Bull Mar Sci. 96(3):487–500. 2020 research paper https://doi.org/10.5343/bms.2018.0067
Variation in diet composition of the mudskipper, Periophthalmodon septemradiatus, from Hau River, Vietnam
1 Department of Biology, Quang Minh Dinh 1 * School of Education, Can Tho Lam Thanh Tran 2 University, 3/2 Street, Xuan 3 Khanh Ward, Ninh Kieu District, Tuyet Thi Minh Tran Can Tho 900000, Vietnam Diem Kieu To 1 2 Bac Lieu University, Bac Lieu Tien Thi Kieu Nguyen 4 City, Bac Lieu 960000, Vietnam Dinh Dac Tran 5 3 Centre for Continuing Education of Soc Trang Province, Soc Trang 950000, Vietnam ABSTRACT.—Periophthalmodon septemradiatus (Hamilton, 4 An Khanh High School, An 1822) is a mudskipper of the Mekong Delta that can be found Khanh Ward, Ninh Kieu District, Can Tho 900000, Vietnam along estuaries and lower reaches of rivers. In the present study, we determined diet and feeding ecology of this species 5 College of Aquaculture and by analyzing the contents within the stomachs of 1360 Fisheries, Can Tho University, 3/2 fish samples collected from August 2017 to July 2018. Data Street, Xuan Khanh Ward, Ninh Kieu District, Can Tho 900000, analysis suggested that P. septemradiatus is a carnivorous fish. Vietnam We found six main food item categories: small fishes, prawns (Acetes spp.), crabs (Uca spp.), molluscs, ants (Dolichoderus * Corresponding author email: sp.), and detritus. Both males and females at different sizes,
Guest Editor: Amy Y Then Section Editor: Rafael J Araújo
Date Submitted: 2 September, 2018. Date Accepted: 15 March, 2019. Available Online: 28 March, 2019.
Food and feeding ecology are necessary to understand fish biology and trophic interactions among species in a fish community (Brodeur and Pearcy 1992, Wootton 1996, Blaber 2000). Diet composition can vary according to fish size, season, and habitat (Aarnio and Bonsdor 1993, Carman et al. 2006, Brush et al. 2012). This vari- ation is driven by fish foraging behavior and food availability (Dinh et al. 2017b). Knowledge on diet and feeding ecology is limited for some gobiid species in the Mekong Delta, where they have been overfished (Trinh and Tran 2012). Therefore, it is crucial to study the feeding ecology of gobiid species in the Mekong Delta, which can be used for fishery assessment and fish population conservation.
Bulletin of Marine Science 487 © 2020 Rosenstiel School of Marine & Atmospheric Science of the University of Miami 488 Bulletin of Marine Science. Vol 96, No 3. 2020
Figure 1. The sampling map in the Mekong Delta. Arrowhead: Sampling area: (1) Long Duc–Soc Trang, (2) An Lac Tay–Soc Trang, (3) Phu Thu–Can Tho, (4) Tan Hung–Can Tho, and (5) Binh Duc–An Giang.
Periophthalmodon is a genus of the subfamily Oxudercinae (Gobiidae) that contains three species including Periophthalmodon freycineti (Quoy and Gaimard, 1824), Periophthalmodon schlosseri (Pallas, 1770), and Periophthalmodon septemradiatus (Hamilton, 1822) (Murdy 1989, 2011, Murdy and Jaafar 2017). However, only P. schlosseri and P. septemradiatus are recorded in Vietnam (Tran et al. 2013). Periophthalmodon septemratidatus is a burrowing and amphibious fish (Martin and Bridges 1999), and is widely distributed in the mangrove swamps and mudflat areas of eastern India, Bangladesh, Myanmar, Thailand, Malaysia, Singapore, Indonesia, and Vietnam (Murdy 1989, 2011, Murdy and Jaafar 2017). The mudskipper P. septemradiatus population has recently declined due to various factors including urbanization, environmental pollution, and climate change (Dinh et al. 2018). However, knowledge of biological characteristics and trophic interactions of this species is not sufficient to build efficient conservation strategies. This study provides knowledge of diet and feeding ecology of male and female P. septemradiatus of different sizes, and in different seasons and habitats. Dinh et al.: Diet of Periophthalmodon septemradiatus 489
Materials and Methods
Study Sites.—We conducted the present study from August 2017 to July 2018 in muddy regions of tributaries of Hau River including Long Duc–Soc Trang (LD; 9°42´55.4˝N, 106°04´28.4˝E), An Lac Tay–Soc Trang (ALT; 9°49´52.4˝N, 105°59´44.5˝E), Phu Thu–Can Tho (PT; 9°59´45.06˝N, 105°48´22.73˝E), Tan Hung– Can Tho (TH; 10°12´07.17˝N, 105°34´43.89˝E), and Binh Duc–An Giang (BD; 10°24´03.54˝N, 105°25´10.82˝E; Fig. 1). Dinh et al. (2018) reported that silt, clay, sand, and organic matter characterizes the mudflat of these five regions. The distance from the river bank to the riverbed of the mudflat was about 2.5 m at the lowest tide for all sites; however, the vegetation in each site differed as follows: the vegetation in LD consisted mainly of the mangrove apple, Sonneratia caseolaris (L.) Engl., and the mangrove palm, Nypa fruticans Wurmb. The slopes of the river bank at this site were approximately 25°. ALT’s vegetation was predominantly S. caseolaris, N. fruticans, and the water trumpet, Cryptocoryne ciliata (Roxb.) Fischer ex Wydler. The slope of the river bank in ALT was also approximately 25°. Because PT was near industrial zones, none of the predominant plants were found in PT’s vegetation. Much like LD and ALT, the slope of the river bank at PT was approximately 25°. The vegetation in TH consisted mostly of the canary wood, Nauclea orientalis (L.) L., and S. caseolaris. The slope of the river banks in TH was approximately 45°. The vegetation in BD con- sisted mostly of N. orientalis, but we did not find S. caseolaris at this location. The slopes of the river bank in BD were also approximately 45°. At these five study sites, there are typically two seasons, including a dry season with little precipitation (January–May) and a wet season with roughly 400 mm pre- cipitation per month (June–December). The mean annual temperature in this region is approximately 27 °C. The tidal amplitude in our study locations is semidiurnal (Le et al. 2006).
Fish Collection.—As fish usually appeared on the mudflat surface at low tide, we used fishing rods to obtain fish specimens of different sizes during low tides. We collected fish for roughly 3 hrs, which coincided with the ebb tide in all five sites. At each site, we chose an area of 30 m2 (15 m along the river bank and 2 m from the river bank to the riverbed) to collect fish monthly. Every field campaign lasted 5 d (1 d per sampling site). After fish collection, we used the external description of Khaironizam and Norma-Rashid (2003) to identify the fish. We used external morphology and genital papilla to differentiate sexes; e.g., the dorsal fin of males was longer, larger, and more colorful than that of females, but the genital papilla of males was smaller and whiter than that of females (Dinh et al. 2018). We fixed specimens in 5% formalin before transport to the laboratory. For fish conservation purposes, we released fish at juvenile stages (e.g., those with total length was <5.0 cm) and at sexual maturation stage (e.g., those with a big abdomen and red genital area, which were about to release gametes) back to their habitat after measuring them.
Diet Composition Analyses.—In the laboratory, we determined fish total length (TL, 0.1 cm) and weight (W, 0.01 g), then we dissected the specimens to re- move the gastrointestinal tract. Next, we examined stomach content to determine diet composition. We used a stereomicroscope and Nguyen et al. (2013) to identify to the lowest possible taxonomic level. Finally, stomach contents were quantified by 490 Bulletin of Marine Science. Vol 96, No 3. 2020
prey occurrence in fish stomach (%Oi = 100 × Oi/N, where Oi is the number of fish consuming prey i and N is the total number of fish examined; Hynes 1950) and the gravimetric method (%Wi = 100 × Wi/Wtotal, where, Wi is weight of prey i, Wtotal is to- tal weight of all prey individuals; Hyslop 1980). Dietary composition was quantified using a combined analysis of prey occurrence and weight, also known as biovolume, preponderance index, or point of prey, and was calculated as %Vi = (100 × Oi × Wi)/
Σ(Oi × Wi), where Vi, Oi, and Wi are the percentage of biovolume, occurrence, and weight of prey i respectively. We used the biovolume value to test if diet composition varied by sex, fish size, season, and site (Natarajan and Jhingran 1961, Hyslop 1980).
Feeding Strategy Analysis.—Amundsen et al. (1996) modified the Costello (1990) graphical method. We used this method to plot the percentage of biovolume vs frequency occurrence of food items to determine diet specialization (e.g., feeding strategy) and prey importance. With this graph, the most important prey items are closer to the top right corner and the prey items, which occur at low level but have important roles, are closer to the top left corner. The least important prey items are closer to the low left corner, and the prey items with high level but least important are closer to the low right corner (Adámek et al. 2007).
Data Analysis.—We used a permutational multivariate analysis of vari- ance (PERMANOVA) using PRIMER v6.1.11 (Clarke and Gorley 2006) with the PERMANOVA+ v1.0.1 add-on package (Anderson et al. 2008) to analyze the bio- volume of all food items to compare diet composition according to sex, size, season, and site (Baeck et al. 2013). If diet composition was significantly different among the above groupings, we would use nonparametric tests to confirm which prey con- tributed to the difference (Dinh et al. 2017b). Accordingly, differences in food com- position between sexes or seasons was investigated using a Mann–Whitney U test. Food items that contributed to the variation of food composition among fish sizes or sites was quantified by the Kruskal–Wallis test. Fish size was divided using the function (TLmax – TLmin)/log10n, where TLmax is the maximum fish total length, TLmin is the minimum fish total length; and n is number of fish collection (Wand 1997). Consequently, four size categories emerged including group 1 (TL < 5.1 cm), group 2 (TL = 5.1–9.0 cm), group 3 (TL = 9.1–11.0 cm), and group 4 (TL > 11.0 cm). We used the χ2 test to investigate if the proportion of empty stomachs differed between wet and dry seasons using SPSS v21. The significance level in all tests was set at P < 0.05. We also performed the Benjamini–Hochberg procedure to lessen the Type I error (Benjamini and Hochberg 1995, McDonald 2014).
Results
General Diet Composition of Periophthalmodon septemradiatus.—A total of 1504 fish, including 930 males and 574 females, were sampled from Hau River (Table 1). There were 1360 fish with stomach contents (874 males and 486 females; Table 1). We identified six main dietary categories: small fishes, shrimps (Acetes spp.), molluscs, crabs (Uca spp.), ants (Dolichoderus sp.), and detritus (Table 2). The occurrence frequency analysis revealed that the mudskipper ingested pri- marily Dolichoderus sp. (68.9%), followed by detritus (30.4%; Table 2). According to prey weight analysis, Dolichoderus sp. and detritus accounted for 60.0% and 26.2% Dinh et al.: Diet of Periophthalmodon septemradiatus 491 F 0.0 0.0 5.3 0.0 0.0 0.0 28.6 50.0 58.3 40.0 20.0 20.0 16.1 empty 0.0 0.0 0.0 0.0 0.0 0.0 0.0 5.6 M Fish with 16.7 12.5 66.7 50.0 21.4 stomach (%) 7 7 2 7 5 6 6 F 11 12 10 19 10 112 Binh Duc–An Giang 6 8 3 9 6 12 16 14 20 24 13 10 M Total fish Total 234 F 6.3 0.0 0.0 0.0 0.0 0.0 0.0 0.0 0.0 4.8 14.3 36.4 14.3 empty 0.0 0.0 0.0 0.0 0.0 0.0 0.0 6.1 M Fish with 27.3 15.4 25.0 33.3 20.0 stomach (%) 5 3 4 2 9 3 7 7 F 11 16 13 13 146 Tan Hung–Can Tho Tan 5 4 8 9 11 13 15 12 15 17 20 18 M Total fish Total 212 F 0.0 0.0 0.0 0.0 0.0 0.0 0.0 0.0 4.3 6.6 37.5 20.0 20.0 empty M Fish with 3.6 0.0 0.0 0.0 0.0 0.0 0.0 0.0 0.0 0.0 0.0 0.0 0.5 stomach (%) M: males and F: females 4 6 8 3 3 F 11 10 13 10 20 10 23 121 Phu Thu–Can Tho 4 11 28 10 14 19 14 19 12 30 17 18 M Total fish Total 196 F 0.0 0.0 0.0 0.0 0.0 0.0 0.0 0.0 11.8 62.2 10.0 16.7 30.1 empty 0.0 0.0 0.0 0.0 0.0 6.3 4.0 4.2 5.0 0.0 7.5 M Fish with 13.0 22.2 stomach (%) collected from five study sites. 3 5 9 6 9 F 37 16 10 10 12 17 12 93 7 23 28 14 13 10 16 25 24 20 14 18 An Lac Tay–Soc Trang An Tay–Soc Lac M Total fish Total 147 F 0.0 0.0 0.0 0.0 10.0 57.1 25.0 18.8 27.3 14.3 20.0 92.3 26.5 empty 0.0 9.1 0.0 8.3 0.0 0.0 0.0 5.3 M Fish with 14.6 33.3 15.4 20.0 12.8 stomach (%) 7 4 7 2 7 F 11 10 13 16 10 12 13 102 Periophthalmodon septemradiatus Long Duc–Soc Trang 11 41 12 22 13 15 13 12 18 30 28 19 M Total fish Total 141 Sample date Table 1. Number of Table Aug 2017 Sep 2017 Oct 2017 Nov 2017 Dec 2017 Jan 2018 Feb 2018 Mar 2018 Apr 2018 May 2018 Jun 2018 Jul 2018 Total 492 Bulletin of Marine Science. Vol 96, No 3. 2020
Table 2. Percentage of the frequency of occurrence, weight, and biovolume of food items of Periophthalmodon septemradiatus.
Occurrence Weight Biovolume Food Male Female All fish Male Female All fish Male Female All fish Small fishes 0.98 0.19 0.71 0.56 0.07 0.39 0.01 0.00 0.01 Acetes spp. 0.69 1.29 0.90 0.54 1.15 0.75 0.01 0.03 0.02 Molluscs 7.79 7.75 7.78 5.12 6.46 5.57 0.91 1.15 0.99 Uca spp. 4.04 3.32 3.79 8.03 5.25 7.09 0.74 0.40 0.61 Dolichoderus sp. 59.27 61.99 60.22 61.74 56.56 60.00 83.43 80.56 82.46 Detritus 27.22 25.46 26.60 24.01 30.51 26.20 14.90 17.85 15.91 of fish diet composition, respectively (Table 2). Based on prey biovolume analysis, the mudskipper ingested predominantly Dolichoderus sp. (82.5%), followed by detri- tus (15.9%; Table 2). This mudskipper also rarely consumed small fishes,Acetes spp., molluscs, and Uca spp.
Diet Composition in Males and Females of Different Sizes, Seasons, and Study Sites.—Occurrence, weight, and biovolume of food item analyses revealed that both male and female P. septemradiatus of different sizes, in different seasons, and at different sites consumed predominantly Dolichoderus sp., followed by detritus (Tables 2–5). Periophthalmodon septemradiatus diet composition did not vary by sex (PERMANOVA: Pseudo-F = 0.41, P = 0.656; Table 2), but varied with fish size (Pseudo-F = 5.17, P = 0.001; Table 3), season (Pseudo-F = 44.99, P = 0.001; Table 4), and site (Pseudo-F = 5.32, P = 0.001; Table 5). Diet composition of fish group 1 was significantly different from fish group t2 ( = 2.72, P = 0.0053) and fish group 3 t( = 3.79, P = 0.001; Table 3). The diet composition of fish in PT was significantly different from LD (t = 4.14, P = 0.01), ALT (t = 2.17, P = 0.022), TH (t = 2.14, P = 0.017), and BD (t = 3.59, P = 0.01; Table 5). Variation of diet composition of different fish sizes was regulated by Uca spp. (Kruskal Wallis H: χ2 = 10.99, P = 0.012), Dolichoderus sp. (χ2 = 23.13, P < 0.001), and detritus (χ2= 36.91, P < 0.001). The difference in fish food -com position between dry and wet seasons was influenced by Uca spp. (Mann–Whitney U = 2.56, P = 0.010), Dolichoderus sp. (U = 7.02, P < 0.001), and detritus (U = 6.37, P < 0.001). Change in diet composition of P. septemradiatus among the five sites was dominated by Dolichoderus sp. (Kruskal Wallis: χ2 = 27.95, P < 0.001), and detritus (χ2 = 22.27, P = 0.001).
Feeding Strategy.—The Costello graphic analysis of the relationship between occurrence and weight of preys showed that P. septemradiatus was a specific feeder, which consumed mainly Dolichoderus sp. and detritus (Fig. 2). Likewise, both males and females in the four fish groups in both dry and wet seasons at all sites showed that P. septemradiatus fed mainly on Dolichoderus sp., followed by detritus (Online Figs. 1–4).
Discussion
The mudskipper P. septemradiatus is predominantely a carnivorous fish, with a high proportion of fauna in its diet. In countries, such as Cambodia, India, Laos, Thailand, and Vietnam (Cuc and Van Mele 1999, Dill 2002), the mudskipper’s main Dinh et al.: Diet of Periophthalmodon septemradiatus 493 = 2.10, P 0.551 = 2.10, P 0.551 = 0.56, P 0.905 = 36.91, P < 0.001 2 2 2 = 10.99, P 0.012 = 23.13, P < 0.001 2 Kruskal–Wallis test Kruskal–Wallis χ χ χ 2 2 χ χ χ 0.14 0.26 5.41 0.06 81.20 12.93 Group 4 Biovolume 0.01 1.01 1.08 0.00 76.69 21.21 Group 3 0.00 1.02 0.27 0.04 81.72 16.96 Group 2 in different fish sizes (total length, TL). Group 1: TL < TL TL). Group 1: fish sizes (total length, in different 0.00 0.99 0.22 5.33 0.01 93.44 Group 1 2.66 1.58 1.14 24.91 49.85 19.85 Group 4 0.28 5.62 8.09 0.01 58.17 27.83 Group 3 Periophthalmodon septemradiatus Weight 0.20 5.94 4.55 1.50 59.85 27.97 Group 2 0.49 5.94 3.65 0.80 73.96 15.17 Group 1 2.27 6.82 9.09 2.27 68.18 27.27 Group 4 1.01 8.79 6.53 0.50 64.32 37.19 Group 3 Occurrence 0.78 8.62 2.98 1.25 68.81 30.56 Group 2 0.36 3.57 1.07 10.00 75.71 21.07 Group 1 spp. Small fishes Acetes Molluscs Uca spp. Dolichoderus sp. Detritus Table 3. Percentage of the occurrence, weight, and biovolume food items Table cm > 11.0 TL cm, and Group 4: = 9.1–11.0 TL = 5.1–9.0 cm, Group 3: TL 5.1 cm, Group 2: Food 494 Bulletin of Marine Science. Vol 96, No 3. 2020
Table 4. Percentage of the occurrence, weight, and biovolume of food items of Periophthalmodon septemradiatus in the dry and wet seasons.
Occurrence Weight Biovolume Food Dry Wet Dry Wet Dry Wet Mann–Whitney U test Small fishes 0.34 1.16 0.28 0.51 0.00 0.01 U = 1.68, P = 0.093 Acetes spp. 0.68 1.29 0.19 1.31 0.00 0.04 U = 1.11, P = 0.265 Molluscs 7.16 10.22 4.20 6.95 0.54 1.52 U = 1.86, P = 0.064 Uca spp. 5.96 3.10 8.31 5.86 0.89 0.39 U = 2.56, P = 0.010 Dolichoderus sp. 77.17 62.61 66.11 53.82 91.25 71.98 U = 7.02, P < 0.001 Detritus 19.59 38.68 20.91 31.55 7.33 26.07 U = 6.37, P < 0.001 prey, Dolichoderus sp., is common everywhere, frequently nests in mangrove forests, and moves around on mud to search for food. Detritus is the second item in diet composition, which can be explained by P. septemradiatus’ feeding activity on mud. The same feeding pattern was also shown in a study in the Navinal coast, India (Bhatt et al. 2009). Similarly, feeding on mud was also found in Boleophthalmus boddarti (Pallas, 1770) (Clayton and Vaughan 1988, Clayton and Wright 1989). Periophthalmodon septemradiatus rarely ingested small fish,Acetes spp., Uca spp., and molluscs, as shown by the lowest percentage of these prey items in its diet. In contrast, the mudskipper P. schlosseri in Malaysian waters is also a carnivore; however, it feeds mainly on Uca spp. (Zulkifli et al. 2012). Another species, Periophthalmus waltoni Koumans, 1941 from the northwest Arabian Gulf is also a carnivore feeding mainly on copepods and fishes (Barak 1994). In mangroves of Chwaka Bay and Mtoni, Tanzania, Periophthalmus argentilineatus Valenciennes, 1837 is also a carnivore and feeds mainly on polychaetes and crabs (Nanjo et al. 2008). The gobies, Oxyeleotris urophthalmus (Bleeker, 1851) (Vo and Tran 2014) and Eleotris melanosoma Bleeker, 1852 (Dinh et al. 2017a), living in the Mekong Delta are also carnivores, consuming mainly decapods. By contrast, diatoms are the primary food item of Boleophthalmus pectinirostris (Linnaeus, 1758) (Yang et al. 2003) and B. boddarti (Ravi 2013, Dinh 2015), which are also omnivores. The gobies, Pseudapocryptes elongatus (Cuvier, 1816) (Tran 2008), Parapocryptes serperaster (Richardson, 1846) (Dinh et al. 2017b), and Stigmatogobius pleurostigma (Bleeker, 1849) (Dinh and Tran 2018), are omnivores, but ingest primarily detritus. Variations in the diet of these gobies suggest that fish diet composition is species-specific. Food consumption of P. septemradiatus did not vary with sex. Likewise, the diet composition of male B. boddarti, living in mudflats of the Mekong Delta, was similar to the diet of females (Dinh 2015). Ravi (2013) indicated that the gut contents of B. boddarti from Pichavaram mangroves on the southeast coast of India varied between males and females. Similarly, the diet of P. barbarus (Linnaeus, 1766) from the Imo estuary, Nigeria, varied by sex, as males ingested more cyanobacteria, Coscinodiscus spp. and Sesarma spp., than did females (Udo 2002a). The mudskipper P. schlosseri, living on the intertidal mudflats of the Puloh River in Malaysia, also had differences in diet composition, as male diet was predominantly composed of Uca spp., whereas females consumed primarily Oryzias sp. (Zulkifli et al. 2012). We also observed that, similar to P. serperaster (Dinh et al. 2017b), increasing body size resulted in differences in diet composition of P. septemradiatus. Larger mudskippers preferred to prey on Uca spp., whereas the smaller fish preferred to prey on Dolichoderus sp. Similarly, the diet of P. waltoni from Khor Al Zubair, Iraq, Dinh et al.: Diet of Periophthalmodon septemradiatus 495 = 2.94, P 0.568 = 2.34, P 0.673 = 4.81, P 0.307 = 1.14, P 0.888 2 2 2 2 = 27.95, P < 0.001 = 22.27, P < 0.001 χ χ χ χ 2 2 Kruskal–Wallis test Kruskal–Wallis χ χ 0.03 0.48 0.71 0.02 BD 72.23 26.54 0.02 1.65 0.48 0.01 Biovolume TH 84.04 13.81 PT 0.00 0.72 0.49 8.68 0.00 90.12 0.01 1.34 1.06 0.05 ALT 83.37 14.18 0.00 1.01 0.43 0.02 LD 75.60 22.93 0.84 3.87 7.59 0.70 BD 54.95 32.05 0.56 7.21 5.80 0.64 TH 62.54 23.24 at different sites. LD: Long Duc–Soc Trang, Trang, Long Duc–Soc LD: sites. different septemradiatus at Periophthalmodon PT 0.01 4.39 6.68 0.15 66.05 22.72 Weight 0.40 7.00 9.82 1.50 ALT 57.03 24.25 0.17 5.81 5.66 1.03 LD 57.13 30.21 1.42 5.66 4.25 1.42 BD 59.91 37.74 1.36 4.09 0.45 TH 11.36 66.82 29.55 PT 0.33 9.45 4.23 0.65 79.15 22.15 Occurrence 0.63 9.38 5.31 1.56 ALT 71.88 28.75 0.66 8.31 3.65 1.00 LD 63.12 36.21 spp. Small fishes Acetes Molluscs Uca spp. Dolichoderus sp. Detritus Table 5. Percentage Table of the occurrence, weight, and biovolume of food items of Tho, and BD: Binh Duc–An Giang. Hung–Can Tan TH: Tho, Thu–Can Phu PT: Trang, Tay–Soc An Lac ALT: Food 496 Bulletin of Marine Science. Vol 96, No 3. 2020
Figure 2. The modified Costello graphics represent feeding strategy based on plotting the relationship between percentage of weight and frequency of occurrence of food items for Periophthalmodon septemradiatus (n = 1360). changed with size as smaller individuals consumed mainly copepods, whereas larger ones were piscivorous (Barak 1994). Size-related change in diet composition was also found in P. barbarus living in the mangroves of Imo River estuary, Nigeria (Udo 2002b) and in Rumuolumeni Creek, Niger Delta, Nigeria (Bob-Manuel 2011). The mudskipper P. argentilineatus from the mangrove estuary of the Urauchi River on Iriomote Island in southern Japan also displayed an ontogenetic dietary shift as the adult diet predominantly consisted of Uca spp., whereas polychaetes predominated in the diet of smaller fish (Nanjo et al. 2008). The mudskipper P. argentilineatus from East Africa also displayed the size-related change of diet as amphipods and copepods were the main dietary items in small fish, whereas Uca spp. contributed mainly to the diet composition the larger individuals (Kruitwagen et al. 2010). Juvenile P. schlosseri and adults from Malaysia consumed the same prey groups, but adults consumed more Uca spp. and fewer fishes than juveniles (Zulkifli et al. 2012). Moreover, based on the frequency of occurrence, Ravi (2013) reported that ontogenetic diet change also occurred in B. boddarti from Pichavaram mangroves on the southeast coast of India, attributed to a reduction in diatoms and an increase in nematodes and polychaetes in adults over the values found in juveniles. The high rainfall in the wet season leads to changes in detritus input (Nedeco 1993), possibly resulting in the seasonal shift in diet composition of P. septemradiatus. Likewise, the diet composition of B. dussumieri (Valenciennes, 1837) from the Ulhas River estuary in northwestern India also changed with season as researchers only found fish eggs in premonsoon and the highest intake of nematodes post-monsoon (Mutsaddi and Bal 1969). Rathod and Patil (2009) indicated that diatoms were the main food item for B. dussumieri during the pre-, post-, and during monsoon periods, which ingest nematodes as an alternate food item. In the mangrove forests of the Imo River estuary, Nigeria, P. barbarus consumed primarily detritus during the wet season and mostly algae during the dry season (Udo 2002b). A seasonal change of diet composition is also found in P. barbarus from the mangroves of the New Calabar River, a tributary river in the adjacent Niger Delta, due to a significant increase of Dinh et al.: Diet of Periophthalmodon septemradiatus 497 unidentified crabs, annelids, nematodes, and Penaeus sp. in the gut contents of this species from the wet to the dry seasons (Chukwu and Deekae 2013). In the Pichavaram mangroves, on the southeast coast of India, there is a significant increase in nematodes in the diet composition of B. boddarti from pre- to postmonsoon (Ravi 2013). Fish diet is also regulated by food availability, e.g., P. serperaster mainly ingested diatoms in Malaysia (Khaironizam and Norma-Rashid 2000), but detritus in the Mekong Delta (Dinh et al. 2017b). Similarly, diet composition of P. septemradiatus also changed with habitat due to the differences in proportion ofDolichoderus sp. and detritus in our five sampling sites. There were various plants (e.g., S. caseolaris, C. ciliata, N. fruticans, Ficus benjamina L., Cyperus elatus L., Aglaodorum griffithii (Schott) Schott, Acrostichum aureum L., Colocasia esculenta (L.) Schott, Ficus microcarpa L.f.; but none of them predominant) in PT and lack of S. caseolaris in BD. For P. argentilineatus in Zanzibar, amphipods and copepods contributed mainly to its diet, whereas polychaetes were the main prey items of this species in mainland Tanzania (Kruitwagen et al. 2007). Likewise, fish eggs and nematodes were found in stomach content of B. boddarti in the Pichavaram mangroves on the southeast coast of India (Ravi 2013), but these items were not found in this species in the Mekong Delta in Vietnam (Dinh 2015). According to the modified Costello graphic, P. septemradiatus could be classified as a specific feeder, but capable to adapt its diet in response to different environmental conditions. In contrast, mudskippers sharing habitats with P. septemradiatus such as P. waltoni (Barak 1994), P. barbarus (Udo 2002a,b, Chukwu and Deekae 2013), P. argentilineatus (Kruitwagen et al. 2007), P. elongatus (Tran 2008), P. schlosseri (Zulkifli et al. 2012),B. boddarti (Ravi 2013, Dinh 2015), and P. serperaster (Dinh et al. 2017b), were classified as generalist feeders. In summary, P. septemradiatus tended to be a carnivorous fish. We found six food item categories in diet composition, including small fishes, Acetes spp., Uca spp., molluscs, Dolichoderus sp., and detritus. The species is also a specific feeder, using mainly Dolichoderus sp. and detritus as food constituents. The diet composition did not vary by sex, but varied by fish size, season, and site. These findings contribute to the current literature on food and feeding ecology of this species. The results of the present study might be used to procure suitable diets for the artificial cultivation of the species for fish population conservation.
Acknowledgments
This research is funded by Vietnam National Foundation for Science and Technology Development (NAFOSTED) under grant number 106-NN.05-2016.30.
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