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Asian Australas. J. Biosci. Biotechnol. 2021, 6 (2), 50-59; doi: 10.3329/aajbb.v6i2.56140
Asian-Australasian Journal of
Bioscience and Biotechnology
ISSN 2414-1283 (Print) 2414-6293 (Online)
www.ebupress.com/journal/aajbb
Review
Trends of bivalve (Bivalvia) research in East Malaysia: a systematic review
Hadi Hamli and Abdulla-Al-Asif*
Department of Animal Science and Fishery, Faculty of Agricultural Science and Forestry, Universiti Putra
Malaysia Campus Bintulu, 97008 Bintulu, Sarawak, Malaysia
*Corresponding author: Abdulla-Al-Asif, Department of Animal Science and Fishery, Faculty of Agricultural
Science and Forestry, Universiti Putra Malaysia Campus Bintulu, 97008 Bintulu, Sarawak, Malaysia. E-mail:
jessoreboyhemel@gmail.com
Received: 03 July 2021/Accepted: 25 August 2021/ Published: 31 August 2021
Abstract: The unique biodiversity in Malaysia makes this country a global hotspot for different aspects of
research. Many European and non-native research activities are conducting by different research groups,
whereas local institutions also collaborate with them to explore the pristine nature of west (peninsular Malaysia)
and East Malaysia (Sarawak and Sabah province). East Malaysia is located in Borneo Island, and the
biodiversity of this area are huge. The current review work scrutinized the information about the research
activities on aquatic bivalve species and their different aspects of the investigation. This investigation revealed,
to date 28 research publications were published on aquatic bivalves from eastern Malaysia, where biodiversity,
conservation and ecology was the major aspect of research. The other aspects were aquaculture, natural history
and taxonomy, nutritional study, reproduction of bivalve, morphology, and pollution can be mentionable. The
major portion of this eastern Malaysia are not investigated and it is assumed that many species are still not
reported. Further studies demand to explore the vast bivalve biodiversity of this part of Malaysia.
Keywords: Mollusca; Bivalvia; Malaysian Borneo; Sarawak; Sabah
1. Introduction
Malaysia is one of the biologically diverse regions on the planet where some fauna have an extremely limited
range and are only found in this landmass (Abdullah et al., 2015; Tong, 2020). Eastern part of Malaysia is well
known as ―Borneo Island‖, and this huge landmass was formed during the Mesozoic era as a result of the
accretion of microcontinental fragments, ophiolite terranes, and Island arc crust onto a Paleozoic continental
core (Balaguru et al., 2003). This phenomenon occurred in millions of years ago but it helps to accumulate huge
number of unique flora and fauna in this bioregion (Galey et al., 2017; Leonard et al., 2015). The Mollusca
fauna were detected unique in nature, especially bivalves; where some of the endemic bivalve species only
found in this biogeographic region (Zieritz et al., 2021, 2020).
Although the availability of bivalve fauna are ample in eastern Malaysia, which are reported by several
European and local research groups (Ashton et al., 2003; Hamli et al., 2012a; Raven, 2019; Zieritz et al., 2020).
The history of bivalve research in eastern Malaysia can be phrased as ―one of the oldest‖ compare to the
peninsular Malaysia, as the first taxonomic checklist of bivalve was published in 1981 from peninsular
Malaysia; while the first bivalve was reported in Eastern Malaysia through the report of Marcia japonica (J. F.
Gmelin 1791) from federal territory of Labuan (Gmelin, 1791) while the first research from the present century
was recorded from Sematan mangrove forest, Sarawak (Ashton et al., 2003; Morris and Purchon, 1981; Way
and Purchon, 1981). The research of Ashton et al. (Ashton et al., 2003) found the first approach to introduce the
bivalve fauna from Malaysian Borneo to the rest of the world; it is assumed that, the major focus of Ashton et
al. (Ashton et al., 2003) work was to assess the crustaceans and gastropods macro-fauna in Sematan mangrove
forest, but very fortunately they reported three species of bivalve. In the last century a noteworthy work was
Asian Australas. J. Biosci. Biotechnol. 2021, 6 (2) 51
conducted by Turner and Santhakumaran (1989) from Pantai river, Sarawak and its adjacent areas and recorded
four endemic bivalve species.
After the initial study, some studies in last decade were also focused on bivalve fauna, targeting heavy metals
accumulation by bivalve and biodiversity studies (Abdullah et al., 2007; Shabdin, 2010; Shabdin and Alfred,
2007). The new era of bivalve research in East Malaysia, especially in taxonomic aspect was introduced by
Wong and Arshad (Wong and Arshad, 2011), where they reported 18 bivalve species from 12 families from
Pulau Mabul, Sabah. The next milestone was settled by Hamli et al. (Hamli et al., 2012a), and they reported 19
species comprising 11 families from different location from Sarawak, Malaysia.
Several gastropod studies were also found from eastern Malaysia including description and identification of
Pachychilidae (Hadi Hamli et al., 2020), diversity of Caenogastropoda (H. Hamli et al., 2020a), investigation of
edible gastropod (Hamli et al., 2013), etc. However, the present focus was only penetrated into the bivalves and
research aspects of bivalves in Sarawak and Sabah.
It is evident that only few academic and research institutions were found involved in the bivalve research in east
Malaysia; where the major portion were contributed by Universiti Putra Malaysia, Bintulu Sarawak campus (13
papers as first author). The other academic institutions such as Universiti Malaysia Sarawak also conducted
several studies.
The good news is that Eastern Malaysia is abundant in undiscovered and unreported bivalve species; the bad
news is that the number of researchers and published documents on various aspects of bivalve fauna were found
limited. Considering these potentiality and gaps in research this review aims to compile and analyze various
aspects of bivalve research conducted in East Malaysia. This review also provide a glimpses of existing research
facilities available in Eastern Malaysia to conduct bivalve research and the institutional framework to support
research.
2. Literature search strategy
The distribution and abundance records of bivalves in Eastern Malaysia (Sarawak and Sabah) (Figure 1) were
accumulated from the existing literature, monographs, reviews, checklists, catalogues, poster, conference paper,
conference poster, websites and fishery reports from East Malaysian water from the time periods of 1791 to
2021. The literature search were performed with Google Scholar web search using "Publish or Perish" software
(Harzing, 2007) from the time period of March 2019 and September, 2021. The specific key words were
inserted and search for the documents [("Malaysia" AND "Borneo") AND ("Bivalvia" OR "Bivalve" OR
"Sarawak" OR "Sabah" OR "Marine Bivalve" OR "Freshwater Bivalve" OR "Macrofauna" OR "Marine
Mussel" OR "Freshwater Mussel" OR "Mollusk" OR "Freshwater Snails" OR "Marine Snails" "Freshwater
Clam" OR "Marine Clam" OR "Macrofauna"]. We extracted the papers related with aquatic Bivalvia in Eastern
Malaysia. After extraction of all related published papers we classified the papers into seven research niche,
including (a) biodiversity, ecology and conservation, (b) aquaculture, (c) natural history and taxonomy, (d)
nutrition, (e) reproduction, (f) morphology, and (g) pollution study.
Figure 1. Map showing the places of bivalve research conducted in east Malaysia.
Asian Australas. J. Biosci. Biotechnol. 2021, 6 (2) 52
3. Bivalves research aspects
3.1. Biodiversity, ecology and conservation
Biodiversity assessment was found one of the major window (57%) in bivalve research in east Malaysia (Figure
4). A total 16 published documents were detected where major portion of the reported bivalve species through
this research aspect. The first bivalve biodiversity in eastern Malaysia was reported by Turner and
Santhakumaran (1989) from Pantai river, Sarawak; while the next report was tracked in 2003 from Semantan
mangrove forest, Sarawak (Ashton et al., 2003).
However, a very recent published document from Lawas seagrass beds, Sarawak recorded 18 species of bivalve
(Al-Asif et al., 2020). The major biodiversity checklist was reported from all over the Sarawak revealed 19
species of bivalves (11 families) in 2012 (Hamli et al., 2012a) (Table 1). However, from Pulau Mabul, Sabah 18
species of bivalve (12 families) were also reported (Wong and Arshad, 2011). The work of Al-Asif et al. (2020),
Hamli et al. (2012a) and Wong and Arshad (2011) were completely reported marine or brackish habitat’s
bivalve species; whereas, Zieritz et al. (2020) reported six species of bivalve, Zieritz and Lopes-Lima (2018)
reported eight freshwater bivalve species from family Unionidae, over the eastern Malaysia. Most of the
biodiversity related published documents were site specific or species/family specific; while the study of Zieritz
et al. (2020), Raven (2019), Hamli et al. (2012b), and Hamli et al. (2012a) covers major area of eastern
Malaysia; especially Hamli et al. (2012b) and Hamli et al. (2012a) considered the whole Sarawak during
sampling.
The study of Al-Asif et al. (2021) recorded 76 freshwater, brackish and marine water bivalve species from
Malaysian Borneo from 12 orders, 18 superfamilies and 27 families; which was the first complete and
comprehensive review of bivalve biodiversity and conservation research from Malaysian Borneo. The study of
Al-Asif et al. (2021) also suggested some conservation aspects of bivalve fauna from Malaysian Borneo which
might be helpful to protect and in some cases introduce of bivalve fauna to its natural ecosystem in East
Malaysia.
The study of Zieritz et al. (2021) reported a completely new freshwater genus, Khairuloconcha from Eastern
Malaysia having two new species, namely, Khairuloconcha sahanae (Zieritz et al. 2021) and Khairuloconcha
lunbawangorum (Zieritz et al. 2021). The study also compared the genetic material with the other species of
Unionida which suggested that these species are native to the eastern Malaysia. They suggested the habitat
protection, reintroduction of species, captive breeding and legislative framework might helpful to support the
sustainability of these newly recorded species.
On the other hand, ecological and biodiversity study of Zakirah et al. (2019) from Buntal Bay, Sarawak
recorded Tellina sp. with some polycheata species. The bivalve biodiversity in major area of Sarawak and Sabah
remains still undiscovered and not reported. Most of the research were conducted from eastern Malaysia at the
sites where vehicles and transportations might access; the major part in deep forest and creek areas are still not
investigated. This circumstance can be considered as the one of the gap for bivalve research.
3.2. Aquaculture
This review finds only one aquaculture related study of Hamli et al. (2020b), and the research team was in a
hunt for a potential phytoplankton candidate for live Sinanodonta woodiana bivalve aquaculture. The result of
the study found some of the phytoplankton for instance, Selenastrum sp., Licmophora sp. and Gloeocapsa sp.
isolated from native pond showed best result during phytoplankton culture and the study recommended to use of
these phytoplankton for bivalve aquaculture, as bivalves are phytoplankton feeder. In a recent publication Hamli
et al. (2019) discussed the potentiality of local bivalve as the potential candidate of aquaculture. It is assumed
that, this wing of bivalve research is going to expand in the east Malaysia in next few decades.
3.3. Natural history and taxonomy
The first report of bivalve species was declared by the research of Gmelin (1791) from federal territory of
Labuan (a small island near Sarawak coast and Malaysian Borneo) with the report of Marcia japonica (J. F.
Gmelin 1791) (reported as Venus japonica Gmelin, 1791). While with in next one hundred years there were no
bivalve study was tracked in Malaysian Borneo, and in 1909 Sowerby (1909) reported Pelecyora exilium (G. B.
Sowerby III, 1909) (reported as Dosinia exilium) from the coast of Sarawak.
The publication of Raven (2019) supports some of the animal dispersal theories presumed previously that some
Mollusca species (reported five bivalve species in total) move and settled one place to another in the north-west
Borneo. He argued that, nipa rafts (Nypa fruticans) might be one of the possible transportation material during
the Cenozoic periods. The dispersal and transportation history of animals are different from bivalve; as these
creatures are slow mover and they can spend their whole life where they born. The study of Raven (2019)
Asian Australas. J. Biosci. Biotechnol. 2021, 6 (2) 53
provided evidence that, bivalve species for example, Neotrapezium sublaevigatum from family Trapezidae,
Magallana rivularis from family Ostreidae might live on the leaf of nipa tree and use it as the dispersal medium
from one place to another.
3.4. Nutrition
The present review found nutritional study of Meretrix lyrata bivalve was solely based on the organ specific
mineral contents (Idris et al., 2017a). The study revealed that, minerals such as, Na and Fe found in high
concentration in the tissues compared to other minerals. The result of Idris et al. (2017a) supports that, being a
marine or brackish habitat species M. lyrata accumulate the elements Na and Fe in high amount and stores them
in their tissue. From this study, it is also revealed that, bivalves can be used as the highly nutritional food items.
3.5. Reproduction
The first reproductive study on bivalve reproduction cycle was conducted by Hamli et al. (2015a); they revealed
that, histological analysis might be helpful for sex identification of Meretrix lyrata; while some of report
suggested that the gender identification of M. lyrata found almost near to impossible (Camacho-Mondragón et
al., 2012). However, the study of Hamli et al. (2015a) provided the first insight of the maturation, spawning
stage and season of the species in eastern Malaysia. Which might opened a window for the wild bivalve
collectors and policy making organization to impose ban on the particular time of the year.
The investigation of Hamli et al. (2017) introduced condition index (CI) to measure, either the female bivalve
M. lyrata individual is ready to spawn or not. The high CI referred, comparatively high body weight, and the
individual is close to maturity stage and early spawning stage, which found directly connected with the breeding
seasons. This study also establish relations between the CI and water quality parameters especially ammonia
nitrogen might be the influential factors with the condition index. Its due to M. lyrata is a benthic animal and
decomposition materials might harmful for the growth and maturity of this species. In another reproductive
investigation revealed that gonadal development of Polymesoda expansa and generate information on spawning
and breeding season of the bivalve species (Idris et al., 2017b).
3.6. Morphology
Morphometric keys were used by Hamli et al. (2015b) in different shell parameters to identify and differentiate
three mangrove calm species namely, Polymesda erosa, P. bengalensis and P. expansa from family
Corbiculidae. The evidence and statistical analysis proved that, features for instance, standard length, ligament
length, ventral posterior margin length, etc. were the key identification parameters to separate these three
species.
The other study of Hamli et al. (2016) investigated inner shell features of mangrove clam Meretrix lyrata, M.
meretrix and M. lusoria and revealed that, the proportional ration standard length for shell wide, ligament
length, anterior length, length of cardinal tooth, adductor scar width scar, posterior adductor scar width scar, and
pallial sinus open scar might be the main morphological features to differentiate these Meretrix sp. from
Sarawak.
A recent study of Idris et al. (2021) revealed 20 bivalve species from 12 families, while suggested ventral
posterior margin length/ distance from the anterior margin to posterior margin and the length from anterior
cardinal tooth to posterior cardinal tooth/ distance from the anterior margin to posterior margin features might
be helpful to identification and differentiate between Geloina species.
3.7. Pollution
So far, one investigation was conducted to assess the impact of heavy metal such as, Cd, Cu, Cr, Pb and Zn on
Meretrix meretrix in two different estuaries in Sabah (Abdullah et al., 2007). This study suggested that, human
intervened estuary with high industrial effluent disposal might force M. meretrix to accumulate the toxic heavy
metals, in their tissue. This study was an eye opening findings in Malaysian estuary; and the study might
helpful to assess the pollution in Malaysian estuary, where bivalve can be used as bio indicator (Table 1).
Table 1. Research aspects on bivalve in eastern Malaysia.
Year Habitat Location Number of species
reported
Number of
family
Research Aspect Sources
2021 Marine and Fresh water Malaysian Borneo 76 27 Biodiversity and
conservation
Al-Asif et al. (2021)
2021 Freshwater Borneo (Sarawak and Sabah) 5 1 Biodiversity,
Multidimensional
Zieritz et al. (2021)
2021 Marine, Brackish and Fresh
water
Sarawak 21 12 Morphology Idris et al. (2021)
2020 Marine Lawas, Sarawak 18 9 Biodiversity Al-Asif et al. (2020)
2020 Freshwater UPM Bintulu, Sarawak 1 1 Aquaculture Hamli et al. (2020b)
2020 Freshwater East Malaysia (Sabah and
Sarawak)
6 1 Biodiversity Zieritz et al. (2020)
2019 Marine Buntal Bay, Sarawak 1 1 Ecology Zakirah et al. (2019)
2019 Brackish North-West Borneo, Sarawak 5 4 Natural History Raven, (2019)
2018 Freshwater East Malaysia (Sabah and
Sarawak)
8 1 Biodiversity Zieritz and Lopes-Lima,
(2018)
2017 Marine Kuching, Sarawak 1 1 Reproduction Hamli et al. (2017)
2017 Marine Kuching, Sarawak 1 1 Nutrition Idris et al. (2017a)
2017 Marine Miri, Sarawak 1 1 Reproduction Idris et al. (2017b)
2017 Marine Marudu Bay, Sabah 7 6 Biodiversity Matsumoto et al. (2017)
2016 Brackish Miri, Sarawak 2 2 Biodiversity Abu Hena et al. (2016)
2016 Marine Kuching, Sarawak 3 1 Morphology Hamli et al. (2016)
2015 Marine Over Sarawak 3 1 Morphology Hamli et al. (2015b)
2015 Marine Kuching, Sarawak 1 1 Reproduction Hamli et al. (2015a)
2014 Marine Kuching, Sarawak 5 3 Biodiversity Shabdin et al. (2014)
2012 Marine and Fresh water Over Sarawak 14 8 Biodiversity Hamli et al. (2012b)
2012 Marine and Fresh water Over Sarawak 19 11 Biodiversity Hamli et al. (2012a)
2011 Marine Sabah 18 12 Biodiversity Wong and Arshad (2011)
2010 Brackish Rajang River, Sarawak 3 3 Biodiversity Shabdin (2010)
2007 Marine and Fresh water Sarawak 4 3 Biodiversity Shabdin and Alfred ( 2007)
2007 Marine Sabah 1 1 Pollution Abdullah et al. (2007)
2003 Marine Kuching, Sarawak 3 3 Biodiversity Ashton et al. (2003)
1989 Marine, Brackish and Fresh
water
Pantai river, Sarawak 6 1 Biodiversity Turner and Santhakumaran
(1989)
1909 Marine Sarawak 1 1 Natural History Sowerby (1909)
1791 Marine Federal Territory of Labuan 1 1 Natural History Gmelin (1791)
Asian
Australas.
J.
Biosci.
Biotechnol.
2021,
6
(2)
54
Asian Australas. J. Biosci. Biotechnol. 2021, 6 (2) 55
4. Research trends
The extracted data analysis from publish or perish software revealed that, the first study on bivalve research in
this century was conducted in eastern Malaysia in 1989 from Pantai river, Sarawak (Turner and Santhakumaran,
1989) and Semantan mangrove forest, Sarawak (Ashton et al., 2003). While the first record was tracked back in
1791 by the report of Marcia japonica (J. F. Gmelin 1791) Gmelin, (1791). With a gap of three years the second
research was published in 2007 (Abdullah et al., 2007; Shabdin and Alfred, 2007). It was also observed that,
since 2014, the bivalve research related publications were very frequent. The trend analysis revealed that,
number of publications are increasing now a days (Figure 2).
Figure 2. Year wise available published documents on bivalve fauna in Eastern Malaysia.
The available publications were checked with Scopus database and found 54% (15 documents) of the
documents were indexed in the Scopus database; where as 46% (13 documents) of the documents were not
indexed in Scopus database (Figure 3). The analysis also suggested that, most of recent year publications were
indexed in Scopus database, which referring the number of good quality publications and researchers are
increasing in this fields. It is also mentionable here that, the publication of the non-Scopus indexed journals are
local but peer reviewed, so the quality of the publications rather not to be questioned. It was found two report
materials (Matsumoto et al., 2017; Zieritz and Lopes-Lima, 2018) published by Universiti Malaysia Sabah
(UMS) and International Union for Conservation of Nature (IUCN), whereas one conference material (poster)
(Abu Hena et al., 2016) was included in the present review, from International Biology Symposium 2016,
organized by Universiti Putra Malaysia. Although these three documents were not indexed in Scopus but they
were approved by either Universiti experts, IUCN expert groups or conference authority.
Figure 3. Sources of available published documents on bivalve fauna in Eastern Malaysia.
1 1 1 1
2
1 1
2
1
2 2
4
1
2
3 3
0
0.5
1
1.5
2
2.5
3
3.5
4
4.5
1791 1909 1989 2003 2007 2010 2011 2012 2014 2015 2016 2017 2018 2019 2020 2021
Numbers
of
published
papers
Years
Scopus Source
54%
Non-Scopus
Source
46%
Asian Australas. J. Biosci. Biotechnol. 2021, 6 (2) 56
Biodiversity was the highest (57%; 16 documents) aspects on bivalve research available in eastern Malaysia ,
followed by reproduction aspect, morphology and natural history and taxonomy (11%; 3 documents each), and
rest of the aspects found less than 5% (1 document), including aquaculture, natural history and taxonomy,
nutrition, morphology, and pollution (Figure 4).
Figure 4. Research aspects on bivalve fauna in Eastern Malaysia (BIOCE=Biodiversity, conservation and
ecology; AQUA = Aquaculture; NHT= Natural History and Taxonomy; REP= Reproduction; NUT=
Nutrition; MOR= Morphology; and POLL=Pollution).
The trend analysis of previously accumulated data indicated that, if current research trends continue, a
significant increase in research publication will occur in the year 2031 (exponential growth), and the number of
publications will continue to grow rapidly thereafter, possibly exceeding previous decades' levels (Figure 5). It
is always hoped, however, that the number of publications will increase in the coming decades. The current
decade demonstrates a rapid exponential growth. Therefore, more academic involvement including existing
universities in east Malaysia will definitely increase the number of research documents and aspects on bivalve
research.
Figure 5. Projections of bivalve research using currently available data and publications (linear vs.
exponential growth).
16
1
3
3
1
3
1
BIOCE AQUA NHT REP NUT MOR POLL
0
0.5
1
1.5
2
2.5
3
3.5
4
4.5
1791
1909
1989
2003
2007
2010
2011
2012
2014
2015
2016
2017
2018
2019
2020
2021
2022
2023
2024
2025
2026
2027
2028
2029
2030
2031
2032
2033
2034
2035
2036
2037
2038
2039
2040
Projection
of
bivalve
research
Years
Asian Australas. J. Biosci. Biotechnol. 2021, 6 (2) 57
The first authorship of a published document is significant, and the majority of available published documents
were first authored at Universiti Putra Malaysia Bintulu Campus (UPMKB) (46%; 13 documents), followed by
Universiti Malaysia Sarawak (UNIMAS) (14%; 4 documents), and Universiti Malaysia Sabah (UMS),
University of Nottingham (UN) and Others (OT) (7%; 2 documents); while the remaining affiliated first authors
contributed 4% each (1 documents) (Figure 6).
Figure 6. Number of published documents based on institutions of first author. (UPMKB= Universiti
Putra Malaysia Bintulu Campus; UN= University of Nottingham; IUCN= International Union for
Conservation of Nature; NBC= Naturalis Biodiversity Center; UMS= Universiti Malaysia Sabah;
UNIMAS= Universiti Malaysia Sarawak; UPM= Universiti Putra Malaysia, Serdang; AU= Aarhus
University; HU=Harvard University; OT=Others).
5. Conclusions
The trends and different aspects of bivalve research are discussed throughout the review. The findings and
discussions of the current review will give a quick insight of 230 years of bivalve research in eastern Malaysia.
The present investigation also discussed the future trends of publication in upcoming two decades. The number
of the bivalve research and aspects are increasing in eastern Malaysia, which can be considered as the positive
changes in the different stakeholders.
Acknowledgements
The research team would like to acknowledge the Ministry of Higher Education Malaysia FRGS research grant
code, FRGS/1/2018/WAB13/UPM/02/2 and department of Animal Science and Fishery, Universiti Putra
Malaysia Bintulu Sarawak campus for the facilities and supports during the study.
Conflicts of interest
None to declare.
Authors’ contribution
Conceptualization: Abdulla-Al-Asif and Hadi Hamli; methodology: Abdulla-Al-Asif; data collection: Abdulla-
Al-Asif; validation: Abdulla-Al-Asif; data curation: Abdulla-Al-Asif; statistics and presentation: Abdulla-Al-
Asif; writing—original draft preparation: Abdulla-Al-Asif and Hadi Hamli; writing—review and editing:
Abdulla-Al-Asif and Hadi Hamli; visualization, Abdulla-Al-Asif; supervision: Hadi Hamli; project
administration: Abdulla-Al-Asif and Hadi Hamli; funding acquisition: Hadi Hamli, all authors have read and
agreed to the published version of the manuscript.
UPMKB
46%
UN
7%
IUCN
3%
NBC
4%
UMS
7%
UNIMAS
14%
UPM
4%
AU
4%
HU
4%
OT
7%
Asian Australas. J. Biosci. Biotechnol. 2021, 6 (2) 58
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Trends of bivalve (Bivalvia) research in East Malaysia: a systematic review

  • 1. Asian Australas. J. Biosci. Biotechnol. 2021, 6 (2), 50-59; doi: 10.3329/aajbb.v6i2.56140 Asian-Australasian Journal of Bioscience and Biotechnology ISSN 2414-1283 (Print) 2414-6293 (Online) www.ebupress.com/journal/aajbb Review Trends of bivalve (Bivalvia) research in East Malaysia: a systematic review Hadi Hamli and Abdulla-Al-Asif* Department of Animal Science and Fishery, Faculty of Agricultural Science and Forestry, Universiti Putra Malaysia Campus Bintulu, 97008 Bintulu, Sarawak, Malaysia *Corresponding author: Abdulla-Al-Asif, Department of Animal Science and Fishery, Faculty of Agricultural Science and Forestry, Universiti Putra Malaysia Campus Bintulu, 97008 Bintulu, Sarawak, Malaysia. E-mail: jessoreboyhemel@gmail.com Received: 03 July 2021/Accepted: 25 August 2021/ Published: 31 August 2021 Abstract: The unique biodiversity in Malaysia makes this country a global hotspot for different aspects of research. Many European and non-native research activities are conducting by different research groups, whereas local institutions also collaborate with them to explore the pristine nature of west (peninsular Malaysia) and East Malaysia (Sarawak and Sabah province). East Malaysia is located in Borneo Island, and the biodiversity of this area are huge. The current review work scrutinized the information about the research activities on aquatic bivalve species and their different aspects of the investigation. This investigation revealed, to date 28 research publications were published on aquatic bivalves from eastern Malaysia, where biodiversity, conservation and ecology was the major aspect of research. The other aspects were aquaculture, natural history and taxonomy, nutritional study, reproduction of bivalve, morphology, and pollution can be mentionable. The major portion of this eastern Malaysia are not investigated and it is assumed that many species are still not reported. Further studies demand to explore the vast bivalve biodiversity of this part of Malaysia. Keywords: Mollusca; Bivalvia; Malaysian Borneo; Sarawak; Sabah 1. Introduction Malaysia is one of the biologically diverse regions on the planet where some fauna have an extremely limited range and are only found in this landmass (Abdullah et al., 2015; Tong, 2020). Eastern part of Malaysia is well known as ―Borneo Island‖, and this huge landmass was formed during the Mesozoic era as a result of the accretion of microcontinental fragments, ophiolite terranes, and Island arc crust onto a Paleozoic continental core (Balaguru et al., 2003). This phenomenon occurred in millions of years ago but it helps to accumulate huge number of unique flora and fauna in this bioregion (Galey et al., 2017; Leonard et al., 2015). The Mollusca fauna were detected unique in nature, especially bivalves; where some of the endemic bivalve species only found in this biogeographic region (Zieritz et al., 2021, 2020). Although the availability of bivalve fauna are ample in eastern Malaysia, which are reported by several European and local research groups (Ashton et al., 2003; Hamli et al., 2012a; Raven, 2019; Zieritz et al., 2020). The history of bivalve research in eastern Malaysia can be phrased as ―one of the oldest‖ compare to the peninsular Malaysia, as the first taxonomic checklist of bivalve was published in 1981 from peninsular Malaysia; while the first bivalve was reported in Eastern Malaysia through the report of Marcia japonica (J. F. Gmelin 1791) from federal territory of Labuan (Gmelin, 1791) while the first research from the present century was recorded from Sematan mangrove forest, Sarawak (Ashton et al., 2003; Morris and Purchon, 1981; Way and Purchon, 1981). The research of Ashton et al. (Ashton et al., 2003) found the first approach to introduce the bivalve fauna from Malaysian Borneo to the rest of the world; it is assumed that, the major focus of Ashton et al. (Ashton et al., 2003) work was to assess the crustaceans and gastropods macro-fauna in Sematan mangrove forest, but very fortunately they reported three species of bivalve. In the last century a noteworthy work was
  • 2. Asian Australas. J. Biosci. Biotechnol. 2021, 6 (2) 51 conducted by Turner and Santhakumaran (1989) from Pantai river, Sarawak and its adjacent areas and recorded four endemic bivalve species. After the initial study, some studies in last decade were also focused on bivalve fauna, targeting heavy metals accumulation by bivalve and biodiversity studies (Abdullah et al., 2007; Shabdin, 2010; Shabdin and Alfred, 2007). The new era of bivalve research in East Malaysia, especially in taxonomic aspect was introduced by Wong and Arshad (Wong and Arshad, 2011), where they reported 18 bivalve species from 12 families from Pulau Mabul, Sabah. The next milestone was settled by Hamli et al. (Hamli et al., 2012a), and they reported 19 species comprising 11 families from different location from Sarawak, Malaysia. Several gastropod studies were also found from eastern Malaysia including description and identification of Pachychilidae (Hadi Hamli et al., 2020), diversity of Caenogastropoda (H. Hamli et al., 2020a), investigation of edible gastropod (Hamli et al., 2013), etc. However, the present focus was only penetrated into the bivalves and research aspects of bivalves in Sarawak and Sabah. It is evident that only few academic and research institutions were found involved in the bivalve research in east Malaysia; where the major portion were contributed by Universiti Putra Malaysia, Bintulu Sarawak campus (13 papers as first author). The other academic institutions such as Universiti Malaysia Sarawak also conducted several studies. The good news is that Eastern Malaysia is abundant in undiscovered and unreported bivalve species; the bad news is that the number of researchers and published documents on various aspects of bivalve fauna were found limited. Considering these potentiality and gaps in research this review aims to compile and analyze various aspects of bivalve research conducted in East Malaysia. This review also provide a glimpses of existing research facilities available in Eastern Malaysia to conduct bivalve research and the institutional framework to support research. 2. Literature search strategy The distribution and abundance records of bivalves in Eastern Malaysia (Sarawak and Sabah) (Figure 1) were accumulated from the existing literature, monographs, reviews, checklists, catalogues, poster, conference paper, conference poster, websites and fishery reports from East Malaysian water from the time periods of 1791 to 2021. The literature search were performed with Google Scholar web search using "Publish or Perish" software (Harzing, 2007) from the time period of March 2019 and September, 2021. The specific key words were inserted and search for the documents [("Malaysia" AND "Borneo") AND ("Bivalvia" OR "Bivalve" OR "Sarawak" OR "Sabah" OR "Marine Bivalve" OR "Freshwater Bivalve" OR "Macrofauna" OR "Marine Mussel" OR "Freshwater Mussel" OR "Mollusk" OR "Freshwater Snails" OR "Marine Snails" "Freshwater Clam" OR "Marine Clam" OR "Macrofauna"]. We extracted the papers related with aquatic Bivalvia in Eastern Malaysia. After extraction of all related published papers we classified the papers into seven research niche, including (a) biodiversity, ecology and conservation, (b) aquaculture, (c) natural history and taxonomy, (d) nutrition, (e) reproduction, (f) morphology, and (g) pollution study. Figure 1. Map showing the places of bivalve research conducted in east Malaysia.
  • 3. Asian Australas. J. Biosci. Biotechnol. 2021, 6 (2) 52 3. Bivalves research aspects 3.1. Biodiversity, ecology and conservation Biodiversity assessment was found one of the major window (57%) in bivalve research in east Malaysia (Figure 4). A total 16 published documents were detected where major portion of the reported bivalve species through this research aspect. The first bivalve biodiversity in eastern Malaysia was reported by Turner and Santhakumaran (1989) from Pantai river, Sarawak; while the next report was tracked in 2003 from Semantan mangrove forest, Sarawak (Ashton et al., 2003). However, a very recent published document from Lawas seagrass beds, Sarawak recorded 18 species of bivalve (Al-Asif et al., 2020). The major biodiversity checklist was reported from all over the Sarawak revealed 19 species of bivalves (11 families) in 2012 (Hamli et al., 2012a) (Table 1). However, from Pulau Mabul, Sabah 18 species of bivalve (12 families) were also reported (Wong and Arshad, 2011). The work of Al-Asif et al. (2020), Hamli et al. (2012a) and Wong and Arshad (2011) were completely reported marine or brackish habitat’s bivalve species; whereas, Zieritz et al. (2020) reported six species of bivalve, Zieritz and Lopes-Lima (2018) reported eight freshwater bivalve species from family Unionidae, over the eastern Malaysia. Most of the biodiversity related published documents were site specific or species/family specific; while the study of Zieritz et al. (2020), Raven (2019), Hamli et al. (2012b), and Hamli et al. (2012a) covers major area of eastern Malaysia; especially Hamli et al. (2012b) and Hamli et al. (2012a) considered the whole Sarawak during sampling. The study of Al-Asif et al. (2021) recorded 76 freshwater, brackish and marine water bivalve species from Malaysian Borneo from 12 orders, 18 superfamilies and 27 families; which was the first complete and comprehensive review of bivalve biodiversity and conservation research from Malaysian Borneo. The study of Al-Asif et al. (2021) also suggested some conservation aspects of bivalve fauna from Malaysian Borneo which might be helpful to protect and in some cases introduce of bivalve fauna to its natural ecosystem in East Malaysia. The study of Zieritz et al. (2021) reported a completely new freshwater genus, Khairuloconcha from Eastern Malaysia having two new species, namely, Khairuloconcha sahanae (Zieritz et al. 2021) and Khairuloconcha lunbawangorum (Zieritz et al. 2021). The study also compared the genetic material with the other species of Unionida which suggested that these species are native to the eastern Malaysia. They suggested the habitat protection, reintroduction of species, captive breeding and legislative framework might helpful to support the sustainability of these newly recorded species. On the other hand, ecological and biodiversity study of Zakirah et al. (2019) from Buntal Bay, Sarawak recorded Tellina sp. with some polycheata species. The bivalve biodiversity in major area of Sarawak and Sabah remains still undiscovered and not reported. Most of the research were conducted from eastern Malaysia at the sites where vehicles and transportations might access; the major part in deep forest and creek areas are still not investigated. This circumstance can be considered as the one of the gap for bivalve research. 3.2. Aquaculture This review finds only one aquaculture related study of Hamli et al. (2020b), and the research team was in a hunt for a potential phytoplankton candidate for live Sinanodonta woodiana bivalve aquaculture. The result of the study found some of the phytoplankton for instance, Selenastrum sp., Licmophora sp. and Gloeocapsa sp. isolated from native pond showed best result during phytoplankton culture and the study recommended to use of these phytoplankton for bivalve aquaculture, as bivalves are phytoplankton feeder. In a recent publication Hamli et al. (2019) discussed the potentiality of local bivalve as the potential candidate of aquaculture. It is assumed that, this wing of bivalve research is going to expand in the east Malaysia in next few decades. 3.3. Natural history and taxonomy The first report of bivalve species was declared by the research of Gmelin (1791) from federal territory of Labuan (a small island near Sarawak coast and Malaysian Borneo) with the report of Marcia japonica (J. F. Gmelin 1791) (reported as Venus japonica Gmelin, 1791). While with in next one hundred years there were no bivalve study was tracked in Malaysian Borneo, and in 1909 Sowerby (1909) reported Pelecyora exilium (G. B. Sowerby III, 1909) (reported as Dosinia exilium) from the coast of Sarawak. The publication of Raven (2019) supports some of the animal dispersal theories presumed previously that some Mollusca species (reported five bivalve species in total) move and settled one place to another in the north-west Borneo. He argued that, nipa rafts (Nypa fruticans) might be one of the possible transportation material during the Cenozoic periods. The dispersal and transportation history of animals are different from bivalve; as these creatures are slow mover and they can spend their whole life where they born. The study of Raven (2019)
  • 4. Asian Australas. J. Biosci. Biotechnol. 2021, 6 (2) 53 provided evidence that, bivalve species for example, Neotrapezium sublaevigatum from family Trapezidae, Magallana rivularis from family Ostreidae might live on the leaf of nipa tree and use it as the dispersal medium from one place to another. 3.4. Nutrition The present review found nutritional study of Meretrix lyrata bivalve was solely based on the organ specific mineral contents (Idris et al., 2017a). The study revealed that, minerals such as, Na and Fe found in high concentration in the tissues compared to other minerals. The result of Idris et al. (2017a) supports that, being a marine or brackish habitat species M. lyrata accumulate the elements Na and Fe in high amount and stores them in their tissue. From this study, it is also revealed that, bivalves can be used as the highly nutritional food items. 3.5. Reproduction The first reproductive study on bivalve reproduction cycle was conducted by Hamli et al. (2015a); they revealed that, histological analysis might be helpful for sex identification of Meretrix lyrata; while some of report suggested that the gender identification of M. lyrata found almost near to impossible (Camacho-Mondragón et al., 2012). However, the study of Hamli et al. (2015a) provided the first insight of the maturation, spawning stage and season of the species in eastern Malaysia. Which might opened a window for the wild bivalve collectors and policy making organization to impose ban on the particular time of the year. The investigation of Hamli et al. (2017) introduced condition index (CI) to measure, either the female bivalve M. lyrata individual is ready to spawn or not. The high CI referred, comparatively high body weight, and the individual is close to maturity stage and early spawning stage, which found directly connected with the breeding seasons. This study also establish relations between the CI and water quality parameters especially ammonia nitrogen might be the influential factors with the condition index. Its due to M. lyrata is a benthic animal and decomposition materials might harmful for the growth and maturity of this species. In another reproductive investigation revealed that gonadal development of Polymesoda expansa and generate information on spawning and breeding season of the bivalve species (Idris et al., 2017b). 3.6. Morphology Morphometric keys were used by Hamli et al. (2015b) in different shell parameters to identify and differentiate three mangrove calm species namely, Polymesda erosa, P. bengalensis and P. expansa from family Corbiculidae. The evidence and statistical analysis proved that, features for instance, standard length, ligament length, ventral posterior margin length, etc. were the key identification parameters to separate these three species. The other study of Hamli et al. (2016) investigated inner shell features of mangrove clam Meretrix lyrata, M. meretrix and M. lusoria and revealed that, the proportional ration standard length for shell wide, ligament length, anterior length, length of cardinal tooth, adductor scar width scar, posterior adductor scar width scar, and pallial sinus open scar might be the main morphological features to differentiate these Meretrix sp. from Sarawak. A recent study of Idris et al. (2021) revealed 20 bivalve species from 12 families, while suggested ventral posterior margin length/ distance from the anterior margin to posterior margin and the length from anterior cardinal tooth to posterior cardinal tooth/ distance from the anterior margin to posterior margin features might be helpful to identification and differentiate between Geloina species. 3.7. Pollution So far, one investigation was conducted to assess the impact of heavy metal such as, Cd, Cu, Cr, Pb and Zn on Meretrix meretrix in two different estuaries in Sabah (Abdullah et al., 2007). This study suggested that, human intervened estuary with high industrial effluent disposal might force M. meretrix to accumulate the toxic heavy metals, in their tissue. This study was an eye opening findings in Malaysian estuary; and the study might helpful to assess the pollution in Malaysian estuary, where bivalve can be used as bio indicator (Table 1).
  • 5. Table 1. Research aspects on bivalve in eastern Malaysia. Year Habitat Location Number of species reported Number of family Research Aspect Sources 2021 Marine and Fresh water Malaysian Borneo 76 27 Biodiversity and conservation Al-Asif et al. (2021) 2021 Freshwater Borneo (Sarawak and Sabah) 5 1 Biodiversity, Multidimensional Zieritz et al. (2021) 2021 Marine, Brackish and Fresh water Sarawak 21 12 Morphology Idris et al. (2021) 2020 Marine Lawas, Sarawak 18 9 Biodiversity Al-Asif et al. (2020) 2020 Freshwater UPM Bintulu, Sarawak 1 1 Aquaculture Hamli et al. (2020b) 2020 Freshwater East Malaysia (Sabah and Sarawak) 6 1 Biodiversity Zieritz et al. (2020) 2019 Marine Buntal Bay, Sarawak 1 1 Ecology Zakirah et al. (2019) 2019 Brackish North-West Borneo, Sarawak 5 4 Natural History Raven, (2019) 2018 Freshwater East Malaysia (Sabah and Sarawak) 8 1 Biodiversity Zieritz and Lopes-Lima, (2018) 2017 Marine Kuching, Sarawak 1 1 Reproduction Hamli et al. (2017) 2017 Marine Kuching, Sarawak 1 1 Nutrition Idris et al. (2017a) 2017 Marine Miri, Sarawak 1 1 Reproduction Idris et al. (2017b) 2017 Marine Marudu Bay, Sabah 7 6 Biodiversity Matsumoto et al. (2017) 2016 Brackish Miri, Sarawak 2 2 Biodiversity Abu Hena et al. (2016) 2016 Marine Kuching, Sarawak 3 1 Morphology Hamli et al. (2016) 2015 Marine Over Sarawak 3 1 Morphology Hamli et al. (2015b) 2015 Marine Kuching, Sarawak 1 1 Reproduction Hamli et al. (2015a) 2014 Marine Kuching, Sarawak 5 3 Biodiversity Shabdin et al. (2014) 2012 Marine and Fresh water Over Sarawak 14 8 Biodiversity Hamli et al. (2012b) 2012 Marine and Fresh water Over Sarawak 19 11 Biodiversity Hamli et al. (2012a) 2011 Marine Sabah 18 12 Biodiversity Wong and Arshad (2011) 2010 Brackish Rajang River, Sarawak 3 3 Biodiversity Shabdin (2010) 2007 Marine and Fresh water Sarawak 4 3 Biodiversity Shabdin and Alfred ( 2007) 2007 Marine Sabah 1 1 Pollution Abdullah et al. (2007) 2003 Marine Kuching, Sarawak 3 3 Biodiversity Ashton et al. (2003) 1989 Marine, Brackish and Fresh water Pantai river, Sarawak 6 1 Biodiversity Turner and Santhakumaran (1989) 1909 Marine Sarawak 1 1 Natural History Sowerby (1909) 1791 Marine Federal Territory of Labuan 1 1 Natural History Gmelin (1791) Asian Australas. J. Biosci. Biotechnol. 2021, 6 (2) 54
  • 6. Asian Australas. J. Biosci. Biotechnol. 2021, 6 (2) 55 4. Research trends The extracted data analysis from publish or perish software revealed that, the first study on bivalve research in this century was conducted in eastern Malaysia in 1989 from Pantai river, Sarawak (Turner and Santhakumaran, 1989) and Semantan mangrove forest, Sarawak (Ashton et al., 2003). While the first record was tracked back in 1791 by the report of Marcia japonica (J. F. Gmelin 1791) Gmelin, (1791). With a gap of three years the second research was published in 2007 (Abdullah et al., 2007; Shabdin and Alfred, 2007). It was also observed that, since 2014, the bivalve research related publications were very frequent. The trend analysis revealed that, number of publications are increasing now a days (Figure 2). Figure 2. Year wise available published documents on bivalve fauna in Eastern Malaysia. The available publications were checked with Scopus database and found 54% (15 documents) of the documents were indexed in the Scopus database; where as 46% (13 documents) of the documents were not indexed in Scopus database (Figure 3). The analysis also suggested that, most of recent year publications were indexed in Scopus database, which referring the number of good quality publications and researchers are increasing in this fields. It is also mentionable here that, the publication of the non-Scopus indexed journals are local but peer reviewed, so the quality of the publications rather not to be questioned. It was found two report materials (Matsumoto et al., 2017; Zieritz and Lopes-Lima, 2018) published by Universiti Malaysia Sabah (UMS) and International Union for Conservation of Nature (IUCN), whereas one conference material (poster) (Abu Hena et al., 2016) was included in the present review, from International Biology Symposium 2016, organized by Universiti Putra Malaysia. Although these three documents were not indexed in Scopus but they were approved by either Universiti experts, IUCN expert groups or conference authority. Figure 3. Sources of available published documents on bivalve fauna in Eastern Malaysia. 1 1 1 1 2 1 1 2 1 2 2 4 1 2 3 3 0 0.5 1 1.5 2 2.5 3 3.5 4 4.5 1791 1909 1989 2003 2007 2010 2011 2012 2014 2015 2016 2017 2018 2019 2020 2021 Numbers of published papers Years Scopus Source 54% Non-Scopus Source 46%
  • 7. Asian Australas. J. Biosci. Biotechnol. 2021, 6 (2) 56 Biodiversity was the highest (57%; 16 documents) aspects on bivalve research available in eastern Malaysia , followed by reproduction aspect, morphology and natural history and taxonomy (11%; 3 documents each), and rest of the aspects found less than 5% (1 document), including aquaculture, natural history and taxonomy, nutrition, morphology, and pollution (Figure 4). Figure 4. Research aspects on bivalve fauna in Eastern Malaysia (BIOCE=Biodiversity, conservation and ecology; AQUA = Aquaculture; NHT= Natural History and Taxonomy; REP= Reproduction; NUT= Nutrition; MOR= Morphology; and POLL=Pollution). The trend analysis of previously accumulated data indicated that, if current research trends continue, a significant increase in research publication will occur in the year 2031 (exponential growth), and the number of publications will continue to grow rapidly thereafter, possibly exceeding previous decades' levels (Figure 5). It is always hoped, however, that the number of publications will increase in the coming decades. The current decade demonstrates a rapid exponential growth. Therefore, more academic involvement including existing universities in east Malaysia will definitely increase the number of research documents and aspects on bivalve research. Figure 5. Projections of bivalve research using currently available data and publications (linear vs. exponential growth). 16 1 3 3 1 3 1 BIOCE AQUA NHT REP NUT MOR POLL 0 0.5 1 1.5 2 2.5 3 3.5 4 4.5 1791 1909 1989 2003 2007 2010 2011 2012 2014 2015 2016 2017 2018 2019 2020 2021 2022 2023 2024 2025 2026 2027 2028 2029 2030 2031 2032 2033 2034 2035 2036 2037 2038 2039 2040 Projection of bivalve research Years
  • 8. Asian Australas. J. Biosci. Biotechnol. 2021, 6 (2) 57 The first authorship of a published document is significant, and the majority of available published documents were first authored at Universiti Putra Malaysia Bintulu Campus (UPMKB) (46%; 13 documents), followed by Universiti Malaysia Sarawak (UNIMAS) (14%; 4 documents), and Universiti Malaysia Sabah (UMS), University of Nottingham (UN) and Others (OT) (7%; 2 documents); while the remaining affiliated first authors contributed 4% each (1 documents) (Figure 6). Figure 6. Number of published documents based on institutions of first author. (UPMKB= Universiti Putra Malaysia Bintulu Campus; UN= University of Nottingham; IUCN= International Union for Conservation of Nature; NBC= Naturalis Biodiversity Center; UMS= Universiti Malaysia Sabah; UNIMAS= Universiti Malaysia Sarawak; UPM= Universiti Putra Malaysia, Serdang; AU= Aarhus University; HU=Harvard University; OT=Others). 5. Conclusions The trends and different aspects of bivalve research are discussed throughout the review. The findings and discussions of the current review will give a quick insight of 230 years of bivalve research in eastern Malaysia. The present investigation also discussed the future trends of publication in upcoming two decades. The number of the bivalve research and aspects are increasing in eastern Malaysia, which can be considered as the positive changes in the different stakeholders. Acknowledgements The research team would like to acknowledge the Ministry of Higher Education Malaysia FRGS research grant code, FRGS/1/2018/WAB13/UPM/02/2 and department of Animal Science and Fishery, Universiti Putra Malaysia Bintulu Sarawak campus for the facilities and supports during the study. Conflicts of interest None to declare. Authors’ contribution Conceptualization: Abdulla-Al-Asif and Hadi Hamli; methodology: Abdulla-Al-Asif; data collection: Abdulla- Al-Asif; validation: Abdulla-Al-Asif; data curation: Abdulla-Al-Asif; statistics and presentation: Abdulla-Al- Asif; writing—original draft preparation: Abdulla-Al-Asif and Hadi Hamli; writing—review and editing: Abdulla-Al-Asif and Hadi Hamli; visualization, Abdulla-Al-Asif; supervision: Hadi Hamli; project administration: Abdulla-Al-Asif and Hadi Hamli; funding acquisition: Hadi Hamli, all authors have read and agreed to the published version of the manuscript. UPMKB 46% UN 7% IUCN 3% NBC 4% UMS 7% UNIMAS 14% UPM 4% AU 4% HU 4% OT 7%
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