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Biogeography 14. 51-56. Sep. 20, 2012

Feeding of the tidepool-dwelling goby Pseudogobius masago on an estuarine

Daisuke Okazaki\ Kouki Kanouz', Toshihiro Yokoo3 and Hiroshi Kohnol

1 Laboratory of Ichthyology, Faculty of Marine Science, Tokyo University of Marine Science and Technology, 4-5-7 Konan, Minato, Tokyo, 108-8477 Japan

2 Center of Environment Studies, Ibaraki University, 1375 Ohu, Itako, Ibaraki, 311-2402 Japan

3 Coastal Research Center, Shimane University, 1060 Nishikawatsu, Matsue, Shimane, 690-8504 Japan

Abstract. To determine dietary preferences and feeding rhythm of the tidepool-dwelling goby Pseudogo- bius masago, we examined contents of 200 specimens (15-24 mm in standard length) collected on a tidal mudflat in the Tama River throughout the diel cycle. Nematodes were the most abundant food items, accounting for 58% of gut contents by volume. Peak feeding occurred at sunset and sunrise, in addition to co- inciding with or high tide. These results suggest that the goby expertly utilizes intertidal prey items including nematodes in relation to diel and tidal cycles.

Key words: Pseudogobius masago, diet, intertidal food, feeding rhythm, tidepool

Introduction Kruck et al., 2009). The goby living in this restricted may have specialized feeding behaviors ex- The goby Pseudogobius masago (Tomiyama, pressed, for example, in dietary preferences and for- 1936) is a small gobiid occurring in the aging rhythms. in Japan, Korea, and Taiwan (Akihito et The dietary items of P. mas ago have been de- al., 2002). It inhabits tide pools and creeks on tidal scribed previously (e.g., Dotu, 1958; Kikuchi & through its juvenile and adult life (Datu, Yamashita, 1992). However, details of food prefer- 1958; Itoh & Mukai, 2007; Uchida et al., 2008). In ences among intertidal dietary items and hourly the Tama River estuary in Tokyo , the goby is feeding rhythms across diel and tidal cycles have one of the most abundant (year-round) in soft- not been examined for the goby. The purpose of this substratum tide pools on tidal mudflats (Okazaki et study was to describe feeding habits of the goby in aI., 2012), although most of the other estuarine relation to (i) food availability in its habitat and (ii) do not use this habitat (Uchida et at., 2008). Several diel and tidal cycles. studies have suggested that shallow pool-dwelling species benefit from extended access to intertidal Materials and Methods foods in sites of low risk (van der Veer & Bergman, 1986; Kneib, 1994; Gibson et al., 2002; Study site The study was conducted in the Tama River estu- ary (35 0 32 ' N, 139 0 46 ' E) located on the west- *Corresponding author: [email protected] ern of Tokyo Bay, central Japan. The estuary

- 51 - Feeding ecology of Pseudogobius masago experiences semidiurnal with amplitudes of Gut content analyses up to approximately 2 m. The tidal from the A total of 200 specimens (20 individuals at each bay flows along the estuary at flood tide. The effect sampling time) of P. masago were selected randomly of freshwater inflows is significant during low tide. from the netted samples. Standard length (SL) mea- The study site was located on a tidal mudflat ap- sured with digital calipers ranged from lS.3 to 23.7 proximately 3.S km from the . Uchida mm (mean ± SD, 19.5 ± I.S mm). There were no et ai. (200S) have provided a map of the study site. significant difference in SL among sampling times

The was about 6S-90 m wide at (one-way ANOVA, Fs.l7l =1.3, P=0.23). Subsequent- tide; it was covered by a muddy sediment ly, the deep UN" shaped gut was removed from each containing about 1O-2S% silty clay «63 IJ. m di- specimen under a binocular microscope. Because ameter) per unit dry weight. The high-tide zone (>SO the stomach was very small, we examined contents cm elevation above the low water level at ordinary included those occurring as far as the first bend of spring tide) on the mudflats had numerous tide pools the gut. Food items in the gut tract of each fish were J (-3S0 ha- ). The pools may be naturally occurring identified (major taxonomic categories) and prey depressions, or they may also have been created by in the gut of each fish were counted. The elasmobranch rays or by human such as percentage volume of each food item in the diet was bait collection. Most of the tide pools were small «4 visually estimated as follows: gut contents were m\ ovoid or irregular in shape, and shallow «S cm squashed on a 1 x 1 mm gridded slide to a uniform maximum depth). There was no rooted macrophyte depth of 0.2-1.0 mm and the volume occupied by vegetation or cobbles. each item was measured. The latter was then divided by the total volume of the gut contents to calculate Fish sampling the percentage volume of that item in the diet. Food We made collections over a 2S-h sampling use was expressed as the mean percent- period through the diel and tidal cycles on 12 and age composition of each item by volume (%V), 13 May 2009, when there was a dense population of which was calculated by dividing the sum total of Pseudogobius masago in soft-substratum tide pools. individual volumetric percentages for the item by The sampling interval was about 3 h, starting at the number of specimens examined (Horinouchi & 13:00 and continuing until 16:30 the next day. In Sano, 2000). The frequency of occurrence (%F) was each of low tide, flood tide, and ebb tide, three tide- also calculated for each item. The vacuity index (VI) 2 pools «2 m ) were randomly selected from the high- was calculated as follows: tide zone. All of the fish visible in each tidepool were VI = (number of specimens with empty guts / caught with a dip net (1S cm wide x 12 cm deep, total number of specimens) x 100 mesh size 1 mm); the net was then used to sweep Because the assumptions of parametric statisti- the entire area of the pool until no more fish were cal analysis were not met even after transformation, taken in three consecutive sweeps, in accordance the non-parametric Kruskal-Wallis test was used to with the methods of Meager et ai. (200S). At high detect differences in gut-content volume across sam- tide, fish were collected from the intertidal mudflat pling times. If differences were significant (P < O.OS), area (the same area that fish sampling was conducted all possible pairs of means were compared using a at low tide, flood tide, and ebb tide) because it was nonparametric Tukey-type post hoc test (Zar, 2010). entirely submerged and the pools were not discern- able. During the sampling period, and water Prey and feeding selectivity ranged from 7-13 and 20.S-29.7" C, re- The abundances of prey animals associated with spectively. All samples were placed on ice and fixed the tide pool substratum were also estimated because in 10% formalin in the field. active of P. masago targeted mainly epi-

- S2- Daisuke Okazaki, Kouki Kanou, Toshihiro Yokoo, Hiroshi Kohno benthic and infaunal prey. Using a cylindrical core ronment. Vanderploeg & Scavia' s relativized e1ec- sampler (9 cm in diameter), a l50-cm3 volume of tivity index (E) (Vanderploeg & Scavia, 1979) was sediment was taken from each of three tide pools calculated as (the same pools that the goby were caught) at each low tide across the study period. Immediately after Wi = (R/P;) / L (R/P;) collection, each sample was fixed in 5% buffered E = [W;-(lIN)] / [W;+(lIN)] formalin. Larger prey animals, such as errant and sedentary polychaetes, were removed by initial sort- where R i = proportion of food item in the diet; Pi ing using a 0.5 mm mesh sieve, and the remaining = proportion of food item in the environment; and N animals, including harpacticoid copepods and nema- = number of kinds of food items. E values range be- todes, were then extracted by decantation through tween + 1 and - 1; values> + 0.3 indicate positive a 0.1 mm-mesh conical net (Yamanishi, 1979). selection of prey items. Nematodes, sedentary and errant polychaetes, and harpacticoid copepods within each sample, which Results were the main food items of the goby in the present study, were counted under a binocular microscope. Of the 200 specimens examined, 177 had food The densities of prey animals in each core sample items in their guts and 23 were empty (VI = 11.5). were calculated as the mean number of individuals Across samples, the major food items were benthic 3 per 150 cm • nematodes, sedentary and errant polychaetes, and Feeding selectivity of the goby was determined harpacticoid copepods; these categories accounted using gut contents and prey abundances in the envi- for 89.1 % of gut contents by volume (Table 1). The

Table.! Percentage volume (%V) and percentage frequency (%F) of food items in the diet of Pseudogobius masago in mudflat tidepools in the Tama River estuary.

Food items %V %F Calanoid and cyclopoid copepods 3.2 16.3 Benthic crustaceans Harpacticoid copepods 6.8 42.5 Cumaceans 0.1 0.5 Unidentified materials 1.9 5.4 Polychaetes Errant polychaetes 10.2 17.9 Sedentary polychaetes 14.5 35.0 Insects Chironomid larvae 0.5 0.6 Nematodes 57.6 89.6 Fish 3.5 4.4 Fish scales 1.7 3.9 Number of fish examined 200 Number of fish with no food 177 Vacuity index 11.5

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Table.2. Mean numbers (±SD) of major benthic prey taxa in the environment and in the gut contents of Pseu- dogobius masago in mudflat tidepools in the Tama River estuary, and the E values calculated using those data.

Prey animals Environment Gut content E No.l150cm 3 (%) No.lfish (%) Harpacticoid copepods 1.0 (0.1) 0.03 0.7(0.4) 1.88 +0.58 Errant polychaetes 17.7 (2.4) 0.59 0.2(0.3) 0.54 -0.90 Sedentary polychaetes 22.7 (7.6) 0.76 0.7(0.6) 1.88 -0.74 Nematodes 2956.7 (342.5) 98.65 35.6(37.4) 95.69 -0.90 four food items were frequently found (17.9-89.6%F; values indicate that gobies positively selected only Table 1). harpacticoid copepods among the four animals (Table Of the major prey items, nematodes were the 2). most abundant animals in the environment, occur- The diel change in VI is shown in Fig. 1a. VI ring at a density of 2,956.7/150 cm3 (98.65% of total values ranged from 0 to 45.0, with the highest value major prey numbers), followed by sedentary occurring near midnight (01:00). polychaetes (0.76%), errant polychaetes (0.59%), Kruskal-Wallis tests demonstrated that gut- and harpacticoid copepods (0.03%) (Table 2). The E content volume differed significantly among times of day (Fig. 1b; H = 63.56, P < 0.001). The highest 3 value (ca.1.9 mm ) occurred at sunset (17:20) on 60 (a) x 12 May and decreased gradually thereafter through C1l ] 40 midnight (Tukey-type post hoc test; all P < 0.05). A » :1: secondary peak in gut content volume occurred im- 20 mediately after sunrise (06:20) on the next day. The >'" o first peak in goby feeding at sunset coincided with M' flood tide, but the secondary peak of feeding at sun- l (b) rise coincided with high tide. §" 2 a > Discussion I o o At the tidal mudflat area in Tama River estuary, o 0 I__ __ ..__ .. Pseudogobius masago ate mainly nematodes, seden- tary and errant polychaetes, and harpacticoid cope- pods. In contrast, Datu (1958) reported that the goby 12:00 16:00 00:00 06:00 12:00 18:00 12 May 13 May feed mainly on containing harpacticoid co- Time (h) pepods in Tatara River estuary, Fukuoka Prefecture (southern Japan). Furthermore, the goby on a tidal Fig.l. Diel changes in vacuity index (a) and volume of gut contents (b) of Pseudogobius masago collected from mudflat in Amakusa, Kumamoto Prefecture (south- tidepools on a tidal mudfl at in the Tama River estuary, ern Japan) are primarily benthic crustacean feeders, Tokyo Bay in the period 12-13 May 2009. Bars in taking mostly harpacticoid copepods (Kikuchi & (b) indicate standard errors. Water height (WH) above low water level of ordinary spring tides and the phase Yamashita, 1992). As is the case for other coastal of tide (E, ebb tide; F, flood tide; H, high tide; L, Jow and estuarine fish species (e.g., Horinouchi & Sano, tide) during the sampling period are presented in the lowermost panel; horizontal gray bars indicate night- 2000; Kanou et ai., 2004), these differences in food time. item rankings may be related partly to differences in

-54 - Daisuke Okazaki, Kouki Kanou, Toshihiro Yokoo, Hiroshi Kohno food availabilities among different localities. pertly utilizes intertidal prey items including nema- In the present study, nematodes and sedentary todes in relation to diel and tidal cycles. However, and errant polychaetes were the most important our sampling design was unable to separate diel and prey items for P. masago; these food items occurred tidal effects on peak feeding of P. masago. To as- abundantly in the goby habitat. However, the fish did certain complex mechanisms that determine feeding not make positive selections for these prey items; rhythm of the goby throughout diel and tidal cycles, there was positive selection only for harpacticoid further experimental studies under field condition, copepods, which were scarce in the sediments. Such including information for predation pressure and selectivity in taking prey animals may have resulted prey availability, will be required. from the generally closer proximity of harpacticoid copepods to the sediment surface in comparison with Acknowledgments infaunal species like nematodes and polychaetes. Schlacher & Wooldridge (1996) also reported that in We are grateful to Y Hoshino (Tokyo University sparid juveniles, foraging is selective for epibenthic of Marine Science and Technology) for assistance in animals rather than infaunal species. fieldwork. We thank M. Moteki (Tokyo University Nematodes are generally considered to be one of of Marine Science and Technology) and Ohta fisher- the most abundant species in sediments men' s cooperative association for their support dur- of estuarine mudflats; diversities and abundances ing this investigation. We also thank M. Horinouchi in the intertidal zone exceed those in the sublittoral (Shimane University) and two anonymous referees (Smol et al., 1994). Nematodes are utilized by preda- for valuable comments. tory such as (Reise, 1985; Couch, 1989; Kneib, 1997). Furthermore, KrUck et al. (2009) References demonstrated that sillaginid juveniles utilize nema- todes over restricted tide periods at pools on tidal Akihito, Sakamoto, K, Ikeda, Y & Sugiyama, K., flat in Moreton Bay, Australia. However, specialist 2002. Gobioidei. In Nakabo, T. (Ed), Fishes of feeding on nematodes, as found in P. masago during Japan with pictorial Keys to the Species, English this study, has not been reported previously among edn: 1139-1310. Tokai University Press, Tokyo. resident fishes on estuarine mudflats (e.g., Kanou et Couch, C. A. , 1989. Carbon and nitrogen isotopes al.,2004). of meiobenthos and their food resources. Estuar. High relative feeding rates during twilight hours . Shelf Sci., 28: 433-441. (dusk and/or dawn) around sunset and sunrise have del Norte-Campos, A. G. C. & Temming, A., 1994. been demonstrated in several visually foraging Daily activity, feeding and rations in gobies and goby species (Villiers, 1982; del Norte-Campos & brown shrimp in the northern Wadden . Mar. Temming, 1994; Kanou et al., 2005). Hesthagen Ecol. Prog. Ser., 115: 41-53. (1976) pointed out that during twilight hours, the Dotu, Y, 1958. The life history of the gobioid fish, goby, Gobius niger, is less vulnerable to predators, Acentrogobius masago (Tomiyama). Sci. Bull. although still able to seek prey visually. On the con- Fac. Agr. Kyushu Univ., 16: 359-370 (in Japanese trary, Healey (1971) observed peak feeding in the with English abstract). goby Pomatoschistus minutus in the Ythan Estuary Gibson, R. N., Robb, L., Wennhage, H. & Burrows, in Scotland to be at high tide. Such may be related M. T., 2002. Ontogenetic changes in depth distri- partly to tidal activities of prey animals. During this bution of juvenile flatfishes in relation to preda- study, peak feeding of P. masago occUlTed at sunset tion risk and temperature on a shallow water nurs- and sunrise, in addition to coinciding with flood tide ery ground. Mar. Ecol. Prog. Ser., 229: 233-244. or high tide. These results suggest that the goby ex- Healey, M. C., 1971. The distribution and abundance

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