 mortality in 2001. Conversely, higher 2002 age-1þ densities offset the lower proportions of cannibals and resulted in age-0 mortalities comparable to those of 2001. Our results suggest that cannibalistic age-1þ rainbow smelt are responsible for most of the observed July–September age-0 mortality. Predicted cannibalism accounted for an average of 89% of the observed decreases in acoustic age-0 density estimates. Our predicted mortality may be conservative, as it is based on peak age1þ feeding after sunset (Parker et al. 2001). We did not examine possible additional consumption of age-0 fish TABLE 3.—Values used to predict age-0 rainbow smelt mortality by cannibalistic age-1þ fish. The beginning and ending dates are the sampling dates (or mean sampling date if over multiple days) used in mortality calculations, and the proportions of age-0 fish cannibalized are the mean proportions of the age-0 population consumed by cannibals on those dates. Proportion age-0 fish cannibalized

Area

Year

Beginning date

Malletts Bay Malletts Bay Malletts Bay Main Lake Main Lake Inland Sea

2001 2001 2002 2001 2002 2001

18 Jun 23 Jul 22 Jul 26 Jul 25 Jul 24 Jul

Ending date 18 18 15 16 18 17

Sep Sep Sep Sep Sep Sep

Beginning date

Ending date

0.0359 0.0121 0.0309 0.0005 0.0073 0.0098

0.0228 0.0228 0.0617 0.0370 0.0097 0.0345


FIGURE 4.—Observed and predicted age-0 (YOY) mortality in 2001 and 2002. Observed mortality is the measured decrease in age-0 abundance, predicted mortality the estimated mortality due to cannibalism. Areas are abbreviated as follows: MB ¼ Malletts Bay, IS ¼ the Inland Sea, and ML ¼ the Main Lake; the numerals 01 and 02 refer to 2001 and 2002, respectively. All estimates are for July–September except MB01*, which is for June–September. The dashed line indicates a 1:1 relationship.

during the dawn crepuscular descent but expect it to be minimal because age-0 fish migrate out of the overlap zone during this time. Although we predict that cannibalism is the main cause of mortality for age-0 rainbow smelt between July and September, other sources of mortality will also contribute to the decline. Physical factors such as extreme weather could cause loss of age-0 fish between sampling periods. Similarly, predation by stocked or native piscivores may contribute to age-0 losses, but these have not been studied in Lake Champlain. Finally, the growth rates of both age-0 and age-1þ rainbow smelt may explain the differences between predicted and observed age-0 mortality in September 2002. As a result of high 2001 cohort densities, age-0 fish had low growth rates and recruited to the age-1þ group in 2002 as smaller individuals (Stritzel Thomson 2006). In 2002, low age-0 densities resulted in larger age-0 individuals (Stritzel Thomson 2006); the smaller age-1þ fish may have been less successful cannibalizing the larger age-0 fish due to gape limitations. This suggests that size dependency be used in future experienced density predictions of cannibalism by including only age-0 fish below a critical size. Cannibalism by rainbow smelt has been estimated in Lakes Ontario (Lantry 1991; Lantry and Stewart 2000), Michigan (Lantry 1991; Lantry and Stewart 2000), and Erie (Parker Stetter et al. 2005). Our estimates of age1þ cannibals compare well with Great Lakes data in July of both years and September 2002. However, June 2001 estimates of the proportion of cannibals are considerably higher than the 2–6% in Lantry and Stewart (2000) and the 2–5% in Parker Stetter et al.

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(2005). The differences between our estimates and those of Lantry and Stewart (2000) probably result from differences in seasonal timing, as Lantry (1991) assessed diet and cannibalism in April (before age-0 fish were abundant) and again in August and October. Estimates by Parker Stetter et al. (2005) are based on May–August data, and the use of a seasonal average may obscure higher cannibalism in June. Our September 2001 estimates are also higher than those Lantry and Stewart (2000) and Parker Stetter et al. (2005) because of high densities of age-0 fish in the metalimnion. The levels of age-0 mortality caused by age-1þ cannibals in our study are substantially higher than that needed to cause abundance cycles in population models (e.g., He and LaBar 1994; Lantry and Stewart 2000). We identified two limitations to using acoustics: increasing noise levels with depth and nontarget organisms. The signal-to-noise ratio increases with depth, and small age-0 rainbow smelt targets may not be detectable within that noise. In addition, mysids are abundant in the Main Lake and may increase the number of small targets (Gal et al. 2004). To avoid biases from noise and mysids, we restricted our analyses to depths less than 22 m. Although 4–22 m covered the overlap between age-0 and age-1þ fish in June and July, this depth limit may have excluded the lower range of vertical overlap in September. Additionally, by applying the proportion of cannibals to age-1þ densities only between 4 and 22 m, our calculations assumed that there were no cannibals in deeper water. Cannibalism in forage species requires further study because it complicates the management of prey fish and piscivore stocks. Highly cannibalistic species such as rainbow smelt can have marked and regular population cycles (Lantry and Stewart 2000) that are not tracked by constant annual stocking of piscivores. Both compensatory (e.g., Frankiewicz et al. 1999; Juanes 2003; Persson et al. 2003) and destabilizing (e.g., Polis 1981; Hammar 2000; Kellison et al. 2002) effects of cannibalism have been observed. Therefore, a better understanding of the relationship between cannibalism and forage fish population stability is needed to ensure effective management applications of stock–recruitment curves (Ricker 1954). Acknowledgments Special thanks to crew of the University of Vermont RV Melosira for assistance in the field. We are grateful to editor Dennis DeVries, an associate editor, and three anonymous reviewers for comments that increased the quality and presentation of this manuscript. This work was sponsored in part by a grant from the National Sea

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Grant College Program, National Oceanic and Atmospheric Administration, U.S. Department of Commerce, to Lake Champlain Sea Grant under grant number NA16RG2206. The views expressed are those of the authors and do not necessarily reflect the views of the sponsors. Mention of brand names does not constitute product endorsement by the U.S. federal government. This is publication number LCSG-OO-06, contribution 227 of the Cornell Biological Field Station. Additional funding was received from the National Science and Engineering Research Council (NSERC) of Canada (NSERC postgraduate scholarship to S.L.P.S.). References Burczynski, J. J., P. H. Michaletz, and G. M. Marrone. 1987. Hydroacoustic assessment of the abundance and distribution of rainbow smelt in Lake Oahe. North American Journal of Fisheries Management 7:106–116. Chevalier, J. R. 1973. Cannibalism as a factor in first-year survival of walleye in Oneida Lake. Transactions of the American Fisheries Society 103:739–763. Evans, D. O., and D. H. Loftus. 1987. Colonization of inland lakes in the Great Lakes region by rainbow smelt, Osmerus mordax: their freshwater niche and effects on indigenous fishes. Canadian Journal of Fisheries and Aquatic Sciences 44:249–266. Feinsinger, P., E. E. Spears, and R. W. Poole. 1981. A simple measure of niche breadth. Ecology 62:27–32. Ferguson, R. G. 1965. Bathymetric distribution of American smelt Osmerus mordax in Lake Erie. Proceedings of the Conference on Great Lakes Reasearch, Great Lakes Research Division, University of Michigan, Publication 13:47–60. Folt, C. L., and P. C. Schulze. 1993. Spatial patchiness, individual performance, and predator impacts. Oikos 68:560–566. Frankiewicz, P., K. Dabrowski, A. Martyniak, and M. Zalewski. 1999. Cannibalism as a regulatory force of pikeperch, Stizostedion lucioperca (L.), population dynamics in the lowland Sulejow reservoir (central Poland). Hydrobiologia 408/409:47–55. Gal, G., L. G. Rudstam, and O. E. Johannsson. 2004. Predicting Mysis relicta vertical distribution in Lake Ontario. Archiv fu¨r Hydrobiologie 159:1–23. Garrison, L. P., W. Michaels, J. S. Link, and M. J. Fogarty. 2000. Predation risk on larval gadids by pelagic fish in the Georges Bank ecosystem, I. Spatial overlap associated with hydrographic features Canadian Journal of Fisheries and Aquatic Sciences 57:2455–2469. Goyke, A. P., and S. B. Brandt. 1993. Spatial models of salmonine growth rates in Lake Ontario. Transactions of the American Fisheries Society 122:870–883. Hammar, J. 2000. Cannibals and parasites: conflicting regulators of bimodality in high latitude Artic charr, Salvelinus alpinus. Oikos 88:33–47. He, X., and G. W. LaBar. 1994. Interactive effects of cannibalism, recruitment, and predation on rainbow smelt in Lake Champlain: a modeling synthesis. Journal of Great Lakes Research 20:289–298.

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