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The mechanisms leading to ontogenetic diet shift in a microcanivore, Pterogobius elapoides (Gobiidae)

The mechanisms leading to ontogenetic diet shift in a microcanivore, Pterogobius elapoides... ECOLOGY & POPULATION BIOLOGY Animal Cells and Systems Vol. 16, No. 4, August 2012, 343349 The mechanisms leading to ontogenetic diet shift in a microcanivore, Pterogobius elapoides (Gobiidae) a b Seung-Ho Choi and Ho Young Suk * a b Department of Animal Resources, National Institute of Biological Resources, Incheon 404-708, Korea; Department of Life Sciences, Yeungnam University, Gyeongsan Gyeongsangbuk-do 712-749, Korea (Received 4 December 2011; received in revised form 27 January 2012; accepted 13 February 2012) A variety of fish species undergo an ontogenetic change in prey selectivity, and several potentially interacting factors, including nutrient requirement, microhabitat change, and foraging ability, may account for the occurrence of the shift. Here we examine the foraging ecology and ontogenetic diet shift of a micro-carnivorous goby, Pterogobius elapoides (serpentine goby), dominant component of fish assemblage in shallow rocky areas off the coast in Korea and Japan. Although most other gobies are primarily benthic carnivores, P. elapoides is a semipelagic fish; however, little is known about how those species change their foraging tactics with growth. In our diet analyses, the most common diet was pelagic copepods and benthic amphipods, and diet shift was observed from pelagic to benthic with growth. The ontogenetic diet shift seems to be the result of the preference for energetically more profitable prey in larger-size classes as well as the results of different prey availability due to among-habitat variation in diet. However, differential food preference does not appear to affect individual scope for searching food. Several factors such as predation pressures and interspecific resource partitioning might contribute to the changes in diet observed among size classes, which were included in our ongoing tests. Keywords: ontogenetic diet shift; foraging behavior; serpentine goby; Pterogobius elapoides; micro-carnivore; Gobiidae Introduction tropical regions (Nelson 2006). Gobies are primarily fish of shallow oceanic habitats including tide pools, A variety of fish species undergo an ontogenetic coral reefs, and sea-grass fields; they are also very change in prey selectivity, that is, from planktivory abundant in brackish water, and a small number of to piscivory (Schmitt and Holbrook 1984; Holbrook gobiid species are also entirely adapted to freshwater et al. 1985; Shibuno et al. 1994; Lockett and Suthers system (Nelson 2006). Although few are valuable as 1998; Graham et al. 2007; Schellelens et al. 2010; food for humans, they are generally of great signifi- Baeck et al. 2011). Many potentially interrelating cance as prey and predator species for commercially factors may account for the occurrence of these shifts important organisms. While the occurrence of onto- (McCormick 1998). Growth-related morphological genetic change in prey selectivity has been reported for differences can lead to differential exploitation of a gobies in several studies (Gibson 1970; Vass et al. food resource and, in turn, changes in microhabitat 1975; Grossman 1980; Grossman et al. 1980; Huh and use, being a function of changing in nutrient require- Kwak 1998a, 1998b, 1999), little is known about how ment (MacNeill and Brandt 1990; Luczkovich et al. those species change their foraging tactics with 1995; Peterson and McIntyre 1998). Likewise, foraging growth. schedule and ability may change with ontogeny, which In this study, we examine the foraging ecology can be compromised with availability and density of of a goby, Pterogobius elapoides (serpentine goby; prey organisms (Clements and Choat 1993; Lukoschek Figure 1), a common component of fish assemblage and McCormick 2001). A thoughtful consideration of in shallow rocky areas off the coast in Korea and how a species exploits its food resource and how that Japan (Masuda et al. 1984; Kim et al. 1986). While changes with growth is prerequisite to any examina- most gobies are benthic carnivores, consuming mainly tion for the pattern and dynamics of species assem- crustaceans and polychaetes (Gibson and Ezzi 1978; blage on temporal and spatial scales (McCormick Grossman et al. 1980; Behrents 1989; Kikuchi 1998). and Yamashita 1992; Aarnio and Bonsdorff 1993; The Gobiid species (gobies), one of the largest Humphries and Potter 1993; Swenson and McCray families of fish with more than 200 genera, are 1996), P. elapoides is a semipelagic fish, seldom settling commonly distributed in temperate, subtropical, and on bottom structure (Do ˘ tu and Tsutsumi 1959). *Corresponding author. Email: hsuk@ynu.ac.kr ISSN 1976-8354 print/ISSN 2151-2485 online # 2012 Korean Society for Integrative Biology http://dx.doi.org/10.1080/19768354.2012.667002 http://www.tandfonline.com 344 S.-H. Choi and H.Y. Suk However, temporal (seasonal) space defense is ob- around 7080 mm in standard length (hereafter SL; served in this species sometimes, but not often, for Do ˘ tu and Tsutsumi 1959). The breeding season of the their benthic feeding territories (personal observation). studied population starts in November and continues P. elapoides is thus expected to undergo distinct well into December. The male builds a nest underneath a pattern of ontogenetic shifts in foraging ecology boulder and provides exclusive paternal care for eggs, from other gobies, even though it has never been which includes fanning and defending the brood until thoroughly investigated. hatching (Do ˘ tu and Tsutsumi 1959). Adult individuals In the present study, we investigated for the first time generally die at the completion of the breeding season. whether diet changes with ontogeny and explored the mechanisms by which partitioning of the food resource occurs among different size classes in P. elapoides. First, Diet analysis the stomach of individuals from different size classes A total of 34 individuals were collected in the study site was dissected open, and the contents inside were using a gill net during the daytime (dates were chosen examined to find differences, if any, in diet taxa. Second, based on the weather condition; 1617 May, 2223 June, information on prey species availability, size-related 17 July, and 6 August in 2000). The captured fishes were feeding mechanics, and microhabitat selectivity was preserved in 10% buffered formalin solution and were used to find the potential factors accounting for the measured to the nearest 0.01 mm by digital calipers. occurrence of the shift. Each individual was allocated into three different size classes: small (5060 mm SL), medium (6170 mm SL), Materials and methods and large ( 70 mm SL). The stomach of each individual was dissected open, and the contents inside Locations and study species were examined under a binocular dissecting microscope. Collections for estimation and observation were carried Prey were removed from the stomach and identified to out on shallow rocky areas off the coast of Kurahashi the lowest taxon feasible. The greatest length or carapace Island (Honmura Bay, the Seto Inland Sea; 3485?14??N, length of all of the individuals was measured to the 132830?0??E) in Japan. P. elapoides is one of the nearest 0.01 mm using an ocular micrometer. Prey dominant inhabitants in our study sites. Many indivi- volume was estimated by measuring the length and duals cruise around boulders and conceal themselves width of each item and calculating its cylindrical or in cracks beneath boulders or inside of brown algae spherical volume, depending on its shape. For each patches to avoid predation (S.-H. Choi, personal ob- sample, the percent composition was calculated in servation). P. elapoides is relatively smaller in size than number and in volume. that of other Pterogobius species. This species exhibit pale brown with six or seven transverse black bands on their body side continuing behind the dorsal and anal fins, which make each individual visually conspicuous Invertebrate fauna (Figure 1). This species reaches sexual maturity at To obtain fauna information of planktonic, algal and benthic invertebrates in the study site, different methods were used for sampling from May to July 2000. Planktonic invertebrates were sampled by quickly sweep- ing a portable handle-fitted plankton net (0.1 mm mesh) in the upper 3050 cm of the sediment. Algal inverte- brates were collected (eight replicates) by taking (into the 0.1 mm mesh bag) parts of algae where fish were feeding. Benthic invertebrates were sampled from substrates taken in the sandy and muddy bottom between boulders (eight replicates) using a metal core (100100 mm). All the samples collected were preserved in 5% formalin solution prior to examination. Each invertebrate were identified and counted, and 50 intact individuals randomly chosen per taxon were measured for their maximum length in the laboratory. The total counts were adjusted to the number per cubic meter for planktonic Figure 1. The serpentine goby, Pterogobius elapoides, hover- invertebrates or per square meter for algal and benthic ing to search prey on the bottom in the ocean around Kurahashi Island, Japan. invertebrates. Animal Cells and Systems 345 Table 1. Individual numbers, numeric occurrence (%; in Foraging behaviors and microhabitat preferences bracket), and mean sizes (mm9standard deviation) of the Foraging behaviors and microhabitat preference (includ- taxa collected from water column, alga, and substratum in ing home ranges) for each of the three size classes were the study site. examined using scan field observations with scuba diving and snorkeling at a chosen time depending on the Prey available from the environments weather condition between 08:00 and 17:00 for 3060 min per dive from May to August in 2000. The Individual Mean body observation was made in depth ranging from 1 to 6 m number (%) size9SD on rocky terrain with cracks and crevices irregularly formed and overgrown brown algae. A total of Water column Copepoda 17 individuals (5378 mm SL) were captured from the Calanoida study site using encircling monofilament nylon net Palacalanus spp. 1487 (56.6) 0.690.17 (151 m; 5 mm square mesh). The collected individuals Copepodid stages 289 (11.4) 0.690.19 were marked by color paint injection (blue acrylic paint) Nauplii 286 (10.9) 0.490.22 over the skin (see Thresher and Gronell 1978 for the Calanus spp. 43 (1.6) 1.891.22 method). After measuring their SL using a scale bar to Poecilostomatoida the nearest 1 mm, each individual was allocated into Corycaeus sp. 85 (3.2) 0.790.08 three size classes (see Diet analysis section) and was Cyclopoida released. Seventeen individuals were tracked down for Oithona spp. 128 (4.9) 0.590.08 observation; small- (N6), medium- (N6), and Harpacticoda large-size class individuals (N5) were observed for Euterpina sp. 45 (1.7) 0.690.06 Others (Copepoda) 85 (3.2) 0.790.34 21, 17, and 27 h, respectively. Cladocera Evadne sp. 25 (1.0) 0.790.10 Appendicularia Results Oikopleura ssp. 98 (3.7) 5.791.67 Ontogenetic shift in diet composition Others 42 (1.6) 1.190.73 The stomach of small-size class P. elapoides contained Algal collections pelagic copepods, amphipods, and branchiopods. More Amphipoda than 90% of the stomach contents (in volume) were Pontogeneia ssp. 1571 (52.7) 1.890.64 Caprella ssp. 234 (7.9) 16.4917.63 pelagic copepods, including Palacalanus spp. (Calanoi- Mysidacea 28 (0.9) 4.591.63 da), Euterpina spp. (Harpacticoda), Oithona spp. Copepoda (Cyclopoida), and Calanus spp. (Calanoida; Figure Harpacticoda 1016 (34.1) 0.790.07 2a). Among them, Palacalanus species were exclusively Crustacea predominant, covering 76.5% in the total volume Tanaidecia 85 (2.9) 2.291.08 (Figure 2a), as expected from the fact that genus Others 48 (1.6) 2.791.55 Palacalanus is the most abundant species found in the Benthic substratum water column (Table 1). Although other copepods, Amphipoda including Oithona spp. and Nauplius spp., were also Melita ssp. 6196 (10.7) 2.091.11 abundant in water column (Table 1), they were rarely Corphium sp. 2327 (4.0) 3.191.56 found in the stomach contents of this size class. Maera sp. 1004 (1.7) 3.891.23 Individuals of medium-size class are likely to Grandidierella sp. 976 (1.7) 2.490.54 consume more diverse items of prey than do smaller Other (Amphipoda) 429 (0.7) 2.791.81 ones (Figure 2b). Copepods, including Harpacticoda, Copepoda Mysidacea, and Calanoida, were no more exclusively Harpacticoida 42878 (74.1) 0.790.05 dominant food items for medium-size class (44.68% in Cumacea 447 (0.8) 3.190.71 number, 23.66% in volume), while various amphipod Polychaeta 2893 (5.0) 22.7916.40 species (algal amphipods such as Pontongeneia spp. and Ostracoda 684 (1.2) 1.090.11 Caprella spp., and benthic amphipods such as Melita spp., Corphium sp., and Cumacea) were more fre- only a minor component volumetrically (4.3390.74%), quently found (47.68% in number, 54.11% in volume; probably due to its relatively small sizes (Figure 2b). On Figure 2b). Big organisms, such as benthic annelid the contrary, Caprella spp., Mysidacea and Polychaeta worms (Polychaeta), were also included in the items. In showed low proportions in numbers but not volume- the medium-size fishes, Harpacticoid is one of the predominant item in number (26.3894.68%) but was trically (Figure 2b). 346 S.-H. Choi and H.Y. Suk and Polychaeta showed high values in volume but not in number (Figure 2c). Although Harpacticoids were the most abundant invertebrate in the substratum (Table 1), they were rarely found in the stomach of large-size fishes. The large fish consumed proportion- ally more benthic amphipods in their diet than did the medium-sized fish (MannWhitney U-test, U108.0, pB 0.001). Ontogenetic shift in foraging behaviors Pterogobius elapoides show three distinct foraging behaviors to catch prey in three types of environ- ments: capturing in mid-water (CM), sucking algal invertebrates (SA), and picking benthic invertebrates (PB). The three size classes significantly differ in occurrence of three different foraging behaviors (x 61.51, df  1, pB 0.001; Table 2). CM and SA were observed in small-size fishes (Table 2). For CM, small-size fishes generally hover in water column around rocks where they rapidly feed on pelagic prey. When potential prey available for SA are found on the surface of brown algae, individuals halt around the algae for 34 seconds and feed on the prey with powerful suction. In this size class, CM was more frequently observed than SA (Wilcoxon singed rank test, z4.15, pB 0.001; Table 2). All types of foraging behaviors were observed in the fishes of medium-size class (Table 2). The frequency of the CM was significantly decreased compared to small- size class (z4.97, pB 0.001), while the frequency of SA was increased relative to the small fish (z4.36, pB 0.001). For PB, individuals search for prey on the substrate surface, and they always stop hovering for a few seconds when they found prey on the substrate. After taking the prey, the fish generally churn the prey with sediment and expel inedible materials out of opercula and mouth. SA seems to be the dominant foraging pattern in medium-size class (Kruskal-Wallis H  262.10, df  2, pB0.001). Capturing in mid-water (CM) and SA were not observed at all among the fishes of large-size class Figure 2. Comparison of numeric (shaded bar) and volu- (Table 2). The frequencies of feeding were the lowest metric (empty bar) occurrence (presented as relative frequen- (9.6497.77) when compared with small-size class cies;%9standard deviation) of major dietary items found in (27.88921.05) and medium-size class (16.8898.53; the stomach contents among three size classes investigated. Kruskal-Wallis test H  104.15, df  2, pB0.001). The stomach contents of the large-size class comprised only of benthic invertebrates, including Microhabitat preferences benthic amphipods, decapods, and Polychaetes Home ranges did not appear to change with growth as (Figure 2c). Benthic amphipods, including Melita this species primarily prefer to stay in areas with spp., Corphium sp., Maera sp., and Grandidierella boulders and sand bottoms around the reefs. However, sp., were the dominant ones in numbers, while pelagic individuals in different size classes showed clear copepods and algal amphipods were not found in the difference in space use, suggesting that P. elapoides stomach items of this size class (Figure 2c). Decapoda undergo vertical microhabitat shifts from water Animal Cells and Systems 347 Table 2. Ontogenetic changes in using different types of foraging behavior by serpentine gobies, that is, capturing in mid-water (CM), sucking algal invertebrate (SA), and picking benthic invertebrates (PB). Size class CM SA PB Small 25.38921.95 (80.08%) 2.5992.10 (19.92%) 0 (0%) Medium 3.4692.30 (25.37%) 11.4798.98 (59.94%) 1.9691.29 (14.69%) Large 0 (0%) 0 (0%) 9.6497.77 (100.00%) Note: Values indicate frequency of the behavior per 10 min (mean9standard deviation) and are also presented on percentage basis (%). columns to the bottom with growth. The individuals in is in perfect agreement with optimal foraging theory of small-size class were usually found around reefs in the Estabrook and Dunham (1976) predicting that onto- middle water column. The individuals in medium-size genetic diet shift of an individual is a stepwise class always swam around reefs with patches of development to maximize its net energy gain. brown algae. The individuals in large-size class gen- Foraging techniques is an essential determinant of erally hovered around reefs in 510 cm upper from the ontogenetic difference in the diets of P. elapoides.CMis bottom. the foraging pattern appropriate for taking small copepods and most frequently observed in small-size class, while large-size individuals generally pick up relatively large benthic invertebrates. The exploitation Discussion of differing prey sources is directly constrained by The most common prey, by number and volumetrically, morphological capacity of feeding apparatus (Schmitt in P. elapoides’ diet were pelagic copepods and benthic and Holbrook 1984; Stoner and Livingston 1984; amphipods. There was an ontogenetic diet shift from MacNeill and Brandt 1990; Peterson and McIntyre pelagic to benthic prey, as well as among-habitat 1998). In the study of a microcarnivorous fish, variation in diet as a result of different prey availability. Cheilodactylus spectabilis, the increase in size of the P. elapoides has been known as omnivorous fish buccal cavity, hyoid complex, and associated muscu- because copepod, organic deposit, and algae particles lature lead directly to an increase in the suction were found from the stomach contents in a previous primarily used to capture prey (McCormick 1998). In study (Do ˘ tu and Tsutsumi 1959), which did not P. elapoides, the increasing size of the feeding apparatus consider the feeding microhabitats and prey availabil- with growth (Kendall’s rank correlation test; gape ity. Algae particles were not found as stomach contents width, t  0.874, pB 0.001; snout length, t  0.890, in our study. Our diet analyses consequently show that pB 0.001; S.-H. Choi and H.Y. Suk, unpublished data) P. elapoides is microcarnivore, as is the case for many may contribute to a feeding on larger prey. However, other gobies (Blaber and Whitfield 1977; Gibson and the present data do not provide any direct evidence for Ezzi 1978; Grossman et al. 1980; Kikuchi and increasing efficiency of handling procedure with the Yamashita 1992; Onadeko 1992; Aarnio and Bonsdorff growth in feeding apparatus. 1993; Humphries and Potter 1993; Swenson and Growth-related preference for different food re- McCray 1996). sources might require individuals to change their The ontogenetic diet shift was the result of the microhabitats, as also shown in many other studies preference for energetically more profitable prey in (Werner and Hall 1988; Clements and Coat 1993; P. elapoides in larger-size classes, as shown in many Lukoschek and McCormick 2001). Vertical up-shifting other microcarnivores (Grossman 1980; Schmitt and in microhabitat was observed in the present study. Holbrook 1984; MacNeill and Brandt 1990; Gill Water column is the perfect place for small individuals and Hart 1994; Luczkovich et al. 1995; Peterson and to feed pelagic organisms with occupying exposed McIntyre 1998). Pelagic copepods, in particular Cala- perches within rocky reef habitats. Although the noida, are generally much smaller than amphipods and medium-sized fish consume prey in the water column, polychaetes that are consumed by the individuals from they seem to prefer to find algal invertebrates, as they medium- and large-size classes. Pelagic copepods may energetically be less profitable, but are valuable for the spend much time for foraging and searching around individuals in the small-size class with reduced hand- algae patches on the reefs. The large-sized fish only ling and foraging efforts and with relatively high feeds on prey found on sediments in the sand bottom. abundance. By contrast, the increased searching and However, ontogenetic shift in food preferences does not capturing efforts for larger individuals can be compen- appear to affect individual scope for searching food, as sated by exploitation of differing prey sources and the the home ranges of individuals from different size increased caloric profitability (Ellison et al. 1979). This classes (collected in the same site) were totally 348 S.-H. Choi and H.Y. Suk Gibson RN, Ezzi IA. 1978. The biology of a Scottish overlapped, and the sizes of the home ranges were not population of Fries’ goby (Lesueurigobius friesii). J Fish different from the individuals in different size classes Biol. 12:371389. (actually decreased with growth). Gill AB, Hart PJB. 1994. Feeding behaviour and prey choice In conclusion, ontogenetic diet shift in P. elapoides is of the threespine stickleback: the interacting effects of prey size, fish size and stomach fullness. 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The mechanisms leading to ontogenetic diet shift in a microcanivore, Pterogobius elapoides (Gobiidae)

Choi, Seung-Ho; Suk, Ho Young
Animal Cells and Systems , Volume 16 (4): 7 – Aug 1, 2012
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ECOLOGY & POPULATION BIOLOGY Animal Cells and Systems Vol. 16, No. 4, August 2012, 343349 The mechanisms leading to ontogenetic diet shift in a microcanivore, Pterogobius elapoides (Gobiidae) a b Seung-Ho Choi and Ho Young Suk * a b Department of Animal Resources, National Institute of Biological Resources, Incheon 404-708, Korea; Department of Life Sciences, Yeungnam University, Gyeongsan Gyeongsangbuk-do 712-749, Korea (Received 4 December 2011; received in revised form 27 January 2012; accepted 13 February 2012) A variety of fish species undergo an ontogenetic change in prey selectivity, and several potentially interacting factors, including nutrient requirement, microhabitat change, and foraging ability, may account for the occurrence of the shift. Here we examine the foraging ecology and ontogenetic diet shift of a micro-carnivorous goby, Pterogobius elapoides (serpentine goby), dominant component of fish assemblage in shallow rocky areas off the coast in Korea and Japan. Although most other gobies are primarily benthic carnivores, P. elapoides is a semipelagic fish; however, little is known about how those species change their foraging tactics with growth. In our diet analyses, the most common diet was pelagic copepods and benthic amphipods, and diet shift was observed from pelagic to benthic with growth. The ontogenetic diet shift seems to be the result of the preference for energetically more profitable prey in larger-size classes as well as the results of different prey availability due to among-habitat variation in diet. However, differential food preference does not appear to affect individual scope for searching food. Several factors such as predation pressures and interspecific resource partitioning might contribute to the changes in diet observed among size classes, which were included in our ongoing tests. Keywords: ontogenetic diet shift; foraging behavior; serpentine goby; Pterogobius elapoides; micro-carnivore; Gobiidae Introduction tropical regions (Nelson 2006). Gobies are primarily fish of shallow oceanic habitats including tide pools, A variety of fish species undergo an ontogenetic coral reefs, and sea-grass fields; they are also very change in prey selectivity, that is, from planktivory abundant in brackish water, and a small number of to piscivory (Schmitt and Holbrook 1984; Holbrook gobiid species are also entirely adapted to freshwater et al. 1985; Shibuno et al. 1994; Lockett and Suthers system (Nelson 2006). Although few are valuable as 1998; Graham et al. 2007; Schellelens et al. 2010; food for humans, they are generally of great signifi- Baeck et al. 2011). Many potentially interrelating cance as prey and predator species for commercially factors may account for the occurrence of these shifts important organisms. While the occurrence of onto- (McCormick 1998). Growth-related morphological genetic change in prey selectivity has been reported for differences can lead to differential exploitation of a gobies in several studies (Gibson 1970; Vass et al. food resource and, in turn, changes in microhabitat 1975; Grossman 1980; Grossman et al. 1980; Huh and use, being a function of changing in nutrient require- Kwak 1998a, 1998b, 1999), little is known about how ment (MacNeill and Brandt 1990; Luczkovich et al. those species change their foraging tactics with 1995; Peterson and McIntyre 1998). Likewise, foraging growth. schedule and ability may change with ontogeny, which In this study, we examine the foraging ecology can be compromised with availability and density of of a goby, Pterogobius elapoides (serpentine goby; prey organisms (Clements and Choat 1993; Lukoschek Figure 1), a common component of fish assemblage and McCormick 2001). A thoughtful consideration of in shallow rocky areas off the coast in Korea and how a species exploits its food resource and how that Japan (Masuda et al. 1984; Kim et al. 1986). While changes with growth is prerequisite to any examina- most gobies are benthic carnivores, consuming mainly tion for the pattern and dynamics of species assem- crustaceans and polychaetes (Gibson and Ezzi 1978; blage on temporal and spatial scales (McCormick Grossman et al. 1980; Behrents 1989; Kikuchi 1998). and Yamashita 1992; Aarnio and Bonsdorff 1993; The Gobiid species (gobies), one of the largest Humphries and Potter 1993; Swenson and McCray families of fish with more than 200 genera, are 1996), P. elapoides is a semipelagic fish, seldom settling commonly distributed in temperate, subtropical, and on bottom structure (Do ˘ tu and Tsutsumi 1959). *Corresponding author. Email: hsuk@ynu.ac.kr ISSN 1976-8354 print/ISSN 2151-2485 online # 2012 Korean Society for Integrative Biology http://dx.doi.org/10.1080/19768354.2012.667002 http://www.tandfonline.com 344 S.-H. Choi and H.Y. Suk However, temporal (seasonal) space defense is ob- around 7080 mm in standard length (hereafter SL; served in this species sometimes, but not often, for Do ˘ tu and Tsutsumi 1959). The breeding season of the their benthic feeding territories (personal observation). studied population starts in November and continues P. elapoides is thus expected to undergo distinct well into December. The male builds a nest underneath a pattern of ontogenetic shifts in foraging ecology boulder and provides exclusive paternal care for eggs, from other gobies, even though it has never been which includes fanning and defending the brood until thoroughly investigated. hatching (Do ˘ tu and Tsutsumi 1959). Adult individuals In the present study, we investigated for the first time generally die at the completion of the breeding season. whether diet changes with ontogeny and explored the mechanisms by which partitioning of the food resource occurs among different size classes in P. elapoides. First, Diet analysis the stomach of individuals from different size classes A total of 34 individuals were collected in the study site was dissected open, and the contents inside were using a gill net during the daytime (dates were chosen examined to find differences, if any, in diet taxa. Second, based on the weather condition; 1617 May, 2223 June, information on prey species availability, size-related 17 July, and 6 August in 2000). The captured fishes were feeding mechanics, and microhabitat selectivity was preserved in 10% buffered formalin solution and were used to find the potential factors accounting for the measured to the nearest 0.01 mm by digital calipers. occurrence of the shift. Each individual was allocated into three different size classes: small (5060 mm SL), medium (6170 mm SL), Materials and methods and large ( 70 mm SL). The stomach of each individual was dissected open, and the contents inside Locations and study species were examined under a binocular dissecting microscope. Collections for estimation and observation were carried Prey were removed from the stomach and identified to out on shallow rocky areas off the coast of Kurahashi the lowest taxon feasible. The greatest length or carapace Island (Honmura Bay, the Seto Inland Sea; 3485?14??N, length of all of the individuals was measured to the 132830?0??E) in Japan. P. elapoides is one of the nearest 0.01 mm using an ocular micrometer. Prey dominant inhabitants in our study sites. Many indivi- volume was estimated by measuring the length and duals cruise around boulders and conceal themselves width of each item and calculating its cylindrical or in cracks beneath boulders or inside of brown algae spherical volume, depending on its shape. For each patches to avoid predation (S.-H. Choi, personal ob- sample, the percent composition was calculated in servation). P. elapoides is relatively smaller in size than number and in volume. that of other Pterogobius species. This species exhibit pale brown with six or seven transverse black bands on their body side continuing behind the dorsal and anal fins, which make each individual visually conspicuous Invertebrate fauna (Figure 1). This species reaches sexual maturity at To obtain fauna information of planktonic, algal and benthic invertebrates in the study site, different methods were used for sampling from May to July 2000. Planktonic invertebrates were sampled by quickly sweep- ing a portable handle-fitted plankton net (0.1 mm mesh) in the upper 3050 cm of the sediment. Algal inverte- brates were collected (eight replicates) by taking (into the 0.1 mm mesh bag) parts of algae where fish were feeding. Benthic invertebrates were sampled from substrates taken in the sandy and muddy bottom between boulders (eight replicates) using a metal core (100100 mm). All the samples collected were preserved in 5% formalin solution prior to examination. Each invertebrate were identified and counted, and 50 intact individuals randomly chosen per taxon were measured for their maximum length in the laboratory. The total counts were adjusted to the number per cubic meter for planktonic Figure 1. The serpentine goby, Pterogobius elapoides, hover- invertebrates or per square meter for algal and benthic ing to search prey on the bottom in the ocean around Kurahashi Island, Japan. invertebrates. Animal Cells and Systems 345 Table 1. Individual numbers, numeric occurrence (%; in Foraging behaviors and microhabitat preferences bracket), and mean sizes (mm9standard deviation) of the Foraging behaviors and microhabitat preference (includ- taxa collected from water column, alga, and substratum in ing home ranges) for each of the three size classes were the study site. examined using scan field observations with scuba diving and snorkeling at a chosen time depending on the Prey available from the environments weather condition between 08:00 and 17:00 for 3060 min per dive from May to August in 2000. The Individual Mean body observation was made in depth ranging from 1 to 6 m number (%) size9SD on rocky terrain with cracks and crevices irregularly formed and overgrown brown algae. A total of Water column Copepoda 17 individuals (5378 mm SL) were captured from the Calanoida study site using encircling monofilament nylon net Palacalanus spp. 1487 (56.6) 0.690.17 (151 m; 5 mm square mesh). The collected individuals Copepodid stages 289 (11.4) 0.690.19 were marked by color paint injection (blue acrylic paint) Nauplii 286 (10.9) 0.490.22 over the skin (see Thresher and Gronell 1978 for the Calanus spp. 43 (1.6) 1.891.22 method). After measuring their SL using a scale bar to Poecilostomatoida the nearest 1 mm, each individual was allocated into Corycaeus sp. 85 (3.2) 0.790.08 three size classes (see Diet analysis section) and was Cyclopoida released. Seventeen individuals were tracked down for Oithona spp. 128 (4.9) 0.590.08 observation; small- (N6), medium- (N6), and Harpacticoda large-size class individuals (N5) were observed for Euterpina sp. 45 (1.7) 0.690.06 Others (Copepoda) 85 (3.2) 0.790.34 21, 17, and 27 h, respectively. Cladocera Evadne sp. 25 (1.0) 0.790.10 Appendicularia Results Oikopleura ssp. 98 (3.7) 5.791.67 Ontogenetic shift in diet composition Others 42 (1.6) 1.190.73 The stomach of small-size class P. elapoides contained Algal collections pelagic copepods, amphipods, and branchiopods. More Amphipoda than 90% of the stomach contents (in volume) were Pontogeneia ssp. 1571 (52.7) 1.890.64 Caprella ssp. 234 (7.9) 16.4917.63 pelagic copepods, including Palacalanus spp. (Calanoi- Mysidacea 28 (0.9) 4.591.63 da), Euterpina spp. (Harpacticoda), Oithona spp. Copepoda (Cyclopoida), and Calanus spp. (Calanoida; Figure Harpacticoda 1016 (34.1) 0.790.07 2a). Among them, Palacalanus species were exclusively Crustacea predominant, covering 76.5% in the total volume Tanaidecia 85 (2.9) 2.291.08 (Figure 2a), as expected from the fact that genus Others 48 (1.6) 2.791.55 Palacalanus is the most abundant species found in the Benthic substratum water column (Table 1). Although other copepods, Amphipoda including Oithona spp. and Nauplius spp., were also Melita ssp. 6196 (10.7) 2.091.11 abundant in water column (Table 1), they were rarely Corphium sp. 2327 (4.0) 3.191.56 found in the stomach contents of this size class. Maera sp. 1004 (1.7) 3.891.23 Individuals of medium-size class are likely to Grandidierella sp. 976 (1.7) 2.490.54 consume more diverse items of prey than do smaller Other (Amphipoda) 429 (0.7) 2.791.81 ones (Figure 2b). Copepods, including Harpacticoda, Copepoda Mysidacea, and Calanoida, were no more exclusively Harpacticoida 42878 (74.1) 0.790.05 dominant food items for medium-size class (44.68% in Cumacea 447 (0.8) 3.190.71 number, 23.66% in volume), while various amphipod Polychaeta 2893 (5.0) 22.7916.40 species (algal amphipods such as Pontongeneia spp. and Ostracoda 684 (1.2) 1.090.11 Caprella spp., and benthic amphipods such as Melita spp., Corphium sp., and Cumacea) were more fre- only a minor component volumetrically (4.3390.74%), quently found (47.68% in number, 54.11% in volume; probably due to its relatively small sizes (Figure 2b). On Figure 2b). Big organisms, such as benthic annelid the contrary, Caprella spp., Mysidacea and Polychaeta worms (Polychaeta), were also included in the items. In showed low proportions in numbers but not volume- the medium-size fishes, Harpacticoid is one of the predominant item in number (26.3894.68%) but was trically (Figure 2b). 346 S.-H. Choi and H.Y. Suk and Polychaeta showed high values in volume but not in number (Figure 2c). Although Harpacticoids were the most abundant invertebrate in the substratum (Table 1), they were rarely found in the stomach of large-size fishes. The large fish consumed proportion- ally more benthic amphipods in their diet than did the medium-sized fish (MannWhitney U-test, U108.0, pB 0.001). Ontogenetic shift in foraging behaviors Pterogobius elapoides show three distinct foraging behaviors to catch prey in three types of environ- ments: capturing in mid-water (CM), sucking algal invertebrates (SA), and picking benthic invertebrates (PB). The three size classes significantly differ in occurrence of three different foraging behaviors (x 61.51, df  1, pB 0.001; Table 2). CM and SA were observed in small-size fishes (Table 2). For CM, small-size fishes generally hover in water column around rocks where they rapidly feed on pelagic prey. When potential prey available for SA are found on the surface of brown algae, individuals halt around the algae for 34 seconds and feed on the prey with powerful suction. In this size class, CM was more frequently observed than SA (Wilcoxon singed rank test, z4.15, pB 0.001; Table 2). All types of foraging behaviors were observed in the fishes of medium-size class (Table 2). The frequency of the CM was significantly decreased compared to small- size class (z4.97, pB 0.001), while the frequency of SA was increased relative to the small fish (z4.36, pB 0.001). For PB, individuals search for prey on the substrate surface, and they always stop hovering for a few seconds when they found prey on the substrate. After taking the prey, the fish generally churn the prey with sediment and expel inedible materials out of opercula and mouth. SA seems to be the dominant foraging pattern in medium-size class (Kruskal-Wallis H  262.10, df  2, pB0.001). Capturing in mid-water (CM) and SA were not observed at all among the fishes of large-size class Figure 2. Comparison of numeric (shaded bar) and volu- (Table 2). The frequencies of feeding were the lowest metric (empty bar) occurrence (presented as relative frequen- (9.6497.77) when compared with small-size class cies;%9standard deviation) of major dietary items found in (27.88921.05) and medium-size class (16.8898.53; the stomach contents among three size classes investigated. Kruskal-Wallis test H  104.15, df  2, pB0.001). The stomach contents of the large-size class comprised only of benthic invertebrates, including Microhabitat preferences benthic amphipods, decapods, and Polychaetes Home ranges did not appear to change with growth as (Figure 2c). Benthic amphipods, including Melita this species primarily prefer to stay in areas with spp., Corphium sp., Maera sp., and Grandidierella boulders and sand bottoms around the reefs. However, sp., were the dominant ones in numbers, while pelagic individuals in different size classes showed clear copepods and algal amphipods were not found in the difference in space use, suggesting that P. elapoides stomach items of this size class (Figure 2c). Decapoda undergo vertical microhabitat shifts from water Animal Cells and Systems 347 Table 2. Ontogenetic changes in using different types of foraging behavior by serpentine gobies, that is, capturing in mid-water (CM), sucking algal invertebrate (SA), and picking benthic invertebrates (PB). Size class CM SA PB Small 25.38921.95 (80.08%) 2.5992.10 (19.92%) 0 (0%) Medium 3.4692.30 (25.37%) 11.4798.98 (59.94%) 1.9691.29 (14.69%) Large 0 (0%) 0 (0%) 9.6497.77 (100.00%) Note: Values indicate frequency of the behavior per 10 min (mean9standard deviation) and are also presented on percentage basis (%). columns to the bottom with growth. The individuals in is in perfect agreement with optimal foraging theory of small-size class were usually found around reefs in the Estabrook and Dunham (1976) predicting that onto- middle water column. The individuals in medium-size genetic diet shift of an individual is a stepwise class always swam around reefs with patches of development to maximize its net energy gain. brown algae. The individuals in large-size class gen- Foraging techniques is an essential determinant of erally hovered around reefs in 510 cm upper from the ontogenetic difference in the diets of P. elapoides.CMis bottom. the foraging pattern appropriate for taking small copepods and most frequently observed in small-size class, while large-size individuals generally pick up relatively large benthic invertebrates. The exploitation Discussion of differing prey sources is directly constrained by The most common prey, by number and volumetrically, morphological capacity of feeding apparatus (Schmitt in P. elapoides’ diet were pelagic copepods and benthic and Holbrook 1984; Stoner and Livingston 1984; amphipods. There was an ontogenetic diet shift from MacNeill and Brandt 1990; Peterson and McIntyre pelagic to benthic prey, as well as among-habitat 1998). In the study of a microcarnivorous fish, variation in diet as a result of different prey availability. Cheilodactylus spectabilis, the increase in size of the P. elapoides has been known as omnivorous fish buccal cavity, hyoid complex, and associated muscu- because copepod, organic deposit, and algae particles lature lead directly to an increase in the suction were found from the stomach contents in a previous primarily used to capture prey (McCormick 1998). In study (Do ˘ tu and Tsutsumi 1959), which did not P. elapoides, the increasing size of the feeding apparatus consider the feeding microhabitats and prey availabil- with growth (Kendall’s rank correlation test; gape ity. Algae particles were not found as stomach contents width, t  0.874, pB 0.001; snout length, t  0.890, in our study. Our diet analyses consequently show that pB 0.001; S.-H. Choi and H.Y. Suk, unpublished data) P. elapoides is microcarnivore, as is the case for many may contribute to a feeding on larger prey. However, other gobies (Blaber and Whitfield 1977; Gibson and the present data do not provide any direct evidence for Ezzi 1978; Grossman et al. 1980; Kikuchi and increasing efficiency of handling procedure with the Yamashita 1992; Onadeko 1992; Aarnio and Bonsdorff growth in feeding apparatus. 1993; Humphries and Potter 1993; Swenson and Growth-related preference for different food re- McCray 1996). sources might require individuals to change their The ontogenetic diet shift was the result of the microhabitats, as also shown in many other studies preference for energetically more profitable prey in (Werner and Hall 1988; Clements and Coat 1993; P. elapoides in larger-size classes, as shown in many Lukoschek and McCormick 2001). Vertical up-shifting other microcarnivores (Grossman 1980; Schmitt and in microhabitat was observed in the present study. Holbrook 1984; MacNeill and Brandt 1990; Gill Water column is the perfect place for small individuals and Hart 1994; Luczkovich et al. 1995; Peterson and to feed pelagic organisms with occupying exposed McIntyre 1998). Pelagic copepods, in particular Cala- perches within rocky reef habitats. Although the noida, are generally much smaller than amphipods and medium-sized fish consume prey in the water column, polychaetes that are consumed by the individuals from they seem to prefer to find algal invertebrates, as they medium- and large-size classes. Pelagic copepods may energetically be less profitable, but are valuable for the spend much time for foraging and searching around individuals in the small-size class with reduced hand- algae patches on the reefs. The large-sized fish only ling and foraging efforts and with relatively high feeds on prey found on sediments in the sand bottom. abundance. By contrast, the increased searching and However, ontogenetic shift in food preferences does not capturing efforts for larger individuals can be compen- appear to affect individual scope for searching food, as sated by exploitation of differing prey sources and the the home ranges of individuals from different size increased caloric profitability (Ellison et al. 1979). This classes (collected in the same site) were totally 348 S.-H. Choi and H.Y. Suk Gibson RN, Ezzi IA. 1978. The biology of a Scottish overlapped, and the sizes of the home ranges were not population of Fries’ goby (Lesueurigobius friesii). J Fish different from the individuals in different size classes Biol. 12:371389. (actually decreased with growth). Gill AB, Hart PJB. 1994. Feeding behaviour and prey choice In conclusion, ontogenetic diet shift in P. elapoides is of the threespine stickleback: the interacting effects of prey size, fish size and stomach fullness. 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Journal

Animal Cells and Systems – Taylor & Francis

Published: Aug 1, 2012

Keywords: ontogenetic diet shift; foraging behavior; serpentine goby; Pterogobius elapoides; micro-carnivore; Gobiidae

References

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  • Feeding habits of Acanthogobius flavimanus in the eelgrass (Zostera marina) bed in Kwangyang Bay
  • Synopsis of the family Gobiidae (Pisces, Perciformes) from Korea
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  • Ontogenetic patterns in diet and feeding morphology in sympatric sparid fishes from seagrass meadows
  • Subcutaneous tagging of small reef fishes