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Long-term changes in a trochid gastropod population affected by biogenic sediment stability on an intertidal sandflat in regional metapopulation context

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Abstract

Although destabilization and stabilization of soft sediments by macro-infauna are regarded as key to understanding benthic community dynamics, how component populations are affected concurrently by both agents was poorly investigated. On an intertidal sandflat, Kyushu, Japan during 1979 − 2014 (previous study) and 2015 − 2019, monitoring was made of the populations of the filter-feeding gastropod, Umbonium moniliferum, the burrow-dwelling ghost shrimp, Neotrypaea harmandi (destabilizer), and the tube-building polychaete, Mesochaetopterus minitus (stabilizer). Results revealed that gastropod population changes were driven by an interplay of shrimp, polychaete, and the stingray, Hemitrygon akajei, foraging for shrimp by sediment excavation. The gastropod went through high abundance (1100 m−2) in 1979, extinction during 1986 − 1997, two marked recoveries with peaks in 2001 and 2009, a slight recovery in 2016, and near extinction in 2019. These changes largely followed the fluctuation in shrimp density across a threshold of 160 m−2 inhibiting gastropod recruitment. The polychaete exhibited intermittent outbreaks with peaks in 2000, 2007, and 2016, with maximum densities of 15,000 − 24,000 m−2. Sandflat topography and sedimentary variables were measured during 2015 − 2017. Sediment stabilization by polychaete aggregations at the mid-tidal zone is suggested to have boosted gastropod recruitment. Release at sea and retrieval on shore of drift cards mimicking gastropod larvae with 3- to 9-day planktonic duration was conducted in 2008 − 2009 to specify source populations sending larvae to the present population. Potential source populations were censused in 1998 and 2017 − 2018. Their recent virtual extinction appears responsible for the present population’s decline from 2011. This raises the need for metapopulation perspective to understand local dynamics.

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Fig. 1
Fig. 2
Fig. 3

adapted from Fig. 11A–D of Tamaki and Takeuchi (2016). The value for 2014 identical to that for March 21, 2015, from which onward values on respective sampling occasions are indicated (Sp, spring; Su, summer). The combined data from March 1 and 30 represented by the latter. The empirical threshold ghost shrimp density, 160 shrimp m−2, above which gastropod recruitment is inhibited, indicated in horizontal broken line. b Yearly change in the abundance of the polychaete worm, Mesochaetopterus minutus (sum of the densities over all transect stations) during the study period. For each year during 1979 − 2014, the summer value given. From March 2015 onward, values on respective sampling occasions are indicated. c Yearly change in coefficient of permission by ghost shrimp [CP (shrimp → gastropod), with the value for March 21, 2015 identical to that for 2014] and coefficient of possible boost by worm for gastropod recruitment [CPB (worm → gastropod)]; see text for these coefficient definitions. d Yearly change in the abundances of the gastropod, Umbonium moniliferum [sum of densities over all transect stations for 0 + old cohort and for combined cohort (i.e., 0 + old cohort and 1 + and older (up to 3 +) cohort; see Supplementary material 1)] during the study period. For each year during 1979 − 2014, the summer value given. From March 2015 onward, values on respective sampling occasions are indicated. Six links between year (X – 1) in panel c and year X in panel d illustrated in arrowed dotted lines, with black for CP [plus, promotion; minus, inhibition with (almost) zero CP] and red for CPB (plus, promotion). Note that (1) each year from 1979 to 2014 in panel d is aligned with its previous year in panels a − c so that a possible influence from ghost shrimp or worm on gastropod recruitment within each same year can easily be traced [i.e., the abundance of gastropod’s 0 + old cohort in the summer of year X reflects that of newly recruited gastropods in October of year (X – 1) and thus mean (± SD) of ghost shrimp in putative October and the abundance of worm in summer are plotted on the (X – 1)-year tick], (2) for the period from March 2015 to August 2019, each real sampling occasion is aligned across all panels, and (3) between 2014 and 2015Sp, the year-tick positions are adjusted between panels a − c and panel d

Fig. 4

adapted from Fig. 5c of Tamaki et al. (2018b) and Figs. 10 and 13 of Tamaki and Takeuchi (2016). In panels a and b, except for the March 2017-data (panel a) and for the May 2016- and March 2017-data (panel b), the summer data indicated for each year. MLWS: mean low water level in spring tide periods

Fig. 5
Fig. 6
Fig. 7

adapted from Fig. 6 of Tamaki et al. (2018b) in broken line connecting plots. Except for the March 2017-data in solid line connecting plots, the summer data indicated for each year. MLWS: mean low water level in spring tide periods. d Ground heights of the sandflat surface relative to mean sea level in Tokyo Bay on the transect in each summer of 2015, 2016, and 2017. e Spatial variations in vane shear strengths at 1-cm and 4-cm depths of the surface sediment on the transect in each summer of 2015 and 2016 and in spring 2017. f Vane shear strengths at 1-cm depth inside and outside polychaete worm (Mesochaetopterus minutus) aggregations around the blue circle point in Fig. 9b, corresponding to varying groundwater tables

Fig. 8
Fig. 9
Fig. 10

adapted from Fig. 11 of Mandal et al. 2010). The quadrature date prior to Release-2: October 3. Two breaks with no card retrieval in the lines with no dots. Parentheses: cards picked up by a person of the local town on one date and handed to us (no retrieval made ourselves on that date)

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Acknowledgements

We thank staffs of Reihoku Town Office and Fisheries Association for allowing for aerial survey, T. Kawamoto, Y. Agata, Y. Takahara, S. Mandal, and S. Sen-ju for drift card practices, K. Watanabe and S. Goto for ground-height measurement, G. Sagara, H. Ohashi, S. Matsushita, Y. Sato, H. Kamoda, M. Kawata, Y. Matsuda, K. Honma, K. Matsumoto, and K. Ishii for benthos sampling and laboratory works, and T. Takikawa, two reviewers, and handling editor for constructive comments on the manuscript. The water-depth data (Fig. 1a) were provided by Hydrographic and Oceanographic Department, Japan Coast Guard.

Funding

Funding This study was partly supported by the Japan Society for the Promotion of Science Grants-in-Aid for Scientific Research KAKENHI JP19310148 and JP26440244 to AT and JP15H02265 to SS.

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Authors and Affiliations

  1. Graduate School of Fisheries and Environmental Sciences, Nagasaki University, Bunkyo-machi 1-14, Nagasaki, 852-8521, Japan

    Akio Tamaki & Seiji Takeuchi

  2. Port and Airport Research Institute, National Institute of Maritime, Port and Aviation Technology, 3-1-1 Nagase, Yokosuka, 239-0826, Japan

    Soonbo Yang & Shinji Sassa

Authors
  1. Akio Tamaki
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  2. Seiji Takeuchi
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  3. Soonbo Yang
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  4. Shinji Sassa
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Contributions

This study was designed by AT; field monitoring was conducted by AT (during 1979–2019) and ST (during 2008–2018); drift card release and retrieval was conducted by AT and ST; laboratory processing of biological samples was conducted by AT; laboratory processing of sediment samples was conducted by ST and AT; data analysis for these samples was conducted by AT and ST; measurement and analysis of sediment hardness and sandflat topography was conducted by SY and SS (during 2015–2017); the manuscript was written by AT with inputs from ST, SS, and SY; the final illustrations were prepared by ST and SY.

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Correspondence to Akio Tamaki.

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Tamaki, A., Takeuchi, S., Yang, S. et al. Long-term changes in a trochid gastropod population affected by biogenic sediment stability on an intertidal sandflat in regional metapopulation context. Mar Biol 168, 26 (2021). https://doi.org/10.1007/s00227-021-03828-9

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