Role of geoenvironmental dynamics in the biodiversity of sandy beaches and sandflats: The ecohabitat chart and its ecological implications

Estuarine, Coastal and Shelf Science 219 (2019) 278–290

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Role of geoenvironmental dynamics in the biodiversity of sandy beaches and sandflats: The ecohabitat chart and its ecological implications

T

Shinji Sassa∗, Soonbo Yang Port and Airport Research Institute, National Institute of Maritime, Port and Aviation Technology, 3-1-1 Nagase, Yokosuka, 239-0826, Japan

A R T I C LE I N FO

A B S T R A C T

Keywords: Macroinfauna Sandy beach Sandflats Geoenvironmental dynamics Biodiversity Restored habitat

Geoenvironmental dynamics of habitats for a number of species and their linkage with biological activity and species diversity remain poorly understood. This study presents an ecohabitat chart showing the relationships between the habitat geophysical environmental conditions and diverse biological activities of species that belong to Arthropoda, Mollusca, and Annelida, from juvenile to adults, on sandy beaches and sandflats. The in situ sediment hardnesses of fifteen sandy beaches and sandflats varied considerably due to suction development and suction-dynamics-induced sediment compaction. The diversity of macroinfauna exhibited distinct changes in their responses to variations of such geophysical environments. Under critical conditions, biological activities, including burrowing, burrow development, and physiological activity, were hindered or prevented from taking place. The developed ecohabitat chart represents a complex interrelationship of the critical geophysical environment among species and revealed a species diversity–geoenvironmental dynamics relationship that was found to be consistent with field evidence. These results demonstrated the important role of the geoenvironmental dynamics in the distributions of species, accounting for the cause and effects involved. The present study may effectively contribute to novel habitat design, assessment and management for the conservation and restoration of sandy beaches and sandflats.

1. Introduction Sandy beaches and sandflats are vital elements in the sustainability of coastal environments since they foster rich natural ecosystems. They also serve for disaster prevention and mitigation as buffer areas in a changing global environment. The conservation and restoration of these habitats are therefore essential for preserving biodiversity, as well as for human society. A rational, physically based management strategy or framework is necessary for obtaining sustainable ecosystem functions and services (Weinstein et al., 2014; Boerema and Meire, 2017). Indeed, species richness and abundance have been considered to be mainly regulated by the physical processes of fluids above the sediments and the associated morphodynamics (McLachlan, 1990; Jaramillo et al., 1993, 1995; Defeo et al., 2001; Brazeiro, 2005; McLachlan and Dorvlo, 2005; Defeo and McLachlan, 2005, 2011; Lastra et al., 2006; Schlacher and Thompson, 2013). However, the role of geoenvironmental dynamics as a manifestation of the geophysical processes in the sediments, which represent habitats themselves, and their linkage with diverse biological activity and species diversity remain poorly understood, although their complete understanding is crucial to the conservation and restoration of habitats.

∗

Recently, Sassa and Watabe (2007) and Sassa et al. (2011) demonstrated that the dynamics of suction, that is, negative pore water pressure relative to atmospheric air pressure, in association with tideand swash-induced fluctuations in groundwater level, bring about significant temporal and spatial evolutions of voids, stiffness and surface shear strengths of intertidal sediments, the magnitudes of which depend strongly on the intensity of the suction dynamics ensuing there. Conceptual models to account for the variations of such a geophysical environment in sandy beaches and sandflats are shown in Fig. 1. The degree of saturation, density and hardness of the intertidal and supratidal sediments depend on the magnitude of suction, owing to the suction-dynamics-induced sediment compaction around air-entry suction saev(Sassa et al., 2014). Indeed, the hardness of surficial intertidal sediments varies by a factor of 20–50 due to suction development and suction-induced void state changes in the essentially saturated states of sandy beaches and sandflats (Sassa and Watabe, 2007; Sassa et al., 2011, 2014). As a consequence of these geoenvironmental dynamics, suction governs various geophysical states of sandy beach and sandflat sediments. The suction-dynamics-induced compaction and associated variations in shear strength of the sediments have also been shown to play a crucial role in intertidal sandbar morphodynamics (Sassa and

Corresponding author. E-mail address: [email protected] (S. Sassa).

https://doi.org/10.1016/j.ecss.2019.02.002 Received 27 August 2018; Received in revised form 29 December 2018; Accepted 3 February 2019 Available online 08 February 2019 0272-7714/ © 2019 The Authors. Published by Elsevier Ltd. This is an open access article under the CC BY license (http://creativecommons.org/licenses/BY/4.0/).

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that affect other fundamental activities such as foraging and breeding (e.g. Gray and Elliott, 2009), the response of the macroinfauna to their abiotic environment has been extensively investigated in relation to the variations in their hydroenvironment, such as tides, waves and currents (Beukema and Vlas, 1989; McLachlan et al., 1993, 1995; Young et al., 1996; Dugan et al., 2000; Norkko et al., 2001: Yannicelli et al., 2002; Hunt, 2005; Nambu et al., 2012). Sediment types and sediment grain sizes have also been associated with their responses (Alexander et al., 1993; Botto and Iribarne, 2000; Nel et al., 2001; Huz et al., 2002; Gibson et al., 2006; Compton et al., 2009, 2013; Fanini et al., 2017). However, the response of macroinfauna to variations in their geophysical environment remains much less understood, in contrast to their response to variations in their hydroenvironment with given sediments. Recent understanding of the salient geophysics involved in intertidal sediments has facilitated close investigation of the linkage between the geophysical environment and diverse biological activities, revealing a range of suitable and critical geophysical environments for the burrowing activities of the sand bubbler crab Scopimera globosa (Sassa and Watabe, 2008), the bivalves Ruditapes philippinarum and Donax semigranosus (Sassa et al., 2011), and the amphipods Haustorioides japonicus and Trinorchestia trinitatis (as Talorchestia brito) (Sassa et al., 2014), and for the physiological activity of the isopod Excirolana chiltoni (Sassa et al., 2014), as well as the foraging activity of the shorebird Calidris alpina (Kuwae et al., 2010). With the above-mentioned background, the hypotheses clarified in this study are fivefold: a) suction dynamics-induced geophysical environments are common throughout various sandy beaches, sandflats and artificially restored habitats with different sediment grain sizes, sorting coefficients, slopes, and fines (silt and clay) contents; b) the diversity of macrofauna respond distinctly to the variations in geophysical environment as manifested in the field; c) there exist critical geophysical environments among species and growth stages; d) such knowledge can be used to develop an ecohabitat chart, which allows us to understand the biodiversity-geoenvironmental dynamics relationship; and e) the chart can be used for novel habitat design, assessment/ monitoring and management. For these purposes, in the present study, an ecohabitat chart was developed by integrating our recent research mentioned above, and by adding new field data and newly examining and clarifying the burrowing responses of diverse invertebrates to a changing geoenvironment, from juveniles to adults that belong to Anthropoda, Mollusca and Annelida, on a unified basis. The ecohabitat chart covers the whole range of variations in the geophysical environment that manifest in sandy beaches and sandflats. Discussions are made on the role of such geoenvironmental dynamics and its ecological implications in sandy beaches and sandflats. The diversity of speciesgeoenvironmental dynamics relationships were substantiated based on the developed chart and in light of the field evidence from two habitat restoration projects. Fig. 1. Conceptual models to account for the variations of (a) degree of saturation Sr, (b). relative density Dr, and (c) vane shear strength τ∗ with suction s in exposed sandy beaches and sandflats. Here, saev denotes the air-entry suction of the sediments above which the sediments become unsaturated.

2. Materials and methods 2.1. Sites Our study sites included fifteen sandy beaches, sandflats and artificial sandflats, as shown in Fig. 2 and Table 1. These habitats are Kujukuri beach (May 2009), Yuigahama beach (Sep. 2010), Yotsugoya beach (Oct. 2009), Tarodai beach (Oct. 2009), Tayuhama beach (Oct. 2009), Sawane beach (Aug. 2010), Shinmachi beach (Aug. 2010), Okoshiki beach (Jun. 2010), Nojima sandflat (Mar. 2009, Sep. 2010), Shirakawa sandflat (Sep. 2009), Isumigawa sandflat (Aug. 2009), Naha sandflats (Jun. 2009, Dec. 2009, Feb. 2011, Sep. 2011, Apr. 2016), Tomioka sandflat (Aug. 2015, Aug. 2016), the Tokuyama artificial sandflat (Sep. 2010, Jun. 2011, Jul. 2016) and the Onomichi artificial sandflat (MLIT, 2006). The intertidal sediments at all these sites were essentially composed of fine-to coarse-grained sands with median grain diameters in the range D50 = 0.11–0.8 mm, where the silt and clay

Watabe, 2009a) and in forming the intertidal flat stratigraphy of sandy, muddy, and sand–mud layered sediments (Watabe and Sassa, 2008). For the diversity of macroinfauna living in sandy beaches and sandflats, burrowing is indispensable for inhabiting sediments. Burrowing performance is thus an important factor in determining the distribution of species (Icely and Jones, 1978; McLachlan, 1990; McLachlan et al., 1993; Thrush et al., 1996; Wada, 2002; Compton et al., 2009) and in forming the macroinfaunal community of intertidal zones (Dugan et al., 2004). The burrowing performance of individual species can also vary depending on their morphology and stages of growth from juvenile to adult (Thrush et al., 1996; Dugan et al., 2000; Dorgan, 2015). Although burrowing is a physical action in sediments 279

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Fig. 2. Locations of study sites involving fifteen sandy beaches, sandflats and artificially restored habitats in Japan. Square, circle, and triangle represent sandy beach, sandflat, and artificial sandflat, respectively.

summarized in Table B1. In essence, these species were selected as representing typical species that belong to Arthropoda, Mollusca, and Annelida on sandy beaches and sandflats and that are commonly seen in Japan.

contents varied widely, as shown in Table 1. Accordingly, these study sites were selected as representing various sandy beaches and sandflats with different sediment grain sizes, sorting coefficients, slopes, and fines contents (Table 1).

2.3. Geophysical measurements

2.2. Species

Relevant physical quantities that represent the geophysical states of sandy beach and sandflat sediments can be described as follows. Suction, s, means the tension of moisture in the sediment (Bear, 1979) and is defined by

The present study targeted diverse species belonging to Arthropoda, Mollusca, and Annelida on sandy beaches and sandflats, including bivalves (Ruditapes philippinarum, Donax semigranosus and Mactra veneriformis), polychaete worms (Ceratonereis erythraeensis and Glycera nicobarica), crabs (Scopimera globosa), shrimps (Alpheus brevicristatus), decapod crustaceans (Nihonotrypaea japonica), amphipods (Haustorioides japonicus and Trinorchestia trinitatis) and isopods (Excirolana chiltoni). The individual species, R. philippinarum, M. veneriformis, C. erythraeensis, G. nicobarica, S. globosa, A. brevicristatus, and N. japonica were collected from four fields, namely, Nojima, Banzu (N35° 24′, E139° 54′), Ena (N35° 8′, E139° 39′) and Furenko (N43° 17′, E145° 22′), H. japonicus, T. trinitatis, and E. chiltoni from Yotsugoya, and D. semigranosus from Yuigahama. The details of these species are

s = ua－uw,

(1)

where ua is the atmospheric air pressure, and uw is the pore water pressure in the sediment. By definition, suction is equal to zero at the groundwater level. The void state of the sediment is represented by void ratio e, which is related to the sediment porosity n:

e= 280

n 1−n

(2)

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2008), the burrowing criteria and burrowing mode adjustment in bivalves at sandy beaches and sandflats (Sassa et al., 2011), and the distribution limits of amphipods (Sassa et al., 2014), and to be closely linked with the foraging mode shift exhibited by shorebirds (Kuwae et al., 2010).

Table 1 Sediment properties of study sites. All the sites are shown in Fig. 2. Sandy beach Study sites

D50a (mm)

Sorting coefficientb

Kujukuri

0.174 1.24–1.25 −0.179 Okoshiki 0.140 1.249–2.094 −0.293 Sawane 0.171 1.256–1.597 −0.207 Shinmachi 0.191 1.253–1.732 −0.389 Tarodai 0.228 1.300–1.391 −0.300 Tayuhama 0.325 1.192–1.300 −0.368 Yotsugoya 0.176 1.253–1.338 −0.209 Yuigahama 0.170 1.280–1.316 −0.174 1) Upper beach face slope,2)Low-tide terrace

Beach face slope

Fcc (%)

Coordinates

1/34

0.08 −0.36 0.55 −21.98 0 −0.17 0.02 −0.06 0 −0.08 0 −0.03 0.01 −0.06 0.25 −0.48

N35° 31′ E140° 27′ N32° 39′ E130° 32′ N38° 0′ E138° 16′ N37° 57′ E138° 20′ N37° 58′ E139° 11′ N37° 58′ E139° 9′ N37° 50′ E138° 52′ N35° 18′ E139° 32′

1/81), 1/ 3232) 1/6 1/6 1/11 1/6 1/13 1/32

2.4. Field surveys The distributions of suction and hardness of the surficial sediments were measured in fifteen sandy beaches and sandflats shown in Fig. 2 and Table 1, during spring low tides from 2009 to 2016. Here, suctions were measured using tensiometers (HG-2100AEL, mol Inc., Japan, Sassa and Watabe, 2007, 2008; Sassa et al., 2011), and vane shear strengths were measured using a compact vane shear testing apparatus (FTD2CN-S, Seiken Inc., Japan) with intersecting vane blades of 40 mm width, 10 mm depth, and 0.5 mm thickness (Fig. 1 of Sassa et al., 2011), by keeping the rotation speed of the vanes less than 60° min−1. These measurements were conducted along the cross-shore transects at 1–5 m intervals in sandy beaches and at 10–25 m intervals in sandflats, depending on the morphology of the sandy beaches and sandflats (Table 1).

slope

Sandflat

2.5. Laboratory burrowing experiments

Study sites

D50a (mm)

Sorting coefficientb

Sandflat slope

Fcc (%)

Coordinates

Isumigawa

0.347 −0.355 0.202 −0.783 0.170 −0.210 0.138 −0.274 0.190 −0.311

1.385–1.422

1/35

1.299–1.799

1/188

1.268–1.539

1/93

1.378–1.836

1/150

1.166–2.864

1/240

0.23 −6.38 0 −1.01 0.43 −2.58 0.48 −26.03 0.01 −2.0

N35° 17′ E140° 24′ N26° 10′ E127° 38′ N35° 19′ E139° 38′ N32° 47′ E130° 35′ N32° 31′ E130° 2′

Naha Nojima Shirakawa Tomioka

For the burrowing experiments in the laboratory, sediment deposits with three different states of packing at Dr = 40%, 60%, and 80% were formed in a transparent cylindrical chamber with 100 mm diameter and 200 mm depth by using the intertidal sediments taken from the Nojima sandflat. Suctions s at the level of the sediment surfaces were varied by changing the water level above and the groundwater level in the sediments. Fig. A1a shows that the vane shear strength τ* increased with increasing suction s and sediment relative density Dr, and depended only on sediment relative density Dr under negative suctions (submerged condition). For accurate and unified control in the laboratory of the vane shear strengths as manifested in the field, in the present study, agar (Sassa and Watabe, 2009b) was used as artificial sediments. The formation of homogeneous artificial sediments proved important, and the corresponding procedures are described as follows. Boiled sea water with an adjusted salinity of 27 was mixed with a powder of agar under a prescribed concentration for 3 h, and the mixture was then refrigerated for 12 h. After bringing it back to normal temperature (20 °C), the uppermost 1 mm-thick surface film was peeled off. The agar sediments were repeatedly formed in this manner, achieving precise control of a wide range of vane shear strengths as manifested in the field, as shown in Fig. A1b. The burrowing responses of juvenile to adult R. philippinarum at eleven size classes (L = 2–4 mm, 4–6 mm, 6–8 mm, 10–12 mm, 14–16 mm, 19–21 mm, 24–26 mm, 29–31 mm, 34–36 mm, 44–46 mm and 49–51 mm; Table A1) were examined, and the results were compared with those on sediments taken from the field, as reported in Sassa et al. (2011). Based on this in-depth clarification and verification, the burrowing responses of five different species, namely, C. erythraeensis, G. nicobarica, N. japonica and A. brevicristatus on the artificial sediments and M. veneriformis on the sediments taken from the field, to varying sediment hardnesses were also examined. Experiments were performed for a 1 h period. Here, for most species, the 1-h period was sufficient to confirm whether or not the burrowing was physically possible. Prior to the experiments, all species were maintained in the laboratory under aerated fresh seawater in the intertidal sediments for over one month to ensure that any endogenous physiological rhythms were abolished (Mcgaw, 2005). In cases where burrowing was possible, an individual burrowed under the sediment surface. In contrast, the whole body remained on the sediment surface when the burrowing was impossible. For the bivalves and shrimp, however, partial burrowing manifested, and thus in order to elucidate their burrowing capabilities, their responses were examined for 6 h. In the bivalves, the starting condition in

Artificial sandflat Study sites

D50a (mm)

Sorting coefficientb

Sandflat slope

Fcc (%)

Coordinates

Onomichi

Max. 0.8 0.111 −0.391

–

1/50

1.340–1.700

1/64

1.07 −89.13 0.06 −39.63

N34° 23′ E133° 16′ N33° 58′ E131° 47′

Tokuyama

a b c

Median grain size. Trask's sorting coefficient. Silt and clay content.

The state of sediment packing, such as dense or loose, can be denoted by the sediment relative density Dr:

Dr =

emax − e emax − emin

(3)

For a given sediment, the maximum void ratio emax represents the loosest possible packing, and the minimum void ratio emin represents the densest possible packing (Lambe and Whitman, 1979). Thus, the Dr value is a normalized index by which to assess the packing states of sandy sediments. The hardness of surficial intertidal sediments can be assessed by the vane shear strength (Amos et al., 1988; Sassa and Watabe, 2007, 2008; Kuwae et al., 2010; Sassa et al., 2011). This method can evaluate the sediment hardness in an in situ undisturbed state by inserting a very thin vane blade into the surficial sediment and measuring the maximum resistance τ* of the sediment to horizontal shearing due to rotation of the vane blade (Fig. 1 of Sassa et al., 2011). Sediment hardness, as assessed by the vane shear strength τ*, has been shown to govern the development of burrows of sand bubbler crabs (Sassa and Watabe, 281

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which the individual touched the sediment surface with its foot (Sassa et al., 2011) was adopted in order to obtain consistent results, after the bivalves showed their “intention” to burrow in the sediments. A total of 1031 individuals whose body sizes ranged from 2 mm to 88 mm and whose body weights ranged from 0.004 g to 31.6 g were used and examined for their responses in the laboratory experiments. In all experiments, the air temperature, the water temperature, and the salinity of the water and pore water were kept essentially constant at 20–21 °C, 19–20 °C, and 27, respectively. 2.6. Superposition and analysis The field and laboratory test results obtained in the present study were combined and superimposed with those of S. globosa (Sassa and Watabe, 2008), D. semigranosus (Sassa et al., 2011), and H. japonicus, T. trinitatis (as T. brito) and E. chiltoni (Sassa et al., 2014), to construct an ecohabitat chart, in light of the results of analysis of the geophysical environmental characteristics of the sandy beaches and sandflats. Specifically, the critical conditions for all species and growth stages were plotted in a space that represents an ecohabitat chart. Here, the linear relationship between suction s and the vane shear strength τ*, as manifested in the diverse fields of the sandy beaches, sandflats and artificially restored habitat was used to convert the vane shear strengths into suction. The biodiversity and geoenvironmental dynamics relationships were assessed by utilizing the developed ecohabitat chart. The related aspects will be described and discussed in detail later in this paper. The methods, results and discussion concerning artificially restored habitats are described in Appendix B of this paper. 3. Results 3.1. Sediment hardness in sandy beaches and sandflats The in situ sediment hardnesses of the sandy beaches and sandflats varied considerably, as shown in Fig. 3a. The hardness of the surficial intertidal sediments increased with increasing suction in the essentially saturated states, and the magnitudes of such variations in the sediment hardness were closely linked with the development of suction that manifested in the field. For instance, at Kujukuri beach, the vane shear strength, τ*, increased from 0.07 kPa at s = −0.2 kPa to 3.65 kPa at s = 2.95 kPa, representing a 52-fold increase in hardness. By contrast, at the Tomioka sandflat, the vane shear strength, τ*, increased from 0.03 kPa at s = −0.3 kPa to 0.12 kPa at s = 0.2 kPa, representing a 4fold increase in hardness. After reaching a peak, further increases in suction brought about declines in the sediment hardnesses. Here, the ranges of suction cover not only intertidal zones but also supratidal zones (s ≈ 10 kPa). In Fig. 3a, all the surficial sediment hardnesses of the sandy beaches and sandflats fell on a linear relationship between τ* and s at s < 2 kPa, as shown in Fig. 3b.

Fig. 3. Measured relationships between sediment hardness and suction at fourteen sandy beaches and sandflats. (a) Vane shear strength versus suction. (b) Vane shear strength versus suction at s < 2 kPa (n = 130, VSS = 0.222 + 0.888s, R2 = 0.811, p < 0.0001).

10–12 mm, 14–16 mm, 19–21 mm, 24–26 mm, 29–31 mm, 34–36 mm, 44–46 mm and 49–51 mm. Based on the shell length, L, versus wet weight, w, relationships shown in Fig. A2, all of these results are summarized in Fig. 4. Since the individuals’ weights varied by more than one-thousand fold, the wet weights are shown on a log scale. In this figure, the previous results of burrowing experiments for juvenile to adult R. philippinarum with L = 5 mm, 10 mm, 20 mm, 30 mm, and 50 mm on the sandflat sediments (Sassa et al., 2011) are also shown for the purpose of comparison. Both results showed three burrowing regimes consistently: complete vertical burrowing, burrowing mode shift, and burrowing failure where burrowing was impossible. The vane shear strengths of the two boundaries between these three regimes are termed critical (CR) and optimum (OP) conditions on the basis of the present results, and are indicated in red and blue lines, respectively, in Fig. 4. Both results showed a reasonable agreement in terms of the vane shear strengths, and a particular conformity on the critical conditions for all growth stages. The results of the burrowing experiments on the other five species, juvenile to adult C. erythraeensis, G. nicobarica, N. japonica, A. brevicristatus and M. veneriformis, are shown in Fig. 5. The critical and

3.2. Burrowing responses of diverse macrofauna The results of the burrowing experiments on the juvenile to adult R. philippinarum under the varying sediment hardnesses as manifested in the field are shown in Table A1. The burrowing responses changed distinctly, depending on the vane shear strengths, τ*. Namely, when τ* was low, all individuals completed vertical burrowing (symbol a). However, with increasing τ*, the bivalves started to shift their burrowing mode, exhibiting inclined/partial burrowing (symbol b) or burrowing failure (symbol c). With a further increase in τ*, all individuals could not burrow, representing the situation where burrowing was impossible. Such burrowing criteria below or above which the bivalves accomplished vertical burrowing or failed to burrow changed markedly with the size classes: L = 2–4 mm, 4–6 mm, 6–8 mm, 282

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formation and destabilized the burrows of T. trinitatis at s = 10 kPa. Hence, this ecohabitat chart represents the critical geophysical environments, not only for burrowing but also for physiological activity, that constitute the basic requirements for the survival of diverse species in Arthropoda, Mollusca and Annelida on sandy beaches and sandflats. The ecohabitat chart also has a two-stage structure, where the region with an abundance of species is enlarged for clarity. Here, the ranges of suction for a given state of sediment packing with Dr = 60% and 80% are shown for the purpose of reference, based on the s versus τ* relationships obtained in the laboratory (Fig. A1a). Overall, the developed ecohabitat chart represents a complex interrelationship of the critical geophysical environment among species. For the purpose of illustration, diverse forms of the observed burrowing activities and photographs of the representative species (see Graphical abstract) are shown in Fig. 6. The Mollusca species and some of the Anthropoda species burrow in sediments without forming burrows. The other Anthropoda species and the Annelida species burrow by forming a variety of burrows. These burrowing activities are supported by the ensuing geophysical environments that vary markedly in space and time, and from field to field. A species diversity–geoenvironmental dynamics relationship was assessed and analyzed by utilizing the ecohabitat chart, by counting the number of species whose critical geophysical environmental conditions, namely critical suctions s, exceeded given varying suctions. A graph of the number of species versus suction thus obtained is shown in Fig. 7. The results clearly indicate a decreasing number of species with increasing suction. The species–suction relationship is not linear. Indeed, the number of species declined rapidly with increasing suction and decreased gradually at even higher suctions.

Fig. 4. Three burrowing regimes of R. philippinarum as obtained from the laboratory burrowing experiments using sediments taken from the Nojima sandflat and agar. The data on the sediments are from Table 2 of Sassa et al. (2011). n = 3 to 9 for each data symbol. The optimum (OP) and critical (CR) conditions represent the vane shear strengths below and above which all individuals accomplished vertical burrowing and failed to burrow, respectively. Open circle indicates that all individuals completed vertical burrowing; open triangle indicates that some individuals exhibited inclined and/or partial burrowing; symbol X indicates that burrowing was impossible; closed circle represents sinking.

optimum conditions varied with species and growth stage. For instance, the optimum conditions for C. erythraeensis exhibited higher ranges than the other species in terms of τ*. The critical conditions of τ* increased toward juvenile stages for A. brevicristatus, whereas there was a peak for N. japonica as well as for R. philippinarum in Fig. 4. Some M. veneriformis individuals could not stand up in partially submerged and exposed conditions, irrespective of the sediment hardness. This means that buoyancy was necessary for the burrowing of this species. By contrast, under submerged conditions, M. veneriformis burrowed in harder sediments than R. philippinarum, by comparing Figs. 4 and 5. The burrowing responses of all species of C. erythraeensis, G. nicobarica, N. japonica, A. brevicristatus, R. philippinarum, M. veneriformis and D. semigranosus are summarized in Fig. A3. The results clearly indicate that there exist three burrowing regimes for all species: the region below OP where all individuals are able to burrow, the transitional region between OP and CR where selections of individuals manifest themselves, and the critical region above CR where burrowing is impossible. These burrowing regimes defined in terms of τ* differed markedly with phylum and species.

4. Discussion 4.1. Role of geophysical environmental dynamics in sandy beaches and sandflats The habitat geophysical environments of the sandy beaches and sandflats shown in Fig. 2 and Table 1 exhibited considerable variations in the sediment hardness (Fig. 3a). Overall, suction plays an important role in controlling the geophysical environment of given habitats from the intertidal to supratidal zones, whose habitat geophysical environmental characteristics are common to all of the sandy beaches, sandflats and artificially reclaimed sandflats, whereas the supratidal zone was typically found only on the exposed sandy beaches. Furthermore, the sandy beaches, sandflats and the artificial sandflat all shared essentially saturated states (Fig. 3b), which were important as habitats, and where diverse species responded distinctly to the varying geophysical environments. Consequently, the severity and gradients of such habitat geophysical environments can be represented by the suctions, as well as the vane shear strengths.

3.3. Ecohabitat chart with relation to biodiversity 4.2. Ecohabitat chart and its ecological implications in the estuarine and coastal ecosystems

The critical conditions for all species and growth stages are plotted in Fig. 6, which represents an ecohabitat chart. All of the critical conditions for the species shown in Figs. 4 and 5 corresponded to the essentially saturated states where a linear relationship holds true between s and τ* (Fig. 3b). For increasing suction, the distribution limits of three amphipods and isopod species with a range of individual weights (MOE, 1998) are plotted, where the cause and effects were confirmed from controlled laboratory experiments (Sassa et al., 2014). That is to say, these critical conditions manifested in such a way that the increased sediment hardness due to suction development and suction-dynamicsinduced compaction prevented burrowing of H. japonicus at s = 2 kPa and T. trinitatis at s = 3 kPa, and an increase in suction hindered uptake, i.e., the sucking of porewater in the sediments, leading to death of the water-breathing infauna E. chiltoni at s = 5 kPa, and the looseness and loss of effective cohesion with excessive suction prevented burrow

The ecohabitat chart developed in this study shows a complex interrelationship of the linkage between the habitat geophysical environments and diverse biological activities, including burrowing, burrow development, and physiological activity, of diverse macroinfauna inhabiting sandy beaches and sandflats. The knowledge obtained should be fundamental and crucial for habitat and ecosystem conservation and restoration. Namely, under conditions where burrowing fails, the macroinfauna cannot live in the sediments any more, exposing themselves to fatal risks from predators (Warner, 1977; Tallqvist, 2001), being washed away by waves and currents (Ratcliffe et al., 1981), and direct heat irradiation (Johnson, 1965) during low tides. Furthermore, burrows function as a base of various fundamental activities such as feeding and breeding (Altevogt, 1955; Christy, 1987), 283

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Fig. 5. Results from the laboratory burrowing experiments on C. erythraeensis, G. nicobarica, N. japonica and A. brevicristatus on the artificial agar sediments and M. veneriformis on the sediments taken from the Nojima sandflat. OP and CR denote the optimum and critical vane shear strengths below and above which all individuals were able to burrow and failed to burrow, respectively, irrespective of their wet weights. Circle, triangle, and symbol X represent burrowing possible, inclined and/or partial burrowing, and burrowing impossible, respectively.

Namely, the waterfront geophysical environments with lower suctions have greater numbers of species than those with higher suctions. Indeed, the two-stage structure of the chart clearly illustrates such characteristics. In light of the habitat geophysical environments, the burrowing capabilities of species that belong to the Arthropoda and Annelida are generally higher than those of the Mollusca species. Their implications in the spatial distributions of each species are described in Appendix B of this paper. While the ecohabitat chart directly targets a total of eleven species, they represent typical species in Arthropoda, Annelida and Mollusca, whose morphology and burrowing forms are notably different, as shown in Fig. 6. This means that the knowledge obtained with respect to the ecohabitat chart should be applicable to other similar species in each phylum of invertebrates, warranting wider application in the framework of ecological restoration (Weinstein et al., 2014). The diversity of species–geoenvironmental dynamics relationships

and hence, preventing the burrow development disables or makes these living activities difficult. Physiological activity such as respiration is essential for any water-breathing infauna in sediments (e.g. Bally, 1983), and thus, hindering the breathing process immediately leads to death. The critical geophysical environments that allow each of those biological activities to take place within such geophysical environments have been shown to vary substantially among species and change with their wet weights denoting the growth stages, as shown in Fig. 6. The habitat geophysical environments cover the whole range of geoenvironmental variations from the essentially saturated states of sandy beaches and sandflats to the supratidal zones of the exposed sandy beaches. The individual wet weights are depicted from 0.001 g to 100 g, which may correspond to the entire scale of the juvenile to adult macroinfauna living there. The ecohabitat chart has relevant structures and characteristics that provide us with a number of observations and/or interpretations. 284

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Fig. 6. The ecohabitat chart. The critical geophysical environments for diverse species in Arthropoda, Mollusca, and Annelida, such as bivalves (Ruditapes philippinarum, Donax semigranosus and Mactra veneriformis), polychaete worms (Ceratonereis erythraeensis and Glycera nicobarica), crabs (Scopimera globosa), shrimps (Alpheus brevicristatus), decapod crustaceans (Nihonotrypaea japonica), amphipods (Haustorioides japonicus and Trinorchestia trinitatis) and isopods (Excirolana chiltoni) on sandy beaches and sandflats are shown, together with the diverse forms of the burrowing activities, as well as photographs of the representative species (see Graphical abstract).

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For all species of the macroinfauna examined in this study, there were optimum geoenvironmental conditions under which all individuals were able to burrow irrespective of their growth stages. Such optimum geophysical environments should closely relate to the population of species, although this was outside the scope of this study. The related information is described in Appendix B of this paper. In the state-of-the-art and practice of ecological restoration, many effects are still understudied (Boerema and Meire, 2017), and new science and technologies, particularly concerning what biophysical factors support ecosystem services, have been desired (Palmer and Filoso, 2009). The present study has demonstrated the crucial role of the geoenvironmental dynamics in biological activities and ecosystems, and provided a new rational basis, namely, the ecohabitat chart, for the framework of ecological conservation and restoration.

5. Conclusions Suction dynamics-induced geophysical processes were shown to govern the manifestation of considerable variations in the geophysical environments of the sandy beaches and sandflats examined here, from essentially saturated states to the supratidal zones of exposed sandy beaches. The diversity of macroinfauna inhabiting the sandy beaches and sandflats exhibited distinct changes in their responses to variations of such geophysical environments. Under critical conditions, biological activities, including burrowing, burrow development, and physiological activity, were hindered or prevented from taking place. All such knowledge was integrated to construct and develop an ecohabitat chart, which represents the complex interrelationships between the habitat geophysical environments and the diverse biological activities among species and their growth stages. The diversity of species–geoenvironmental dynamics relationships based on the ecohabitat chart were shown to be consistent with the field evidence obtained through two habitat restoration projects. The present results demonstrate the crucial role of the habitat geophysical environments in the distribution of diverse species, and account for the cause and effects underlying such close linkage of the biodiversity–geoenvironmental dynamics of sandy beaches and sandflats. The present study will facilitate novel design, assessment and management for conservation and restoration of habitats of estuarine and coastal macroinfaunal ecosystems.

Fig. 7. The number of species versus suction obtained from the ecohabitat chart.

based on the ecohabitat chart shows that the number of species that can adapt to and live in the geoenvironment decreases with increasing magnitude of suction. This stems from the fact that a large number of species can burrow in soft sediments; however, increasing sediment hardnesses due to suction development and suction-dynamics-induced compaction disable burrowing of species, increasing suction yields less saturation and hinders the water-breathing process in sediments, and excessive suction leads to loss of effective cohesion and destabilizes the burrows. Such species diversity–geoenvironmental dynamics relationships have been shown to be consistent in nature with what has been observed in the field from two habitat restoration projects (Fig. B2). A short discussion of the geoenvironmental dynamics-based habitat design, assessment and management is given in Appendix B of this paper. The concept that large-scale community patterns involving species diversity are regulated by the hydrodynamic processes above the sediments and the associated morphodynamics has gained widespread support (e.g. McLachlan, 1990; Jaramillo et al., 1993, 1995; Defeo et al., 2001; Brazeiro, 2005; Lastra et al., 2006; Defeo and McLachlan, 2011). However, the present study clearly shows the important role of the sediment geophysical processes in the diversity of macroinfauna on sandy beaches and sandflats. The ecohabitat chart also illustrates how rich natural ecosystems manifest themselves through the complex interrelationship among the diverse species.

Acknowledgement This research was supported by the Japan Society for the Promotion of Science Grants-in Aids for Scientific Research (JP15H02265 and JP20360216).

Appendix A Table A1 Protocol for burrowing experiments on R. philippinarum. Agar concentration (g/l)

τ* (kPa)

Shell length L (mm) 2–4

1

0.01

1.25

0.02

1.5

0.03

1.75

0.04

2

0.05

4–6

6–8

10–12

14–16

19–21

n=1 Sink

n=1 Sink n=4 a=4

24–26

29–31

n=4 a=4

n=4 a=4

n=4 a=4

n=4 a=4

n=4 a=4

n=3 a=3

n=3 a=3

34–36

44–46

49–51

n=1 Sink

n=1 Sink

n=1 Sink n=3 a=3 n=7 a = 3, b=4

n=4 b=4

(continued on next page) 286

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Table A1 (continued) Agar concentration (g/l)

τ* (kPa)

Shell length L (mm) 2–4

4–6

2.25

0.06

2.5

0.08

n=8 a=8

n=5 a=5

2.75

0.10

3

0.13

n=5 a = 2, b = 1, c=2 n=7 a = 1, c = 6

3.25

0.15

n=6 b = 1, c = 5

n=5 a = 2, b = 1, c=2 n=8 a = 2, b = 1, c=5 n=9 b = 2, c = 7

n=4 c=4

n=4 c=4

3.5

3.75

4

0.18

0.21

0.24

4.25

0.27

4.5

0.30

n=3 c=3

6–8

n=8 a=8

10–12

n=4 a=4

14–16

n=4 a=4

19–21

24–26

29–31

34–36

44–46

49–51

n=4 a=4

n=3 a=3 n=3 b = 2, c = 1

n=3 a=3 n=3 b=3

n=3 b=3 n=3 a = 1, b = 1, c=1 n=3 b = 1, c = 2

n=3 c=3

n=8 b=8 n=7 b = 3, c=4 n=7 b = 1, c=6 n=4 c=4

n=3 c=3

n=4 c=4

b = 1,

n=5 a = 2, b = 1, c=2 n=3 b = 2, c = 1

b = 2,

n=3 c=3

n=3 a=3 n=3 a = 2, c=1 n=3 a = 1, c=2 n=3 a = 1, c=2 n=3 b = 2, c=1 n=3 c=3

b = 1,

n=3 c=3

n=3 c=3

n=4 a=4 n=4 a=4

n=5 a=5

n=8 a=8

n = 12 a = 12

n=6 a = 3, b = 1, c=2 n=7 a = 1, b = 1, c=5 n=7 b = 1, c = 6

n=5 a=5

n=4 a=4

n=6 a = 2, b = 2, c=2 n=6 a = 1, b = 1, c=4 n=4 c=4 n=4 c=4

n=4 a = 1, b = 1, c=2 n=8 a = 2, b = 1, c=5 n=4 a = 1, c = 3 n=4 c=4 n=4 c=4

n=4 a = 2, c=1 n=8 a = 2, c=4 n=4 a = 2, c=1 n=8 b = 1, n=4 c=4

n=5 c=5 n=4 c=4

c=7

n=3 b=3

n=3 c=3

τ*: Vane shear strength. Air temp.: 20.8 ± 1.1 °C, Water temp.: 19.2 ± 1.1 °C, Salinity: 27. Symbols a, b, and c denote the observed results. The symbol a means that the individual completed vertical burrowing. The symbol b means that the individual exhibited inclined burrowing and/or partial burrowing. The symbol c means that the burrowing was impossible. Air and water temperatures are mean values ± SE.

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Fig. A1. Sediment hardnesses simulated in the laboratory. (a) Vane shear strength versus suction for three different sediment relative densities. The sediments were taken from the Nojima sandflat; (b) Vane shear strength versus agar concentration (n = 22, y = 0.011x2.191, R2 = 0.998, p < 0.0001). Data represent mean values ± SE.

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Fig. A2. Relationship between shell length and wet weight of R. philippinarum. (n = 1083, y = 0.0002x3.031, R2 = 0.990, p < 0.0001).

Fig. A3. Index of burrowing activity versus vane shear strength for seven species of macroinfauna that belong to Annelida, Anthropod and Mollusca. The results shown in Figs. 4 and 5 and the data from Fig. 6 of Sassa et al. (2011) are summarized in this figure.

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Appendix B. Supplementary data Supplementary data to this article can be found online at https://doi.org/10.1016/j.ecss.2019.02.002.

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