Ecosystem Health and Sustainable 2 Agriculture

Ecology and Animal Health

Editors: Leif Norrgren and Jeffrey M. Levengood

CSDCentre for sustainable development Uppsala.  The North American Great Lakes/St. Lawrence River and Estuary

Thiamine Deficiency in Aquatic Food Chains 20 The Cumulative Result of Ecosystem Disruption by Clupeids?

John D. Fitzsimons Great Lakes Laboratory for Fisheries and Aquatic Sciences, Burlington, Canada Martha Wolgamood Michigan Department of Natural Resources, Mattawan, MI, USA Charles P. Madenjian and David B. Bunnell United States Geological Survey, Ann Arbor, MI, USA

Clupeid fish such as herring (Clupea spp), shad (Dorosoma levels to support fish nutrition (Saunders and Henderson, spp), and alewives (Alosa pseudoharengus) have long been 1974; Honeyfield et al., 2005; Fitzsimons et al., 1998, recognised as a source of thiaminase activity in aquatic 2005b; Tillitt et al., 2005). food chains throughout North America and the Baltic Sea Clupeids contain some of the highest thiaminase lev- (Deutsch and Hasler, 1943; Neilands 1947; Gnaedinger els reported in aquatic organisms (Tillitt et al., 2005; and Krzeczkowski, 1966; Ji and Adelman, 1998; Tillitt et Honeyfield et al., 2005, 2007; Wistbacka and Bylund, al., 2005; Honeyfield et al. 2007; Wistbacka and Bylund, 2008). It is only recently, however, that the process by 2008). Thiaminase is an enzyme, possibly of bacterial ori- which clupeids exert aquatic ecosystem disruption and gin (Honeyfield et al., 2002; Tillitt et al., 2005), which is cause thiamine deficiency with this enzyme has become thought to be involved in the destruction of thiamine in the evident. In the laboratory, it is possible to cause thiamine gut of predators that consume prey fish containing thiami- deficiency in captive fish fed a diet consisting exclusively nase. This leads to reduced uptake of thiamine by clupeid of clupeids (Saunders and Henderson, 1974; Honeyfield predators and eventually thiamine deficiency if thiami- et al., 2005). In the wild, this was thought to be unlikely, nase activity is high enough and clupeids comprise a high however. Diets in the wild consisting predominantly of enough proportion of the diet (Honeyfield et al., 2005). prey from a diverse prey community, either lacking or When fish containing high levels of thiaminase are fed having low levels of thiaminase, were believed to reduce to captive foxes or mink, this results in Chastek paralysis the overall influence of individual prey fish species con- (Green et al., 1937; Deutsch and Hasler, 1943). Similarly taining high levels of thiaminase. As a result, having thia- on fish farms, salmonines fed fish containing high levels minase-rich prey in the diet was thought to be tolerable of thiaminase also develop thiamine deficiency (Allan, for a limited period of time (see Saunders and Henderson, 1958; Saunders and Henderson, 1969). It should be noted, 1974). Predators of clupeids including Atlantic cod however, that in spite of their high thiaminase content, (Gadus morhua) from the Gulf of St Lawrence have species like alewives appear to contain adequate thiamine apparently tolerated a diet comprised of Atlantic her-

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ring (Clupea harengus) when that diet also included eu- a major and sustained increase in the amount of natural phausiids, shrimp, crab, mysids, capelin and polychaetes reproduction by lake trout suggests that other factors in (Hanson and Chouinard, 2002). Similarly, Baltic salmon addition to alewife predation may be limiting lake trout (Salmo salar) apparently tolerated a diet of sprat (Sprattus reproduction In Lake Ontario (Fitzsimons et al., 2003; B. sprattus) and Baltic herring (Clupea harengus membrus) Lantry pers. comm.). Thiamine deficiency effects are im- that also included other prey such as three-spine stick- plicated since lake trout egg thiamine concentrations re- leback (Gasterosteus aculeatus), perch (Perca fluviatilis mained unchanged between 1994 and 2004 (Fitzsimons et L.), smelt (Osmerus eperlanus L.), sandeel (Ammodytes al., 2007), but the effects of the deficiency in Lake Ontario sp.), bream (Abramis brama L.) and eelpout (Zoarces vi- will remain of uncertain importance until there is a major viparus L.) for millennia in the Baltic Sea (Hansson et al., change in lake trout diets and its effect on natural repro- 2001; Wistbacka and Bylund, 2008). duction can be assessed. For Lake Huron, Fitzsimons et In contrast to the conditions described above where al. (2009b) reported that relief from the thiamine-reduc- predators appeared to co-exist with clupeids containing ing effects of alewives made a greater contribution than high levels of thiaminase in their diet, such is not the relief from alewife predation to increased natural repro- case for salmonines in the North American Great Lakes, duction by lake trout following the collapse of alewives as is best typified by lake trout (Salvelinus namaycush) in this lake. As a result of their high thiaminase content, (Fitzsimons et al., 2003). As a result of aggressive stock- the potential for alewives to have unique depensatory ef- ing programs, the abundance of adult lake trout in the fects on predators like lake trout in the North American Great Lakes has increased markedly from its former de- Great Lakes may be widespread (Walters and Kitchell, pressed state that was the result of overexploitation and 2001). An understanding of the mechanisms leading up sea lamprey (Petromyzon marinus) parasitism (Hatch et to this depensation has remained incomplete until only al., 1981; Holey et al., 1995; Rutherford, 1997; Hansen, recently as the implications of the dominance of a thia- 1999: Bronte et al., 2007). Despite these efforts, many minase-rich prey fish such as alewives in the diets of top of these lake trout stocks, especially in Lakes Ontario predators have become more fully understood. and Michigan but less so in Lake Huron, show little evi- There are several recent, although indirect, exam- dence of significant natural reproduction (Madenjian and ples from both marine and freshwater environments that DeSorcie, 1999; Madenjian et al., 2004; Fitzsimons et when clupeids become abundant enough in the diet of a al., 2003). All of these stocks are dependent on alewives predator, they can negatively affect recruitment and this (Lantry, 2001; Madenjian et al., 1998, 2006). Predation may be related to their high thiaminase content. For ex- by alewives on larval lake trout has been proposed as a ample the most productive period of Atlantic salmon in major contributor to the lack of natural reproduction by the north-east Atlantic Ocean was associated with the col- lake trout in the Great Lakes, based on work conducted lapse of Norwegian spring-spawning herring (C. haren- in Lake Ontario but the results are ambiguous, being gus), a species that was formerly their major food source confounded by simultaneous changes in lake trout egg and is known to be thiaminase-rich (Wistbacka et al., deposition indices and the potential for thiamine deficien- 2002; Haugland et al., 2006). Similarly, a recent increase cy to affect vulnerability of larval lake trout to alewife in recruitment of lake trout occurred in Lake Huron fol- predation (Krueger et al., 1995, O’Gorman et al. 1998, lowing the collapse of alewife in this lake (Riley et al., Fitzsimons et al. 2009a, unpublished data). A shift in the 2007). Prior to their collapse, alewives had been one of springtime distribution of alewives to further offshore in the most important diet items of lake trout in Lake Huron Lake Ontario (O’Gorman et al., 2000) and away from the (Madenjian et al., 2006). The situation in Lake Champlain majority of lake trout spawning reefs in this lake was as- mirrors that in Lake Huron in that the recent addition to sociated with a significant increase in lake trout natural and subsequent expansion of alewives in Lake Champlain reproduction (Fitzsimons, 1995; Perkins and Krueger, reduced egg thiamine in lake trout (unpublished data) and 1995; unpublished data). Although proof that alewife resulted in high levels of Cayuga Syndrome (Fisher et al. predation was exerting a negative effect, the absence of 1996), a thiamine deficiency mortality syndrome, in the

168 The North American Great Lakes/St. Lawrence River and Estuary

progeny of resident Atlantic salmon (K. Kesley, VDNR, of alewives. Acute mortality resulting from EMS, which Grand Isle, VT, pers. comm.). Prior to alewives occurring ranges from approximately to 20 to 30% (Fitzsimons et in Lake Champlain, there had been no evidence of Cayuga al., 1999), but can be upwards of 70% (Fitzsimons et al., Syndrome in resident Atlantic salmon. Collectively, this 2007), is generally insufficient to totally block reproduc- suggests that high consumption of prey fish containing tion by lake trout. Nevertheless ongoing recruitment fail- high levels of thiaminase, e.g. clupeids, can under certain ure in stocks exhibiting thiamine deficiency (Fitzsimons circumstances impose negative impacts on fish stocks. and Brown, 1998), coupled with a lack of other plausible The conditions under which this occurs and the full range explanations (Fitzsimons et al., 2003), suggests thiamine of biological effects have only recently been elaborated deficiency may be imposing effects in addition to acute and are the subject of this review. mortality that can lead to recruitment failure. This no- tion prompted investigation into the effects of thiamine deficiency on the larval growth, foraging and predator avoidance of lake trout, because these early life history Effects of Thiamine Deficiency by Life attributes have well-established links with early survival. Stage and Relationship to Recruitment This culminated in research reported by Fitzsimons et al. (2009a), who found a direct relationship between larval As a disruptor of ecosystem function, the effect of thia- lake trout growth, foraging rate, and predator avoidance, mine deficiency resulting from a high thiaminase diet and egg thiamine concentration. Of these effects, growth has few parallels in nature in terms of the magnitude of impairment was apparently the most sensitive effect of potential negative effects. Thiamine deficiency appears thiamine deficiency. The threshold egg thiamine concen- fully capable of causing mortality and other effects at tration established by these authors for a 50% decline in multiple life stages and as a result has the potential to growth (5.1 nmol/g) was approximately three-fold higher block reproduction in a variety of top predators, leading than what they had previously reported for 50% EMS (1.6 to population declines and possibly even extinctions (see nmol/g) (Fitzsimons et al., 2007). By relating their growth Ketola et al., 2000). effect threshold to the current distribution of egg thiamine For Great Lakes Basin salmonines, the acute mortality levels in lake trout, these authors estimated that for Lakes effects of thiamine deficiency affecting embryonic stages Erie, Ontario and Michigan, 46, 77, and 97% of lake trout have been the most obvious and hence the most studied ef- families, respectively, would spawn eggs with at least a fects (Fitzsimons, 1995; Fisher et al., 1996; Marcquenski 50% reduction in growth. This was compared with 0, 46 and Brown, 1997; Brown et al., 1998). These effects are and 38% of lake trout families from Lakes Erie, Michigan referred to as Early Mortality Syndrome or EMS in Great and Ontario, respectively, having egg thiamine concentra- Lakes salmonines or Cayuga Syndrome in Finger Lakes tions resulting in 50% or greater EMS. While it might be Atlantic salmon. The involvement of thiamine in their ae- argued that reduced growth in and of itself is not directly tiology has been confirmed in that the syndromes can be lethal, reduced growth may contribute to mortality and ul- both reduced by thiamine prophylaxis (Fitzsimons, 1995; timately recruitment failure. Growth directly affects size Fitzsimons et al., 2001a; Brown et al., 2005a) and induced and size is directly related to swimming speed (Blaxter, by thiamine antagonists (Amcoff et al., 1999; Fitzsimons 1986; Webb and Weihs, 1986). Reduced swimming speed et al., 2001 a, b). Their presence has been linked to re- makes larval fish more susceptible to predation (Blaxter, duced egg thiamine levels, which have been directly relat- 1986; Werner and Gilliam, 1984; Zaret, 1980; Brooking ed to the amount of alewives in maternal diets (Fitzsimons et al., 1998) while reducing foraging efficiency (Blaxer, et al., 1999; Fitzsimons and Brown, 1998; Brown et al., 1986; Webb and Weihs, 1986), both of which can contrib- 2005b, c; Fitzsimons et al., 2007; Fisher et al., 1996; ute to mortality in the wild (Miller et al., 1988; Houde, Honeyfield et al., 2005). 1997). In support of the notion that sublethal effects may Mortality alone seems insufficient to explain the re- be a significant but unrecognised impact of thiamine de- cruitment failure of lake trout associated with consumption ficiency, Fitzsimons et al. (2009b) found that a fry emer-

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gence index (FEI) for larval lake trout in Lake Huron was tality (Everitt, 2006). Gradient and flow on the Salmon directly related to egg thiamine concentration. The oc- River during the time that Everitt (2006) conducted his currence of EMS in their study was relatively low (e.g. studies was much higher than on the Platte River when <15%). They attributed the thiamine effect on FEI to a Fitzsimons et al. (2005a) conducted their studies (Ketola greater susceptibility of thiamine-deficient fry to preda- et al., 2009). Although part of the Chinook salmon mortal- tion by crayfish, which may have been exacerbated by the ity occurring on the Salmon River may have been related altered behaviour of thiamine-deficient fry making them to the effects of angling (Bendock and Alexandersdottir, both more readily detectable (e.g. hyperexcitability) and 1993) or temperature stress (Richter and Kolmes, 2005), attacked (e.g. lethargy, loss of equilibrium). mortality was still higher than expected. Subsequent work Thiamine levels of adult salmonines feeding heavily on with Lake Ontario Chinook salmon (Fitzsimons et al. alewives appear to be negatively affected by such a diet 2011a; Figure 20.1) has revealed extremely low muscle based on comparisons of tissue thiamine concentrations thiamine concentrations in Lake Ontario Chinook salmon between populations having a high proportion of alewives which are at or below levels associated with lethargy in in their diet and populations having a much smaller pro- other salmonines (Brown et al., 2005d; unpublished data). portion of alewives or no alewives at all (Brown et al., Thiamine deficiency, because it causes increased plasma 2005d). Negative effects resulting from such depressed concentrations of lactate (Combs, 1992), would have ex- levels have been reported for adults of several species acerbated the negative effects of angling and temperature of salmonines. Effects include altered behaviour (Brown stress that lead to the build-up of lactic acid in the blood et al., 2005d), impaired migration (Ketola et al., 2005), and that have been associated with mortality (Wood et impaired spawning habitat use (Ketola et al., 2009) and al., 1983). In addition, thiamine plays a central role in the mortality (Fitzsimons et al., 2005a). production of ATP equivalents that support metabolism. Mortality in the wild of adults affected with thiamine As a result, during periods of vigorous activity such as deficiency may be quite high. Fitzsimons et al. (2005a) that caused by angling or high temperature there may be discussed at least two instances of massive die-offs of Lake additional demands on thiamine reserves and if these are Michigan coho salmon (Oncorhynchus kisutch) during already depleted by a thiaminase containing diet mortality 2001 in Platte Bay prior to fish entering the Platte River on may result (Fitzsimons et al., 2005a). their spawning run in 2001. In contrast, females entering Relatively little is known about the effects of thiamine the lower part of the river in the same year as the die-offs deficiency at the juvenile stage, even though they may occurred exhibited few signs of thiamine deficiency (e.g. be feeding on much the same prey as adults, including lethargy) and had muscle thiamine levels averaging 0.97 alewives (Madenjian et al., 1998). Juveniles appear to be nmol/g, which was above the 0.59 nmol/g level associated more sensitive to the effects of thiamine deficiency than with lethargy (Brown et al., 2005d)., The upstream spawn- adults (Morito et al., 1986; Ketola et al. 2008). Recent ing migration of coho salmon on the Platter River affected work in Lake Ontario on the ontogeny of thiamine defi- thiamine levels since the signs of thiamine deficiency (e.g. ciency in lake trout suggests there is a strong potential for lethargy) increased to approximately 20% in fish reaching effects to occur throughout almost the entire period of pis- a hatchery 15 km upstream of where fish first entered the civory including the juvenile period. Alewives are the most Platte River (Fitzsimons et al., 2005a). Thiamine levels in significant prey species in the diet of salmonines in Lake fish exhibiting thiamine deficiency signs at the hatchery Ontario (Lantry, 2001) and both lake trout (Fitzsimons et were less than half those of fish first entering the river. al. 2011b; Figure 20.1) and Chinook salmon (Figure 20.2) Associated with increased signs of thiamine deficiency show evidence of ontogenetic declines in muscle thiamine was co-occurring mortality, which was significantly re- relative to reference populations. Such declines are pre- duced in coho salmon given a thiamine injection upon sumed to represent a diet containing a high proportion of entry into the river. Similarly for Lake Ontario Chinook alewives. This is based on the knowledge that as well as salmon (O. tshawytscha) ascending the Salmon River in being dominant in the diet of salmonines, alewives are the 2004-2005, there was upwards of 60% pre-spawning mor- major prey species in Lake Ontario (Owens et al., 2003).

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Figure 20.1. Relationship between muscle thiamine concentra- tion (pmol/g) and fork length (mm) for lake trout from Lakes Ontario (alewife diet) and Superior (low alewife diet) and Spray Lake (non alewife diet). From Fitzsimons et al., 2011a.

Figure 20.2. Relationship between muscle thiamine concen- tration (pmol/g) and fork length (mm) for Chinook salmon from Lakes Ontario (alewife diet) and Superior (low alewife diet). Source: Fitzsimons et al., 2011b.

Analysis of stomach contents and stable isotopes confirms associated with altered behaviour (Brown et al. 2005d) the fact that alewives are the dominant diet item for both that could increase susceptibility to predation (Mesa, lake trout and Chinook salmon (Fitzsimons et al. 2011a, 1994; Carlson et al., 1998; Conte, 2004; Ketola et al., b). Reference populations used to establish the degree of 2009). As a result, the effects of thiamine deficiency on thiamine deficiency in Lake Ontario lake trout had either juveniles may be extensive. It is noteworthy that follow- lesser amounts of thiaminase-containing prey (e.g. rain- ing a decline in slimy sculpins in Lake Ontario (Owens bow smelt (Osmerus mordax) and alewives; Harvey and et al., 2003), there was a coincident drop in the survival Kitchell, 2000) (e.g. Lake Superior) or no thiaminase- index for three-year-old lake trout their major predator (B. containing prey in their diet (e.g. Spray Lake). A small Lantry, USGS, pers. comm.; Owens and Bergstedt, 1994). proportion of juvenile lake trout in Lake Ontario had mus- Sculpins essentially lack thiaminase (Tillitt et al., 2005), cle thiamine levels similar to those associated with acute and historically comprised the bulk of the diet of juvenile mortality in captive adult lake trout (Brown et al., 2005d), lake trout in Lake Ontario (Elrod and O’Gorman, 1991). whereas a larger proportion had levels at or below those At the time of the sculpin decline, alewives were the next

171 The North American Great Lakes/St. Lawrence River and Estuary

most abundant prey fish in Lake Ontario and thus most feeding habits (filter feeding, particle feeding; Janssen, likely replaced sculpins in lake trout diets. Other poten- 1976) and competition with and predation on other prey tial prey fish were either less abundant or declining (e.g fish, allows clupeids such as alewives to suppress other smelt), or of such low abundance (e.g. emerald shiner prey fish (Madenjian et al., 2008; Bunnell et al., 2006). (Notropis atherinoides), three-spine stickleback) that Such was the case for alewives in the Great Lakes where they were unlikely to make a contribution to lake trout di- they have been strongly implicated in the suppression of ets (Owens et al., 2003). Therefore it seems reasonable to several native species although documentation of effects conclude that when slimy sculpins declined, juvenile lake on cisco (Coregonus artedii) until redently were largely trout switched their diet from one that was thiaminase- circumstantial and thought to be without merit (Crowder, poor (e.g. sculpin) to one that was thiaminase-rich (e.g. 1980, 1986; Madenjian et al., 2008; Bunnell et al., 2006). alewife). As a result, lake trout may have suffered direct Cisco was historically one of the most important prey fish and indirect mortality from thiamine deficiency effects, in all five of the North American Great Lakes (Fitzsimons but more work is required to confirm this. and O’Gorman 2006). As early as the 1800s it was specu- lated that the expansion of alewives in Lake Ontario fol- lowing the loss of Atlantic salmon the top predator (Smith 1892), had resulted in dramatic declines in cisco (Mather, Ascendancy of Clupeids in Aquatic Food 1881), considered to be one of the most abundant spe- Chains and Trophic Cascade Effects cies prior to the invasion of the lake by alewives in 1873 (Rathbun and Wakeham, 1897). However, ������������Madenjian et Having demonstrated that significant negative impacts al. (2008) presented evidence that cisco are only mini- can result from thiamine deficiency in Great Lakes sal- mally affected by alewife because the time window for monines, potentially blocking natural reproduction for alewife to predate on larval cisco is small as a result of lake trout (Fitzsimons et al., 2003; Bronte et al., 2003) limited overlap in habitat. Nevertheless, Dunlop et al. and Atlantic salmon (Ketola et al., 2000), emphasis has (2010) provided evidence for Lake Huron of increased switched to understanding causes and how to manage the abundance of cisco following the collapse of alewives in problem. This includes the particular reasons why clu- this lake. Their observations when combined with those peids such as alewives should reach such high levels of of others finding increased cisco abundance following abundance to nearly dominate prey communities and as a the decline of alewives (Dobiesz et al., 2005; Warner et result dominate predator diets. It is also of interest to know al., 2009) stongly implicate alewives in supressing cisco why clupeids of all fish should have such high thiaminase populations. Although the shift from alewife to cisco in levels and what factors regulate thiaminase activity, and Lake Huron suggests relief from either predation or com- finally what, if anything can be done to mitigate effects. petition, the nature of the negative interaction between Large dominant top predators that are at the top of alewives and ciscoes has not been established. It may food chains are successful in part because of ‘cultiva- involve changes in the abundance of large zooplankters tion’ effects where they crop down forage species that are such as Limnocalanus, since alewife planktivory is high- potential competitors or predators (Walters and Kitchell, ly size-selective and has been implicated in regulation of 2001). Due to their relatively high fecundity and toler- Limnocalanus in Lake Michigan (O’Gorman et al., 1991, ance of a wide range of environmental conditions (Scott Barbiero et al., 2009). Alternatively a negative interaction and Crossman, 1973), and inate capacity to recover after may be the result of reduced predation by alewives on catastropic declines, clupeids have the potential to readily young of the year but not egg and larval stages of cisco, exploit a reduction in predation pressure from such top since the seasonal depth distribution of alewives does not predators, allowing them to achieve rapid population ex- overlap the spawning habitat of cisco (Wells, 1968). pansion and reach high levels of abundance (Smith 1970; As a result of their potential to attain high population O’Gorman and Schneider 1986; Hutchings and Reynolds, abundance while suppressing alternate prey species, clu- 2004). This high abundance when coupled with diverse peids can in turn dominate the diets of predators. This

172 The North American Great Lakes/St. Lawrence River and Estuary

would be more likely to occur when the population con- Lass, 1995), cod recruitment remained low, suggesting trol formerly provided by a predator was interrupted for that other processes were limiting reproductive success a sufficient period of time to allow clupeid populations (Bagge, 1994). Documentation of extensive cod egg pre- to build up to a high level and become dominant. For dation by sprat and herring (Koster and Mollmann, 1997) example, evidence of large alewife populations, usually and the resulting development of cod recruitment models evident as major die-offs (Brown, 1972; O’Gorman and (Koster et al., 2001 a, b) revealed that egg predation had Schneider, 1986), were not documented until the 1960s become a strong, albeit not the only regulator, of cod re- and 1970s even though alewives first entered the Great cruitment in the Baltic Sea. Lakes in the 1800s (Ketola et al., 2000) and by the 1950s The relative influence of clupeid egg predation on cod were found in all of the Great Lakes. In Lake Michigan, as a depensatory factor of cod in the Baltic Sea seemed proliferation of alewives did not occur until approximate- much stronger than possible thiamine deficiency effects. ly one decade after the crash of the lake trout population High consumption of clupeids by cod appeared to be in this lake, which was due to a combination of over- without consequence of thiamine deficiency induced em- fishing and sea lamprey parasitism (Hatch et al., 1981; bryonic effects usually associated with high clupeid con- Holey et al., 1995; Rutherford, 1997). This pattern was sumption. Instead cod egg thiamine status was not affected repeated throughout the Great Lakes (Smith, 1995). High (Amcoff et al., 1999), nor was larval survival responsive clupeid population abundance can be sustained even if to thiamine prophylaxis suggestive that cod were able to predator abundance returns to near normal, as is evident maintain adequate thiamine nutrition (Mellargaard, 1996; for the Great Lakes (Madenjian et al., 2002; Mills et al., Nissling and Vallin, 1996). Thiamine deficiency effects 2003). Despite the restoration of lake trout stocks in Lake were in fact more evident in other apparently more sensi- Michigan by stocking, first begun in the mid-1960s and tive species such as Baltic salmon and sea trout (S. trutta) which continues today (Holey et al., 1995), large popula- that presumably have a greater proportion of clupeids tions of alewives persist in the face of large adult stocks in their diet now than before cod declined, as evidenced of lake trout that have resulted from over four decades by reduced egg thiamine concentrations (Amcoff et al., of stocking, and which consume primarily alewives 1999). The build-up in clupeid bimass, elevated occur- (Madenjian et al., 1998, 2002; Bronte et al., 2007). rence in the diet of salmonines and resulting thiamine de- The pattern of ecosystem change associated with a ficiency is very similar to the situation for salmonine top build-up in clupeid abundance and development of thia- predators in the Great Lakes. mine deficiency that follows declines in the abundance of the top predator, appears to be similar across ecosystems and has been attributed to multi-level trophic cascades (Harman et al., 2002; Casini et al., 2008, 2009). Recent Factors Affecting Thiaminase Activity changes in the Baltic Sea show a similar chronology to in Clupeids and Their Influence on the Great Lakes, of a build-up in clupeid abundance, in Thiamine Deficiency this case sprat and Baltic herring, following the loss of the top predator, in this case Baltic cod. The loss of cod has The particular reasons why clupeids consistently have been related to a period where saltwater intrusions from some of the highest thiaminase activity observed amongst the North Sea did not occur. The ensuing stagnation of the telosts remains unclear (Nielands, 1947; Greig and Baltic Sea resulted in a significant decline in Baltic cod as Gnaedinger, 1971; Tillitt et al., 2005; Honeyfield et al., a result of embryonic mortality caused by low dissolved 2007; Wistbacka and Bylund, 1998). In a review of phy- oxygen (Mackenzie et al., 1996). The decline in cod was logenetic and ecological characteristics associated with followed by a dramatic increase in the abundance of sprat thiaminase activity in Noth American Great Lakes fishes, and Baltic herring (Sparholt, 1994). Despite partial recov- Riley and Evans (2008) found, based on diverse measures ery of dissolved oxygen levels following a major inflow to of thiaminase activity, that taxonomically more ancestral the Baltic Sea from the North Sea in 1993 (Matthaus and species (Anguilliformes, Clupeiformes, Cypriniformes,

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Siluriformes) were more likely to show thiaminase activ- immune system and health of an organism and possible ity than the more derived species (protoacanthopterygians regulation of thiaminolytic bacteria which have been iso- and neoteleosts). In addition, these authors found that spe- lated from alewives (Honeyfield et al., 2002). Fluctuations cies that fed at lower trophic levels and occupied benthic in alewife thiaminase activity resulting from fluctuations habitats appeared more likely to show thiaminase activity. in feeding activity could in turn lead to fluctuations in the Within alewives, where most work has been done to expression of thiamine deficiency in alewife predators. understand thiaminase dynamics, there is evidence that Undernutrition due to insufficient intake of energy and/or thiaminase activity varies among seasons, within and macronutrients due to deficiencies in specific micronutri- among lakes, and is related to the size of alewife (Tillitt et ents can impair the immune system, suppressing immune al., 2005; Fitzsimons et al., 2005b) suggesting that a va- functions that are fundamental to host protection (Marcos riety of factors may be involved in modulation of thiami- et al., 2003). Sheldon and Blazer (1991) reported that bac- nase activity. Whether such factors are related to variation tericidal activity in channel catfish (Ictalurus punctatus) in diet, habitat, or some other factor or factors, is unclear. was positively correlated with dietary highly unsaturated Fitzsimons et al. (2005b) found that thiaminase activity fatty acids (HUFAs). Eicosanoids, which control inflam- of Finger Lakes alewives was inversely correlated to lipid mation and immunity, consist of prostaglandins, prosta- level and that lipid level was correlated with lake chlo- cyclins, thromboxanes and leukotrienes and are primarily rophyll-a, a measure of lake productivity. As such, lake derived from the fatty acids arachidonic and linoleic acids productivity through its influence on lipid content may (M. Arts, Environment Canada, pers. comm.). A relation- influence thiaminase activity. Effects of lake productiv- ship between health and thiaminase activity has been con- ity on alewife lipid content is consistent with the timing firmed for common carp (Cyprinus carpio), which exhibit- of a decline in energy density for Lake Ontario alewives ed elevated muscle thiaminase activity after injection with between 1978 and 1990 (Rand et al., 1994). For alewives, live Aeromonas salmonicida (Wistbacka et al., 2009). energy density is directly related to lipid content (Rottiers Tillitt et al. (2005) felt that there was strong evidence and Tucker, 1982). Rand et al. (1994) attributed the de- for a bacterial origin for the thiaminase found in fishes. cline in energy density of alewives, especially during the They based this on the thiaminase gene having been latter part of the period 1978 to 1990, to a decline in lake cloned in Paenabacillus thiamimolyticus (Abe et al., productivity, most likely due in part to a decline in zoo- 1987), these bacteria having been isolated and cultured plankton density (O’Gorman et al., 1997). from the alewife digestive tract (Honeyfield et al., 2002), Fish lipid content is known to be affected by the li- and the fact that the distribution of thiaminase in fishes is pid content of the diet and feeding rate (Madenjian et consistent with areas where bacteria are concentrated in al., 2000). Hence the higher thiaminase activity noted by fishes (Fujita, 1954; Zajicek et al., 2005). Further, these Tillitt et al. (2005) in Lake Michigan alewives in spring authors stated that the biochemical characteristics of thia- relative to summer and autumn may be a reflection of minase, including temperature and pH optima in fishes, either the lower lipid levels observed in alewives dur- particularly Lake Michigan alewives, were consistent ing the spring relative to the summer and autumn (Flath with a bacterial source (see Zajicek et al., 2005). Given and Diana, 1985), or the lower feeding activity noted for the possible role of lipids in immune function, high lipid alewives in the spring relative to the summer and autumn levels may be involved in down-regulation of thiaminase- (Stewart and Binkowski, 1986), or some combination of producing bacteria, whereas low lipids may be involved these. Thiaminase activity of alewives collected in the in the up-regulation of thiaminase-producing bacteria. winter, the period of lowest feeding activity (Stewart and This in turn may influence the occurrence of thiamine Binkowski, 1986), was twice that of alewives collected deficiency in predators, since fluctuations in the thiami- during the summer, when feeding activity is expected to nase activity of a particular prey species may lead to fluc- be much higher (unpublished data). tuations in the amount of thiamine assimilated from prey The apparent relationship between lipid and thiaminase species by a predator. Honeyfield et al. (2005) found that activity may be as a result of the effect of lipids on the thiamine levels in the eggs of lake trout fed mixtures of

174 The North American Great Lakes/St. Lawrence River and Estuary

alewives, which are thiaminase-rich, and bloaters, which although the mode of uptake was not described (Arsan, are thiaminase-poor, were directly related to the average 1970; Arsan and Malyareevskaya, 1969). Zajicek et al. amount of thiaminase activity in the diet. (2005) measured thiaminase activity albeit at low levels There appears to be support for the notion that lipid in net plankton, Mysis and Diporeia from lakes Michigan can influence thiaminase activity in clupeids in the wild and Superior. All of these biota are potential prey of and affect their potential to cause thiamine deficiency ef- alewives (Hondorp et al., 2005) More comprehensive fects. The importance of diet and specifically its influence sampling in Lake Michigan (unpublished data) found on lipid stores and resulting thiaminase activity was sug- thiaminase activity in net plankton and Mysis of up to gested in work by Wistbacka and Bylund (2008). These 20% of the average measured in alewives from this lake authors found, albeit indirectly, that the thiaminase activ- (Tillitt et al., 2005). Furthermore, while thiaminase levels ity of Baltic herring appeared to be inversely related to were similar in net plankton and Mysis, they were three- their lipid content. During the period 1979-1991 when the fold higher than in Diporeia (unpublished data), suggest- M74 prevalence in Baltic salmon was low, the fat content ing that if diet was an important vector for thiaminase of Baltic herring in the main basin of the Baltic Sea was activity in alewives, the composition of the diet could be almost twice as high as in the most serious M74 period quite important. 1991-2002 (Wistbacka and Bylund, 2008). Wistbacka et Attempts at experimentally determining the role of dif- al. (2002) had earlier indicated that Baltic herring, with ferent factors in controlling thiaminase activity have had their high thiaminase activity, were the immediate causal little success but have provided some surprising results factor for the M74 syndrome in Baltic salmon, and this in terms of the dynamic nature of thiaminase activity in was the case for both time periods. clupeids. Experimentally stressing Seneca Lake alewives Variation in prey fish lipid stores and its effect on in the laboratory by either varying the salt content of thiaminase activity may also be responsible for variation holding water or food limitation in order to induce stress in EMS in coho salmon. In Lake Michigan, there was a and affect circulating white blood cells (Pickering, 1984; dramatic upward shift in the occurrence of EMS in coho Barton et al., 1987) did not affect their thiaminase activity salmon after 1990, after dreissenids had invaded the lake (Lepak et al., 2008). However, Lepak et al. (2008) found (Brown et al., 2005b). Coho salmon in Lake Michigan that the thiaminase activity of alewives held in the labora- eat alewives almost exclusively, feeding almost exclu- tory and fed a thiaminase free diet prior to experimenta- sively on large alewives in the second year of life prior tion was over two-fold higher than the thiaminase activ- to spawning (Madenjian et al., 1998a, b). The lipid con- ity of alewives immediately after collection from Seneca tent of large (≥ 120 mm) alewives dropped by upwards of Lake. The authors were unable to provide an explanation 50% following the invasion of Lake Michigan by dreis- for this difference. They felt it was unrelated to stress as senids in the late 1980s (Hondorp et al., 2005; Madenjian alewives grew well in the laboratory with little mortality, et al., 2006b). Madenjian et al. (2006) attributed the drop which they would not have expected had the fish been in lipid content to the decreased importance of Diporeia under stress. Similar effects were seen with Baltic herring in the diet, most likely the result of a decline in Diporeia held in captivity for 25 days, where there was an eleva- in Lake Michigan (Nalepa et al., 2005, 2006). Diporeia tion in thiaminase activity compared with that of herring is relatively high in lipid content (Hondrop et al., 2005) immediately after capture (Wistbacka and Bylund, 2008). compared with other invertebrates and a decrease in its Whether such changes involve effects on immune func- importance in the diet of alewives would be expected to tion, possibly by modulation of eicosanoid biosynthesis lead to decreases in both lipid content and energy density mediated by stress or trauma, remains to be determined. of alewives, since the two are correlated (Rottiers and Lack of identification of a factor or factors associated Tucker, 1982; Madenjian et al., 2000). with captivity that causes elevation in thiaminase activity Diet may also be a direct source of thiaminase for fish. is a major impediment to experimentation and to further Increased thiaminase activity was measured in fish ex- understanding of the importance of the regulation of thia- posed to toxic blue-green algae containing thiaminase minase activity in alewives.

175 The North American Great Lakes/St. Lawrence River and Estuary

Relationship between Alewife declined midway through the the time series used by Abundance and Thiamine Deficiency Fitzsimons et al. (1999) and this may have affected alewife thiaminase activity and altered their ability to Given the ability of alewives to cause thiamine deficien- cause thiamine deficiency (see Fitzsimons et al. 2005b). cy in proportion to their importance in the diet of labora- Due to the ongoing uncertainty as to the relationship tory fish a similar relationship would be expected among between alewives and the occurrence of EMS in feral wild populations although such a relationship if it exists fish we reevaluated the relationship between alewife may have changed over time (Honeyfield et al. 2005). abundance and the occurrence of EMS in families of Fitzsimons et al. (1999) correlated a measure of alewife coho salmon for Lake Michigan using new information. abundance with EMS, an indicator of thiamine deficien- For this we focused on the biomass of large alewives, cy; for Lake Michigan these authors reported a signifi- ages one to three, as they accounted for almost 90% of cant but negative and weak correlation(r2=0.14) between the biomass of large alewives in Lake Michigan between trawl catch abundance of adult alewife and the occur- the ages of one and six during the period 1999 to 2007 rence of EMS in coho salmon that ranged from 0 to close (Warner et al. 2008). Alewife biomass for a given year to 100%. Of the salmonines found in the Great Lakes and age was determined from abundance at age three coho salmon show the highest consumption of alewives when alewives are fully recruited to bottom-trawl gear so are likely to be the most responsive to changes in using the methods described in Madenjian et al. (2005). alewife abundance (Jude et al. 1987; Madenjian et al. We used trawl data collected by the Great Lakes Science 1998b; Lantry 2001). These authors used EMS as their Center (see Madenjian et al., 2005). Data on the propor- measure of thiamine deficiency because of its strong tion of coho salmon families with EMS were derived relationship with egg thiamine (Hornung et al., 1998; from the records of the Michigan Department of Natural Honeyfield et al., 1998) and the lack of historical data on Resources, Fish Health Laboratory (see Honeyfield et thiamine levels at the time. Fitzsimons et al. (1999) were al., 1998), which has maintained long-term observations unable to find similar negative correlations between of the occurrence of EMS in families of coho salmon alewife abundance and the occurrence of EMS in Lake ascending the Platte River. We focused on coho salmon Michigan lake trout, which they attributed to the greater ascending a single river since Wolgamood et al. (2005) diet diversity of lake trout compared to coho salmon had documented among river variation in EMS for Lake (Jude et al. 1987; Madenjian et al., 1998). The results of Michigan coho salmon. For the purposes of this analysis Fitzsimons et al. (1999) however, seem to run counter to the association established between alewives in the diet and reductions in egg thiamine (Fitzsimons and Brown, Table 20.1. Summary of number of Lake Michigan (Platte River) female coho salmon sampled, proportion of families developing EMS, and mean 1998; Honeyfield et al., 2005). Moreover the diet of sal- EMS in affected families for the period 1997 to 2007 (M. Wolgamood, monines seems to be opportunistic (Warner et al. 2008) Michigan Department of Natural Resources, Mattawan, Michigan, un- such that salmonines should make the greatest usage of published data). the most abundant food source. Hence during years of Year N Percentage of Mean EMS (%) in high alewife abundance, salmonines should make the families affected affected families greatest usage of alewives and this in turn should result 1999 30 96 100 in high EMS, not low EMS, unless other factors are at 2000 30 100 84 play. Its noteworthy however, that the data of Fitzsimons 2001 22 100 100 et al (1999) was based on all sizes of alewives and it 2002 25 8 32 has been established that in the their second year of life, 2003 20 5 53 coho salmon fed almost exclusively on large (>120 mm) 2004 21 33 57 alewives although smaller amounts of small alewives are 2005 27 4 22 also consumed (Madenjian et al. 1998). Moreover the 2006 30 60 73 lipid content of large alewives (Madenjian et al 2006b) 2007 24 42 88

176 The North American Great Lakes/St. Lawrence River and Estuary

Figure 20.3. Annual variation in the proportion of coho salmon families with EMS ascending the Platte River for the period 1999 to 2007 (Source: M. Wolgamood, Michigan Department of Natural Resources, Mattawan, Michigan, unpublished data).

Figure 20.4. Relationship between the arc-sin of the annual proportion of coho salmon families ascending the Platte River with EMS and estimated biomass of alewives ages one to three based on bottom trawling for the period 1999 to 2007 (Source: USGS, Ann Arbor, Michigan, unpublished data). we defined EMS as any family having a hatch to feed- of finding a positive relationship between the occurrence ing fry mortality greater than 20% (Brown et al., 2005c). of EMS and alewife biomass that was expected based on EMS data are summarised in Table 20.1 and Figure 20.3. earlier observations linking elevated EMS and reduced Using a restricted range of ages for alewives (ages egg thiamine with alewife consumption (Fitzsimons and one to three) that better reflects those consumed by coho Brown, 1998, Honeyfield et al., 2005). The relationship salmon (Madenjian et al. 1998) and constitutes a major here suggests that during periods of extreme alewife portion of the biomass for this species in Lake Michigan abundance that from the historical record appear to be (Warner et al. 2009) we found that the occurrence of EMS rare, most coho salmon families may show some level in coho salmon families was related to alewife biomass of EMS with corresponding effects on reproduction al- by an exponential relationship (F=45.4, p<001; Figure though these are uncertain since the amount of EMS in a 20.4). The use of a restricted age range and the greater given family does not appear correlated to the proportion range in biomass of alewives for this time series relative of families exhibiting EMS (Wolgamood et al., 2005). to historic (Figure 20.5), may have increased the likehood During periods of lower alewife abundance it’s evident

177 The North American Great Lakes/St. Lawrence River and Estuary

Figure 20.5. Biomass of alewives ages one to three based on bottom-trawling in Lake Michigan during the period 1981-2007 (Source: USGS, Ann Arbor, Michigan, unpublished data).

that a greater proportion of coho salmon families would tivity in alewives (Lepak et al., 2008; unpublished data). not be expected to show EMS although thiamine deficien- An understanding of controlling factors could potentially cy effects on other endpoints for coho salmon are uncer- be used to develop management actions (e.g. increase tain. Fitzsimons et al. (2009a) noted for larval lake trout lake productivity to affect alewife lipid level) to regu- that growth was a more sensitive endpoint to the effects late alewife thiaminase activity to a level consistent with of thiamine deficiency than EMS. Nevertheless natural natural reproduction by their predators (see Fitzsimons reproduction by coho salmon in Lake Michigan although et al., 2007). That such a level exists is suggested by limited, has been reported for some time (Madenjian et self-sustaining lake trout populations co-existing with al., 2002). Although the mechanisms involved in limiting alewives in at least two Finger Lakes, although additional the occurrence of EMS among coho salmon families dur- mitigating factors may also be involved (Fitzsimons et ing periods of reduced alewife biomass remain unclear al., 2007). As a result, other actions may be more appro- they may involve greater diet diversity as suggested by priate for affecting thiaminase intake by predators until Brown et al (2005c). Increased utilization of prey fish in a better understanding of factors controlling thiaminase the diet having lower (e.g. rainbow smelt) or no thiami- activity of particular prey species like alewives becomes nase (e.g. yellow perch) (Jude et al., 1987; Madenjian et available. One such action may be to restore prey diver- al., 1998b; Tillitt et al., 2005) would conceivably result in sity to the extent that the relative consumption of thia- a greater uptake of thiamine from the diet. minase-containing prey fish is considerably reduced and hence does not lead to thiamine deficiency effects in their predators. In some Great Lakes this appears be occurring naturally with the invasion and rapid population increase Future Directions in the aquatic invasive species round goby (Neogobius melanostoma) (Schaeffer et al., 2005a). This species ap- Attempts at experimentally determining the factors con- parently has low thiaminase activity based on collections trolling thiaminase activity in alewives have yielded few in Lake Michigan (Tillitt et al., 2005). In western Lake tangible results on the factors controlling thiaminase ac- Ontario after a ten year period during which lake trout

178 The North American Great Lakes/St. Lawrence River and Estuary

fed almost exclusively on alewives, as many as 20% of Although the complete elimination of alewives from lake trout now appear to be consuming gobies based on the diet of salmonines may seem like an extreme man- stomach content analysis (Fitzsimons et al., 2009c). This agement action, such a step may be necessary in or- appears to be sufficient to affect lake trout egg thiamine der to restore normal thiamine nutrition for top preda- levels, since average egg thiamine concentrations of lake tors like lake trout which appear to be more sensitive trout collected during 2007 were almost two-fold higher to the thiamine lowering effects of an alewife diet than than in 2003, when gobies were probably absent from the Chinook salmon (Fitzsimons et al., 2007). It is not clear diet (unpublished information). Similarly in Lake Huron, how effective restoration of essentially thiaminase-free egg thiamine levels in lake trout stocks from the Thunder prey fish would be in restoring thiamine levels in preda- Bay area that fed almost exclusively on gobies were over tors if alewives were still present and still being con- twice that of offshore stocks of lake trout that fed almost sumed. During the 1980s and 1990s, the prey commu- exclusively on alewives (J. Johnson, MI DNR, and D. nity of Lake Michigan was dominated by bloater chub Honeyfield, USGS, pers. comm.). (Madenjian et al., 2002) yet lake trout continued to feed A passive rather than a directed approach to the resto- as heavily on alewives then as in the 1970s, when bloat- ration of the prey fish community to eliminate thiamine ers were scarce. This dietary preference was reflected deficiency effects may, however, have unintended con- in egg thiamine levels as well (Fitzsimons and Brown, sequences on the reproductive success of predators. This 1998; Honeyfield et al., 2005). In Lake Huron, it was seems to be the case for gobies and lake trout. Large pop- only after a major collapse in alewife stocks occurred ulations of gobies can have negative consequences for (Shaeffer et al., 2005b), forcing lake trout to adopt new lake trout, as gobies are significant lake trout egg and fry diet choices that lacked alewives, that there was a meas- predators (Chotkowski and Marsden, 1999; Fitzsimons urable increase in egg thiamine levels (D. Honeyfield, et al., 2006). Gobies have been associated with the near pers comm.; Fitzsimons et al., 2009b). Thiamine lev- elimination of emergence of fry for at least one lake trout els are now adequate for reproduction, as indicated by spawning reef in Lake Ontario (Fitzsimons et al., 2009c), increased, spatially extensive and sustained natural re- although additional work is required to determine the production by lake trout in Lake Huron (Riley et al., spatial extent of lake trout egg and fry predation by go- 2007). Although other factors such as relief from pre- bies in the lake. dation of alewives on larval lake trout may also have Restoration of native species like ciscoes, which lack been involved (see Krueger et al., 1995), Fitzsimons et thiaminase activity, has been advocated (Fitzsimons and al. (2009b) concluded that for Lake Huron there was lit- O’Gorman, 2006), but impediments to restoration of wild tle evidence to support relief from an alewife predation stocks in the Great Lakes are not always clear but as point- effect as an explanatory variable. These authors found ed out by Dunlop et al. (2010) may well involve alewives. a general lack of overlap between the timing of larval Accordingly the presence of alewives may make it un- lake trout emergence and onshore migration of alewives. likely that restoration of native prey species like ciscoes Although changes in lake trout spawner abundance co- would be fully successful. Lake Huron had the lowest incident with the decline in alewives may have also abundance of alewives (with the exception of Superior) contributed to increased lake trout reproduction, these before alewives crashed there in 2002-2003 yet the abun- authors found that the spatial and temporal patterns of dance of cisco remained low (Dobiesz et al. 2005). It was natural recruits were not consistent with the spatial and only after the alewife population crashed in Lake Huron temporal patterns of spawner abundance. To support that there has been consistent evidence of spatially and their claim that relief from thiamine deficiency rather temporally extensive recruitment of cisco in this lake. In than predation may have been a major contributor to the contrast, for Lakes Ontario and Michigan, where alewife increase in lake trout natural reproduction, Fitzsimons et abundance is much higher, cisco stocks are spatially re- al. (2009b) documented increases in egg thiamine levels stricted and show only limited recruitment (J. Hoyle, ON following the crash in the alewife stock and showed that MNR, R. Claramunt, MI DNR, pers. comm.). a lake trout fry emergence index (FEI) was positively

179 The North American Great Lakes/St. Lawrence River and Estuary

Figure 20.6. Schematic of proposed cascade of events in the expansion of clupeids, resulting thiaminase dynamics, and thiamine deficiency effects following the loss of a top predator (Source: Authors).

correlated with egg thiamine levels, while the occurrence elimination of natural reproduction in the predator, pos- of EMS was negatively correlated with FEI. sibly leading to population extirpation as appears to have been the case for Lake Ontario and Finger Lakes Atlantic salmon (Ketola et al., 2000). Alternatively a variety of other less extreme scenarios not leading to population ex- Conclusions tirpation are also possible, depending on the severity of the thiamine deficiency and associated effects although To conclude, the loss of predator control on clupeids can the sustainability of these scenarios remains to be dem- set off a cascade of events wherein clupeid populations onstrated expand, suppress other prey fish species, and eventually become the dominate prey fish (Figure 20.6). In this po- Acknowledgements sition, clupeids can dominate predator diets, especially if The authors are indebted to Chuck Madenjian and David the abundance of predators has already been depressed Bunnell of USGS Ann Arbor, Michigan, US for making by other factors. Depending on their thiaminase activ- trawl data for Lake Michigan alewives available and sug- ity, which may be under the control of ecosystem factors gestions for it’s analysis. such as productivity and possibly mediated through the immune system, clupeids can exert a variety of nega- tive impacts at multiple life stages of a predator by the ensuing thiamine deficiency. These negative impacts can culminate in their most extreme case in the virtual

180 References

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