ISSN 2185-2995

Laguna (2010) 17: 15-21

High tide dispersion of marine benthic foraminifera into brackish
waters: implications for dispersion processes during sea-level rise
Ritsuo Nomura1・Koji Seto2・Akira Tsujimoto3
Abstract: We observed that benthic foraminifera utilize suspended particles as atransportation medium during dispersion to other areas. Six cylindrical bottles (7.3 cm
diameter, 15.5 cm height), placed at 1 meter depth intervals at one location in brackish

Lake Nakaumi (sample location depth 6.5 m), contained a number of live individuals of

Quinqueloculina tubilocula. The occurrence of Quinqueloculina was associated with an
exceptionally high tide event related to a low atmospheric pressure front on September

1st, 2002. They were most abundant in the bottle at 3 meters depth and least abundant at

6 m depth. The high tide event was very unusual in this region, which normally has very
moderate tidal amplitudes. The presence of this exotic marine benthic foraminifer in abrackish lake indicates that one of the most effective methods of dispersion for both live anddead foraminifera is on suspended particles during high tides. High organic matter content

in suspended particles provides sufficient food to maintain live foraminifera. The occurrenceof Q. tubilocula in an oligohaline to mesohaline brackish water system is good evidence thathigh tides can contribute to dispersion, and thus dispersion can also be facilitated by a risein sea-level.

Key words: high tide dispersion, foraminifera, suspended particles, sea-level rise, lagoon

Introduction

are able to move in and on the sediment surface,

There has been a long standing discussion on the

millimeters per hour (Kitazato, 1988). Some sort ofthey are surprisingly slow, moving at speeds of a few

dispersion processes of benthic foraminifera. Manytransport mechanism is therefore needed to account for

micropaleontologists have encountered occurrences ofthe long distance transport implied by the presence of

exotic foraminiferal taxa in indigenous assemblages.

exotic foraminifera in local assemblages. Alve (1999)

In ecological studies of planktonic foraminifera usingsuggested four different ways of dispersion: (1) releaseplankton tows, live and dead benthic foraminifera haveof both sexually and asexually produced individuals

been collected combined with the expected planktonic

into the water column, (2) meroplanktonic adaptation,assemblages (Murray, 1965; Lidz, 1966; Loose, 1970;(3) self locomotion, and (4) passive entrainment into the

Hueni et al., 1978). Although live benthic foraminifera

water column. Post-mortem transportation mechanisms

1

Foraminiferal Laboratory, Faculty of Education and Research Center for Coastal Lagoon Environments, Shimane University, Matsue, 690-8504, Japan

2

Research Center for Coastal Lagoon Environments, Shimane University, Matsue, 690-8504, Japan

3

Faculty of Education, Shimane University, Matsue, 690-8504, Japan

Reccived: 24 November 2010, Accepted: 29 December 201015

Ritsuo Nomura・Koji Seto・Akira Tsujimoto

have been well studied (summarized by Murray, 1991).

of bottom water ranges from 21 ‰ in winter to 33 ‰ inmechanism, although others are attested, such as bed

is highly nutrient rich, which has triggered a red-tide

Suspension load transport is the most commonly reported

summer, with an average of 29 ‰. Lake Nakaumi waterload and turbidity currents. Small and well preserved

event in every year of recent times. Because the lake isforaminiferal tests in suspension loads are almost

connected to the Sea of Japan through a narrow channel

always due to dead individuals. Empty tests are easy

(about 230 m width), the water circulation of Laketo suspend in the water column and disperse widely

Nakaumi is suppressed, and it has been estimated to takeunder turbulent conditions. However, there have been

about one week for the replacement of lake water withvery few observations of transport of living individuals.

coastal sea-water (Okuda, 1997).

The increased mass may make living individuals more

Although foraminiferal abundance in sediment samples

difficult to suspend initially, but there are a number

is very high in this eutrophic lake, the assemblage is veryof mechanisms that will keep foraminiferal tests insuspension. Tidal effect and the mixing potentials

simple, only represented by Ammonia “beccarii” andTrochammina hadai (Nomura and Seto, 1992). These twomaintaining suspension in estuary systems (Wanghadai is common in deeper, organic rich, argillaceousof freshwater and seawater can be major causes for

taxa have different ecological preferences. Trochammina

and Murray, 1983). Murray (2006) summarized thesediments, while Ammonia “beccarii” lives in a wider

recent work on foraminiferal dispersion in both coastal

range of salinity and substrate conditions, including

and deep-sea areas. Propagule dispersion at the earlylower mesohaline conditions and coarse-grained sandreproductive stage, as proposed by Alve and Goldstein

sediments (Nomura and Seto, 1992).

(2002, 2003), is clearly an attractive mechanism when

considering the mixed occurrence of both indigenous andexotic foraminifera.

In order to examine annual change in estuarine

foraminiferal productivity, the dynamics of bottom

sediments, and the dispersion processes of sedimentary

particles in relation to wind stresses, tidal effects, andthe magnitude of precipitation, we placed plastic bottles
at different depths in brackish Lake Nakaumi from
December, 2001 to January, 2003. During the earlystages of this research, we found live foraminifera inthese traps associated with suspended particles (Nomura
and Seto, 2004). This observation, foraminifera using

suspended organic particles, seems to be good evidence
for dispersion by passive entrainment, which would be

Fig. 1 Index map and major foraminiferal taxa. (1)paper we report the occurrence of marine foraminifera

trap and Nakaumi Observatory, depth ca. 6.5 m. (2)an effective way to expand a species’ habitat. In thisNO with arrow indicating the position of the sedimentin brackish waters and discuss the implications of the

Quinqueloculina tubilocula Zheng collected in thepresence of these exotic foraminifera in terms of asediment trap. (3) Ammonia “ beccarii” (Linné) (4)response to sea-level rise.

Trochammina hadai Uchio. These specimens were
stained with rose-bengal solution.

Waters of Lake Nakaumi and foraminiferal
assemblage
Lake Nakaumi is a typical brackish lake, sitting

in between Miho Bay, part of the Sea of Japan, andmesohaline Lake Shinji (Fig. 1). A stable halocline
develops at depths 3-4 m throughout the year. The salinity

16

High tide dispersion of marine benthic foraminifera into brackish waters:
implications for dispersion processes during sea-level riseThis trap was emplaced for intervals of approximately

Methods and Results

one month.

A total of six plastic bottles (7.3 cm diameter; 15.5

The above mentioned live and dead foraminifera

cm height) were placed in the central part of the lakewere commonly found in these bottles, particularly

approximately 10 km upstream of the Sakai Channel

foraminifera were trapped in these bottles, and they(latitude 35°27’58.59” N; longitude 133°11’25.92” E),in the three traps set below the halocline depth. Live

(Figs. 1, 2). Each bottle trapped suspended sediments

were common from July to October (Table 1; Fig. 2).

over one meter intervals at a location of 6.5 meters depth.

Dead foraminiferal tests decreased significantly from

Fig. 2 Monthly occurrence of live foraminifera at different depths in 2002. Individual numbers are actual count per thebottle and per sampling interval. Interval 1 = Dec. 16, 2001 - Jan. 7, 2002; Interval 2 = Jan. 7 - Feb. 17; Interval 3 =Feb. 17 - Mar. 8; Interval 4 = Mar. 8 - Apr. 6; Interval 5 = Apr. 6 - May 6; Interval 6 = May 6 - Jun. 13; Interval 7 = Jun.
13 - Jul. 12; Interval 8 = Jul. 12 - Aug. 10; Interval 9 = Aug. 10 - Sep. 11; Interval 10 = Sep. 11 - Oct. 13; Interval 11 =Oct. 13 - Nov. 8; Interval 12 = Nov. 8 - Dec. 5. Note abundant Quinqueloculina tubilocula occurred at 3 m depth in theInterval 9.

Table 1 Foraminiferal occurrences shown in Figure 2.

17

Ritsuo Nomura・Koji Seto・Akira Tsujimoto

December to early May. Live Trochammina hadai wasshallowed when seawater influx triggered the mixing

the upper bottles above the halocline. Live Ammonia

water. Immediately prior to this unusual tide the water

generally abundant in the deeper bottles and rare inof deep high salinity water and shallow low salinity“beccarii” is active and occurred even at 1m depth. In the2002 trapped sediment, A. “beccarii” was less abundantlevel was + 48 cm at T. P., and the 42 cm level increase
was made up of central Nakaumi water.

during the spring bloom, but in general A. “beccarii” ismore common in comparison with T. hadai.

Quinqueloculina tubilocula is common in the Sakai

Channel, but this form does not occur in the main body ofLake Nakaumi. In the sediment trap emplaced in August
10 to September 11, 2002, we found live individuals of Q.
tubilocula in association with the Nakaumi assemblage ofA. “beccarii” and T. hadai (Figs. 1, 2). Dead individualsof Q. tubilocula were not found in this assemblage.
All individuals are small in size (< 250 μm length inmax.). The maximum occurrence was 528 individuals

in the bottle at 3 meters depth, and the minimum was 14

individuals in the bottle at 6 meters. The standing crop of
this species accounts for 74 % of the assemblage. Only a

few individuals of Q. tubilocula occurred in the months
before and after the event-driven month. This event was
clearly a very exceptional occurrence.

Fig. 3 Tide level changes at the Nakaumi Observatory

Discussion

in 2002. Abnormal tidal height occurred on September

1, 2002. (Data from Ministry of Land, Infrastructure andQuinqueloculina occurrence in the time of high tide

Although these Quinqueloculina tubilocula individuals

Transport). Numerals in parentheses indicate the date of

population through the influx of seawater into Lakeeach sample.

Nakaumi system is not adequate to transport living Q.

Implications for marine foraminifera in lagoon

the Sea of Japan; for instance, the annual amplitudeSuspended load transport is clearly the most likely

bottle exchange. Number in box indicates the month ofwere clearly transported from the Sakai Channel
Nakaumi, the normal exchange of seawater in theenvironments and in response to sea-level rise

tubilocula into the lake. Tidal amplitudes are small in
was usually 33.6-43.3 cm at the Sakai tidal observatory

explanation for the occurrence of exotic foraminifera

only occurrence of marine forms in our sediment traps

tidal currents can be transported for long distances andin recent 8 years (2002-2009). This event was thein the Lake Nakaumi traps. Suspended material inthroughout the life of this study. They did not occur

these can contribute to assemblages that mix exotics

under the normal tidal mixing regime in other seasons

with indigenous taxa. The chances of long distanceand other years, except for 2002 in the studied years

transport of foraminiferal tests increase with increased(2000-2003).

tidal strength. Wang and Murray (1983) discussed the

An exceptionally high tide occurred on September 1st,transport of foraminifera in brackish systems as based on

2002 (Fig. 3). This high tide was caused by an unusually

the mixing of freshwater and seawater. Under microtidal

strong atmospheric low pressure passing through thisconditions (when mixing is weak), however, the potential

area. When the water level rose to about + 90 cm atfor foraminiferal transport is small. Our observations

the Mean Sea Level of Tokyo Bay [traditionally usedindicate that dispersion of marine forms into brackish

as Tokyo Peil (T. P.) in Japan], the halocline depth

regions is effective when there is a marked increase18

High tide dispersion of marine benthic foraminifera into brackish waters:
implications for dispersion processes during sea-level risein sea level even though the tidal effects are small.

This makes sense because there is a strong counterflow of marine water carrying significant quantities ofsuspended matter. In addition we have noted that all the
miliolid individuals in our traps were small in size andlive (stained in rose bengal). Nomura and Seto (2004)
reported that suspended particles in Lake Nakaumi

contain numerous live foraminifera of the major taxa in

Lake Nakaumi, A.“beccarii” and Trochammina hadai.
Suspended particles are primarily composed of thedinoflagellate Procentrum minimum, both live and dead,and contain high amounts of organic matter. AlthoughFig. 4 Underwater photograph showing suspended

tubilocula actually attached to the suspended particles

bar = 7 cm.

we did not confirm the occurrence of Quinqueloculina

particles (marine snow) and a sediment trap bottle. Scalein situ in either that report or this study, sediments in therespective bottles are clearly derived from suspended
particles (Fig. 4). Underwater photographs in Lake

Nakaumi show numerous suspended particles, similar tomarine snow, and they are mostly composed of organic-rich phytodetritus. Foraminifera are able to utilize
these particles for food resources during the time when

they are being transported on the particles.The trapped

sedimentary organic carbon content in our sampler
bottles varies with season and depth, but a high rate of
sediment deposition is observed in summer and autumn,
when the average flux was 0.2~0.35 mgC/cm2/day (Fig.
5). In the deep-sea, benthic foraminifera are able toutilize seasonally variable inputs of organic matter, as afood resource (Gooday, 1988; Gooday and Turley, 1990),

and similarly coastal foraminifera show a strong responseto the input of large amounts of organic matter (Schönfeld

and Numberger, 2007). The flux of sedimentary organic

matter trapped in the bottles seems to be sufficient to

Fig. 5 Annual change and depth difference of the organic

foraminifera have different feeding strategies. Someaverage of 1-3 m and 4-6 m depths, respectively.

maintain live foraminifera for some time. Deep-sea

carbon flux. Fluxes in upper and lower water are theforms are able to ingest 8.8 mgC/m2/day of sedimentaryorganic matter. Phytophagous taxa ingest 2.9 ± 2.4 mg/

during the 1940s and 1950s (Nomura, 2003). Sea-level

deep-sea benthic foraminifera ingestion potentials, themeasured at various locations around the island of

m /day (Nomaki et al., 2006). Compared with theseduring this period was characterized by a higher position2

suspended particles in Lake Nakaumi contain much more

Honshu (Senjyu et al., 1999). In these periods, suspended

than sufficient organic carbon.

particles with live miliolids may have been transported

The occurrence of this marine form as a result of theinto Lake Nakaumi by counter-flow and particles settled

unusually high tide event suggests that future increases

to deposit foraminiferal tests on the lake floor. High tideof sea-level could affect foraminiferal dispersal. In coreduring a period of sea-level rise makes it easy to set up

sediments from the central part of Lake Nakaumi, thea strong counter-flow current and consequently transport

same form of miliolid foraminifera frequently occurredmarine suspended particles into estuarine lakes. Our
19

Ritsuo Nomura・Koji Seto・Akira Tsujimoto

long-term monitoring underwater camera has shown

Observatory.

that the soft bottom sediments are easily re-suspended
as particles by wind-induced bottom currents. In thisReferencescase the wind speed was greater than 10 m/s. Suspended
foraminiferal tests or sediment particles with included

Alve, E. (1999) Colonization of new habitats by benthic

foraminifera are able to combine with other suspended

foraminifera: a review. Earth-Science Reviews, 46:organic particles and be transported upstream into the167-185.

brackish lake system.

Alve, E. and Goldstein, S. T. (2002) Resting stage in

We are therefore able to use these occurrences of marine

benthic foraminiferal propagules: A key feature forexotic foraminifera in the sediments of oligohaline todispersal? Evidence from two shallow-water species.

mesohaline water bodies as an indicator of marine water

Journal of Micropalaeontology, 21: 95-96.

intrusion. This could be very useful in the study of recent

Alve, E. and Goldstein, S. T. (2003) Propagule transportsea-level change; exotic forms are a good indicator ofas key method of dispersal in benthic foraminifera

marine water movement.

(Protista). Limnology and Oceanography, 48: 21632170.

Gooday, A. J. (1988) A response by benthic foraminifera

Conclusions

to the deposition of phytodetritus in the deep sea.

Marine Quinqueloculina tubilocula was found in small

Nature, 332: 70-73.

sediment traps (7.3 cm diameter; 15.5 cm height) placed

Gooday, A. J. and Turley, C. M. (1990) Response by

Ammonia “beccarii” and Trochammina hadai make up

ocean floor: a review. Philosophical Transactions of thein central Lake Nakaumi, where the two native forms

benthic organisms to inputs of organic material to thethe entire foraminiferal assemblage. The occurrence

Royal Society London, Series A, 331: 119-138.

of this form coincided with an unusually high tide on

Hueni, C. M., Anepohl, J., Gevirtz, J. and Casey, R.

and Seto, 2004) that benthic foraminifera live on or inof oceanographic processes of the South Texas outer

September 1st, 2002. Based on our observation (Nomura(1978) Distribution of living fortaminifera as indicators

suspended organic particles, we conclude that this marine

continental shelf. Transaction of the Gulf Coast

form was transported along with suspended particles

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brackish water sediments are a good indicator of theLidz, L. (1966) Planktonic foraminifera in the waterof marine exotics in brackish lagoonal lake sediments

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