THE EFFECTS OF SEASONAL TEMPERATURE AND PHOTOPERIOD MANIPULATION ON REPRODUCTION IN THE EASTERN ELLIPTIO ELLIPTIO COMPLANATA.
North American freshwater mussels (Unionidae) have undergone serious decline over the past 100 y. Habitat degradation, over exploitation, and the introduction of exotic species are all contributing factors to this loss (Ricciardi & Rasmussen 1999, Ricciardi et al. 1998, Strayer et al. 2004, Williams et al. 1993). At the last comprehensive evaluation over 20 y ago, only 24% of the 297 native freshwater mussel species in North
America were considered stable and 72% were considered to be endangered, threatened, or of special concern (Williams et al. 1993, Lydeard et al. 2004).
Freshwater mussels provide numerous benefits to both lentic and lotic ecosystems, and the potential loss of mussels could be devastating to these ecosystems. Mussels impact sediment transport and nutrient dynamics, provide habitat to other benthic organisms, and act as a food source for fish and other aquatic species (Allen & Vaughn 2011, Amyot & Downing 1991, McCall et al. 1979, Nalepa et al. 1991, Negus 1966, Strayer et al. 1994, Vaughn & Hakenkamp 2001). Beyond their ecological functions, mussels are also economically important.
Humans have used freshwater mussels as a food source, for monitoring and detecting pollution, and for their shells and pearls (Metcalfe & Charlton 1990, Strayer et al. 2004, Williams et al. 1993).
Fully understanding the factors that regulate freshwater mussel reproduction could enhance laboratory propagation, host fish identification studies, and population recovery efforts.
Research has shown a combination of factors, including temperature, photoperiod, food availability, and chemical cues, can regulate gamete development, spawning activity, and glochidial release. Studies on the zebra mussel Dreissena polymorpha (Pallas, 1771) found that temperature, photoperiod, and food availability influence gonad development
(Borcherding 1995, Wacker & von Elert 2003). Wacker and von Elert (2003) also found that temperature played an important role in triggering zebra mussel spawning. Similarly, temperature, more specifically degree days, and food availability have been shown to influence gamete development and release in the freshwater mussels Quadrula pustulosa (I. Lea, 1831), Quadrula cylindrica (Wright, 1898), and Quadrula quadrula (Rafinesque, 1820) (Galbraith & Vaughn 2009).
Chemical cues, such as serotonin and dopamine, have also been shown to affect spawning in zebra mussels (Ram et al. 1993) and the freshwater mussel Elliptio complanata (Lightfoot, 1786) (Gagne et al. 2004).
The production of viable glochidia, the parasitic larval stage of freshwater mussels, on a predictable schedule and the ability to prolong glochidia availability would greatly aid in current research and recovery efforts. Extending the reproductive period would benefit studies on mussel development and host fish suitability and greatly aid in hatchery propagation. The objectives of this study were to (1) determine the reproductive season of a single mussel species, Elliptio complanata, from Pine Creek, Tioga County, PA, and (2) determine whether photoperiod and water temperature can be manipulated to control the timing of glochidial release.
MATERIALS AND METHODS
The eastern elliptio Elliptio complanata (Bivalvia: Unionidae) is a medium sized (shell length usually less than 127 mm) freshwater mussel common in streams and rivers along the Atlantic Coast of North America (Nedeau 2008). Mature E. complanata were collected from a large pool in Pine Creek (Tioga County, PA, a tributary to the West Branch of the Susquehanna River) in December 1994 when the natural water temperature and photoperiod were at a seasonal low. Mussels were taken to the U.S. Geological Survey Northern Appalachian Research Laboratory in Wellsboro, PA. The specimens were individually measured for shell length, weighed, and inscribed with an identification number using a rotary engraver.
The mussels were fed daily with phytoplankton and detritus obtained from a concrete pond, commercial algae (Algamac-2000, algae paste), and/or decomposed leaf and grass litter at a rate adjusted to that which produced visible algal settling or mussel pseudofecal output.
Experiments were conducted in eight 1.2-m-diameter circular fiberglass tanks operating as a flow-through system. Each tank consisted of a sand/gravel substrate at a depth of 25 cm, a center drainpipe, and a polystyrene cover. Water from two separate supply lines (10[degrees]C ambient; 23[degrees]C heated) was blended to obtain desired temperatures above 10[degrees]C. Internal 1 HP
Ranco chillers were used to control for water temperatures below 10[degrees]C. Two incandescent light bulbs controlled by a programmable digital timer were set above each tank on the polystyrene cover.
Three environmental treatments and one control were randomly assigned to the tanks, resulting in two replicates per treatment. The control had a water temperature and photoperiod regime mimicking natural conditions for Pine Creek. Water temperature conditions for the control were based on data obtained from Flippo (1975), and photoperiod data came from the PA Game Commission. Temperature ranged between 0.5[degrees]C and 22[degrees]C and photoperiod varied between 9.5 and 15 h of daylight seasonally. Midwinter conditions were prolonged for 6 (treatment A) and 12 (treatment B) wk starting January 1, 1995.
Treatment C was similar to the control, except that a water temperature minimum of 10[degrees]C was maintained during the winter (Fig. 1).
Either 45 or 46 mussels were randomly assigned to each tank. As methods for nonlethal sex determination were not known at the time, sex ratio within the tanks was not controlled.
Reproductive activity was recorded daily, with the exception of most Sundays. Released glochidia were removed from experimental tanks with a pipette and categorized as immature or mature. Mature, fully developed glochidia were released individually, as mucous strands, or as leaf-shaped packets where movement within the membrane was observed. Glochidia packets were carefully collected and counted, but because of the flow-through nature of each tank, there was the potential for some loss. Counts of mature glochidia represent packages of glochidia, not individuals, as either leaf-shaped conglutinates or mucous strands. Survival of the adult mussels was assessed at the end of the study.
Differences in shell length, mussel weight, and survival were analyzed between treatments with ANOVA and within treatments with paired t-tests. Interactions between temperature and photoperiod could not be addressed as they were not independently manipulated. Total numbers of mature and immature glochidia were not normally distributed, and therefore, nonparametric tests were used to assess differences within and between treatments. The production of mature and immature glochidia was compared within treatments with a related sample
Wilcoxon signed rank test and between treatments with an independent samples Kruskal--Wallis test. Data were evaluated using SAS and SPSS statistical software and considered significant when P < 0.05.
There was no significant difference in the initial, final, or change in length and weight of mussels between the treatments (Table 1). After the study, there was a significant increase in shell length (tdr-358 = 1.97, P < 0.0001) and decrease in weight (tdr-358 = 1.97, P < 0.0001). Survival during the study was high and ranged between 96% and 100% with no difference between treatments (F3,4 = 6.59, P = 0.14; Table 1).
Initial conglutinates released were white and leaf-shaped, containing mostly immature glochidia. In the control, immature glochidia were released in early June, 3 days before the release of mature glochidia. The time period between the release of immature and mature glochidia was greater in the manipulated treatments. Immature glochidia were observed mid-June in treatment A (6-wk delay), with a 27-day delay until mature glochidia were released. Treatment B (12-wk delay) had an 18-day delay between immature and mature glochidia, with immature glochidia observed in early August. Immature glochidia were released in late May in treatment C (natural with 10[degrees]C low), with a 7-day delay until mature glochidia were released.
Mature conglutinates were composed of fully developed glochidia packaged within a clear matrix, and final release typically occurred as free individuals extruded on thin mucus-like strands.
A summary of the production of mature glochidia packages is presented in Figure 2. Control mussels cultured under a natural photoperiod and water temperature regime released mature glochidia between the fifth and 21stt of June when the temperature ranged between 16.6[degrees]C and 18.7[degrees]C and the photoperiod was at 15 h of light. In treatment C, mature glochidia were also observed in early June between the fifth and 26th.
During this time, water temperatures varied between 16.6[degrees]C Total packages of glochidia observed Average number of glochidia packages and 19.2[degrees]C and again photoperiod was at 15 h of daylight.
Mature glochidia were not released until July 13th in treatment
A, proportional to its 6-wk delay in water temperature and photoperiod. Mature glochidia in this treatment were released between the temperatures of 16.9[degrees]C and 20.4[degrees]C. During this time, the photoperiod increased from 14.75 to 15 h of daylight.
Mature glochidia continued to be observed in treatment A until
August 15th. Finally, mature glochidia were released between
August 22nd and September 21stt in treatment B, also proportional to its temperature and photoperiod delay (12 wk).
During this time, water temperatures varied between 15.3[degrees]C and 19.0[degrees]C and the photoperiod ranged between 14.75 and 15 h of daylight.
Average production of packages of glochidia by treatment is summarized in Figure 3A. The average proportion of immature glochidia produced per day did not differ significantly from the average proportion of mature glochidia produced on that day within any of the treatments (control: War=16 = 0.1.143, P = 0.253; A: War=26 = 0.1.288, P = 0.198; B: War=26 = 0.012, P = 0.990; C: War=22 = 0.911, P = 0.362). The total number of immature or mature glochidia packages produced also did not differ between treatments (immature: H3,7 = 1.898, P = 0.594; mature: H3,7 = 0.6.167, P = 0.104). Total immature and mature glochidia observed as a function of water temperature are presented in Figure 3B. Immature glochidia were observed between 11.6[degrees]C and 19.0[degrees]C, whereas mature glochidia were observed between 15.3[degrees]C and 20.4[degrees]C.
The eastern elliptio Elliptio complanata collected from Pine
Creek, Tioga County, PA, cultured under natural water temperature and photoperiod conditions released mature glochidia in mid-June with rising temperatures between 16.6[degrees]C and 18.7[degrees]C and a photoperiod consisting of 15 h of daylight. Time period of reproductive activity can differ within species at varying locations. For example, E. complanata inhabiting
Ocqueoc Lake, MI, began releasing glochidia in late April, with maximum glochidial release around mid-May at a temperature of 20[degrees]C (Matteson 1948). Gravid E. complanata were observed from early May and late June in the Broad River, SC, between water temperatures of 19[degrees]C and 26[degrees]C; however, evidence of two brooding cycles was found in this drainage (Price & Eads 2011).
In this study, glochidial release of E. complanata reached its maximum at 18[degrees]C at 15 h of daylight.
Because photoperiod and water temperature were not independently manipulated, it is not possible to determine which variable had a greater influence on glochidia production during this study. Field investigations have found that both water temperature and photoperiod influence Elliptio complanata reproduction in the upper Susquehanna River; significant relationships between the timing of brooding glochidia and water temperature, accumulated thermal units, and photoperiod, along with air temperature and discharge, were found (Franzem et al. 2019). Although accumulated thermal units (a measure of cumulative thermal experience) was identified as the best predictor of E. complanata timing for brooding, some interactions with other variables and evidence that multiple environmental factors may be necessary to cue brooding were noted (Franzem et al. 2019). Similarly, Galbraith and Vaughn (2009) found temperature (accumulated degree days) and interactions between temperature, photoperiod, and food availability to influence timing and gamete development in three other species of freshwater mussels found in south central United States. Further studies are necessary to continue to investigate and independently manipulate these environmental cues in relation to freshwater mussel gamete development and spawning to fully understand which variables drive these processes. Studies are also needed to investigate which environmental variables would cause a single species to exhibit two brooding cycles in one geographic location (Price & Eads 2011) and only one cycle in other locations (present study, Franzem et al. 2019).
Prolonged winter conditions delayed reproduction proportional to the length of treatment, and slightly warmer winter conditions had a slight effect on the timing of larval release with no lag in the release of mature glochidia between the control and 10[degrees]C low treatments. Because of the present study's low sample size, statistical analysis could not be conducted on the timing of release. In the wild, shifts in glochidia production in response to shifting thermal conditions could negatively affect reproduction if host fish are no longer available. As systems fluctuate in response to climate change, streams and rivers may experience changing thermal conditions, and the potential effects on freshwater mussel reproduction warrant further investigation.
The current data indicate that the seasonal availability of
Elliptio complanata glochidia can be extended 3-fold using photoperiod and water temperature manipulation. Studies using the creeper Strophitus undulatus (Say, 1817) were successful in a 4-wk seasonal delay in glochidial release, indicating that this manipulation can be used with other species of mussels
(Van Snik Gray et al. 2002).
Manipulating temperature and photoperiod increased the time period between the release of immature and mature glochidia.
In the control and treatment C, mature glochidia were observed 5 and 7 (respectively) days after immature glochidia were initially released. This time delay increased to 18 and 26 days for the manipulated treatments. The release of immature glochidia has been noted in other mussel species, such as
Elliptio arca (Conrad, 1834) and Quadrula asperata (I. Lea, 1861), but is often associated with handling stress (Haag &
Warren 2003, Yeager & Neves 1986). Environmental stress, such as hypoxia, has also induced gill evacuation and the release of immature glochidia in Unio pictorum (Linnaeus, 1758) and
Unio tumidus (Retzius, 1788) (Aldridge & McIvor 2003).
Manipulating the environmental conditions during this study may have served as an unintentional stressor for the mussels, leading to early release of immature glochidia, and account for the observed delays; however, mussel survival was high in all treatments.
Results of this study demonstrate the ability to culture viable glochidia on a predictable schedule and the ability to prolong glochidia seasonal availability. Results also indicate the ability of freshwater mussels to adjust their reproductive activity, although with increased variability in the release of immature glochidia and timing of release, to slightly shifted seasonal temperatures and photoperiods. Simple temperature and photoperiod manipulation can aid in the propagation and research of freshwater mussels.
The authors thank C. Johnson for her assistance during the experiment, and H. Galbraith and D. Spooner for comments that greatly improved the quality of the manuscript. Any use of trade, product, or firm names is for descriptive purposes only and does not imply endorsement by the U.S. government.
Funding for this project was provided through the U.S. Geological
Survey Fisheries Program. Associated data for this project can be found online at https://doi.org/10.5066/P9PNY317.
Aldridge, D. C. & A. L. Mclvor. 2003. Gill evacuation and release of glochidia by Unio pictorum and Unio tumidus (Bivalvia: Unionidae) under thermal and hypoxic stress. J. Molluscan Stud. 69:55-59.
Allen, D. C. & C. C. Vaughn. 2011. Density-dependent biodiversity effects on physical habitat modification by freshwater bivalves.
Amyot, J.-P. & J. A. Downing. 1991. Endo- and epibenthic distribution of the unionid mollusc Elliptio complanata. J. N. Am. Benthol. Soc. 10:280-285.
Borcherding, J. 1995. Laboratory experiments on the influence of food availability, temperature and photoperiod on gonad development in the freshwater mussel Dreissena polymorpha. Malacologia 36:15-27.
Flippo, H. N., Jr. 1975. Temperatures of streams and selected reservoirs in Pennsylvania. Bulletin no. 11. Harrisburg, PA: Department of
Environmental Resources, Commonwealth of Pennsylvania. 95 pp.
Franzem, T. P., M. Kugler, R. LaRochelle, P. H. Lord, D. Stich & A.
M. Gascho Landis. 2019. Reproductive phenology of Elliptio complanata in an upper Susquehanna River tributary of New York.
Northeast. Nat. (Steuben) 26:119-128.
Gagne, F., M. Fournier & C. Blaise. 2004. Serotonergic effects of municipal effluents: induced spawning activity in freshwater mussels.
Fresenius Environ. Bull. 13:1099-1103.
Galbraith, H. S. & C. C. Vaughn. 2009. Temperature and food interact to influence gamete development in freshwater mussels. Hydrobiologia 636:35-47.
Haag, W. R. & M. L. Warren, Jr. 2003. Host fishes and infection strategies of freshwater mussels in large mobile basin streams, USA.
J. N. Am. Benthol. Soc. 22:78-91.
Lydeard, C., R. H. Cowie, W. F. Ponder, A. E. Bogan, P. Bouchet, S. A.
Clark, K. S. Cummings, T. J. Frest, O. Gargominy, D. G. Herbert, R. Hershler, K. E. Perez, B. Roth, M. Seddon, E. E. Strong & F. G.
Thompson. 2004. The global decline of nonmarine mollusks. Bioscience 54:321-330.
Matteson, M. R. 1948. Life history of Elliptio complanatus (Dillwyn, 1817). Am. Midl. Nat. 40:690-723.
McCall, P. L., M. J. S. Tevesz & S. F. Schwelgien. 1979. Sediment mixing by Lampsilis radiata siliquoidea (Mollusca) from western
Lake Erie. J. Great Lakes Res. 5:105-111.
Metcalfe, J. L. & M. N. Charlton. 1990. Freshwater mussels as biomonitors for organic industrial contaminants and pesticides in the
St. Lawrence River. Sci. Total Environ. 97-98:595-615.
Nalepa, T. F., W. S. Gardner & J. M. Malczyk. 1991. Phosphorus cycling by mussels (Unionidae: Bivalvia) in Lake St. Clair. Hydrobiologica 219:239-250.
Nedeau, E. J. 2008. Freshwater mussels and the Connecticut River
Watershed. Greenfield, MA: Connecticut River Watershed Council. pp. 84-85.
Negus, C. L. 1966. A quantitative study of growth and production of unionid mussels in the River Thames at Reading. J. Anim. Ecol. 35:513-532.
Price, J. E. & C. B. Eads. 2011. Brooding patterns in three freshwater mussels of the genus Elliptio in the Broad River in South Carolina.
Am. Malacol. Bull. 29:121-126.
Ram, J. L., G. W. Crawford, J. U. Walker, J. J. Mojares, N. Patel, P. P.
Fong & K. Kyozuka. 1993. Spawning in the zebra mussel (Dreissena polymorpha): activation by internal or external application of serotonin.
J. Exp. Zoo!. 265:587-598.
Ricciardi, A. & J. B. Rasmussen. 1999. Extinction rates of North
American freshwater fauna. Conserv. Biol. 13:1220-1222.
Ricciardi, A., R. J. Neves & J. B. Rasmussen. 1998. Impending extinctions of North American freshwater mussels (Unionoida) following the zebra mussel (Dreissena polymorpha) invasion. J. Anim.
Strayer, D. L., J. A. Downing, W. R. Haag, T. L. King, J. B. Layzer, T.
J. Newton & J. S. Nichols. 2004. Changing perspectives on pearly mussels, North America's most imperiled animals. Bioscience 54:429-439.
Strayer, D. L., D. C. Hunter, L. C. Smith & C. K. Borg. 1994. Distribution, abundance, and roles of freshwater clams (Bivalvia, Unionidae) in the freshwater tidal Hudson River. Freshw. Biol. 31:239-248. 384 BLAKESLEE AND LELLIS
Van Snik Gray, E., W. A. Lellis, J. C. Cole & C. S. Johnson. 2002. Host identification for Strophitus undulates (Bivalvia: Unionidae), the creeper, in the upper Susquehanna River basin, Pennsylvania Am.
Midl. Nat. 147:153-161.
Vaughn, C. C. & C. C. Hakenkamp. 2001. The functional role of burrowing bivalves in freshwater ecosystems. Freshw. Biol. 46:1431-1446.
Wacker, A. & E. von Elert. 2003. Food quality controls reproduction of the zebra mussel (Dreissena polymorpha). Oecologia 135:332-338.
Williams, J. D., M. L. Warren, Jr., K. S. Cummings, J. L. Harris &
R. J. Neves. 1993. Conservation status of freshwater mussels of the United States and Canada. Fisheries (Bethesda, Md.) 18:6-22.
Yeager, B. L. & R. J. Neves. 1986. Reproductive cycle and fish hosts of the rabbit's foot mussel, Quadrula cylindrical strigillata (Mollusca:
Unionidae) in the upper Tennessee River drainage. Am. Midl. Nat. 116:329-340.
CARRIE J. BLAKESLEE (*) AND WILLIAM A. LELLIS
U.S. Geological Survey, Leetown Science Center, Northern Appalachian Research Laboratory, 176 Straight Run Road, Wellsboro, PA 16901
(*) Corresponding author. E-mail: firstname.lastname@example.org
TABLE 1. Effect of environmental treatment on growth and survival of Elliptio complanata during the experimental study. Treatment Average ([+ or -]SE) Control A Initial length (mm) 96.8 ([+ or -]0.87) 97.2 ([+ or -]0.66) Final length (mm) 97.9 ([+ or -]0.87) 98.3 ([+ or -]0.65) Length change (mm) 1.1 ([+ or -]0.14) 1.0 ([+ or -]0.16) Initial weight (g) 95.6 ([+ or -]2.5) 97.1 ([+ or -]2.3) Final weight (g) 94 ([+ or -]2.4) 95.8 ([+ or -]2.3) Weight change (g) -1.6 ([+ or -]0.17) -1.3 ([+ or -]0.20) Survival (%) 97.8 ([+ or -]0.0) 100 ([+ or -]0.0) Treatment Average ([+ or -]SE) B C Initial length (mm) 95.1 ([+ or -]1.03) 96.6 ([+ or -]0.83) Final length (mm) 95.7 ([+ or -]1.04) 97.5 ([+ or -]0.84) Length change (mm) 0.61 ([+ or -]0.17) 0.91 ([+ or -]0.17) Initial weight (g) 91.1 ([+ or -]2.7) 96.0 ([+ or -]2.6) Final weight (g) 89.9 ([+ or -]2.7) 94.5 ([+ or -]2.5) Weight change (g) -1.2 ([+ or -]0.17) -1.6 ([+ or -]0.17) Survival (%) 96.7 ([+ or -]1.01) 98.9 ([+ or -]1.11) Average ([+ or -]SE) F[.sub.crit] P-value Initial length (mm) 2.63 0.33 Final length (mm) 2.63 0.17 Length change (mm) 2.63 0.17 Initial weight (g) 2.63 0.36 Final weight (g) 2.63 0.38 Weight change (g) 2.63 0.47 Survival (%) 6.59 0.14 Final length and weight over the 1-y study period differed significantly across treatments ([t.sub.df=358] = 1.97, P < 0.0001; [t.sub.df=358]= 1.97, P < 0.0001, respectively), but no significant differences were found between treatments in length, weight, changes in length and weight, or survival (ANOVA critical values given) during the study.
|Printer friendly Cite/link Email Feedback|
|Author:||Blakeslee, Carrie J.; Lellis, William A.|
|Publication:||Journal of Shellfish Research|
|Date:||Aug 1, 2019|
|Previous Article:||ITEROPARITY OR SEMELPARITY IN THE JUMBO SQUID DOSIDICUS GIGAS: A CRITICAL CHOICE.|
|Next Article:||OPTIMIZATION AND PHYSICOCHEMICAL CHARACTERIZATION OF CHITOSAN AND CHITOSAN NANOPARTICLES EXTRACTED FROM THE CRAYFISH PROCAMBARUS CLARKII WASTES.|