Disrupted seasonal cycle of the warm-adapted and main zooplankter of Lake Biwa, Japan
Graphical abstract
Introduction
Variations of environmental conditions throughout the year play an important role in influencing the abundance of organisms across time. Many species have developed behavioral and life-history strategies to exploit specific periods of the year best matching their optimal niche requirements for reproduction, growth, and minimizing exposure to stressful periods (Ji et al., 2010). However, environmental variations due to global changes are having profound effects on the seasonal abundance of organisms. Notably, the seasonality of many aquatic organisms has been affected by climate and human-related changes (Edwards and Richardson, 2004). Several zooplankton exhibited earlier appearance of their seasonal peak in response to global warming (Edwards and Richardson, 2004), but the shift is not consistent for all functional groups (Costello et al., 2006). Another effect of climate change on zooplankton is an increase in voltinism (Winder et al., 2009).
Lake ecosystems are particularly sensitive to climate change (Shimoda et al., 2011), and lentic zooplankton populations, with their limited capacity for long-range migration to seek optimal conditions elsewhere, are more susceptible to such changes. Being entrapped, lentic zooplankton’s most common response to climate warming is a change in their seasonality (Adrian et al., 2006, Seebens et al., 2007, Winder et al., 2009). Such response impacts the zooplankton community as a whole and may alter the food-web structure (Nakazawa and Doi, 2012). Warming is predicted to affect different trophic levels unequally, and such asynchronous modifications of the seasonal cycle may result in a mismatch or a better match between trophic levels and functional groups (Thackeray et al., 2010).
The seasonal pattern of plankton abundance results from the combined effect of top-down and bottom-up controls, the life-cycle traits of the species, and physical factors. The contribution of different factors varies with the trophic state of the lake and the lake’s latitudinal location (Sommer et al., 2012). Furthermore, the annual phenology of species is affected by inter-annual variations in temperature, which, in turn, depend on variations in atmospheric modes of circulation (Manca et al., 2014) or climate change (Adrian et al., 2009). Any changes in these forcing factors (e.g., warming) and/or trophic controls are likely to affect the seasonal pattern of species.
The phenology of lacustrine copepods is strongly related to climate forcing (Manca et al., 2014), water temperature (Adrian et al., 2006, Winder et al., 2009), and fluctuation in resource availability (Winder et al., 2009). Under sufficient food supply, water temperature is the main parameter that controls seasonal copepod population dynamics (Halsband-Lenk et al., 2004). In temperate lakes, the effects of food and predation may be of minor importance for long-term changes in copepod dynamics (Gerten and Adrian, 2002). Conversely, in subtropical lakes, food availability and phytoplankton dynamics are more important (Chang et al., 2014). Fish predation also can regulate zooplankton seasonal succession in both deep (Yoshida et al., 2001b) and shallow (Jeppesen et al., 1997) lakes. Given the differences in the contribution of temperature, food, and predation, all three external factors need to be considered to understand changes in copepod seasonal dynamics.
Additionally, there is a strong species-specific response to the changes (Gerten and Adrian, 2002), and most species-specific responses have been investigated on populations from mid- and high latitude regions (Ji et al., 2010). Compared to temperate species, species from tropical systems and/or warm-adapted species may exhibit different reaction norms due to the evolution of thermal adaptations that result in different life-history patterns (Roff, 1992). Such life-cycle traits of planktonic species were shown to govern their phenological response to climate warming (Adrian et al., 2006). “How do warm-adapted copepods differ from their temperate congeners?” remains a question to be answered.
Lake Biwa, the largest lake in Japan, has experienced eutrophication and warming over the past several decades. Nutrient loading increased between the 1960s and-1970s, and has contributed to the appearance of Uroglena americana and cyanobacterial blooms starting in 1977 and 1983, respectively (Kumagai, 2008). Following the enforcement of a water treatment regulation in 1980, nutrient loading was progressively reduced and then stabilized after 1985 (Kumagai, 2008). However, since the late 1980s, the surface temperature of the lake has risen by 1 °C, adding another element of external forcing to consider for the Lake Biwa ecosystem (Hsieh et al., 2010). Changes in nutrients and physical conditions due to eutrophication and warming have led to the reorganization of Lake Biwa phytoplankton community (Hsieh et al., 2010, Tsai et al., 2014) and, in turn, the zooplankton (Hsieh et al., 2011). Fluctuations in the mesozooplankton from the 1960s to late 1980s was related to the change in the trophic status of the lake, while the variations from the late 1980s to 2005 were caused by warming (Hsieh et al., 2011). Additionally, fisheries catch data revealed a decrease in planktivorous fishes since 1990 (Maehata, 2012). Along with these changes in Lake Biwa’s environment over the last decades, Hsieh et al. (2011) noted that several zooplankton taxa exhibited phenological shifts, but they did not provide any details on those shifts and their triggering factors remain to be determined.
The calanoid copepod Eodiaptomus japonicus is an important endemic species of Japan, with a distribution spanning over the entire Japanese main island (Makino et al., 2013). In Lake Biwa, E. japonicus dominates the zooplankton community year-round (Hsieh et al., 2011, Liu et al., 2020), and is an essential prey for the commercial fishes Ayu (Plecoglossus altivelis; Kawabata et al., 2006) and Isaza (Gymnogobius isaza; Briones et al., 2012). The sole detailed study on E. japonicus phenology was conducted over a three-year period and revealed a population composed of overlapping cohorts and a bimodal annual pattern (Kawabata, 1987b). High egg production was observed in June and from August to October (Kawabata, 1987b). However, the appearance of the first and second abundance peak varies interannually, and the sources of such variation were only speculative (Kawabata, 1987b). There is a need to understand E. japonicus variable population dynamics and identify its main drivers. Eodiaptomus japonicus is adapted to high temperature, suggesting their population dynamics may be decoupled from temperature increases (Liu et al., 2014). Differences in the body size of adults reared in the lab at satiety and individuals from the field suggested a strong food limitation (Liu and Ban, 2018). A strong size-selective predation pressure was suggested by the impact of planktivorous fish predation on Lake Biwa’s zooplankton biomass (Liu et al., 2020).
We investigated mechanisms driving copepod phenology, and in particular, the case of a food-limited warm-adapted species. We tested the hypothesis that in a food-limited environment, temperature alone does not lead to the appearance of several abundance peaks during the year, but rather the combination of food availability and predation does. To test our hypothesis, we evaluated the response of various life-cycle traits of E. japonicus to environmental variations in Lake Biwa using an extensive dataset over a 45-yr time period (1966–2010). We applied wavelet analysis to examine the disruption in the seasonal cycle previously noticed; and cluster analysis to identify the external factors associated with the different forms the seasonal cycle can take (i.e., bimodal, plurimodal). Finally, we assessed which of the environmental variations among food availability, predation, and temperature, or combinations of these factors, could explain the dynamics of this species.
Section snippets
Study-site
Lake Biwa is the oldest and largest lake in Japan (surface area: 670 km2, maximum depth: 104 m). The lake comprises a mesotrophic north basin and a eutrophic south basin, and is located in the subtropical zone (35°20′N). Monitoring started in 1962 by the Shiga Prefectural Fisheries Experiment Station (SPFES) for fisheries management purposes. Our analyses were based, in part, on data from this lake-monitoring program. We analyzed monthly samples from a station in the middle of Lake Biwa’s north
Results
The results obtained on EjT and the sum of CI to CVI stages were similar. We, therefore, only present the results for EjT.
Discussion
Our results highlighted large variances of seasonal dynamics in E. japonicus abundance in Lake Biwa during 1966–2010 with different seasonal patterns among the years. The disrupted seasonal dynamics of E. japonicus population were mediated through interaction effects with food conditions and predation pressure, and the influence level varied with other environmental factors such as temperature.
Declaration of Competing Interest
The authors declare that they have no known competing financial interests or personal relationships that could have appeared to influence the work reported in this paper.
Acknowledgments
We sincerely thank the people who contributed to the zooplankton field sampling in Lake Biwa these past years. We express our gratitude to Emi Doi for her continued efforts in the zooplankton counting and body size measurement. We are grateful to the scientists of the Shiga Prefectural Fisheries Experiment Station for collecting zooplankton samples and environmental data. This work was supported by grants from the Ministry of Agriculture, Forestry and Fisheries, Japan for a research project
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