Biodiversity Data Journal : Research Article
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Research Article
Intertidal insects associated with halophytic Suaeda (Amaranthaceae) in Japan: a case study in Saga, northern Kyushu
expand article infoAkihito Kita‡,§, Ayman Khamis Elsayed‡, Makoto Tokuda‡,|
‡ Faculty of Agriculture, Saga University, Saga, Japan
§ Saga Prefectural Space and Science Museum, Takeo, Japan
| The United Graduate School of Agricultural Sciences, Kagoshima University, Kagoshima, Japan
Corresponding author: Makoto Tokuda (tokudam@cc.saga-u.ac.jp)
Academic editor: David Bilton
Received: 10 Dec 2021 | Accepted: 30 Mar 2022 | Published: 28 Apr 2022
© 2022 Akihito Kita, Ayman Elsayed, Makoto Tokuda
This is an open access article distributed under the terms of the Creative Commons Attribution License (CC BY 4.0), which permits unrestricted use, distribution, and reproduction in any medium, provided the original author and source are credited.
Citation: Kita A, Elsayed AK, Tokuda M (2022) Intertidal insects associated with halophytic Suaeda (Amaranthaceae) in Japan: a case study in Saga, northern Kyushu. Biodiversity Data Journal 10: e79184. https://doi.org/10.3897/BDJ.10.e79184
 Open Access

Abstract

In contrast to a great diversity in insects in terrestrial and freshwater ecosystems, few known species have adapted to inhabit marine environments. In this study, we surveyed insects associated with halophytic plants of Suaeda (Amaranthaceae) distributed in intertidal zones, in northern Kyushu, Japan. On four Japanese native species of Suaeda, we found insects belonging to five orders and 18 species. Amongst them, the genus Clanoneurum (Diptera: Ephydridae) and Coleophora deviella (Lepidoptera: Coleophoridae) were newly reported from Japan; and Orthotylus (Melanotrichus) parvulus (Hemiptera: Miridae) was newly recorded from Kyushu. The seasonal occurrence of several insects on Suaeda is reported.

Keywords

halophyte, insect fauna, intertidal zone, Suaeda

Introduction

Insects have achieved a great diversity in terrestrial and freshwater ecosystems, but they seldom inhabit marine environments (e.g. Cheng 1976, Ward 1992). Only some insect taxa are known to adapt to intertidal zones and very few in neritic and oceanic environments (Ward 1992, Ikawa et al. 2012, Kaiser et al. 2016).

In intertidal zones, Coleoptera are the most dominant group in terms of the number of genera reported and followed by Diptera, Collembola and Hemiptera (Ward 1992). These insects exhibit various adaptations to seawater, such as plastron respiration under seawater and behavioural avoidance of submergence (Hinton 1976, Ward 1992). Adaptive mechanisms of intertidal insects to marine habitats are interesting study subjects to understand their survival strategies in harsh environments for many insects.

Some herbivorous insects are associated with halophytes growing in the intertidal zones (Foster and Treherne 1975, Dorchin 2001, Dorchin and Freidberg 2008, Cho et al. 2015, Elsayed et al. 2015). As herbivory critically affects some plant community structures in intertidal zones (Rand 2002, Pennings et al. 2007), further intensive studies of herbivores are important to understand their role in determining plant community structures in intertidal zones.

The genus Suaeda (Amaranthaceae) consists of approximately 100 species and most of them grow in coastal areas and tidal wetlands (Yonekura 2017). Several studies have reported insects on Suaeda, such as a psyllid (Hemiptera: Sternorrhyncha) associated with Suaeda japonica Makino in Korea (Cho et al. 2015); gall midges (Diptera: Cecidomyiidae) in the Holarctic Region and South America (Kieffer 1909, Kieffer and Jörgensen 1910, Felt 1918, Mamaev and Mirumian 1990, Dorchin 2001, Dorchin and Freidberg 2008, Skuhravá et al. 2014, Elsayed et al. 2015) and their hymenopteran parasitoids (Gates et al. 2018), a leaf beetle in North America (von Groll et al. 2022) and lepidopterans in various localities worldwide (Paik et al. 2013, Adamski et al. 2018, Karisch et al. 2020, Budashkin and Bidzilya 2021). However, information on insect fauna associated with Suaeda is still fragmental and comprehensive studies have never been conducted as far as we know.

The area facing the Ariake Sea in Saga Prefecture has the largest mudflats in Japan, owing to the largest tidal range in the country, which provides a suitable habitat for halophytes including Suaeda (Henmi et al. 2017, Tokuda 2019). In the present study, we periodically surveyed the insect fauna associated with four Suaeda species in Saga, Japan and examined the seasonal occurrence of several dominant insect species to reveal their ecological aspects.

Materials and Methods

Study plants

Four native species of Suaeda are known to be distributed in Japan (Yonekura 2017): Suaeda glauca (Bunge) Bunge distributed in Honshu and Kyushu, Japan as well as in eastern Siberia, Ussuri, Mongol, China and Korean Peninsula; Suaeda maritima (L.) Dumort. subsp. asiatica H. Hara distributed widely in East Asia including Honshu and Kyushu, Japan; Suaeda malacosperma H. Hara distributed in western Honshu and Kyushu, Japan, as well as in Korean Peninsula; and S. japonica distributed in northern Kyushu, Japan and Korean Peninsula. They are all annual plants (Yonekura 2017). We investigated insects associated with all four native Suaeda species in this study.

Periodical investigations

Field investigations were conducted at the following six census sites in Saga Prefecture: Benga, Imari City (S. glauca); Iida, Kashima City (S. maritima asiatica); Muta, Tara Town (S. maritima asiatica); Inuido, Saga City (S. malacosperma); Edo, Saga City (S. japonica); and Higashiyoka, Saga City (S. japonica) (Fig. 1). Amongst them, Benga faces the Genkai Sea, i.e. areas between the Japan Sea and the East China Sea and the other five sites are located alongthe coastline of the Ariake Sea. The investigations were conducted at two-week intervals from April to November 2015 and monthly from December 2015 to December 2016.

Figure 1.  

Map of census sites. Suaeda plants were surveyed at the following sites: S. glauca in Benga, S. japonica in Edo and Higatayoka, S. malacosperma in Inuido and S. maritima asiatica in Iida and Muta.

At each census site, insects on Suaeda plants were collected by an approximately five-minute sweeping on each census date (qualitative survey). In 2016, three quadrats (1 m × 1 m) were set in Suaeda communities and insects inhabiting there were visually investigated in each quadrat (quantitative survey) and collected by net sweeping. Collected insects were kept either as dried specimens or in 99% ethanol for future DNA analyses.

Inventory data of insects on each Suaeda species were based on both qualitative and quantitative surveys and the seasonal occurrence data of major species were on the qualitative survey.

Results and Discussion

Insect fauna

Throughout the field surveys, we found 18 insect species belonging to five orders from Suaeda (Table 1).

Table 1.
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Insects found on Suaeda species and their feeding habit. Abbreviations of Suaeda plants are as follows: SG, S. glauca; SJ, S. japonica; SMRT, S. maritima asiatica; and SMRC, S. maracosperma. P: present on the plant.

Order

Family

Species

Feeding habit

SG

SJ

SMRT

SMRC

Orthoptera

Tettigoniidae

Gampsocleis buergeri

Omnivore

P

Tetrigidae

Euparatettix insularis

Herbivore

P

Hemiptera

Aphididae

Aphis sp.

Herbivore

P

P

P

Miridae

Orthotylus (Melanotrichus) parvulus

Herbivore

P

P

P

Coleoptera

Curculionidae

Baris scolopacea

Herbivore

P

P

Coccinellidae

Coccinella septempunctata

Predator

P

Harmonia axyridis

Predator

P

Propylea japonica

Predator

P

Chrysomelidae

Medythia nigrobilineata

Herbivore

P

Oedemeridae

Eobia cinereipennis

Herbivore

P

Diptera

Ephydridae

Clanoneurum sp.

Herbivore

P

P

Syrphidae

Metasyrphus nitens

Herbivore

P

Epistrophe balteata

Herbivore

P

Lepidoptera

Coleophoridae

Coleophora deviella

Herbivore

P

P

Noctuidae

Sarcopolia illoba

Herbivore

P

Noctuidae

Spodoptera litura

Herbivore

P

P

Crambidae

Spoladea recurvalis

Herbivore

P

P

Geometridae

gen. sp. (unidentified)

Herbivore

P

P

Number of insect species found

7

12

4

5

In Orthoptera, Gampsocleis buergeri de Haan (Tettigoniidae) and Euparatettix insularis Bey-Bienko (Tetrigidae) were found respectively on S. glauca (in 2015) and S. malacosperma. Amongst them, G. buergeri is distributed in western Honshu and northern Kyushu, Japan and E. insularisis is in Honshu, Shikoku, Kyushu, the Izu Islands, the Ogasawara Islands and Korean Peninsula (Ichikawa et al. 2006). Both species are polyphagous and not specialists of Suaeda plants.

In Hemiptera, Aphis sp. (Aphididae) was found on all four Suaeda species surveyed (Fig. 2A). This species is probably undescribed and a specialist of Suaeda plants (Y. Matsumoto, personal communication). Orthotylus (Melanotrichus) parvulus (Miridae) was found on S. maritima asiatica and S. japonica (Fig. 2E). This species is associated with S. maritima asiatica and Salicornia europaea (Amaranthaceae) and is distributed in the Palearctic Region, but in Japan, it was only known from Tsushima Island and Hyogo Prefecture, Honshu (Yasunaga et al. 2001, Yasunaga et al. 2016, Shishido and Yasunaga 2016). We newly report this species from Kyushu, as mentioned earlier and S. japonica is a new host record for this species.

Figure 2.  

Insects found on Suaeda plants. A A nymph of Aphis sp. (Hemiptera: Aphididae) found on S. maritima asiatica in Iida; B An adult of Baris scolopacea (Coleoptera: Curculionidae) found on S. glauca in Benga; C An adult of Clanoneurum sp. (Diptera: Ephidridae) found on S. japonica in Edo; D An adult of Coleophora deviella (Lepidoptera: Coleophoridae) found on S. japonica in Edo; E An adult of Orthotylus (Melanotrichus) parvulus (Hemiptera: Miridae) found on S. maritima asiatica in Muta; and F An adult of Spoladea recurvalis (Lepidoptera: Crambidae) found on S. glauca in Benga.

In Coleoptera, Baris scolopacea Germar (Curculionidae) was found on S. japonica and S. glauca in 2015 (Fig. 2B). This weevil is distributed in Honshu, Shikoku, Kyushu, Tsushima, Amami-Oshima and Kuroshima in Japan, as well as in Korea and China (Yoshihara 2016). In western parts of Japan, B. scolopacea is associated with Amaranthaceae and induces galls on Achyranthes sp., Chenopodium spp. and Dysphania anthelmintica (L.) Mosyakin et Clemants (= Ambrina anthelmintica (L.) Spach) (Yoshihara 2016). In this study, we did not find galls on Suaeda plants. As we found stem galls on Atriplex patens (Litv.) Iljin (Amaranthaceae) growing close to Suaeda, the weevil is possibly responsible for them. Three widely distributed species of Coccinellidae in Japan were found on S. japonica, namely Harmonia axyridis (Pallas), Coccinella septempunctata L. and Propylea japonica (Thunberg). As these coccinellids are predatory species (Sakamoto 2018), they probably visit Suaeda plants to feed on aphids and other insects. Furthermore, Medythia nigrobilineata (Motschulsky) (Chrysomelidae) was found on S. malacosperma and Eobia cinereipennis (Motschulsky) (Oedemeridae) was on S. glauca (in 2015). Medythia nigrobilineata is distributed in Hokkaido, Honshu, Shikoku, Kyushu, Sado, Tsushima, the Goto Islands, the Korean Peninsula, China and eastern Siberia and is known to feed on Fabaceae (Morimoto and Hayashi 1986). As we found wild fabaceous plants near the census site of S. malacosperma, the species may accidentally visit S. malacosperma from them. Eobia cinereipennis is distributed in Hokkaido, Honshu, Shikoku, Kyushu, Izu Islands, Amami Islands, Ryukyus and Korea. Although this species is a flower-visiting species inhabiting seasides (Morimoto and Hayashi 1986), it was collected in June which is not the flowering season of S. glauca. For this reason, this species probably visited S. glauca by chance while visiting the flowers of other plants growing around S. glauca.

In Diptera, Clanoneurum sp. (Ephidridae) was found on S. japonica and S. maritima asiatica (Fig. 2C) and two species of Syrphidae, namely Epistrophe balteata de Geer and Metasyrphus nitens Zetterstedt, were found on S. japonica. The genus Clanoneurum is newly reported from Japan in this paper. This genus contains four species worldwide (GBIF Secretariat 2019). Further taxonomic studies are needed to confirm whether the species found in this study is undescribed. As the syrphids are found in October, the flowering season of S. japonica, they might visit the flowers of the plant. The pollination ecology of these Suaeda plants is an important study subject in the future.

In Lepidoptera, Coleophora deviella Zeller (Coleophoridae) was found on S. japonica and S. maritima asiatica (Fig. 2D). This species is known in the western Palaearctic Region (from Spain to southern Russia) and is associated with several species of Amaranthaceae including S. maritima (Anikin 1988, Ellis 2020). This is the first record of C. deviella from the eastern Palearctic Region. Two species of polyphagous Noctuidae were found in this study; Sarcopolia illoba (Butler) was on S. glauca and Spodoptera litura (Fabricius) was on S. glauca and S. japonica. Both species are polyphagous species (Yoshimatsu et al. 2011). In addition, Spoladea recurvalis (Fabricius) (Crambidae) was found on S. japonica, S. glauca and S. maritima asiatica (Fig. 2F). This species is polyphagous and known to be associated with Amaranthaceae and some other plants (Yoshimatsu and Miyata 2011). Spoladea recurvalis was previously collected over the East China Sea and, in Kyushu, large numbers of individuals have been collected in autumn along the coast, suggesting its long-distance migration habit (Yoshimatsu and Miyata 2011). In addition, larvae of an unidentified species of Geometridae were found on S. japonica and S. maritima asiatica.

Seasonal occurrence

Amongst insects found on Suaeda species, the seasonal occurrence of Aphis sp., Clanoneurum sp. and C. deviella was investigated in the quantitative survey in 2016 by counting individuals of Aphis sp., leaves mined by Clanoneurum sp. and larval cases formed by C. deviella on plants, respectively.

In Edo and Higashiyoka, the number of Aphis sp. individuals peaked in September (Fig. 3A). In addition, another small peak was detected in July in Edo. As no individuals were found in May and from October to December, this species may exhibit host alternation, but hosts, other than Suaeda, are not yet known at present.

Figure 3.  

Seasonal changes in densities of major insects on Suaeda. A Seasonal changes in the number of Aphis sp. individuals (per plant) on Suaeda plants in 2016; B Seasonal changes in the number of mines (per plant) produced by Clanoneurum sp. larvae on Suaeda plants in 2016 and C Seasonal changes in the number of larval cases (per plant) formed by Coleophora deviella on Suaeda plants in 2016.

Mines produced by Clanoneurum sp. were found from July to October in Iida and Muta (Fig. 3B). At both census sites, two peaks were found in summer (July or August) and autumn (October). The first peak was larger than the second in Iida and vice versa in Muta. These results suggest that the species is bivoltine.

The number of larval cases formed by C. deviella gradually increased from summer to autumn and peaked in September or October in all localities (Fig. 3C), suggesting the univoltine life cycle of this species.

Conclusions

In this study, we recognised 18 insect species on Suaeda plants and investigated seasonal occurrence of several herbivorous species. Amongst the insects, Aphis sp. is probably an undescribed species; O. parvulus was newly recorded from Kyushu; the genus Clanoneurum and C. deviella were newly reported from Japan. As mentioned in the Introduction, faunistic studies of insects associated with Suaeda is limited worldwide, but our findings indicate diverse fauna of insects, especially halophyte-associated herbivores adapting to intertidal zones.

Acknowledgements

We thank S. Iwamura for his valuable information on Suaeda plants. Our thanks are extended to Y. Matsumoto, Y. Nakatani, Y. Sakamaki, M. Suwa and H. Yoshitake for identifying Aphis sp., O. (M.) parvulus, Clanoneurum sp., B. scolopacea and C. deviella, respectively and for giving us useful information about these insects. We are grateful to S. Adachi-Fukunaga, A. Tetsuka, M. Okuzono and other members of the Laboratory of Systems Ecology, Faculty of Agriculture, Saga University for their kind help in field surveys.

Ethics and security

  • This work is original research carried out by the authors.
  • All authors agree with the contents of the manuscript and its submission to the journal.
  • No part of the research has been published in any form elsewhere, unless it is fully acknowledged in the manuscript.
  • The manuscript is not being considered for publication elsewhere while it is being considered for publication in this journal.
  • Any research in the paper not carried out by the authors is fully acknowledged in the manuscript.
  • All appropriate ethics and other approvals were obtained for the research.

Author contributions

Conceptualisation: [Makoto TOKUDA]; Methodology: [Akihito KITA], [Makoto TOKUDA]; Data Analysis: [Makoto TOKUDA]; Investigation: [Akihito KITA], [Ayman Khamis ELSAYED], [Makoto TOKUDA]; Data Curation: [Akihito KITA], [Makoto TOKUDA]; Writing-Original Draft Preparation: [Akihito KITA], [Makoto TOKUDA]; Writing-Review and Editing: [Akihito KITA], [Ayman Khamis ELSAYED], [Makoto TOKUDA]; Visualisation: [Akihito KITA], [Ayman Khamis ELSAYED], [Makoto TOKUDA]; Supervision: [Makoto TOKUDA]; Project Administration: [Makoto TOKUDA].

All authors have read and agreed to the published version of the manuscript.

Conflicts of interest

The authors declare no conflict of interest.

References

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