Multi-scale and multi-system perspectives of zooplankton structure and function in Canadian freshwaters
Publication: Canadian Journal of Fisheries and Aquatic Sciences
1 April 2021
Abstract
This review provides a Canadian perspective on freshwater zooplankton diversity and ecology across scales and systems. It aims at describing how zooplankton are diverse in forms and functions, and constitute a key component of plankton food webs, a model for ecological theories and a sentinel for monitoring ecological integrity and function in lakes facing environmental changes and anthropogenic stressors. These objectives are addressed across a continuum of scales (continental, regional and local) and systems (reservoirs, lakes and ponds). This perspective shows that the environmental control of zooplankton biodiversity, community structure and function in Canada is complex and variable. Zooplankton communities demonstrated a wide range of responses to anthropogenic disturbances across scales and systems due to interactions with watershed biogeochemistry and climate. This review supports the Multiple Forces hypothesis where forcing by abiotic factors (climate, nutrients, morphometry and chemistry) has a fundamental role at continental scale over Canadian ecoregions, and at regional scale in the Boreal ecozones. In contrast, forcing by biotic factors (algal resources and predators) is relatively more influential at local scale, in resort and urban regions. The challenge for future research will be to combine all new concepts and approaches in a global perspective to better understand the responses of freshwater zooplankton to multiple environmental changes and anthropogenic stressors in Canada.
Résumé
La présente synthèse offre une perspective canadienne sur la diversité et l’écologie du zooplancton d’eau douce à plusieurs échelles spatiales et dans différents systèmes. Elle montre comment le zooplancton présente une diversité de formes et de fonctions et constitue un élément clé du réseau trophique du plancton, un modèle pour les théories écologiques et une sentinelle pour surveiller l’intégrité écologique des lacs face aux changements environnementaux et aux facteurs de stress anthropiques. Ces objectifs sont abordés dans un continuum d’échelles (continentales, régionales et locales) et de systèmes (réservoirs, lacs et étangs). Cette perspective démontre que les contrôles environnementaux de la biodiversité, de la structure et de la fonction du zooplancton lacustre au Canada sont complexes et variables. Le zooplancton présente un large éventail de réponses aux perturbations anthropiques à différentes échelles et dans différents systèmes en raison des interactions avec la géochimie et le climat du bassin versant. La synthèse appuie l’hypothèse du contrôle multiple selon lequel le forçage par des facteurs abiotiques (climat, nutriments, morphométrie et chimie) joue un rôle fondamental à l’échelle continentale dans les écorégions canadiennes et à l’échelle régionale dans les écozones boréales. En revanche, le forçage par des facteurs biotiques (ressources algales et prédateurs) est plus influent à l’échelle locale, dans les lacs des régions périurbaines et urbaines. Le défi futur consistera à combiner tous les nouveaux concepts et approches dans une perspective globale pour mieux comprendre les réponses du zooplancton d’eau douce aux multiples changements environnementaux et facteurs de stress anthropiques au Canada. [Traduit par la Rédaction]
Introduction
In Canada, lakes are dominant features of the landscape and a legacy for the future of limnology (Boggero et al. 2014). Since the mid-20th century, limnology has been a crucial research theme in ecology, leading to the development of theories, models, new visions and approaches for assessing the effects of environmental changes and anthropogenic stressors on the ecological quality and conservation status of inland waters (Miranda et al. 2019). Freshwater lakes are among the most valuable ecosystems on earth as they hold a relatively rare (about 3% of earth water) and essential water resource that provide a wide range of provisioning, regulatory and cultural services (Gleick 1998; Corvalan et al. 2005; Dudgeon et al. 2006). However, their biodiversity and ecological integrity are endangered by multiple and often increasing anthropogenic stressors, including acidification and eutrophication, land use, invasion of exotic species, pollution, overfishing and climate change (Collen et al. 2014; Reid et al. 2019). A recent meta-analysis of the net-effects of these multiple stressors in freshwater ecosystems demonstrated complex additive, synergetic or antagonistic interactions (Jackson et al. 2016). Accordingly, one of the major challenges for limnology in the 21st century is to measure and model response of ecosystems to complex and cumulative effects of climate change and anthropogenic disturbances, and to explain patterns of distribution, abundance and function of freshwater organisms across scales and systems (see Stendera et al. 2012 for a review). Understanding the importance of local and regional environmental changes on lake ecosystems is particularly relevant to Canada, considering its freshwater resources. How these ecosystems will respond to current and future changes in environmental and anthropogenic stressors across large-scale Canadian landscapes is still unclear.
Microorganisms are the foundation of plankton food webs (Sommer and Stibor 2002), biogeochemical processes (Cotner and Biddanda 2002) and lake productivity (Havens and Beaver 2010). However, knowledge and prediction of the effects of environmental changes, either natural or anthropogenic, on microorganisms is still limited compared to macroorganisms and this remains a gap in effective ecosystem management (Fontaneto et al. 2006; Martiny et al. 2006; Fontaneto 2011).
In freshwaters, microorganisms such as zooplankton are an ideal model to investigate the ecological quality of ecosystems and determine how natural and anthropogenic processes influence diversity patterns, species distributions and functions. Zooplankton have proven to be a valuable biosentinel to track changes in ecological integrity of lake ecosystems (Jeppesen et al. 2011; Valois et al. 2011; Anas et al. 2017). Zooplankton is sensitive to lake acidification (Pinel-Alloul et al. 1990, 1995; Yan et al. 1996; Keller et al. 2002) and eutrophication (Ejsmont-Karabin 2012; Ejsmont-Karabin and Karabin 2013; Haberman and Haldna 2014) as well as watershed land-use disturbances caused by agriculture, deforestation, and residential development (Stemberger and Lazorchak 1994; Patoine et al. 2000; Gélinas and Pinel-Alloul 2008a). Invasion of exotic species (Yan et al. 2008) and calcium decline in softwater boreal lakes (Jeziorski et al. 2008) associated with climate warming (Carter and Schindler 2012; Carter et al. 2017) have known impacts on zooplankton communities and in turn on entire food webs through cascading effects (Schindler et al. 2005). Overall, changes in spatial patterns in zooplankton community structure, which occur on a hierarchical continuum of scales (Pinel-Alloul and Ghadouani 2007), are the result of multiple natural ecological processes and anthropogenic disturbances acting from local to global scales. As both natural and anthropogenic processes operate differently over geographical scales, a landscape perspective across ecoregions is now required to model large-scale spatial patterns of freshwater biota and predict their responses to environmental changes (Soranno et al. 2010; Loewen et al. 2019).
In this review, we present a Canadian perspective on freshwater zooplankton diversity and ecology. We describe the biodiversity of zooplankton, its role in plankton food webs, its potential as a model system for ecological theories and as a sentinel for biomonitoring of lakes. These objectives are addressed across a continuum of scales (continental, regional and local) and systems (reservoirs, lakes and ponds) by comparing spatial patterns of zooplankton structure and function in major types of freshwater ecosystems in Canada. We will examine different hypotheses addressing spatial patterns in zooplankton biodiversity and community structure at the continental scale of Canada, the regional scale of lake districts of the boreal ecoregions, and the local scale of peri-urban and urban lakes and ponds. To assess continental-scale patterns, we will describe how climate gradients and historical biogeography control biodiversity and distribution of crustacean species in lakes across ecozones at the scale of Canada. To evaluate the responses of boreal lakes to watershed disturbances at a regional scale, we will assess the influence of reservoir impoundment, water acidification, and watershed deforestation on zooplankton diversity and composition across different ecoregions of the Canadian Boreal ecozone. At a local scale, we will present how watershed disturbances by residential and urban development influence zooplankton diversity and community structure in periurban lakes of resort areas in southern Québec and in urban lakes of a large Canadian city. The final goal for this review is to identify gaps in zooplankton research across ecosystems and evaluate future needs for a comprehensive understanding of the effects of environmental changes on Canadian freshwater systems.
Zooplankton as a source of biodiversity in forms and functions
Freshwater zooplankton are represented by a diversity of microscopic animals which have adapted to their changing environment through a large variety of forms and functions (Balian et al. 2008). Zooplankton is represented by diverse taxonomic groups composed of protozoans, rotifers, cladocerans and copepods. Hereby, we will focus on four major groups: Rotifera, Cladocera, Calanoida and Cyclopoida Copepoda (Fig. 1). They are diverse in forms and functions varying in size, morphology, life history, and reproductive and feeding modes.
Fig. 1.
Rotifera is a phylum of some 1850 species (Segers 2002) and an important component of microbial food webs in a variety of freshwater habitats (Wallace and Ricci 2002). They are diverse in morphology, living alone (e.g., Keratella cochlearis) or in colony (e.g., Conochilus unicornis) (Fig. 1a). They are phenotypically plastic and have developed defenses (long spines and large lorica) against invertebrate predators such as large carnivorous rotifers (Asplanchna) or cyclopoid copepods (Stemberger and Gilbert 1984; Gilbert 2013). Rotifers are opportunistic and colonising species, called r-strategists, with rapid reproduction and short life cycles of a few days to weeks. Reproductive modes vary from exclusive sexual reproduction with gametogenesis (Seisonidae), cyclical parthenogenesis and gametogenesis (Monogonta), to exclusive ameiotic parthenogenesis (Bdelloidae) (Wallace 2002). Asexual reproduction by cyclical parthenogenesis is the general mode in most species, but sexual reproduction between females and dwarf males with the production of dormant resting eggs may alternate with asexual reproduction in unstable environments. Interestingly, the bdelloid rotifers (Fig. 1a) found in littoral zones of lakes and ponds are exclusively parthenogenetic (Birky and Gilbert 1971; Birky 2004). They have the ability to survive in harsh environments by entering a state of desiccation-induced dormancy (Ricci 2001). They have survived for more than 80 million years without sex (Welch and Meselson 2000) scavenging new genes from bacteria, fungi and other pond life microorganisms. Rotifer’s feeding strategies range from suspension feeding on bacteria and algae to omnivory and carnivory on protozoa and other zooplankton (Pourriot 1977). Most of the rotifers are primarily detritivores and herbivores feeding on organic matter and algae (Starkweather 1980), but a few species (Asplanchna spp.) are omnivorous preying on large algae and zooplankton (Gilbert 1980).
Cladocerans are small crustaceans (0.3–10 mm), commonly called water fleas, found in pelagic and littoral zones in most freshwater habitats. Cladocera are members of the phylum Arthropoda, the subphylum Crustacea, and the class Branchiopoda (Frey 1987; Fryer 1987). Worldwide, freshwater cladocerans accounted for a total of ∼150 species (Korovchinsky 1996, 1997). In North America, thirty to fifty common pelagic species are recorded, including the common Daphnia (Dodson et al. 2010; Pinel-Alloul et al. 2013). Except for a few species (Polyphemus pediculus, Leptodora kindtii, Bythotrephes longimanus), they have a non-segmented body, a down-turned head with a single median compound eye and a rostrum, and a shell carapace covering the thorax and abdomen (Fig. 1b). Cladocerans are r-strategist species with short life cycles of a few months. They reproduce principally by asexual cyclical parthenogenesis. They use sexual reproduction only in adverse conditions, forming males and resting eggs that allow the species to survive. Resting eggs (called ephippia), which are similar to plant seeds, can survive several hundreds of years in lake sediment, be dispersed by birds and aquatic mammals and recolonize new habitats (Pietrzak and Slusarczyk 2006; Šlusarczyk et al. 2006, 2019).
The feeding strategies of the cladocerans are very diverse ranging from herbivore-detritivore to carnivore behaviors (Smirnov 2017), using various modes for collecting food in suspension in water or on various substrates. Pelagic cladocerans such as Holopedium, Daphnia, Ceriodaphnia, and Bosmina are considered as herbivores-detritivores collecting and filtering small algae as well as organic particles and bacteria. Littoral cladocerans living on macrophytes, rocks and sediments feed on various organic particles from algae to decomposed matter. Filter feeding is performed by sedentary Sida and Simocephalus spp. Chydorids and macrothricids can be coprophagic feeders eating on chironomid fecal pellets. Some species (Scapholeberis) found in small urban ponds collect pollen and organic matter deposed on the surface film of water (Pinel-Alloul and Mimouni 2013). Finally, some chydorids (Pseudochydorus) and large cladocerans in the littoral (Polyphemus) and pelagic (Leptodora, Bythothrephes) habitats are carnivorous species predating rotifers and small cladocerans.
Freshwater copepods are composed of three groups of free-living small crustaceans: the Calanoida, Cyclopoida, and Harpacticoida. Calanoids and cyclopoids are generally pelagic, whereas harpacticoids are epibenthic. In this review, we will focus only on the pelagic calanoids and cyclopoids (Fig. 1c). Worldwide, copepods are tremendously diverse, with 2814 known species inhabiting freshwaters (Boxshall and Defaye 2008; Dussart and Defaye 2002, 2006) and 33 Calanoida and 17 Cyclopoida common pelagic species recorded in Canadian lakes (Pinel-Alloul et al. 2013). Copepods have a segmented bullet-shaped body of small size typically between 0.5 to more than 3 mm (Reid and Williamson 2010). The head is fused with the first one or two thoracic segments forming a cylindrical cephalothorax, while the remainder of the thorax has three to five segments, each with limbs. The abdomen contains five segments without any appendages, and it ends with a furca. Calanoids have long antennae as long as or longer than the body itself whereas cyclopoids have antennae shorter rarely extending beyond the cephalothorax. Copepods are sexual organisms with complex reproductive strategies, called K-strategists, in which periods of rapid development of distinct instars alternate with periods of arrested development in diapause (Hairston and Bohonak 1998). Their life cycles include 6 nauplii stages, 5 copepodite stages and the male and female adult stages (Fig. 1c). The entire life cycle from hatching to adulthood can take a few weeks to several months or years depending of the species and environmental conditions. Males find a mate by detecting pheromones emitted by females in the open water. During mating, the male grips the female with its geniculated antennae and deposits spermatophores on the female’s genital opening to fertilize eggs. Eggs are carried by adult females in one (Calanoida) or two (Cyclopoida) bundles attached to their abdomen until hatching. Copepods can interrupt their development by diapausing in deep waters or sediments, either as resting eggs for the calanoids (Hairston and Van Brunt 1994) or as active or encysted copepodite stages for the cyclopoids (Pinel-Alloul and Alekseev 2019). Feeding strategies of copepods range from herbivory to carnivory. Many planktonic calanoid copepods are commonly described as suspension-feeders eating algae and microzooplankton (Vanderploeg and Paffenhöfer 1985; Wong and Chow-Fraser 1985). Many cyclopoid copepods switch from herbivory to omnivory and carnivory during their development from nauplius to copepodites and adults. They have a raptorial mode of feeding using their mandibles to prey on a variety of animals such as protozoans and microzooplankton (Leblanc et al. 1997).
Zooplankton as a keystone player in plankton food web models and biomanipulation of lakes
Food webs are a powerful way to describe complex ecological relationships from micro- to macroorganisms, as well as patterns of biodiversity and energy flow in freshwaters (Thompson et al. 2012). Since the eighties, the classical concept of the pelagic food chain (McQueen et al. 1986) was expanded to include the microbial loop (Porter et al. 1988) and to give a comprehensive representation of the structure of plankton food webs and their control by bottom-up versus top-down processes (Auer et al. 2004). Zooplankton is central to plankton food web models. Zooplankton organisms act as a trophic bottleneck between algal resources and vertebrate and invertebrate predators. At the base of the food web, phytoplankton composition and size can be regulated by nutrient availability or enrichment. Such regulation is commonly referred to as “bottom-up” control. At the top of the food web, piscivorous fish can exert “top-down” control via predatory cascades on planktivorous fish.
This simple model of food webs was adopted by managers and applied in whole-lake biomanipulation and restoration projects to control algal blooms in temperate, subtropical and tropical lakes (Crisman and Beaver 1990; Lazzaro 1997; Carpenter et al. 2001; Jeppesen et al. 2005; Søndergaard et al. 2007). Removal of planktivorous fish by selective fishing or through the introduction of piscivorous fish can increase the abundance of efficient zooplankton filterers such as large daphnids, recognized as “engineer species”. Herbivory by such large species of daphnids can in turn reduce algal biomass and indirectly increase water transparency (Havens and Beaver 2010). While being quite efficient in mesocosms, biomanipulation had nonetheless a moderate and short-term success in real case situations because of the complexity and heterogeneity of plankton food webs (Benndorf 1995; DeMelo et al. 1992; Hansson et al. 1998). A meta-analysis of biomanipulation experiments in 123 lakes (Bernes et al. 2015) has concluded that removal of planktivorous and benthivorous fish is a useful means of improving water quality in eutrophic lakes, and tends to be particularly successful in relatively small lakes with short retention times and high phosphorus levels. Nonetheless successes and failures have occurred across a wide range of conditions. Biomanipulation was more often successful in temperate lakes inhabited by visual zooplanktivorous fish than in subtropical and tropical lakes inhabited by omnivorous fish (Lazzaro 1997). Even in temperate lakes, trophic cascades and biomanipulation proved more successful in mesotrophic lakes than in oligotrophic and eutrophic lakes because the coupling between zooplankton and phytoplankton and the cascading effect of the predation of piscivorous fish were stronger in lakes of intermediate productivity (Elser and Goldman 1991). Overall, biomanipulation success is dependent on the structural complexity of pelagic food webs resulting from bottom-up and top-down control mechanisms (Mehner et al. 2002). The consideration of scales is important for understanding trophic interactions within pelagic food webs and in turn for effective management of ecosystems. The structure of food web networks can be influenced by local-scale variations in lake size and depth, nutrient enrichment and trophic status (Benndorf et al. 2002), as well as by regional-scale variations in watershed disturbances and anthropogenic stressors in lacustrine landscapes (Pinel-Alloul et al. 2002). Any change in the composition of the macrozooplankton (large cladocerans and copepods) and microzooplankton (rotifers, protozoans) components may profoundly affect top-down control of pelagic food webs, nutrient cycling and lake productivity (Sommer and Sommer 2006), and indirectly alter ecosystem responses to environmental changes and anthropogenic stressors.
Zooplankton as a model for ecological theory
Freshwater zooplankton is a model for theoretical ecology, as the importance of scale, function and evolution to plankton ecology is well recognized and has helped develop concepts of metacommunities (Leibold et al. 2004). Zooplankton is a spatially well-structured and dynamic community influenced by many abiotic and biotic processes (Fig. 2) interacting differently along a continuum of scales within and among lakes (Pinel-Alloul and Ghadouani 2007).
Fig. 2.
Spatial heterogeneity has been recognized as a multiscale characteristic of zooplankton community within lakes since the 1990s (Pinel-Alloul 1995). Large-scale patterns in zooplankton distribution are prevalent on the horizontal axis of lakes and related to hydrodynamic currents induced by dominant winds, river inflows and upwelling (Pinel-Alloul et al. 1999). In contrast, small-scale patterns are most common on the vertical axis of lakes and induced by antipredator vertical migration (Masson et al. 2001; Gélinas et al. 2007; Slusarczyk and Pinel-Alloul 2010) or feeding behaviours (Angeli et al. 1995; Pinel-Alloul et al. 2008). Across landscapes, zooplankton is seen as a “Complex Adaptive System” (CAS) (Leibold and Norberg 2004; Norberg 2004) in which spatial patterns in composition and structural traits result not only from local (environmental filters within lakes) but also from regional processes related to plankton dispersal and hydrological connectivity among lakes. Regional diversity can also promote local diversity by reversing the negative effect of novel invasive species and support the ecology theory of the Spatial Insurance hypothesis (Loewen and Vinebrooke 2016). In addition to these ecological processes, biogeographical and evolutionary history could also have strongly regulated zooplankton metacommunities patterns in the past (Leibold et al. 2010; Henriques-Silva et al. 2016). Since 2000, the meta-ecosystems concept has served to develop a more complex view of zooplankton spatial heterogeneity across multiple scales and systems (Loreau et al. 2003). This point of view states that the physical, chemical and biological features of lake ecosystems are controlled by hierarchical processes and cross-scale interactions acting at local and regional scales within freshwater, terrestrial and human landscapes (Soranno et al. 2010, 2014). Consequently, biomonitoring of freshwater ecosystems should follow natural and anthropogenic land features from large ecoregions and ecoprovinces to smaller boreal lake districts, and peri-urban regions (Hawkins et al. 2000; Cheruvelil et al. 2008).
Zooplankton as a sentinel for monitoring Canadian lake ecological integrity and response to global change and anthropogenic stressors
Research conducted in my laboratory on freshwater zooplankton in Canada has adopted a multi-scale and multi-system framework with a landscape perspective. In this section, patterns of variation of zooplankton biodiversity and community structure are presented at continental, regional and local scales, and in different types of ecosystems. How zooplankton communities in Canadian lakes are influenced by climate, environmental gradients and human disturbances is examined across scales going from macroecology to microecology. Focus is made on studies testing the Multiple Forces hypothesis (Fig. 2) (Pinel-Alloul 1995) on the environmental control of zooplankton community structure and diversity across scales and lake ecosystems in Canada. Case studies are reported across a geographical gradient going from continental to local scales and along a disturbance gradient ranging from pristine lakes to lakes disturbed by watershed land-use, and finally to managed urban lakes and ponds (Fig. 3; see Table S1, Supplemental material1). This review adopts a multifaceted framework for examining patterns in zooplankton biodiversity and community structure across scales and systems, using different attributes and sampling methods (Fig. 3). Finally, based on the research programs conducted by Canadian limnologists, this synthesis will show that zooplankton spatial heterogeneity and environmental control result from complex and multiple ecological processes varying among scales and systems (Fig. 4).
Fig. 3.
Fig. 4.
Macroecological patterns in crustacean zooplankton in Canada: the role of climate, biogeography and lake environments
Macrosystems Ecology (MSE) (Heffernan et al. 2014; Levy et al. 2014) is a powerful framework to study spatial patterns of freshwater microorganisms in response to environmental changes at global scale. Since the last century, biologists have intensively applied macroecology theory to analyse large-scale diversity patterns of macroorganisms in terrestrial ecosystems, in relation with the metabolic theory and the energy-richness hypothesis; this hypothesis predicts a decrease in diversity with the lower solar energy and temperatures associated with higher latitudes (Hillebrand 2004; Mittelbach et al. 2007; Hawkins et al. 2007). In contrast, knowledge of macroecological patterns of aquatic microorganisms in relation to energy radiation is still in its infancy (Fontaneto et al. 2006; Martiny et al. 2006) even though lakes and ponds are now recognised as model systems for macroecological research (Hortal et al. 2014). At a global scale, few studies have reported on biogeographical diversity patterns of freshwater fish (Kerr and Currie 1999) and algae (Vyverman et al. 2007; Stomp et al. 2011) with much more limited studies focusing on zooplankton. More recently, studies on large-scale spatial patterns of freshwater zooplankton gave additional evidence of the influence of latitudinal gradients in climate, biogeography and lake trophic status for shaping species richness and community structure. Across America, crustacean zooplankton communities in lakes and reservoirs in temperate and tropical regions varied with latitude and trophic status (Pinto-Coelho et al. 2005). Eutrophic ecosystems supported greater crustacean abundance at all latitudes. However, cladocerans and cyclopoids were more abundant in eutrophic lakes and reservoirs, whereas calanoids were more abundant in oligotrophic temperate lakes (Pinto-Coelho et al. 2005).
Canadian studies were among the first providing a comprehensive model relating diversity patterns of pelagic crustaceans to environmental gradients along a wide range of physiographic, climatic and lake environments in North America (Pinel-Alloul et al. 2013; Henriques-Silva et al. 2016). Overall, at least 83 crustacean species (33 Copepoda Calanoida, 33 Cladocera, and 17 Copepoda Cyclopoida) inhabited the pelagic zone of 1665 Canadian lakes distributed in 47 ecoprovinces across the latitudinal gradient (Pinel-Alloul et al. 2013). Crustacean species richness in Canadian lakes was comparable to that observed in other large-scale and multiple-year surveys along altitudinal and latitudinal gradients (Arnott et al. 1998; Shurin et al. 2007; Hessen et al. 2006, 2007; Lyons and Vinebrooke 2016). Species richness of pelagic crustacean zooplankton in Canada ranged from 3–10 species per lake (average local species richness) to 7–44 species per ecoprovince (average regional species richness) or 5–82 species (based on the Jackknife Index) (Fig. 5). Species-rich lakes were typically located in the ecoregions of the Boreal Shield and Boreal Plain and in the Hudson-Erie and the Great Lakes-Saint Lawrence Plains. In contrast, the species-poor lakes were found in the northern and arctic ecoregions. The maps of distribution of crustacean species across Canadian ecoregions reflected their thermal preference in relation to latitudinal climate, their mating system (asexual or sexual reproduction), and their past colonisation during the last glaciation in Canada. According to the macroecology theory, the Canadian model established for lake crustacean zooplankton fully supported the species richness-energy hypothesis that inferred a higher diversity at lower latitude and higher temperature (Hillebrand 2004), consistent to that found for fish (Kerr and Currie 1999). The latitudinal gradients in solar radiation and air temperature were the strongest drivers of spatial patterns in crustacean zooplankton diversity (regional species richness and Jackknife diversity index per ecoprovince) at the continental scale of Canada (Pinel-Alloul et al. 2013) (Table S11). Mean daily global solar radiation and temperature explained 51% of the large-scale variation in regional species richness among ecoprovinces, supporting the energy-diversity hypothesis. Moreover, the observed increase in local species richness with ecoprovince area supported the area-diversity hypothesis (Pinel-Alloul et al. 2013).
Fig. 5.
The pan-Canadian model of freshwater crustacean diversity also supported the Multiple Forces hypothesis (Fig. 5), as large-scale species richness patterns were mainly controlled by abiotic factors related to latitudinal climatic gradients, ecoprovince area, and past biogeography related to glacial history (Table S11), as reported in Norway (Hessen et al. 2006, 2007) and southern Québec (Pinel-Alloul et al. 1990). In addition, biotic factors such as mating systems and life-cycle strategies of species interacted and influenced the geographical range size (GRS) of lake crustacean zooplankton at continental scale. Obligate sexual copepods had a smaller GRS and steeper latitudinal gradients than the cyclic parthenogenetic cladocerans (Henriques-Silva et al. 2016). First, cladoceran species were generally widespread whereas most copepods had a spatially-restricted distribution. Cladocerans showed the usual decrease in species diversity towards northern latitudes associated with an increase in average GRS and were highly influenced by climatic conditions. Copepods, on the contrary, did not show any significant relationship with latitude and their distribution was more related to historical factors related to glaciation and dispersal limitation. At a regional scale in mountain lakes of western North America, macrospatial distribution patterns of obligate sexual copepods are also more constrained by dispersion limitation than parthenogenetic asexual cladocerans (Loewen et al. 2019). These striking differences found among macroecological patterns in cladocerans and copepods were probably due to their mating system, which influenced many processes such as the susceptibility to Allee effects in earlier stages of colonization, how rapidly they can adapt to local conditions and monopolize resources as well as the number of generations needed during the growing season to produce diapausing eggs for the copepods (De Meester et al. 2002). Notably, previous research involving large-scale patterns in diversity and distribution of freshwater microcrustaceans often neglected the potential effects of these fundamental life-history differences. For instance, Mazaris et al. (2010) could not find either spatial or environmental predictors that accounted for zooplankton large-scale compositional patterns in lakes in northern and central Greece and this could result from pooling both cladocerans and copepods in the same analysis. In contrast, Leibold et al. (2010) have shown that cladocerans responded more to local-scale lake environmental factors (e.g., limnological variables) while copepod distribution was better related to biogeographic events. Their findings corroborate the Canadian model, and show that even at broader scales, cladocerans continue to respond strongly to the environment (e.g., large-scale climatic gradient) because they were less dispersal-limited while copepods distribution was more regulated by historical factors, mating strategy and dispersal barriers (e.g., Beringian refuge; Rocky Mountains) (Henriques-Silva et al. 2016).
Regional-scale spatial patterns in freshwater zooplankton: the impacts of impoundment, water acidification and watershed deforestation
With the increasing development and extraction of natural resources starting in the 1970s, Canadian freshwater ecosystems were not exempt from degradation recorded at the regional scales (Christensen et al. 2006; Kreutzweiser et al. 2013). Among the most common perturbations, hydrological disturbance due to reservoir impoundment, watershed land-use and deforestation, eutrophication and acidic deposition, as well as species invasion have been identified as major stressors of boreal ecosystems (Keller 2009). However, understanding the individual and combined impacts of such stressors on the ecological integrity and function of boreal lakes is a complex issue due to region specific responses and complex interactions between natural factors and climate (Schindler 2001). This section provides key case studies using zooplankton as an effective bioindicator to track the effects of major anthropogenic perturbations on boreal lakes and reservoirs.
Reservoir impoundment
Dams and impoundments of rivers created for generation of hydroelectric power had profound impacts on freshwater environments, ecological processes and biota (Marty et al. 2004). The creation of large reservoirs in northern Québec in the 1970s and their long-term (7-years) ecological monitoring have provided a unique opportunity to assess the impacts of impoundments on zooplankton communities in boreal lakes and rivers (Pinel-Alloul et al. 1982, 1989). Impoundment of reservoirs has been associated with an increase in zooplankton biomass and changes in community composition in both inundated rivers and lakes. The flooding phase induced a trophic upsurge of the whole planktonic food-web due to the release of nutrients and labile organic matter from inundated soils and vegetation, as observed in other northern reservoirs in Canada (Duthie and Ostrofsky 1975). Variation in the intensity and length of the trophic upsurge depends on the initial trophic state of the flooded ecosystem but also on landscape characteristics such as soil thickness, type of vegetation and its degradability. In most boreal ecosystems, a return to baseline conditions was observed after 15 to 20 years (Marty et al. 2004).
Overall, zooplankton species assemblages in reservoirs were similar to those observed in natural lakes and rivers of the James Bay area (Pinel-Alloul et al. 1979). However, the trophic upsurge induced by flooding constitutes a bottom-up forcing that increases nutrients, and in turn phytoplankton and zooplankton biomass (Table S11). Zooplankton biomass was 2–6-fold higher in the new reservoir LG-2 compared to reference lakes (Pinel-Allout and Méthot 1984). After flooding, cladocerans and rotifers responded rapidly to the trophic upsurge, since they are generally more adapted to variable hydrological characteristics of reservoirs (Marty et al. 2004). Thus, zooplankton communities within reservoirs are usually dominated by fast-growing organisms (r-strategist species) such as cladocerans and rotifers compared to copepods that have a longer development time (K-strategist species). Increase in zooplankton biomass was related to higher temperature, nutrients and algal biomass in flooded lake sites, and to longer water residence time in flooded river sites (Méthot and Pinel-Alloul 1987; Pinel-Alloul et al. 1989). Overall, water residence time was the best predicting variable of zooplankton biomass, followed by water temperature, total phosphorus, chlorophyll a, and turbidity (Marty et al. 2004). The gradual increase in zooplankton biomass lasted for the first 4–5 years after impoundment. At short-term, there was no decline in productivity as nutrient concentrations remained stable.
A comparative analysis among reservoirs in northern Québec provided a more comprehensive perspective of long-term changes in zooplankton community in new and older reservoirs, compared to reference lakes (Marty et al. 2004). This analysis based on the estimation of limnoplankton biomass (zooplankton and large algae > 53 µm) indicated a dampening in bottom-up forcing with years as older reservoirs supported lower limnoplankton biomass than new reservoirs. In general, zooplankton communities benefited from the large inputs of detritus and algal resources in new impoundments, compared to river and lake environments. However, the bottom-up forcing lasted only for less than a decade (5–10 years) as older reservoirs supported similar zooplankton communities and biomass as the reference lakes.
Acidic deposition
The acidification of lake ecosystems is a complex process as it may be caused by natural characteristics of watersheds (granitic rock geology, drainage of organic acids from wetlands) or by anthropogenic sources (dry and wet acidic atmospheric depositions due to mining emissions). During the 1980s, acidification of lakes emerged as a major concern in the Boreal Canadian Shield, and large-scale lake surveys were conducted in northeastern Ontario (Locke and Sprules 1994; Yan et al. 1996, 2008; Keller 2009) and southern Québec (Pinel-Alloul et al. 1990, 1995). Zooplankton has been shown to be an excellent indicator of water acidification which results in the decline of species richness and changes in species assemblages (Brett 1989). Acidic lakes (pH < 5.5) were poor in species and characterized by acid-tolerant rotifers (Keratella taurocephala), and small cladocerans (Bosmina sp., Diaphanosoma sp.) and copepod calanoids (Leptodiaptomus minutus); they lacked acid-sensitive species such as large cladocerans (Daphnia) and some other copepods (Epischura lacustris, Skistodiaptomus oregonensis, Diacyclops bicuspidatus thomasi) (Pinel-Alloul et al. 1990; Valois et al. 2011). Spatial patterns in zooplankton community structure revealed strong gradients related to natural and anthropogenic acidification. However, the response of zooplankton to recent declines in the rate of acidic deposition from atmospheric sources was confounded by interactions with other factors such as climate, watershed geology, lake morphology, and predator and invasive species (Pinel-Alloul et al. 1995; Christensen et al. 2006; Yan et al. 2008; Anas et al. 2017; Couture et al. 2021) (Table S11).
Lake recovery from acidification and other multiple stressors remains an important issue for the ecological integrity of boreal lakes (Valois et al. 2011). After the reduction in Canadian sulfur emissions and the Canada–US air quality agreement, liming experiments were conducted to accelerate lake recovery (Yan et al. 1996). Although results were encouraging, recovery success varied among lakes and crustacean groups. Crustacean species richness increased by 2-folds after neutralization, but copepods recovered more rapidly than cladocerans (Yan et al. 2004). The severity of past acidification, water conditions, and biological resistance to colonisation affected lake recovery (Arnott et al. 2001). For instance, zooplankton community in more acidic lakes (pH 4.5) did not completely recover 15 years after neutralization whereas recovery was completed within 10 years of liming in less acidic lakes (pH 5.7) (Yan et al. 1996). Paleolimnological studies showed that cladoceran assemblages were more strongly affected by acidification in clear-water lakes with low dissolved organic carbon content than in naturally acidic and dystrophic lakes with high dissolved organic carbon content (Korosi and Smol 2012). Another important threat for crustacean zooplankton in softwater boreal lakes of Canada is the decline of calcium concentrations consequent to reduced acidic deposition and lower inputs of calcium from catchment (Jeziorski et al. 2008). With a decline of calcium concentrations near or below 1.5 mg·L–1, keystone herbivores such as Daphnia with high calcium demand for moulting might be replaced by the large gelatinous cladoceran Holopedium gibberum, a Ca-poor competitor adapted to low-calcium and brown-water lakes, and less vulnerable to invertebrate and fish predation. This widespread process, known as jellification of lakes (Jeziorski et al. 2015), has also been shown to be associated with climate warming. It has the potential to negatively impact planktonic food webs, and the functions and services provided by boreal lakes throughout the Northern Hemisphere (Weyhenmeyer et al. 2019).
A recent review (Lacoul et al. 2011) assessing the biological consequences of surface water acidification in the Atlantic Provinces of Canada reported that, despite a decreasing trend in sulfate deposition since the 1990s, recovery in base cations (calcium, magnesium) and pH are not yet being reached due to acid-shock episodes in response to rapid snowmelt during early spring or rain-fall events. Similar results were reported in a large-scale study of 73 lakes in southern Québec based on the comparison of two years (1982–2017) (Couture et al. 2021). Despite a sharp temporal 3-fold decrease in lake sulfate concentration, only a slight rise in pH and a small drop in calcium were recorded. The 2017 lake survey in southern Québec still supported a multiple forcing of spatial patterns in zooplankton community by large-scale gradients in climatic conditions, lake exposure to acidic deposition, and local-scale changes in lake water quality and morphology, as observed 35 years ago in 1982 (Fig. 6). No major changes in zooplankton assemblages were detected over time since the 1980s. Segregation of zooplankton species with respect to acidification indicators (calcium, pH) in southern Québec in both 1982 (Pinel-Alloul et al. 1990) and 2017 (Couture et al. 2021) reflects the classification established by Lacoul et al. (2011) across eastern Canada. Previous studies indicated that critical thresholds of pH (4.5 to 6) and calcium (Ca) (1.5–2 mg·L−1) in Boreal Shield lakes might have detrimental effects on zooplankton diversity and success of key and vulnerable species such as Daphnia (Yan et al. 1996; Holt and Yan 2003; Jeziorski et al. 2008, 2015). The large-scale survey of lakes conducted in 2017 in southern Québec further highlighted the importance of calcium thresholds in supporting key zooplankton attributes such as the diversity and the abundance of crustaceans (Couture et al. 2021). In contrast no clear pH threshold could be identified for either zooplankton diversity or abundance. A recent analysis of the multi-trophic responses of lake plankton food webs (phytoplankton, zooplankton and fish) to environmental gradients in southern Québec highlighted the complex ecosystemic responses of lakes to large-scale spatial heterogeneity in climate, lake morphometry and water quality (Taranu et al. 2021). In the Boreal Plain and Taiga Shield ecozones in northeast Alberta, zooplankton metacommunity structure was also under the multiple control of natural abiotic (water chemistry, lake depth) and anthropogenic (industrial emissions) factors, as well as biotic factors related to predation regime and species invasion (Bythotrephes) (Yan et al. 2008; Jeziorski et al. 2015; Anas et al. 2017).
Fig. 6.
Watershed deforestation and clear-cut harvesting
Following the 1988 Yellowstone’s fires, many studies documented the impacts of natural wildfires on terrestrial and aquatic ecosystems (Turner et al. 2003). Clear-cut logging and wildfires are the most important perturbations of the boreal forest (Canadian Forest Service 1998), but their respective effects on lakes have remained largely unknown until the 1990s. Because of the importance of boreal forests to the Canadian economy and the need for new legislation favourable to the protection of ecosystems, the Canadian forestry industry partnered with research centers and created the Sustainable Forest Management Network (SFMN) in 1995 to address issues related to sustainable forest management practices (University of Alberta 2020). The SFMN comparative study remains the only one that has compared the impact of logging to those of wildfires at the scale of watersheds, thus providing a framework allowing one to compare the impacts of human-made catchment-scale perturbations (logging) to those of a natural, unpredictable, uncontrollable perturbation (wildfire). However, comparing both types of perturbation on comparable terms proved difficult because wildfires generally affected greater surface areas of catchments (91% on average) relative to logging (47% on average). Since 1995, large-scale studies using comparative, BACI (Before and After Controlled Impact), and paleolimnological approaches were conducted in Québec, Ontario and Alberta (Carignan and Steedman 2000).
Because of its trophic position between primary producers (phytoplankton) and secondary consumers (planktivorous fish), zooplankton have been considered sensitive to changes originating at either end of the trophic food chain (McQueen et al. 1986). Since changes in nutrient availability or in the fish community structure can originate from the alteration of a lake’s catchment, zooplankton has the potential to serve as an indicator of catchment-scale perturbations (Schindler 1987). The effects of natural fires and forest harvesting on zooplankton communities have been evaluated in the Boreal Shield lakes of Québec (Patoine et al. 2000, 2002a, 2002b) and Ontario (Lévesque et al. 2017), and in the Boreal Plain lakes of Alberta (Prepas et al. 2001) (Fig. 7). The comparison of ecosystemic responses of Boreal Shield and Boreal Plain lakes to wildfire and clearcut logging disturbances served to develop better forestry management (Pinel-Alloul et al. 2002; Prepas et al. 2003).
Fig. 7.
The impacts of logging and wildfires on zooplankton communities were examined in a large-scale comparative experiment set in the Canadian Boreal Shield forest, in the province of Québec (Patoine et al. 2000). Thirty-eight (38) lakes were selected based on their similarity in terms of depth, surface area and drainage ratio. They included 20 lakes whose catchments have not been perturbed during the 80 years before the study, 9 lakes whose catchments have been logged in 1995, one year prior to the beginning of the study, and 9 lakes whose catchments have been burnt by wildfires, also one year before the first year of sampling. The impacts of logging and wildfires on water quality, plankton and fish were examined using the same set of lakes. Impacts differed quantitatively and qualitatively between logging and burning for water quality and phytoplankton community attributes. Quantitatively, the concentrations of some nutrients and chlorophyll a were positively related to indicators of catchment forest loss. Since forest loss in the burnt group was on average greater than in the logged group, nutrient and chlorophyll a increases were generally greater in the burnt group than in the logged group of lakes. Logging effect was characterized by higher concentrations of dissolved organic carbon (DOC), unnoticed after wildfires (Carignan et al. 2000). The resulting decrease in light penetration in the logged group of lakes explained why phytoplankton did not increase as much in the logged group (∼+40% Chl-a relative to the reference group in the first year) relative to the burnt group (∼+60%), despite similar increases in nutrient loadings in both logged and burnt groups (Planas et al. 2000).
The impacts on zooplankton community structure were monitored for up to three years after wildfire and logging disturbances using different attributes: zooplankton and limnoplankton biomass (Patoine et al. 2000), species richness and assemblages (Patoine et al. 2002a), and crustacean biomass size structure (Patoine et al. 2002b). Among these attributes, the biomass size structure of the crustaceans appeared to be the most sensitive, revealing a significant biovolume increase of larger-sized organisms (>1000 µm, mainly large cladocerans and cyclopoid copepods) in the “burned-lakes” group during two years following wildfires (Patoine et al. 2002b) (Table S11). This was hypothetically attributed to an increased availability of calcium in the burned group. Indeed, as calcium can be a limiting element essential to the carapace of Daphnia (Hessen et al. 2000), its increased availability in the burned group could have favored increased growth of large species of cladocerans such as Daphnia. Limnoplankton biomass also indicated a gradual increase in the biomass of a small size fraction (100–200 µm, mainly rotifers and algae) in the burned-lakes group during the first and second years, but not the third year after perturbations (Patoine et al. 2000). In the logged lakes, there was no detectable variation in the biomass of rotifers, cladocerans and cyclopoid copepods, but the biomass of calanoid copepods decreased significantly (Patoine et al. 2000). There were no significant changes in zooplankton species richness and composition one year after wildfire and logging disturbances (Patoine et al. 2000a) (Table S11).
Overall, the impacts of watershed perturbation by logging or wildfires seem stronger at the base of the food web (nutrients, phytoplankton), intermediate at the zooplankton community level, and weaker at the fish community. The increase in rotifer biomass in the burnt group of lakes can hypothetically be attributed to a bottom-up effect (trophic upsurge) (Fig. 7) where increased nutrients inputs from ashes deposited in the watershed at spring lead to increased biomass of algae grazable by rotifers. In contrast, the decrease of calanoids in the logged group of lakes could result from their grazing activity being negatively impacted by decreased light availability, a consequence of increased concentrations of dissolved organic carbon observed specifically in the logged group of lakes. Differences in fish abundance and composition were not detected among the reference, logged, and burnt groups of lakes (St-Onge and Magnan 2000).
As these results based on comparative studies might be affected by the potential confounding effect of uncontrolled variability in lake and watershed characteristics on the observed among-group differences (logging vs wildfires), further studies testing the impacts of watershed clearcut logging adopted a before-after comparison impact (BACI) design that controls for natural year-to-year changes in climate conditions (Winkler et al. 2009; Lévesque et al. 2017). These BACI studies conducted in the boreal forest have confirmed that long-term variations in zooplankton abundance and composition in Boreal Shield lakes were more related to variations in climatic or limnetic conditions than to short-term effects of logging activities (Lévesque et al. 2017). In addition, comparative studies indicated that the impacts were minor when clearcut logging was limited to less than 40% of the catchment’s surface or in lakes with small drainage ratio (watershed area/lake area ratio < 4) (Pinel-Alloul et al. 2002; Prepas et al. 2003; Deininger et al. 2019). Compared to the Boreal Shield lakes, the zooplankton of Boreal Plain lakes seems more sensitive to logging, as Prepas et al. (2001) have reported significant decreases of cladocerans and calanoids in logged lakes relative to reference lakes (attributed to an increase of inedible cyanobacteria algae subsequent to increased nutrient exports from the catchment). Overall, the studies on lakes of the boreal ecozones support the Multiple Forces hypothesis showing greater influence of long-term abiotic and climate forcing than short-term effect of wildfire and clearcut logging watershed disturbances (Fig. 7).
After the 1988 Yellowstone fires studies (Turner et al. 2003), concerns regarding climate changes and one of its immediate consequence (increased fire frequency) have contributed to maintaining an interest in the ecological consequences of wildfires. The most recent reviews suggest that the response of lakes to wildfires may be weaker but longer-lasting than that of rivers (McCullough et al. 2019) and that the environmental setting of the system studied (its type, size, location) plays an important role in the observed response, or lack thereof (Robinne et al. 2020). Paleoecological studies suggest that the impact of wildfires on zooplankton species composition may only become apparent at decadal time scales, at least in lakes of the Canadian West Coast (Bredesen et al. 2002).
Local-scale spatial patterns in freshwater zooplankton: the effects of residential and urban developments
Landscape limnology evaluating land-water interactions is essential for a comprehensive management of lakes in modern human-dominated landscapes (Soranno et al. 2010). Lakes should not be managed as if there are all the same, but should be classified within management-relevant classes according to different watershed land uses. Zooplankton which responds to bottom-up forcing by increasing nutrient inputs is a relevant indicator of watershed disturbances (Stemberger and Lazorchak 1994; Haberman and Haldna 2014). In the USA, a landscape perspective was applied to compare zooplankton communities in shallow lakes of different watershed land uses (natural, agricultural and urban) in southeastern Wisconsin (Dodson et al. 2005). Zooplankton community structure (species richness and composition) was indirectly associated with watershed land uses, via their effects on nutrient inputs, riparian vegetation and hydrological continuum. Natural lakes with more vegetation in the littoral zone favoured higher zooplankton species richness. Lakes in agricultural landscapes with wide riparian vegetative zones had also more taxa than agricultural and urban lakes with narrow riparian or unvegetated littoral zones. In Canada, the lack of specific ecological assessments in periurban and urban lakes still makes it difficult to predict how zooplankton and the overall lake food web responds to different watershed land uses associated to residential and urban developments.
Residential development
Canada is one of the countries in the world experiencing rapid increase of small lakes and ponds in cities, and periurban regions (Bourne et al. 2003). These freshwater habitats support key ecosystem services such as water resources and recreational activities which contribute to human well-being and regional economies (Corvalan et al. 2005; White et al. 2010). Since the 1970s, periurban lakes in different regions of Canada have faced increasing residential development in their watersheds. Forest clearing, cottaging, shore erosion, discharge of fertilizers, harvesting of submerged wood debris and macrophytes are among the most important threats that may affect directly or indirectly lake ecosystems (Christensen et al. 1996; Jennings et al. 2003). Identifying the effects of land-cover disturbances by residential development on ecological integrity and biota of lakes is crucial for the ecological management of watersheds and lakes at local scale. However, only a small number of studies have been carried out in lakes of periurban and resort regions in Canada, despite the rapid conversion of watersheds for cottaging and residential land-use.
The first initiative deployed in the districts of Muskoka and Hamilton Counties in southern Ontario has quantified the effects of lakeshore development on inland waters (Lakeshore Capacity study, Dillon et al. 1994). Trophic status models based on hydrological budgets and phosphorus mass balances were applied for predicting nutrients (total phosphorus: TP), algae biomass (as chlorophyll a), and water clarity from watershed characteristics. Yan (1986) was the first to predict the bottom-up effect of increasing nutrient (TP) on zooplankton biomass in resort lakes in central Ontario. Zooplankton biomass averaged 57 mg·m−3 and increased from 25 to 100 mg·m−3 along a TP range of 5 to 20 µg·L−1, typical of these nutrient-poor oligotrophic lakes.
In Québec, trophic status models (TP-Chl a) were also used to predict the increase in the biomass of algae >20 µm in response to nutrient enrichment in oligo-mesotrophic lakes of the Laurentian and Eastern Townships regions (TP: 3–34 µg·L−1) (Masson et al. 2000), and across a larger range of trophy (TP: 10–100 µg·L−1) (Watson et al. 1992). In these lakes, the response of zooplankton community to nutrient enrichment was evaluated using limnoplankton size fractions (Masson et al. 2004). Zooplankton mean biomass ranged from 40 to 388 mg·m−3 among lakes along a TP gradient of 3 to 34 mg·m−3, and the two large size fractions (>500 µm: large cladocerans and copepods; >200 µm: small cladocerans and copepods) accounted for most of the total biomass. At the regional scale, bottom-up forcing by increasing nutrients (TP) was predominant in the control of epilimnetic zooplankton biomass for all size fractions. At local scale, other factors (depth of the euphotic zone, water temperature and transparency, and types of fish community) also affected zooplankton size structure and biomass. The contribution of the large size fraction > 500 µm was lower than that of the size fraction 200–500 µm in the epilimnion of lakes without piscivore fish, and increased by two-fold in lakes with piscivores, indicating top-down trophic cascades. The biomass of the two large size fractions in the metalimnion increased in clear lakes with piscivore fish, and inversely in lakes without piscivores because macrozooplankton gained from the deep chlorophyll maxima in the metalimnion of stratified lakes, when devoid of planktivore predation (Pinel-Alloul et al. 2008; Pannard et al. 2015). Hence, the large-scale study of Masson et al. (2004) supported the Multiple Forces hypothesis (Pinel-Alloul 1995) as zooplankton size structure was controlled by both bottom-up (nutrient and algal resources) and top-down (planktivory) forces acting at regional and local scales.
The Multiple Forces hypothesis was further enforced when using zooplankton functional traits (Litchman et al. 2013) to investigate the determinants of crustacean zooplankton community structure in lacustrine districts of southern Québec (Barnett and Beisner 2007; Barnett et al. 2007; Vogt et al. 2013). Zooplankton functional diversity was strongly correlated with bottom-up variables related to lake productivity (nutrients, water transparency, and chlorophyll a). This relationship was driven by the predominantly herbivorous cladocerans found in the large size fractions, as these depended on lake primary productivity and phytoplankton community structure (ratio diatoms/chrysophytes to cyanobacteria). The relative importance of bottom-up and top-down drivers of zooplankton size structure was examined in three different lacustrine landscapes of Québec varying by their trophic status (Finlay et al. 2007). The small-size fractions (200–1000 µm) responded to trophic gradients whereas the large size fraction (>1000 µm) responded to fish predation. The bottom-up forces (algal resources and nutrients) were stronger drivers of zooplankton size structure in lakes with residential and agricultural watersheds (Eastern Townships – Laurentian regions), whereas top-down forces were more important in lakes with unperturbed watersheds (Gouin region) (Table S11) (Finlay et al. 2007).
To specifically evaluate the effects of residential development of watersheds, crustacean zooplankton community were compared in lakes of the Laurentian region (Québec) along a gradient of residential disturbance (Gélinas and Pinel-Alloul 2008a, 2008b). Gradients in residential development ranged from 0 to 340 dwelllings·km−2 at the watershed scale but could reach 686 dwellings·km−2 when considering a 50-m wide nearshore strip of land. Gradients in land-cover disturbance varied from 0 to 53% of cleared forest in the watershed and 0 to 86% in the nearshore (<50 m). The land-cover cascade (LCC) concept (Burcher et al. 2007) coupling land and water, was combined with path analysis to identify the proximal and intermediate factors linking residential disturbances to crustacean zooplankton responses (Gélinas and Pinel-Alloul 2008a). Human disturbances on the nearshores and watersheds (residential density and % of cleared forest) induced a nutrient enrichment which had cascading effects on algal biomass, water clarity and crustacean zooplankton biomass and assemblages (Fig. 8). Large-scale residential development of watersheds had a greater influence than did the clearing of forested lands. Crustacean biomass increased with residential development, especially in watershed with more than 200 dwellings·km−2. Cascading effects varied among crustacean functional groups. The strongest cascade effects were observed for the small cladocerans (Bosmina, Ceriodaphnia, Diaphanosoma, small Daphnia species) and cyclopoids through nutrient enrichment. Cascading effects were weaker for the large cladocerans (Daphnia, Holopedium) and calanoids; these were more affected by changes in the depth of the euphotic zone and the level of zooplanktivory. These large Daphnia reside in deeper zones close to the metalimnion in stratified lakes where they can graze on deep chlorophyll layers while avoiding fish predation (Gélinas and Pinel-Alloul 2008b; Pinel-Alloul et al. 2008). As seen in other north-temperate lakes (Dodson et al. 2005; Hoffmann and Dodson 2005), the post-1970s transformation of pristine lacustrine environments into recreational lakes in Canadian periurban and resort regions has promoted nutrient transfers from watersheds to lakes and indirectly affected zooplankton crustacean community diversity, biomass and structure.
Fig. 8.
Urban development
The importance of small ponds and lakes for sustaining aquatic biodiversity and zooplankton communities has been less investigated in urban landscapes than in resort and agricultural landscapes. Urban ponds and lakes represent diverse types of freshwater habitats, some of them tailored to human needs (Hassall 2014). Urban waterbodies constitute a mosaic of environmental habitats favouring high heterogeneity among community assemblages. Even if many individual ponds may contain few species, they contribute greatly to aquatic biodiversity in cities (Mimouni et al. 2015). They also represent key ecosystems especially suited for testing ecological and evolutionary theories (Leibold 1999; De Meester et al. 2005). Moreover, blue spaces contribute to a wider range of ecosystem services in cities by providing natural spaces and restorativeness which favour human health and well-being (White et al. 2010). Management practices must maintain a large diversity of aquatic habitats and organisms to sustain ecological values and biodiversity in urban regions (Hassall 2014; Mimouni et al. 2015).
In Europe, several bioindicators have been used to assess patterns of biodiversity and community structure in farm and urban ponds. Plants, amphibians, insects and benthic macroinvertebrates have been the most used (Oertli et al. 2005; Hassall 2014). In contrast, planktonic organisms at the base of trophic food webs, responding directly to watershed disturbances, have been less investigated. Despite increasing conversion of urban regions for residential and industrial land uses in Canada (BiodivCanada 2011), few attempts have been made to advance the ecological knowledge of urban waterbodies and assess their potential for sustaining aquatic biodiversity. Recently, environmental monitoring of urban freshwaters, based on planktonic indicators, has been developed in large Canadian cities. For phytoplankton, Rolland et al. (2013) recorded harmful cyanobacteria blooms as an indicator of water quality in the Lake St Charles, the drinking water supply for Québec City. Vincent and Kirkwood (2014) found dominant phytoplankton groups (blue-green and euglenid algae) to be potential indicators of eutrophic and high organic conditions in urban stormwater ponds from Durham region in Ontario. Lévesque et al. (2020) evaluated changes in biodiversity, size-fractionated biomass and community structure of phytoplankton to assess the effects of limnological features and management practices in urban ponds and lakes of Montréal City. Phytoplankton indicators based on in situ fluorometry and biovolume of functional groups of the microphytoplankton (>25 µm) were fairly coherent in characterising the typology of urban waterbodies and showed potential for their biomonitoring.
The use of zooplankton as an indicator of water quality and biodiversity in urban ponds and lakes is also appealing because it responds quickly to changes in watershed land-use (Dodson et al. 2005; Gélinas and Pinel-Alloul 2008a), water chemistry (Pinel-Alloul et al. 1990), and hydroperiod length in temporary ponds (Boven and Brendonck 2009). Recently, several studies have evaluated how zooplankton communities respond to spatial heterogeneity in limnological features and management in urban ponds and lakes (Pinel-Alloul and Mimouni 2013; Mimouni et al. 2015, 2016, 2018). We evaluated zooplankton species richness, community structure and functional diversity in the pelagic and littoral zones of 18 urban ponds and lakes of Montréal City during summer 2010 and 2011 (Mimouni et al. 2018). The typology of the selected waterbodies was representative of those found in dense urban areas of North American cities. Urban lakes and ponds of Montréal City represented an important reservoir of biodiversity (Mimouni et al. 2015), sustaining levels of zooplankton species richness greater than or comparable to other small lakes in agricultural landscapes (Dodson et al. 2005; Drenner et al. 2009). Zooplankton species richness in the urban region accounted for a total of 90 taxa, rotifers being the most diverse (60 taxa), followed by cladocerans (24 taxa) and copepods (6 taxa). Local species richness varied from 2 to 26 taxa among waterbodies (Mimouni et al. 2015). Cladocerans and rotifers contributed the most (41% and 55%, respectively) to spatial heterogeneity in zooplankton assemblages (beta diversity) among waterbodies. Biotic factors such as macrophyte cover accounted for 63% of the variation in species richness, followed by abiotic factors such as waterbody size (12%) and nutrient enrichment (8%). This supports the hypothesis of higher effects of biotic factors such as the presence of macrophytes and fish (Fig. 9). Lakes with riparian vegetation and fish supported higher zooplankton diversity than artificial and managed small ponds without fish and vegetation. Cladoceran assemblages (mostly Chydoridae, Daphnidae, Bosminidae, and Sididae species) were good indicators of the waterbody typology based on hydroperiod (temporary vs permanent), size (surface, depth), trophy (nutrient, algal biomass), fish and invertebrate predators (presence/absence) (Pinel-Alloul and Mimouni 2013). In temporary ponds devoid of algal resources and predators, management practices such as water emptying at fall and refilling at spring created special niches for rare neuston-feeder species such as Simocephalus spp. and Scapholeberis. Within permanent lakes, zooplankton species richness was noticeably higher in the littoral zone than in the pelagic zone, as observed in European studies on urban ponds (Peretyatko et al. 2009; Kuczyńska-Kippen 2009).
Fig. 9.
The new knowledge developed in these studies can help managing urban ponds and lakes in a way that ensures the maintenance of biodiversity at regional and local scales. For instance, practices favoring a large diversity of permanent and temporary habitats with vegetated littoral zones should be incorporated in conservation plans of large cities, based on zooplankton (Mimouni et al. 2018) or macroinvertebrate indicators (Liao et al. 2020).
Zooplankton as an indicator of environmental changes and anthropogenic stressors in Canadian freshwaters
Climate warming
Climate warming is an important issue in Canada where scenarios suggest greater impacts in northern territories. In Lake Erie, the stronger winds cooling the epilimnion and warming up the hypolimnion cause a shortened stratification and a deeper thermocline (Liu et al. 2014). Recently, whole-lake manipulations using BACI design served to evaluate zooplankton responses to active mixing and thermocline deepening as expected with climate warming (Sastri et al. 2014; Gauthier et al. 2014). Total crustacean zooplankton biomass was enhanced under simulated climate warming. Food web transfer efficiency was reduced under scenarios of warmer climate, promoting stronger top-down cascading effects. Climate warming by only 2 °C could also reduce beta-diversity by increasing synchrony in species assemblages and dynamics in pond zooplankton metacommunities (Thompson et al. 2015). In the future, lakes should be used as sentinels for long-term monitoring of ecological changes with climate warming as recently implemented in the NSERC Canadian Pulse Network project (Huot et al. 2019). Climate change will also likely have an impact on water level fluctuations, invasion by aquatic plants, and cyanobacteria bloom dynamics in a variety of aquatic ecosystems.
The environmental control of zooplankton biodiversity, community structure and function in Canada is complex and variable across scales and systems. The Canadian perspective we have presented indicates that zooplankters are sensitive indicators of the effects of environmental changes and anthropogenic stressors. Several attributes such as diversity, community structure, and functional groups respond as well to environmental changes (abiotic and biotic) as to anthropogenic disturbances in watersheds. This review supports the Multiple Forces hypothesis (Pinel-Alloul 1995) where forcing by abiotic factors (climate, nutrients, morphometry and chemistry) have a primordial role at larger spatial scales, namely: 1) the continental scale, over Canadian ecoregions; 2) at regional scales, in the Boreal ecozones. In contrast, forcing by biotic factors (algal resources and predators) is more influential at local scales, in resort and urban regions (Fig. 4). Furthermore, zooplankton communities demonstrated a wide range of responses to anthropogenic disturbances across scales and systems due to interactions with watershed biogeochemistry and climate change.
Perspectives for future research on freshwater zooplankton in Canada
Zooplankton is a valuable model for assessing biodiversity patterns at multiple scales and across ecosystems. Future research will likely confirm that zooplankton continues to be a key indicator of the impacts of multiple and more complex stressors such as climate warming and land use, perhaps at a variety of scales from individual lakes to continents. However, ecological monitoring of lakes requires an expertise in taxonomy, which is becoming a rare skill in laboratories more oriented toward molecular biology and genetics. Taxonomic expertise based on species morphology should be maintained and developed in complement to biomolecular tools.
This review clearly indicates that large databases on zooplankton community structure at a continental scale are crucial for testing macroecological patterns. More efforts should be invested in compiling and modernizing existing but disparate databases that help us understand spatial patterns in zooplankton diversity, community structure and function among ecosystems. Once assembled, these integrated databases could become appropriate resources for studies at scales not considered previously. At present, modern techniques can help to assemble and share such databases for future researchers. For example, research groups such as the GRIL (Interuniversity research group in limnology) is now creating an extensive and modern lake database that includes abiotic and biotic components, to address macroecological and microecological hypotheses and build environmental models that test complex interactions between environments and plankton communities. Past studies on the continental-scale distribution of crustacean zooplankton species in Canadian lakes (Pinel-Alloul et al. 2013) can serve as a baseline for understanding future departures from current conditions, based on probable scenarios of climate warming.
Monitoring of zooplankton based on landscape ecology and regional typology of lakes is also crucial for evaluating the cumulative effects of anthropogenic disturbances, environmental in interaction with climatic changes. Whole-lake experiments conducted at the watershed scale were a unique opportunity to evaluate the effects of watershed disturbances by wildfires and clear-cut logging (Carignan and Steedman 2000; Prepas et al. 2003). All these surveys indicated that interactions between climatic factors and perturbations are an important source of zooplankton variation and should be incorporated in future study designs.
Recently, new concepts and paradigms based on macroecology and novel methodological frameworks have offered new perspectives for studying the ecological and evolutionary forces that influence patterns in the abundance, distribution, traits and diversity of species across scales and systems. For example, macroecological research (Hortal et al. 2014) provided valuable insights to study environmental and spatial processes influencing spatial patterns of different freshwater communities from bacteria to fish (Beisner et al. 2006), and especially of crustacean zooplankton across lacustrine landscapes (Havens et al. 2015; Pinel-Alloul et al. 2013; Pinto-Coelho et al. 2005). Elsewhere, a heuristic framework integrating species composition and functional traits has been introduced to study patterns of functional biodiversity and environmental linkages of freshwater zooplankton across ecosystems (Barnett et al. 2007; Litchman et al. 2013). New sampling technologies such as continuous plankton recording, optical plankton counting, video-recording and fluorometry were also developed to describe spatial patterns in zooplankton size structure and abundance within lakes in response to eutrophication (Sprules and Munawar 1986), watershed deforestation (Patoine et al. 2002b), as well as local changes in algal resources and fish predation (Angeli et al. 1995; Masson et al. 2001; Pinel-Alloul et al. 2008). The future challenge will be to combine all these concepts and approaches in a holistic perspective to examine the response of freshwater zooplankton to multiple environmental changes and anthropogenic stressors in Canada.
Most of the studies presented here are the result of a long-term collaboration with colleagues and students in the “Groupe de Recherche Interuniversitaire en Limnologie” (GRIL) and in different institutes and universities across Canada and the World. I acknowledge Kasimier Patalas from the Freshwater Institute (Environment Canada) who provided the unique database on freshwater crustaceans, in more than 2000 lakes sampled between 1960 and 1990, including my own data in Québec for the global scale survey. This project is a perfect example of how a long-term collaboration with governmental scientists and GRIL members gave me the opportunity to test ecological theory on microorganisms with a team of M.Sc. and Ph.D. students, and researchers in limnology and zooplankton ecology, geography and biostatistics. Without this collaborative effort, my research program could not have been accomplished with success.
Acknowledgements
This perspective is based on a plenary talk for the Society of Canadian Limnologists and Canadian Conference for Fisheries Research presented in London (Ontario) in January 2019 by Bernadette Pinel-Alloul (BPA), the director (1989–1999) of the Interuniversity research group in limnology (GRIL) at the Université de Montréal. BPA research program has been funded by the NSERC Discovery Grant (RGPIN/04875–2015) during all her carreer. BPA provided the data on most of the research projects conducted in her laboratory since the 1970s and lead the writing of the paper. Alain Patoine (AP) and Jérôme Marty (JM) collaborated in the writing and final editing of the paper. AP leads the writing of the section on the effects of watershed deforestation and JM on reservoir impoundments. The final edition benefited from the inputs of research colleagues at the University of Montréal, Christiane Hudon and Antonia Cattaneo. Mentors of BPE in freshwater ecology are also acknowledged: Etienne Magnin at the University of Montréal, and in zooplankton taxonomy, Bernard Dussart from France. BPA thanks colleagues, postdoctoral fellows, assistants and graduate students who have shared her research program and her fascination with zooplankton. None of her research contributions would have been completed without the ideas of wonderful scientists and colleagues, Ellie Prepas, Victor Alekseev, Alessandra Giani, Beatrix Beisner, Ricardo Pinto Coelho, Nadine Angeli, and the hard work of her research assistant, Ginette Méthot, and her numerous Ph.D. and M.Sc. students.
Footnote
1
Supplementary data are available with the article at https://doi.org/10.1139/cjfas-2020-0474.
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Canadian Journal of Fisheries and Aquatic Sciences
Volume 78 • Number 10 • October 2021
Pages: 1543 - 1562
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Received: 18 December 2020
Accepted: 15 February 2021
Accepted manuscript online: 1 April 2021
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Bernadette Pinel-Alloul, Alain Patoine, and Jérôme Marty. 2021. Multi-scale and multi-system perspectives of zooplankton structure and function in Canadian freshwaters. Canadian Journal of Fisheries and Aquatic Sciences.
78(10): 1543-1562. https://doi.org/10.1139/cjfas-2020-0474
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