Effects of Trematode Infection on Metabolism and Activity in a Freshwater Snail, Semisulcospira Libertina

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Effects of Trematode Infection on Metabolism and Activity in a Freshwater Snail, Semisulcospira Libertina DISEASES OF AQUATIC ORGANISMS Vol. 45: 141–144, 2001 Published June 20 Dis Aquat Org Effects of trematode infection on metabolism and activity in a freshwater snail, Semisulcospira libertina Kazuko Shinagawa*, Misako Urabe**, Makoto Nagoshi*** Department of Biological Science, Faculty of Science, Nara Women’s University, Kitauoyanishi-machi, Nara 630-8506, Japan ABSTRACT: Changes in the metabolism and activity of the freshwater snail Semisulcospira libertina infected with larval trematodes were studied experimentally. In snails up to 11 mm in shell width, crawling distance, feeding frequency, and the proportion of individuals located on vertical walls did not differ among snails infected with mature or immature cercariae, or uninfected snails (p > 0.05). In snails larger than 11 mm, individuals infected with mature cercariae tended to feed more frequently during the light period (p = 0.0081), but the distance they crawled and the proportion of individuals located on vertical walls did not differ, regardless of infection (p > 0.05). Infection with mature cer- cariae significantly increased the oxygen consumption rate (p = 0.016), which was measured only in the large size. KEY WORDS: Semisulcospira libertina · Larval trematodes · Activity · Metabolism Resale or republication not permitted without written consent of the publisher INTRODUCTION of many species of trematodes (Ito 1964, 1988). We reported that snails infected with larval trematodes Many studies have reported the behavioral alter- were found in deeper locations than uninfected snails ation of hosts caused by parasitic infection and inter- (Shinagawa et al. 1999a). The pattern of water depth pret this as an induced adaptation by parasites to selection by infected and uninfected snails also dif- facilitate transfer to the next-stage hosts. This ‘manip- fered under experimental conditions, although the pat- ulation’ hypothesis has received much attention from tern did not replicate field distribution (Shinagawa et evolutionary ecologists (Swennen 1969, Curtis 1990, al. 1999b). In contrast to field observations, large (shell 1993, Levri & Lively 1996). However, ecological or width >11 mm) infected snails, especially those in- behavioral changes also occur in hosts even when par- fected with immature cercariae or parthenitae, tended asites are not dependent on predation for transfer to to select shallow sites relative to uninfected snails (Shi- next-stage hosts, and the adaptive significance for nagawa et al. 1999b). Thus, factors other than the parasites is unclear (Shinagawa et al. 1999a,b). direct interference by parasites to water-depth selec- In Japan, a freshwater prosobranchia snail, Semisul- tion by hosts affect the habitat shift of large infected cospira libertina (Gould), is the first-intermediate host snails in the field. We examined crawling distance and feeding fre- Present addresses: quency as indicators of activity and physiological con- ***Fumigaoka-machi 15-18, Tondabayashi, Osaka 584-0094, dition. These factors might cause a habitat shift in Japan infected snails, as Semisulcospira generally feeds on ***(Corresponding author.) Japan Science and Technology the surface of stones or sediments while active and Corporation, Aqua Restoration Research Center, Kasada, Kawashima-cho, Hashima-gun, Gifu 501-6021, Japan. hides under stones or in sediments while resting (Mori E-mail: [email protected] 1946, Urabe 1998). The proportion of individuals loca- ***Shimizu 856-36, Anno, Mie 514-2305, Japan ted on vertical walls was also investigated to examine © Inter-Research 2001 142 Dis Aquat Org 45: 141–144, 2001 changes in adhesion since pathological changes in the After these experiments, the snails were dissected foot surface of host gastropods were reported (Thomp- to determine trematode infection. The cercariae iden- son et al. 1993). Oxygen consumption was measured to tified were Metagonimus sp. (experimental second- determine basal metabolism. These parameters were intermediate host, a freshwater goby, Rhinogobius compared in small and large snails separately, since flumineus, unpubl. data), Centrocestus armatus (sec- the effect of infection on water-depth selection differs ond-intermediate host, cyprinid fish), Cercaria yoshi- according to host size (Shinagawa et al. 1999b). We dae (second-intermediate host, copepods), Cercaria discuss the possibility that changes in metabolism or innominata (second-intermediate host, fish: Shimazu, activity resulting from infection cause the water-depth Nagano Prefectural College, pers. comm.), Cercaria shift. nipponensis (life history unknown), and Cercaria A by Makita et al. (1996) (life history unknown). An uniden- tified oculate furcocercous cercaria was also found. MATERIALS AND METHODS The snails were classified as uninfected snails (U- snails), or snails infected with Metagonimus sp. (Me- All the snails studied were collected from the Takami snails), C. armatus (Ca-snails) or C. yoshidae (Cy- River, Kotsukawa, Higashi-Yoshino, Nara Prefecture snails). The other 4 species were not categorized for (136°0’ E, 34°24’ N) between July and October 1995 or species because too few snails were infected. Snails between April and October 1996. A total of 158 snails infected with mature cercariae of any species, includ- with a shell >7 mm wide were collected for the labora- ing 4 minor species, were grouped as ‘M-snails’. Snails tory experiment. infected with unidentifiable immature cercariae or An aquarium with internal dimensions of 87 × 42.5 × parthenitae were not categorized for species but classi- 54 cm was used for the laboratory experiment. Three fied as ‘IM-snails’. horizontal planes 4 to 6 cm wide were fixed at the bot- CD, F and V were compared among U-snails, IM- tom, middle and top of the aquarium. They were con- snails and each species category by Kruskal-Wallis nected with ramps inclined at 33°. A paste of flour and test and multiple comparisons using the Bonferroni fish pellet was provided as food at the 14 points on the method. If the number of snails classified by trematode planes and the ramps. The water was aerated and reg- species was insufficient for statistics, M-snail was used ulated at 20°C. The aquarium was under a 13 h light as the category. and 11 h dark cycle. More details of the sampling loca- We divided the snails into ‘small’ (shell width up to tion and the experimental conditions have been re- 11 mm) and ‘large’ (more than 11 mm) size classes after ported elsewhere (Shinagawa et al. 1999b). Shinagawa et al. (1999b), to reduce the effects of size Snails were measured for shell width and individu- on measurements of physiological condition. The small ally marked with color paint and released in the aquar- size class comprised 34 U-snails, 5 M-snails (1 Ca- ium on the middle plane (27 cm deep). Six to 16 snails snail, 1 Cy-snail, 2 snails infected with Cercaria innom- were used for 1 experimental session. After acclimati- inata and 1 snail with Cercaria A) and 3 IM-snails. The zation for 24 to 38 h, data recording began and contin- large size class comprised 77 U-snails, 20 Me-snails, 5 ued for 48 h. The location of each snail in the aquarium Ca-snails, 3 Cy-snails and 6 IM-snails. Five snails was recorded once every hour. We calculated the fol- infected with mature cercariae (2 snails infected with lowing parameters for the light and dark periods sepa- C. innominata, 1 snail with C. nipponensis, 1 snail with rately: mean crawling distance h–1 (CD), feeding fre- the oculate furcocercous cercaria, and 1 snail doubly quency (observed frequency of feeding per number of infected with C. nipponensis and the oculate furcocer- observations) (F), and the frequency of location on ver- cous cercaria) were excluded from the analysis but not tical walls (observed frequency of location on vertical the oxygen consumption rate determination. walls per number of observations) (V). The experiment In the 78 snails that were measured for oxygen con- was repeated 11 times, and each snail was used only sumption, all infected snails were more than 11 mm in once. shell width and in the large size class (minimum After the observation, 78 of the snails were selected 11.6 mm). Thus, the size effect on oxygen consumption randomly and oxygen consumption rate was mea- could not be tested by division into the 2 size classes, sured. Individual snails were put in a 200 ml bottle unlike the other values. Therefore, the oxygen con- filled with water and kept in a 20°C incubator for 1 h. sumption rates of infected and large U-snails were com- Then the dissolved oxygen was measured by the Win- pared using regression lines on shell size to determine kler method. The rate of oxygen consumption was cal- size effect. Both the oxygen consumption rate and shell culated from the difference in dissolved oxygen width were log transformed. For U-snails, only data for between the bottles containing snails and a control snails whose shell width was in the range of infected bottle without snails. snails were selected for analysis (total n = 67). Shinagawa et al.: Trematode infection in a freshwater snail 143 Table 1. Comparison of crawling distance (CD), feeding rate (F) and the rate of location on vertical walls (V) among infection cat- egories in each size class. Values were tested by Kruskal-Wallis test. Ca: snails infected with Centrocestus armatus; Cy: snails infected with Cercaria yoshidae; IM: snails infected with unidentifiable immature cercariae or parthenitae; M: snails infected with mature cercariae of any species; Me: snails infected
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