Seasonal Changes of Shallow Aquatic Ecosystems in a Bird Sanctuary Pond

ABSTRACT The seasonal effects of nutrient loading from migratory waterfowl on water and the successive changes of the aquatic ecosystem based on each biomass of phytoplankton, zooplankton and submerged macrophytes were surveyed in Tsubasa Pond, Yonago Waterbird Sanctuary, Japan. The pond’s water quality gradually deteriorated with the influx of migratory waterfowl. The concentration of total nitrogen corresponded rapidly with waterfowl biomass. Peak concentrations of total phosphorus and chlorophyll a (Chl.a) were observed about one month later when the migratory waterfowl had flown away. After one month, the peak concentration of Chemical Oxygen Demand (CODMn) appeared. Thus, the water quality of the pond had gotten worst after the waterfowl had flown away. Then, decrease of Chl.a concentration and increase of zooplankton density were observed in spring. In summer, the population of a submerged macrophyte increased temporarily and water quality recovered. These results indicated that the primary producer in the bird sanctuary pond alternated from phytoplankton to submerged macrophyte in one year

Address correspondence to Masako Nakamura, The United Graduate School of Agricultural Sciences, Tottori University, Email: himasako4713@yahoo.co.jp

Seasonal Changes of Shallow Aquatic Ecosystems in a Bird Sanctuary Pond

Masako NAKAMURA*, Tohru YABE**, Yuichi ISHII**, Kaname KAMIYA***, Morihiro AIZAKI****

*The United Graduate School of Agricultural Sciences, Tottori University, 4-101

Koyama-Minami, Tottori-City, Tottori 680-8553, Japan

**Environmental Biology Division, National Institute for Environmental Studies, 16-2

Onogawa, Tsukuba-City, Ibaraki 305-8506, Japan

***Nakaumi Waterbird International Exchange Fund Foundation, Yonago Waterbird Sanctuary,

665, Hikonashinden, Yonago-City, Tottori, 683-0855, Japan

****Faculty of Life and Environmental Science, Shimane University, 1060 Nishikawatsu-cho, Matsue-City, Shimane 690-8504, Japan

ABSTRACT

The seasonal effects of nutrient loading from migratory waterfowl on water and the successive changes of the aquatic ecosystem based on each biomass of phytoplankton, zooplankton and submerged macrophytes were surveyed in Tsubasa Pond, Yonago Waterbird Sanctuary, Japan The pond’s water quality gradually deteriorated with the influx of migratory waterfowl The concentration of total nitrogen corresponded rapidly with waterfowl biomass Peak

concentrations of total phosphorus and chlorophyll a (Chl.a) were observed about one month

later when the migratory waterfowl had flown away After one month, the peak concentration of Chemical Oxygen Demand (CODMn) appeared Thus, the water quality of the pond had gotten

worst after the waterfowl had flown away Then, decrease of Chl.a concentration and increase of

zooplankton density were observed in spring In summer, the population of a submerged macrophyte increased temporarily and water quality recovered These results indicated that the primary producer in the bird sanctuary pond alternated from phytoplankton to submerged macrophyte in one year

Keywords: migratory waterfowl, seasonal changes of water quality, shallow aquatic ecosystems

INTRODUCTION

Waterfowl such as Anseriformes (geese, swans, and wild ducks), cormorants, egrets, coots, gulls and other seabirds have various impacts on water environment Especially, the effects of waterfowl on water quality are important for aquatic ecosystem and there

have been much studies on that (Gould and Fletcher, 1978; Bédard et al., 1980; Portnoy, 1990; Bales et al., 1993; Dobrowolski et al., 1993; Baxter and Fairweather, 1994; Manny et al., 1994; Marion et al., 1994; Enari and Shibasaki, 1995; Smith and Craig, 1995; Gwiazda, 1996; Kitchell et al., 1999; Hahn et al., 2007; Nakamura et al., 2010)

Anseriformes are typically migrating waterfowl to Japan in winter They affect lake and pond ecosystems greatly because they have big bodies and form in large groups (Jefferies, 2000) Most Anseriformes are herbivorous and tend to feed in paddy fields in

Japan (Takeichi and Arita, 1994; Yamamoto et al., 1999; Shimada, 2002) In case their

feeding and roosting places are different, they are considered to work as transporters of nutrients from the feeding place to the roosting place Thus, it is considered that Anseriformes play a role in the purification of feeding places (Gere and Andrikovics,

1992; Tamisier and Boudouresque, 1994; Yamamuro et al., 1998) On the other hand,

they play a role in the eutrophication of roosting places Indeed, eutrophication was

found in Anseriformes roosting area, and it was considered to occur due to the addition

of nutrients from migratory Anseriformes (Enari and Shibasaki, 1995; Ogawa et al., 1997; Pettigrew et al., 1998; Kitchell et al., 1999; Olson et al., 2005) However, most of

these studies were carried out only during the period of stay of migratory Anseriformes

Only Olson et al (2005) have performed a short period study after the Anseriformes

flew away

In this study, the first objective is to clarify the seasonal effects of nutrient loading from waterfowl on water throughout the year in a bird sanctuary pond The second is to discuss the successive changes of the aquatic ecosystem based on each biomass of phytoplankton, zooplankton and submerged macrophytes in the pond

MATERIALS AND METHODS

Study Site

This study was conducted in Tsubasa pond in Yonago Waterbird Sanctuary that is home

to many Anseriformes, and is the largest place for wintering tundra swans (Cygnus

columbianus) in western Japan Yonago Waterbird Sanctuary, located in Tottori

Prefecture, Japan (35º 26” N, 133º 172” E), was constructed after partial reclamation on Lake Nakaumi in 1994 The sanctuary consists of Tsubasa pond and surrounding a reed wetland (Fig 1) The pond area is 17 ha with an average water depth of 60 cm, and a volume of 102,000 m3 Water temperature varied from 2ºC to 30ºC, and salinity varied from 3 psu to 8 psu The inflow water to Tsubasa Pond is basically rainfall, and the outflow water to Lake Nakaumi is through the overflow of artificial drain ditch

Observation, Sampling and Analysis

The number of waterfowl was counted identifying their species at the observation center shown in Fig 1 Observations were conducted between two and four times in a month from March 1999 to September 2000, and the total number of observations was forty The total waterfowl weight (TWW) in an observation was calculated as follows;

TWW = Σ NB k × AW k (1)

where, n is the number of species in an observation, while NBk and AWk are the number

of birds of each species and the average weight of each species, respectively It was

found out that avian basal metabolism is proportional to the body weight (Nagy et al.,

1999), and birds excrete at a rate of about 20% of basal metabolism (Kurechi and Otsu, 1983) Hence, in this study, the excretion was evaluated by using the body weight study Water samples were collected at the pond shore as shown in Fig 1 so as not to disturb the waterfowl migration The samples were placed in polypropylene bottles, immediately cooled with ice and taken to the laboratory After subsamples for total nitrogen (TN), total phosphorus (TP) and chemical oxygen demand (CODMn) measurements were taken, the remaining water sample was filtered through a glass fiber filter (GF/F, Whatman, USA) The solid samples remaining on filters were used for

Chlorophyll-a (Chl.a) measurement

Samples for TN and TP concentrations were determined with a continuous-flow

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Fig.1 - Location of Yonago Waterbird Sanctuary and Tsubasa Pond, with water sampling

point (●), Shaded area shows the land and dotted area shows the reed bed

analyzer (AAII, Bran+Luebbe, UK) after alkaline peroxydisulfate digestion and

peroxydisulfate digestion, respectively (APHA et al., 1998) Samples for CODMn was

measured by the potassium permanganate method (JISC, 1998) while Chl.a

concentration was measured by the SCOR/UNESCO method with methanol extraction

(Marker et al 1980)

Phytoplankton and zooplankton samples were collected twice a month from March to November 1999 from the water surface Phytoplankton with unfiltered water were fixed with a glutaraldehyde solution Samples of zooplankton were collected using a plankton net (NXX25) and fixed in the same manner as for phytoplankton Plankton genera were identified and counted under a microscope (BH2-PFK-1, OLYMPUS, Japan) according

to Mizuno (1977) and Akiyama (1996)

The standing crop of dominant submerged macrophytes was surveyed every month from March to November 1999 The aboveground parts were collected, using a 15 cm ×

15 cm quadrate, from four sites each month Collected samples were dried at 80ºC for

48 hours and the dry weights were measured

RESULTS AND DISCUSSION

Seasonal Change of TWW

At Tsubasa Pond, a maximum of about 500 geese, 1,000 swans and 10,700 wild ducks migrated during the study period Among the waterfowl observed in the study pond, the geese, swans, ducks, grebes, cormorants, herons, egrets, coots, snipes, plovers and gulls are generally known to excrete in water The sum of the weight of each species during the surveillance period was calculated Then, the 10 species of cormorants, geese, swans, and ducks, accounted for more than 98% of TWW during the surveillance period Total weight of each species and its ratio to TWW for 10 dominant species are shown in Table

1

As a result of the observations, seasonal change of TWW in Tsubasa Pond was divided into four terms : term S3 (March), migrating waterfowl flying to the north; term A (April

- August), absence of migrating waterfowl using the pond; term S1 (September), a large amount of migrating waterfowl arriving from the north; term S2 (October - February), waterfowl using the pond as a wintering place Thus, migratory waterfowl stayed

Table 1 - Total weight of each species and its ratio to the sum of TWW for 10 dominant

species Average weights of each species were the average of minimum and maximum weight data (Wild Bird Society of Japan, Ehime Branch, 1995;

Higuchi et al., 1996)

M A M J J A S O N D J F M A M J J A S

A S1 S2

0 2500 5000 7500 10000

Month

M A M J J A S O N D J F M A M J J A S

M A M J J A S O N D J F M A M J J A S

A S1 S2

S3 A S1 S2 S3 A S1

S3 A S1 S2 S3 A S1

0 2500 5000 7500 10000

Month

Fig.2 - Seasonal change of TWW in Tsubasa Pond Shaded area indicates a period when

migratory waterfowl were staying in the pond

mainly in the pond at S2

The seasonal change of TWW is shown in Fig 2 TWW was 5,000 kg at the beginning

of the study period It decreased rapidly in March 1999 (term S3) because most waterfowl had flown to the north It was below 400 kg in May 1999, during term A TWW increased in September 1999, in term S1, with the arrival of the migratory waterfowl and sometimes reached to about 7,500 kg in term S2 Since March 2000, it decreased rapidly and was less than 400 kg in April 2000, which was term A again

Seasonal Changes in Water Quality

The seasonal changes in water quality are shown in Fig 3 TN concentration of 3.0 mg/L was observed at the beginning of the study period, in term S3, and decreased

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Fig.3 - Seasonal changes in water quality of Tsubasa Pond Shaded area indicates a

period when migratory waterfowl were staying in the pond

during term S3 to a low value of 0.7 mg/L in July, in term A TN concentration increased rapidly to a maximum value of 5.8 mg/L which was observed in December 1999, during term S2 Then it started to decrease in the latter part of term S2 (Fig 3-a) TP concentration of 0.33 mg/L was observed at the beginning of the study period, in term

S3, and subsequently decreased to 0.05 mg/L in July (term A) In terms S1 and S2, TP concentration increased and showed a maximum value of 0.38 mg/L in March 2000, in term S3 (Fig 3-b) CODMn concentration of 12.6 mg/L was observed at the beginning of the study period, in term S3 and showed little fluctuation In the latter part of term S2

and S3, CODMn concentration increased and showed a maximum value of about 100

mg/L in April 2000, in term A (Fig 3-c) Chl.a concentration of 95.9 mg/L was

observed at the beginning of the study period, in term S3, and decreased to about 10

mg/L in June 1999, in term A Chl.a concentration showed a peak in the beginning of

term S2 and then it increased rapidly Then, it showed a maximum peak of 153 mg/L in March 2000, in term S3 (Fig 3-d)

0 25 50 75 100

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Chl.a zoo plankton submerged macrop hyte

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1999

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a

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aa

Fig.4 - Seasonal changes of Chl.a concentration, zooplankton density and aboveground

biomass of a dominant submerged macrophyte in Tsubasa Pond between March and November 1999

Seasonal Changes of Plankton and Submerged Macrophyte

The genera of Anabaena, Merismopedia, Oscillatoria, Melosira, Cyclotella, Navicula,

Gyrosigma, Chlamydomonas, Synura and Euglena were observed during the study

period The dominant genera were Euglena in March and Cyclotella in October Eight genera of zooplankton and protozoa such as Difflugia, Arcella, Stylonychia, Brachionus,

Keratella, Monostyla, Asplanchna and Mesocyclops were observed

A high density of zooplankton was observed at the end of April and May, and the

dominant genera were Keratella and Difflugia, respectively One of the submerged macrophytes, Potamogeton pectinatus, dominated and covered in the pond during

summer and autumn The other submerged macrophytes, Najas marina, Zannichellia

palustris, Ruppia maritima and Chara sp., were also observed in summer (Kamiya and

Kunii, 2001)

Seasonal changes of Chl.a concentration, zooplankton density and aboveground

biomass of a dominant submerged macrophyte, P pectinatus, are shown in Fig 4 The

concentration of Chl.a increased rapidly in March, and zooplankton density showed

peaks in April and June The zooplankton density increased rapidly after the decrease in

Chl.a concentration The aboveground biomass of P pectinatus was observed first in

May and covered the pond’s surface between July and August The biomass showed a peak in August

Effects of Waterfowl on Water Quality and Successive Seasonal Changes of Shallow Aquatic Ecosystem

Relative values of water qualities and some ecosystem components in Tsubasa Pond were calculated using monthly average data and the values are shown in Fig 5 The TN observed to have their perks in term S3 and A, respectively When the worst water quality was observed in term S3 after the waterfowl flew away, a peak was observed in the order of TP and CODMn In term A, when Chl.a concentration decreased rapidly,

zooplankton proliferated Subsequently in this term, water quality was maintained in a

better condition for submerged macrophytes and P pectinatus prosperedtemporarily It was considered that the primary producer changed from phytoplankton to submerged

TN

TP

Chl.a

COD

Submerged macrophyte zooplankton

0 25 50 75 100

0 25 50 75

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Fig.5 - Relative values of water quality parameters and some ecosystem components in

Tsubasa Pond (term S3: March, term A: April - August, term S1: September, term

S2: October - February)

macrophyte between term S3 and A Then sunlight easily seemed to reach the pond bottom with a decrease of plankton biomass The shallowness of the whole pond might have caused such a dynamic change of primary producer The pond alternated between submerged-macrophytes-dominant clear-water state and phytoplanktons-dominant turbid-water state in one year It was found that there is a difference in the case of

catastrophic changes reported by Scheffer et al (2001) and this study, i.e in a bird

sanctuary pond aquatic ecosystem changes cyclicly

ACKNOWLEDGMENTS

We would like to thank the staffs and the volunteers of Yonago Waterbird Sanctuary, especially K Kirihara, for counting the waterfowl Special thanks are forwarded to Professor S Otani of the Faculty of Education, Shimane University, for his assistance in the determination of phytoplankton We thank K Fujioka, T Kuwabara, A Takahashi and the other 1999 - 2001graduates of Environmental Ecology Engineering Laboratory, Faculty of Life and Environmental Science, Shimane University for conducting the sampling and chemical analyses Also, we are indebted to General Manager N Nakajima, Senior Researcher M Tamaoki and the other members of Environmental Biology Division, National Institute for Environmental Studies for improving our English and for making valuable comments on drafts

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