Freshwater Bivalve Ecotoxoicology - Chapter 3 pps

The distribution of any given mussel species depends on three factors Brim Box, Dorazio, and Liddell 2002, which correspond to different, increasingly finer levels of organization: 1 the

3 A Brief Look at Freshwater

Mussel (Unionacea) Biology

G Thomas Watters

A BRIEF HISTORY

As with all aspects of natural history, the early study of freshwater mussels passed through some interesting times After the Renaissance, a renewed interest in the sciences in general made the study of even God’s lowliest creatures an acceptable avocation Arm-chair naturalists, often relying

on information unchanged from Aristotle, reported on the creation of pearls from dew swallowed

by swimming mussels (Boetius in Rennie 1829), the ability of molluscs to voluntarily leave their shell (Wood 1815), and the infection of mussels by mange and gangrene (Poupart 1706) But the

“enlightened” study of freshwater mussel biology begins with the Dutch haberdasher, Leeuwen-hoek, who turned the fledgling hobby of microscopy towards mussels He removed eggs and glochidia from the marsupia of an Anodonta, describing them in 1695 and illustrating them in

1697 He clearly believed that glochidia were larval mussels, referring to them as “oysters not yet born.” But a century later Rathke (1797) stated that glochidia were parasites infesting the gills of mussels, despite Leeuwenhoek’s claims to the contrary (see Heard 1999b) Rathke named the presumed parasites Glochidium parasiticum, from which we derive the name for these larvae

A debate ensued over their true nature To resolve the matter, the Academie de Sciences Naturelles

of Paris formed a committee to investigate the matter In 1828, the committee reported that glochidia were indeed larvae rather than parasites, although they arrived at this conclusion in

a round-about manner (Blainville 1828) In 1832, Carus carefully followed the development of unionid eggs and finally, conclusively demonstrated that glochidia were larval mussels

The study of mussels had begun to mature In the spirit of the age, scientists began to study mussels for mussels’ sake Pre´vost (1826) in Europe and Kirkland (1834) in the United States experimentally determined that most mussels had separate male and female sexes Louis Agassiz turned his considerable talent and ego towards mussels, observing annular growth rings on shells, noting (but without realizing the importance of) the correlation between fish and mussel distri-butions, and bemoaning the fact that the science was conducted by “amateurs” (Agassiz 1862a, 1862b) One such “amateur” was de Quatrefages (1836), who carefully documented the existence

of internal organs in glochidia (heart, stomach, intestines)—organs that did not exist De Quatre-fages was eventually debunked by Schmidt (1856)

At this time, the fish-mussel connection was still unsuspected In 1862, the British clergyman, Houghton, reported glochidia attached to fish and artificially infested fish with the parasites (Heard 1999a) This was the first hint that glochidia might be parasites on fish In 1866, Leydig noted (as a footnote to the dissertation of Noll, his student) that glochidia were found attached to fish, appa-rently unaware of Houghton’s work The same year another worker, Forel (1879), confirmed this observation Again unaware of Houghton’s previous experiment, Braun and Schierholz in the winter of 1877–1878 independently attempted to artificially infest fish with glochidia, but

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Schierholz’s experiment failed (Schierholz 1889) Braun succeeded in infesting fish with Anodonta (1878a, 1878b), thus confirming Houghton’s results Glochidia had come full-circle: from larvae to parasites to parasitic larvae (Figure 3.1)

ECOLOGY

Unlike most infaunal marine bivalves, North American freshwater mussels lack true siphons or tubes for water intake and release Because of this, most species are confined to burrowing only to the posterior edge of the shell This is important because, for most freshwater mussels, burial depth does not become a buffer from chemicals, temperature extremes, or predation However, a few species, such as Pleurobema clava, may spend much of their life buried several centimeters beneath the surface, relying on water to percolate between the substrate particles for food and oxygen In temperate regions, mussels may burrow deeper into the substrate during winter as well

The distribution of any given mussel species depends on three factors (Brim Box, Dorazio, and Liddell 2002), which correspond to different, increasingly finer levels of organization: (1) the overlying distribution of hosts; (2) the distribution of mussels within a river reach; and (3) the distribution of mussels on a microhabitat scale Obviously, a mussel may not exist without its host but the converse is not true Although there is a strong correlation between fish and mussel species richness for a drainage (Watters 1992), most mussels occupy only a portion of the overall range of their presumed hosts Apparently, there is more to the story than just the distribution of the host At the second level of organization, the within-stream distribution, the host’s distribution probably is still important The so-called, “big river” mussel species occur there because of the requirements of their hosts; there is nothing to prevent these mussels from living in small creeks beyond host availability It is at the third level, microhabitats, that mussel distribution becomes confusing Intuitively, we would suppose that microhabitats would be the eventual determinant of where mussels live, but time and again no clear-cut cause and effect is evident For example, Brim Box, Dorazio, and Liddell (2002) found the distribution of only one of five species to be related to substrate composition Strayer and Ralley (1993) found no strong relationship between the distri-bution of six mussel species and microhabitat variables except for water current speed and variability Other studies also point out the weak association between mussel distribution and microhabitats (Tevesz and McCall 1979; Strayer 1981; Holland-Bartels 1990) It appears that

Juvenile

Growth

Sperm Glochidia

FIGURE 3.1 A typical freshwater mussel life cycle

stream hydro- and geomorphology variables, such as sheer stress and flow refugia, are the most important factors in mussel distribution on a fine scale (Strayer 1993; Vaughn 1997; Strayer 1999) Mussels feed by filtering out material from the water with their extensive gills, which are much larger than is needed for respiration The gills have a fine mesh-size indicative of a preference for minute food items The natural components of mussel food have not been completely identified Whereas Allen (1914, 1921), Churchill and Lewis (1924), and Fikes (1972) found the gut to contain mostly diatoms and other algae, Imlay and Paige (1972) believed that mussels fed on bacteria and protozoans Bisbee (1984) found different proportions of algal species in the guts of two mussel species, suggesting preferences between species The comprehensive study of Nichols and Garling (1998) demonstrated that mussels were omnivores, feeding on detritus and zooplankton, as well as algae and bacteria

We now know that adults and juveniles do not feed upon the same material Newly-metamor-phosed juveniles do not filterfeed with their gills (which are mere buds at this stage) but rather feed

on interstitial nutrients using cilia on their foot and mantle Eventually, functional gills are formed, and there is a change to a filterfeeding mode (Tankersley, Hart, and Weiber 1997) Again, the exact food items of juveniles are the subject of debate Yeager, Cherry, and Neves (1993) believed food for juveniles consisted of interstitial bacteria, whereas an algal/silt mix was suggested by Humphrey and Simpson (1985) and Gatenby, Neves, and Parker (1993) Small amounts of silt have been found

to enhance survivorship in cultured mussels, both adults and juveniles (Hudson and Isom 1984; Humphrey 1987; Hove and Neves 1991), probably by introducing bacteria, zooplankton, and micronutrients Juveniles grow best and have a higher survivorship when fed a diet high in lipids (Gatenby, Neves, and Parker 1997)

REPRODUCTION

Freshwater mussels typically are dioecious, but hermaphrodites have been found in many species (Poupart 1706; Fischerstrom 1761; van der Schalie 1966, 1970; Heard 1979) Some species are believed to be wholly hermaphroditic, such as Toxolasma parvus, Lasmigona compressa, and Utterbackia imbecillis (Ortmann 1912; Utterback 1916) The relative proportion of hermaphrodites among otherwise dioecious species may increase under low population densities as a means of augmenting declining population numbers (Kat 1983; Bauer 1987b) As hermaphrodites, these species may be best suited as colonizing forms capable of establishing themselves under low initial population densities or in headwater or otherwise isolated situations

Spawning, the release of gametes, occurs at different times and frequencies depending on the species and latitude Sperm may be released as “sperm balls” or discs—apparently hollow structures composed of sperm, flagellae facing outwards, which propel themselves through the water to a limited extent These spheres disassociate to fertilize eggs (Barnhart and Roberts 1997) Spawning takes place in the spring for most amblemines and in the summer for most anodontines and lampsilines These spawning patterns are described below in more detail Mussels may migrate horizontally to congregate during spawning, presumably to increase spawning success by increasing the density of individuals (Amyot and Downing 1998) Spawning also is associated with vertical migration in the substrate In a study of the vertical movement of eight mussel species composed of both amblemine and lampsiline taxa, Watters, O’Dee, and Chordas (2001) found that all studied taxa migrated to the surface in April–May, presumably to spawn This migration was remarkably synchronized across the eight species and apparently was triggered by spring water temperatures Although most North American mussels have a single spawning season per year, there is evidence that some species have multiple broods (Howard 1915; Ortmann 1919; Gordon and Smith 1990; Howells 2000)

Eggs are fertilized in the suprabranchial chambers of the gills, and developing embryos are moved to the marsupial regions of the gill where they are “brooded” until released This marsupial

region physiologically isolates the developing larvae (Kays, Silverman, and Dietz 1990) and acts as

a source of maternal calcium for the construction of the glochidial shell (Silverman, Steffens, and Dietz 1985) During the gravid period, this region of the gill may not function as a site of respiration (Richard, Dietz, and Silverman 1991), or it functions in a much limited capacity (Allen 1921; Tankersley and Dimock 1992) The marsupial region may remain nonrespiratory even during the nonbreeding season (Richard, Dietz, and Silverman 1991)

Glochidia are a type of veliger larvae; freshwater mussels lack the trochophore precursor stage found in many other molluscs Although glochidia have been recovered from Quaternary sediment cores (Brodniewicz 1968, 1969), we have no way of knowing when or how larval mussels became parasitic during their 250C million year evolution Watters (2001) outlined the early phylogenetic history of North American mussels, suggesting that glochidia may have been parasitic at least as early as the Cretaceous and that the explosion in mussel diversity seen during the late Mesozoic may be correlated with the rise of teleost fishes, their hosts The earliest mussels may have lacked planktonic larvae, having instead brooded their larvae Other freshwater bivalves, such as sphaer-iids, also brood their larvae When expelled, these larvae may have fortuitously attached to passing fish Over time, the adaptive significance of the increased dispersal powers of these glochidia led to

a phoretic relationship As glochidia developed more efficient means of remaining attached to fish (e.g., hooks, etc.), a true parasitic symbiosis arose This may have begun when glochidial attach-ment caused physical harm to the fish, eliciting a wound reaction and triggering immune system responses These early mussels probably brooded relatively few glochidia The earliest adaptations

to their new parasitic life involved increased fecundity (as with most parasites) and the develop-ment of efficient glochidial delivery systems, such as conglutinates The earliest parasitic mussels were conglutinate-producing forms related to recent amblemines They produced relatively few glochidia

North American glochidia typically occur in three morphological forms The triangular, hooked glochidia of most anodontines and some amblemines is the most prevalent Most lampsilines have non-hooked, D-shaped glochidia The third morphological type, the “pick-ax” glochidium, occurs

in Potamilus These glochidia may be divided into two functional groups The first, the gill parasites, comprising most of the lampsilines, lack macroscopic attachment devices The inner rims of the glochidial shells are set with numerous fine points that enable the glochidia to grip the gill filaments The second type, glochidia specializing in the attachment to the outside of their host, the fins, barbels, or skin have better-developed attachment structures—simple or toothed hooks, particularly developed in anodontines and Potamilus These glochidia apparently require greater

“gripability” due to the fact that they are more prone to being dislodged than are gill parasites, which are protected to some degree by the opercles of the host Mechanically, glochidia fall into two groups based upon their shell-musculature design (Hoggarth and Gaunt 1988) Some are adapted for maximum glochidial shell sweep, increasing the potential area of attachment Others emphasize closure force to minimize dislodgement Some glochidia apparently can detect the presence of hosts through substances in host’s mucus or blood (Shadoan and Dimock 2000) Henley and Neves (2001) identified fibrinogen as one such substance Once released, glochidia may persist for several weeks and be carried by currents for considerable distances (Fisher and Dimock 2000; Zimmerman and Neves 2002), but they are heavily preyed upon by planarians, hydras, aquatic insects, etc

Glochidia tend to be overdispersed within a host population That is, the parasite burden is carried by a relatively small portion of the available host population For example, of 3441 fish examined in a study of Lake Otsego, only six carried glochidia (Weir 1977) Only 14 percent of the

4800 fish examined in a study of the North Fork Holston River had glochidia (Neves and Widlak 1988) This is due to the mechanisms that mussels utilize to parasitize hosts: lures and conglutinates that tend to heavily parasitize only the few fish that actually attack these structures whereas the majority of the host population never comes into contact with them

Once encapsulated, glochidia are true parasites on the host, feeding on host tissue enclosed between the glochidial shells and on their own larval adductor muscle (Arey 1924b, 1932a; Blystad 1924; Fisher and Dimock 2002a) The glochidial shell is perforated (Rand and Wiles 1982; Jeong, Min, and Chung 1993; Kwon et al 1993), but whether nutrients move through these pores is uncertain Rather, nutrient uptake is probably through the microvillae of the mantle (Wa¨chtler, Dreher-Mansur, and Richter 2001) or the mushroom body (Fisher and Dimock 2002b) Most glochidia do not increase in size while encapsulated, margaritiferids being a notable exception Glochidia apparently do little harm to their hosts When parasitized in a laboratory setting, fish often are lethargic for several hours to a day post infestation but return to normal within several days with no obvious side effects Reports of host mortality from overinfestation are rare and are usually based on artificial situations in which enormous numbers of mussels come into close, constant contact with captive fish These occurrences tend to involve fingerling or young-of-year fish kept in hatcheries where mussels have colonized the ponds (Moles 1983) Even so, infestations

as high as 736 glochidia per fish have been reported from hatchery situations with no adverse effects (Margaritifera margaritifera on Atlantic salmon) (Bruno, McVicar, and Waddell 1988)

Potential hosts may possess one of two types of immunity to attached glochidia Natural immunity occurs in unsuitable hosts, which have tissue responses against the glochidia (Howard 1914; Bauer and Vogel 1987) Acquired immunity occurs when a suitable host has been previously parasitized and has built up a temporary immunity The number of exposures needed to achieve acquired immunity depends on the degree of prior infestations and the duration between them (Lefevre and Curtis 1910; Surber 1913; Reuling 1919; Arey 1924a; Bauer 1987a) For example, for largemouth bass exposed to Lampsilis cardium, three to four exposures over 30-day intervals are required to elicit complete immunity (Watters 1996) Acquired immunity to one unionid species was thought to give the host immunity to others (Reuling 1919), but this has not been substantiated Indeed, largemouth bass possessing a complete immunity to L cardium were successfully infected

by glochidia of U imbecillis (Watters 1996) and even its congener Lampsilis fasciola (Watters and O’Dee 1997) Although acquired immunity may be demonstrated in the laboratory, acquired immunity in the wildcaught fishes has been observed only once, and its overall prevalence in wild fishes is unknown (Watters and O’Dee 1996) In both natural and acquired immunity, encysted glochidia are killed by the host and either sloughed off or absorbed (Arey 1932b; Fustish and Millemann 1978; Zale and Neves 1982; Waller and Mitchell 1989) Acquired immunity apparently may be lost if no subsequent reinfestation occurs within a certain time period, and the fish may become susceptible to parasitization again (O’Dee 2000) However, the amount of time needed to lose acquired immunity is not precisely known

Metamorphosis from glochidium to juvenile mussel takes place within the capsule in two stages (Fisher and Dimock 2002b, for U imbecillis) First, during the first four days, the larval adductor muscle is digested by a region of the glochidia called the mushroom body Second, during the last four days, the juvenile anatomical structures appear The triggers for metamorphosis and the duration of the parasitic phase vary with mussel species and host species Metamorphosis on different host species infested with the same mussel at the same time may be delayed by weeks depending on the host Metamorphosis is triggered and regulated by water temperature Heinricher and Layzer (1999) and Watters and O’Dee (1999) demonstrated that a temperature threshold existed below which metamorphosis was significantly delayed, perhaps indefinitely Glochidia remained encapsulated until the threshold was surpassed, at which time metamorphosis took place Conversely, the duration of metamorphosis decreases with increasing temperature (Barnhart and Roberts 1997) until an upper threshold is reached At this point, glochidia may break free of the capsule, fail to metamorphose, and die (Dudgeon and Morton 1984) Most North American mussels have a parasitic duration of 2–6 weeks, but European species may persist for ten months (Wa¨chtler, Dreher-Mansur, and Richter 2001)

Once free of the host, the newly metamorphosed juvenile assumes a life style quite unlike those

of adults Realization of this fact has been slow in coming These juveniles may burrow to several

centimeters beneath the surface where they rely on water percolating between the interstices of substrate particles for food and oxygen New juveniles feed by ciliary currents on their foot and mantle—gills are present at this stage only as buds and have no filtering abilities (Yeager, Cherry, and Neves 1994) They are feeding on detritus and other interstitial material Thus, juveniles and adults probably are utilizing different food types and living in different micro-environments and are susceptible to different changes in habitat and water chemistry Efforts to protect the habitat of adult mussels may therefore be inadequate to protect juveniles

REPRODUCTIVESTRATEGIES

Freshwater mussel reproductive strategies represent two mutually exclusive, adaptive choices, each choice favoring a certain aspect of the mussel life cycle at the expense of other aspects These choices have far-reaching behavioral and phylogenetic implications Both choices have evolved to increase the efficiency of completing the life cycle, either by specializing on a small subset of potential hosts or by generalizing on a wide variety

Parasites in general compensate for their improbable life histories by increasing fecundity— increasing the chances of a larvae surviving to reproduce by making so many offspring that even the most complex life cycle will be completed simply by the sheer number of attempts Freshwater mussels, once they entered into their parasitic symbiosis with fish, also increased their fecundity as

a hedge against their new life cycle It has been estimated that as few as ten in one million larvae successfully attach to a host (Bauer 2001b) Such an increase in offspring numbers carries heavy physiological burdens: calcium reserves for glochidial shells, maintenance of the surrounding marsupial medium, loss of respiratory function in the marsupial gills, increase in overall size dictated by the needs of the marsupium, etc Any means of reducing this burden would be positively adaptive Because the offspring number is driven by the success of completing the life cycle, perhaps the most obvious way to reduce the offspring number is to increase the efficiency with which a glochidium successfully “finds” a host If more glochidia were more efficient parasites, then fewer offspring would be needed to attain the same level of life cycle success

Historically mussels were considered broadcasters—simply releasing vast quantities of larvae into the water, chancing that the right host would be in the right place at the right time We now know that true broadcasters are quite rare Nearly all mussels investigated have evolved means of luring the correct host to their glochidia Two mechanisms are apparent: lures and “conglutinates” (Haag, Butler, and Hartfield 1995)

Lures are the hallmark of lampsiline mussels and consist of highly specialized portions of the female mussel’s mantle that mimic, in one way or another, host–prey items (Haag, Warren, and Shillingsford 1999; Haag and Warren 1999, 2000) Lures may be quite mimic-model specific For instance, many Lampsilis species have mantle flaps resembling small “minnows,” complete with eye spots, fins, and swimming motions Others are less model specific, consisting of synchronous movements of papillae (some Villosa), writhing caruncles (Toxolasma), or other displays that are not recognizable (to humans at least) as specific mimics Lures function by drawing the host to the female mussel, fooling the would-be predator into striking at a food item Upon striking, the mussel releases a cloud of glochidia, parasitizing the host In at least some species, the female closes her shells upon the extended marsupia, causing them to rupture

“Conglutinates” is a collective term for structures fabricated by the female mussel, containing glochidia, that mimic host prey items These are eaten by hosts that would normally feed on the conglutinate model As with lures, conglutinates may be generalized or mimic specific Fusconaia and Pleurobema release packets of glochidia that resemble “worms.” Strophitus releases maggot-like conglutinates The most complex conglutinates yet seen are fashioned by Ptychobranchus, where the conglutinates bear striking resemblances to fish eggs, fish fry (Barnhart and Roberts 1997; Watters 1999), insect larvae (Hartfield and Hartfield 1996), or simulid pupal cases Several species assemble individual conglutinates into a single “superconglutinate” that may be played out

at the end of mucus strands by the female (Haag, Butler, and Hartfield 1995; Hartfield and Butler 1997; O’Brien and Brim Box 1999) Hosts are infested when they attempt to ingest these structures During ingestion, the host often flushes glochidia over its gills, where they attach Although most of the glochidia are lost or ingested, enough successfully attach to make this strategy worthwhile Conglutinates typically are composed of glochidia embedded in a mucus matrix (most anodon-tines) or glochidia attached to each other by the adhesive properties of their egg membranes (most amblemines) In some groups, not all eggs are fertilized; these become structural cells, giving the conglutinate, in which the glochidia are embedded or attached, form and color (Barnhart 1997) How these eggs are “turned off” is of great interest In some groups (Strophitus, for example) the glochidia are tethered to the conglutinate by a glochidial thread

Because lures and conglutinates are more efficient at reaching a host, glochidial numbers may

be much fewer than needed for a comparable broadcaster Even though there is a physiological cost

to producing conglutinates or lures, it is compensated for by the decrease in numbers of glochidia required to parasitize a host by broadcasting Some mussels make less than 100 conglutinates, each containing less than 20 glochidia; some presumed broadcasters may produce several million glochidia Furthermore, the glochidial stage is thought to be the life stage having the greatest mortality; this would be especially important for broadcasting species (Jansen, Bauer, and Zahner-Meike 2001)

The development of lures and conglutinates has enormous consequences for the biology and evolution of freshwater mussels, setting them on apparently irreversible and diverging courses (Bauer 2001a) These developments have conservation consequences as well These adaptive choices are host specialization and host generalization They are driven by the very adaptations just discussed: lures, conglutinates, and broadcasting

A mantle lure the size, color, and shape of a small minnow represents a large suite of “can” and

“cannot” consequences for the mussel—so does a conglutinate fashioned after a simulid larva These devices play to a small, select audience Minnow lures attract large, predatory fish, not darters, sculpins, sticklebacks, or lampreys If one artificially parasitizes such a mussel with these unlikely attackers, more often than not, the attackers do not act as “good” hosts This is because the mussel and its true hosts have already entered into the host-parasite Arms Race In a teleological sense, the mussel is continuously designing a better mouse trap, a better and more efficient means of luring the correct host to its glochidia and ensuring that its larvae can withstand the host’s biological defenses The host on the other hand is continuously tweaking its immune system to ward off the parasite The race is on—but to the exclusion of other potential hosts By customizing the lure or conglutinate and its glochidia to a specific host, the mussel loses the ability

to use other hosts The lure so effective for bass has no charm for darters The conglutinate shaped like a tiny fish egg holds no magic sway over walleye Furthermore, the fine tuning that allows the glochidia to survive the immunological onslaught from its “preferred” host no longer works against other hosts By specializing in particular hosts, the mussel is set on an irreversible path This specialization may differ even between closely related mussel taxa (Riusech and Barnhart 2000)

On the other hand, some mussels clearly seem to be host generalists; they are able to successfully parasitize a wide range of hosts Many anodontines fall into this category

There are obvious trade-offs between host specialists and host generalists Specialists are more efficient at contacting their hosts and so require fewer glochidia; however, they may only use a small subset of the once available host pool Therefore, they are susceptible to extirpation should their hosts disappear from the immediate vicinity Generalists usually are not efficient at contacting hosts (some are broadcasters) and require large numbers of glochidia, but may successfully para-sitize those hosts they do manage to contact They are less susceptible to loss of any specific host species However, simulations show that specialists are less affected by changes in overall host abundance than are generalists; this is due to the efficiency with which specialists can use lower numbers of hosts (Watters 1997) Generalists have evolved to exploit new habitats and new hosts; specialists have evolved to persist under low host densities

Because of the stochastic elements of the mussel-host relationship, the greater the number of hosts available to the mussel the better But once the host pool abundance drops below a critical threshold the mussel population may be extirpated simply by probabilistic effects That is, mussels, whether specialists or generalists, may decline even though their hosts are present, if the host pool drops below this threshold (Watters 1997)

REPRODUCTIVEPATTERNS

Sterki (1895) noted that North American mussels could be divided into two behavioral groups based upon the duration that glochidia are held in the marsupia These groups came to be known as tachytictic or short-term breeders and bradytictic or long-term breeders Tachytictic breeders spawn

in the spring or summer and release their glochidia later the same year, usually by July or August Bradytictic breeders spawn in the summer or early autumn, form glochidia, and typically hold these larvae in the marsupium, overwintering them until the following spring or summer Anodontines and lampsilines tend to be bradytictic; amblemines tend to be tachytictic Some bradytictic forms apparently metamorphose the same year without overwintering, but there is evidence that these glochidia experience more mortality once on the host than those glochidia that overwinter in the marsupium (Corwin 1921; Higgins 1930; Tedla and Fernando 1969; Zale and Neves 1982) But some mussels release glochidia in autumn or winter to overwinter on their hosts (Watters and O’Dee 1999, 2000), where they remain dormant until a threshold temperature is reached the following spring, at which time they metamorphose and excyst This third reproductive pattern, termed host overwintering, plays a prominent role in some species, such as Pyganodon grandis and Leptodea fragilis Overwintering of glochidia on hosts increases the dispersal of the species by allowing the glochidium to remain attached to its mobile hosts for a greater duration than would occur with tachytictic or bradytictic species Host overwintering may confer greater fitness as well

on the newly metamorphosed juveniles If survival is correlated to the duration of the first year’s growth before winter, then host overwintering juveniles have the longest growing season In bradytictic species, rising spring water temperatures result in glochidial release—metamorphosis

is not until several weeks later But in host overwintering forms, spring temperatures result in metamorphosis—and an increased growth period the first year Tachytictic species metamorphose later than any other group and have the shortest growing season; tachytictic forms are probably the most primitive

As with reproductive strategies, there are tradeoffs between reproductive patterns as well Although no studies have addressed the issue, it is likely that glochidia are more at risk while attached to the hosts than when brooded in the female’s marsupium While on the hosts, they may

be damaged or knocked off, or the host may die By this reasoning, host overwintering would be the most risky The tradeoff is between the increased risk of mortality vs the increased dispersal and lengthened growing season The least risky is tachyticty, where the glochidial stage accounts for the shortest portion of the mussel’s life in comparison with bradyticty or host overwintering, but also has the shortest growing season The middle ground is bradyticty, which ensures a longer growing season than tachytictic forms and an equal amount of dispersal Finally, there is mounting evidence that some temperate species have multiple broods (Watters and O’Dee 2000) In these cases, a species may have both tachytictic (in the summer) and bradytictic (over winter) reproduction It remains to be seen how widespread is such a “hedging” of patterns

There is relatively little information on the precise timing of glochidial release or the triggers causing their release Watters and O’Dee (2000) found that Lampsilis radiata luteola released glochidia year-round as a function of water temperature—the higher the temperature the greater the number of glochidia released Such a pattern is difficult to explain by the models of tachyticty, bradyticty, or host overwintering Yet in the same study, Amblema plicata released a single, very short-lived burst of glochidia in July Clearly there are two very different modes of glochidial release as evidenced by these two species; in one, constant glochidial release tracked water

temperature, in the other, glochidial release occurred as a single event triggered by a threshold water temperature These represent fundamental differences and deserve more study

PARTING COMMENTS

The effects of pollutants on this complex life cycle are covered in detail elsewhere in this volume, but several important points need to be made here More than one animal is involved Efforts to conserve and manage any given mussel species are futile if the host(s) is not conserved and managed as well Fish and mussels are very different creatures with very different life styles, requirements, and tolerances Ecotoxicological concerns cannot concentrate on one without the other Mussels are parasites Mussels cannot be treated as free-living organisms, although they are commonly considered as such Conservationists and researchers need to be aware of the unique aspects of the parasitic life cycle, including fecundity and host-parasite interactions Mussels have different life stages Like most invertebrates, mussels have larval and juvenile stages that are ecologically and physiologically different from their adult forms What may be only marginally harmful to an adult may be lethal to a juvenile Not all mussels are created equal It is perhaps human nature to regard other animals as a single entity What harms one animal harms them all Mussels are often thought of in this way; we speak of a pollutant affecting a mussel bed or a river reach as if all mussels respond the same way But we know this to be wrong Mussels run the gamut

in their tolerances and susceptibilities like any other kind of animal Derailing the mussel’s life cycle is dangerously simple precisely because of its complex nature

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