Short winters threaten temperate fish populations

Abstract

Although climate warming is expected to benefit temperate ectotherms by lengthening the summer growing season, declines in reproductive success following short, warm winters may counter such positive effects. Here we present long-term (1973-2010) field patterns for Lake Erie yellow perch, Perca flavescens, which show that failed annual recruitment events followed short, warm winters. Subsequent laboratory experimentation and field investigations revealed how reduced reproductive success following short, warm winters underlie these observed field patterns. Following short winters, females spawn at warmer temperatures and produce smaller eggs that both hatch at lower rates and produce smaller larvae than females exposed to long winters. Our research suggests that continued climate warming can lead to unanticipated, negative effects on temperate fish populations.

Figure 1. Lake Erie juvenile yellow perch abundance versus mean winter ice cover, 1973–2010.

Winter ice cover was measured as the per cent of lake surface area covered by ice during the winter (February-March) before spawning in (a) western and (b) central Lake Erie in year t (year in which each cohort was hatched). Two-dimensional Kolmogorov–Smirnov tests determined whether changes in the variance of juvenile abundance were related to ice cover from the previous winter. This distribution-free test identifies a threshold value of ice cover (indicated by vertical dashed lines) that maximizes the difference in variance of juvenile abundance between the two sides of the threshold. P values indicate if the variance of juvenile abundance significantly differs between the two sides of the threshold. Above the threshold, juvenile abundance may be high or low, but below the threshold, only low abundances occur. Thus, winter duration appears to ‘set the stage' for future high recruitment to the fishery. Juvenile (age-0) abundance was determined from annual, fisheries-independent Ohio Department of Natural Resources-Division of Wildlife bottom trawling surveys conducted during October of year t, and is presented as catch-per-unit-effort (CPUE; # of individuals per trawl minute) for both (a) western and (b) central Lake Erie.

Figure 2. Lake Erie yellow perch cohort size at age-2 and lifetime harvest by cohort plotted against juvenile abundance, 1987–2010.

Juvenile(age-0) abundance (1987–2010) was determined from annual, fishery-independent Ohio Department of Natural Resources-Division of Wildlife bottom trawling surveys conducted during October in (a) western and (b) central Lake Erie, and is presented as CPUE (# of individuals per trawl minute) in year t (year in which each cohort was hatched). Estimates of cohort size at age-2 in year t+2 for (a) western and (b) central Lake Erie (1987–2010) were generated by the Great Lakes Fishery Commission's Lake Erie Yellow Perch Task Group. Lifetime harvest by cohort in (c) western and (d) central Lake Erie is the cumulative harvest by commercial fishers and recreational anglers (1987–2008) at ages 2–5 (that is, years t +2 through t+5). Linear regression was used to relate cohort size at age-2 and lifetime harvest by cohort to fall juvenile abundance. Results indicate fall juvenile abundance is a good proxy for future recruitment to age-2, when yellow perch typically become reproductively mature and enter the fishery. Thus, recruitment to the fishery is strongly influenced by factors operating prior to first fall of life, with strong recruitment events supporting Lake Erie's commercial and recreational fisheries for many years afterwards.

Figure 3. Lake Erie yellow perch (a) embryo hatching success and (b) larval size-at-hatching versus individual egg mass when exposed to a short and long winter in the laboratory.

Winter-duration treatments used in our experiment were based on historical (1994–2010) field measurements of water temperature from a central Lake Erie water intake located near Cleveland, OH, USA (41° 32′ 53′′ N, 81° 44′ 60′′ W). The short winter duration (52 days) was similar to the number of days below 5 °C recorded during winter 1999 (N=59 days below 5 °C), which was, until 2012, the warmest winter on record for Ohio (1895–2013). Our long winter duration (107 days) was equal to the mean number of days below 5 °C observed during 1994–2010. Each winter duration treatment had six replicate tanks, although fertilized samples for embryo hatching success and larval size-at-hatching were only obtained from four replicate tanks in each treatment. All data are presented as tank means±1 s.e. (1–3 observations per tank). Large eggs hatched at higher rates (linear regression: embryo hatching success=0.37·egg mass−0.5) and produced larger larvae (linear regression: larval total length=0.27·egg mass+4.3) than small eggs.

Figure 4. Mean daily water temperature from short and long winter-duration treatments used in a controlled laboratory experiment with Lake Erie yellow perch.

Winter-duration treatments used in our experiment were based on historical (1994–2010) field measurements of water temperature from a central Lake Erie water intake located near Cleveland, OH, USA (41° 32′ 53′′ N, 81° 44′ 60′′ W). The short winter duration (52 days) was similar to the number of days below 5 °C recorded during winter 1999 (N=59 d below 5 °C), which was, until 2012, the warmest winter on record for Ohio (1895–2013). Our long winter duration (107 days) was equal to the mean number of days below 5 °C observed during 1994–2010. The duration of spawning is shown for each treatment. Labels indicate the dates and water temperatures during which females spawned. Despite earlier arrival of suitable spawning temperatures (8–14 °C within grey shading; this study) following a short winter, females did not initiate spawning at these ‘normal' temperatures in our experiment, and instead spawned at warmer temperatures during the ‘normal' spawning period (that is, mid-April through May1418).

Figure 5. Relationship between (a) bottom water temperature and date and (b–d) the probability that a yellow perch female was spent and bottom water temperature during spring 2010–2012 in western Lake Erie.

Bottom water temperatures in (a) are presented as means±s.d. for each sampling event (2010: N=9–20, 2011: N=9–20, 2012: N=4–9 observations per sampling event) and related to date, in each year, with linear regression. Coloured lines in (b–d) were determined by logistic regression; dashed lines in b indicate 95% confidence intervals. Dates in (b–d) identify the date on which bottom water temperatures reached 10 °C in each year (determined from regressions conducted on data in (a)). Solid black lines in (b–d) indicate probabilities determined for 8, 10 and 12 °C each year. During (b) 2010 and (c) 2011, spawning had begun by the time the temperature reached 8 °C and was well under way by the time temperatures reached 10 °C. During (d) 2012, the year with the earliest spring, fish were not yet spawning when the temperature reached 8 °C, and were barely spawning at 10 °C. Instead, spawning was concentrated at warmer temperatures than during (a) 2010 and (b) 2011. The asterisks indicate that the probability of females being spent at 8, 10 and 12 °C differed in 2012 (P<0.05; 95% confidence intervals do not overlap) when compared with 2010 and 2011, which had similar probabilities across all temperatures (P>0.05; 95% confidence interval overlap).