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Temperature-related intraspecific variability in the behavioral manipulation of acanthocephalan parasites on their gammarid hosts.

Abstract. Understanding the effect of temperature on ecologically important species has become a major challenge in the context of global warming. However, the consequences of climate change cannot be accurately predicted without taking into consideration biotic interactions. Parasitic infection, in particular, constitutes a widespread biotic interaction, and parasites impact their hosts in multiple ways, eventually leading to consequences for communities and ecosystems. We explored the effect of temperature on the anti-predator behavior of a keystone freshwater invertebrate, the amphipod Gommants fossarum. Gammarids regularly harbor manipulative acanthocephalan parasites that modify their anti-predator behavior in ways that potentially increase the probability of trophic transmission to their definitive hosts. We investigated the impact of temperature on gammarids infected by two acanthocephalan parasites, Pomphorhynchus tereticollis and Polymorphus minutus. Uninfected and naturally infected gammarids were acclimatized to different temperatures, and their behavior was measured. Our results showed that the effect of infection on the phototaxis of gammarids increased with increasing temperature, with a stronger effect induced by P. tereticollis. In contrast, temperature had no effect on the alteration of refuge use or geotaxis observed in infected gammarids. Our results provide the first direct evidence that temperature can affect the extent of behavioral alteration brought about by certain parasite species. However, the consequences of increased trophic transmission remain elusive; the supposedly key anti-predatory behavior was not significantly affected by exposure of gammarids to different temperatures.


Although parasites have been ignored for decades in the field of ecology, they are now widely recognized as important actors within ecosystems (Hudson et al., 2006; Lefevre et al., 2009; Hatcher et al., 2012). Parasitic organisms may represent close to half of all biodiversity, according to certain estimations (Poulin and Morand, 2000; Dobson et al., 2008), making parasitic infection one of the most common biotic interactions. Parasites have multiple impacts on their hosts that can have consequences on larger scales (Lefevre et al., 2009; Hatcher et al., 2012). Differential pathogenic effects on several competing host species might, for instance, reverse the outcome of competition or lead to the coexistence of species that would exclude each other in the absence of parasites (Hatcher et al., 2012). Parasites with complex life cycles that rely on trophic transmission are particularly likely to affect many components of the ecosystems, because they are embedded in large food webs and have the potential to affect several host species in succession. Some of these parasites, in particular, can induce phenotypic changes in their intermediate hosts that are supposed to increase the probability of predation by their definitive hosts, thus increasing their own probability of transmission (Poulin and Thomas, 1999; Moore, 2002). Many of these effects lead to deep changes in communities and ecosystems such that these parasites are sometimes referred to as ecosystem engineers (Thomas et al., 1998, 1999; Sato et al., 2012).

In the current context of global change, understanding how environmental conditions might alter ecologically important species has become a major challenge, notably due to the necessity of making accurate predictions about the consequences of such changes. Taking into consideration biotic interactions, and those with parasites, in particular, is therefore very important, especially when considering that climate change may have unpredictable consequences on both inter-and intra-specific interactions (Tylianakis et al., 2008; Rosenblatt and Schmitz, 2014). Temperature stands as a major parameter affecting many parasite-host systems (Marcogliese, 2001 ; Harvell et al., 2002; Barber et al., 2016), and it is likely that the impact of global change on ecologically important species may depend on the parasites they harbor. Notably, the nature of the cumulative effect of parasitism and temperature on hosts, whether additive or interactive, is hardly predictable (Labaude et al., 2017).

Gammarids are widespread and abundant crustacean am-phipods that are often seen as key species in freshwater ecosystems. There, they constitute both important prey and predators for many species, modulating the composition of freshwater macroinvertebrates (Degani et al., 1987; Friberg et al., 1994; MacNeil et al., 1997; Kelly et al., 2002). They also play a major role in the maintenance of water quality through their roles as scavengers and shredders (MacNeil et al., 1997), particularly by consuming dead leaves (Piscart et al., 2009; Constable and Birkby, 2016). Gammarids are thus of significant ecological and economic importance; water quality is a key parameter in the emergence of waterborne diseases, ecosystem functioning, and maintenance of biodiversity (Klaphake et al., 2001).

Gammarids serve as intermediate hosts for several species of acanthocephalan parasites, those that use either birds or fish as definitive hosts. These parasites affect their gammarid hosts in several ways. Acanthocephalan parasites can manipulate the behavior of gammarids in a way that appears to increase their probability of being preyed upon by their definitive hosts (Lagrue et al., 2007; Perrot-Minnot et al., 2007; Dianne et al., 2011; but see Perrot-Minnot et al., 2012). Along with other impacts that parasites can have on their hosts, such as alteration of food consumption (Fielding et al., 2003; Medoc et al., 2011; Labaude et al., 2017) or metabolic rate (Rumpus and Kennedy, 1974; Labaude et al., 2015a), such behavioral manipulations might affect the role of gammarids within ecosystems.

Temperature affects several traits in the association of acanthocephalan parasites and their gammarid hosts. Both time of development of parasites (Olson and Pratt, 1971; Tokeson and Holmes, 1982) and their success in establishing themselves in their definitive fish host (Sheath et al., 2016) depend on temperature. Yet temperature also affects the metabolism (Pockl and Humpesch, 1990), growth (Moenickes et al., 2011 ), and consumption of gammarids (Foucreau et al., 2016), which potentially affect their interaction with parasites. In addition, the cumulative effect of acanthocephalan parasites and temperature on gammarids' feeding behavior depends on the gammarids' aggregation context, with the two parameters having different consequences for leaf consumption by isolated individuals and individuals in groups (Labaude et al., 2017).

Temperature may also lead to variation in the rapidity or intensity of parasite manipulation (i.e., how parasites manipulate host behavior in connection with predation probability), whether directly or due to its effects on other parameters. Thus far, however, there is only indirect evidence of temperature's effects (reviewed in Labaude et al., 2015b). For instance, gammarids that were experimentally infected during winter were slower to display altered behaviors than those gammarids that were infected in spring by the same parasite populations (Franceschi et al., 2010). Such results might arise from a positive effect of temperature on host and parasite metabolism. Continuing this hypothesis, it is possible that higher temperatures experienced by infected gammarids also lead to stronger manipulation in those cases where such manipulation depends on host or parasite metabolism. Moreover, gammarid survival decreases at high temperatures (Maazouzi et al., 2011 ; Foucreau et al., 2014), for which parasites would benefit by increasing their manipulations to secure their transmission (Thomas et al., 2002, 2011 ). Given the predicted increase of temperature in the coming years, improving our understanding of the consequences of temperature on host-parasite relationships is particularly relevant (Labaude et al., 2017).

We tested the effect of exposure to different temperatures on the behavioral changes induced by two acanthocephalan species, the fish parasite Pomphorhynchus tereticollis (Rudolphi, 1809) and the bird parasite Polymorphus minutas (Zeder, 1800), on their gammarid host Gammarus fossarum Koch, 1836. These parasites manipulate different behaviors that are believed to be specific to the definitive host species (Tain et al., 2006). While P. tereticollis induces an inversion of the photo-phobic behavior of its intermediate host (Tain et al., 2006) and a decrease in its use of refuges (Perrot-Minnot et al., 2007), infection by P. minutus leads to reversed geotaxis, with gam-marid individuals staying closer to the water surface than the uninfected ones (Bauer et al., 2005). We relied on gammarids that were naturally infected with cystacanth parasites, that is, those at the last larval stage that is infective for the definitive host and at which such changes occur in hosts, and studied the effect of acclimatization at different temperatures on the behavior of uninfected and infected individuals.

Materials and Methods

Sampling and acclimatization

Gammarus fossarum individuals were collected in the Norges River (eastern France, 47[degrees]21 '43' N, 5[degrees]09'30" E, where gammarids are infected with Pomphorhynchus tereticollis), in September 2015, and in the Veze River (eastern France, 47[degrees]14'2" N, 5[degrees]34'37" E, where gammarids are infected with Polymorphus minutus) in June 2016, using a kick sampling method with ahand net. The Norges River contains only Gammarus fossarum species (Lagrue et al., 2014; Labaude et al., 2017). Although Lagrue et al. (2014) found that more than half of the gammarids from the Veze River belonged to the closely related Gammarus pulex species, more recent genetic analyses of 457 individuals sampled in the Veze River in May 2015 showed that about 90 percent (n = 410)belonged to G. fossarum (S. Labaude, unpubl. data). Given the small proportion of G. pulex--and since the two cryptic species are often considered as a single taxonomic unit (Karaman and Pinkster, 1977)--all individuals were used in this study. The brightly colored cystacanth stages of these parasites are visible through the gammarid cuticle, allowing preliminary selection of infected individuals directly in the field. Uninfected individuals were also collected.

Individuals from each population were randomly allocated to several groups that were acclimatized at different temperatures for 12 days in the laboratory. Those from the Norges River were acclimatized at three temperatures (10 [degrees]C, 14 [degrees]C. or 18 [degrees]C). In contrast, animals from the Veze River were separated into two temperature groups only (14[degrees]C or 18[degrees]C), due to sampling limitations resulting from the low prevalence of infection with Polymorphus minutus. Temperatures were chosen in accordance with naturally fluctuating temperatures experienced by gammarids in their habitat (Pockl et al., 2003), and fell within the range of temperatures measured within the two rivers in 2015 (S. Labaude, unpubl. data). To limit stress, animals were maintained together in groups at each temperature in an oxygenated mix of water collected in their river and dechlorinated, UV-treated tap water. They were fed ad libitum with conditioned elm leaves and maintained under a 12 h : 12 h light : dark cycle regime. Due to different technical requirements associated with the behavioral tests, water temperature was controlled in two different ways. Because individuals had to be visible from above during the behavioral tests, individuals from the Norges River were maintained in water baths, following Labaude et al. (2017). Boxes containing individuals (and additional test devices) were plunged into water that was constantly pumped through a temperature control device (TANK TK-1000 Chiller; Teco Energy, Tampa, FL). Animals from the Veze River, which were tested in vertical devices, were maintained and tested in refrigerators with transparent doors (Liebherr FKv 5443; Liebherr, Bulle, Switzerland). These two systems allowed for acclimatization and experiments for each population at all temperatures to occur concomitantly in the same room. Water temperature was controlled daily using digital thermometers.

Phototaxis and refuge use

Overall, 368 individuals (167 infected by Pomphorhynchus tereticollis and 201 controls) from the Norges River were used for phototaxis tests. Of these, 176 individuals (76 infected and 100 controls) were randomly chosen to be tested for refuge use. The two sets of experiments were conducted during the same day.

After the period of acclimatization to different temperatures, single individuals were introduced into horizontal glass tubes (22-cm long, 3.2-cm diameter) containing a dark zone (half of the tube was covered with black plastic to ensure complete opacity) and a light zone, following the design described in Perrot-Minnot (2004). Before gammarids were introduced, tubes were filled with aerated water. Water temperature was maintained during the course of the experiment with the same device as described for acclimatization. After 5 min of habituation in the tube, the position of every individual was recorded every 30 s over 5 min and scored as 0 (dark zone) or 1 (light zone). Summed phototaxis scores for each individual ranged from 0 (strongly Photophobic, always in the dark zone) to 11 (strongly photophilic, always in the light zone).

To test for the use of refuges, single individuals were placed in boxes (10.5 x 16 cm) filled with 250 ml of oxygenated water with the temperature controlled for each group, as previously described. A refuge was available in each box and consisted of a saucer of a terracotta pot (8.5-cm diameter) cut in half, with a 1-cm hole in the convex part (see Dianne et al., 2014). After 5 min of habituation of gammarids in the device, the position of each individual was recorded every 2 min over a 30-min observation period and scored as 0 (outside the refuge) or 1 (inside the refuge). Summed refuge scores ranged from 0 (always outside the refuge) to 16 (always inside the refuge) for each individual.

For the two tests, a random number was assigned to each individual to ensure that the experimenter was unaware of individuals' infection status.


A total of 51 individuals that were infected by Polymorphus minutus and 59 uninfected animals from the Veze River were used for geotaxis tests.

Geotaxis, or the response of individuals to gravity, was estimated as the average vertical position of individuals in the water column. After the acclimatization period, single individuals were introduced into 500-ml-graduated measuring cylinders (35 cm high, 6 cm diameter) filled with aerated water. Cylinders were divided vertically into five zones of equal height. A plastic net was placed along the inside wall of each cylinder, providing gammarids a substrate on which to cling, as is available on river banks. This factor was important because both swimming and clinging behaviors can be altered by the parasite (Bauer et al., 2005). Each cylinder was placed in a refrigerator at the relevant temperature. Light was directed only horizontally, through the glass door, thus preventing any confounding vertical phototactic reaction. After 2 min of habituation in the cylinder, the position of each gammarid was recorded every 30 s for 5 min; a score was given according to the zone within the water column (from 1 for the bottom to 5 for the top). Summed geotaxis scores ranged from 11 (always at the bottom) to 55 (always at the top) for each individual.

Measurements and dissections

At the end of the experiment, the sex of each individual was determined using the size and shape of its first and second pairs of gnathopods, which are sexually dimorphic in amphipods (Hume et al., 2005). All individuals were measured (height of the fourth coxal plate) using a Nikon ZMZ1500 dissecting microscope (Nikon, Tokyo, Japan) and LUCIA G ver. 4.81 software (Informer Technologies, Roseau, Dominica), and dissected. The developmental stage (acanthella or cysta-canth) and the species of parasites found within the gammarids were determined based on morphological identification. Because manipulation of the parasite depends on both acanthocephalan species and developmental stage, only individuals harboring Pomphorhynchus tereticollis (for the phototaxis and refuge use tests) and Polymorphus minutus (for the geotaxis tests) parasites at the cystacanth stage were retained (hereafter referred as "parasitized" individuals). Individuals harboring other acanthocephalan species (e.g., a few Pomphorhynchus laevis and Echinorhynchus truttae were found) or acanthella stages were discarded. Gammarids in which no parasite could be found were considered as "control" individuals.

Data analyses

None of the three score groups (phototaxis scores, refuge scores, and geotaxis scores) met conditions of normality or homoscedasticity (i.e., homogeneity of variance), even after data transformation. We therefore used nonparametric statistics. In both populations, gammarid size did not differ between the parasitized and control individuals (data not shown) and thus was not considered in subsequent analyses. Comparisons between males and females for each infection status and at each temperature showed no differences in the scores of individuals for the three behaviors tested (data not shown). Therefore, sex was not considered in subsequent analyses.

First, the effect of temperature on each score was assessed using Kruskal-Wallis tests. The effect size of the differences between each temperature was then calculated for each score and for each infection status (control or parasitized) using Cliff's delta (Cliff, 1996). Cliff's delta was also used to compare the scores between control and parasitized individuals at each temperature. Cliff's delta is a scaleless parameter, ranging from -1 to 1, that is robust to non-normally distributed data. It is used to represent the size of the effect, which, in this case, was the difference between two groups, as well as the direction of this difference. Moreover, its confidence intervals can be used to assess the significance between these differences, replacing classical statistic tests or post hoc tests. Medians and 95% confidence intervals of the Cliff's delta were calculated using the R package "orddom" (ver. 3.1) (Rogmann, 2013). Other statistical analyses were performed using R ver. 3.1.1 software (R Core Team, 2014).


Temperature significantly affected the amount of time spent in light (i.e., the "phototaxis score") of Gammarus fossarum individuals infected by Pomphorhynchus tereticollis (Kruskal-Wallis, [[chi].sub.2] = 22.86, df = 2, P < 0.0001, Fig. 1 A), and control individuals (Kruskal-Wallis, [[chi].sub.2] = 23.30, df = 2, P < 0.0001, Fig. 1A). The phototaxis score was significantly higher at 14 [degrees]C and 18 [degrees]C than at 10[degrees]C in both parasitized and control individuals (Fig. 2A). However, while there was a clear trend for the phototaxis score to increase with temperatures between 14 [degrees]C and 18[degrees]C for parasitized individuals, the photo-taxis score of control individuals did not differ significantly between these two temperatures (Fig. 2A); indeed, a trend of scores to decrease was noted. As a result, the difference in behavior between the control and parasitized individuals was significant at 14 [degrees]C and 18[degrees]C, with a stronger effect seen at 18[degrees]C(Fig. 2B).



Temperature had no effect on time spent inside refuges ("refuge score") for both the control (Kruskal-Wallis, [[chi].sub.2]=0.57, df = 2, P = 0.75, Fig. 1B) and infected individuals (Kruskal-Wallis, [[chi].sub.2] = 183, df = 2, P = 0.40, Fig. 1B). The refuge score of individuals parasitized by Pomphorhynchus tereticollis was lower than that of the controls (Fig. 1B), illustrating a lower trend for use of refuges, but this difference was significant only at 18 [degrees]C (Fig. 2B). The nonsignificant differences were probably due to high inter-individual variation relative to the small sample size.

Correlations between phototaxis scores and refuge scores were all non-significant. The only trend observed was a negative correlation in parasitized individuals at 18 [degrees]C (Table 1 ), with the more photophilic animals spending more time out of the refuges.

The geotaxis score of Gommants fossarum individuals infected by Polymorphus minimis was significantly higher than the score of control individuals (Figs. 2B, 3). Geotaxis scores were not influenced by temperature, with no differences noted between the two temperatures tested for both the parasitized and control individuals (Figs. 2, 3).


The temperature to which Gammarus fossarum individuals were exposed for two weeks affected the intensity of their phototaxis, particularly in those infected with Pomphorhynchus tereticollis parasites. However, temperature had no impact on the time spent by any gammarids inside refuges, either the infected or control animals. No effect of temperature was found on gammarids' geotaxis, whether infected or not by Polymorphus minutus parasites.

The differences in phototaxis observed between infected and control individuals across the three tested temperatures suggest that parasite manipulation was less efficient at low temperatures. Although both infected and uninfected animals were Photophobic at low temperatures, a gradual reversal of photophobia was observed in infected individuals at higher temperatures. This phenomenon stabilized in control individuals at the highest temperature. The increase in manipulation of gammarids by Pomphorhynchus tereticollis may have been due to a physiological effect of temperature. Indeed, the metabolism of ectotherm species increases with temperature (Gil-looly et al., 2001), including in acanthocephalan parasites, which develop faster at high temperatures (Olson and Pratt, 1971; Tokeson and Holmes, 1982). Thus, if manipulation of host behavior is influenced by the physiology of parasites, it is possible that increased temperatures led to more pronounced manipulation. However, such a phenomenon does not explain the increased phototaxis that was also observed in uninfected individuals between 10 [degrees]C and 14 [degrees]C. The differences in phototactic behavior observed at different temperatures may instead stem from the mechanisms underlying this behavior. Serotonin plays a major role in the expression of phototactic behavior in gammarids: Pomphorhynchus parasites increase brain serotoninergic activity of gammarids (Tain et al., 2006, 2007), and experimental injection of serotonin in uninfected individuals mimics the behavioral changes induced by parasites (Perrot-Minnot et al., 2014). The mechanisms by which acanthocephalans induce modifications in gammarids' serotoninergic activity are unknown (Lafferty and Shaw, 2013). However, serotonin production increases with increased temperatures in invertebrates (Stefano and Catapane, 1977; Stefano et al., 1978); many visual neural processes in invertebrates are also affected by increasing temperatures (Lim-Kessler et al., 2008). These changes are associated with modifications of other neuromodulators (Stefano and Catapane, 1977; Stefano et al., 1978), such that the consequences of the modifications can hardly be predictable. However, an increase in serotonin levels could explain the increase of phototaxis between the lowest temperature and the highest temperatures in our study, including in uninfected gammarids. It is possible that in infected individuals the level of serotonin due to increased temperature and parasitic infection combine in the gammarid brain to produce a higher photophilic response. Serotonin levels were not measured here. Therefore, since the invertebrate nervous system has a number of mechanisms designed to maintain homeostatic function in spite of temperature-driven changes (Lim-Kessler et al., 2008), further studies are needed to explore the mechanisms of the link between temperature, acanthocephalan parasites, and photophily in gammarids to verify this hypothesis.

Although variations in serotonin levels explain variations in the phototaxis behavior of gammarids, they have no significant effect on the gammarids' ability to use refuges (Perrot-Minnot et al., 2014). This fact may explain why there was no significant effect of temperature on this trait, and why there was no correlation between these two behaviors. Similarly, the manipulation of Gammarus fossarum by Polymorphu minutas, in terms of geotaxis, was not affected by temperature, although the lowest temperature was not tested. However, alteration of geotaxis may not rely on the same mechanisms as the ones involved in changing phototaxis. Indeed, Tain et al. (2006) showed that the geotaxis of gammarids was not affected by experimental injections of serotonin, and infection by P. minutus did not induce modifications in the serotoninergic activity of gammarids. A recent study suggested a role of anerobic metabolism and hypoxia in the manipulation induced by P. minutas: uninfected Gammarus roeseli displayed a negative geotaxis under hypoxia, while an injection of lactate and succinate in uninfected gammarids also mimicked the parasite-induced reversion of geotaxis (Perrot-Minnot et al., 2015). It would be interesting to test the effect of temperature variations large enough to induce higher changes in the amount of oxygen dissolved in the water. If this were the mechanism, we would expect the geotaxis of both infected and uninfected individuals to increase at high temperatures.


Overall, our study suggests that temperature may be responsible for variations in efficiency of manipulation by acanthocephalans of certain gammarid behaviors. Global temperature increase, in particular, may induce higher manipulation efficiency of some parasites, while other aspects of manipulation, or behavioral changes in other species, might not be affected. Some of our results were in line with those obtained by Benesh et al. (2009) in isopods. They found that the intensity of phenotypic changes induced by the acanthocephalan Acanthocephalus lucii varied between seasons, but experimental exposure to different temperatures did not change parasitic manipulation intensity of host behavior. Our study showed that some components of parasite-induced behavioral changes may be affected by temperature variation. Although the metabolism of acanthocephalan parasites is highly dependent on temperature, thus resulting in longer developmental time during cold periods (Olson and Pratt, 1971 ; Tokeson and Holmes, 1982), variations in the rapidity of their transmission to the next host may also arise from differences in their manipulation--and partly explain the seasonal distribution documented in some acanthocephalan parasites (Van Cleave, 1916; Muzzall and Rabalais, 1975: Brown, 1989).

Parasites have numerous effects on communities and ecosystems, especially through manipulation of their hosts' behavior (for reviews, see Lefevre et al., 2009; Labaude et al., 2015b). Consequently, modifications in parasitic manipulation following changes in temperature are also likely to have consequences at larger scales. Acanthocephalan parasites notably are responsible for many modifications in the ecology of gammarids, including their feeding behavior and microhabitat choice (MacNeil et al., 2003; Labaude et al., 2017). More to the point, an increase in facilitation of predation induced by parasites in response to increasing temperature may affect food webs through changes in the interaction between gammarids and their predators, as well as the dynamics of the populations of parasites, hosts, and their predators. However, further studies are needed to determine the effect of temperature on the ecological outcome of manipulation, that is, temperature's effects on ease of predation induced by parasites. Indeed, infected gammarids are more preyed upon by the definitive hosts of parasites than are uninfected gammarids (Bethel and Holmes, 1977; Perrot-Minnot et al., 2007; Jacquin et al., 2014), but only certain behavioral changes have been shown to be linked to predation enhancement. More precisely, in gammarids the presence of refuges and the intensity of their use were directly linked to differences in the predation rate of gammarids infected by Pomphorhynckus parasites versus their uninfected counterparts (Kaldonski et al.,, 2007; Dianne et al., 2011, respectively); no such link was seen in the parameter of intensity of change in phototaxis (Perrot-Minnot et al., 2012). Similarly, the reversed geotaxis behavior was responsible for increased predation in gammarids infected by Poly-morphus parasites (Jacquin et al., 2014). It is worth noting here that the only behavior affected by temperature is the one for which no causal link with predation enhancement could be established. However, many other parameters may interact to affect the success of predation. Gammarid behavior depends on predation risk (Medoc et al., 2009; Durieux et al., 2012; Lewis et al., 2012), while temperature may also alter the behavior of the predators themselves (Brett, 1971 ; Elliott, 1976). Temperature is likely to affect other parameters, such as parasite reproduction (Barber et al., 2016), leading to modifications in the population dynamics of both hosts and parasites that are hardly predictable.

Finally, we did not control environmental conditions during parasite development, a paramater that can lead to other sources of variability. For instance, acanthocephalans develop faster at high temperatures (Olson and Pratt, 1971; Tokeson and Holmes, 1982), and their manipulation efficiency increases with time after they have reached the cystacanth stage (Franceschi et al., 2008; Labaude et al., 2015a). Thus, it cannot be ruled out that in our experiments involving naturally infected gammarids, those individuals maintained at 18 [degrees]C harbored parasites that had already reached their highest manipulative intensity, while the manipulative intensity of gammarids kept at lower temperatures was still increasing. In addition, gammarid metabolism increases with temperature to a certain extent (Roux and Roux, 1967; Pock1 and Humpesch, 1990; Issartel et al., 2005), along with their mortality (Maazouzi et al., 2011; Foucreau et al., 2014). Because parasites depend completely on the survival of their hosts before transmission, they would benefit by increasing their manipulation efforts when their hosts' life expectancy decreases in order to secure their transmission (Thomas et al., 2002, 2011). Consistent with this hypothesis, Poulin (1993) found that the intensity of behavioral changes induced by trematode parasites was greater when their intermediate fish hosts were older. However, contradicting this hypothesis is the observation that no significant changes in refuge use were observed in Gammarus pulex that were infected with Pomphorhynckus laevis under different survival conditions (Labaude et al., 2015a). Thus, future studies may benefit from investigating the effect of temperature, using experimental infestations, to control for environmental conditions during development of parasites.


We thank the ANR (Agence Nationale de la Recherche, Paris) (Grant ANR-13-BSV7-0004-01) for financial support. SL was supported by a Doctoral grant from the Ministere de l'Education Nationale, de l'Enseignement Superieur et de la Recherche. We thank the associate editor, Charles Derby, Zen Faulkes, and the anonymous reviewers for their helpful comments.

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Universite de Bourgogne Franche-Comte, UMR CNRS 6282 Biogeosciences, Dijon, France

Received 2 March 2017; Accepted 20 March 2017: Published online 17 May 2017.

(*) To whom correspondence should be addressed. E-mail: s.labaude
Table 1
Correlations (Spearman's rho) between phototaxis and refuge use scores
in control and parasitized Gammarus fossarum, at each temperature (10
[degrees]C, 14 [degrees]C, and 18 [degrees]C

Infection status   Temperature   Spearman's rho   P-value

Control           10[degrees]C      -0.167      0.344
                  14[degrees]C      -0.310      0.124
                  18[degrees]C      -0.053      0.743
Parasitized       10[degrees]C      -0.017      0.936
                  14[degrees]C      -0.186      0.432
                  18[degrees]C      -0.416      0.020 (*)

(*) Non-significant difference after Bonferroni correction.
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Author:Labaude, Sophie; Cezilly, Frank; Rigaud, Thierry
Publication:The Biological Bulletin
Date:Apr 1, 2017
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