Limnology (2017) 18:153–166 DOI 10.1007/s10201-016-0498-3

RESEARCH PAPER

Factors controlling changes in the aquatic macrophyte communities from 1984 to 2009 in a pond in the cool-temperate zone of

1 1 2 Yoshifumi Sakurai • Kazuo Yabe • Koji Katagiri

Received: 30 November 2015 / Accepted: 16 July 2016 / Published online: 9 August 2016 Ó The Japanese Society of Limnology 2016

Abstract We investigated changes in aquatic macrophyte were WD and Cl-. Because the concentration of C1- was communities over 25 years in Utonai-ko (42°420N, low, the change in aquatic macrophyte communities likely 141°420E) in northern Japan and determined the major resulted from the increase in WD. change-producing factors using canonical correspondence analysis (CCA) of 21 measured hydrochemical variables Keywords Water depth Á Hippuris vulgaris Á with potential to influence the occurrence of communities. Myriophyllum spicatum Á Vallisneria asiatica Á Canonical We then examined the corresponding changes in the correspondence analysis 25-year fluctuation trends in the communities and mea- sured variables. The most prominent changes were a decline in the Hippuris community and an increase in the Introduction Vallisneria and Myriophyllum communities. CCA revealed that the leading variable was significant wave height The occurrence of aquatic macrophyte communities is (SWH), followed by water depth (WD), total nitrogen (T- affected by many environmental variables. Physical attri- N), dissolved oxygen (DO), pH, chlorine ion (Cl-), trans- butes of water, including water depth (WD), water- parency, mud thickness, and suspended solids (SS). The table fluctuation, transparency, and suspended solids (SS), Hippuris community was positively correlated with T-N are known factors that influence species occurrence of and Cl- and negatively with SWH, WD, DO, and pH. All aquatic macrophytes (Havens 2003; Feldmann and Noges of these variables were likewise correlated with the Val- 2007; Maltchik et al. 2007; Moore et al. 2010; Yu et al. lisneria and Myriophyllum communities but in the reverse 2013). The increasing water table in summer can result in direction. SS and transparency exhibited no correlations. decreases in Potamogeton pectinatus (L.) Bo¨erner and During the 25 years, WD and T-N increased, but annual Chara tomentosa L. (Blindow 1992). Drawdowns of a maximum wind velocity and Cl- decreased. Fluctuation of floodplain pond increase species richness of aquatic DO was \2mgml-1 and pH was consistent. Considering macrophytes (Maltchik et al. 2007), and the reduced spe- the direction of correlations and 25-year trends, vital fac- cies richness of submerged aquatic macrophytes because of tors for the change in aquatic macrophyte communities the stress produced by a high water table is recovered during drought years (Havens et al. 2004). Large water table fluctuations increase the number of species that can Handling Editor: Munemitsu Akasaka. tolerate the stresses involved in winter drawdowns (Mjelde et al. 2013). Declines in transparency decrease the abun- & Yoshifumi Sakurai dance of P. malaianus Miq. and Myriophyllum spicatum L., [email protected] (Amano and Ooishi 2009). High turbulence levels suppress 1 Graduate School of Sapporo City University, the growth of young Vallisneria spiralis L. (Ellawala et al. Geijutuno-mori-1, Minamiku, Sapporo 005-0864, Japan 2013). Large variation in sediment composition increases 2 Public Works Research Institute, Nanbara-1-6, species richness and heterogeneity of the macrophyte Tuskuba 305-8516, Japan communities in rivers (Pedersen and Riis 1999). 123 154 Limnology (2017) 18:153–166

Water chemistry also affects species composition of The goals of this study were to (1) clarify 25 years of aquatic macrophyte communities. Changes in species change in the occurrence and distributional patterns of composition can be related to the concentration of miner- aquatic macrophyte communities classified by species als, acidity, electrical conductivity (EC), and alkalinity composition in the pond, (2) determine major factors cor- (Kunii 1991). Excessive macronutrients (such as phos- related with current communities, and (3) elucidate the phorus and nitrogen) reduce the abundance of aquatic main factor that caused large-scale changes in those com- macrophyte communities because of decreased trans- munities in the pond. parency caused by planktonic algal blooms (Dodson et al. 2000; Takamura et al. 2003). Competitive exclusion by invasive aquatic macrophytes, Methods Elodea nuttallii (Planch.) St. John (Nagasaka et al. 2002) and M. spicatum (Ali and Soltan 2006), or the semiemer- Study site gent Phalaris arundinacea (Katagiri et al. 2010), reduces the richness of macrophyte species and the diversity of Utonai-ko (42°420N, 141°420E and 3 m in altitude) is sit- their communities. Furthermore, fishes and herbivorous uated *8 km from the coast of the Pacific Ocean on the waterfowl reduce the biomass of aquatic macrophytes northern part of the Yufutsu Plain (Fig. 3). The shape of (Donk and Otte 1996). Four polyphenolic compounds Utonai-ko is a triangle composed of northwest, southeast, secreted by M. spicatum suppress the growth of Micro- and southwest shores. It originally had 9.5 km of shoreline cystis aeruginosa Kizing (Nakai et al. 1998). and 2.43 km2 area. Since 1991, this pond and the sur- Consequently, multiple variables must be examined to rounding areas have been on the List of of identify the major factors controlling the occurrence of International Importance (Ministry of the Environment, aquatic macrophytes in a study area (Katagiri et al. 2010). Japan 2015). Pumice-fall deposits accumulated at ground Long-term alternation of aquatic macrophyte communities surface of this area, which fell in 1739 following eruption in have been documented using inventory data of the volcano, Mt. Tarumae (Yamada et al. 1963; Ikeda (Jensen et al. 2000), aerial photographs (Partanen et al. et al. 1995; Hasegawa et al. 2013). The bottom sediment in 2009), and satellite images (Nishihiro et al. 2014) from the pond was coarse sand made of pumice deposits in many different years, composition of pollen in sediment places, but in some places, loose mud overlay the coarse (Kowalewski et al. 2013), and direct examination over sand (Geographical survey institute 2003). The mean 21 years (Sakurai and Kasumigaura River Office 2004). annual temperature between 1981 and 2010 was 7.6 °C, These studies, however, estimated changes in aquatic mean annual precipitation 1198 mm, and 79 % of precip- macrophyte communities in relation to a limited number of itation fell from May to November (Tomakomai Weather environmental variables, including WD, transparency, and Station 2010). Mean water temperature (WT) from May to chemical oxygen demand, which resulted in insufficient November was 15.8 °C ( Government 2007), analyses of the relationships between communities and when the aquatic macrophytes M. spicatum and V. asiatica environmental factors. If the probable mechanisms for Miki, and others, grow. changes in communities can be elucidated, past changes in As shown in Fig. 3, Bibi River and two small rivers communities can be predicted by the records of major flowed into the pond. Elevation of the bottom (surface of factors (Takamura et al. 2003). Accordingly, to determine pumice sediments under the loose mud) was 0.6–1.1 m the mechanisms involved in long-term changes in aquatic a.s.l. in most parts of the pond (Hokkaido Government macrophyte communities in a freshwater lentic system, 2011). In the interior areas, blocks E1–E2 and D3–D4 were confirmation of detailed aquatic macrophyte communities, lower than neighboring areas because water ran from the identification of major environmental factors controlling largest inlet (the mouth of the Bibi River) through these the occurrence of communities, and successive records of blocks to the outlet. Two interior blocks next to E2 (the environmental factors and occurrence of communities are block in the watercourse), C2 and D2, were flatter and needed. higher, and their respective heights were 1.1–0.9 m and Between 1984 and 2003, large-scale spatial and tem- 0.8–0.7 m. poral alteration of aquatic macrophyte communities have Water levels of Utonai-ko have been recorded since been recorded three times at Utonai-ko, a small pond 1969 at a monitoring station located on the northwest shore located in northern Japan in the cool-temperate zone (To- of the pond. Water levels decreased from 2.3 m a.s.l. in makomai City 1987; Hokkaido Government 2004, 2010). 1962 to 1.6 m a.s.l. in 1976, presumably because of the Major hydrochemical variables were continuously exam- short-cut of the lower stream (Hokkaido Government ined during this period (Hokkaido Government 1984– 2007), and then increased since 1977, irrespective of 2010). fluctuations in precipitation. To increase the water level, 123 Limnology (2017) 18:153–166 155 the course of the Yufutsu River next to the Bibi River was WD in 2003 was also estimated using MT data from that altered to flow into the pond in 1997, and a weir was built year. We examined WD and MT in 2009 directly and in 1998 at the outlet to increase water levels for conser- adjusted it using the median water level. vation of the freshwater lentic system. Water level has been We collected two 2000-ml plastic containers of water at maintained at 2.0 m since 1999 (Geographical Survey *20-cm depth from each survey point, which were Institute 2003). immediately stored in an icebox and then kept at 4 °Cin The riverine system of the Bibi River has been signifi- the laboratory (Water Chemistry Center in Docon Co., cantly influenced by nutrient loading since 2005 (Hokkaido Ltd.). Chemical variables of sampled water were analyzed

Government 1984–2010). The concentration of NO3-N in within 2–3 days after collection, according to Japanese the Bibi River was extremely high in the headwater spring Industrial Standards Committee (2008). T-N was analyzed (13.36 mg/L-1) because of agricultural land use but grad- by ultraviolet absorptiometry (Shimadzu UV-160A) and ually decreased downstream (2.3 mg/L-1 in Utonai-ko), total phosphorus (T-P) by the potassium peroxydisulfate being diluted by water from many tributaries (Hokkaido decomposition method. The concentration of major Government 2007). cations, Ca2?,Mg2?,Na?, and K?, were analyzed by flame atomic absorption spectrometry (Hitachi Z-5010);

Species composition of communities NH4-N was analyzed by indophenol blue absorptiometry and environmental variables (Hitachi UV-2810), whereas those of anions, SO42-,Cl-,

NO3-N, and NO2-N, were analyzed by ion chromatography Species composition of aquatic macrophyte communities (Dionex IC25). Alkalinity was analyzed by sulfuric acid in the pond was recorded at 81 evenly distributed survey titration, PO4-P by molybdenum blue absorptiometry, DO points in 1984 by Nakai (1987), 25 survey points in 1994 by the Winkler method, and SS by the glass-fiber filter- (Hokkaido Government 2010), and 135 survey points in paper method (pore size 1.0 lm). EC and WT were 2003 (Hokkaido Government 2004). To determine factors examined at each survey point using an EC meter (DKK- controlling aquatic macrophyte communities, we examined TOA CM-21P), and pH was examined using a pH meter the communities and hydrochemical environmental vari- (DKK-TOA HM-21P). ables in September 2009 at 135 survey points, locations of To determine annual trends for hydrochemical variables, which in the pond did not correspond with those surveyed we used water-chemistry variables, including T-N, Cl-, in 1984. In addition, we examined Najas and Hippuris SS, pH, and DO, continuously monitored three or four communities at 40 survey points in September 2010 and times a year since 1984 (Hokkaido Government 1984– 2013. 2010), and a moving average for the five variables was Species composition in 1 m 9 1 m quadrats, which calculated. We also estimated the annual trend for turbu- were marked at 10-cm intervals, was recorded, and cov- lence level, expressed by significant wave height (SWH) at erage of each species was determined in 5 % increments. maximum wind velocity. SWH was calculated using the Concurrently, coverage of submerged species was exam- formula of Wilson (1965). Wind velocity and direction of ined using a water glass, and physical variables of WD, the strongest wind between April and October was selected mud thickness (MT), transparency, and current velocities at from observational data of the Tomakomai Weather Station the middle and bottom depths (CVM, CVB) were exam- (2010), and fetch was measured as the length of open-water ined using a ruler, measuring pole, visibility meter surface between the pond shore and each survey point. (Satoshouji JIS k0102), and current meter (Dentan Tk’- 105x), respectively. All physical variables were examined Statistical analyses three times at each survey point, and their mean values were used for further analysis. First, we classified species composition data of communi- We used the daily water levels (altitudinal) observed ties collected from 1984 to 2009 at 376 survey points using from 1969 to 2010 and obtained the median value for daily TWINSPAN (Hill 1979; Peck 2010). Before the analysis, water levels for the growing season of aquatic macrophytes percentage data for coverage of each species were arcsine- (May to November) for each year. In 1984, elevation of the square-root transformed, and rare species that occurred less bottom surface (surface of pumice deposit) at each survey than five times were excluded. Pseudospecies cut levels of point was calculated from the water level at the monitoring 0, 0.1 (corresponding to 3.2 %), 0.2 (11.2 %), 0.3 station on the survey day by subtracting water depth (24.5 %), and 0.4 (43.0 %) of coverage were adopted. recorded at each survey point (Nakai 1987). Then, WD was Distribution of communities classified by TWINSPAN was obtained from the median water level by subtracting the mapped using ArcGIS 10 (Esri, Japan). Locations of survey elevation of the bottom surface and thickness of mud points were obtained from maps of community distribution recorded during 1995 (Hokkaido Government 2011). The produced for 1984 (Nakai 1987) and 2003 (Hokkaido 123 156 Limnology (2017) 18:153–166

Government 2004) and GPS records from 2009. We did not the survey points on average and occurred at all survey use data collected in 1995 because of insufficient survey points (frequency = 100 %). This community type was points. characterized by frequent occurrence of V. asiatica. Second, we analyzed relationships among community Hippuris vulgaris L. was dominant in the Hippuris types classified in the TWINSPAN analysis and envi- community, in which it exhibited high coverage (87.50 %) ronmental variables using data collected from 2009 to and occurred at all survey points classified (fre- 2013. Because data frequency were not normally dis- quency = 100 %). Hydrilla verticillata (L.f.) Royle and M. tributed, Kruskal–Wallis tests and Steel–Dwass nonpara- spicatum frequently occurred in this community type. metric multiple comparisons (Zar 1999)wereemployedto Nuphar japonicum DC densely covered the Nuphar determine how community types differed with respect to community with high frequency (mean cover- the 23 environmental variables. Next, canonical corre- age = 67.23 %, frequency = 96.36 %). V. asiatica and M. spondence analysis (CCA) was used to detect environ- spicatum cohabited 50.91 % of the survey points in this mental gradients associatedwiththeoccurrenceof community, and Nymphaea tetragona Georgi and P. community types (Ter Braak 1986). Monte Carlo tests octandrus Poir also occurred frequently. Sparganium (with 199 permutations) of constrained ordination scores emersum Rehmann densely covered the Sparganium for environmental variables were performed to assess the community with high frequency (66.73 and 96.15 %, significance of correlations. respectively). M. spicatum and V. asiatica also occurred TWINSPAN was performed using PC-ORD version 6 frequently. for Windows (MjM Software Design) and CCA using V. asiatica was sparse in the Vallisneria community, but CANOCO version 4.5 (Microcomputer Power). Kruskal– it occurred frequently (54.61 and 92.78 %, respectively). Wallis tests and Steel–Dwass nonparametric multiple M. spicatum and, to a lesser extent P. octandrus and H. comparisons were performed using SYSTAT 13.1 (Systat verticillata, occurred with V. asiatica. Software, Inc.). M. spicatum densely covered the Myriophyllum com- munity with high frequency (61.66 and 97.03 %, respec- tively). H. verticillata, P. octandrus, V. asiatica, and Najas Results marina L. frequently occurred with low coverage in this community. Classification of aquatic macrophyte communities N. marina occurred in all survey points of the Najas community and exhibited dense coverage (79.81 %). M. TWINSPAN classified the aquatic macrophyte communi- spicatum, P. octandrus, H. verticillata, and Trapa japonica ties of Utonai-ko into eight types (Fig. 1). The character- Flerov frequently occurred at low coverage rates. istics of each community type are listed by dominance and T. japonica densely covered the Trapa community with frequency of indicator species in Table 1. high frequency (76.52 and 95.65 %, respectively). M. spi- The Zizania community was dominated by an emergent catum, P. octandrus, and H. verticillata frequently occur- plant, Zizania latifolia Turcz, which covered 79.61 % of red as well.

Fig. 1 TWINSPAN process. At each branch, indicator species and eigenvalues are presented

123 inlg 21)18:153–166 (2017) Limnology Table 1 Species components of eight aquatic macrophyte communities Community name Mean coverage (%) Frequency (%) Hippuris Zizania Nuphar Sparganium Vallisneria Myriophyllum Najas Trapa

tableHippuris vulgaris L. 87.50 100.00 0.26 5.26 0.18 1.03 Zizania latifolia Turcz. 79.61 100.00 1.27 7.27 Nuphar japonicum DC. 0.41 8.11 2.24 10.53 67.23 96.36 2.31 11.54 0.92 1.98 Sparganium emersum Rehman 2.45 14.55 66.73 96.15 1.31 4.95 Vallisneria asiatica Miki 0.74 8.11 6.18 42.11 9.05 50.91 4.33 23.08 54.61 92.78 14.28 53.47 1.73 15.38 1.41 17.39 Nymphaea tetragona Georgi 0.14 2.70 1.23 20.00 0.49 3.09 Potamogeton octandrus Poir 1.23 20.00 1.98 21.65 15.79 57.43 19.23 69.23 0.65 13.04 Myriophyllum spicatum L. 1.22 24.32 1.71 21.05 7.18 50.91 15.58 61.54 11.44 63.92 61.66 97.03 9.62 76.92 5.11 34.78 Hydrilla verticillata (L.f.) Royle 2.16 43.24 1.86 16.36 2.31 11.54 1.19 14.43 12.13 58.42 6.15 53.85 10.22 73.91 Najas marina L. 0.41 8.11 0.26 5.26 0.27 5.45 2.55 19.59 8.37 38.61 79.81 100.00 10.11 69.57 Trapa japonica Flerov 0.14 2.70 0.45 9.09 0.67 3.85 0.59 9.28 0.74 5.94 31.54 53.85 76.52 95.65 Potamogeton crispus L. 0.14 2.70 4.87 10.53 0.27 5.45 3.37 3.85 2.40 12.37 0.97 2.97 1.73 15.38 Potamogeton perfoliatus L. 0.68 13.51 0.26 5.26 7.23 21.82 8.94 30.77 6.49 14.43 3.00 16.83 1.73 15.38 0.65 13.04 Potamogeton pusillus L. 0.26 5.26 0.41 3.64 0.19 3.85 0.10 2.06 0.20 3.96 Schoenoplectus validus (Vahl) T. Koyama 2.50 15.79 1.64 7.27 2.06 4.12 0.05 0.99 Phragmites australis (Cav.) Trin. ex Stend 4.08 21.05 0.05 0.99 Sparganium erectum L. 2.24 10.53 11.00 16.36 1.73 15.38 Potamogeton natans L. 2.41 18.18 2.21 19.23 0.23 2.06 1.16 7.92 Trapa incisa Sieb. et Zucc. 0.53 10.53 0.64 3.64 0.05 1.03 2.52 5.94 1.35 7.69 Myriophyllum verticillatum L. 1.01 2.70 0.50 5.45 0.67 3.85 0.49 3.09 0.87 5.94 Ceratophyllum demersum L. 0.36 7.27 0.05 1.03 0.77 8.91 0.22 4.35 Najas yezoensis Miyabe 0.81 16.22 0.27 5.45 0.19 3.85 0.46 4.12 0.25 4.95 21.92 61.54 3.59 43.48 Potamogeton oxyphyllus Miq. 0.19 3.85 1.75 8.25 2.28 10.89 15.19 30.77 Potamogeton maackianus A. Benn. 0.14 2.70 0.45 9.09 0.69 13.86 0.43 8.70 Potamogeton pectinatus L. 0.68 13.51 0.18 3.64 0.62 7.22 0.05 0.99 0.38 7.69 1.30 26.09 Spirodela polyrhiza (L.) Schleid. 1.22 24.32 0.05 0.99 Potamogeton heterophyllus L. 1.42 21.62 0.64 12.73 0.05 1.03 0.15 2.97 Cicuta virosa L. 0.14 2.70 0.92 5.26 0.18 1.03 0.05 0.99 Utricularia vulgaris L. var. japonica (Makino) Tamura 1.22 24.32 1.23 12.73 0.05 1.03 0.15 2.97 0.38 7.69 Potamogeton alpinus Balb. 0.68 13.51 0.32 1.82 2.79 11.54 0.47 2.97 Charophytes 0.41 3.64 2.96 8.25 0.40 2.97 Total numbers of species 19 14 26 15 23 27 13 11 123 Mean speacies richiness 3.4 2.7 4.3 3.0 4.2 4.2 5.2 4.0 Indicator species of TWINSPAN are listed from the top to the line 11 157 158 Limnology (2017) 18:153–166

Change in aquatic macrophyte communities shore blocks, C1, D1, and C3, and then disappeared in in the pond 2009. The Trapa community was distributed at both shores and interior areas of the eastern area, D1–E3, and F2 and In 1984, the Hippuris community occupied 39.5 % of the C3, but thereafter was confined to shore blocks C1 and D1 pond, whereas it decreased to 3.0 % in 2003 and to 0.8 % in 2003 and D1, E1, and E3 in 2009. in 2009 (Fig. 2). Conversely, both the Vallisneria and Myriophyllum communities increased from 38.1 to 48.5 % Relationships between environmental variables and further increased to 77.9 % at these time points. Four and community types communities, Zizania, Sparganium, Nuphar, and Najas, increased until 2003 and then decreased until 2009. The Except T-P and NO2-N, all 21 environmental variables Trapa community continuously decreased. showed significant differences among communities The Hippuris community was distributed at the two (Table 2). The concentration of T-N was higher in the southern lake shores and at flat and shallow blocks of the Hippuris community than that in the Vallisneria and interior (blocks C2 and D2 in Fig. 5) in 1984 but was Myriophyllum communities, and NO3-N was highest in the confined to a bay and blocks A3 and B3 afterward (Fig. 3). Najas community. The concentration of NH4-N was rela- The Vallisneria and Myriophyllum communities were tively high in the Vallisneria and Myriophyllum commu- sporadically distributed in the interior areas in 1984 and nities, although it was low across all communities. The spread to the entire pond, including the entire shoreline, concentration of PO4-P was high in the Myriophyllum until 2009. The Sparganium and Nuphar communities were community. not recorded in 1984: The Sparganium community occur- EC was high in the Hippuris and Najas communities but red around the inlet of the main stream (Bibi River) at E1 low in the Vallisneria and Myriophyllum communities. The 2- and F1 and of a small river (C2) in 2003 and at E1, F1, and concentration of SO4 was low in the Hippuris commu- F2 in 2009. The Nuphar community sporadically occurred nity. Concentrations of the other minerals, Ca2?,Mg2?, in all shoreline areas of the pond in 2003 and 2009, Na?,K?, and Cl-, were low in the Vallisneria and decreasing in occurrence at survey points. In 1984, the Myriophyllum communities, whereas except for K?, mean Najas community was confined to the interior block E2; values were highest in the Hippuris community. In the however, in 2003, the community shifted to some of the Vallisneria and Myriophyllum communities, values of DO, pH, and WD were higher than that of the other commu- nities, whereas SS and MT were low. Mean values of the 100% following variables were extremely high in particular community communities: SS in the Zizania and Trapa communities, Hippuris WT in the Najas community, MT in the Najas and Trapa Zizania communities, and CVM and CVB in the Sparganium 80% community. DO, pH, and WD were lowest in the Hippuris Sparganium community. Transparency was highest in the Najas com- Nuphar munity. SWH was lowest in the Hippuris community, Vallisneria whereas that in the other seven communities was approx- 60% imately equal. As a whole, T-N and minerals, except for Myriophllum 2- SO4 , were characteristically higher in the Hippuris Najas community than in the Vallisneria and Myriophyllum Trapa communities. DO, pH, and WD values were high in the 40%

occurrence ratio Vallisneria and Myriophyllum communities, but those of SS and MT were low. In CCA ordination of communities constrained by 20 significant environmental variables, the first four axes 20% accounted for 29.2, 22.3, 20.4, and 8.8 % of the total variance (80.7 % in total), according to their respective eigenvalues: 0.954, 0.730, 0.665, and 0.290. All four axes were statistically significant (Monte Carlo test P \ 0.005). 0% Because the fourth axis exhibited lower interset correla- 1984 2003 2009 tions of environmental variables and represented unappar- Fig. 2 Change over 25 years of aquatic macrophyte communities in ent relationships between communities and environmental Utonai-ko variables, we considered the first three axes in the analysis 123 Limnology (2017) 18:153–166 159

Fig. 3 Topography and change over 25 years of aquatic macrophyte communities in Utonai-ko. The number of contour lines depicts the surface elevation of the pond bottom (surface of pumice sediments under the loose mud)

(Fig. 4). In all diagrams (Axes 1 and 2, and Axes 1 and 3), occurrence of the communities in Utonai-ko, were SWH, the Hippuris community was positively correlated with WD, T-N, DO, pH, Cl-, transparency, MT, and SS in T-N, EC, Ca2?,Mg2?,Na?, and Cl- and negatively cor- descending order of the magnitude of correlations. 2- related with SWH, NO3-N, NH4-N, PO4-P, and SO4 . The results were reverse for the Vallisneria and Myriophyllum Fluctuation of wind velocity, water level, MT, T-N, communities, they were negatively correlated with the DO, pH, Cl2, and SS over 25 years former variables and positively with the latter, and had positive correlations with DO, WD, and pH. Annual mean water level in 1984 was 1.81 m, gradually Both the Zizania and Trapa communities in Axes 1 and increased to 2.12 m in 2000, and was maintained at 2 were positively correlated with SS and negatively cor- *2.0 m through 2003, except during years with low pre- related with transparency. The Najas community was cipitation—between 2007 and 2009. Therefore, water positively correlated with MT, WT, and NO3-N in Axes 1 levels increased 0.2 m over the 25 years. Heavy flooding and 3. Plots representing the Sparganium and Nuphar that caused high water levels (C2.4 m) for [10 days in a communities were scattered around the origin of all three year occurred approximately once every 2 years (Fig. 5). axes. The magnitude of correlations with K?, current The strongest annual winds were mostly southerly, and the velocities, and PO4-P were small. Results indicated that the annual maximum wind velocities declined after 1990. The major variables, which were highly correlated with the concentration of T-N increased gradually from

123 160 123

Table 2 Means ± standard deviations (SD) for 21 environmental variables in the eight communities Community name Average HPvalue Hippuris Zizania Sparganium Nuphar Vallisneria Myriophyllum Najas Trapa

Chemical variables T-N (mg/L-1 ) 6.1 ± 3.0a 1.1 ± 0.7b 1.0 ± 0.6b 1.0 ± 0.7b 0.7 ± 0.6c 0.6 ± 0.5c 1.1 ± 0.5b 0.7 ± 0.4b 1.36 63.5 \0.0001 -1 b ab b ab c c a ab NO3-N (mg/L ) 0.003 ± 0.001 0.826 ± 0.759 0.872 ± 0.848 0.766 ± 0.661 0.612 ± 0.573 0.373 ± 0.516 1.184 ± 0.597 0.460 ± 0.567 0.56 79.9 \0.0001 -1 bc bc c b a a b bc NH4-N (mg/L ) 0.0020 ± 0.044 0.085 ± 0.017 0.103 ± 0.035 0.113 ± 0.061 0.106 ± 0.060 0.091 ± 0.075 0.094 ± 0.011 0.080 ± 0.024 0.09 37.5 \0.0001 -1 b b b b c a b b PO4-P (mg/L ) 0.00 ± 0.00 0.02 ± 0.03 0.04 ± 0.04 0.02 ± 0.03 0.01 ± 0.02 0.03 ± 0.07 0.04 ± 0.04 0.03 ± 0.03 0.02 24.7 \0.0001 EC (mS/m-1 ) 16.0 ± 2.6a 12.9 ± 2.3b 13.8 ± 4.0b 13.7 ± 2.1a 11.6 ± 1.9c 10.8 ± 1.9c 16.2 ± 2.4a 12.7 ± 2.3b 12.7 80.9 \0.0001 2- -1 b b b b a a b b SO4 (mg/L ) 1.9 ± 1.9 5.1 ± 1.9 5.5 ± 2.0 5.2 ± 4.0 4.9 ± 1.7 4.5 ± 1.5 6.2 ± 1.2 4.0 ± 0.8 4.57 47.8 \0.0001 Ca2? (mg/L-1 ) 14.1 ± 2.6a 10.0 ± 2.9c 12.9 ± 7.5c 13.4 ± 5.1b 9.6 ± 3.5d 8.8 ± 2.6d 11.1 ± 2.3b 8.8 ± 1.8c 10.5 47.6 \0.0001 Mg2? (mg/L-1 ) 3.8 ± 1.0a 2.6 ± 0.7b 3.3 ± 1.8b 3.5 ± 1.1a 2.6 ± 0.8c 2.6 ± 0.9c 2.9 ± 0.5a 2.3 ± 0.4b 2.88 38.0 \0.0001 Na? (mg/L-1 ) 12.4 ± 2.5a 8.4 ± 1.3c 10.0 ± 2.6bc 9.7 ± 1.4b 7.8 ± 2.6d 8.4 ± 2.4d 8.4 ± 2.3bc 8.5 ± 0.8bc 8.93 60.5 \0.0001 K? (mg/L-1 ) 2.6 ± 0.5a 2.3 ± 0.8a 3.0 ± 1.1a 2.8 ± 1.3a 2.1 ± 0.8b 2.0 ± 1.9b 2.5 ± 0.6a 2.4 ± 0.7a 2.32 33.7 \0.0001 Cl- (mg/L-1 ) 15.2 ± 5.8a 7.7 ± 1.7a 9.1 ± 2.4a 9.7 ± 1.5b 7.9 ± 1.7c 8.1 ± 3.3c 7.7 ± 0.5a 8.3 ± 1.2a 8.95 67.4 \0.0001 DO (%) 3.2 ± 2.0bc 4.0 ± 2.4c 6.0 ± 0.7bc 6.4 ± 1.1bc 6.9 ± 1.1a 7.1 ± 0.9a 8.6 ± 1.8b 5.0 ± 1.3bc 6.27 96.6 \0.0001 pH 6.56 ± 0.13b 6.77 ± 0.14b 6.96 ± 0.18b 6.97 ± 0.13b 6.98 ± 0.16a 6.97 ± 0.10a 7.02 ± 0.11b 6.77 ± 0.10b 6.9 89.3 \0.0001 SS (mg/L-1 ) 23.0 ± 20.7a 55.8 ± 97.1a 17.9 ± 24.0b 7.0 ± 8.2a 9.2 ± 18.9c 7.5 ± 8.5c 8.8 ± 4.9a 35.7 ± 34.7a 15.6 70.4 \0.0001 Physical variables WT (°C) 13.7 ± 2.2a 19.8 ± 3.3a 16.7 ± 2.3a 16.7 ± 2.0a 16.9 ± 1.5b 16.8 ± 1.2b 23.0 ± 1.1a 21.6 ± 2.7a 17.6 98.9 \0.0001 WD (cm) 19.8 ± 8.0c 33.6 ± 16.1c 65.4 ± 10.3c 70.0 ± 11.8c 65.9 ± 14.5b 76.8 ± 15.8a 72.1 ± 13.6c 50.1 ± 8.7c 61.5 104.7 \0.0001 MT (cm) 6.7 ± 8.9ab 39.1 ± 32.8ab 30.1 ± 35.3b 12.3 ± 18.3ab 4.6 ± 15.8d 6.5 ± 13.7c 84.5 ± 14.2a 64.0 ± 23.3ab 17.6 84.5 \0.0001 CVM (m/s-1 ) 0.0 ± 0.0b 0.01 ± 0.02b 0.08 ± 0.08b 0.02 ± 0.04b 0.02 ± 0.04a 0.01 ± 0.02a 0.01 ± 0.01b 0.01 ± 0.01b 0.02 35.9 \0.0001 CVB (m/s-1 ) 0.0 ± 0.0a 0.01 ± 0.02a 0.06 ± 0.08a 0.01 ± 0.01a 0.02 ± 0.04b 0.01 ± 0.01b 0.01 ± 0.01a 0.01 ± 0.01a 0.01 36.9 \0.0001 Transparency (cm) 30.0 ± 0.0a 23.2 ± 9.4d 30.5 ± 5.5d 29.6 ± 1.2a 29.4 ± 3.0c 29.9 ± 0.4b 33.7 ± 4.9a 23.1 ± 9.4d 29.1 45.8 \0.0001 SWH (m) 0.08 ± 0.03d 0.36 ± 0.05a 0.32 ± 0.07a 0.36 ± 0.06a 0.35 ± 0.06a 0.34 ± 0.07a 0.36 ± 0.01a 0.37 ± 0.02a 0.37 62.8 \0.0001

Number of sites 21 13 11 17 47 53 17 15 18:153–166 (2017) Limnology Difference for each variable among communities was determined by H and the corresponding P value using the Kruskal–Wallis test. The same letter indicates nonsignificant differences between communities according to the Steel–Dwass multiple test (P [ 0.05). Alphabetized letters based on the decision order for mean group values SWH significant wave height, CVB current velocity at bottom depth, CVM current velocity at middle depth, MT mud thickness, WD water depth, WT water temperature, T-N total nitrogen, SS suspended solids, DO dissolved oxygen Limnology (2017) 18:153–166 161

Fig. 4 Canonical correspondence analysis (CCA) ordination of plots graphs are Hippuris, Najas, and Trapa communities (right), and the of aquatic macrophyte communities and 21 environmental variables. other five communities (left). Axis 1, Axis 2, and Axis 3 represent the The upper graphs are Hippuris, Myriophyllum, and Vallisneria relationships between the environmental variables and fluctuation communities (right), and the other five communities (left). The lower trends in communities in all graphs

0.30–0.69 mg/L-1 (1984) to 1.50–1.82 mg/L-1 (2000), and MT increased between 1995 and 2003, decreasing which was approximately three times higher than in 1984, slightly until 2009 (Fig. 6). After which T-N was maintained at high values, 1.52–2.06 mg/L-1 in 2003 and 1.85 mg/L-1 in 2009. Although the concentration of Cl- was not measured after Discussion 2004, it decreased gradually from 6.33–15.33 mg/L-1 (1984) to 4.3–5.6 mg/L-1 (1998), *50 % of the value in CCA and the Kruskal–Wallis test revealed that SWH 1984. Cl- then slightly increased and became exhibited the highest correlation with the occurrence of stable (7.0–7.6 mg/L-1 in 2003). SS values showed no aquatic macrophyte communities in Utonai-ko, followed tendencies, and pH values slightly fluctuated from 7 to 8 by WD, T-N, DO, pH, Cl-, transparency, MT, and SS in between 1984 and 2009. DO concentration increased descending order of magnitude of correlation. The most gradually from 8.3 mg/L-1 (1984) to 11.6 mg/L-1 (2010), significant changes in the communities occurred recently in

123 162 Limnology (2017) 18:153–166

Fig. 5 Change over 25 years 40 above 2.3m for three flooding events (C2.3, above 2.4m 30 C2.4, and C2.5 m), water level, above 2.5m annual maximum wind velocity, days 20 T-N, pH, dissolved oxygen 10 - (DO), Cl , and suspended solids 0 (SS) in Utonai-ko 1984 1985 1986 1987 1988 1989 1990 1991 1992 1993 1994 1995 1996 1997 1998 1999 2000 2001 2002 2003 2004 2005 2006 2007 2008 2009 2010 2.8

2.6

2.4

2.2

2

1.8

1.6 water level (median elevation) and flooding and elevation) (median levelwater water level elevation (m) 1984 1995 1987 1991 1994 1986 1990 1998 1985 1989 1997 2002 1988 1993 1996 2001 1992 1999 2000 2004 2003 2007 2008 2006 2005 2010 2009 Year

30 SW SSW SE NNW SE SE SSE SW 20 SE N SE SE SE ESE SW ESE N SE SE SE SSWSSW N SE SE SSW ESE 10

0 wind velocity(m/s) wind annual maximum maximum annual 4 ) 3

2

1 T-N(mg/l 1985 1988 1990 1993 1995 1998 2000 2003 2005 2010 1984 1986 1989 1994 2001 2006 2008 1987 1991 1992 1996 1997 1999 2002 2004 0 2007 2009

9

8

pH 7

6 1988 1993 1996 1997 2005 2008 2010 1985 1987 1991 1992 2000 2001 2002 2004 2006 2009 1984 1986 1989 1990 1994 1998 1999 1995 2003 2007 13

11

9 DO(mg/l) 198 8 199 0 199 5 199 7 199 9 200 4 200 6 200 8 201 0 198 5 198 7 198 9 199 1 199 2 199 4 199 6 199 8 200 0 200 1 200 3 200 5 200 7 200 9 7 198 4 198 6 199 3 200 2

30 20

(mg/l) 10 - 0 Cl

80 60 40 20 SS( (mg/l) 0 1987 1991 1986 1990 1985 2005 1989 1984 1995 1988 1999 1994 2007 2003 1998 1993 2006 2002 1997 1992 2010 2001 1996 2009 2000 2008 2004 Year

123 Limnology (2017) 18:153–166 163

100 40 1995 30 1984 80 2003 20 60 10

2009 0 40 40

number 2003 20 30 20 0 10 ˂1 1≤,≤10 10˂,≤20 20˂,≤30 30˂,≤40 40< (cm) 0 class of mud thickness 40 30 2009

Fig. 6 Changes in the mud thickness from 1995 to 2009 number of occurrence 20 10 Utonai-ko, being a decrease of the Hippuris community 0 ≥ 90 and increase of the Vallisneria and Myriophyllum com- 0-9 10-19 30-39 40-49 50-59 80-89 20-29 60-69 70-79 munities. SWH decreased from 1984 to 2009, which was depth(cm) expected to increase the Hippuris community and decrease community: the Vallisneria and Myriophyllum communities. These Hippris Zizania communities, however, changed in the reverse direction Sparganiumu Nuphar Myriophyllum Vallisneria through the years. Therefore, although SWH should affect Najas Trapa the occurrence of communities, it cannot explain the major changes observed in community occurrence. During Fig. 7 Years of change in the number of occurrences (left) and changes in the aquatic macrophyte communities over this occurrence ratio (right) of aquatic macrophyte communities along the 10-cm intervals of water depth same period, WD increased and distribution area of the Hippuris community prominently decreased, whereas that of the Vallisneria and Myriophyllum communities of WD. Because a low concentration of Cl- does not increased. Thus, WD could explain the changes in occur- restrict the occurrence of aquatic macrophytes (Kadono rence of these communities. Drastic declines of aquatic 1982), it was judged as being less effective than WD in macrophyte communities in were also explaining the observed changes in communities. Trans- caused by increased water levels (Nishihiro 2011). T-N parency, SS, and MT were not effective factors in increased from 1984 to 2009, which was expected to explaining Hippuris, Vallisneria, and Myriophyllum com- increase the Hippuris communities and decrease the Val- munity distributions. As the result, the most effective factor lisneria and Myriophyllum communities. A positive cor- correlated with the major changes over 25 years in Utonai- relation between T-N and the occurrence of the Hippuris ko was WD. Changes in the distribution pattern of aquatic community has also been reported in a small river (Katagiri macrophyte communities from 1984 to 2009 are shown in et al. 2010). As previously stated, however, these com- relation to WD in Fig. 7. In 1984, WDs were shallower munities changed in the reverse direction. Therefore, T-N than 60 cm in most parts of Utonai-ko. Furthermore, in cannot explain the changes observed in community 2003, shallow areas (0–29 cm) were not surveyed because occurrence. DO in Utonai-ko increased from 1984 to 2009, many had no plants (Hokkaido Government 2004). which could explain changes in the occurrence of com- The Hippuris community dominated the shallow areas in munities. DO, however, was considered ineffective in 1984 (0–29 cm depth), and the Vallisneria and Myriophyl- altering community occurrence, because the change in DO lum communities occurred from 20 to 29 cm and dominated levels was negligible through the years: \2mgml-1. deeper areas. The Hippuris community in 2003 and 2009 was Because pH values were constant from 1984 to 2009, it distributed scarcely in shallow areas (10–29 cm), and the cannot explain the change in community occurrence. Vallisneria and Myriophyllum communities occurred from The concentration of Cl- decreased from 1983 to 2009 30 to 39 cm and dominated the deeper areas. Accordingly, in and could explain the decrease in the Hippuris community Utonai-ko pond, the Hippuris community was distributed in and increase in the Vallisneria and Myriophyllum com- shallower waters, and the Vallisneria and Myriophyllum munities, as well as WD. Concentration of Cl- was low; communities were in deeper water. H. vulgaris grew in the however, \100 mg/L-1 in Utonai-ko, and the correlation shallow littoral zone, tolerated well the drawdown of lakes with the occurrence of communities was smaller than that (Mjelde et al. 2013), and is considered to be a drawdown-

123 164 Limnology (2017) 18:153–166 tolerant competitor, which has the advantage in shallow and Nuphar communities did not correlate with any vari- areas (Greulich and Bornette 1999; Mjelde et al. 2013). ables in this study. Occurrence of the Hippuris community was negatively Flooding disturbance is also an important factor in the correlated with WD in the shallow upstream of a small river occurrence of aquatic macrophytes (Kautsky 1988; Murphy (Katagiri et al. 2010). These findings support that the major et al. 1990; Abernethy et al. 1996; Greulich and Bornette habitat of H. vulgaris is shallow water. 1999; Pedersen and Riis 1999; Willby et al. 2000; Sharip V. asiatica and M. spicatum also grow in deeper areas in et al. 2012). However, because flooding by heavy rains other regions: 1.0–8.0 m for V. asiatica (Kautsky 1988; caused by tropical depressions consistently occurred Nagasaka et al. 2003; Hasegawa and Yoshizawa 2013) and between late summer and autumn every 2 or 3 years 0.2–6.0 m for M. spicatum (Nagasaka et al. 2002; Haga (Fig. 7), this disturbance cannot explain the change in et al. 2006; Feldmann and Noges 2007; Hasegawa and aquatic macrophyte communities over the past 25 years. Yoshizawa 2013). Moreover, we found that the Vallisneria M. spicatum is a disturbance-adapted competitor, shoots of community dominated shallower areas than did the which can rapidly recover after destruction of communities Myriophyllum community; the former dominated the 60- to (Kautsky 1988; Murphy et al. 1990; Abernethy et al. 1996); 79-cm-deep areas in 2003 and 40- to 59-cm-deep areas in this would result in the predominance of Myriophyllum- 2009, whereas the latter dominated the deeper areas dominated communities in large areas in Utonai-ko pond. (C80 cm in 2003 and C60 cm in 2009). In Utonai-ko, the mean catch of Cyprinus carpio L was Wave action affects the occurrence of aquatic macro- 1.4 ± 0.19 t from 1988 to 2010. Although the catch fluc- phyte communities by removing biomass or increasing tuated with 5-year periods, it has not changed significantly turbidity (Jupp and Spence 1977; Chambers 1987; Durarte over 22 years (Hokkaido Government 1989–2011). Many and Kalff 1986). In 1984, the Hippuris community was Auser albifrons frontalis Scopoli and other herbivorous distributed in shallow areas, C2 and D2, of the interior area waterfowl come to the pond for foraging from October to and along the southern shores (Fig. 3). The shallow area on November, and the maximum number of A. albifrons the northwest shore had no plants, because wave action observed within a day was 3480 in 2015 (Nakamura 2015). caused by a southerly monsoon (Tomakomai Weather Although we cannot evaluate the effects of waterfowl Station 2010) decreased the aquatic macrophyte commu- foraging, they might not be significant, because the birds nities and restricted the occurrence of H. vulgaris. The use the pond outside of the growing season for aquatic margins of the southern shores formed a steep slope or macrophytes. Because allelopathic compounds produced cliff, rimmed by a several-meter-wide and a 1-m-high bank by M. spicatum do not suppress other aquatic macrophytes, on which large and emergent plants (Phragmites australis and blue-green algae (Nakai et al. 1998; Chase and Knight (Cav.) Trin and Carex lyngbyei Hornem) grew densely. 2006) and planktonic algal blooms did not occur in Utonai- Accordingly, topography of the southern shore caused the ko, this factor was also discounted. shallow flat areas to disappear by increasing the water In conclusion, 25 years of change in the distribution of table after 1984. Increasing the water levels, therefore, aquatic macrophyte communities in Utonai-ko was caused caused the shallow areas to disappear from the interior area by the increase in WD of the pond, which has decreased the and the southern shores, resulting in the significant recent habitat of the Hippuris communities and extended those of decline of the Hippuris community. the Vallisneria and Myriophyllum communities. The occurrence of the Zizania and Trapa communities were positively correlated with SS and negatively with Acknowledgments We would like to thank Mr. N. Matusmoto for transparency. Because SS reduces water transparency his technical advice in the interpretation of water chemistry data, and Editage (http://www.editage.jp) for English-language editing. We are (Hanashiro et al. 1994; Ito and Mizoguti 1995), trans- also grateful to the Hokkaido Government Iburi General Subprefec- parency showed the highest negative correlation with SS tural Bureau for providing data on water levels at Utonai-ko. This (r =-0.477, P \ 0.001) in Utonai-ko. Reduction of study was partly supported by funds provided as grants in aid for transparency because of the increase in SS reduces the scientific research (Number 21510242) from the Ministry of Educa- tion, Science and Culture, Japan. biomass of submerged aquatic macrophytes and their communities (Havens 2003). The Najas community was positively correlated with MT and expanded from 1995 to 2003, corresponding to the References increase in MT, but then disappeared in 2009. Neverthe- less, mud was apparently thicker in 2009 than in 1995. Abernethy VJ, Sabbatini MR, Murphy KJ (1996) Response of Elodea canadensis Michx. and Myriophyllum spicatum L. to shade, Therefore, MT cannot explain the change in community cutting and competition in experimental culture. Hydrobiologia occurrence in Utonai-ko pond. Changes in the Sparganium 340:219–224

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