QUALITATIVE AND QUANTITATIVE BEHAVIORAL TRAITS IN A COMMUNITY OF FURCOCERCARIAE TREMATODES: TOOLS FOR SPECIES SEPARATION?

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1 J. Parasitol., 93(6), 2007, pp American Society of Parasitologists 2007 QUALITATIVE AND QUANTITATIVE BEHAVIORAL TRAITS IN A COMMUNITY OF FURCOCERCARIAE TREMATODES: TOOLS FOR SPECIES SEPARATION? M. J. Santos, A. Karvonen*, J. C. Pedro, A. Faltýnková, O. Seppälä*, and E. T. Valtonen* Department of Zoology-Anthropology, Faculty of Sciences, University of Porto, Praça Gomes Teixeira, Porto and CIMAR CIIMAR, Rua dos Bragas, 289, Porto, Portugal. mjsantos@fc.up.pt ABSTRACT: Many trematode cercariae show distinct behavioral features, which have commonly been used in species identification in combination with morphological characteristics. However, information regarding cercariae behavior has often not been quantified in detail, or it is scattered in the literature, which is why the appropriate level of precision in behavioral identity, particularly in groups of cercariae species showing considerable morphological overlap, has not been properly established. In this study, we investigated one such group, the furcocercariae trematodes, by studying their behavior in a community consisting of 8 species (Diplostomum pseudospathaceum, Ichthyocotylurus variegatus, Cotylurus brevis, Cercaria spinulosa, Australapatemom sp., Australapatemom burti, Sanguinicola sp., and Bilharziella polonica) in central Finland. Our aim was not to develop an identification formula on the basis of behavior but to investigate and propose characteristic measurements applicable in separation of cercariae species. We used a 2-level approach, first recording qualitative behavioral traits of the cercariae, including swimming type and resting position; and, second, more detailed quantitative behavioral characteristics, such as resting time, swimming time, and swimming speed. Essentially, species showing a 2-phase behavior were distinguishable according to qualitative traits (resting position), whereas with those showing continuous swimming behavior, a combination of qualitative and quantitative traits (swimming speed) was required. These results suggest that characteristics of cercariae behavior can not only be used in species identification but also in general life history comparisons investigating details of the cercariae transmission. Many trematode cercariae show distinctive behavioral patterns, which are often related to the location of the next host species (reviewed by Combes et al., 1994; Haas, 1994). These behavioral characteristics, in combination with morphological characteristics, have also been used by ecologists working on cercariae life histories, or using these organisms as tools in research on parasite host relationships for the purpose of elucidating cercariae species identity. The original idea of behavioral identification of cercariae dates back to the early works of Miller (1928) and Cort and Brackett (1937), but a clear line that shows how this information could be used has still not been established. This is partly because descriptions on cercariae behavior have often lacked detailed quantifications or are scattered in the literature. However, information on the appropriate level of precision in behavioral identity, applicable to species identification, is needed especially in communities of cercariae species showing considerable morphological overlap. One such group of cercariae is the furcocercariae where morphological characteristics found in the adults are less clear for the cercariae stage. The present study examined whether and how cercariae behavior could be used as a tool in the separation of species in a community of furcocercariae at a single geographical location. Our overall purpose was not to develop a detailed identification formula for a specific set of species because we clearly recognize that values obtained for each species are case sensitive due to variation in physical and biological conditions, including temperature, water chemistry, host condition, and host and parasite genetics. Instead, we recorded a set of behavioral variables under standardized laboratory conditions to study their usefulness as a tool in species separation and general life history comparisons. We used a set of 8 fur- Received 14 February 2007; revised 26 April 2007; accepted 11 May * Department of Biological and Environmental Science, P.O. Box 35, FI University of Jyväskylä, Finland. Department of Electronics, Telecommunications and Informatics, University of Aveiro, Campus Universitario, Aveiro, Portugal. Institute of Parasitology, Biology Centre, Czech Academy of Sciences, Branišovská 31, České Budějovice, Czech Republic. cocercariae species and extended our analysis on 2 levels of cercariae behavior. First, we recorded qualitative swimming pattern of the cercariae, which included features such as presence or absence of resting phase and bending of the body or tail. Second, we quantified other behavioral features such as cercariae resting time between swimming phases (for types showing a 2-phase behavior) and swimming speed (applicable for most cercariae types). Finally, we discuss the applicability of these characteristics in the identification of different cercariae types and their usefulness for ecological groups working with furcocercariae species. MATERIALS AND METHODS Samples of snails consisting of Lymnaea stagnalis, Valvata macrostoma, Bathyomphalus contortus, and Planorbarius corneus were collected from Lake Konnevesi (62 37 N; E), central Finland, in August Sampling was conducted in a shallow littoral zone with a bottom substratum of sand and small rocks. A small sampling area ( m) was used to exclude differences in environmental conditions experienced by the snails. All snails were brought to the laboratory and checked for the release of furcocercariae by placing them individually in a small amount of water for a few hours. Eight species of 8 furcocercariae were found: Diplostomum pseudospathaceum (Niewiadomska, 1984), Ichthyocotylurus variegatus (Creplin, 1825), Cotylurus brevis (Dubois et Rausch, 1950), Cercaria spinulosa (Ginetsinskaya, 1959), Australapatemom sp., Australapatemom burti (Miller, 1923), Sanguinicola sp., and Bilharziella polonica (Kowalewski, 1895) (Table I). At first, all species were identified according to their morphology using the works of Odening and Bockhardt (1971), Combes (1980), Niewiadomska et al. (1997), and Gibson et al. (2002). During the snail collection, infected snails were stored in a cold room (8 C) to prevent further cercariae release during which they were fed with lettuce and detritus from the lake. For the observations on cercariae behavior, all snails were maintained in 20 C, which induced the cercariae production. Due to low prevalence of infection in the snails, cercariae of D. pseudospathaceum, I. variegatus, C. brevis, C. spinulosa, Australapatemom sp., and Sanguinicola sp. were each extracted from 3 individual snails. Although cercariae characteristics of 1 species may differ between different host individuals, i.e., between parasite genotypes, the variation observed in the present study was quite low (average overlap in cercariae values from different snails was %; see Results), which suggests that a sample of 3 snails was sufficient to capture the variation for the purpose of this study. Several newly emerged cercariae (maximum age 2 hr) of each species were then extracted from the 3 individual snails. In some cases, different numbers 1319

2 1320 THE JOURNAL OF PARASITOLOGY, VOL. 93, NO. 6, DECEMBER 2007 TABLE I. Qualitative behavioral characteristics of the 8 furcocercariae species (Diplostomum pseudospathaceum, Ichthyocotylurus variegatus, Cotylurus brevis, Cercaria spinulosa, Australapatemom sp., Australapatemom burti, Sanguinicola sp., and Bilharziella polonica) sampled from Lake Konnevesi, central Finland, in August Species Snail host Next host Swimming type Resting position D. pseudopathaceum L. stagnalis Fish Stop and go Tail bent 90 I. variegatus V. macrostoma Fish Stop and go Proximal tip of body bent, furcae in 90 angle C. brevis L. stagnalis Snail Continuous C. spinulosa L. stagnalis Fish Stop and go Straight tail and body, furcae in 180 angle Australapatemom sp. V. macrostoma Leech Continuous A. burti B. contortus Leech Stop and go Straight tail and body, furcae in 180 angle Sanguinicola sp. V. macrostoma Fish Stop and go Tail and body curved, body perpendicular to tail B. polonica P. corneus Bird Continuous Body perpendicular to tail* * Cercariae attached occasionally to water surface when a resting position was observed. of cercariae were extracted because snails shed too few cercariae. Parasite species A. burti and B. polonica were released only by single snails; therefore, quantitative measurements from these cercariae were not included in the between-species analysis, but they were still used to describe the overall qualitative behavioral features (see below). First, cercariae were studied under a binocular microscope in 20 C for qualitative behavioral features, i.e., swimming type (continuous or with separate resting and swimming phases [referred to as stop and go types]) and resting position (position of the furcae, bending of the body or tail) (Table I). Second, quantitative behavioral measurements were made. In stop and go types, these included resting time between the swimming phases (seconds), swimming time (seconds), distance swum during the swimming phase (millimeters), and swimming speed (millimeters per second), the latter of which was calculated from the measurements of swimming distance (millimeters) and swimming time (seconds). In some species, however, swimming times were long, in which cases the distance was measured during a shorter period, i.e., not corresponding to the distance swum during a complete swimming phase. Percentage of resting time for each activity cycle (resting time and swimming time combined), the number of cycles per min, and the movement per minute were also calculated. For continuous swimmers, swimming speed (millimeters per second) was calculated from the ratio between the distances swum (millimeters) during a period of time (seconds) (Table II). Behavioral parameters were determined by placing a group of cercariae of each species into a closed chamber (a mm Petri dish with a water volume of 9.6 ml), where they were monitored using a binocular microscope connected to a video camera. The size of the chamber was selected so that it did not constrain cercariae movement, but made it possible to acquire a focused image of the cercariae. This was verified in a series of preliminary trials with smaller containers, where constrained cercariae movement was clearly observed. All measurements were made from cercariae, which did not contact the walls of the chamber during their period of movement. This ensured best possible resemblance to a natural situation. Behavioral parameters for the cercariae were recorded in a horizontal or vertical setup depending on the main direction of movement of each cercariae species. This was assessed so that in cases where the cercariae showed clear tendency towards upper layers of the water column, the chamber was used in its vertical position and the binocular microscope tilted accordingly. In species showing no tendency, i.e., uniform distribution in the water column, measurements were taken using both orientations of the chambers. Overall, the selection of chamber did not affect cercariae behavior in these species, because no difference in the resting time (2-way analysis of variance [ANOVA] on log-transformed data from 2 cercariae species [cercariae species and type of chamber as factors: F 3, , P 0.757]) or swimming speed (ANOVA on log-transformed data from 2 cercariae species: F 3, , P 0.085) was detected between the chambers. Some swimming times were on the order of a tenth of a sec, which obviated the use of any humanoperated chronometer. In such cases, cercariae movement was first recorded with a video camera and then replayed in slow motion. This procedure was also of paramount importance for the accurate measurement of swimming distance. The data were analyzed using 1-way AN- TABLE II. Measures of the quantitative behavioral characteristics (mean SE) for the 8 furcocercariae species (Diplostomum pseudospathaceum, Ichthyocotylurus variegatus, Cotylurus brevis, Cercaria spinulosa, Australapatemom sp., Australapatemom burti, Sanguinicola sp., and Bilharziella polonica) sampled from Lake Konnevesi, central Finland, in August 2005: swimming phase (time, distance, and speed), resting phase (time and percentage of resting in 1 cycle, i.e., swimming time and resting time combined), and movement (number of cycles per minute and movement potential during 1 min). Note that the values for A. burti and B. polonica were measured from cercariae originating from single snails; therefore, they should be interpreted with caution. Swimming phase Resting phase Movement Species n of cercariae (n of snails) Time (s) Distance (mm) Speed (mm/s) Time (s) %of resting in 1 cycle Frequency (cycles/min) Movement during 1 min (mm) D. pseudospathaceum 75 (3) I. variegates 31 (3) C. brevis 29 (3) n.a.* n.a n.a. n.a. n.a C. spinulosa 31 (3) Australapatemom sp. 37 (3) n.a. n.a n.a. n.a. n.a A. burti 8 (1) Sanguinicola sp. 21 (3) B. polonica 6 (1) n.a. n.a n.a. n.a. n.a * n.a. not applicable. not a reliable quantitative metric (see text).

3 SANTOS ET AL. BEHAVIORAL TRAITS IN CERCARIAE 1321 FIGURE 1. Resting positions of the stop and go type cercariae: Diplostomum pseudospathaceum (A), Ichthyocotylurus variegatus (B), Cercaria spinulosa (C), Australapatemon burti (D), and Sanguinicola sp. (E). Bar 200 m. OVA on log-transformed data or nonparametric Kruskal Wallis test when the assumptions of the parametric tests could not be met. RESULTS Overall, the cercariae species in this study included 3 continuous swimmers and 5 stop and go types (Table I). Resting positions of the stop and go types were species specific, with differences in bending of the body, tail, and furcae, with an exception of C. spinulosa and A. burti whose resting positions were similar (Fig. 1). Also, 1 of the continuous swimmers, B. polonica, showed occasional resting position when the cercariae attached to the water surface for short periods. All cercariae moved with their tail first. For the purpose of this study, 3 quantitative parameters were subjected to statistical analysis, i.e., resting time and swimming time (for stop and go types), and swimming speed (for both types). Resting time of C. spinulosa was highly variable (ranging from 0.4 sec to 100 sec), which was a specific feature for this species, but prevented us from obtaining reliable measurements of resting time. As such, resting time was measured from 3 species, i.e., D. pseudospathaceum, I. variegatus, and Sanguinicola sp. Australapatemom burti was excluded from the analyses because the cercariae originated from only 1 snail. Within the species, the average overlap in values of resting times for the cercariae originating from different individual snails was 62.7%. However, in Sanguinicola sp., cercariae resting times differed between the snails so that the cercariae values from the first snail did not overlap with the third snail, but both did so with the second snail possessing intermediate values. In between-species comparisons, resting times were significantly different among all 3 species (1-way ANOVA on log-transformed data: F 2, , P 0.001), although values of individual cercariae overlapped to some extent (Fig. 2; Table II). Similarly, swimming times of the cercariae species were significantly different (Kruskal Wallis test: , df 2, P 0.001), but individual values overlapped again between the species. Swimming speed was not measured for Sanguinicola sp. cercariae, because they exhibited a somewhat circular swimming trajectory from which the swimming distance could not be measured reliably. Also, A. burti and B. polonica were excluded because all cercariae came from individual snails. Again, within the 5 other species, the average overlap in values of swimming speeds for the cercariae originating from different individual FIGURE 2. Resting times (seconds) of the 4 stop and go type cercariae: Diplostomum pseudospathaceum, Ichthyocotylurus variegatus, Australapatemon burti, and Sanguinicola sp. Note that the cercariae of A. burti originated from a single snail and therefore the values were not used in the between-species analysis. snails was 51.4%. Swimming speed was also significantly different between the species (1-way ANOVA on log-transformed data: F 4, , P 0.001) (Fig. 3; Table II). Multiple comparisons revealed that the species fell into 3 groups: the first group was formed by faster swimming D. pseudospathaceum and I. variegatus; the second group by C. brevis with an intermediate speed; and the third group by C. spinulosa and Australapatemom sp., with slower swimming speed (Tukey s test: P for all comparisons) (Fig. 3; Table II). DISCUSSION Trematode cercariae generally show a high diversity of detailed behavioral features (Combes et al., 1994; Haas, 1994), which could help to elucidate species identities in cercariae FIGURE 3. Swimming speed (millimeters per second) of the 7 furcocercariae species: Diplostomum pseudospathaceum, Ichthyocotylurus variegatus, Cotylurus brevis, Cercaria spinulosa, Australapatemom sp., Australapatemom burti, and Bilharziella polonica. Different letters (a c) denote statistically significant differences (P 0.001) after Tukey s pairwise comparisons, i.e., cercaria species marked with different letters differ statistically. Note that the cercariae of A. burti and B. polonica originated from single snails; therefore, the values were not used in the between-species analysis.

4 1322 THE JOURNAL OF PARASITOLOGY, VOL. 93, NO. 6, DECEMBER 2007 showing significant morphological overlap. We examined this in 1 such group by determining qualitative and quantitative behavioral features of a community of furcocercariae species under standardized conditions. Our aim was to sort out the details of how this information could be used in species separation, essentially to determine the level of precision at which this could work. First, measurements of cercariae behavior are generally case sensitive, i.e., influenced by conditions where the measurements are taken, but some comparisons of the species specific characteristics to existing data can be made. Overall, resting positions of the stop and go types resembled those described previously for D. pseudospathaceum, I. variegatus, C. spinulosa, A. burti, and B. polonica (Szidat, 1929; Zajíček and Valenta, 1964; Odening and Bockhardt, 1971; Niewiadomska and Kiseliene, 1994). However, to our knowledge, behavioral characteristics have not been described previously for Sanguinicola sp.; thus, this work provides the first data for this genus. Swimming times for the cercariae of D. pseudospathaceum were lower compared with the closely related species, D. spathaceum (Karvonen et al., 2006), although the absolute difference in the mean values was small and may very well reflect differences in the measurement conditions. In contrast, the swimming speed of the cercariae was very similar compared with D. spathaceum (Graefe and Burkert, 1972), which could reflect similarities in the life cycles (next host characteristics) of these species. Similarly, Zajíček and Valenta (1964) reported high swimming times from A. burti, which is consistent with our observations, although measurements were made from cercariae of an individual snail. In general, qualitative characteristics of cercariae behavior, such as the type of swimming (stop and go or continuous) and resting position, are likely to be related to the location of the next host. For example, most of the stop and go types in this study infect fish as the second intermediate host, although broad generalizations cannot be made from the present data. Similarly, quantitative characteristics may also be related to transmission, although this has probably received less attention. Measurements of these from a broader range of cercariae species could reveal general patterns related to transmission to certain types of hosts. Second, qualitative behavioral patterns with respect to species separation were species specific, particularly in stop and go types. Diplostomum pseudospathaceum exhibited a resting position, with the tail bent in a 90 angle, which has been used as a distinctive characteristic for D. spathaceum and D. pseudospathaceum, and also for other species of the genus (e.g., Niewiadomska and Kiseliene, 1994; Karvonen et al., 2006). However, the taxonomy of Diplostomum species has been problematic (Valtonen and Gibson, 1997), and it remains unclear how other features of cercariae behavior differ among the numerous Diplostomum species described previously (Niewiadomska and Kiseliene, 1994; but see Karvonen et al., 2006). Resting positions of the other species were also different, except for C. spinulosa and A. burti. In these species, the most obvious qualitative difference was that they were released from different snail host species. It has been proposed that trematodes show very strict host specificity in their molluscan hosts (e.g., Gibson and Bray, 1994), suggesting that the host species could reflect parasite species identity. However, strict host specificity of trematodes is not supported by recent studies (e.g., Donald et al., 2004; Karvonen et al., 2006), which suggests that it is not a reliable measure of species identity. For example, D. spathaceum infects at least 3 different snail species in the present study system, although L. stagnalis clearly is the primary host (Karvonen et al., 2006). Thus, other behavioral measures to differentiate C. spinulosa and A. burti are needed. In cercariae showing continuous swimming, identification based on behavior is generally not that straightforward, as the resting stages are absent. The species observed in this study were also very similar, except for B. polonica, which showed occasional attachment to the water surface making this species clearly different from the 2 similar species, i.e., C. brevis and Australapatemom sp. Quantitative measurements of swimming speed, however, indicated differences between these 2 species without any between-species overlap in the observations of individual cercariae. In general, swimming speed was a relatively consistent measure, showing less within-species variation compared, for example, with resting times of the stop and go types. Furthermore, it divided the species into 3 separate groups, with little or no overlap in individual values between the groups (particularly the groups with highest [D. pseudospathaceum and I. variegatus] and lowest values [C. spinulosa and Australapatemom sp.]). All this information suggests that swimming speed could provide a consistent measure for separation of cercariae species. It is clear that the measurement of swimming speed is technically more challenging compared with, for example, the measurement of resting time of cercariae. Nevertheless, our overall experience is that this rapidly becomes a straightforward methodology once the measurement system has been established. In conclusion, our results suggest that qualitative behavioral traits of cercariae combined with quantitative analysis when necessary can be used in the separation of furcocercariae species. As stressed here, these traits, as well as any morphological traits, are likely to be case sensitive to some extent and thus influenced by measurement conditions (see Cort and Brackett, 1937) and specific characteristics of local host and parasite populations. Indeed, this may be 1 of the reasons for general taxonomic confusion associated with some trematode groups. Overall, this suggests that the selection of available and appropriate behavioral variables is likely to be specific to each particular population and species composition. Hence, it is important to establish a set of variables, which could include those described here, or other more suitable variables. An interesting next step would also be to explore how behavioral traits differ among closely related species within a genus or among species with similar next host characteristics. Although some qualitative and quantitative differences have been reported in such groups (e.g., Cort and Brackett, 1937; Karvonen et al., 2006), more comprehensive studies are needed focusing on issues of species separation and life history comparisons. ACKNOWLEDGMENTS We thank Professor Katarzyna Niewiadomska (University of Warsaw, Warsaw, Poland) for help and suggestions. This study was supported by Portuguese National Science Foundation FCT sabbatical grant BSAB 492/2005, Kone Foundation, and the Academy of Finland Centre of Excellence in Evolutionary Research.

5 SANTOS ET AL. BEHAVIORAL TRAITS IN CERCARIAE 1323 LITERATURE CITED COMBES, C Atlas mondial des cercaires. Mémoires du Muséum National d Histoire Naturelle, Série A, Zoologie 115: , A. FOURNIER, H. MONE, AND A. THERON Behaviours in trematode cercariae that enhance parasite transmission: Patterns and processes. Parasitology 109(Suppl.): S3 S13. CORT, W.W.,AND S. BRACKETT Identification of strigeid cercariae by differences in their behavior during free life. Journal of Parasitology 23: DONALD, K. M., M. KENNEDY, R. POULIN, AND H. G. SPENCER Host specificity and molecular phylogeny of larval Digenea isolated from New Zealand and Australian topshells (Gastropoda: Trochidae). International Journal for Parasitology 34: GIBSON, D. I., AND R. A. BRAY The evolutionary expansion and host-parasite relationship of the Digenea. International Journal for Parasitology 24: , A. JONES, AND R. A. BRAY Keys to the Trematoda. Vol. 1. CAB International, Wallingford, U.K., 521 p. GRAEFE, G., AND D. G. BURKERT Zur Lokomotionstechnik von Diplostomatiden- und Echinostomatiden-Cercarien (Trematoda). Zoologischer Anzeiger 188: HAAS, W Physiological analyses of host-finding behaviour in trematode cercariae: Adaptations for transmission success. Parasitology 109(Suppl.): S15 S29. KARVONEN, A., P. TERHO, O. SEPPÄLÄ, J. JOKELA, AND E. T. VALTONEN Ecological divergence of closely related Diplostomum (Trematoda) parasites. Parasitology 133: MILLER, H. M Variety of behavior of larval trematodes. Science 68: NIEWIADOMSKA, K Verification of the life-cycles of Diplostomum spathaceum (Rudolphi, 1819) and D. pseudospathaceum Niewiadomska, 1984 (Trematoda, Diplostomidae). Systematic Parasitology 8: , AND V. KISELIENE Diplostomum cercariae (Digenea) in snails from Lithuania. II. Survey of species. Acta Parasitologica 39: , E. T. VALTONEN, AND R. SIDDAL Cercariae from Lymnaea stagnalis in lake Kuuhankavesi (central Finland). Acta Parasitologica 42: ODENING, K., AND I. BOCKHARDT Der Lebenszyklus des Trematoden Cotylurus variegatus im Spree-Havel-Seengebiet. Biologisches Zentralblatt 90: SZIDAT, L Zur Entwicklungsgeschichte des Bluttrematoden der Enten, Bilharzia polonica Kow. I. Morphologie und Biologie der Cercariae von Bilharziella polonica Kow. Zentralblatt für Bakteriologie, I. Abteilung 111: VALTONEN, E.T., AND D. I. GIBSON Aspects of the biology of diplostomid metacercarial (Digenea) populations occurring in fishes in different localities of northern Finland. Annales Zoologia Fennici 34: ZAJICEK, D., AND Z. VALENTA Contribution to the occurrence of furcocercous cercariae in some regions of Bohemia. Československá Parasitologie 11:

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