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Keywords:

  • climate change;
  • lake ice;
  • thermal niche

Abstract

  1. Top of page
  2. Abstract
  3. First thoughts
  4. Thermal niche of fishes
  5. Long-term trends and variability in lake ice cover
  6. Final thoughts
  7. References
  8. Electronic References

These perspectives on climate change come largely from two views, i.e. that of a fish and fisheries ecologist with an autecological interest and that of a limnologist interested in long-term dynamics and change. Ideas about the thermal niche evolved from the late F. E. J. Fry's (University of Toronto) paradigm of fish response to environmental factors and the late G. Evelyn Hutchinson's (Yale University) formalization of the niche concept. In contrast, ideas about climatic change and variability have been shaped by long-term observation records from lakes around the northern hemisphere. The history of each set of ideas, i.e. the thermal niche of fishes and learning from nature's long-term dynamics, is briefly reviewed in the context of climatic change.


First thoughts

  1. Top of page
  2. Abstract
  3. First thoughts
  4. Thermal niche of fishes
  5. Long-term trends and variability in lake ice cover
  6. Final thoughts
  7. References
  8. Electronic References

Deduction and induction are two central paradigms for achieving new understanding about the world around us and how it works (Rothschild, 2006). Both, of course, play an immense role in the present understanding of climate change and climate change effects on fish and fisheries ecology. The idea of the fish thermal niche developed from both approaches, but perhaps more commonly from induction, experimentation and the elimination of alternate hypotheses to provide weight to an overriding theory about the role of temperature in the life of fishes. The changes in ice cover of lakes around the northern hemisphere, e.g. Lake Mendota, WI, U.S.A., are clearly deductive where the patterns observed in nature contribute to the developing understanding of climatic change. The unfolding stories arising from both inductive and deductive approaches can excite the minds of scientists; the new findings and understanding also can, at intervals, add the shout of ‘Eureka!’ to that of Archimedes.

Here, the history and evolution of the ideas of fish thermal niches and observations of lake-ice seasonality over the years are briefly presented, contrasted and discussed. The comments do not constitute a complete analysis of the history or the literature but come largely from the work in North America and at the Center for Limnology at the University of Wisconsin-Madison, U.S.A.

Thermal niche of fishes

  1. Top of page
  2. Abstract
  3. First thoughts
  4. Thermal niche of fishes
  5. Long-term trends and variability in lake ice cover
  6. Final thoughts
  7. References
  8. Electronic References

The two heroes in this short story about the thermal niche of fishes are the late F. E. J. Fry of the Zoology Department at the University of Toronto, Ontario, Canada, and the late G. E. Hutchinson at Yale University, New Haven, CT, U.S.A. These ideas are considered and reviewed in more detail in Magnuson et al. (1979) in the first paper explicitly on the thermal niche and in Magnuson & DeStasio (1997) who reviewed the idea and research. Fry along with many students developed a framework for fish physiology and behaviour as influenced by environmental factors (Fry, 1947, 1971). Hutchinson formalized the ecological concept of the N-dimensional niche (Hutchinson, 1957).

Fry's work was beginning to be published in the 1950s and stimulated ecology students at that time to conduct simple laboratory experiments on fish activity at different temperatures in class projects at the University of Minnesota, St. Paul, MN, U.S.A. Crude as the equipment and experiments that were conducted by one of those students, the present author, were, the fish tested were found to have higher endurance speeds at intermediate temperatures than at cooler or warmer temperatures. In retrospect such findings were not too surprising, but such experimentation lingered in the minds of young scientists and catalysed further inquiry over their careers.

Fry provided the quantitative tools and knowledge to distribute and evaluate the well-being of a fish species along physical–chemical gradients such as temperature, salinity, dissolved oxygen and pH that directly influenced the physiology of the fish. Fry, his students, colleagues and followers, quantified the levels of an environmental factor for fishes that were lethal, controlled their physiological performance and activity, limited their activities, masked the role of other environmental factors and directed where they chose to be along an environmental gradient. The most useful of these modes of action from an ecological perspective for temperature turned out to be controlling and directive factors, but the ideas of lethal and limiting factors were also of use. The role of temperature in the fishes living as ectothermic heterotherms caused many to think of temperature as the master factor in the life of fishes. Certainly for freshwater fishes, temperature is one of the broad groups by which both anglers and scientists know the freshwater fishes (i.e. cold, cool and warm-water fishes) first described by Hokanson (1977) as temperate stenotherms, temperate mesotherms and temperate eurytherms. Fry's original contributions are often cited in current papers on thermal ecology of fishes.

The second hero identified in the thermal niche story, G. E. Hutchinson, formalized the idea of the N-dimensional niche in the 1950s and early 1960s (Hutchinson, 1957, 1967). Hutchinson provided the concept of niche dimensions over which a species played out its life and interacted with other species. Many useful definitions or ideas came from the Hutchinsonian niche. These included: niche width, fundamental (non-interactive) and realized (interactive) niche, species packing, niche compression, niche shift (interactive segregation) and niche complementarity. Examples of all these have been analysed in fish ecology and have been useful in the development of the ideas of the thermal niche and of temperature as an ecological resource (Magnuson et al., 1979). Individual contributions of Hutchinson, his students, colleagues and followers focused on niche ecology rather than niche ecology of fishes. His papers on the niche concepts are seldom cited in papers on thermal ecology of fishes.

Hutchinson considered the niche axes to characterize an N-dimensional hypervolume which he often portrayed in two dimensions, for example, temperature and food particle size for zooplankton (Hutchinson, 1967). Fry did not quantify biological factors such as food particle size or predation risk, but did consider food quantity in a physiological context. Current ecological knowledge allows a richer mix of niche axes for fishes to be analysed quantitatively.

An early paper on the N-dimensional niche of fishes considered temperature, salinity and oxygen as lethal factors in the survival of fish eggs (Alderdice & Forrester, 1971; Magnuson & DeStasio, 1997). The three axes were visualized graphically and provided a useful portrayal of the N-dimensional world of a fish species. Four or more axes are difficult, if not impossible, to represent graphically. Multivariate statistics provide tools for such complex hypervolumes to be analysed and for different environmental factors to be weighted in regard to their importance in a complex world. Most of these efforts do not frame the question in the context of the Hutchinsonian N-dimensional niche nor in the actual levels of these factors in the lives of fishes.

F. E. J. Fry and G. E. Hutchinson are identified here as the two heroes for the development of the thermal niche of fishes, first and foremost, because they generated and evaluated ideas during their careers that allowed others to understand the world they saw and extend these concepts into their areas of the sciences. In reality, the ideas provided a wonderful context to view the world of fishes. Occasionally, today's scientists lose sight of their histories and heroes and discourage scientists from going beyond the electronic resources and imposed limitations on the citation of the early papers. Successive citation of the next most recently published paper in a topic area has a real potential of scientists losing touch with their intellectual roots and heroes. This certainly appears to be the case for Hutchinson in the literature on thermal ecology of fishes and may even be the case with Fry's contributions in most places. Fry's founding ideas are well appreciated and remembered among the next generations studying the thermal ecology of fishes at the University of Toronto where he practised his science.

Papers from the Wisconsin group on temperature as a niche axis are grouped in Table I by topics beginning with the thermal niche, then distribution of fishes in inland and marine thermal gradients and finally application to global warming. These researches were stimulated by the ideas of Fry and Hutchinson. The availability of funding for these researches came from the idea of thermal pollution as a waste product of electric power generation in the 1970s, fish distribution studies in the Laurentian Great Lakes (Wisconsin Sea Grant Program) and oceanic fronts (U.S. Office of Naval Research) in the 1980s and concerns about the effects of climate change in the 1990s and 2000s. The papers provide examples of the use of the rich context provided by the Fry and the Hutchinson paradigms to a broad range of issues and questions across what might appear as dissimilar environments at first glance, i.e. small lakes and streams, great lakes and oceanic fronts.

Questions addressed by the Wisconsin group were ecological in nature and attempted to observe whether fishes exhibited behaviours and distributional patterns expected from considering fish thermal physiology and behaviour in the context of thermal habitat as an ecological resource. Several of these ecological consequences of treating temperature as an ecological niche axis in the life of fishes serve as illustrations (Fig. 1). The relation between the realized thermal niche occupied by fishes during day in the thermal outfall of an electricity generation facility on Lake Monona, WI, U.S.A., relates rather closely to the fundamental thermal niche as determined from laboratory preferences [Fig. 1(a)]. Thermal niche overlap is apparent for some species. In laboratory studies both intraspecifc [Fig. 1(b)] and interspecific interactions [Fig. 1(c)] influence fish distributions in temperature gradients. An individual or a species displaced from its preferred temperature would see declines in fitness owing to reduced growth rates from living at suboptimal temperatures. Small bluegills Lepomis macrochirus Rafinesque do not remain at their preferred temperatures when a larger dominant L. macrochirus is at that temperature. Comanche Springs pupfish Cyprinodon elegans Baird & Girard in the presence of the pecos gambusia Gambusia nobilis (Baird & Girard) experiences a niche shift to cooler temperatures and a compression of its realized thermal niche. In Lake Michigan [Fig. 1(d)], fish species and age groups are distributed across the thermal gradient during day as determined by bottom trawling at the depths where the thermocline intersects the lakebed. This distribution reveals species packing or the segregation of species and age groups across the thermal gradient. Especially interesting is the segregation of young-of-the-year (YOY) from adult alewife Alosa pseudoharengus (Wilson) that would have the effect of reducing competition between adults and their young. Complementarity in resource use (thermal habitat and prey types) is apparent in the same Lake Michigan trawl samples [Fig. 1(e)]. Species or age groups that occupy similar thermal habitats differ more in prey types, whereas those eating more similar prey types tend to occupy more different thermal habitats. These and other ecological consequences of thinking of temperature as an ecological resource in addition to thinking of temperature as a physiological factor are considered in more detail in Magnuson et al. (1979), Magnuson & DeStasio (1997) and other papers listed in Table I.

image

Figure 1. Ecological consequences of the thermal niche of fishes and thinking of thermal habitat as an ecological resource. (a) The relation between the realized and the fundamental thermal niche of fishes from distribution in a thermal plume during day in Lake Monona, WI, U.S.A., and temperature preferences determined in the laboratory, modified from Neill & Magnuson (1974). (b) Intraspecific, modified from Magnuson et al. (1979), and (c) interspecific competition, modified from Gelbach et al. (1978), both influencing the realized thermal niche in laboratory experiments. (d) The phenomenon of species packing and segregation of species that were caught in bottom trawls during the day across a thermal gradient in Lake Michigan, U.S.A. Species that were relatively uncommon are indicated in black, modified after Brandt et al. (1980). (e) Complementarity in the use of food and thermal habitat, modified from Crowder et al. (1981). Species and age pairs that had <50% overlap in both thermal habitat and prey types are not shown. CPUE, catch per unit of effort; YOY, young-of-the-year.

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Many researchers and research groups have incorporated the ideas that evolved from combining the ideas of Fry and Hutchinson. Their combined ideas have been very useful to the Wisconsin group, the Toronto group and other scholars around the world (Graham & Harrod, 2009) and other reviews relevant to the thermal ecology of fishes (Table I). The influence of the legacy of these creative scientists is clear.

Long-term trends and variability in lake ice cover

  1. Top of page
  2. Abstract
  3. First thoughts
  4. Thermal niche of fishes
  5. Long-term trends and variability in lake ice cover
  6. Final thoughts
  7. References
  8. Electronic References

The second story is about a seemingly simple record of ice freeze and breakup dates and ice-cover duration on lakes over many years. A climate record, so simple, that it does not even require a thermometer or any scientific instrument to collect the data. Long-term records around the northern hemisphere did not originate within the sciences but rather from the practical need for information or even the curiosity that causes many to note the first blooming date of a spring flower or the arrival of migrant birds. Yet, today, the records provide powerful long-term data sets from which researchers can deduce information about climate change and variability.

Climate change is difficult for scientists and non-scientists alike to detect and evaluate because most humans are out of touch with long-term change and what is happening at broad spatial scales. Memories are imperfect and individuals are, more poetically, lost in the ‘invisible present' (Magnuson, 1990, 2008; Magnuson et al., 2006) and the ‘invisible place’ (Swanson & Sparks, 1990; Magnuson et al., 2006). Long-term records of ice-on day, ice-off day and duration of ice cover on Lake Mendota provide a useful example to open up a time series. Ice cover in a single year on Lake Mendota represents the invisible present and place. The record provides no temporal or spatial context. Looking at longer portions of the 150 year record available for Lake Mendota first reveals the high inter-year variability, then the influences of the inter-year dynamics of the El Niño and La Niña phenomena and other large-scale climatic drivers such as the North Atlantic Oscillation. Finally, the full record (Fig. 2) reveals a slow march of the ice dates to later ice on, earlier ice off, and shorter ice-cover duration. When viewing the ice measurements over the last 150 years, the linear trend only explains c. 9–19% of the variability in the time series; the remaining 91–81% results from inter-year variability depending on the ice measure. Not surprisingly perceiving the signal (trend) from the noise (inter-year variability) is difficult and, in a short time series, impossible.

image

Figure 2. Long-term changes in ice seasonality (a) ice-on day, (b) ice-off day and (c) ice-cover duration for Lake Mendota, WI, U.S.A. Ice dates are plotted against the start year of the winter seasons from 1852–1853 to 2009–2010. The 10 cold (inline image) and 10 warm (inline image) extremes winters are indicated except that 13 extremes are marked for ice-off cold extremes (b) owing to four ties at 109 days.

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With the longer records, some of the sources of that variability among years are possible to partition because their dynamics are embedded in that noise. For Lake Mendota (Anderson et al., 1996; Namdar Ghanbari et al., 2009) and for selected lakes around the world (Livingstone, 2000; Magnuson et al., 2005; Bonsal et al., 2006), some of the variability has been associated with various large-scale climate drivers such as the North Atlantic Oscillation, the Pacific Decadal Oscillation, the Southern Oscillation Index and the Atlantic Multidecadal Oscillation. The longer the period of the oscillation, the more difficult it is for observers to distinguish such variability from long-term trends because the short-term trends that they may reveal can persist over interdecadal and multidecadal periods which are themselves often longer than the age of many young observers. Fortunately, today even a young scholar can exhibit the wisdom of an elder by extracting well-managed data sets from websites; in the case of lake ice, for example, the U.S. National Oceanic and Atmospheric Administration's Snow and Ice Data Center has the northern hemisphere data and the North Temperate Lakes Long-Term Ecological Research Program on North Temperate Lakes has records for Lake Mendota and other Wisconsin lakes.

Lake Mendota provides the context to analyse trends and variability over 150 years that is a relevant scale in human and ecological time. But declining ice cover from a single lake does not necessarily indicate a global pattern of warming. Examining lakes regionally and around the northern hemisphere (Magnuson et al., 2000; Benson et al., 2009), however, indicates that the trends are regional and global in nature (Fig. 3). A few exceptions occur and trends vary from lake to lake and region to region; however the pattern is clear and Lake Mendota is in no way unique.

image

Figure 3. Trends in ice break-up and freeze dates of eight lakes in the Northern Hemisphere from 1843 to 2009. Running means with a 1-3-5-3-1 low pass filter are presented along with the linear slopes. Locations are WI, Wisconsin, U.S.A.; SU, Finland; NY, New York, U.S.A.; R, Russia. Data are at the Snow and Ice Data Center of the U.S. National Oceanic and Atmospheric Administration.

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The lake-ice record of Lake Suwa in the Japanese Alps has the longest observed annual lake-ice record; the data are for ice-on day (Arai, 2000, 2009). The record begins in 1443 and originated from a custom of the Shinto Shrine; today it is maintained by the shrine and local climate services. When corrected for the 1 month calendar change that occurred in Japan in the late 1800s, the rate of change in the ice-on day changed dramatically during the early 1800s from c. 1 day later century−1 over the preceding centuries to c. 19 days later century−1 in the 1800s and 1900s. Unfortunately, other records with annual ice dates over so many years do not exist for lake ice. Fortunately, the declines in ice for some valley glaciers are also several centuries long and reveal a change in the rate of melt back in the early 1800s as well (Oerlemans, 2005; Lemke et al., 2007).

Climate change sceptics raise the issues of emails leaked from the University of East Anglia, U.K., in November 2009, as a reason to discount climate sciences in general and the Intergovernmental Panel on Climate Change in particular (Revkin, 2009). The individual climate scientists involved have been exonerated by a British Parliamentary committee (Jasanoff, 2010), but the need for more complete sharing of data and computer codes was made. Independent records such as the lake-ice records provide a view of trends and variability in climate over the past 150 years that is independent from the records and analyses called into question through the leaked emails. Other independent data records also exist. More quantitatively even though the number of lakes is small compared with the larger and denser data sets on air temperature itself, the coherence between ice duration over the past 150 years and northern hemisphere land temperatures is rather high. Lake-ice trends and variability have both signal (trend) and noise (interannual and interdecadal variability) in common with the air temperature changes that are occurring. The Wisconsin group is now analysing long-term changes in extreme ice dates, that is, unusually early and late ice-on and ice-off days as well as unusually short and long durations of ice cover.

The lake-ice observations support the large and growing evidence that the world is warming and that seasonality is changing on average towards earlier springs, longer summers, later autumns and shorter winters. Individually and collectively these observations provide unusually strong deductive evidence for the changing climate. The Sherlock Holmes of today would certainly have said ‘Elementary, my dear Watson’.

Final thoughts

  1. Top of page
  2. Abstract
  3. First thoughts
  4. Thermal niche of fishes
  5. Long-term trends and variability in lake ice cover
  6. Final thoughts
  7. References
  8. Electronic References

Some may ask what is the connection between the two contrasting stories reviewed briefly here? Why were these two chosen? One reason, of course, was that the researchers at the Center for Limnology were involved in both, i.e. a bias of location and participation. The most important connection between these two research stories is that both inductive and deductive approaches are needed to reveal that climate is changing and that these changes influence fishes. One explanation at Wisconsin for the decline in thermal niche research and the rise of long-term ecological research in the early 1980s was that the rationale for long-term research was compelling and opportunities for long-term research were surfacing through the U.S. National Science Foundation in the form of the U.S. Long-Term Ecological Research (LTER) programme.

The most direct scientific interconnection between the niche ecology and the lake-ice seasonality is found in the lives of fishes where shorter periods of ice cover and the corresponding longer periods of warmer temperatures have direct influences. Depletion of dissolved oxygen beneath the ice is less likely to produce anoxia with shorter durations of ice cover and thus winter kill of fishes in many shallow ice-covered lakes is reduced in a warming world (Fang & Stefan, 2009). This change in ice cover might appear to be a win–win for anglers and fishes alike as game fishes can establish and could persist in what were once winter-kill lakes. But even here the consequence should be more nuanced. A community of small fishes [central mudminnow Umbra limi (Kirtland), a number of small cyprinids and other species], well adapted to surviving the conditions of a small winter-kill lake, are intolerant to predation by fish predators that establish in a lake that does not winter-kill or one that has migratory connections for annual reinvasion (Tonn & Magnuson, 1982; Magnuson et al., 1989b). Thus, these assemblages of fishes will become rarer as ice cover declines (Lodge, 1993; Magnuson et al., 1997).

The two examples, long-term lake-ice records and the thermal niche of fishes, described here differ greatly in so many respects. They differ in the fundamental scientific logic involved, the physical and the biological worlds they revealed, the scientific tools used and perhaps even the kinds of minds drawn to the venture. But clearly the integration of findings from induction and deduction is a necessity to advance the science of climate change and variability in the lives of fishes.

The first example, the thermal niche of fishes, had two clear heroes recognized for the major ideas they formulated and tested. Together their ideas and research shaped major areas of research for students and colleagues who persist to this day. Interestingly, they did not form a synthesis team or research team to integrate the linkages between their ideas and contributions. This was done by scores of others influenced by their ideas and research.

The second example, learning from lake-ice time series, based on observed changes in lake ice cover over longer and broader temporal and spatial scales, is clearly deductive science. For the particular example of lake ice, no identifiable hero or heroes set about to provide the record or the ideas to be investigated. The record began and accumulated through efforts of those with no knowledge of its eventual value or use in scientific analyses. For a time series such as the lake-ice records, the generations of observers are perhaps the heroes of such science. Perhaps the unknown heroes are those come to be known but seldom recognized, i.e. the mentors, shamans and grandparents who have shared the information and their knowledge that came from accumulated experience. In the case of lake ice and other records of seasonality or phenology, the experience was recorded quantitatively over years making it far more valuable. While no heroes can be named for most individual time series, several names come to mind for a general appreciation and advocacy for long-term research in the ecological sciences and what it can reveal. To name but three, consider E. D. Le Cren (1985) at Windermere, U.K., G. E. Likens (1983) at Hubbard Brook and Mirror Lake, NH, U.S.A. and the late J. L. Brooks at the U.S. National Science Foundation (Callahan, 1984; Magnuson et al., 2006).

I thank N. D. Magnuson, S. Sharma, I. Winfield (the Guest Editor) and two anonymous reviewers for reading the manuscript and making many helpful suggestions and changes. B. J. Benson assisted with the data preparation for Fig. 3 and W. Feeny prepared the figures. Thank you all very much!

References

  1. Top of page
  2. Abstract
  3. First thoughts
  4. Thermal niche of fishes
  5. Long-term trends and variability in lake ice cover
  6. Final thoughts
  7. References
  8. Electronic References
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Electronic References

  1. Top of page
  2. Abstract
  3. First thoughts
  4. Thermal niche of fishes
  5. Long-term trends and variability in lake ice cover
  6. Final thoughts
  7. References
  8. Electronic References