Biodiversity of gastropoda in the coastal waters

of Ambon Island, Indonesia

Dominggus Rumahlatu, Fredy Leiwakabessy

Biology Education Study Program, Faculty of Teacher Training and Education Science,
Pattimura University, Ambon, Indonesia. Corresponding author: D. Rumahlatu,
[email protected]

Abstract. Gastropods belonging to the mollusk phylum are widespread in various ecosystems.
Ecologically, the spread of gastropoda is influenced by environmental factors, such as temperature,
salinity, pH and dissolved oxygen. This research was conducted to determine the correlation between the
factors of physico-chemical environment and the diversity of gastropoda in coastal water of Ambon
Island, Indonesia. This research was conducted at two research stations, namely Station 1 at Ujung
Tanjung Latuhalat Beach and Station 2 at coastal water of Waitatiri Passo. The results of a survey
revealed that the average temperature on station 1 was 31.14°C while the average temperature of
station 2 was 29.90° C. The average salinity at Station 1 was 32.02%o whereas the salinity average at
Station 2 was 30.31%o. The average pH in station 1 and 2 was 7.03, while the dissolved oxygen at
station 1 was 7.68 ppm which was not far different from that in station 2 with the dissolved oxygen of
7.63 ppm. The total number of species found in both research stations was 65 species, with the types of
gastropoda were found scattered in 48 genera, 19 families and 7 orders. The most commonly found
gastropods were from the genus of Nerita and Conus. 40 species were found in station 1 and 40 species
were found in station 2. The results of the analysis showed the diversity value was very high with the
diversity average of gastropoda in station 1 as much as 3.64 and in station 2 as much as 3.60 and
classified into moderate category. In addition, the results of the correlation analysis showed that there
was a significantly positive correlation between physical-chemical environmental factors (temperature,
salinity, pH and dissolved oxygen) and the diversity of gastropoda in Coastal Waters of Ambon Island.
Key Words: coastal area, diversity, gastropods, environmental factors, physio-chemical parameters.

Introduction. Gastropods belonging to the phylum of mollusks have the largest species
reaching 100.000 species and spreading in almost all continents (Ruppert et al 2004;
Strong et al 2008). Gastropoda can be found abundantly in sea water ecosystems,
freshwater or estuary area (Galan et al 2015; Gregoric & de Lucia 2016; Miloslavich et al
2013; Maia & Countinho 2013; Ruppert et al 2004) and classified as detritus feeder (Liu
et al 2014). The main characteristic of this organism is having a single shell, threaded,
having a well developed head and equipped with tentacle, and having eyes and radula
(Pyron & Brown 2016). In marine ecosystem, gastropoda can be found in the intertidal
zone (O'Dwyer et al 2014) as well as in the deep sea (Ramirez-Llodra & Olabarria 2005;
Braga-Henriques et al 2011). Asserted by Rahmawati et al (2015) that gastropoda are
scattered on sandy clay sediments with high content of organic C. However, Ríos-Jara et
al (2001) states that most of the mollusks which have important economic value are
distributed in coastal waters.
Although it can found in a variety of habitats, the spread of gastropoda is highly
correlated with the condition of the place of the living organisms, or instance the factors
of physics, chemistry, and biology such as the texture of the sediment, temperature,
salinity, pH, organic matter content and oxygen (Pyron & Brown 2016). The
environmental factor is classified as the major factor that supports the life of gastropoda
because of the low migration capabilities. Sharma et al (2013) reported that the physical
and chemical conditions of the waters showed a significant effect on the diversity of the
gastropoda in Indian waters. Garg et al (2009) examined the environmental factors of
electrical conductivity, pH, alkalinity, phosphate, sodium and potassium on the diversity
of gastropoda in India. Sahin (2012) examines the environmental factors such as,
dissolved oxygen (DO), temperature, NO2-N and NO3–N, and its relation to the
AACL Bioflux, 2017, Volume 10, Issue 2.
http://www.bioflux.com.ro/aacl
285
distribution of gastropoda in Turkey. Salam & Nasar (2012) also examined the
environmental factors such as temperature, pH, TDS, TSS, DO and BOD and its
relationship with the diversity of gastropoda in Iraq. Similarly, Blanco & Cantera (1999)
analyzed the environmental factors, such as DO, temperature, and pH which affected the
vertical distribution of gastropods mangrove forests in Colombia. The results of these
studies generally found that the diversity of gastropoda was influenced by environmental
factors.
Some of the environmental factors that affect the distribution of gastropoda are
temperature, salinity, pH and DO. Increased industrial activity has an impact on the
increasing levels of CO2 nearly 40% of the total of carbon dioxide in atmosphere.
Increased level of CO2 causes the seawater to become more acidic, increases the
temperature, hypoxia or decreased DO in below the threshold tolerance as well as
changes in salinity (Parker et al 2013). Llovel & Terray (2016) found that the water
temperature continues to increase rapidly from year 2005 until year 2014. The increased
water temperature is caused by the imbalance of energy in the atmosphere, so that it is
accommodated in the sea (Abraham et al 2013). The changes in physico-chemical factors
of the water will greatly affect the biological system of aquatic organisms, especially
gastropoda. Gastropoda are known to only survive and adapt in a narrow temperature
tolerance (Harley et al 2009) and lead to stress beyond the optimal temperature range,
thus causing metabolic malfunctions (Nguyen et al 2012). Gastropoda which are Phylum
of mollusks are also vulnerable to ocean acidification because the calcium carbonate shell
clams erodes when exposed to low pH (Parker et al 2013) and excessive hydrogen ions in
the ocean could interfere the formation of the shell (Orr et al 2005). Mollusks tend to
have lower metabolic rates and cannot easily compensate the interference of pH
(Wittmann & Pörtner 2013). Condition of chronic stress of sub-optimal conditions can
result in decreased growth and reproduction, increased susceptibility to disease and
decreased survival rate (Hooper et al 2014; Kroeker et al 2013; Byrne & Przeslawski
2013). The latest analysis has identified mollusk as one of the invertebrate taxa which
are the most vulnerable in the changing ocean conditions (Wittmann & Pörtner 2013;
Kroeker et al 2013).
Moluccas sea waters are classified as large bodies of water as well as having
abundant resources. One of the abundant resources is gastropoda. Gastropoda in the
waters of Moluccas are abundant with uniform distribution pattern. This is because the
condition of the waters of Moluccas is classified as good for the life of the organism.
However, the problem that commonly happens is the fluctuated water temperature due
to climate change. The average temperature on the island of Ambon, Moluccas Islands
(Indonesia) is 27.1°C with temperature variation of diurnal range of 5.8°C. The highest
average temperature occurred in January and the lowest temperature occurred in June,
respectively 28°C and 26°C (78.8°F) with a fluctuation range of 2°C between the months
(ClimaTemps.com 2015). The monthly temperature fluctuations of less than 5°C indicate
that the Ambon areas are categorized as hyperoceanic type, subtype extremely
hyperoceanic (Kottek et al 2006). In addition, water climate changes, like the rainy
season, will cause fluctuations in water quality, namely salinity, pH, and DO in the water.
The precipitation average on the island of Ambon, Moluccas Islands (Indonesia) reaches
3,459 mm/year or 288.3 mm/month. The period of precipitation 181 days/year with the
precipitation levels of more than 0.1 mm, where the highest precipitation occurs in
November (638 mm) and the lowest occurs in June (114 mm). Department of
Meteorology Climatology and Geophysics (2016) indicated that the Ambon area was
categorized as medium rainfall (precipitation) areas (100-300 mm) until the beginning of
January 2017. Precipitation causes agitation in the water column, so that it may cause
upwelling that can cause the availability of dissolved oxygen becomes less.
Based on the description above, this research is important to be conducted in order
to assess the diversity of gastropods and its correlation with environmental factors
(temperature, salinity, pH, and oxygen) in coastal waters of the island of Ambon.

Material and Method. This research was conducted in July and December 2016 at two
stations of coastal waters of the island of Ambon, namely in the coastal waters of

AACL Bioflux, 2017, Volume 10, Issue 2.

http://www.bioflux.com.ro/aacl
286
Waitatiri in Passo village (station 1) and in the waters of Ujung Tanjong in Latuhalat
village (station 2) (Figure 1). The data were collected by using sampling technique to
measure the environmental factors (temperature, salinity, pH, and DO in sea water) and
the enumeration of the types of gastropods with in-situ.
The data collection was done during the lowest tide, beginning with determining the
area of sampling, and after that making the vertical line transect from the limit of the
highest tides as many as 10 transect lines (toward the ocean) with the distance between
transect lines 50 m. 10 plots with a size of 1x1 m were made on each transect with the
distance between the plots 10 m, so that there were 100 plots for each station of data
collection.

Figure 1. Map of research location (Note: - station 1, - station 2).

The measurement of the environmental factors (temperature, salinity, pH and DO) was
done on each plot for 10 transect lines. The tools for measuring temperature, salinity,
pH, and DO of sea water were thermometer, refragtometer, pH meter, and the DO meter
respectively. The data collection for the types of gastropods was done by enumeration
and taking pictures of each type of gastropods in the research locations. After that, each
type of gastropods was identified using the identification books by Sabelli (1979).
The calculation of the diversity index of gastropoda was done descriptively by using
the Shannon-Wiener formula, as follows:

Η’ = − ∑ Pi ln Pi
(Ludwig & Reynolds 1988)
Where: Pi = ni/N;
Η’ - Shannon–Wiener diversity;
ni - total individuals species-I;
N - total number of individuals of all species, with the criteria of diversity, namely
low (H<2) moderate (2<H<4), and high (H>4).
To examine the correlation between the environmental factors and the diversity of
gastropoda, the available data were analyzed using multiple linear regression analysis.

AACL Bioflux, 2017, Volume 10, Issue 2.

http://www.bioflux.com.ro/aacl
287
 Results and Discussion

Conditions of the physio-chemical environmental factors in the research

ocation. The results of the measurement of physico-chemical environmental factors
(Table 1) in both research stations showed that the average temperature in station 1 was
31.14°C while the average temperature of station 2 was 29.90oC. The average salinity in
station 1 was 32.02‰, while the average salinity in station 2 was 30.31‰. The average
pH in station 1 and 2 was 7.03 while the DO at Station 1 was 7.68 ppm which was not far
different from that at Station 2 with 7.63 ppm. These results showed that the physical-
chemical water factors in both stations were not much different.

Table 1
Condition of physio-chemical environmental factors in the research location

Average values for the environmental factors

Station 1 Station 2
Transect
Temp. Salinity DO Temp. Salinity DO
pH pH
(C) (‰) (ppm) (C) (‰) (ppm)
1 31.15±0.03 32.01±0.03 7.04±0.01 7.69±0.01 30.01±0.01 30.10±0.01 7.02±0.01 7.62±0.02
2 31.11±0.01 32.01±0.03 7.04±0.01 7.68±0.02 29.97±0.02 30.31±0.02 7.03±0.01 7.62±0.04
3 31.16±0.04 32.02±0.02 7.04±0.01 7.7±0.01 29.89±0.01 30.34±0.01 7.02±0.03 7.62±0.04
4 31.14±0.02 32.02±0.02 7.03±0.02 7.68±0.02 29.87±0.04 30.33±0.01 7.02±0.02 7.63±0.01
5 31.12±0.01 32.02±0.02 7.03±0.02 7.68±0.02 29.87±0.02 30.34±0.01 7.03±0.03 7.62±0.01
6 31.18±0.05 32.03±0.01 7.03±0.02 7.68±0.02 29.87±0.03 30.34±0.01 7.02±0.03 7.63±0.01
7 31.16±0.04 32.02±0.02 7.04±0.01 7.7±0.01 29.88±0.03 30.34±0.02 7.03±0.02 7.63±0.02
8 31.13±0.01 32.01±0.03 7.05±0.01 7.7±0.01 29.87±0.03 30.34±0.03 7.03±0.03 7.62±004
9 31.15±0.03 32.02±0.02 7.04±0.01 7.7±0.01 29.86±0.03 30.33±0.01 7.02±0.04 7.62±0.04
10 31.12±0.01 32.02±0.02 7.03±0.02 7.58±0.09 29.87±0.03 30.33±0.04 7.02±0.04 7.61±0.02
Average 31.14 32.02 7.03 7.68 29.90 30.31 7.03 7.63
Station 1: The Coastal Waters of Ujung Tanjong Latuhalat village, Station 2: The Coastal Waters of Waitatiri
Passo village.

Types of gastropoda collected. The results of the identification of the types of

gastropoda on both stations showed that the number of species found in both the
research station was about 40 species. There was a difference in the species found in
station 1 and those found in station 2. Thus, the total number of the species found in
both stations was 65 species (Table 2). This means that there were some species found
in station 1, but they were not found in station 2, and vice versa.
The types of gastropoda found in both research stations were then grouped into
the order of taxa (Table 3). The types of gastropods found were spread in 48 genera, 18
families and 6 orders. The most commonly type of gastropods was from the genus of
Nerita and Conus.

AACL Bioflux, 2017, Volume 10, Issue 2.

http://www.bioflux.com.ro/aacl
288
 Table 2
Types of gastropods obtained in the location of the data collection

Location
No Species
Station 1 Station 2
1 Naria boivinii - +
2 Monetaria annulus + +
3 Monetaria moneta + +
4 Monetaria caputserpentis + +
5 Lyncina lynx + +
6 Lyncina leviathan + -
7 Erronea caurica + +
8 Erronea xanthodon + -
9 Conus ebraeus - +
10 Dauciconus jorioi + -
11 Tenorioconus mappa jesusramirezi + -
12 Leporiconus glans + -
13 Magelliconus mgelliconus hilli (var.) + +
14 Tesselliconus eburneus crassus + -
15 Fulgiconus marielae + +
16 Calibanus furvus granifer (var.) - +
17 Stomatella monteiroi - +
18 Trochus rotus - +
19 Chlorodiloma crinita + +
20 Clanculus scotti - +
21 Turbo articulatus + -
22 Tectus fenestratus + -
23 Astralium stellar + -
24 Imbricaria olivaeformis - +
25 Mitra paupercula + +
26 Acanthina unicornis - +
27 Neorapana tuberculata + +
29 Ocinebrina nicolai + +
30 Hexaplex cichoreum - +
31 Pterochelus triformis - +
32 Morula anaxares + +
33 Nerita planospira + +
34 Nerita maxima - +
35 Nerita plicata + -
36 Nerita semirugosa + -
37 Nerita quadricolor + -
38 Neritina chrysocolla + -
39 Nerita fragum + -
40 Clithon faba + -
41 Clithon squarrosa - +
42 Clithon subrugatus - +
43 Microtralia insularis - +
44 Cidarina cidaris - +
45 Angaria delphinus - +
46 Microtralia insularis - +
47 Turritella gemmata - +
48 Turritella attenuate + +
49 Colpospira sinuata - +
50 Volutharpa ampullacea morchiana - +
51 Engina mendicaria + +
52 Pisania tritonoides + +
53 Pisania striata + -

AACL Bioflux, 2017, Volume 10, Issue 2.

http://www.bioflux.com.ro/aacl
289
 Location
No Species
Station 1 Station 2
54 Cantharus cancellaria - +
55 Gemophos tinctus - +
56 Monostiolum nigricostatum - +
57 Afer lansbergisi + -
58 Morus cerith - +
59 Cerithium muscarum + -
60 Oliva reticulata azona (var.) + -
61 Omphalius pfeifferi carpenteri + -
62 Lambis cristinae + -
63 Cymatium (Monoplex) krebsii + -
64 Cranopsis cucullata + -
65 Trumphis distorta + -

Table 3
Composition of Gastropoda taxa found in the location of the data collection

Order Family Genus Species

Naria Naria boivinii
Monetaria annulus
Monetaria Monetaria moneta
Monetaria caputserpentis
Littorinimorpha Cypraeidae
Lyncina lynx
Lyncina
Lyncina leviathan
Erronea caurica
Erronea
Erronea xanthodon
Stomatella Stomatella monteiroi
Trochus Trochus rotus
Chlorodiloma Chlorodiloma crinita
Trochidae
Clanculus Clanculus scotti
Tectus Tectus fenestratus
Astralium Astralium stellar
Calliotropidae Cidarina Cidarina cidaris
Vetigastropoda
Angariidae Angaria Angaria delphinus
Acanthina Acanthina unicornis
Neorapana Neorapana tuberculata
Ocinebrina Ocinebrina nicolai
Muricidae
Hexaplex Hexaplex cichoreum
Pterochelus Pterochelus triformis
Morula Morula anaxares
Nerita planospira
Nerita maxima
Nerita plicata
Nerita
Nerita semirugosa
Nerita quadricolor
Cycloneritimorpha Neritidae
Nerita fragum
Neritina Neritina chrysocolla
Clithon squarrosa
Clithon Clithon subrugatus
Clithon faba
Eupulmonata Ellobiidae Microtralia Microtralia insularis
Turritella gemmata
Turritella
Sorbeoconcha Turritellidae Turritella attenuate
Colpospira Colpospira sinuata

AACL Bioflux, 2017, Volume 10, Issue 2.

http://www.bioflux.com.ro/aacl
290
 Order Family Genus Species
Volutharpa Volutharpa ampullacea morchiana
Engina Engina mendicaria
Pisania tritonoides
Pisania
Pisania striata
Buccinidae
Cantharus Cantharus cancellaria
Gemophos Gemophos tinctus
Monostiolum Monostiolum nigricostatum
Afer Afer lansbergisi
Morus Morus cerith
Cerithiidae
Cerithium Cerithium muscarum
Olividae Oliva Oliva reticulata azona (var.)
Omphalius Omphalius pfeifferi carpenteri
Turbinidae
Turbo Turbo articulatus
Neogastropoda Strombidae Lambis Lambis cristinae
Ranellidae Monoplex Cymatium (Monoplex) krebsii
Fissurelidae Cranopsis Cranopsis cucullata
Pseudolividae Trumphis Trumphis distorta
Imbricaria Imbricaria olivaeformis
Mitridae
Mitra Mitra paupercula
Conus ebraeus
Dauciconus jorioi
Conus
Tenorioconus mappa jesusramirezi
Leporiconus glans
Conidae Tesselliconus Tesselliconus eburneus crassus
Magelliconus magelliconus hilli
Magelliconus
(var.)
Fulgiconus Fulgiconus marielae
Calibanus Calibanus furvus granifer (var.)

The number of species found in both research stations was still more than the results of
the research conducted by David (2013), who found as many as 86 species in 16
sampling locations in India, and Mohanraj et al (2015) who found as many as 40 species
from three different islands in Karsuvar, India. Jumawan et al (2015) found 31 species
belonging to the class of gastropoda on the island of Mindanao, Philippines. This means
that the coastal waters of the island of Ambon have the highest number of species of
gastropods.
The high number of species in both the research stations indicated a high diversity
of gastropods. The average diversity of gastropoda in station 1 was 3.64 and the average
diversity in station 2 was 3.60 (Table 4).
Table 4
Diversity of gastropods

Station 1 Station 2
Transect H’ Transect H’
1 3.66 1 3.60
2 3.66 2 3.61
3 3.66 3 3.61
4 3.65 4 3.61
5 3.62 5 3.59
6 3.64 6 3.60
7 3.64 7 3.62
8 3.64 8 3.60
9 3.64 9 3.60
10 3.64 10 3.58

AACL Bioflux, 2017, Volume 10, Issue 2.

http://www.bioflux.com.ro/aacl
291
Based on the classification by Ludwig & Reynolds (1988), it can be concluded that the
diversity of gastropoda in both research stations was categorized as moderate.
The diversity of gastropoda which is categorized as moderate could mean that
there are variations in the characteristics of gastropoda at all hierarchy of life, ranging
from molecule until ecosystem (Mouchet et al 2010; Morris et al 2014). The diversity of
gastropoda can also explain some aspects of the community structure or ecosystem like
variations of functional character, complexity of food chain, and the number o functional
species in an ecosystem (Mason et al 2005). The analysis of such diversity is beneficial to
determine the environmental conservation policies. Cadotte et al (2011) explains that the
main objective of conservation and restoration is to maintain biological diversity and
ecosystem services provided by this diversity. The advantages of the diversity
measurement are because the information about the species has been included. A high
diversity indicates a variety and density of organisms. Based on those opinions, it can be
concluded that gastropods in the coastal waters of Ambon Island have high variations
and density.

The correlation between physio-chemical factors and the diversity of

gastropoda. The data of physio-chemical environmental factors and the diversity of
gastropoda on both research stations were analyzed using linear regression statistics.
The results of the regression analysis showed that the factors of temperature, salinity
and DO had an effect on the diversity of gastropod in coastal waters of Ambon Island
(Table 5).

Table 5
Results of Linear Regression Analysis

Independent B Standardized Prob

t-test Alpha Note
variables coefficient (sig t)
Temperature 0.928 10.591 0.000 0.05 Significant
Salinity 0.887 8.140 0.000 0.05 Significant
Ph 0.645 3.582 0.002 0.05 Significant
DO 0.824 6.171 0.000 0.05 Significant

The environmental factor that has a significant effect on the diversity of gastropoda is the
water temperature. The results of the statistical analysis showed that there was a
significant positive correlation between the temperature of the sea water and the
diversity of gastropoda. This means that the gastropoda is very fond of aquatic
environments with relatively high temperatures. Sokolova & Portner (2003) explain that
gastropoda in the intertidal zone in tropical areas like water with a temperature of 28-
30°C, but its metabolism may occur between a temperature of 25oC and 40oC. The
results of the present research are consistent with the opinion of Garg et al (2009), who
explains that there are two factors affecting the abundance of gastropods at high water
temperature conditions. These factors are: (1) the number of decomposers is more on
high water temperature so that organic matter and macrofit look at the bottom of the
water; (2) an increase in water temperature will activate the decomposition of organic
matter in the sediment. The results of the research by Matsukura et al (2009) on
freshwater gastropods showed that low temperatures can cause osmotic stress in cells
and cause intracellular damage. A research conducted by Zhang et al (2016) also found
that low temperature (15°C) can affect the digestive, respiratory and excretion of
gastropoda, Nassarius festivus.
Another factor affecting the diversity of gastropoda is salinity. The present research
also found that there was a significant positive correlation between salinity and diversity
of gastropoda. This means that gastropoda prefer high salinity water. Salinity is an
environmental factor that greatly affects the vitality of marine organisms. Therefore, the
stability of the population is determined by the organism ability to withstand the
fluctuations in salinity waters (Javanshir 2013). Koprivnikar & Poulin (2009) explained

AACL Bioflux, 2017, Volume 10, Issue 2.

http://www.bioflux.com.ro/aacl
292
that marine organisms are generally resilient to salinity up to 35 psu or equal to 35 ppm.
The results of this research showed that the average salinity of sea water at Station 1
was 7.68 ppm and the average salinity of station 2 was 7.63 ppm. This means that the
salinity in both research stations was still within the range of tolerance, so that it did not
disturb the physiological activity of gastropoda. A laboratory experience conducted by
Samiei et al (2011) showed that the rate of metabolism of Nassarius deshayesianus
(Issel, 1866) will decline if salinity is increased up to 41 psu. Xiao et al (2014) explains
that salinity is the limiting factor of the distribution of aquatic organisms and its influence
on physiological processes is like hemolymph osmolarity and the water content in tissues
that can lead to death of the organism.
The next environmental factor is pH, which is also known to have an effect on the
distribution of gastropods. The results of this research show that the pH factor has a
correlation with the diversity of gastropoda. The results of the measurement of pH show
that the average pH in station 1 and 2 was at 7.3 and shows a significant effect on the
diversity of gastropoda. Positive correlation means that the higher the pH, the higher the
diversity of gastropoda. Various researches have found that the increased acidity of sea
water over the past decades has influenced a variety of aquatic organisms. Several other
researches have found that acidic water will reduce the thickness of shell and increase
metabolism (hipermetabolism) Bibby et al (2007), disorders of the ability to regulate
haemolymph osmosis and ion concentration (Ewald et al 2009), increase the needs of
energy, so cell size decreases, but the mass of the body increases (Harvey et al 2016).
Another environmental factor is the DO, which is also known to have an effect on
the diversity of gastropoda. The results of this research indicate that there is a significant
correlation between DO and the diversity of gastropods. The results of analysis showing a
positive correlation means that the higher the level of the DO, the higher the diversity of
gastropoda. Ekau et al (2010) explains that oxygen is one of the important elements in
the metabolism of aquatic organisms. An extremely low concentration of DO will lead to
hypoxia, thereby disrupting the various levels of biological systems. At the individual
level, hypoxia can cause physiological changes and disrupt the life cycle, growth capacity,
reproduction ability, and susceptible to disease. At the community level, hypoxia can
cause changes in the density and distribution as well as damages the community
composition by eliminating sensitive species as well as providing opportunities for
tolerant species to grow more (Weisberg et al 2008). The research conducted by McClain
& Rex (2001) found that the level of DO had a significant effect on the body size of
gastropoda that live in the deep sea.

Conclusions. The diversity of gastropods in coastal waters of the island of Ambon

(coastal waters of Waitatiri village and waters of Ujung Tanjong of Latuhalat Village are
categorized as moderate (2<H'<4) with a number of species of gastropoda were found to
be quite high (65 species, 48 genera, 18 families, and 6 orders). The high gastropoda
species found is associated with the environmental factors corresponding to the life of
gastropoda, namely temperature (ranging from 29.90 to 31.4oC), salinity (ranging from
30.31 to 32.02‰), pH (ranging from 7.03 to 7.68), and DO (7.63 to 7.68 ppm). In
addition, based on the analysis of the correlation, it was revealed that there was a
significant positive correlation between physical-chemical environmental factors
(temperature, salinity, pH, and DO) and the diversity of gastropoda in Coastal Waters of
Ambon Island.

Acknowledgments. The authors thank the Dean of the Faculty of Education, University
of Pattimura by the Research Grants for Lecturers fiscal year 2016. We also thank Ayu
Rahaweman who helped for the data collection.

References

Abraham J. P., Baringer M., Bindoff N. L., Boyer T., Cheng L. J., Church J. A., Conroy J.
L., Domingues C. M., Fasullo J. T., Gilson J., Goni G., Good S. A., Gorman J. M.,
Gouretski V., Ishii M., Johnson G. C., Kizu S., Lyman J. M., Macdonald A. M.,

AACL Bioflux, 2017, Volume 10, Issue 2.

http://www.bioflux.com.ro/aacl
293
 Minkowycz W. J., Moffitt S. E., Palmer M. D., Piola A. R., Reseghetti F.,
Schuckmann K., Trenberth K. E., Velicogna I., Willis J. K., 2013 A review of global
ocean temperature observations: implications for ocean heat content estimates and
climate change. Reviews of Geophysics 51:450–483.
Bibby R., Harding P. C., Rundle S., Widdicombe S., Spice J., 2007 Ocean acidification
disrupts induced defences in the intertidal gastropod Littorina littorea. Biology
Letters 3(6):699–701.
Blanco J. F., Cantera J. R., 1999 The vertical distribution of mangrove gastropods and
environmental factors relative to tide level at Buenaventura Bay, Pacific Coast of
Colombia. Bulletin of Marine Science 65(3):617–630.
Braga-Henriques A., Carreiro-Silva M., Porteiro F. M., de Matos V., Sampaio I., Ocana O.,
Avila S. P., 2011 The association between a deep-sea gastropod Pedicularia sicula
(Caenogastropoda: Pediculariidae) and its coral host Errina dabneyi (Hydrozoa:
Stylasteridae) in the Azores. Journal of Marine Science 68(2):399–407.
Byrne M., Przeslawski R., 2013 Multistressor impacts of warming and acidification of the
ocean on marine invertebrates’ life histories. Integrative and Comparative Biology
53(4):582-596.
Cadotte M. W., Carscadden K., Mirotchnick N., 2011 Beyond species: functional diversity
and the maintenance of ecological processes and services. Journal of Applied
Ecology 48:1079–1087.
David A., 2013 Biodiversity and distribution of marine gastropods (Mollusca) during pre-
and post-monsoon seasons along the Goa coastline, India. Journal of the Marine
Biological Association of India 55(1):17-24.
Ewald M. L., Feminella J. W., Lenertz K. K., Henry R. P., 2009 Acute physiological
responses of the freshwater snail Elimia flava (Mollusca: Pleuroceridae) to
environmental pH and calcium. Comparative Biochemistry and Physiology Part C
150:237–245.
Ekau W., Auel H., Pörtner H.-O., Gilbert D., 2010 Impacts of hypoxia on the structure
and processes in pelagic communities (zooplankton, macro-invertebrates and fish).
Biogeosciences 7:1669–1699.
Galan G. L., Ediza M. M., Servasques M. S., Porquis H. C., 2015 Diversity of Gastropods
in the selected rivers and lakes in Bukidnon. International Journal of Environmental
Science and Development 6(8):615-619.
Garg R. K., Rao R. J., Saksena D. N., 2009 Correlation of molluscan diversity with
physicochemical characteristics of water of Ramsagar reservoir, India. International
Journal of Biodiversity and Conservation 1(6):202-207.
Gregoric G., de Lucıa M., 2016 Freshwater gastropods diversity hotspots: three new
species from the Uruguay River (South America). PeerJ 4:e2138; DOI
10.7717/peerj.2138.
Harley C. D., Denny M. W., Mach K. J., Miller L. P., 2009 Thermal stress and
morphological adaptations in limpets. Functional Ecology 23(2):292-301.
Harvey B. P., McKeown N. J., Rastrick S. P. S., Bertolini C., Foggo A., Graham H., Hall-
Spencer J. M., Milazzo M., Shaw P. W., Small D. P., Moore P. J., 2016 Individual and
population-level responses to ocean acidification. Scientific reports 6:20194, DOI:
10.1038/srep20194.
Hooper C., Day R., Slocombe R., Benkendorff K., Handlinger J., Goulias J., 2014 Effects
of severe heat stress on immune function, biochemistry and histopathology in
farmed Australian abalone (hybrid Haliotis laevigata × Haliotis rubra). Aquaculture
432:26-37.
Javanshir A., 2013 How salinity changes in an intertidal zone may affect population
dynamics of Littorina scabra (Linaeus 1758) in northern coasts of Persian Gulf.
Turkish Journal of Fisheries and Aquatic Sciences 13:133-138.
Jumawan J. H., Tripoli F. F. D., Boquia E. E. S., Niez K. L. M., Veronilla J. A. H., Dellomes
S. A., Udtie R. M., Seit N. K., Hasim N. A., Gatinao M. J. O., 2015 Species diversity
and spatial structure of intertidal mollusks in Padada, Davao del Sur, Philippines.
AACL Bioflux 8(3):301-309.

AACL Bioflux, 2017, Volume 10, Issue 2.

http://www.bioflux.com.ro/aacl
294
Koprivnikar J., Poulin R., 2009 Effects of temperature, salinity, and water level on the
emergence of marine cercariae. Parasitology Research 105:957–965.
Kottek M., Rieser J., Beck C., Rudolf B., Rubel F., 2006 World Map of the Köppen-Geiger
climate classification updated. Meteorologische Zeitschrift 15(3):259-263.
Kroeker K. J., Kordas R. L., Crim R., Hendriks I. E., Ramajo L., Singh G. S., Duarte C. M.,
Gattuso J. P., 2013 Impacts of ocean acidification on marine organisms: quantifying
sensitivities and interaction with warming. Global Change Biology 19(6):1884-1896.
Liu W., Tanimura A., Imai T., Kanaya G., Niiyama T., Maegawa S., Kohzu A., Kimura T.,
Toyohara H., 2014 Distribution of gastropods in a tidal flat in association with
digestive enzyme activities. Plankton & Benthos Research 9(3):156–167.
Llovel W., Terray L., 2016 Observed southern upper-ocean warming over 2005–2014 and
associated mechanisms. Environmental Research Letters 11:1-13.
Ludwig J. A., Reynolds J. F., 1988 Statistical ecology: a primer on methods and
computing. John Wiley & Sons, New York, 337 pp.
Maia R. C., Coutinho R., 2013 The influence of mangrove structure on the spatial
distribution of Melampus coffeus (Gastropoda: Ellobiidae) in Brazilian estuaries.
Pan-American Journal of Aquatic Sciences 8(1):21-29.
Mason N. W. H., Mouillot D., Lee W. G., Wilson J. B., 2005 Functional richness, functional
evenness and functional divergence: the primary components of functional
diversity. Oikos 111:112-118.
Matsukura K., Tsumuki H., Izumi Y., Wada T., 2009 Physiological response to low
temperature in the freshwater apple snail, Pomacea canaliculata (Gastropoda:
Ampullariidae). The Journal of Experimental Biology 212:2558-2563.
Mouchet M. A., Villeger S., Mason N. W. H., Mouillot D., 2010 Functional diversity
measures: an overview of their redundancy and their ability to discriminate
community assembly rules. Functional Ecology 24:867–876.
Morris E. K., Caruso T., Buscot F., Fischer M., Hancock C., Maier T. S., Meiners T., Müller
C., Obermaier E., Prati D., Socher S. A., Sonnemann I., Wäschke N. O., Wubet T.,
Wurst S., Rillig M. C., 2014 Choosing and using diversity indices: insights for
ecological applications from the German Biodiversity Exploratories. Ecology and
Evolution 4(18):3514–3524.
McClain C. R., Rex M. A., 2001 The relationship between dissolved oxygen concentration
and maximum size in deep-sea turrid gastropods: an application of quantile
regression. Marine Biology 139:681-685.
Miloslavich P., Cruz-Motta J. J., Klein E., Iken K., Weinberger V., 2013 Large-scale spatial
distribution patterns of gastropod assemblages in rocky shores. PLoS ONE 8(8):1-
13.
Mohanraj J., Chelladurai G., Balakrishnan S., Kuam I. V., 2015 Gulf of Mannar Island
coral reef associated gastropods assemblages: Distribution and diversity pattern.
Journal of Coastal Life Medicine 3(9):691-695.
Nguyen K. D., Morley S. A., Lai C. H., Clark M. S., Tan K. S., Bates A. E., Peck L. S.,
2012 Upper temperature limits of tropical marine ectotherms: global warming
implications. PLoS One 6(12):29-40.
O’Dwyer K., Kamiya T., Poulin R., 2014 Altered microhabitat use and movement of
littorinid gastropods: the effects of parasites. Marine Biology 161:437–445.
Orr J. C., Fabry V. J., Aumont O., Bopp L., Doney S. C., Feely R. A., Gnanadesikan A.,
Gruber N., Ishida A., Joos F., Key R. M., 2005 Anthropogenic ocean acidification
over the twenty-first century and its impact on calcifying organisms. Nature
437(7059):681-686.
Parker L. M., Ross P. M., Connor W. A. O., Portner H. O., Scanes E., Wright J. M., 2013
Predicting the response of molluscs to the impact of ocean acidification. Biology
2:651-692.
Pyron M., Brown K. M., 2015 Introduction to mollusca and the class Gastropoda. Elsevier
Inc Chapter 18. doi: org/10.1016/B978-0-12-385026-3.00018-8.
Rahmawati R., Sarong M. A., Muchlisin Z. A., Sugianto S., 2015 Diversity of gastropods
in mangrove ecosystem of western coast of Aceh Besar District, Indonesia. AACL
Bioflux 8(3):265-271.

AACL Bioflux, 2017, Volume 10, Issue 2.

http://www.bioflux.com.ro/aacl
295
Ramirez-Llodra E., Olabarria C., 2005 Aspects of the distribution, population structure
and reproduction of the gastropod Tibia delicatula (Nevill, 1881) inhabiting the
oxygen minimum zone of the Oman and Pakistan continental margins. Journal of
Sea Research 54:299–306.
Ríos-Jara E., Pérez-Peña M., Beas-Luna R,. López-Uriarte E., Juárez-Carrillo E., 2001
Gastropods and bivalves of commercial interest from the continental shelf of Jalisco
and Colima, México. Revista de Biología Tropical 49(3-4):859-863.
Ruppert E. E., Fox R. S., Barnes R. D., 2004 Invertebrate zoology. Thomson Learning,
Inc, Belmont, California.
Sabelli B., 1979 Simon and Schuster’s guide to shells.Simon & Schuster Inc., New York.
Sahin S. K., 2012 Gastropod species distribution and its relation with some physico-
chemical parameters of the Malatya’s streams (East Anatolia, Turkey). Acta
Zoologica Bulgarica 64(2):129-134.
Samiei J. V., Liñares J. A. N., Abtahi B., 2011 The Antagonistic effect of raised salinity on
the aerobic performance of a rocky intertidal gastropod Nassarius deshayesianus
(Issel, 1866) exposed to raised water temperature. Journal of the Persian Gulf
(Marine Science) 2(6):29-36.
Sharma K. K., Bangotra K., Saini M., 2013 Diversity and distribution of Mollusca in
relation to the physico-chemical profile of Gho-Manhasan stream, Jammu (J & K).
International Journal of Biodiversity and Conservation 5(4):240-249.
Sokolova I. M., Pörtner H. O., 2003 Metabolic plasticity and critical temperatures for
aerobic scope in a eurythermal marine invertebrate (Littorina saxatilis, Gastropoda:
Littorinidae) from different latitudes. The Journal of Experimental Biology 206:195-
207.
Strong E. E., Gargominy O., Ponder W. F., Bouchet P., 2008 Global diversity of
gastropods (Gastropoda; Mollusca) in freshwater. Hydrobiologia 595:149-166.
Weisberg S. B., Thompson B., Ranasinghe J. A., Montagne D. E., Cadien D. B., Dauer D.
M., Diener D., Oliver J. S., Reish D. J., Velarde R. G., Word J. Q., 2008 The level of
agreement among experts applying best professional judgment to assess the
condition of benthic infaunal communities. Ecological Indicators 8:389-394.
Wittmann A. C., Pörtner H. O., 2013 Sensitivities of extant animal taxa to ocean
acidification. Nature Climate Change 3(11):995-1001.
Xiao B. C., Li E., Du Z-Y., Jiang R.-I., Chen L-Q., Yu N., 2014 Effects of temperature and
salinity on metabolic rate of the Asiatic clam Corbicula fluminea (Müller, 1774).
SpringerPlus 3:1-9.
Zhang H., Shin P. K. S., Cheung S. G., 2016 Physiological responses and scope for
growth in a marine scavenging gastropod, Nassarius festivus (Powys, 1835), are
affected by salinity and temperature but not by ocean acidification. Journal of
Marine Science 73(3):814–824.
*** ClimaTemps, 2016 Ambon, Maluku Islands Climate & Temperature. Available at:
www.maluku.climatemps.com/temperatures.php
*** Department of Meteorology Climatology and Geophysics, 2016 The trend of daily
heavy rains number occurrence (rainfall 50 mm/day) at Maluku and Papua. Annual
Report of Department of Meteorology Climatology and Geophysics, Indonesia.

Received: 18 February 2017. Accepted: 21 March 2017. Published online: 24 March 2017.
Authors:
Dominggus Rumahlatu, Pattimura University, Faculty of Teacher Training and Education Science, Biology
Education Study Program, Indonesia, Ambon 97233, Ir. M. Putuhena Street, e-mail:
[email protected]
Fredy Leiwakabessy, Pattimura University, Faculty of Teacher Training and Education Science, Biology Education
Study Program, Indonesia, Ambon 97233, Ir. M. Putuhena Street, e-mail: [email protected]
This is an open-access article distributed under the terms of the Creative Commons Attribution License, which
permits unrestricted use, distribution and reproduction in any medium, provided the original author and source
are credited.
How to cite this article:
Rumahlatu D., Leiwakabessy F., 2017 Biodiversity of gastropoda in the coastal waters of Ambon Island,
Indonesia. AACL Bioflux 10(2):285-296.

AACL Bioflux, 2017, Volume 10, Issue 2.

http://www.bioflux.com.ro/aacl
296