The influence of changes in the degree and frequency of disturbance on the annual salt marsh plant (Suaeda maritima, Artemisia fukudo) communities in estuarine tidal flats: A case study of the Kushida River in Mie Prefecture, Japan

In this study, we examined the influence of changes in the degree and frequency of disturbance in estuarine tidal flats on the annual salt marsh plant communities (Suaeda maritima, Artemisia fukudo) in Mie Prefecture, Japan. Suaeda maritima and Artemisia fukudo communities occur in the branch river of the Kushida River. Although the areas occupied by these communities were very small in 2006, the Suaeda maritima community expanded significantly to 3609 m in 2008, and the Artemisia fukudo community expanded significantly to 2726 m in 2008 and 10,396 m in 2010. Before the onset of the investigation period in 2006, the overflow warning water level (3.5 m) and the flood fighting corps standby water level (3.0 m) each occurred on one day in August 2004 and October 2004, respectively; at those times, the water volume exceeded 1000 m∙s and 1500 m∙s, respectively. We suggest that because much of the estuarine tidal flat erodes when the water volume exceeds 1000 m∙s, the establishment of the Suaeda maritima and Artemisia fukudo communities is delayed until sufficient substrate is formed by the deposition of new sediment. In contrast, a water level of 2 3 m was observed on one day each in 2005, 2007 and 2009, with average water volumes of 488.5, 566.4 and 690.1 m∙s, respectively. We suggest that following the repeated disturbances caused by water levels of 1 3 m and flow volumes of 500 700 m∙s over the bare ground exposed after flooding and erosion, Suaeda maritima is a pioneer species that colonizes on bare ground deposited by sediment transported from upstream and the sea during high tides, and following the same level of disturbance, Artemisia fukudo is secondary colonizer that has germinated and grown on the sediment deposited on the Suaeda maritima community.


INTRODUCTION
Many salt marsh plants are found in the estuarine tidal flat of the Kushida River, including the annual plants Suaeda maritima and Artemisia fukudo.These species are listed as Red Data Book species by [1,2].In recent years, these species have undergone declines due to coastal development, bank protection and other factors.Several environmental factors influence the habitat preferences of plants in estuarine tidal flats, including elevation and flood frequency [3], soil environment (salinity, humidity, particle size distribution, depth, oxidation-reduction potential), disturbance by floods, competition with other plants and other factors [4,5].The composition of the salt marsh plant community is influenced by sediment dynamics and the physical environment [6,9].In particular, the distributions of Suaeda maritima and Artemisia fukudo communities in Kushida River varied greatly among the study years of 2006, 2008 and 2010.These species broadly distributed in estuarine tidal flats with high flow volumes and water levels [10].Consequently, we hypothesized that changes in the degree and frequency of disturbances through changes in water volume and water level extremes influence the distributions of Suaeda maritima and Artemisia fukudo; however, few detailed studies have been conducted on this process.
In this study, we examined the influence of changes in the degree and frequency of disturbance in estuarine tidal flats on the distribution of annual salt marsh plants (Suaeda maritima, Artemisia fukudo).In particular, we investigated the effects of water volume and water level, which are considered the main environmental influences on distribution in these communities, and assessed the effects of disturbance on distribution change in the estuarine tidal flats of the Kushida River.

Study Site
The Kushida River is a first-class river that is 85 km long, with a basin area of 461 km 2 .The river flows through Mathuzaka City in Mie Prefecture.The headwaters are on Takami Mountain (altitude 1249 m), located on the border of Higashiyoshino, Yoshino District, Nara Prefecture and Mathuzaka City in Mie Prefecture, and the river empties into Ise Bay.
The study site was chosen because it is readily disturbed by river flooding in the estuarine tidal flat of the Kushida River (Figure 1).

Vegetation Sampling Methods
The vegetation survey was conducted during July of 2006, 2008 and 2010.The vegetation map was created based on the plant communities observed in aerial photographs; local confirmation of the plant community was conducted in cases where discrimination based on aerial photographs was difficult.We surveyed the study site to map the distribution of plant communities (1:2500).Vegetation data were used to develop a physiognomic vegetation map using GIS (Arc-View 3.1).
Data on water volume and water level were obtained from the observation station near the estuarine tidal flats.For the period of observation under analysis, we assumed that changes to the river environment preceding the survey had a large influence on the delta.Therefore, we used the data spanning the period from July 2004 to July 2010.

Classification of Vegetation Types
The vegetation types were classified as either 1) salt marsh plants or 2) exotic and upland plants (herbs).Salt marsh plants were defined as plants growing in the areas surrounding marshes and bogs near the mouth of the lagoon and river in the coastal zone, and upland plants were classified as plants growing in areas of strong anthropogenic influence, such as reclaimed areas [12] and environments with low soil moisture [13].Exotic plants were defined as plants brought in from foreign countries, and it is generally assumed that these plants were introduced after the Edo period in Japan [14].In addition, we classified the vegetative areas as either soil sedimentation disturbance areas (areas that transitioned from salt marsh plants to terrestrial vegetation or from bare ground to salt marsh vegetation), soil erosion disturbance areas (areas that transitioned from terrestrial vegetation to salt marsh vegetation or from salt marsh vegetation to bare ground) or no vegetation areas (bare ground) to evaluate evidence of disturbance in the vegetation changes of the salt marsh plant -land plant community based on the vegetation division maps of 2006, 2008 and 2010.

Area of the Plant Communities in the Study Site
The area occupied by the plant communities over the entire study site increased in 2008 to 2010 and in 2006 to 2008; in particular, the areas of the annual salt marsh plant communities of Suaeda maritima and Artemisia fukudo expanded substantially in the branch river.The majority areas of the branch river were occupied by bare land in 2006; in 2008, the Suaeda maritima community expanded; and in 2010, the Artemisia fukudo community expanded (Figures 2 and 3).Relative to the other vegetation types, the area of the annual salt marsh plant   1, Figure 5).

Changes in the Vegetation of the Annual Salt Marsh Plant Community
Our investigation of the change in the vegetation of the annual salt marsh plant communities (Suaeda maritima and Artemisia fukudo) indicated that the change in area from bare ground to the Suaeda maritima community was highest between 2006 and 2008 and that the change in area from bare ground to the Artemisia fukudo community was highest between 2008 and 2010.In addition, the area of change from bare ground to the Suaeda maritima community and from the Suaeda maritima community to the Artemisia fukudo community both ex-ceeded 2000 m 2 (Table 2) Our investigation of the disturbance status of the entire study area based on vegetation changes indicated that the area of soil sedimentation disturbance was approximately 20% between 2006 and 2008; however, this area expanded to approximately 45% between 2008 and 2010.The area of soil erosion disturbance was 4.8% between 2006 and 2008 and expanded to 19.3% between 2008 and 2010.In contrast, the area of no vegetation was in excess of 70% between 2006 and 2008 and reduced to half that amount between 2008 and 2010 (Figure 6).

Changes in Flow Volume and Water
Level before and after the Investigation Period Water levels exceeded 2 -3 m primarily in August-October 2004 and exceeded 1.0 m in September 2005, July 2007 and August and October 2009.During the remaining periods, water levels were below 0.5 m (Figure 7).Flow volume was 500 -1500 m 3 •s −1 in August-October     3).

Changes in the Degree and Frequency of Disturbance on Suaeda maritima, Artemisia fukudo Communities
The areas of the annual salt marsh plant communities of Suaeda maritima and Artemisia fukudo in the branch river of the Kushida River were very small in 2006 (Table 1, Figure 5).In 2006, before the investigation period,    3).Disturbances of this scale were not observed during the investigation period.With respect to the growth environment of these species, Suaeda maritima disseminates its seed via the tide [15] and may form soil seed bank [16].The Suaeda maritima community occurs at low elevations that are disturbed by flooding at high tide [3].In addition, the Suaeda maritima community prefers the fine gravel and pebble gravel substrate that occurs below the spring high tide level [17].In contrast, Artemisia fukudo grows in the mud substrate that is flooded by seawater during the high tide in the river tidal area, and it is a winter annual plant that flowers during the autumn [18][19][20].
As the annual salt marsh plant communities of Suaeda maritima and Artemisia fukudo grow in low areas disturbed by flooding, erosion of the estuarine tidal flat can readily occur when the water level reaches either the overflow warning water level (3.5 m) or the flood fighting corps standby water level (3.0 m) and when the water volume exceeds 1000 m 3 •s −1 .Therefore, it seems likely that the re-establishment of the plant community and the growth of these species are delayed until new substrate is formed by sedimentation.Following a major flooding disturbance, the Suaeda maritima community expanded substantially to 3609 m 2 in 2008, and the Artemisia fukudo community expanded significantly to 2726 m 2 in 2008 and to 10,396 m 2 in 2010 (Table 1, Figure 5).A water level of 2 -3 m occurred between July and October on one day each in 2005, 2007 and 2009, when the average water volume was 488.5, 566.4 and 690.1 m 3 •s −1 , respectively (Table 3).With respect to the amount of change in vegetation in the annual salt marsh plant community, the greatest change in area from bare ground to the Suaeda maritima community occurred between 2006 and 2008, and the changes in area from bare ground to the Artemisia fukudo community and from the Suaeda maritima community to Artemisia fukudo community were highest between 2008 and 2010 (Table 2).With respect to the elevations of the Suaeda maritima and Artemisia fukudo communities, dense growth of the Suaeda maritima community occurred at an elevation (T.P.:Tokyo Peil) between 0.785 and 1.063 m [17].Dense growth of the Artemisia fukudo community occurred at a T.P of approximately 1.1 m [21].The fructification rate of Artemisia fukudo was higher at a T.P of 1.3 -1.5 m than at 1.0 m or less.This result may reflect the short period of pollination and the overabundance of pollen at lower elevations, where the inundation period is extensive [22].We suggest that, although we found on the ground that Artemisia fukudo and Suaeda maritima were co-occured, Artemisia fukudo grows more readily than Suaeda maritima at higher elevations.Consequently, it seems likely that, following the repeated disturbances of water levels of 1 -3 m and flow volumes of 480 -700 m 3 •s −1 over the bare ground eroded by massive flooding in 2004, the Suaeda maritima community was established on the higher ground formed by the sediment transported from upstream and the sea during high tides and subsequently deposited.In addition, when this same level of disturbance occurred, Artemisia fukudo germinated and grew on the ground that was made higher by the sediment deposited on the Suaeda maritima community.
Based on the extent of vegetation change due to disturbance that occurred over the entire study site, the area of soil sedimentation disturbance was approximately 20% between 2006 and 2008 and expanded to approximately 45% between 2008 and 2010.The area of soil erosion disturbance was 4.8% between 2006 and 2008 and expanded to approximately 19.3% from 2008 to 2010 (Figure 6).The study site was strongly influenced by the disturbance activities of sedimentation and erosion between 2008 and 2010 relative to the period between 2006 and 2008.Because the area was strongly influenced by sedimentation, we postulate that the area of the Artemisia fukudo community expanded to a greater extent than the Suaeda maritima community.

Figure 2 .
Figure 2. Temporal changes in the vegetation of the Kushida River delta.

Figure 3 .
Figure 3. Temporal changes in vegetation type in the Kushida River delta.

Figure 4 .
Figure 4. Changes in the component ratio of each vegetation type in the Kushida River delta.

Figure 5 .Figure 6 .
Figure 5. Change in area of the annual salt marsh plant communities in the Kushida River delta.
2004 and was generally lower, at 200 -600 m 3 •s −1 , in September 2005, July 2007, September 2008 and August and October 2009 (Figure 8).Regarding the number of days per normal water level category, including before and after the investigation period (July 2004-July 2010), the overflow warning water level (3.5 m) and flood fighting corps standby water level (3.0 m) each occurred on one day in 2004, with the water volume exceeding 1000 m 3 •s −1 and 1500 m 3 •s −1 , respectively.A water level of 2-3 m occurred on one day each in 2004, 2005, 2007 and 2009, with a water volume of approximately 480 -690 m 3 •s −1 .A water level of 1 -2 m was observed during eight days in 2004 and one day each in 2005 and 2009, with an average flow volume of 230 -280 m 3 •s −1 .Water levels of 0 -1 m occurred in all years (Table

Table 1 .
Areas of the plant communities in the tidal flats of the Kushida River estuary.

Table 2 .
Changes in the area of the annual salt marsh plant communities (Suaeda maritima, Artemisia fukudo).

Table 3 .
Number of days and average water volumes of each normal water level category, including before and after the investigation period (July 2004-July 2010).