Reconstructing fish populations using Chaoborus (Diptera: Chaoboridae) remains – a review

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Reconstructing fish populations using Chaoborus (Diptera: Chaoboridae) remains – a review Jon N. Sweetman, John P. Smol Paleoecological Environmental Assessment and Research Laboratory (PEARL), Department of Biology, Queen’s University, Kingston, Ont., Canada K7L 3N6

Abstract Fish are an important component of many lakes, and a valuable resource in many countries, yet knowledge of how fish populations have fluctuated in the past is very limited. One potential source of information on fisheries dynamics is paleolimnology. This paper reviews the use of the sedimentary remains of the dipteran insect Chaoborus (commonly referred to as the phantom midge) in reconstructing past presence or absence of fish populations. We provide a brief overview of the ecology of Chaoborus larvae, and review the factors believed to be important in determining their distribution and abundance. In particular, we outline the important role fish have in structuring chaoborid assemblages. We highlight several recent studies utilizing Chaoborus remains in reconstructing past fish dynamics, including their use in determining the effects of acidification and piscicide additions on fish populations, and to tracing fish introductions into previously fishless lakes. We conclude by discussing the potential applications of other aquatic invertebrates, such as the Cladocera and Chironomidae, to infer changes in fish populations, and suggest that by integrating the information provided by these different proxies, we may further improve our ability to infer changes in past fish populations. r 2006 Elsevier Ltd. All rights reserved.

1. Introduction Fish are keystone species in many aquatic food webs, where they may regulate the abundance and diversity of prey organisms through top-down effects (e.g., Northcote, 1988; Carpenter and Kitchell, 1993; Vanni et al., 1997). Freshwater fish are also a valuable resource for both recreational and commercial fisheries. Understanding how stocks have fluctuated in the past, and what may have been the causative factors for any changes in past abundances are important components of effective fish management (e.g., Finney et al., 2000, 2002; Gregory-Eaves et al., 2003; Sweetman and Finney, 2003; Holtham et al., 2004). Unfortunately, historical records of fish populations (and especially freshwater stocks) are generally non-existent, and fish fossils, such as scales, are typically rare in most sediment profiles (Patterson and Smith, 2001; Davidson et al., 2003). However, since fish may significantly influence the abundance and diversity of their prey, the remains of Corresponding author. Tel.: +1 613 533 6193; fax: +1 613 533 6617.

E-mail address: [email protected] (J.N. Sweetman). 0277-3791/$ - see front matter r 2006 Elsevier Ltd. All rights reserved. doi:10.1016/j.quascirev.2006.01.007

prey taxa preserved in lake sediments can potentially be used to infer past changes in fish dynamics. Potential paleoindicators of fish populations are the larvae of the phantom midge, Chaoborus (Fig. 1). Chaoborus larvae are often the top invertebrate predators in the pelagic region of many lakes (McQueen et al., 1999; Riessen, 1999). However, their abundances are influenced, to a large extent, by fish predation (Pope et al., 1973; von Ende, 1979; Yan et al., 1985; Elser et al., 1987; McQueen et al., 1999; Wissel et al., 2003). In lakes without fish, larger, non-migratory chaoborid species (e.g., Chaoborus americanus Johannsen, C. crystallinus De Geer, C. obscuripes Wulp) dominate (Pope et al., 1973; Borkent, 1981; Uutala, 1990; Berendonk and Bonsall, 2002; Wissel et al., 2003). In lakes with planktivorous fish, these nonmigratory species are preyed upon, often to the point of extirpation (e.g., Pope et al., 1973; Northcote et al., 1978; von Ende, 1979; Uutala, 1990). Other Chaoborus taxa (e.g., C. flavicans Meigen, C. punctipennis Say, C. trivitattus Loew) are capable of vertically migrating to the hypolimnion or into the sediments during the day, where they may avoid predation by visually feeding planktivorous fish

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Fig. 1. Lateral view of fourth larval instar of Chaoborus flavicans showing location of head capsule and the hydrostatic air-sacs used in regulating buoyancy in modern Chaoborus larvae. Modified from Johannsen (1934).

Fig. 2. Head capsule of fourth instar Chaoborus larva showing location of mandible as well as other mouthparts occasionally preserved in lake sediments. Modified from Borkent (1979).

(Dawidowicz et al., 1990). These taxa are capable of coexisting with fish. Thus, Chaoborus taxa can be used, in an indirect and relatively coarse fashion, to track largescale changes in fish stocks. Chaoborus are well suited for paleolimnological studies for a variety of reasons. Their chitinized mandibles (Figs. 2 and 3) are well preserved, and are commonly found in lake sediments (Frey, 1964; Stahl, 1969; Uutala, 1990). Chaoborus mandibles can be analyzed using the same methods used for chironomid remains, for which preparation techniques have been well established (see Walker, 2001). Chaoborid mandibles, in fact, are often included in chironomid-based studies (e.g., Walker et al., 2003; Heiri and Lotter, 2003; Heiri, 2004). Chaoborid mandibles are easily identified to the subgenus or species taxonomic level (Uutala, 1990; Fig. 3) and, therefore, shifts in Chaoborus taxa, and hence past fish status, can be detected from the sediment record. Despite their potential, Chaoborus remains have been relatively under-utilized in paleolimnological studies (Smol, 2002). The purpose of this paper is to provide a review of the application of Chaoborus remains to infer changes in fish populations. We conclude with a discussion of possible future applications of the Chaoboridae in paleoecology, and the potential use of other related invertebrate taxa, such as the Cladocera and Chironomidae, in evaluating changes in fish status. 2. Overview of Chaoborus ecology 2.1. Life history

Fig. 3. Examples of Chaoborus mandibles recovered from lake sediments: (A) Chaoborus (Sayomyia), (B) C. americanus, (C) C. flavicans, and (D) C. trivittatus. Scale bar equals 100 mm. Modified from Uutala (1990).

The Chaoboridae are holometabolous and have four larval instars. The larval stages are followed by a brief pupal stage. Upon ecdysis, a non-aquatic adult chaoborid emerges (Borkent, 1979; Hershey and Lamberti, 2001; Ouimet, 2001). The aerial adult life stage is generally short lived (usually less than 10 days), lasting only long enough for reproduction to occur and to lay eggs (Berendonk and Bonsall, 2002). Most of a chaoborid’s life is spent in the aquatic larval phases, with the fourth instar lasting the longest (Riessen, 1999). In temperate regions, most Chaoborus species are univoltine, with the larval period usually lasting 1–2 years (Wood, 1956; Fedorenko, 1975; Ouimet, 2001). Times for development of the larval phases are highly dependent on factors, such as temperature and food availability (Ouimet, 2001). The fourth instar larvae

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typically overwinter in permanent water bodies, and pupate the following spring or summer. The only known exceptions are C. cooki Sæther and C. nyblaei Zetterstedt, which have diapausing eggs and are adapted to living in temporary ponds (Borkent, 1981). 2.2. Foraging behavior Chaoborus larvae are tactile, ambush predators (Swift and Fedorenko, 1975; Riessen, 1999). Their body is almost completely transparent, with the exception of two sets of hydrostatic air-sacs that regulate buoyancy (Fig. 1). The larvae remain almost motionless in the water column, relying on their mechanoreceptors to detect hydrodynamic disturbances made by nearby prey, which they capture using their prehensile antennae and mandibles (Swift and Fedorenko, 1975; Fig. 2). The first two instars feed primarily on smaller invertebrates, such as rotifers and copepod nauplii, whereas the third and fourth instars feed on larger zooplankton prey, such as cladocerans and copepods (Moore et al., 1994; Riessen, 1999).

2015

Table 1 Types of vertical migrations exhibited by larvae of Holarctic Chaoborus species (after Borkent, 1981) Species

Migration type

C. C. C. C. C. C. C. C. C. C.

Reduced Reduced Reduced Reduced Reduced Full Full Full Full Full

americanus (Johannsen) obscuripes (Wulp) crystallinus (De Geer) cooki (Sæther) pallidus (Fabricius) trivittatus (Loew) flavicans (Meigen) albatus (Johnson) punctipennis (Say) astictopus (Dyar and Shannon)

2.3. Factors regulating Chaoborus populations As mentioned previously, the primary factor believed to influence the species structure and abundance of larval Chaoborus species is the presence or absence of planktivorous fish (von Ende, 1979; Berendonk et al., 2003; Wissel et al., 2003). Because these invertebrates are relatively large and often motionless in the water column, they are extremely susceptible to visually feeding planktivorous fish. In order to minimize fish predation, Chaoborus are relatively transparent and some taxa undergo diurnal vertical migrations when fish densities are high (McQueen et al., 1999). In these species, the larvae are capable of migrating in and out of the hypolimnion and/or bottom substrates, and thus avoiding predation by visually feeding planktivorous fish during the day, but migrating upward at night to feed in the surface waters (Dawidowicz et al., 1990; McQueen et al., 1999; Voss and Mumm, 1999). As a result, these migratory species can coexist with fish populations (Pope et al., 1973; von Ende, 1979; Wissel et al., 2003; Table 1). Other chaoborid species lack this ability to use these vertical refugia, and exhibit only limited migrations that restrict them to the upper surface waters (Borkent, 1981; Berendonk et al., 2003; Table 1). Non-migratory taxa are rarely found in lakes with fish populations (Borkent, 1981). In fishless lakes, Chaoborus species can be extremely abundant. For example, Pope et al. (1973) found that, in a series of fishless lakes in Quebec, C. americanus were found at densities as high as 1157 larvae m 2. Xie et al. (1998) reported larval densities of C. flavicans of over 23,000 m–2 in a fishless pond in Japan. Recently, Wissel et al. (2003) examined the distribution of Chaoborus species in 56 lakes in central Ontario, Canada, in relation to lake morphometry, water chemistry and fish predation, in order to determine which factors

Fig. 4. Living fourth instar Chaoborus, showing differences in size and pigmentation of larvae: (A) C. punctipennis, (B) C. flavicans, and (C) C. americanus. Photo: Joelle Young, York University.

were important in determining the abundance and composition of species. Similar to previous studies, they found a clear distinction between the occurrence of the nonmigratory C. americanus (Fig. 4C), which was restricted to fishless lakes, and migratory Chaoborus species found in lakes containing fish (Fig. 5). In the fishless lakes, C. americanus appeared to be more abundant at higher nutrient concentrations. Interestingly, the abundance of C. punctipennis, a species that occurs in lakes with fish, did not appear to be primarily regulated by fish presence, but by the occurrence of other larger chaoborid species (Wissel et al., 2003; Fig. 5). C. punctipennis is a relatively small, transparent taxon (Fig. 4A), which typically maintains its position fairly high in the water column, even during the day, despite possible fish predation (Tsalkitzis et al., 1994; Wissel et al., 2003). As larger Chaoborus species can feed on C. punctipennis, there was a negative correlation between the abundance of larger taxa and C. punctipennis. Similarly, Fischer and Frost (1997) found that neither food limitation nor fish predation appeared to be important factors limiting C. punctipennis abundance, but invertebrate predation had a potentially important role in constraining this taxon. Wissel et al. (2003) found that C. punctipennis tended to occur in shallower lakes with larger surface areas (Fig. 5). This may be because fish densities were lower in

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less common. Fortunately, the mandibles alone are usually sufficient for identification of remains to the subgenus or species taxonomic level (Uutala, 1990). The main characteristics used in identification of the mandibles are the size, shape, and position of the subordinate tooth, located between the medial and posterior teeth (Fig. 5). Uutala (1990) provided a key to eastern North American species, and Rumes et al. (2005) provide a description and illustrations of the mandibles of East African species. No other detailed taxonomic descriptions of Chaoborus remains have been published for other regions. 4. Paleolimnological applications

Fig. 5. Canonical correspondence analysis (CCA) of Chaoborus distribution in relation to environmental variables for 54 central Ontario lakes (modified from Wissel et al., 2003). Open small circles represent the individual lakes. Black dots indicate the centroids for each chaoborid group. Lengths of arrows represent the relative importance of environmental variables.

these lakes, or because there were more opportunities for horizontal refugia (Burks et al., 2002). The two larger species of Chaoborus in Wissel et al.’s (2003) study lakes that were able to coexist with fish (i.e., C. trivittatus and C. flavicans, Fig. 4B) were more abundant in lakes with higher dissolved organic carbon (DOC) concentrations. As DOC may reduce visibility, high concentrations may also decrease predation pressure from fish. However, in a subsequent study, Persaud and Yan (2003) suggested, based on in situ lake experiments, that UV radiation may increase Chaoborus mortality in clear lakes; DOC attenuates UVR in lakes. 2.4. Distribution Chaoborus species are widely distributed and well represented in both temperate and tropical climates (e.g., Borkent, 1981; Colless, 1986; Halat and Lehman, 1996; Sæther, 1997; Berendonk, 2002; Rumes et al., 2005). They are found on all the continents, with the exception of Antarctica (Borkent, 1993). Borkent (1981) provided a detailed description of the distribution of chaoborid species in the Holarctic region. 3. Preservation of Chaoborus remains in sediments In sediments, typically only the chitinized mandibles of the larvae are well preserved and recovered in sufficient quantities for paleolimnological inferences (Fig. 5). Frey (1964) also reported the occurrence of pre-mandibular fans, antennal segments, pre-labral scales, and respiratory horns of pupae in sediments, but these structures are much

In some of the earliest paleolimnological studies, researchers often recognized the subfossil remains of Chaoborus, along with chironomid head capsules, in pollen slide preparations (Frey, 1964). For example, Deevey (1942), in his classic study of Linsley Pond, Connecticut, USA, first reported finding the mandibles and premandibular fans of Chaoborus, which he identified as C. punctipennis, based on the modern taxa in the lake. Most early studies interpreted the presence of Chaoborus remains as associated with severe anoxic conditions (Frey, 1964; Uutala, 1990). Because Chaoborus was capable of migrating out of the oxygen-depleted hypolimnion, they were thought to be capable of withstanding anoxic conditions that were even too severe for the most tolerant chironomids (e.g., Chironomus; Frey, 1964; Stahl, 1966). This view is primarily because Thienemann’s (1925) original descriptions of lake types reported the absence of Chaoborus from oligotrophic lakes, but usually recorded in eutrophic lakes, and almost always present in dystrophic lakes. Chaoborus has been shown to withstand extremely low oxygen concentrations (Jager and Walz, 2002). In lakes with hypolimnetic oxygen depletion, diel vertical migration may allow Chaoborus to avoid predators (Rine and Kesler, 2001). However, oxygen concentrations do not appear to affect the degree of migration by Chaoborus (Goldspink and Scott, 1971). 4.1. Estimating the effects of acidification on fish populations In the last half of the twentieth century, many lakes in both Europe and North America became acidified due to increased atmospheric emissions of sulfur and nitric oxides (Schindler, 1988). In many of these lakes, it was thought that fish populations severely declined or were extirpated due to lake acidification. However, because historical records of fish abundances were usually absent, it was difficult to explicitly link fish losses with acidification. Unlike fish populations, Chaoborus taxa, however, can withstand strongly acidic conditions (Walker et al., 1985). Nilssen et al. (1984) observed shifts in Chaoborus species in a series of acidified lakes from Scandinavia following the

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2017

Fig. 6. Chaoborus mandible accumulation rates from Windfall Pond, Deep Lake, and Upper Wallface Pond. Modified from Uutala (1990).

loss of fish. Following acidification, migratory chaoborid taxa were replaced by C. obscuripes, a non-migratory species (Nilssen et al., 1984). In eastern North America, subfossil chaoborid mandibles were used successfully to infer changes in fish populations with the onset of acidification (Johnson and McNeil, 1988; Johnson et al., 1990; Uutala, 1990; Kingston et al., 1992; Uutala et al., 1994; Uutala and Smol, 1996). Within northeastern North America, five species of Chaoborus are typically present (Uutala, 1990; Uutala and Smol, 1996). As discussed previously, C. americanus is a relatively large species (Fig. 4C), which does not undertake vertical migrations, and is easily preyed on by fish. As such, it is an excellent indicator of fishless conditions in lakes (Pope et al., 1973; von Ende, 1979; Wissel et al., 2003). C. trivitattus is capable of only weak vertical migrations and is a relatively large taxon. As a result, it is only common in lakes with relatively few fish (Uutala and Smol, 1996). Larvae of the other three species (C. albatus Johnson, C. flavicans, and C. punctipennis) may coexist with planktivorous fish, by undergoing vertical migrations, and by avoiding surface waters and visually feeding fish predators during the day (Table 1). Using Chaoborus remains in sediments, Uutala (1990) inferred past fish status in a series of lakes in Adirondack Park, New York, USA (Fig. 6). Based on diatom-inferred pH reconstructions, Windfall Pond did not appear to have been acidified (Charles et al., 1990). In this lake, Chaoborus (Sayomyia) (C. albatus/punctipennis) was present throughout the core at relatively low abundances, suggesting that the lake had viable fish populations over the last few hundred years (Fig. 6). In Deep Lake, the dominant Chaoborus species was C. trivittatus prior to the 1930s. However, Deep Lake became acidified by about 1930, based on chrysophyte and diatom-inferred pH data (Smol et al., 1984; Charles et al., 1990; Smol and Dixit, 1990). C. americanus appeared in the sediment record following the acidification period, and replaced C. trivittatus as the

dominant species, suggesting that fish populations were eliminated as the lake acidified (Fig. 6). In Upper Wallface Pond, diatom inferences suggested that the lake was naturally acidic (Charles et al., 1990). Based on the continued presence of C. americanus mandibles throughout the sediment core, even prior to the period of human impacts, Uutala (1990) determined that the lake was also naturally fishless (Fig. 6). Despite some lakes being naturally acidic and lacking fish populations, several naturally acidic lakes have been limed and stocked in unsuccessful attempts at ‘remediation’ (Smol, 2002). Clearly, these are misguided mitigation efforts, and paleoecological studies could have an important role in assisting restoration programs. 4.2. Tracking fish introductions in previously fishless lakes In many lakes and ponds, non-native fish species have been introduced through stocking programs or by intentional or unintentional transplanting by humans (Donald et al., 2001; Pister, 2001). Most fish introductions have been implemented somewhat haphazardly, with little consideration of the potential effects on existing fish populations. The goal of most fish additions was to increase fish stocks for recreational use (Knapp et al., 2001; Pister, 2001). As in the case of acidified lakes, there are generally no historical records of native fish populations in these lakes prior to introductions, and little or no data exist on how fish introductions affected lake ecology. Lamontagne and Schindler (1994) attempted to examine the stocking history of three lakes in the Canadian Rocky Mountains through a paleolimnological study using chaoborid remains. They examined Chaoborus mandibles in three lakes located in Jasper National Park, Alberta, Canada: Cabin, Caledonia, and Celestine lakes. All three lakes were stocked with salmonid fish in the 1920s and 1930s, but it was unclear whether native fish populations existed in the lakes prior to stocking. In order to establish

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the relationship between the occurrence of Chaoborus species to fish abundance in the Canadian Rocky Mountain lakes, they first surveyed 43 lakes in Jasper and Banff National parks, and found that, similar to the acidification studies in eastern Canada, C. americanus was the only species inhabiting fishless lakes, and only occurred in three lakes with low fish density (Lamontagne et al., 1994). Other lakes that supported fish either had only C. flavicans present, or chaoborids were absent (Lamontagne and Schindler, 1994; Lamontagne et al., 1994). Using the above information, paleolimnological analyses of 210Pb-dated sediment cores revealed that, in both Cabin and Celestine lakes, C. americanus was abundant in the nineteenth century (along with C. trivittatus in Cabin Lake), but were eliminated following fish stocking (Fig. 7). In Caledonia Lake, however, only C. flavicans was present throughout the sediment core (Fig. 7), suggesting that this lake had a viable fish population prior to stocking. Drake and Naiman (2000) also attempted to use paleolimnological techniques to examine the effects of stocking and subsequent removal of fish in naturally fishless lakes in Mt. Rainier National Park, Washington, USA. Chaoborus remains were not recovered in any of their stocked lakes, and were only found in one unstocked lake. However, because multiple proxies were examined, and they had only limited material available (i.e., 0.25 mL of wet sediment) for all invertebrate analyses, these may have been insufficient sediment for an accurate assessment of Chaoborus remains (Uutala, 1990; Walker, 2001).

4.3. Determining the effects of piscicide additions on fish populations In the 1950s and 1960s, many organochlorine-based pesticides were introduced into lakes either unintentionally through groundwater or surface runoff, intentionally as part of mosquito and other control programs, or in some instances as piscicides to remove native fish populations prior to stocking with sport fish (Miskimmin and Schindler, 1994; Smol, 2002). The additions of such chemicals into lakes had, in many instances, dramatic impacts on non-target biota. In Clear Lake, California, USA, for example, large concentrations of dichloro diphenyl dichloroethane (DDD) were added to the lake in the 1950s in an attempt to control the large swarms of the Clear Lake gnat (Chaoborus astictopus Dyar and Shannon), which were viewed as a nuisance because of the large aggregations of adults around the lakeshore (Hunt and Bischoff, 1960). Following treatment, the lake water contained about 0.02 ppm DDD (Hunt and Bischoff, 1960). This resulted initially in a 99% reduction in the densities of Chaoborus larvae in the lake, but surviving midges developed a resistance to the pesticide, and recovered despite additional applications of DDD (Apperson et al., 1978). The subsequent biomagnification of the insecticide into the food web and nesting birds in the area

Fig. 7. Density of Chaoborus mandibles per gram organic matter from Rocky Mountain lakes: (A) Cabin Lake, (B) Celestine Lake, and (C) Caledonia Lake. Modified from Lamontagne and Schindler (1994).

were widely reported in Carson’s (1962) book ‘‘Silent Spring’’. Another organochlorine, toxaphene, was widely applied as an agricultural insecticide but was also used in some lakes as a piscicide as an alternative to rotenone (Smol, 2002). Miskimmin and Schindler (1994) used paleolimnological techniques to examine the long-term effects of toxaphene additions applied in 1961–1962 to two lakes in central Alberta, Canada. Following toxaphene additions, Chatwin Lake, which received 0.0184 ppm toxaphene in 1962, showed large decreases in the accumulation of planktonic cladoceran remains and in the mandibles of the dominant Chaoborus taxon (C. flavicans; Fig. 8A). Subsequently, there was an increase in C. americanus, beginning in the 1970s, indicating the poor survival of the stocked fish (Fig. 8A). In Peanut Lake, which received lower concentrations of toxaphene (0.0075 ppm), shortterm toxic effects were not observed. However, with the elimination of predation pressure from the native fish population, planktonic cladocerans increased (Fig. 8B). As

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a result of the loss of fish and the increase in cladoceran prey, chaoborids increased in abundance (Fig. 8B). Hynynen et al. (2004) included Chaoborus remains in a multi-proxy study of the effects of heavy pulp mill discharges on Lake Lievestuoreenja¨rvi, Finland. They found that populations of C. flavicans peaked in abundance during the early 1960s, at the early stages of pollution to the lake (a period of initial nutrient loading), but the chaoborid population collapsed in the 1970s, and has remained low since that time. 5. Potential applications of other aquatic invertebrates to infer changes in fish populations Several studies have utilized cladoceran zooplankton remains as a tool for evaluating past changes in fish communities (e.g., Hrba´cˇek, 1969; Kerfoot, 1974, 1981; Kitchell and Kitchell, 1980; Leavitt et al., 1989, 1994; Salo et al., 1989; Sanford, 1993; Jeppesen et al., 1996, 2001a, 2002, 2003; Verschuren and Marnell, 1997; Amsinck et al., 2003, 2005; Sweetman and Finney, 2003), or to track climate change in fishless lakes (Manca and Comoli, 2004). Changes in both the size structure and abundance of zooplankton can occur due to shifts in levels of fish abundance (Nilssen, 1978; Kerfoot, 1981; Leavitt et al., 1989; Jeppesen et al., 1996, 2002; Sweetman and Finney, 2003). The application of cladoceran remains in paleolimnological studies has been reviewed recently by Korhola and Rautio (2001) and Jeppesen et al. (2001b). One of the most promising developments has been the publication of a series of cladoceran-based transfer functions that allow quantitative estimates to be made of planktivorous fish densities (Jeppesen et al., 1996, 2003; Amsinck et al., 2005). While cladoceran zooplankton have shown to be a promising tool to infer changes in fish abundance, factors other than fish predation, such as changes in the abundance of invertebrate predators, can also affect zooplankton (Nilssen, 1978; Blumenshine and Hambright, 2003; Sagrario and Balseiro, 2003; Sweetman and Finney, 2003). This, of course, is also true to some extent for Chaoborus taxa. Clearly, the use of multiple proxies (i.e., cladoceran zooplankton and chaoborids, as well as other indicators) will strengthen our ability to infer past changes in fish populations. The Chironomidae, or non-biting midges, are another group of aquatic dipterans that are frequently used in paleoecological research (see recent reviews by Walker, 2001; Porinchu and MacDonald, 2003). Unlike the Chaoboridae, in which typically only the mandibles preserve, the entire chironomid head capsule, which is chitinized, is usually recovered in lake sediments. Chironomids are typically the dominant benthic macroinvertebrates in lakes (Mousavi et al., 2002; Porinchu and MacDonald, 2003). Most avid fly fishing enthusiasts are well aware that chironomid midges can be an important component of the diet of fish. Predation by fish may potentially be an important factor in structuring chirono-

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mid communities (Hershey, 1985; Goyke and Hershey, 1992; Rieradevall et al., 1995; Mousavi et al., 2002). Generally, it is thought that larger, free-swimming larvae, such as the Tanypodinae, are more susceptible to fish predation than tube-dwelling taxa (Oliver, 1971; Hershey, 1987; Mousavi et al., 2002). Despite the potential of fossil chironomids in tracking past changes in fish populations, there has been little research completed thus far. Uutala (1986) examined the chironomid assemblages in some acidified lakes in Adirondack Park, New York, USA. Deep Lake, as discussed previously for Chaoborus mandibles, became acidified by about 1930; this coincided with marked increases in C. americanus mandibles as the lake lost its native fish populations (Uutala, 1990; Fig. 6). Uutala (1986) also observed an increase in the overall accumulation rate of chironomid head capsules after 1955, and recorded slight increases in Procladius, Pentaneurini, and Corynoneura (which are all free living and susceptible to fish predation) in the surface sediments of the Deep Lake core. He suggested the increases in these taxa might be related to the disappearance of native fish in the lake following acidification. Miskimmin and Schindler (1994) also recorded increases in chironomid accumulation rates following additions of toxaphene in Peanut and Chatwin lakes (Fig. 8). They did not, however, identify individual chironomid taxa. Heiri and Lotter (2003) suggested that the absence of the tanypod Procladius in the most recent sediments of a small alpine lake in Switzerland, Sa¨gistalsee, might be due to fish stocking in the last 40 years. Evans (1995) also examined chironomid remains in response to fish migrations in Toolik Lake, Alaska. Porinchu and MacDonald (2003) suggested that reconstructing fluctuations in fish populations could be a ‘‘fruitful area of future research’’ for chironomid paleoecologists. Chironomids may provide additional information that, together with other indicators of changes in fish status, may help improve our ability to understand how stocks have fluctuated in the past. 6. Summary Fish are an important part of many freshwater ecosystems, and understanding how fish populations have fluctuated in the past is of fundamental interest to paleoecologists, fisheries scientists, and the public at large. Unfortunately, records of past fish populations can be difficult to obtain, as reliable records of fish fossils are rarely available. Mandibles of the larvae of the phantom midge Chaoborus, however, are well preserved in sediments, and can be used to infer changes in past fish populations. The occurrence of specific Chaoborus taxa in lakes is determined to a large extent by fish presence or absence, as non-migratory chaoborid taxa are unable to coexist with visually feeding planktivorous fish, whereas chaoborids with the ability to migrate out of the pelagic region can tolerate the presence of fish. To date, the number of studies using sedimentary Chaoborus

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Fig. 8. Accumulation rates of chironomid head capsules, Chaoborus mandibles, and planktonic cladoceran remains from 210Pb-dated sediment cores: (A) Chatwin Lake and (B) Peanut Lake. From Miskimmin and Schindler (1994).

assemblages to infer shifts in fish abundance has been limited, but chaoborid remains have been used successfully to reconstruct changes in fish abundance associated with acidification, fish stocking, and historical applications of piscicides. Multi-proxy investigations incorporating Chaoborus remains along with other invertebrates, such as cladocerans and chironomids, may improve our ability to infer changes in fisheries. Acknowledgments We would like to acknowledge the pioneering work of Allen Uutala, who inspired this research and made a significant contribution to the use of Chaoborus remains in paleoecology. Paleolimnological research in our lab is

funded primarily by the Natural Sciences and Engineering Research Council of Canada.

References Amsinck, S.L., Jeppesen, E., Ryves, D., 2003. Cladoceran stratigraphy in two shallow brackish lakes with special reference to changes in salinity, macrophyte abundance and fish predation. Journal of Paleolimnology 29, 495–507. Amsinck, S.L., Jeppesen, E., Landkildehus, F., 2005. Relationships between environmental variables and zooplankton subfossils in the surface sediments of 36 shallow coastal brackish lakes with special emphasis on the role of fish. Journal of Paleolimnology 33, 39–51. Apperson, C.S., Yows, D., Madison, C., 1978. Resistance to methyl parathion in Chaoborus astictopus from Clear Lake, California. Journal of Economic Entomology 71, 772–773.

ARTICLE IN PRESS J.N. Sweetman, J.P. Smol / Quaternary Science Reviews 25 (2006) 2013–2023 Berendonk, T.U., 2002. Distribution and ecology of phantom midge larvae in southern France and Italy (Diptera: Chaoboridae). Studia Dipterologica 9, 109–112. Berendonk, T.U., Bonsall, M.B., 2002. The phantom midge and a comparison of metapopulation structures. Ecology 83, 116–128. Berendonk, T.U., Barraclough, T.G., Barraclough, J.C., 2003. Phylogenetics of pond and lake lifestyles in Chaoborus midge larvae. Evolution 57, 2173–2178. Blumenshine, S.C., Hambright, H.D., 2003. Top-down control in pelagic systems: a role for invertebrate predation. Hydrobiologia 491, 347–356. Borkent, A., 1979. Systematics and bionomics of the species of the subgenus Schadonophasma Dyar and Shannon (Chaoborus, Chaoboridae, Diptera). Quaestiones Entomologicae 15, 122–255. Borkent, A., 1981. The distribution and habitat preferences of the Chaoboridae (Culicomorpha, Diptera) of the Holarctic region. Canadian Journal of Zoology 59, 122–133. Borkent, A., 1993. A world catalogue of fossil and extant Corethrellidae and Chaoboridae (Diptera), with a listing of references to keys, bionomic information and descriptions of each known life stage. Entomologica Scandinavica 24, 1–24. Burks, R.L., Lodge, D.M., Jeppesen, E., Lauridsen., T.L., 2002. Diel horizontal migration of zooplankton: costs and benefits of inhabiting the littoral. Freshwater Biology 47, 343–365. Carpenter, S.R., Kitchell, J.F. (Eds.), 1993. The Trophic Cascade in Lakes. Cambridge University Press, Cambridge. Carson, R.L., 1962. Silent Spring. Houghton-Mifflin, Boston. Charles, D.F., Binford, M.W., Fry, B.D., Furlong, E., Hites, R.A., Mitchell, M., Norton, S.A., PAtterson, M.J., Smol, J.P., Uutala, A.J., White, J.R., Whitehead, D.R., Wise, R.J., 1990. Paleoecological investigation of recent lake acidification in the Adirondack Mountains, N.Y. Journal of Paleolimnology 3, b195–b241. Colless, D.H., 1986. The Australian Chaoboridae (Diptera). Australian Journal of Zoology, Supplement 124, 1–66. Davidson, T.A., Sayer, C.D., Perrow, M.R., Tomlinson, M.L., 2003. Representation of fish communities by scale sub-fossils in shallow lakes: implications for inferring percid–cyprinid shifts. Journal of Paleolimnology 30, 441–449. Dawidowicz, P., Pijanowska, J., Ciechomski., K., 1990. Vertical migration of Chaoborus larvae is induced by the presence of fish. Limnology and Oceanography 35, 1631–1637. Deevey Jr., E.S., 1942. Studies on Connecticut lake sediments. III. The biostratonomy of Linsley Pond. American Journal of Science 240, 313–338. Donald, D.B., Vinebrooke, R.D., Anderson, R.S., Syrgiannis, J., Graham, M.D., 2001. Recovery of zooplankton assemblages in mountain lakes from the effects of introduced sport fish. Canadian Journal of Fisheries and Aquatic Sciences 58, 1822–1830. Drake, D.C., Naiman, R.J., 2000. An evaluation of restoration efforts in fishless lakes stocked with exotic trout. Conservation Biology 14, 1807–1820. Elser, M.M., Von Ende, C.N., Sorrano, P., Carpenter, S.R., 1987. Chaoborus populations—response to food web manipulation and potential effects on zooplankton communities. Canadian Journal of Zoology 65, 2846–2852. Evans, R., 1995. Paleolimnological analysis of chironomids to detect fish immigration into Toolik Lake, AK, in the Holocene. MS Thesis, University of Cincinnati, Cincinnati, 107pp. Fedorenko, A.Y., 1975. Instar and species-specific diets in two species of Chaoborus. Limnology and Oceanography 20, 238–249. Finney, B.P., Gregory-Eaves, I., Sweetman, J., Dougas, M.S.V., Smol., J.P., 2000. Impacts of climatic change and fishing on Pacific salmon abundance over the past 300 years. Science 290, 795–799. Finney, B.P., Gregory-Eaves, I., Douglas, M.S.V., Smol., J.P., 2002. Fisheries productivity in the northeastern Pacific Ocean over the past 2,200 years. Nature 416, 729–733. Fischer, J.M., Frost, T.M., 1997. Indirect effects of lake acidification on Chaoborus population dynamics: the role of food limitation and

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predation. Canadian Journal of Fisheries and Aquatic Sciences 54, 637–646. Frey, D.G., 1964. Remains of animals in Quaternary lake and bog sediments and their interpretation. Ergebnisse der Limnologie 2, 1–114. Goldspink, C.R., Scott, D.B., 1971. Vertical migration of Chaoborus flavicans in a Scottish loch. Freshwater Biology 1, 411–421. Goyke, A.P., Hershey, A.E., 1992. Effects of fish predation on larval chironomid (Diptera, Chironomidae) communities in an arctic ecosystem. Hydrobiologia 240, 203–211. Gregory-Eaves, I., Smol, J.P., Douglas, M.S.V., Finney, B.P., 2003. Diatoms and sockeye salmon (Oncorhynchus nerka) population dynamics: reconstructions of salmon-derived nutrients over the past 2,200 years in two lakes from Kodiak Island, Alaska. Journal of Paleolimnology 30, 35–53. Halat, K.M., Lehman, J.T., 1996. Temperature-dependent energetics of Chaoborus populations: hypothesis for anomalous distributions in the great lakes of East Africa. Hydrobiologia 330, 31–36. Heiri, O., 2004. Within-lake variability of subfossil chironomid assemblages in shallow Norwegian lakes. Journal of Paleolimnology 32, 67–84. Heiri, O., Lotter, A.F., 2003. 9000 years of chironomid assemblage dynamics in an Alpine lake: long-term trends, sensitivity to disturbance, and resilience of the fauna. Journal of Paleolimnology 30, 273–289. Hershey, A.E., 1985. Effects of predatory sculpin on the chironomid communities in an arctic lake. Ecology 66, 1131–1138. Hershey, A.E., 1987. Tubes and foraging behavior in larval Chironomidae—implications for predator avoidance. Oecologia 73, 236–241. Hershey, A.E., Lamberti, G., 2001. Aquatic insect ecology. In: Thorpe, J.H., Covich, A.P. (Eds.), Ecology and Classification of North American Freshwater Invertebrates. Academic Press, San Diego, pp. 733–775. Holtham, A.J., Gregory-Eaves, I., Pellatt, M.G., Selbie, D.T., Stewart, L., Finney, B.P., Smol, J.P., 2004. The influence of flushing rates, terrestrial input and low salmon escapement densities on paleolimnological reconstructions of sockeye salmon (Oncorhynchus nerka) nutrient dynamics in Alaska and British Columbia. Journal of Paleolimnology 32, 255–271. Hrba´cˇek, J., 1969. On the possibility of estimating predation pressure and nutrition level of populations of Daphnia (Crustacea, Cladocera) from their remains in sediments. Mitteilungen Internationale Vereinigung fu¨r Theoretische und Angewandte Limnologie 17, 269–274. Hunt, E.G., Bischoff, A.I., 1960. Inimical effects on wildlife or periodic DDD applications to Clear Lake. California Fish and Game 46, 91–106. Hynynen, J., Paloma¨ki, A., Merila¨inen, J.J., Witick, A., Ma¨ntykoski, K., 2004. Pollution history and recovery of a boreal lake exposed to a heavy bleached pulping effluent load. Journal of Paleolimnology 32, 351–374. Jager, I.S., Walz, N., 2002. Chaoborus flavicans (Diptera) is an oxyregulator. Archiv fu¨r Hydrobiologie 155, 401–411. Jeppesen, E., Madsen, E.A., Jensen, J.P., Anderson., N.J., 1996. Reconstructing the past density of planktivorous fish and trophic structure from sedimentary zooplankton fossils: a surface sediment calibration data set from shallow lakes. Freshwater Biology 36, 115–127. Jeppesen, E., Jensen, JP., Skovgaard, H., Hvidt., C.B., 2001a. Changes in the abundance of planktivorous fish in Lake Skanderborg during the past two centuries—a palaeoecological approach. Palaeogeography, Palaeoclimatology, Palaeoecology 172, 143–152. Jeppesen, E., Leavitt, P., De Meester, L., Jensen, J.P., 2001b. Functional ecology and palaeolimnology: using cladoceran remains to reconstruct anthropogenic impact. Trends in Ecology & Evolution 16, 191–198. Jeppesen, E., Jensen, J.P., Amsinck, S., Landkildehus, F., Lauridsen, T., Mitchell, S.F., 2002. Reconstructing the historical changes in Daphnia mean size and planktivorous fish abundance in lakes from the size of

ARTICLE IN PRESS 2022

J.N. Sweetman, J.P. Smol / Quaternary Science Reviews 25 (2006) 2013–2023

Daphnia ephippia in the sediment. Journal of Paleolimnology 27, 133–143. Jeppesen, E., Jensen, J.P., Lauridsen, T.L., Amsinck, S.L., Christoffersen, K., Sondergaard, M., Mitchell., S.F., 2003. Sub-fossils of cladocerans in the surface sediment of 135 lakes as proxies for community structure of zooplankton, fish abundance and lake temperature. Hydrobiologia 491, 321–330. Johannsen, O.A., 1934. Aquatic Diptera. Part I. Nemocera, exclusive of Chironomidae and Ceratopogonidae. Memoirs of the Cornell University Agricultural Experimental Station 164, 1–70. Johnson, M.G., McNeil, O.C., 1988. Fossil midge associations in relation to trophic and acidic state of the Turkey Lakes. Canadian Journal of Fisheries and Aquatic Sciences 45 (Suppl. 1), 136–144. Johnson, M.G., Kelso, J.R.M., McNeil, O.C., Morton., W.B., 1990. Fossil midge associations and the historical status of fish in acidified lakes. Journal of Paleolimnology 3, 113–128. Kerfoot, W.C., 1974. Net accumulation rates and the history of cladoceran communities. Ecology 55, 51–61. Kerfoot, W.C., 1981. Long-term replacement cycles in cladoceran communities—a history of predation. Ecology 62, 216–233. Kingston, J.C., Birks, H.J.B., Uutala, A.J., Cumming, B.F., Smol, J.P., 1992. Assessing trends in fishery resources and lake water aluminum from paleolimnological analyses of siliceous algae. Canadian Journal of Fisheries and Aquatic Sciences 49, 116–127. Kitchell, J.A., Kitchell, J.F., 1980. Size-selective predation, light transmission, and oxygen stratification—evidence from the recent sediments of manipulated lakes. Limnology and Oceanography 25, 389–402. Knapp, R.A., Corn, P.S., Schindler, D.E., 2001. The introduction of nonnative fish into wilderness lakes: good intentions, conflicting mandates, and unintended consequences. Ecosystems 4, 275–278. Korhola, A., Rautio, M., 2001. Cladocera and other branchiopod crustaceans. In: Smol, J.P., Birks, H.J.B., Last, W.M. (Eds.), Tracking Environmental Change Using Lake Sediments: Zoological Indicators. Developments in Paleoenvironmental Research, vol. 4. Kluwer Academic Publishers, Dordrecht, pp. 5–42. Lamontagne, S., Schindler, D.W., 1994. Historical status of fish populations in Canadian Rocky Mountain lakes inferred from subfossil Chaoborus (Diptera, Chaoboridae) mandibles. Canadian Journal of Fisheries and Aquatic Sciences 51, 1376–1383. Lamontagne, S., Donald, D.B., Schindler, D.W., 1994. The distribution of four Chaoborus species (Diptera: Chaoboridae) along an elevation gradient in Canadian Rocky Mountain lakes. Canadian Journal of Zoology 72, 1531–1537. Leavitt, P.R., Carpenter, S.R., Kitchell, J.F., 1989. Whole-lake experiments: the annual record of fossil pigments and zooplankton. Limnology and Oceanography 34, 700–717. Leavitt, P.R., Hann, B.J., Smol, J.P., Zeeb, B.A., Christie, C.E., Wolfe, B., Kling, H.J., 1994. Paleolimnological analysis of whole-lake experiments: an overview of results from Experimental Lakes Area Lake227. Canadian Journal of Fisheries and Aquatic Sciences 51, 2322–2332. Manca, M., Comoli, P., 2004. Reconstructing long-term changes in Daphnia’s body size from subfossil remains in sediments of a small lake in the Himalayas. Journal of Paleolimnology 32, 95–107. McQueen, D.J., Ramcharan, C.W., Demers, E., Yan, N.D., Conforti, L.M., Perez-Fuentetaja, A., 1999. Chaoborus behavioural responses to changes in fish density. Archiv fu¨r Hydrobiologie 145, 165–179. Miskimmin, B.M., Schindler, D.W., 1994. Long-term invertebrate community response to toxaphene treatment in 2 lakes: 50-yr records reconstructed from lake sediments. Canadian Journal of Fisheries and Aquatic Sciences 51, 923–932. Moore, M.V., Yan, N.D., Pawson, T., 1994. Omnivory of the larval phantom midge (Chaoborus spp.) and its potential significance for fresh-water planktonic food webs. Canadian Journal of Zoology 72, 2055–2065.

Mousavi, S.K., Sandring, S., Amundsen, P.A., 2002. Diversity of chironomid assemblages in contrasting subarctic lakes—impact of fish predation and lake size. Archiv fu¨r Hydrobiologie 154, 461–484. Nilssen, J.P., 1978. Selective vertebrate and invertebrate predation—some paleolimnological implications. Polish Archives of Hydrobiology 25, 307–320. Nilssen, J.P., Ostdahl, T., Potts, W.T.W., 1984. Species replacements in acidified lakes: physiology, predation or competition? Report of the Institute of Freshwater Research, Drottningholm 61, 148–153. Northcote, T.G., 1988. Fish in the structure and function of fresh-water ecosystems: a top-down view. Canadian Journal of Fisheries and Aquatic Sciences 45, 361–379. Northcote, T.G., Walters, C.J., Hume, J.M.B., 1978. Initial impacts of experimental fish introductions on the macrozooplankton of small oligotrophic lakes. Internationale Vereinigung fu¨r Theoretische und Angewandte Limnologie Verhandlungen 20, 2003–2012. Oliver, D.R., 1971. Life history of the Chironomidae. Annual Review of Entomology 16, 211–230. Ouimet, C., 2001. Implications of Chaoborus pupation and ecdysis in cold water. Freshwater Biology 46, 1169–1177. Patterson, W.P., Smith, G.R., 2001. Fish. In: Smol, J.P., Birks, H.J.B., Last, W.M. (Eds.), Tracking Environmental Change Using Lake Sediments: Zoological Indicators. Developments in Paleoenvironmental Research, vol. 4. Kluwer Academic Publishers, Dordrecht, pp. 173–187. Persaud, A.D., Yan, N.D., 2003. UVR sensitivity of Chaoborus larvae. Ambio 32, 219–224. Pister, E.P., 2001. Wilderness fish stocking: history and perspective. Ecosystems 4, 279–286. Pope, G.F., Carter, J.C.H., Power, G., 1973. Influence of fish on distribution of Chaoborus spp. (Diptera) and density of larvae in Matamek River system, Quebec. Transactions of the American Fisheries Society 102, 707–714. Porinchu, D.F., MacDonald, G.M., 2003. The use and application of freshwater midges (Chironomidae: Insecta: Diptera) in geographical research. Progress in Physical Geography 27, 378–422. Rieradevall, M., Garcia-Berthou, E., Prat, N., 1995. Chironomids in the diet of fishes in Lake Banyoles (Catalonia, Spain). In: Cranston, P.S. (Ed.), Chironomids: from Genes to Ecosystems. CSIRO Australia, East Melbourne, pp. 335–342. Riessen, H.P., 1999. Chaoborus predation and delayed reproduction in Daphnia: a demographic modeling approach. Evolutionary Ecology 13, 339–363. Rine, H.E., Kesler, D.H., 2001. A long-term study of larval Chaoborus punctipennis (Diptera: Insecta) vertical migration and the role of critical oxygen concentration. Journal of Freshwater Ecology 16, 145–150. Rumes, B., Eggermont, H., Verschuren, D., 2005. Representation of aquatic invertebrate communities in subfossil death assemblages sampled along a salinity gradient of western Uganda crater lakes. Hydrobiologia 542, 297–314. Sæther, O.A., 1997. Diptera: Chaoboridae, phantom midges. In: Nilsson, A. (Ed.), Aquatic Insects of NW Europe. A Taxonomic Handbook. Apollo, Stenstrup, pp. 335–342. Sagrario, M.D.G., Balseiro, E., 2003. Indirect enhancement of large zooplankton by consumption of predacious macroinvertebrates by littoral fish. Archiv fu¨r Hydrobiologie 158, 551–574. Salo, J., Walls, M., Rajasilta, M., Sarvala, J., Rasanen, M., Salonen, V.P., 1989. Fish predation and reduction in body size in a cladoceran population—paleoecological evidence. Freshwater Biology 21, 217–221. Sanford, P.R., 1993. Bosmina longirostris antennule morphology as an indicator of intensity of planktivory by fishes. Bulletin of Marine Science 53, 216–227. Schindler, D.W., 1988. Effects of acid-rain on fresh-water ecosystems. Science 239, 149–157. Smol, J.P., 2002. Pollution of Lakes and Rivers: a Paleoenvironmental Perspective. Arnold Publishers, London.

ARTICLE IN PRESS J.N. Sweetman, J.P. Smol / Quaternary Science Reviews 25 (2006) 2013–2023 Smol, J.P., Dixit, S.S., 1990. Patterns of pH change inferred from chrysophyte microfossils in Adirondack and northern New England lakes. Journal of Paleolimnology 4, 31–42. Smol, J.P., Charles, D.F., Whitehead, D.R., 1984. Mallomonadacean microfossils provide evidence of recent lake acidification. Nature 307, 628–630. Stahl, J.B., 1966. Ecology of Chaoborus in Myers Lake, Indiana. Limnology and Oceanography 11, 177–183. Stahl, J.B., 1969. The uses of chironomids and other midges in interpreting lake histories. Mitteilung Internationale Vereinigung fu¨r Theoretische und Angewandte Limnologie 17, 111–125. Sweetman, J.N., Finney, B.P., 2003. Differential responses of zooplankton populations (Bosmina longirostris) to fish predation and nutrientloading in an introduced and a natural sockeye salmon nursery lake on Kodiak Island, Alaska, USA. Journal of Paleolimnology 30, 183–193. Swift, M.C., Fedorenko, A.Y., 1975. Some aspects of prey capture by Chaoborus Larvae. Limnology and Oceanography 20, 418–425. Thienemann, A., 1925. Die binnengewasser Nittelewopas Eine limnologische Einfuhrung. Binnengegewa¨sser 1, 1–225. Tsalkitzis, E., Yan, N.D., McQueen, D.J., Popiel, S.A., Demers, E., 1994. Habitat separation among three temperate Chaoborus species. Archiv fu¨r Hydrobiologie 129, 385–403. Uutala, A.J., 1986. Paleolimnological assessment of the effects of lake acidification on Chironomidae (Diptera) assemblages in the Adirondack region of New York. Ph.D. Thesis State University of New York, Syracuse, NY. Uutala, A.J., 1990. Chaoborus (Diptera: Chaoboridae) mandibles— paleolimnological indicators of the historical status of fish populations in acid-sensitive lakes. Journal of Paleolimnology 4, 139–151. Uutala, A.J., Smol, J.P., 1996. Paleolimnological reconstructions of longterm changes in fisheries status in Sudbury area lakes. Canadian Journal of Fisheries and Aquatic Sciences 53, 174–180. Uutala, A.J., Yan, N.D., Dixit, A.S., Dixit, S.S., Smol, J.P., 1994. Paleolimnological assessment of damage to fish communities in three acidic, Canadian Shield lakes. Fisheries Research 19, 157–177.

2023

Vanni, M.J., Layne, C.D., Arnott, S.E., 1997. ‘‘Top-down’’ trophic interactions in lakes: effects of fish on nutrient dynamics. Ecology 78, 1–20. Verschuren, D., Marnell, L.F., 1997. Fossil zooplankton and the historical status of westslope cutthroat trout in a headwater lake of Glacier National Park, Montana. Transactions of the American Fisheries Society 126, 21–34. von Ende, C.N., 1979. Fish predation, interspecific predation, and the distribution of two Chaoborus species. Ecology 60, 119–128. Voss, S., Mumm, H., 1999. Where to stay by night and day: size-specific and seasonal differences in horizontal and vertical distribution of Chaoborus flavicans larvae. Freshwater Biology 42, 201–213. Walker, I.R., 2001. Midges: Chironomidae and related Diptera. In: Smol, J.P., Birks, H.J.B., Last, W.M. (Eds.), Tracking Environmental Change Using Lake Sediments: Zoological Indicators. Developments in Paleoenvironmental Research, vol. 4. Kluwer Academic Publishers, Dordrecht, pp. 43–66. Walker, I.R., Fernando, C.H., Paterson, C.G., 1985. Associations of Chironomidae (Diptera) of shallow, acid, humic lakes and bog pools in Atlantic Canada, and a comparison with an earlier paleoecological investigation. Hydrobiologia 120, 11–22. Walker, I.R., Levesque, A.J., Pienitz, R., Smol., J.P., 2003. Freshwater midges of the Yukon and adjacent Northwest Territories: a new tool for reconstructing Beringian paleoenvironments? Journal of the North American Benthological Society 22, 323–337. Wissel, B., Yan, N.D., Ramcharan, C.W., 2003. Predation and refugia: implications for Chaoborus abundance and species composition. Freshwater Biology 48, 1421–1431. Wood, K., 1956. Ecology of Chaoborus (Diptera: Culicidae) in an Ontario lake. Ecology 37, 639–643. Xie, P., Iwakuma, T., Fujii, K., 1998. Studies on the biology of Chaoborus flavicans (Meigen) (Diptera: Chaoboridae) in a fish-free eutrophic pond, Japan. Hydrobiologia 368, 83–90. Yan, N.D., Nero, R.W., Keller, W., Lasenby, D.C., 1985. Are Chaoborus larvae more abundant in acidified than in non-acidified lakes in central Canada? Holarctic Ecology 8, 93–99.