TROPHIC ECOLOGY OF LARVAL AND JUVENILE AMPHIDROMUS
GOBIES (PISCES: GOBIIDAE) IN CIMAJA ESTUARY,
PALABUHANRATU BAY
ARIZONA STATE UNIVERSITY
ABS 370 – ECOLOGY
SPRING 2024
Introduction:
Estuary is a meeting place between two waters that have different characteristics. The
two waters are fresh water from river flow and sea water that enters the estuary through tidal
energy (Indarmawan and Manan 2011). Estuaries are characterized by fertile environmental
conditions and fluctuate with the tidal pattern. The dynamics of these environmental
conditions can affect the survival of biota in the waters. Estuaries have ecological functions to
support various aspects of fish life such as providing spawning habitat, as a food store (Blaber
1997) and a place to nurture various stages in the life stadia of fish (larvae, yuwana and
adults) (Costa et al. 2002). In addition, estuaries are habitats with high biota diversity, both
migratory and resident biota. The migratory biota in question are diadromous fish (Walther et
al. 2011).
Diadromous fishes are a group of migratory fishes that move between freshwater
habitats to marine areas or vice versa (Quinn et al. 2009; Iida et al. 2017). In their movement,
diadromous fish utilize the estuary as a transition area (Iida et al. 2017). Diadromous fishes
found in estuaries consist of anadromous, catadromous and amphidromous fishes. The term
amphidromous is used to name a group of fishes that migrate or move at certain phases of
their life cycle, but not for reproductive purposes (Myers 1949).
Based on the origin of the word, amphidromus comes from two words, namely amphi,
meaning two and draimen which means movement. Furthermore, McDowall (2007) explains
that freshwater amphidromes are a group of fish that spawn in freshwater areas. The newly
hatched larvae are rheoplanktonic and will be drifted by river currents to marine waters. The
larvae will perform their first predation in marine waters to grow and develop until the
postflexion stage. Postflexion larvae will turn into yuwana and return to freshwater to grow
into adults and spawn (Keith 2003). This makes the estuary a very important area in
determining the success of the recruitment process and the survival of freshwater
amphidromous fish (Simanjuntak et al. 2021).
One of the factors that support the successful recruitment of amphidromous fish to
freshwater is the availability of food. This is because the recruitment process requires
considerable energy (Gosal et al. 2013). The food will be used as a source of material and
energy for the growth and development of organs needed to improve swimming ability
(McDowall 2007).
Developed amphidromous fingerlings with sufficient swimming ability will begin to
move for recruitment to freshwater through river mouths (Ellien et al. 2016). During this
movement, there is also an ontogenetic change in habitat from pelagic to bento-pelagic larvae
(Augspurger et al. 2016). This migration is also accompanied by a change in the type of
ontogenetic diet shift (Henseler et al. 2020).
Fish diet is fundamental information to explain the role of a fish species in the
ecosystem. Ramírez-Luna et al. (2008) and Hajisamae et al. (2003) explain the role of a
species in the ecosystem based on food utilization will explain the position of t he species in
the food chain or known as trophic level. The study of trophic levels of fish species is very
important in ecosystem-based fish resource management, one of which is as a reference for
assessing the effects of fishing on food webs in aquatic ecosystems (Stergiou and Karpouzi
2002).
The Cimaja Estuary is one of the potential amphidromus fisheries in the coastal
Palabuhanratu Bay, Sukabumi District (Simanjuntak et al. 2021). Local fishermen refer to all
amphidromous fingerlings as impun, which mostly consist of fish from the Gobiidae family
(Affandi 1994; Simanjuntak et al. 2021). The local community generally utilizes impun as a
food commodity. The capture of amphidromous fingerlings takes place massively and has
even become a routine tradition every month called Nyalawean. Uncontrolled fishing through
nyalawean activities is feared to reduce population numbers and affect the sustainability of
amphidromous fish in the Cimaja Estuary.
Overutilization certainly has an impact on the balance of the food chain and interactions
between fish species in utilizing natural food resources (Widarmanto et al. 2019). Efforts to
manage the Cimaja Estuary ecosystem are needed to maintain the sustainability of
amphidromous fish resources. In this management effort, basic data and information on
trophic ecology are needed. Given the absence of studies on trophic ecology of
amphidromous fish juveniles, especially the Gobiidae family, conducted in the Cimaja
Estuary, research with the aim of revealing food composition, feeding strategies and trophic
levels of amphidromous fish juveniles in the Cimaja Estuary, Palabuhanratu Bay, Sukabumi,
West Java needs to be carried out.
1.1 Research Procedure
The research was conducted in two stages, namely in situ data collection and laboratory
analysis. In situ data collection includes measurement of physical-chemical parameters of
waters and capture of larvae and yuwana amphidromus fish Family Gobiidae. The sample
analysis stage includes identification of amphidromus fish species both morphologically and
molecularly and food analysis is carried out in the laboratory.
1.1.1 Measurement of Physical-Chemical Parameters of Waters
The physical parameters of the waters observed and measured in situ consisted of
temperature and turbidity, while the chemical parameters included salinity, acidity (pH) and
dissolved oxygen (DO). The instruments used to measure the physical-chemical parameters
of the waters consisted of a thermometer (temperature), turbidimeter (turbidity), refractometer
(salinity), pH meter (pH), and DO meter (dissolved oxygen).
Secondary data in the form of high tides were obtained from the website
www.tides.big.go.id. Physical-chemical data was used to determine the environmental
conditions of the Cimaja Estuary during the study.
1.1.2 Sampling of Fish Larvae and Yuwana
Sampling of larvae and yuwana was conducted using seser or sirib fishing gear. Seser
or better known as sirib is a fishing gear categorized as a lift net. It consists of a square piece
of fine mesh supported by four wooden slats, each about 1.5 meters long. The sirib net has a
mesh size of 0.48 mm (Annida et al. 2021; Simanjuntak et al. 2021). Siribs are used by local
communities to catch fish larvae and yuwana in the estuary (Imron et al. 2018). Siribs are
positioned against the current from the sea towards the estuary. It is lifted as soon as the water
mass passes through the net. Captured fish larvae and yuwana are put into a temporary fishing
container made of plastic material (Annida et al. 2021; Simanjuntak et al. 2021). Fish
sampling using flippers was conducted actively with a duration of 1.5 hours at each station.
This duration was determined by taking into account the length of time the tide occurs. Tidal
energy is utilized by amphidromous fish juveniles to recruit into the estuary (Simanjuntak et
al. 2021).
Captured larval and juvenile samples were separated into two types of preservation
based on their purpose. Samples of amphidromous fish juveniles for morphological
identification were preserved using 10% formalin for 3 hours of immersion. Samples were
then rinsed under running water and preserved again in 80% ethanol solution. This
preservation technique is used to maintain the color pattern of the melanophore which is one
of the characteristics of morphological identification of fish juveniles (Simanjuntak et al.
2020). The samples for molecular identification (DNA Barcoding) were preserved in 96%
ethanol solution (Wulandari et al. 2019).
1.1.3 Morphological Identification of Fish Larvae and Yuwana
Fish larvae and yuwana samples were taken to the Macro Biology Laboratory 1 (BIMA),
Department of Aquatic Resources Management, Faculty of Fisheries and Marine Science,
Bogor Agricultural University for morphological identification. Morphological identification
was carried out using a Nikon type 104 stereo microscope. Identification was carried out to
the lowest taxon referring to Leis and Carson (2000), Hiroshi et al. (2004), Miller and
Kendall (2009) and Okiyama (2014). The development of amphidromous fish fry stadia was
also observed with reference to Kendall et al. (1984). Each fish sample was measured for
body length (mm) using an ocular micrometer and photographed for documentation.
1.1.4 Molecular Identification of Fish Larvae and Yuwana
Identification of juveniles is more difficult than that of adults. The lack of information
on tropical fish larvae and juveniles in estuaries, coupled with the high diversity of fish
species in these waters, makes this a problem in the taxonomic process. Morphological
identification is generally only able to reach the family or genus level, while the molecular
approach can identify specimens up to species. The process of molecular analysis through
DNA bar code identification was carried out at the Bionesia Laboratory (BIONESIA)
Jembrana, Bali. The molecular identification process was carried out on the COI gene marker
with Fish F1R1 Primer.
Identification of DNA barcodes includes several stages of work including collection of
tissue samples, isolation and purification of DNA, visualization and amplification of DNA
and DNA barcode sequencing. Tissue samples were collected by sorting larval and juvenile
fish that had been preserved using 96% ethanol based on morphological characteristics. The
number of fish larvae and juveniles identified using DNA varied by stadia and size.
Larval stadia with a size of less than 5 mm were taken as samples, while for juvenile
stadia or with a size of more than 5 mm, at least 5 samples were taken for each species. DNA
isolation and purification were carried out to separate total DNA from preservatives and other
cell components because contamination from preservatives can interfere with the process of
reading or identifying DNA barcodes. The results of the DNA bar code reading were then
aligned with the Genetic Data Bank on the NCBI website. This alignment was carried out
with the help of the Basic Local Allignment Search Tools (BLAST) tool on the NCBI
website.
1.1.5 Identification of Larval and Juvenile Fish Diets
Observations of fish food began with dissections performed under a stereo microscope.
Samples of fish containing food were selected as many as
30 individuals for each species and their permanence in each month of observation. Digestive
tract contents in the form of phytobenthics and zoobenthics were identified by referring to
several identification books such as Yamaji (1979), Chihara and Murano (1997) and Davis
(1955). The identified digestive tract contents were counted in number and measured in
volume (biovolume) for further analysis.
1.2 Data Analysis
1.2.1 Larval and Juvenile Abundance of Fishes of the Family Gobiidae
The abundance of larval and juvenile fish was analyzed after identification using
morphological approaches and DNA Barcoding. The total number of larval and juvenile fish
caught was analyzed using the abundance of catch per unit of fishing effort (CPUE)
calculated using the following formula (Gulland 1983):
1.2.2 Larval and juvenile species composition of fishes of the Gobiidae family
Catch composition to see the percentage of larval and juvenile fish species caught at
each station based on day and night time in each sampling month. Catch composition analysis
was calculated using Odum's (1993) formula as follows:
1.2.3 Food Type Composition of Fish Larvae and Juveniles
The diet composition of larval and juvenile fish was analyzed using the Index of the
Largest Part (IBT) formula. Index of the Largest Part (IBT) is the presentation of a particular
type of food to all food organisms utilized by larval and juvenile fish (Natarajan and Jhingran
1961). The formula for the Index of Largest Part (IBT) is as follows:
The results of food composition analysis become a reference in the classification of
trophic level of fish. Trophic level is determined based on the type of food that is dominantly
utilized by fish (Zahid et al. 2015).
1.2.4 Fish Eating Strategy
Feeding strategies were determined by correlating the percent frequency of occurrence
and percent organism-specific abundance using Coestello's (1990) graph modified by
Amundsen et al. (This analysis compares food abundance and frequency of occurrence to
determine the feeding importance of each type of food taxa obtained (Subjak 2013).
3.1 Aquatic Environmental Conditions
The condition of the water environment at the research site during sampling is
presented in Tables 1 and 2. The physical-chemical parameter values of the water were quite
varied.
The tide height varied considerably during the study time. During the day, the tide
height values ranged from 0.06 to 0.6 meters. The highest tidal height was recorded at station
2 in January, while the lowest tidal height occurred at station 1 in December. At night the
high tide has a range of values between 0.03 to 0.26 meters. The highest value of tide height
at night occurred at station 2 in March and the lowest tide height occurred at station 1 in
December.
The turbidity value of the waters at the study site tends to decrease every month of
observation. The range of turbidity values during the day is between 31.79 to 58.17 NTU.
The lowest turbidity occurred at station 2 in May, while the highest turbidity value was
recorded at station 1 in December. At night, the range of water turbidity values was 22.26 to
38.28 NTU. The lowest turbidity value occurred at station 2 in April, and the highest turbidity
value was recorded at station 1 in December. The highest water turbidity occurred at station 1 in
December.
The water temperature range value obtained during the day is between 29 to 31ºC.
The lowest temperature occurs at station 1 in January to March while the highest temperature
occurs at station 2 in December, April and May. At night the value of the water temperature
range is 27 to 30ºC. The lowest temperature measured occurred at station 2 in January, while
the highest temperature at night occurred at station 2 in December, April and May.
Salinity values in Cimaja estuary during the day ranged from 4.0 to 29.0 psu. The
highest salinity was found at station 2 in January, while the lowest salinity value occurred at
station 1 in December. While at night, salinity values tend to be lower, ranging from 2.0 to
13.0 psu. The highest salinity occurred at station 2 in March and the lowest at station 1 in
May.
The degree of acidity (pH) of the waters recorded during the day ranged from 7.41 to
7.83. The highest pH value occurred in January at station 2, while the lowest pH occurred in
May at station 1. The pH value of the waters at night has a value that tends not to be much
different, which ranges from 7.31 to 7.70. The highest average pH value occurred at station 2
from December to March, while the lowest pH value occurred at station 1 in April.
Dissolved oxygen during the day during the six months of the study had a range of
values between 5.7 to 6.7 mg/l. The highest dissolved oxygen value occurred at station 1 in
December and the lowest occurred at station 2 in April. While at night, the range of dissolved
oxygen recorded was 5.3 to 6.6 mg/l. The highest oxygen value was recorded at station 2 in
December and the lowest dissolved oxygen value occurred at station 2 in May.
The range of dissolved oxygen values in the Cimaja Estuary was 5.3 to 6.7 mg/l. The
estuary in Sukabumi District has a rocky bottom substrate with steep coastal contours. This
causes high water turbulence. The turbulence of the water causes the process of dissolved
oxygen in the water to form quite well (Simanjuntak et al. 2021; Setyawan and Pamungkas
2017).
Good water conditions will support the success of the recruitment process and the
continuity of the larval and juvenile fish feeding process. Generally, fish in the larval and
juvenile fish stages are visual feeders (Holt 2011) so that clear waters tend to be favored for
the foraging process. Cimaja Estuary has a low turbidity level ranging from 22.6 to 58.17
NTU, so the number of larval and juvenile fish of the Gobiidae family that recruit and forage
is also high in the estuary. Watanabe et al. (2013) also explained that under these conditions
the abundance of phytobenthics which are the main food of amphidromous fish will be more.
Temperature is one of the factors that is very influential for the life of aquatic biota
because it affects the process of growth and metabolism. Some of the factors that cause this
are water depth and research location. Research sites located in estuary areas tend to have
higher water temperatures. This is due to the movement of freshwater masses from the river
flow into marine waters. The friction of the sea water mass can generate heat due to friction
between water molecules, so that the water temperature will become warmer (Sidabutar et al.
2019). In addition, The intensity of sunlight exposure during the day can also increase
water temperature. This is because the process of sunlight causes the transfer of heat energy
to the water (Vroom et al. 2017).
High tides are strongly associated with the successful recruitment of larval and
juvenile Gobiidae fish into the Cimaja Estuary (Miller and Kendall 2009). The Cimaja
Estuary experiences semi-diurnal tides, which have 2 high and 2 low tides in 24 hours
(Fathurahman et al. 2021). Simanjuntak et al. (2021) explained that the tide occurs at 03.00 at
night and 15.00 in the afternoon. The limited swimming ability of the larval and juvenile
stadia causes these two fish stadia to utilize tidal waters for recruitment into river waters.
Furthermore, Simanjuntak et al. (2021) revealed that the success of the amphidromous fish
recruitment process to the Cimaja Estuary is inseparable from the tidal waters. This is because
river currents entering marine waters will reduce the movement of larvae and juveniles that
will carry out recruitment so that the presence of high tides will "push" amphidromous fish
larvae and juveniles into fresh waters more easily (Keith et al. 2008). The stored energy can
be used for settlement or occupying the substrate of the riverbed and foraging (Iida et al.
2015; Prabowo 2022).
Salinity conditions are very important for aquatic biota because they affect the
osmoregulation process in the body of biota. Salinity is often related to tidal conditions. This
is because, when the tide occurs, sea water with higher salinity will enter and carry some of
the water mass to the estuary area (Simanjuntak et al. 2021; Oto 2020). Tidal conditions are
also known to affect the pH of the waters. So that when salinity has increased due to the
influence of tides, the pH of the waters will also tend to increase. This is because seawater is
generally more alkaline with an acidity value of >6.0 (Proum et al. 2017; Patty and Akbar
2018).
3.2 Diversity of Larvae and Juveniles of Fish Family Gobiidae in Cimaja Estuary
Based on the results of morphological identification, eight species of amphidromous
fish larvae and yuwana Family Gobiidae were obtained at the research site (Table 3).
Furthermore, through the molecular approach, two of the eight species were successfully
identified, namely Stiphodon semoni and Schismatogobius marmoratus. As for 1 type of fish
can only be identified up to the genus stage, namely Mugilogobius sp. The existence of
technical constraints that occur during the molecular identification process causes 5 other fish
species to only be identified up to the genus level through morphological approaches.
Morphological identification of fish is done by observing the melanophore pattern of
fish which becomes a marker to distinguish one species from another. Melanophore is a
pattern that characterizes fish larvae that will last until the fish reaches adult stadia. Another
morphological identification is counting the number of myomers (Leis and Carson 2000).
The flexion stage is characterized by bending at the end of the notochord at the base
of the tail. However, movement is still limited because the ossification process
(reinforcement) of the fin fingers is still developing, and the body color tends to be clear. The
postflexion stage is a continuation of the flexion stage. This stadia is characterized by better
organ development and fin fingers that have been formed although not perfect, so that the
movement has been better than the previous stadia. This stadia is also characterized by the
development of a disc-shaped pelvic fin that will be used to attach to the substrate of riverbed
rocks in the Cimaja Estuary for recruitment and feeding.
The yuwana stadia are characterized by the growth of scales (squamation), the
development of organs and fins that are getting better and the color of the body begins to
resemble its parents. Gobiidae family fish obtained during the study consisted of three stadia
namely flexion, postflexion and yuwana. The yuwana stadia obtained although it does not
have the characteristics as previously described but it was found that squamation had
occurred, although the body color was still clear resembling the postflexion stadia. So that the
fish obtained is called early juvenile (Keith 2003; Leis and Carson 2000; Miller and Kendall
2009; McDowall 2007).
The body length range of Gobiidae family fish obtained in Cimaja Estuary during the
study period ranged from 4.9 - 26.3 mm. Flexion stadia larvae had a body length between 4.9
- 6.8 mm, postflexion stadia larvae 6.9 - 11.8 mm, and yuwana stadia ranged from 11.9 - 26.3
mm. Amphidromous fish of the Gobiidae family generally recruit at the postflexion stadia.
This is because the swimming ability at this stadia is better than the previous stadia (Keith
2003; Keith et al. 2015). In several other studies (Iida et al. 2008; Radtke et al. 2001; Shen
and Tzeng 2008; Zakaria 2018) explained that the amphidromous fish of the Gobiidae Family
that recruited in the postflexion stadia (Keith 2003; Keith et al. 2015) into estuary waters tend
to be in postflexion stadia with different body lengths. This is due to the influence of
environmental conditions and the acquisition of nutrients that occur, thus affecting the growth
rate of the fish body.
3.3 Abundance, Diversity and Dominant Species of Larvae and Juveniles of Fish Family
Gobiidae in Cimaja Estuary
During the six months of research, 33,417 larvae and juveniles of amphidromous fish
of the Gobiidae family were obtained in the Cimaja Estuary, consisting of eight genera with
different abundances. The abundance of larval and juvenile amphidromous fish of the
Gobiidae family from December 2020 to May 2021 is presented in Table 5. The abundance of
larval and juvenile fish that recruited to the Cimaja Estuary had a higher variation in numbers
when compared to other estuaries in Sukabumi District. Simanjuntak et al. (2021) explained
that this is because the Cimaja Estuary has a rocky and sandy water substrate that is favored
by amphidromous fish juveniles.
The abundance of larval and juvenile fish was higher in January compared to May.
This is because May is classified as the dry season (Baihaqi 2022). The dry season tends to
cause lower tides (Purnaini et al. 2018). On the other hand, Belhassan (2011) also explained
that low rainfall conditions will cause the recruitment process of amphidromous fish Family
Gobiidae to be disrupted.
The abundance of amphidromous fish species of the Gobiidae family that recruited to
the Cimaja Estuary had varying values (Table 5). The least fish species found to be recruiting
was Mugilogobius sp. with abundance values ranging from 0.50 to 21.50 Ind./hour. The most
abundant fish species was Sicyopterus sp. 2 with values ranging from 1.69 to 84.85 Ind./hour.
The abundance of fish of Sicyopterus sp. 2 can be attributed to the timing of fish spawning,
the suitability of substrate conditions, and the environmental conditions of these waters
(Effendi 2002).
The amphidromous fish of the Gobiidae family found recruiting to the Cimaja Estuary
consisted of postflexion larval and yuwana stadia. The dominant stadia found at stations 1 and
2 of the Cimaja Estuary, both during the day and at night, were the yuwana stadia. In the
research of Yamasaki et al. (2007) explained that fish of the Gobiidae family that recruits to
estuary waters is generally in the postflexion larval stadia and also yuwana. This is associated
with the readiness of its body organs, namely the pelvic fin. Postflexion larvae and yuwana
fish of the Gobiidae family will experience morphological adaptations in the form of pelvic
fin development. The pelvic fins, which have developed to the shape of a sticking disk, will
stick to the rocks so as not to be carried away by the river current. However, the number of
postflexion larval stadia fish that recruited to the Cimaja Estuary was lower. Meanwhile, the
abundance of juvenile stadia was higher, because the previous larval stadia that had recruited
in the early months had undergone stadia changes to become juvenile stadia.
3.4 Food Organism Groups and Species Found in Larvae and Juveniles of Fishes of the
Gobiidae Family
The number of larval and juvenile fish of the Gobiidae family dissected to analyze the
contents of the digestive tract was 3,175 individuals, out of a total catch of 33,417
individuals. The types of food organisms identified came from two categories, namely
phytobenthic and zoobenthic. Phytobenthics obtained are included in the benthic microalgae
(BMA) group. The benthic microalgae category has the highest number of genus compared to
zoobenthic (Table 8).
Benthic food species are dominant in the digestive tract of both larvae and yuwana fish
of the Gobiidae family, indicating that these fish search and feed on the bottom of the water.
Fitzsimons et al. (2003) described changes in the position of the mouth and the development
of the pelvic fins of larval and juvenile S. stimpsoni in several estuaries around Hawai'i
Island, helping the settlement process on the riverbed. As their pelvic fins are used to attach
and rest on rocks against the current, the fish's mouth will begin to feed on benthic algae and
diatoms growing on the rock surface (Nishimoto and Fitzsimons 1998). Rocky substrates on
the bottom of flowing rivers (Sandy et al. 2021) and receive sun exposure (Rusmiati et al.
2021), generally become a growing medium for benthic algae which are food for larvae and
juveniles of fish of the Gobiidae family (Muthiadin et al. 2020). Larvae and juveniles of
Sicyopterus spp. and Stiphodon spp. are also reported to predominantly feed on benthic
microalgae as their main food (Fitzsimons et al. 2003; Julius et al. 2005).
Furthermore, Bacillariophyceae are diatoms from the benthic microalgae group that
are widely distributed and able to adapt to various water conditions (Odum 1996; Pratama et
al. 2019). Benthic microalgae of the Bacillariophyceae, Chlorophyta, and Cyanophyta species
are found attached to rock surfaces and are the main food for S. stimpsoni larvae and
juveniles (Fitzsimons et al. 2003).
3.5 Diversity and Composition of Larval and Juvenile Diets of Fishes of the Gobiidae
Family
Once the eggs have hatched, the fish larvae will undergo changes to reach the juvenile
and adult stages. This requires the acquisition of sufficient nutrients and energy (Holt 2011).
The end of the larval stage will be marked by the development of organs and related
components the process of food uptake that has been completed and is functioning properly
(Russo et al. 2009).
Newly hatched larvae of the amphidromous fish family Gobiidae have a yolk sac that
is used as a source of nutrition and energy while other organs are developing. This feeding
process is called "endogenous feeding". Then, when the yolk-sac is depleted, the larval fish
will begin its first predation process in marine waters (exogenous feeding) (Keith 2003). The
transition from endogenous to exogenous feeding requires organs and components related to
food uptake to be functional and ready for use (Osse and van den Boogaart 1999; Holt 2011).
Larval survivorship of Gobiidae family fishes on first exogenous feeding tends to be low
(Keith 2003). Generally, the mouth position of Gobiidae larvae is terminal. However, at the
juvenile stage, the position of the mouth changes to sub terminal. This is a physiological
adaptation strategy that makes it easier for them to feed during recruitment (Fitzsimons et al.
2003). The diet composition of Stiphodon elegans larvae and yuwana is presented in Tables 9
and 10. The types of food eaten by S. elegans larvae are less than yuwana. S. elegans larvae
ate small amounts of zoobenthics. The dominant food eaten by larvae was Tabellaria, while
yuwana ate Tabellaria and Surirella.
Based on the results obtained, there are differences in the type of food in all species of
amphidromous fish Family Gobiidae both larval and juvenile stadia in the Cimaja Estuary.
Larval stadia eat more food of smaller size, namely Nitzschia species, while yuwana stadia
tend to prefer Surirella and Tabellaria species. The difference that occurs can be said to be
due to the size dimensions of the two types of food (Munk 1997). Larval food types have size
dimensions that tend to be smaller than those of yuwana (Heudre et al. 2021; Julius et al.
2005). Larvae that have a smaller body size will eat foods that match the size of their mouth
opening.
The occurrence of differences in the contents of the digestive tract of fish based on
increasing stadia also occurs in larvae and yuwana fish of the Gobiidae family, S. stimpsoni
(Julius et al. 2005). The food type of the juvenile stadia is larger in size dimension than the
previous stadia. Changes in the contents of the digestive tract in both stadia indicate a growth
process in these fish (Rakauskas et al. 2008).
Ontogenetic diet shift is a change in diet that occurs in one type of fish due to
ontogenetic morphology that occurs. Ontogenetic morphology generally occurs during the
process of increasing fish stadia (Kanou et al. 2005 and Specziár 2005). Changing the type of
food consumed along with the development of age or stadia in amphidromous fish is done as
an adaptation to fulfill its nutrition and energy (Keith and Lord 2011). This aims to optimize
growth and as a survival strategy during the recruitment process (Keith et al. 2008;
Barbeyron et al. 2017).
The dominant ontogentic morphology that occurs in larval and juvenile fishes of the
Gobiidae family is an increase in mouth opening width (Kanou et al. 2004a), changes in the
digestive tract (Bruce 1995), eye development (Arnold and Holford 1990), and fin
development and body shape (Kido 1996a; Kanou 2004b). Ontogenetic diet shift along with
ontogentic morphology in amphidromous fishes of other Gobiidae families are A. flavimanus
(Kanou et al. 2004b; Kanou et al. 2005; Sakai et al. 2000), and N. melastanomus (Olson and
Janssen 2017; Hempel et al. 2018; Henseler et al. 2020), which is an increase in food size
dimensions along with an increase in body size.
Fish in the yuwana stage have actively searched for prey, compared to the previous
stadia which are passive and tend to depend on prey that is only in front of them (Yúfera and
Darias 2007). Furthermore, yuwana that have developed a good size of mouth opening, jaw,
and tooth growth will also eat differently. Prey is not only eaten but will be bitten and then
swallowed. In contrast to the larval stadia, which only directly swallow their prey because of
the limited organs available (Bochdansky et al. 2008). So this makes it possible for the
yuwana stadia to prey on food that is larger than the type of food consumed in the larval
stadia.
This happens because of the need for greater fulfillment of nutrients for the growth
process. There are nutritional requirements needed for the growth process from larvae,
yuwana to adult fish (Lawson et al. 2018). In addition, the search for food has been
optimized, namely larger fish have a wider range of capabilities and tend to consume larger
food to maximize their energy gain (Gerking 1994; Simanjuntak et al. 2022).
The food composition of larvae and yuwana fish of the Gobiidae family in the Cimaja
Estuary during the six months of observation had diverse results. The main type of food
obtained was benthic microalgae of diatom species from the class of Bacillariophyceae with
different genus. However, at night there is an additional type of food, namely from the
zoobenthic group, although the amount is not abundant. In general, amphidromous fish of the
Gobiidae family that recruit to estuary waters are benthic feeders (Charlebois et al. 1997;
Adámek et al. 2007).
Some fish species of the Gobiidae family in Pabean Bay are generally benthic feeders
by eating benthic microalgae (phytobenthic). The main types of food obtained are
Bacillariophyceae from the genus Gyrosigma, Navicula, Nitzschia, and Surirella. While from
the Cyanophyceae class, the genus Oscillatoria (Khoncara et al. 2018; Salindeho 2021).
Benthic microalgae diatom species are single-cell plants. These diatoms live at the bottom of
the water and attach to the surface of the substrate (benthic). So that diatoms can be said to
play a role in the food network of fish larvae and yuwana (Nurlaelatun et al. 2018; Padang
2011; Rusmiati et al. 2021).
Larval and juvenile fish of the Gobiidae family studied by Ara et al. (2010) also have
a diet that tends to come from benthic microalgae (phytobenthic), which makes them included
in the herbivore group. Juniar et al. (2019) also suggested that the food of the Gobiidae
family, which is a local fish in East Java, consumes generally diatoms with one type of
Nitzschia.
The composition of food consumed by larvae and yuwana fish of the Gobiidae family
in the Cimaja Estuary at night experienced an increase in food types compared to the daytime.
The type of food found duri n g t h e d a y was benthic microalgae, but at night there
was an additional type of food, namely zoobenthic, although benthic microalgae still
dominated the composition of food both day and night. Pratama et al. (2019) and
Rahmatullah and Karina (2016) explain that Bacillariophyceae diatoms are generally found
not only during the day but also at night in estuary waters. This is due to the fulfillment of
nutrients for a larger body development period, where zoobenthics contain more nutrients
than benthic microalgae (phytobenthics) (Lawson et al. 2018). Furthermore, Odum (1996)
explains that this is because Bacillariophyceae in waters have the ability to adapt easily,
resistance to extreme environmental conditions and reproduce quickly, which can divide
twice in less than 36 hours compared to other types of food. Radiarta (2013) explains that the
abundance of benthic microalgae and zoobenthics in estuary waters tends to be high. This is
because estuary waters are the meeting point between sea water and river water, so they are
rich in nutrients and nutrients needed by aquatic organisms.
The presence of food in the form of zoobenthics consumed by larval and juvenile fish
of the Gobiidae family illustrates the efforts to fulfill the nutritional needs of these fish. It is
known that zoobenthic species have more diverse nutritional content, especially protein,
which is needed in the growth phase of fish compared to benthic microalgae (Buckley and
Durbin 2006), so that fish larvae and juveniles will utilize this type of food even though in
limited quantities. Differences in the types of food consumed by larval and juvenile fish in
each year
The month of observation is inseparable from the availability of food in nature. The
adaptive nature of fish in utilizing the types of food available in nature is an evolutionary
process towards the characteristics of natural foods that are limited in nature (Herder and
Schliewen 2010). The type of food available will be used as energy gain to optimize the
process of growth and recruitment of fish. Therefore, the feeding strategy of fish in utilizing
the available food species will affect the population of the fish species in nature. Fish species
that are unable to develop a "wide" feeding strategy will potentially experience population
decline (Effendi 2002).
The ANOVA variance test results showed that there was no significant difference in
p-value (0.910) between the diet composition of larval and juvenile amphidromous fishes of
the Gobiidae family during the day and night. This reinforces the reasoning that larval and
juvenile amphidromous fishes of Gobiidae carry out the recruitment process while feeding.
Gobiidae larvae and juveniles are known to recruit during the day and night when the highest
tide occurs. Food is needed to meet the large energy needs during the recruitment process to
the Cimaja Estuary (Watanabe et al. 2013).
3.6 Trophic Levels of Larvae and Yuwana of Amphidromus Fish Family Gobiidae
Trophic levels of larval and juvenile amphidromous fish of the Gobiidae family in
each month of observation a re presented based on the type and stadia of fish observed
(Figure 4). Trophic level is the position of an aquatic organism in the food web. Trophic
levels also indicate each organism's role in the food web (Stergiou et al. 2007).
The trophic level of each fish species and stadia during the study ranged from 2.00-
2.04. The highest trophic level was occupied by Mugilogobius sp. larval stadia in March with
a trophic value of 2.04, while Schismatogobius marmoratus larval stadia in May had the
lowest trophic value with a value of 2.00. The trophic level values of larval and juvenile fish
in each month of observation tended to increase. This is because the observed Gobiidae fish
experienced stadia development. Fish that experience stadia development generally
experience morphological changes along with the development of their body (ontogenetic
morphology) which is related to changes in food types as the fish ages (ontogenetic diet shift).
Fish stadia development affects the type of food eaten because there is a positive
correlation between body size and trophic level (Ratsgoo and Navarro 2016; Hedianto and
Sentosa 2019). This condition applies to the majority of fish that replace food types along
with the development of digestive organ formation (Bishop and Wear 2005). In the next
phase, fish will follow the feeding habits of their parents. Puvanendran et al. (2004) also
stated that changes in the type of food consumed will provide the necessary nutrients and
energy intake. Fish that move and hunt for prey require energy, so to compensate for the
process of finding prey and optimizing body growth, good energy efficiency is needed.
In the results of the study there are types of fish that occupy trophic positions that are
not in accordance with the position that should be, this is because these fish species tend to
only eat the types of food available in nature (Herlevi et al. 2018), so that even though the
type of fish at that stadia requires certain foods in the growth process, it will still depend on
the food available in nature (Rakauskas et al. 2008).
Trophic groups or trophic guilds are determined by the main food of the food
composition utilized by each type and stadia of fish (Hedianto and Santosa 2019). Fish
trophic groups are divided into true herbivores that predominantly eat algae (TL1), omnivores
that tend to eat plants (TL2), omnivores that tend to eat zooplankton animals (TL3),
carnivores whose main diet is decapods and fish (TL4), and carnivores whose main diet is
fish and Cephalopods (TL5).
All fish species obtained both larval and juvenile stadia are categorized as functional
group TL1, namely true herbivores with algivorous trophic unions. Algivores are types of fish
that only eat algae in the waters. Categorized as algivorous because all fish species
encountered trophic values range from 2.0-2.1. Although the algae consumed are included in
benthic microalgae because they are microscopic. The thing that distinguishes is the
dominance of food types in each fish and each stadia, so it can be said that the more the fish
stadia increase, the trophic position increases even though the trophic functional group
remains TL1. Simanjuntak and Zahid (2009) explained that the larger the size of the fish, the
more diverse the food types. This happens because during the early stages of its life, fish will
tend to look for food that suits its body condition and will change at the next stage. In the
yuwana stadia, fish will generally follow the eating habits of their parents (Effendi 2002).
3.7 Feeding Strategies of Larval and Juvenile Fishes of the Gobiidae Family Amphidromus
Feeding strategies of larval and juvenile amphidromous fish of the Gobiidae family in
the Cimaja Estuary during the six months of observation are presented in Tables 24-27. Fish
feeding strategies are categorized into specialist, generalist or a combination of the two.
Generalist means that the fish species utilizes a variety of different food taxa with a low
frequency of occurrence. A specialist, on the other hand, indicates a fish species that utilizes a
small number of food taxa with a high frequency of occurrence (Effendi 2002). Based on the
diverse number of taxa of these food types, fish feeding strategies are further categorized into
several traits.
Euriphagics utilize many rare taxa with a low frequency of occurrence. Conversely,
each fish species can be said to be stenophagic if it utilizes few natural food taxa (dominant
taxa) with a high frequency of occurrence. Slightly different, fish that utilize only one type of
natural food taxa with a high frequency of occurrence are also called monophagic (dominant
taxa). Opportunistic traits are indicated when fish species utilize natural food species with a
low frequency of occurrence with a high proportion of utilization rates and numbers of
natural food taxa (Bruton 1990; Subjak 2013; Hedianto and Sentosa 2019).
Based on the Coestello charts of the eight different fish species at both fish stadia
showed diverse values. The feeding strategies developed by the fish were specialist-
generalist, generalist-europhagic, specialist-stenophagic, specialist-europhagic, and
generalist-stenophagic. The diverse values obtained each month of observation are due to the
availability of natural food in nature (Ara et al. 2010).
Larval amphidromous Gobiidae fish found in the Cimaja Estuary generally develop a
generalist-stenophagic feeding strategy, while the juvenile stadia develop a specialist-
europhagic feeding strategy. The larval stadia of fish are generalists by utilizing various types
of natural food taxa available in nature. This strategy can be said to be a successful adaptation
of fish larvae in the Cimaja Estuary in utilizing natural food in the context of the recruitment
process to estuaries and rivers (Prabowo 2022). The stenophagic nature of food taxa
utilization by fish larvae is due to the fact that food utilization by fish larvae is still limited by
the width of the mouth opening (Kido 1996a), the movement and swimming speed of fish
larvae (Holt 2011) and the view of prey (Nunn et al. 2007).
Therefore, although larval stages utilize a variety of foods in nature, there is a
tendency to consume certain types of food that are suitable for the conditions of the stadia.
Fish larvae tend to be generalists about the various types of natural foods available in nature
because larvae need energy from food for their growth process towards the next stage (Holt
2011).
In yuwana stadia the feeding strategies obtained were generally specialist with
euriphagic utilization properties. This feeding strategy explains that yuwana stadia utilize a
variety of food types but there are some taxa that are eaten with high frequency. Yuwana
stadia fish already have a preference for certain types of food compared to previous stadia
(Munk 1997). This is because yuwana stadia have resembled their parents and therefore tend
not to have the same limitations on predation as earlier stadia (Chesney 2008; Holt 2011).
Ecological pressure in the Cimaja Estuary also has the potential to reduce the
availability of natural food. This will also cause food competition between fish species to
increase. To maintain the high survival rate of larval and juvenile amphidromous fish of the
Gobiidae family in nature, good adaptability of fish to changes in environmental conditions is
required. Reducing ecological pressure in the Cimaja Estuary will maintain natural food
sources in nature so that the survival of larval and juvenile amphidromous fish Family
Gobiidae is maintained.
3.8 Recommendations for the Management of Larval and Juvenile Fish of the Gobiidae
Family
The ecological study of the larval and juvenile diet of amphidromous fish of the
Gobiidae family explains that these fish utilize estuary waters for recruitment and foraging.
Benthic microalgae and zoobenthics attached to the bottom substrate become a food source
for larval and juvenile amphidromous fish Family Gobiidae in the Cimaja Estuary. This is
utilized by both stadia as food used to support the process of body growth and stadia
development and as a source of energy to move against the river current.
The existence of anthropogenic activities in the Cimaja Estuary, namely rock and sand
mining that has been going on for a long time, has caused environmental degradation for the
Cimaja River. This has at least made the width of Cimaja River increase every year and
caused heavy overflow of river water when rain occurs. Another anthropogenic activity is the
massive capture of amphidromous fish of the Gobiidae family that recruits to the Cimaja
Estuary. The fish caught are those in the larval and juvenile stages. Even the utilization of
these fish has become a routine tradition every month in Palabuhanratu Bay, called
Nyalawean.
In Julius et al. (2005) specifically explained that the disturbance of the river body will
affect the feeding process of yuwana Family Gobiidae. Overflowing water during heavy rains
or an increase in the speed of river currents can occur because the rocks at the bottom of the
water that can inhibit the flow of the river have been reduced. Overflowing river bodies
during floods will also cause a decrease in the amount of algae cover on rock surfaces. This
will cause Gobiidae family yuwana, which use algae attached to rock substrates as their main
food source, to change their diet or if they cannot, will experience starvation.
Communities on the coast of Cimaja River tend to utilize existing resources without
considering their sustainability. One of them is mining rocks and sand in the river body. This
is because river rocks and sand are open access and supported by demands that tend to
increase, encouraging some parties to behave less wisely in utilizing them. Based on these
conditions, it is feared that Cimaja River will experience habitat degradation, so it is
necessary to reduce or even prohibit rock and sand mining activities in the Cimaja Estuary
because it can cause ecological pressure that can endanger not only the lives of larvae and
yuwana but also natural food sources found in nature.
This condition needs to be considered after seeing that the Cimaja Estuary area is an
important area for high amphidromous fish resources, especially the Gobiidae fish group.
This is reinforced by the results of the food analysis carried out in this study which explains
that the larvae and yuwana of Gobiidae fish utilize estuary waters as a search area feeding
with several main types of food utilized such as the Bacillariophyceae group.
Limiting the time of capture of larval and juvenile amphidromous fish of the Gobiidae
family can be done to allow time for these fish to maintain the availability of their species in
nature. The nyalawean tradition is an activity to capture amphidromous fish larvae and
yuwana that recruit from the sea to the river. This tradition is carried out collectively every 2-
8 days before entering the new moon phase (Pasisingi and Abdullah 2018; Simanjuntak et al.
2021). The time span chosen is also related to the dark moon phase that occurs. Larvae and
juveniles of amphidromous fish of the Gobiidae family generally utilize this condition to
avoid predators (Imron et al. 2018). In addition, during the dark moon phase, the light
distribution is minimal, so fish tend to group more and gather in the area of fishermen's lights
(Suhendar et al. 2016).
This tradition will certainly disrupt the recruitment process of larval and juvenile fish
into the Cimaja Estuary and affect its stock population. In previous research, Simanjuntak et
al. (2021) explained that the recruitment of amphidromous fish of the Gobiidae family in the
Cimaja Estuary occurs at 2 times, namely day and night based on the highest tide of sea
water. Cimaja Estuary experiences semi-diurnal tides, namely 2 high tides and 2 low tides in
24 hours. The highest tide in the Cimaja Estuary occurs at 03.00 at night and 15.00 at noon.
Therefore, fishing restrictions can be made by allowing the capture of amphidromous fish
larvae and yuwana on the second tide and prohibiting fishing on the first tide. This is intended
to provide opportunities for some fish to recruit into the estuary to maintain their population
existence.
The third form of management is the implementation of conservation areas. In the
research results, it was explained that Cimaja Estuary has a high value of diversity and
abundance of amphidromous fish of the Gobiidae Family compared to other estuaries in
Palabuhanratu Bay (Baihaqi 2022). This is due to the suitability of habitat conditions for
fishes of the Gobiidae Family that carry out recruitment and feeding activities, so it is
necessary to protect the Cimaja Estuary area through its designation as a conservation area.
The conservation area in question is a resource protection and preservation area. The capture
or utilization activities in any way are prohibited or restricted.
This management strategy of limiting fishing time and establishing conservation areas
can be applied as well as local culture-based resource management, lubuk larangan in North
Sumatra. Widarmanto (2018) argues that lubuk larangan is the establishment of protection
areas and fishing time for fisheries resources that are regulated according to local customary
law. The local customary rule is to leave a river hole for a specified period of time not to be
harvested or caught so that the fish have enough time to breed. If fisheries resources are
caught outside the specified time, village sanctions or customary sanctions will be imposed.
4.1 Conclusion”
Using morphological and molecular approaches, it was found that there were eight
species of amphidromous fish larvae and juveniles of the family Gobiidae that recruited to the
Cimaja Estuary, consisting of Stiphodon elegans, Stiphodon semoni, Sicyopterus sp. 1,
Sicyopterus sp. 2, Sicyopterus sp. 3, Sicyopterus sp. 4, Schismatogobius marmoratus and
Mugilogobius sp. In January, higher abundance of larvae and juveniles was recorded
compared to the other observation months. Furthermore, the diversity of larval and juvenile
fish species that recruited to the Cimaja Estuary was relatively similar between time and
observation stations with the dominant species found being Sicyopterus sp. 2. The stadia
composition obtained in the study consisted of flexion, postflexion, and yuwana.
Most of the fish found utilized benthic microalgae and zoobenthics as their food
source. With the dominant amount utilized, benthic microalgae from the Bacillariophyceae
class. Furthermore, the difference in the main food of larvae and yuwana is that larvae utilize
more Nitzschia species, while yuwana dominantly utilize Surirella and Tabellaria species.
The difference in food composition is influenced by the development of organ readiness.
Thus, the larval fish stage tends to develop a generalist-stenophagic feeding strategy, while
the yuwana stage is specialist-europhagic. The trophic level obtained in larval and juvenile
amphidromous fish of the Gobiidae family ranges from 2.0-2.1 which makes it have a
functional role in the ecosystem as an algivore.
