Freshwater polychaetes (Manayunkia speciosa) near the Detroit River, western Lake Erie: Abundance and life‐history characteristics

JGLR-01094; No. of pages: 14; 4C: Journal of Great Lakes Research xxx (2016) xxx–xxx

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Freshwater polychaetes (Manayunkia speciosa) near the Detroit River, western Lake Erie: Abundance and life‐history characteristics Don W. Schloesser a,⁎, David M. Malakauskas b, Sarah J. Malakauskas b a b

U.S. Geological Survey, Great Lakes Science Center, 1451 Green Road, Ann Arbor, MI 48105, USA Francis Marion University, P.O. Box 100547, Florence, SC 29502, USA

a r t i c l e

i n f o

Article history: Received 26 January 2016 Accepted 20 June 2016 Available online xxxx Communicated by Lee Grapentine Index words: Detroit River Polychaete Ecology Great Lakes Life history Annelid

a b s t r a c t Freshwater polychaetes are relatively rare and little-studied members of the benthos of lakes and rivers. We studied one polychaete species (Manayunkia speciosa) in Lake Erie near the mouth of the Detroit River. Abundances at one site were determined between 1961 and 2013 and life‐history characteristics at two sites were determined seasonally (March–November) in 2009–2010 and 2012–2013. Life‐history characteristics included abundances, length‐frequency distributions, presence/absence of constructed tubes, sexual maturity, and number and maturation of young of year (YOY) in tubes. Long-term abundances decreased in successive time periods between 1961 and 2003 (mean range = 57,570 to 2583/m2) but few changes occurred between 2003 and 2013 (mean = 5007/m2; range/y = 2355–8216/m2). Seasonal abundances varied substantially between sites and years, but overall, abundances were low in March–April, high in May–August, and low in September–November. Although reproduction was continuous throughout warmer months, en masse recruitment, as revealed by length–frequency distributions, occurred in a brief period late‐June to mid-July, and possibly in early-September. All life history characteristics, including tube construction, were dependent on water temperatures (N 5 °C in spring and b 15 °C in fall). These results generally agree with and complement laboratory studies of M. speciosa in the Pacific Northwest where M. speciosa hosts parasites that cause substantial fish mortalities. Although abundance of M. speciosa near the mouth of the Detroit River was 33-fold lower in 2013 than it was in 1961, this population has persisted for five decades and, therefore, has the potential to harbor parasites that may cause fish mortalities in the Great Lakes. Published by Elsevier B.V. on behalf of International Association for Great Lakes Research.

Introduction The freshwater polychaete, Manayunkia speciosa Leidy, is relatively rare and has a wide, but discontinuous geographic range throughout coastal areas of the United States, including the Laurentian Great Lakes (Pettibone, 1953; Hazel, 1966; Holmquist, 1967). While its geographic origin is unknown, it is generally believed that M. speciosa is native to the eastern United States and that this taxon is a freshwater relic, separated from ancestral marine populations by geologic and climatic events (Croskery, 1978). M. speciosa was previously believed to be limited to a Nearctic distribution, but a recent discovery of it in the Uruguay River, South America, has expanded the range of this polychaete (Armendariz et al., 2011). This recent increase in geographic distribution of M. speciosa has been speculated to be a result of invasions mediated by shipping canals and ballast-water discharges (Meehean, 1929; Brehm, 1978; Armendariz et al., 2011). Several species of freshwater polychaetes have been introduced into new habitats as a result

⁎ Corresponding author. E-mail address: [email protected] (D.W. Schloesser).

of human activities, including M. speciosa in the Great Lakes (Glasby and Timm, 2008; Schloesser, 2013). Historically, M. speciosa has been a relatively little-studied taxon, likely because it is inconspicuous in benthic samples (Pettibone, 1953; Holmquist, 1967) and typically comprises b 1% of the total benthos (e.g., Malakauskas and Wilzbach, 2012; Schloesser, 2013). However, discovery that M. speciosa is an intermediate host for two myxozoan parasites (Ceratonova shasta Noble and Parvicapsula minibicornis Kent) (Bartholomew et al., 1997, 2006) that can cause substantial mortalities (e.g., 40%) of juvenile chinook salmon (Oncorhynchus spp.; Foott et al., 1999, 2004) in the Pacific Northwest has sparked interest in the general ecology of this polychaete. Additionally, it was recently reported that M. speciosa hosts two additional parasites in Lake Erie, including an undescribed species of Ceratonova (Malakauskas et al., 2015, 2016). While some studies contain information on the distribution of M. speciosa (e.g., Hiltunen, 1965; Poe and Stefan, 1974; Willson et al., 2010), relatively little is known about patterns in its temporal abundances and seasonal life history characteristics. For example, most studies of this taxon only reported the presence and anecdotal observations of life history characteristics (e.g., Hazel, 1966; Holmquist, 1967; Spencer, 1976). To date, the most detailed studies of

http://dx.doi.org/10.1016/j.jglr.2016.07.006 0380-1330/Published by Elsevier B.V. on behalf of International Association for Great Lakes Research.

Please cite this article as: Schloesser, D.W., et al., Freshwater polychaetes (Manayunkia speciosa) near the Detroit River, western Lake Erie: Abundance and life‐history characteristics, J. Great Lakes Res. (2016), http://dx.doi.org/10.1016/j.jglr.2016.07.006

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D.W. Schloesser et al. / Journal of Great Lakes Research xxx (2016) xxx–xxx

abundance and distribution of this taxon are for populations in the Klamath River in the Pacific Northwest (Stocking and Bartholomew, 2007) and for populations in the Laurentian Great Lakes (Schloesser, 2013). In the Klamath River, M. speciosa occurs in both lentic and lotic habitats, with the most stable populations present near river mouths that empty into reservoirs. Typically, this taxon is absent from main areas of reservoirs and is primarily confined to the main-river stem including runs, pools, and riffles (Stocking and Bartholomew, 2007). It has been suggested that the primary habitat for this taxon is in areas of high stability, such as in stands of filamentous algae, boulders, and behind rock outcroppings because it appears this taxon is readily entrained in substrates that are displaced by flow-mediated disturbance (Stocking and Bartholomew, 2007; Malakauskas and Wilzbach, 2012; Malakauskas et al., 2013). The occurrence of M. speciosa in the Great Lakes, with emphasis on populations in western Lake Erie, was reviewed by Schloesser (2013). In brief, M. speciosa was first found in two harbors of the Great Lakes in 1929 and 1936 (Meehean, 1929; Krecker, 1939). In western Lake Erie, no individuals were found in the 1930s, rather it was found 30 years later in 1961 when it was found to be the second most abundant benthic taxon (Hiltunen, 1965). No records of M. speciosa occurred in this 30 year period, probably because no open-water surveys were conducted, and its small size may have prevented its collection and identification in nearshore areas where a few smallbenthic surveys were performed. The population of M. speciosa then decreased in abundance in successive sampling periods of 1982, 1993, and 2003 (Schloesser, 2013). Between 1961 and 2003, M. speciosa was primarily distributed and most abundant near the mouth of the largest tributary of Lake Erie–the Detroit River. Because this taxon was not found prior to the late-1920s and it has a discontinuous distribution in the Great Lakes, it has been identified as an exotic species (Krecker, 1939; Hiltunen, 1965; Schloesser, 2013). However, M. speciosa in the Great Lakes may have simply been too rarely found to establish its occurrence and, in addition, its small size could explain why it was not reported in the early- to mid-1900s. Therefore, because some study methods may not have been adequate to retain and enumerate this taxon, it is possible that this taxon is not exotic but simply was not found and identified in early benthic work in the Great Lakes (reviewed by Schloesser, 2013). The present study was undertaken to determine long-term temporal abundances (1961–2013) and seasonal life‐history characteristics (2009–2010 and 2012–2013) of M. speciosa near the mouth of the Detroit River, western Lake Erie. Study sites near the mouth of the Detroit River were selected because this taxon has become increasingly difficult to find in the Great Lakes, including western Lake Erie and several other areas, where it was once common in the 1970s (Hiltunen, 1969; Hiltunen, 1971; Hiltunen and Manny, 1982; Schloesser, 2013). In addition, we examined life‐history characteristics of this taxon because little is known about its life‐history, especially in wild populations (Willson et al., 2010; Alexander et al., 2014). Methods Abundance of Manayunkia speciosa was examined at one site (15D, 42o 02.000′ N, 83o 09.100′ W; Carr and Hiltunen, 1965) in 1961, 1982, 1993, 2003, 2004, 2008, 2009, 2010, and 2013 (Fig. 1). This site was selected because it is a place where M. speciosa was most abundant in western Lake Erie in 1961, 1982, 1993, and 2003 (Hiltunen, 1965; Schloesser, 2013). In addition, changes in seasonal abundances and life-history characteristics of this taxon were examined at site 15D in 2009 and 2010. However, since M. speciosa occurred at relatively low abundances at site 15D, this caused discontinuous length– frequency distributions, so another site (site 111; 42o 02.086′ N, 83o09.058′ W) with higher densities of this taxon was sampled in 2012 and 2013. This second site was 0.3 km southwest of site 15D.

Collection and analysis methods used to obtain long-term abundances of M. speciosa at site 15D were consistent and comparable to those used in long-term temporal studies of western Lake Erie (Schloesser, 2013). Detailed methods can be found in Carr and Hiltunen (1965), Schloesser et al. (2000), and, specifically for M. speciosa in Schloesser (2013). In brief, samples were collected for long-term temporal studies with a Peterson sampler in 1961 and a Ponar sampler in 1982–2013. A Peterson to Ponar conversion factor allowed direct comparison of abundances between the Peterson- and Ponar-sampling periods (Schloesser, 2013). For each temporal period, three individual samples were collected, washed over a standard sieve (ca. 0.56 mm), and individually preserved in 10% formalin. In the laboratory, samples were washed over a 0.25 mm sieve, and M. speciosa (Fig. 2) were examined at 7× magnification. Seasonal abundances and life‐history characteristics of M. speciosa were obtained from a total of 42 sampling periods in ice-free seasons at site 15D in 2009–2010 (n = 16) and at site 111 in 2012–2013 (n = 26). Methods of collection and examination were similar to methods used to obtain long-term abundances, except samples were collected with a petite Ponar and rose bengal was added to the 10% formalin preservative. In 2009, 6 sample collections were obtained between 15 June and 23 November; in 2010, 10 collections between 10 May and 23 October; in 2012, 10 collections between 11 May and 22 October; and in 2013, 16 collections were obtained between 14 March and 22 November. Individual M. speciosa were enumerated and measured to the nearest 0.1 mm and categorized as not in tube, in tube without brooding young-of-the-year (YOY), and in tube with YOY (Fig. 2). In addition, tubes that contained YOY without a larger individual were enumerated. These categories were obtained from one individual sample replicate and occasionally from additional samples in attempts to obtain more individuals for greater discrimination of length–frequency distributions. Visual inspection of length–frequency distributions was performed to separate cohorts/age classes of M. speciosa. Developmental stages of YOY in tubes were obtained from YOY in randomly selected tubes that contained adults and YOY from site 15D in 2009 and site 111 in 2012. Individual YOY were examined at 60 × magnification and classified by life stage based on Willson et al. (2010). Life stage designations of Willson et al. (2010) were modified for this study as follows: 1) stages one and two were combined into one category because deformation of embryos was caused by the formalin-based fixative, and 2) stages four and five were combined into one category because movement of live YOY is necessary to separate these stages. Therefore, in the present study, the three YOY categories include egg/embryo, larva, and subjuvenile. Sex determinations of individual M. speciosa were obtained from site 15D in 2009 and site 111 in 2012. When possible, 100 individuals in tubes were randomly selected and examined for each sample date. For samples that contained fewer than 100 adults, all adults were examined. Because individuals were stained with rose bengal, individuals were ‘destained’ using several changes of 95% ethanol to allow sex determination. Sexual maturity was determined only for intact, undamaged individuals at 100 × to 400 × magnification. Some individuals appeared to have disintegrated reproductive tissue and could not be reliably separated from individuals with immature reproductive structures. Thus, individuals with disintegrated reproductive tissues were classified as immature. An additional set of 100 individuals were selected from 25% of samples and examined to ensure consistent results. Taxonomic identifications were based primarily on presence of tentacles on the anterior end of individuals. This feature is easily visible in individuals not designated as YOY. Verification of species was based on preliminary molecular data (Malakauskas et al., 2016) and information obtained from an ongoing genetic review of the genus (personal communication, G. Rouse, Scripps Institution of Oceanography, University of California–San Diego, La Jolla, CA).

Please cite this article as: Schloesser, D.W., et al., Freshwater polychaetes (Manayunkia speciosa) near the Detroit River, western Lake Erie: Abundance and life‐history characteristics, J. Great Lakes Res. (2016), http://dx.doi.org/10.1016/j.jglr.2016.07.006

D.W. Schloesser et al. / Journal of Great Lakes Research xxx (2016) xxx–xxx

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Fig. 1. Locations of sites 15D (upper right dot) and 111 (lower left dot) where collections of Manayunkia speciosa were made near the mouth of the Detroit River in western Lake Erie (insert of Great Lakes) 1961–2013. Grey lines are relative depth contours. Shipping channels are in light grey shading.

Information on habitat characteristics was obtained at site 15D in July 2010 and site 111 in August 2012. At site 15D, SCUBA was used to visually describe structural relief features and collect 5-cm-diameter core samples of surface sediment in areas of different structural relief (i.e., n = 15 in flat-smooth areas and n = 15 in depressions). Temperature data were obtained from the Great Lakes Average GLSEA Surface Water Temperature on-line (http://coastwatch.glerl.noaa.gov/statistic/ avg-sst.php?lk=g&yr=2013). Long-term abundance data were square-root transformed to meet assumptions of normality and were analyzed using a General Linear Model ANOVA. A Tukey–Kramer post hoc test was used to test pairwise significance. A Spearman rank test was used to evaluate correlations between temperature and either percentage of adults with YOY in tubes or percentage of individuals in tubes for the 2013 sampling year, which had the most complete data. A t-test was used to compare abundance of individuals inside and outside of substrate depressions. Results Abundances Long-term abundances of Manayunkia speciosa decreased at site 15D near the mouth of the Detroit River in western Lake Erie between 1961 and 2013 (Table 1). Substantial decreases occurred in successive sampling periods over the first four decades of time (1961–2003), including a 15% decrease of densities between 1961 and 1982, a 2-fold decrease between 1982 and 1993, and a 10-fold decrease of densities between 1993 and 2003. After 2003, relatively low and stable densities occurred through 2013. Overall, mean densities significantly decreased from 57,570 individuals/m2 in 1961 to 4222/m2 in 2013 (ANOVA, P b 0.01, F(8,18) = 7.15), a 14-fold decrease. Significant differences occurred between densities in 1961 and all years except 1982 and 1993 and between 1982 and all years except 1961, 1993, and 2004 (Tukey–Kramer, P b 0.05). Changes in seasonal abundances indicated large differences between populations of M. speciosa at two relatively close sites (15D

and 111, ca. 0.3 km apart) (Fig. 3, Electronic Supplementary Material (ESM) Table S1). In addition, two observations at site 15D in 2009 and 2010 also raised concern about the adequacy of quantitative population estimates. First, in fall 2009, an unexpected small increase in densities occurred between 23 October and 23 November (Fig. 3). Second, in spring 2010, there was no observed YOY recruitment as found in spring 2009 and relatively small increases in densities also occurred in fall 2010. Our assessment was that too few individuals were collected to discern seasonal abundances and life‐history patterns at site 15D in 2009 and 2010. Therefore, another site (111, Fig. 1) with greater densities was sampled in 2012 and 2013 (Fig. 3, ESM Table S1). Site 111 was found to have 10- to 40-fold greater densities (range = 9892 to 89,904 individuals/m2) of M. speciosa than site 15D. Abundances at site 111 yielded more consistent and discernable seasonal patterns of abundance, typical of a benthic organism in temperate latitudes (i.e., increases in warmer months of the year). Overall coefficient of variation of three replicate samples per date at site 15D in 2009 and 2010 was higher (mean = 31% and 27%, respectively) than variability at site 111 in 2012 and 2013 (mean = 18% and 21%, respectively). Overall, abundances were higher in warmer months than in colder months of the year. Life-history Life‐history characteristics of 26,207 M. speciosa specimens were examined (ESM Table S2). Of the total 26,207 individuals, 12,060 (46%) were not in tubes and 14,147 (54%) were in individual tubes. Of the 14,147 individuals in tubes, 10,302 (73%) occurred in tubes without young-of-the-year (YOY) and 3875 (27%) occurred in tubes with YOY. Only 412 tubes (3% of 14,147 tubes with individuals) were found to contain YOY but no adult. Length–frequency distributions of M. speciosa at two sites over 4 years (Figs. 4–7, ESM Table S2) revealed: 1) lengths of individuals ranged between 0.5 and 4.6 mm; 2) unimodal distributions (33 of 42) occurred primarily in spring (March to early June), summer (late‐July to August), and fall (September to November); 3) bimodal distributions (9 of 42) occurred in late spring and early summer (17 June to 16 July); 4) mean

Please cite this article as: Schloesser, D.W., et al., Freshwater polychaetes (Manayunkia speciosa) near the Detroit River, western Lake Erie: Abundance and life‐history characteristics, J. Great Lakes Res. (2016), http://dx.doi.org/10.1016/j.jglr.2016.07.006

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D.W. Schloesser et al. / Journal of Great Lakes Research xxx (2016) xxx–xxx

Fig. 2. Individual Manayunkia speciosa (a) not in a tube, (b) in a tube with young-of-theyear (YOY, oblong balls at the posterior end of tube), and (c) female and YOY removed from a tube.

Table 1 Densities (number/m2 ± SE) and percent coefficient of variations (CV) of three replicate samples of Manayunkia speciosa at site 15D near the mouth of the Detroit River in western Lake Erie 1961–2013. Date 1961 1982 1993 2003 2004 2008 2009 2010 2013

(13 June) (10 June) (11 June) (29 April) (3 May) (8 April) (17 April) (30 March) (14 March)

Sample A

Sample B

Sample C

Mean

SE

% CV

36,612 37,191 38,883 2087 11,632 9256 5372 2541 4318

112,078 74,195 6788 5351 6983 14,235 3843 2252 4421

24,021 37,459 30,326 310 6033 103 5186 2273 3925

57,570 49,615 25,332 2583 8216 7865 4800 2355 4222

27,495.1 12,290.4 9595.5 1476.2 1729.8 4138.3 481.6 93.2 151.0

83 43 66 99 36 91 17 7 6

lengths of individuals with unimodal distributions were higher immediately before occurrence of bimodal distributions; 5) YOY were uncommon to absent in early‐spring (March‐May) and late‐fall (late‐October to November); 6) YOY were only found in tubes with individuals N1.3 mm; and 7) most to all length classes of adults N 1.3 mm contained YOY, except at site 15D, which exhibited discontinuous length distributions probably as a result of low numbers of measured individuals (n = 28–398 individuals per period) in July through October. Abundance increases attributed to en masse reproduction were most discernable at site 111 in 2013 which had the highest densities and greatest sampling frequency (n = 16, Fig. 7). At this site, YOY production was evident when relatively small individuals entered the population as exhibited by small-length groups on 17 June, 24 June, 8 July, and 16 July. This YOY recruitment group was no longer observed by 25 July. In addition, a few YOY individuals may have been recruited and visible in length–frequency distributions as evidenced as possible bimodal curves on 4 and 17 September 2013. Although not as continuous as at site 111 in 2013, similar bimodal peaks in abundances attributed to en masse reproduction also occurred in summers at site 15D on 9 July 2009, 1 July 2010, and at site 111 on 27 June 2012 (Figs. 4–6). Overall, length–frequency distributions (above), sexual maturity of adults in tubes, presence/absence of YOY in tubes, numbers of YOY in tubes, proportions of individuals in tubes (rs(14) = 0.67, P = 0.0044; rs(14) = 0.58, P = 0.018, respectively), and development stages of YOY in tubes indicated reproduction and tube construction was initiated as water temperatures increased in May, continued through summer, and declined as temperatures began to decrease in late‐ September (Tables 2 and 3, Figs. 3, 8 and 9). At site 15D in 2009, the proportion of sexually mature adults was low in April (58%), increased in June (99%), and decreased in August (51%) (Table 2). At site 111 in 2012, proportions of mature adults were high in May (88%) and June (90%), decreased and remained relatively low between June (61%) and early‐September (62%), and decreased substantially in late September (21%) and early‐November (5%) when temperatures approached 12 °C. Overall, males appeared to become sexually mature earlier in the spring than females, and females appeared to remain sexually mature longer into fall than males. For all 4 years, YOY were absent in colder-sampling periods 14 March to 17 April (n = 3 periods) and 15 September to 23 November (n = 5 periods) and present in warmersampling periods 10 May–22 October (n = 34 periods) (Figs. 4–7). At site 111 in 2013, temperatures were b5 °C in three sampling periods March and April when no YOY individuals were found in tubes (Fig. 8, Table 2, ESM Table S2). As temperatures increased April to mid-May (4–10 °C) and mid-May to mid-June (10–16 °C), percent individuals with YOY in tubes increased from 0 to 10% and 10% to 40%, respectively. Between mid-June and mid-July, when water temperatures ranged between 16 and 23 °C, proportions of tubes with YOY ranged between 40% and 46%. After mid-July, presence of YOY declined from 40% to 30% in mid-September and to 0% in early‐November. Although to a lesser extent than the YOY pattern, proportions of adults in tubes paralleled seasonal temperatures at site 111 in 2013 (Figs. 3 and 8, ESM Table S2). As temperatures increased in spring, the proportion of adults in tubes increased from 7% in mid-March to 86% in mid-June. After mid-June, proportions in tubes remained relatively stable at between 54% and 68% between late‐June and mid-September. As temperatures declined in fall between mid-September and late‐November, proportions of adults in tubes declined from 54% to 8% (Fig. 3). In addition to regulation of YOY production and tube construction (above), mean and maximum numbers of YOY per tube were lower in colder months before May and after September than in warmer months of the year (Table 3). Similarly, YOY development stages indicated that YOY in mid-May were exclusively eggs/embryos which indicated initiation of seasonal reproduction (Fig. 9). Proportions of YOY development stages were relatively consistent in summer between mid-June and mid-September but by late‐September, proportions of mature stages (i.e., larva and subjuvenile) began to increase and by late‐October, as

Please cite this article as: Schloesser, D.W., et al., Freshwater polychaetes (Manayunkia speciosa) near the Detroit River, western Lake Erie: Abundance and life‐history characteristics, J. Great Lakes Res. (2016), http://dx.doi.org/10.1016/j.jglr.2016.07.006

D.W. Schloesser et al. / Journal of Great Lakes Research xxx (2016) xxx–xxx

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Fig. 3. Mean numbers (number/m2 ± SE) of Manayunkia speciosa (A) and surface temperatures (B) at site 15D June 2009 to October 2010 and at site 111 (numbers = C, temperatures = D) May 2010 to November 2013.

Fig. 4. Length–frequency distributions and mean lengths (±SE) of distinguishable length groups of Manayunkia speciosa at site 15D near the mouth of the Detroit River in western Lake Erie 15 June to 23 November 2009. Dark bars are length categories where one or more individuals occurred in a tube with young-of-the-year (YOY). Arrows indicate visual separation of length groups indicative of YOY recruitment.

Please cite this article as: Schloesser, D.W., et al., Freshwater polychaetes (Manayunkia speciosa) near the Detroit River, western Lake Erie: Abundance and life‐history characteristics, J. Great Lakes Res. (2016), http://dx.doi.org/10.1016/j.jglr.2016.07.006

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D.W. Schloesser et al. / Journal of Great Lakes Research xxx (2016) xxx–xxx

Fig. 5. Length–frequency distributions and mean lengths (±SE) of distinguishable length groups of Manayunkia speciosa at site 15D near the mouth of the Detroit River in western Lake Erie 10 May to 22 October 2010. Dark bars are length categories where one or more individuals occurred in a tube with young-of-the-year (YOY). Arrows indicate visual separation of length groups indicative of YOY recruitment.

water temperatures approached 15–10 °C, subjuveniles dominated proportions of YOY in tubes. Although the smallest adult individual in a tube with YOY was 1.3 mm (Fig. 7, 9 August 2013), mean lengths of individuals with YOY in tubes ranged between 1.99 and 2.65 mm per samplng period and were higher than mean lengths of individuals without YOY in tubes for all sampling periods (Table 3). Habitat Petite Ponar samples, sediment core samples, and SCUBA observations at site 15D indicated surface substrates consisted of silt and fine sand (1–3 cm depth) with minimal relief, except for small half-moon depressions (7–15 cm diameter and depth) that were randomly spaced at 1–2 m intervals. Abundances (mean ± SE, range in parentheses) of M. speciosa obtained by SCUBA inside and outside of substrate depressions at site 15D were 5.53 ± 1.218 (0–16) individuals and 3.87 ± 0.716 (0–8) individuals, respectively. Differences between mean abundances of M. speciosa inside and outside substrate depressions were not significant (P N 0.05, df = 28). At site 111, most petite Ponar samples (ca., 90%) indicated that surface substrates were also

composed of silt and fine sand. However, some petite Ponar samples at site 111 (ca. 10%) contained small irregular-shaped gravel (1–3 cm diameter) with little silt and fine sand. Discussion To date, this is the most thorough study of abundances and seasonal life history characteristics of Manayunkia speciosa outside a laboratory. Direct comparison of the present study with other studies was limited because of the lack of previous studies of this taxon. Therefore, we primarily used laboratory data of M. speciosa collected from the Klamath River of the Pacific Northwest and data for natural populations of other close congeneric taxa for comparisons in the present study Abundance Abundances of M. speciosa at site 15D between 1961 and 2013 closely parallel historic abundances of this taxon in western Lake Erie as reviewed by Schloesser (2013). In brief, biologists were surprised in 1961 when this taxon was the second most abundant and widespread

Please cite this article as: Schloesser, D.W., et al., Freshwater polychaetes (Manayunkia speciosa) near the Detroit River, western Lake Erie: Abundance and life‐history characteristics, J. Great Lakes Res. (2016), http://dx.doi.org/10.1016/j.jglr.2016.07.006

D.W. Schloesser et al. / Journal of Great Lakes Research xxx (2016) xxx–xxx

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Fig. 6. Length–frequency distributions and mean lengths (±SE) of distinguishable length groups of Manayunkia speciosa at site 111 near the mouth of the Detroit River in western Lake Erie 11 May to 22 October 2012. Dark bars are length categories where one or more individuals occurred in a tube with young-of-the-year (YOY). Arrows indicate visual separation of length groups indicative of YOY recruitment.

taxon in western Lake Erie because it had not been found there before (Hiltunen, 1965). Invasion and colonization by this taxon probably began in the mid-1930s when a few individuals were found 70 km east of the mouth of the Detroit River (Krecker, 1939). After 1961, long-term decreases in abundances occurred across much of the western portion of western Lake Erie (Schloesser, 2013). Causes for decreased abundances of M. speciosa at site 15D near the mouth of the Detroit River in western Lake Erie between 1961 and 2011 are unknown because little information exists about environmental requirements of this taxon (Mackie and Qadri, 1971; Poe and Stefan, 1974). To date, two hypotheses have been suggested for decreases in abundances; the first is a reduction of nutrient concentrations (Schloesser, 2013). It has been proposed that M. speciosa is an indicator of moderate-organic pollution (Poe and Stefan, 1974), but intolerant of severe pollution (Mackie and Qadri, 1971), including toxicants (Burt et al., 1991). In accord with these findings, Stocking and

Bartholomew (2007) reported an absence of M. speciosa from anoxic sediments in the Klamath River, California. However, other authors have also suggested that nutrients may actually enhance abundances of M. speciosa. For example, greater abundances of M. speciosa in the lower Klamath River are coincident with a greater availability of fixed nitrogen and a greater overall abundance of suspension feeders (Malakauskas and Wilzbach, 2012). In the St. Marys River of the Great Lakes, M. speciosa was found to be a dominant invertebrate in benthic assemblages in pollution-impacted sites, including those downstream of sewage treatment plants, and generally only absent in areas with toxicants (Burt et al., 1991). Indirect evidence for effects of nutrients on M. speciosa is found in studies of a congener, Manayunkia aestuarina, which is reported to be an opportunistic and pollution-tolerant species (McLusky et al., 1980). For example, populations of M. aestuarina increased in abundance from 250,000 m− 2 in 1980 to over 3 million m−2 in a period of 15 months in a heavily polluted area in the Forth

Please cite this article as: Schloesser, D.W., et al., Freshwater polychaetes (Manayunkia speciosa) near the Detroit River, western Lake Erie: Abundance and life‐history characteristics, J. Great Lakes Res. (2016), http://dx.doi.org/10.1016/j.jglr.2016.07.006

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D.W. Schloesser et al. / Journal of Great Lakes Research xxx (2016) xxx–xxx Table 2 Total percentages of sexually mature and percentages of male and female of total sexually mature Manayunkia speciosa near the mouth of the Detroit River in western Lake Erie 2009 and 2012. Numbers of examined individuals in parentheses. Total sexually mature

Fig. 7. Length–frequency distributions and mean lengths (±SE) of distinguishable length groups of Manayunkia speciosa at site 111 near the mouth of the Detroit River in western Lake Erie 14 March to 22 November 2013. Dark bars are length categories where one or more individuals occurred in a tube with young-of-the-year (YOY). Arrows indicate visual separation of length groups indicative of YOY recruitment.

Estuary, United Kingdom (Bagheri and McLusky, 1982). In addition, M. aestuarina was the only taxon to exhibit significant positive response to increased nutrient enrichment which suggests that this polychaete may be more sensitive to pollution than many other benthic taxa (Mitwally and Fleeger, 2013).

Site 15D—2009 16 April (280) 15 June (153) 19 August (100)

58% (162) 99% (151) 51% (51)

Site 111—2012 11 May (104) 15 June (100) 27 June (100) 11 July (100) 26 July (100) 8 August (104) 22 August (100) 11 September (100) 24 September (100) 22 October (100)

88% (92) 90% (90) 61% (61) 60% (60) 72% (72) 70% (73) 78% (78) 62% (62) 21% (21) 5% (5)

Sexually mature Males

Females

72%

28%

45%

55%

57%

43%

55%

45%

44%

56%

49%

51%

38%

62%

57%

43%

52%

48%

36%

64%

52%

48%

57%

43%

20%

80%

Decreases in abundance of M. speciosa near the Detroit River followed decreases of organic pollution in Lake Erie between the 1960s and 2000s (Jimenez et al., 2011; Soster et al., 2011). Overall, nutrient status of western Lake Erie shifted from eutrophic waters in the 1950s, to mesotrophic, and in some areas, to oligotrophic waters in the early 2000s (Wright and Tidd, 1933; Beeton, 1965; Makarewicz, 1993; Fitzpatrick et al., 2007). Moreover, declines in M. speciosa in the 1960s through the 1980s are coincident with marked reduction in total phosphorus near the Detroit River (Manny et al., 1988). The second hypothesis to explain decreases in abundance of M. speciosa and other benthic organisms in Lake Erie is competition for food by exotic dreissenid mussels (Dreissena polymorpha and D. bugensis) introduced into the Great Lakes in the mid-1980s (Nalepa and Schloesser, 1993; Stewart and Haynes, 1994; Haynes, 1997). However, to date, both increases and decreases of M. speciosa have been associated with colonization by dreissenid mussels (Haynes, 1997; Howell et al., 1996; Strayer and Smith, 2001; Dermott and Geminiuc, 2003). In the present study, near the mouth of the Detroit River and much of western Lake Erie, decreases in abundance of M. speciosa began before dreissenid mussels invaded and colonized (i.e., 1961–1982) the Great Lakes in the mid-1980s (Nalepa and Schloesser, 1993; Schloesser, 2013). Therefore, it is not likely dreissenid mussels were a major factor in decreases of abundances of M. speciosa in western Lake Erie, at least before the mid-1980s. Reasons why M. speciosa continues to persist at sites 15D and 111 near the mouth of the Detroit River and not at other areas throughout western Lake Erie are unknown. This taxon has disappeared from over 80% of the area where it was once found in western Lake Erie (Schloesser, 2013). Speculation is that persistent populations may be attributed to a combination of feeding requirements and abiotic factors, such as water currents. This taxon is considered to be a suspension feeder, and while it has been proposed that it feeds on substrates (Lewis, 1968), substrate feeding has not been demonstrated. In addition, occurrence of M. speciosa in discontinuous patches indicates it

Please cite this article as: Schloesser, D.W., et al., Freshwater polychaetes (Manayunkia speciosa) near the Detroit River, western Lake Erie: Abundance and life‐history characteristics, J. Great Lakes Res. (2016), http://dx.doi.org/10.1016/j.jglr.2016.07.006

D.W. Schloesser et al. / Journal of Great Lakes Research xxx (2016) xxx–xxx

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Table 3 Mean lengths (± SE) of adult Manayunkia speciosa without and with young-of-the-year (YOY) in tubes, and mean and maximum numbers of YOY in tubes near the mouth of the Detroit River in western Lake Erie 2013. Numbers of examined individual in parentheses. Mean length (mm) of adults without YOY in tubes 14 March 3 April 17 April 16 May 11 June 17 June 24 June 3 July 8 July 16 July 25 July 9 August 15 August 4 September 17 September 5 November 22 November

1.97 ± 0.056 (37) 1,82 ± 0.031 (134) 1.94 ± 0.033 (93) 2.01 ± 0.020 (310) 2.11 ± 0.016 (476) 2.34 ± 0.019 (366) 2.11 ± 0.034 (283) 2.57 ± 0.052 (121) 2.13 ± 0.050 (92) 1.90 ± 0.036 (235) 1.62 ± 0.027 (227) 1.56 ± 0.012 (935) 1.79 ± 0.015 (460) 1.80 ± 0.014 (1299) 1.55 ± 0.017 (792) 1.90 ± 0.253 (171) 1.88 ± 0.066 (23)

Mean length (mm) of adults with YOY in tubes

Mean number of YOY per tube

Maximum number YOY per tube

(0) (0) (0) 2.31 ± 0.039 (34) 2.29 ± 0.016 (318) 2.50 ± o.016 (317) 2.38 ± 0.021 (193) 2.65 ± 0.044 (84) 2.33 ± 0.039 (62) 2.30 ± 0.035 (95) 1.85 ± 0.035 (94) 1.88 ± 0.017 (251) 2.06 ± 0.027 (112) 2.1 ± 0.096 (499) 1.99 ± 0.014 (332)

1.5

3

7.0

21

7.8

20

6.2

17

6.2

16

5.9

16

5.9

18

4.3

14

3.4

11

2.3

7

4.3

14

3.8

14

(0) (0)

may principally be a suspension feeder as substrate feeders typically show negative correlations with substrate patches and often exhibit territoriality (Zettler and Bick, 1996). Abundances in core samples from site 15D indicate no preference by this taxon to occur inside and outside substrate depressions. Therefore, it is likely the availability of suspended food particulates in water of the Detroit River is more important than substrate composition to populations of M. speciosa. Similarly, abundances of other suspension feeders is known to be dependent on water carried food materials (Richardson and MacKay, 1991). Interestingly, in Lake St. Clair, located immediately upstream of the Detroit

River, M. speciosa was found at several sites in the late‐1970s, but these populations were absent in 2012 (unpub. data, D.W. Schloesser; Schloesser, 2013). Speculation is that M. speciosa persists near the Detroit River because of decreased water velocity near the mouth of the river which could increase food delivery to benthic fauna. In addition, turbulent currents caused by storms over Lake Erie may re-suspend particles from substrates and provide this taxon with food. Sediment resuspension has been proposed as one mechanism that may allow indirect suspension feeding of settled materials (Lick et al., 1995). Riverestuary interfaces have been shown to support robust populations of

Fig. 8. Percentages of Manayunkia speciosa in tubes and in tubes with YOY and surface water temperature and at site 111 near the mouth of the Detroit River 14 March to 22 November 2013.

Please cite this article as: Schloesser, D.W., et al., Freshwater polychaetes (Manayunkia speciosa) near the Detroit River, western Lake Erie: Abundance and life‐history characteristics, J. Great Lakes Res. (2016), http://dx.doi.org/10.1016/j.jglr.2016.07.006

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D.W. Schloesser et al. / Journal of Great Lakes Research xxx (2016) xxx–xxx

Fig. 9. Proportions of development stages of young-of-the-year Manayunkia speciosa and surface water temperatures (dashed line) at site 111 near the mouth of the Detroit River in western Lake Erie 11 May to 22 October 2012.

suspension feeders in other systems (Bate et al., 2002). Moreover, sponges and bryozoans were occasionally found in samples with M. speciosa which suggests that the mouth of the Detroit River is suitable for other suspension feeders. We also note that M. speciosa has been found in association with sponges in the Klamath River (Stocking and Bartholomew, 2007; Malakauskas and Wilzbach, 2012) and a congeneric, M. baicalensis, has been found near the freshwater sponge, Lubomirskia baicalensis, in Lake Baikal (Kamaltynov et al., 1993). Thus, adequate suspended food is likely one determinant of abundance for M. speciosa near the mouth of the Detroit River. Zettler and Bick (1996) studied mesoscale dispersion of the suspension-feeding polychaete, Marenzelleria viridis, and found the local distribution of this taxon was probably due to sediment structure and relief. Direct SCUBA observations at site 15D indicated that substrates were primarily of silt and fine sand (1–2 cm thick) over coarse sand and small gravel intermixed with semi-circle depressions (10–20 cm diameter) of similar composition. This bottom topography may explain greater patchiness in distribution of M. speciosa at site 15D relative to site 111, although we have no direct observations of substrates at site 111. Pudovkina et al. (2016) suggested that substrates were an important factor in speciation of Manayunkia in eastern Russia, with different species exhibiting fidelity to particular substrate compositions. Zettler and Bick (1996) found M. viridis on slight elevations of 5–10 cm, though they could not say if these elevations were formed by currents. Other investigators have noted greater abundances of freshwater macroinvertebrates on crests of substrate elevations formed by currents (Blettler et al., 2010). Determination of seasonal abundances is one key component to assess life history characteristics of wild populations of M. speciosa and many other benthic organisms. For example, densities and their associated measure of dispersion (i.e., SE and CV) at site 15D in 2010 did not allow adequate assessment of young-of-the-year (YOY) production. However, at relatively high densities (e.g., at site 111 in 2012 and 2013), clear patterns of recruitment of YOY to the population were observed. These data indicate assessments of M. speciosa populations near the mouth of the Detroit River and, probably elsewhere, require relatively high densities to obtain clear information about seasonal abundance of this taxon. In habitats of higher complexity than at sites 15D and 111, there may be need to increase the number of samples (i.e., number of collected individuals) and frequency of sampling to obtain information about life-cycle patterns. Efforts needed to obtain life-cycle patterns in other water bodies is likely to be greater than that in western Lake Erie because Lake Erie has low-habitat complexity compared to other water bodies where this taxon is found (Carr and Hiltunen, 1965; Hiltunen, 1965; Schloesser et al., 2000). Therefore,

continued work with different methodologies may be necessary to establish a minimum protocol to characterize populations of M. speciosa. Reproduction Overall, available information indicates YOY production and tube construction (as measured by proportion of adults in tubes) closely paralleled water temperatures. However, the unexpected relationship between tube construction and water temperatures suggests that tube construction may primarily be related to YOY production. To date, there are no direct observations to support dependence of tube construction on YOY production (Willson et al., 2010). It may be possible that tubes, as well as YOY production, cannot be maintained at water temperatures below about 10 °C as observed in the present study. Another possibility is that adults voluntarily leave tubes and ‘migrate’ at cold temperatures. Regardless of the possible association, it is apparent that YOY production and tube construction of M. speciosa were dependent on warmer temperatures that occurred between mid-May and late‐September. Continual summer reproduction of YOY as evidenced in the present study agrees with results by Willson et al. (2010), who reported substantial reproduction of M. speciosa in early‐spring (mid-April) through summer months in the Klamath River. This is also similar to findings for reproductive cycles of M. aestuarina that occurred in warm months of the year (Shütz, 1965; Bagheri and McLusky, 1982; Bell, 1982; Bick, 1996). Therefore, continuous recruitment of small YOY (b0.04 mm) to the population in the present study probably did occur but was not detected by length–frequency distributions because individuals, smaller than 0.4 mm and not in tubes, would have passed through the 0.5 mm sieve used to sieve debris from samples. Another possibility is that YOY remain in tubes until they are about 0.5 mm long and are recruited directly into the measured population in the present study (Willson et al., 2010). However, observations of YOY in tubes indicate eggs/ embryos often occurred at the posterior end of tubes, which may indicate they were expelled from tubes and entered the population at a small size and, therefore, were undetected outside tubes in the present study. The cause for en masse reproduction of M. speciosa in late‐spring and early summer is unknown. However, evidence supports temperature and perhaps associated food “pulses,” as determinant factors that may regulate reproduction of M. speciosa (Shütz, 1965; Bagheri and McLusky, 1982; Bell, 1982; Bick, 1996; Willson et al. 2010). In the Klamath River, M. speciosa was reproductively active in mid-April through summer months. This is also similar to findings for reproduction of M. aestuarina that begins between March and May and ends in August and September (Shütz, 1965; Bagheri and McLusky, 1982; Bell, 1982; Bick, 1996).

Please cite this article as: Schloesser, D.W., et al., Freshwater polychaetes (Manayunkia speciosa) near the Detroit River, western Lake Erie: Abundance and life‐history characteristics, J. Great Lakes Res. (2016), http://dx.doi.org/10.1016/j.jglr.2016.07.006

D.W. Schloesser et al. / Journal of Great Lakes Research xxx (2016) xxx–xxx

Moreover, other polychaetes in the Sabellida also show reproductive activity associated with temperature. For example, the Hawaiian sabellid, Sabellastarte spectabilis, matures with temperatures of 24–25 °C, and its reproduction typically occurs between March and November, with peak reproduction in October (Bybee et al., 2007). Similarly, Bispira volutacornis from the west coast of Ireland spawns between late-July and early-September coinciding with maximum water temperatures of about 14–16 °C (Nash and Keegan, 2003). Murray et al. (2011) hypothesized that temperature may drive reproduction in Sabella pavonina, which reproduces from May to June at temperatures between 13 and 18 °C. In addition, Willson et al. (2010) reported that M. speciosa females began brooding YOY earlier and produced a greater number of offspring at warm than colder temperatures. However, observations in the Klamath River indicate some M. speciosa may overwinter as eggs (unpublished data, D. Malakauskas), which contributes to evidence that tubes are not maintained in winter. Collections of bare rocks from the Klamath River in early‐spring and cultured for several weeks yielded larvae and adults that continued to grow and build tubes (unpublished data, D. Malakauskas). This suggests that M. speciosa may overwinter as eggs, and possibly as larvae and adults, in rock crevices. It is also speculated that individuals may overwinter in interstitial spaces in the hyporheic zone. Sexual maturity In the present study, M. speciosa reached sexual maturity at a minimum length of 1.3 mm as evidenced by YOY in tubes with individuals. This contrasts with a length of about 2.0 mm reported for M. speciosa in the Klamath River, California (Willson et al., 2010). Some of these discrepanciesare probably due to use of formalin in the present study, which has been shown to shrink the body of Chaoborus fly larvae by 8–14% (Lasenby et al., 1994). In addition, measurements of M. speciosa from the Klamath River were obtained for live and relaxed individuals (Willson et al., 2010). Bick (1996) reported that males of M. aestuarina reached reproductive maturity before females in the Baltic Sea, and that March was the month in which the highest proportion of mature males occurred. In the present study, we observed the greatest proportion of mature male M. speciosa in April (ca., 72% of mature individuals), and by May, proportions of male and female individuals were about the same (55% and 45%, respectively). Fecundity Estimates of fecundity/brood-size of M. speciosa in Lake Erie are limited to generalities because of possible disturbance of individuals in tubes caused by sampling methodologies. To date, studies suggest an overall-mean fecundity rate of 10–12 YOY per female for Manayunkia species (Bick, 1996; Willson et al., 2010). In the present study, mean numbers of YOY in tubes ranged between 1.5 and 7.9 per tube (maximum range = 3–21/per tube). Willson et al. (2010) found a maximum of 35 YOY in one tube with an adult in the Klamath River in May. A maximum number of YOY produced by a single lab-reared female was 36 over one season, though no more than 11 were observed in a tube at one time. However, more definitive estimates of fecundity and tube abandonment (below) of Manayunkia species may be required to better define this life history parameter. Behavior The present study indicates that a large proportion of M. speciosa occurred outside tubes for most of the season and tubes were not maintained in colder months of the year. The occurrence of some individuals not in tubes in warmer months of the year can be attributed to dislodgement during sample collection. However, sample processing was probably not the only contributor to finding individuals outside of tubes.

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Therefore, we hypothesize that some unknown proportion of adults in any population may voluntary leave tubes for some unknown reason. This is supported by a total of 46% of individuals not found in tubes (n = 14,147, ESM Table S2). In colder months of the year, individuals may abandon tubes to migrate and/or be unable to maintain tubes at cold temperatures. Inability to maintain bio-generated biostructures is also known for zebra mussels (Dreissena polymorpha) which are unable to produce byssal threads at temperatures below 5 oC (Kobak, 2006; Garton et al., 2014). Support for abandonment and/or inability to support tubes is suggested by observations in the Klamath River where tubes of M. speciosa appear to disintegrate in the late‐fall (personal communication, J. Strange, Stillwater Science, Arcata, CA) and these populations have been found to exist without tubes in spring. Together, these data, and observations of M. speciosa occupancy on apparently bare rocks (see above reproduction), suggest voluntary tube abandonment and/or tube disintegration in cold months of the year. To date, the behavior of M. speciosa has been limited to laboratory studies (Willson et al., 2010; Malakauskas et al., 2013). These studies have consistently shown that Manayunkia spp. may abandon tubes when disturbed (Bell, 1982; Willson et al., 2010; Malakauskas et al., 2013). Specifically, Willson et al. (2010) noted that adults in tubes with YOY were less likely to leave tubes than males and non-brooding females, but when they did leave tubes, they often forced juveniles out as well. Bell (1982) found that many adults and most YOYs were dislodged from tubes during sample processing. In the present study, this would mean that about half of the individuals not in tubes would leave tubes caused by physical dislodgement during sample collection while on a boat, a timespan of under 10 min per sample. This is possible because laboratory studies indicate that M. speciosa can evacuate tubes in less than 1 min (personal observation, S. Malakauskas). Although unknown, it is believed that all individuals live in tubes. If this is correct, then about 23% of females would be expected to be dislodged from tubes during collection because this is one-half the proportion of adults found outside of tubes (other 23% = males not in tubes). However, only 3% of tubes contained YOY without a female present, yet 27% (ESM Table S2) contained YOY and a female in tubes. This near-total lack of YOY in tubes without an adult female seems to indicate that if females leave tubes voluntarily then associated YOY are also expelled from tubes. However, it may simple be that the lack of YOY in tubes without a female supports the theory that brooding females are unlikely to leave their tubes when brooding YOY (Willson et al., 2010; Malakauskas et al., 2013). However, it is possible a disproportionate number of males leave/exist outside tubes but this theory has no evidence. Size In the present study, M. speciosa reached a maximum length of 4.5 mm, but a typical length of about 3.0 mm was most common. Monthly mean sizes of this taxon ranged between 1.52 and 3.02 mm. In the Klamath River, few individuals exceeded 4.0 mm in total length, though it is difficult to make direct comparisons with the current study because Willson et al. (2010) measured live individuals rather than formalin-fixed individuals. Nonetheless, it appears that individual M. speciosa in the Klamath River do not reach as great a size as individuals near the mouth of the Detroit River in Lake Erie. Bell (1982) reported that M. aestuarina, in a salt marsh in South Carolina, reached a size of about 3.0 mm, while Bick (1996) reported a size of about 4.0 mm for M. aestuarina in the Baltic Sea, with both studies reporting lengths of individuals preserved in formalin. Therefore, there are likely genetic or environmental factors that drive morphologic plasticity of populations of Manayunkia species. Life span Interpretation of length–frequency distributions over 4 years at two sites revealed some insights into the life span of M. speciosa near the

Please cite this article as: Schloesser, D.W., et al., Freshwater polychaetes (Manayunkia speciosa) near the Detroit River, western Lake Erie: Abundance and life‐history characteristics, J. Great Lakes Res. (2016), http://dx.doi.org/10.1016/j.jglr.2016.07.006

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D.W. Schloesser et al. / Journal of Great Lakes Research xxx (2016) xxx–xxx

mouth of the Detroit River in western Lake Erie. Overall, it appears individuals of this taxon live about 10 months, but the possibility of a longer life span cannot be eliminated. Support for a 10-month life span includes 1) occurrence of relatively large overwintered individuals in spring; and 2) occurrence of distinct unimodal peaks composed of large individuals of length–frequency distributions in mid-summer. Occurrence of large individuals in fall after reproduction stopped (October–November) and in spring before reproduction began (March–April) indicates overwinter survival and a minimum life span of about 5–7 months. In addition, persistence of larger length–frequency groups through mid-summer (July) when bimodal peaks occurred supports the addition of 3 months to the life span (May–July). Therefore, available data indicate a minimum life span of 10 months (October–July). Because bimodal peaks of length–frequency distributions did not continue through summer and disappearance of larger peaks of length–frequency distributions did not occur, it is not possible to determine if the life span of some individuals was N 10 months. It is possible, individuals could live multiple years, but data in the present study are inconclusive beyond a 10-month life span. Taxa, such as Hexagenia spp. mayflies, exhibit consistent distinctive bimodal peaks associated with observable mating behavior and subsequent definable recruitment and separation of cohorts/ages of nymphs as evidenced by length–frequencies that remain visible throughout a 2-year life-cycle (Schloesser and Nalepa, 2001). In addition, disappearance of cohorts of mayflies associated with emergence from the water verifies distinct cohort/age groups. In contrast, M. speciosa exhibited only unimodal distributions after en masse reproduction in June–July. Our interpretation of this is that age classes (YOY and 10 month-plus classes) of M. speciosa become integrated into one peak as YOY grow and become part of the population of older-aged individuals. The presence of large individuals after June–July also supports the survival of age 10 month-plus individuals after en masse events that cause bimodal peaks in spring. This is in agreement with findings of Willson et al. (2010) for M. speciosa in the Klamath River, California and Bick (1996) for M. aestuarina in the Black Sea where mature polychaetes remained alive after reproduction. Willson et al. (2010) determined that M. speciosa has a life span of about 1 year, and we have no evidence to negate this assumption, and the continued presence of relatively large, non-YOY individuals after en masse events leads to an assumption that this taxon lives longer than 10–12 months. Regardless, it appears M. speciosa does not appear to die off en masse, but rather mortality occurs over a period of months in their second summer of existence. This could be because M. speciosa is iteroparous and its reproductive season lasts for several months, so M. speciosa populations exhibit a somewhat undeterminable age structure. Further evidence of life span would be visible in length– frequency distributions if reproduction were dependent on age alone. However, this is not the case for M. speciosa in western Lake Erie, which exhibited continuous reproduction by YOY and 10 month-plus individuals once a minimum length of 1.3 mm was attained. If this were not the case and spawning occurred only en masse, it would be possible to track age classes based on presence of YOY in tubes from June to July and the absence of YOY in larger length classes typical of age 1+ individuals. Therefore, available data indicate that M. speciosa in western Lake Erie exhibits only one en masse reproductive event per year and YOY and 10 month-plus age individuals continually reproduce when individuals grow to a length of 1.3 mm. These spawning characteristics negate the possibility of using length–frequency distributions to definitively define the life span of M. speciosa based on length–frequency distributions in western Lake Erie and possibly in waters elsewhere. However, laboratory observations by Willson et al. (2010) and length– frequency distribution suggest a life span of about 1 year. Mortality The present study suggests mortality of M. speciosa was similar to mortalities found in laboratory studies. Willson et al. (2010) estimates

a survival rate of 25% after 10 months, although individuals in laboratory studies were subject to regular disturbance and handling stress, which likely increased mortality. However, in the Black Sea, M. aestuarina, a closely related species to M. speciosa, exhibited an estimated survival rate of juveniles of 15–20% (Bick, 1996). The difference between minimum and maximum abundances at site 111 in 2012–2013 and at site 15D in 2009–2010 showed a five-fold change in seasonal abundance. Because M. speciosa sex ratios are equally distributed, this would suggest a fecundity of 10 eggs per female and a 20% survivorship. However, a fecundity of 10 or 12 eggs does not seem sufficient to explain the 12-fold increase in total abundance of M. aestuarina in 15 months reported by Bagheri and McLusky (1982), particularly given that M. aestuarina may experience greater predation when their densities are high (Bell, 1980; Kneib, 1985). However, our estimates of mortality are confounded by a lack of data on survivorship of embryonic and larval individuals which may account for some of the discrepancy in fecundity estimates, as well as the effects of resource limitation. More accurate fecundity estimates will likely require different field sampling methodologies than those used in the aforementioned studies. Habitat Substrate diversity available to M. speciosa at the mouth of the Detroit River in western Lake Erie is relatively limited compared to other places where M. speciosa and its congeners have been studied (Stocking and Bartholomew, 2007; Malakauskas and Wilzbach, 2012). Near the mouth of the lower Detroit River in western Lake Erie, surface substrates are relatively flat and composed primarily of silt and sand with occasional patches of exposed gravel, except near shipping lanes where large gravel, rocks, and bedrock occur (personal observations, G. Kennedy, Great Lakes Science Center, Ann Arbor, MI). In the Klamath River of the Pacific Northwest, maximum densities of M. speciosa occur in protected areas among algae and detritus where water velocities are reduced (Stocking and Bartholomew, 2007; Malakauskas and Wilzbach, 2012; Malakauskas et al., 2013). The negative correlation between water flow and abundances probably exists where M. speciosa is found on mobile substrates because mobile substrates would prohibit individuals from remaining stationary in currents (Willson et al., 2010; Malakauskas et al., 2013). Substrates near the mouth of the Detroit River where M. speciosa is found are largely silt, sand, and gravel. Therefore, in the present study, we speculate M. speciosa is vulnerable to shifting currents of the Detroit River and currents caused by waves and surges associated with storms of the open waters of Lake Erie. Even substrate depressions observed at site 15D did not appear to be current-refuges for M. speciosa because their abundances inside and outside substrate depressions were similar. It is possible, gravel patches observed in petite Ponar samples at site 111 did provide current-refuges which would account for higher abundances at this site than at site 15D where no exposed patches of gravel were observed by SCUBA. However, if exposed gravel at site 111 did provide habitat/current-refuges, the coefficient of variation would likely be higher at site 111 than 15D, which, on average, it was not. It is probable lower abundances at site 15D contributed to higher coefficient of variability than at site 111, thus, lower abundances could mask differences between habitat use by M. speciosa. Overall, studies to date indicate abundances of M. speciosa can vary up to 10-fold between sites located close together (e.g., 0.3 km, Lake Erie) in low-diversity habitats. Conclusions Decreases in abundances of Manayunkia speciosa near the mouth of the Detroit River between 1961 and 2013 agree with decreases observed throughout much of western Lake Erie between 1961 and 2003. To date, no known causes have been linked to decreases of M. speciosa in western Lake Erie. However, the primary known change

Please cite this article as: Schloesser, D.W., et al., Freshwater polychaetes (Manayunkia speciosa) near the Detroit River, western Lake Erie: Abundance and life‐history characteristics, J. Great Lakes Res. (2016), http://dx.doi.org/10.1016/j.jglr.2016.07.006

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that has affected Lake Erie is nutrient reductions associated with pollution-abatement programs initiated in the early‐1970s, which may have caused declines in M. speciosa. This is the first detailed study of life‐history characteristics of M. speciosa in wild populations and, in general, it supports laboratory studies of M. speciosa in the Pacific Northwest (Willson et al., 2010; Malakauskas et al., 2013). Overall, studies of field and laboratory populations indicate that M. speciosa inhabits a wide variety of habitats; exhibits higher abundances in periods of degraded water quality; exhibits large variation of abundances between closely located sites (e.g., 0.3 km, Lake Erie); has a 10 month-plus life-cycle; becomes sexually mature at lengths N1.3 mm and can produce maximums of between 21 (present study) and 35 (Willson et al., 2010) young per female per brood; develops young in tubes, produces young, and constructs tubes in warm months of the year; ceases production of young and construction of tubes at water temperatures below 10 °C; and changes in life history characteristics are more easily observed when densities are high (e.g., seasonal mean average ≥ 40. 000/m2) than when they are low (e.g, ≤6000/m2). To date, the only known importance of M. speciosa populations is that they can harbor parasites that damage populations of salmonid fishes in the northwestern United States, and possibly elsewhere where persistent populations of M. speciosa and parasites occur. Lake Erie of the Great Lakes is one such place where M. speciosa has occurred for over 50 years. Therefore, future studies on parasite presence and abundance in M. speciosa in the Great Lakes, as well as surveys for other populations of M. speciosa in the Great Lakes, would be judicious, particularly since Malakauskas et al. (2016) recently reported a new species of Ceratonova in Lake Erie. Additionally, reasons for the longterm decline of M. speciosa abundance throughout western Lake Erie between 1961 and 2003 are unknown, but further efforts directed to elucidate causative reasons for this decline could aid in the development of management strategies to reduce incidence of parasitic infection in salmonids in the northwestern United States and, possibly, in the Great Lakes. Acknowledgments This is Contribution Number 2063 of the Great Lakes Science Center, U.S. Geological Survey, Ann Arbor, Michigan. Use of trade, firm, or product names is for descriptive purposes only and does not imply endorsement by the U.S. Government. Appendix A. Supplementary data Supplementary data to this article can be found online at http://dx. doi.org/10.1016/j.jglr.2016.07.006. References Alexander, J.D., Hallett, S.L., Stocking, R.W., Xue, L., Bartholomew, J.L., 2014. Host and parasite populations after a ten year flood: Manayunkia speciosa and Ceratonova (syn. Ceratomyxa) shasta in the Klamath River. Northwest Sci. 88, 219–233. Armendariz, L.C., Paola, A., Capitulo, A.R., 2011. Manayunkia speciosa Leidy (Polychaeta: Sabellidae): introduction of this nonindigenous species in the Neotropical Region (Uruguay River, South America). Biol. Invasions 13, 281–284. Bagheri, E.A., McLusky, D.S., 1982. Population dynamics of oligochaetes and small polychaetes in the polluted Forth estuary ecosystems. Neth. J. Sea Res. 16, 55–66. Bartholomew, J.L., Whipple, M.J., Stevens, D.G., Fryer, J.L., 1997. The life cycle of Ceratomyxa shasta, a myxosporean parasite of salmonids, requires a freshwater polychaete as an alternate host. J. Parasitol. 83 (5), 859–868. Bartholomew, J.L., Atkinson, S.D., Hallet, S.L., 2006. Involvement of Manayunkia speciosa (Annelida: Polychaeta: Sabellidae) in the life cycle of Parvicapsula minibicornis, a myxozoan parasite of Pacific salmon. J. Parasitol. 92 (4), 742–748. Bate, G.C., Whitfield, A.K., Adams, J.B., Huizinga, P., Wooldridge, T.H., 2002. The importance of the river-estuary interface (REI) zone in estuaries. Water SA 28 (3), 271–279. Beeton, A.M., 1965. Eutrophication of the St. Lawrence Great Lakes. Limnol. Oceanogr. 10 (2), 240–254. Bell, S.S., 1980. Meiofauna–macrofauna interactions in a high salt marsh habitat. Ecol. Monogr. 50 (4), 487–505.

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Please cite this article as: Schloesser, D.W., et al., Freshwater polychaetes (Manayunkia speciosa) near the Detroit River, western Lake Erie: Abundance and life‐history characteristics, J. Great Lakes Res. (2016), http://dx.doi.org/10.1016/j.jglr.2016.07.006