Hydrobiologia 459: 9–18, 2001. © 2001 Kluwer Academic Publishers. Printed in the Netherlands.
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Consequences of a drought on freshwater gastropod and trematode communities Claudia G´erard Laboratoire de Zoologie et d’Ecophysiologie, UMR CNRS 6553, Universit´e de Rennes I, Avenue du G´en´eral Leclerc, 35042 Rennes c´edex, France Tel.: (33)0299281444. Fax: (33)0299281612. E-mail:
[email protected] Received 18 February 1999; in revised form 16 January 2001; accepted 7 February 2001
Key words: drought, freshwater gastropods, trematodes, community structure, dynamics, colonization
Abstract The impact of a drought on freshwater snail and trematode communities was investigated in a lake. Before the drought, 15 gastropod species (Valvatidae, Planorbidae, Lymnaeidae, Ancylidae, Physidae) and 10 trematode species (cercariaeum, xiphidiocercariae, echinostome, furcocercariae, notocotyle, lophocercous) were recorded. The rate of parasitism was 5.13% and there were 11 host species. The 2 major consequences of desiccation were the disappearance of snails, except Valvata piscinalis and Lymnaea peregra, and the absence of trematodes infecting the surviving snails. As soon as favourable conditions were restored, the littoral area was recolonized, first by hygrophilic and amphibious species, second by aquatic species. Nine months after the drought, the gastropod community was restored. Recolonization by the trematodes was delayed compared with that of gastropods. During the study, the overall prevalence was equal to 0.36% and only 4 trematode species and 5 host species were recorded. Because of the great variability of freshwater ecosystems, long-term studies are necessary to understand the dynamics of snail and trematode populations and determine the regulatory effect of parasitism in the field.
Introduction Populations of freshwater snails are subjected to severe ecological constraints imposed by large temporal fluctuations in their environment. Their success depends on their physiological capacity to tolerate these fluctuations (Russel-Hunter, 1961). Biotic constraints, including parasitism, predation and competition, are added to these environmental constraints. Numerous experiments demonstrate the negative effects of larval trematodes on the fecundity, survival and growth of the snail hosts (for reviews, see Thompson, 1985; Hurd, 1990). The regulatory impact of the parasites on the host populations, supposed in theory (Anderson, 1978; Anderson & May, 1978), has been suggested recently by Gérard (1997, 1998) in a field study, based on a mathematical model which demonstrated an inverse relation between the frequency of the snails and the rate of parasitism. In that study, the gastropod and trematode communities were not sub-
jected to an external disturbance of their environment. There is a developing body of literature demonstrating changes in helminthic parasite fauna in relation to aquatic pollution (Khan & Thulin, 1991; Valtonen et al., 1997; Lafferty, 1997), and according to Siddall et al. (1993), snail-trematode associations may provide a sensitive and valuable biologically-based index of environmental disturbance. The severe drought of summer 1996 subsequently affected this ecosystem (Combourg lake in France), so I measured the impact of this stress on the structure of the snail and trematode communities through the dynamics of the populations. Sampling undertaken from December 1994 to June 1996 provided a baseline record of the populations before perturbation.
Materials and methods The study was carried out in the Combourg lake, a
10 Table 1. Gastropod community in Combourg lake before drought (frequency = number of species A × 100 / total number of gastropods) Dec-94
Mar-95
Valvatidae:
Valvata cristata Valvata pulchella Valvata piscinalis
23.4 0.7 0.3
18.7 0.8 0.4
Planorbidae:
Planorbis planorbis Planorbarius corneus Gyraulus albus Gyraulus laevis Armiger crista Segmentina nitida
5.8 0.9 64.6 0.2 0.3 0.5
2.2 0.4 70.9
Lymnaea peregra Lymnaea auricularia Lymnaea stagnalis Lymnaea palustris
0.7 0.1 0.6 0.2
Acroloxidae:
Acroloxus lacustris
1.0
Physidae:
Physella acuta
0.6
Lymnaeidae:
Total number of gastropods
pool of shallow stagnant water in Ille-et-Vilaine, eastern Brittany, France (48◦ 24 N, 1◦ 45 W, area ≥20 hectares). Animals were collected in a littoral area 100 m long, 2.5 m wide and 1.0 m maximum depth (sampling area in previous studies (Gérard, 1997, 1998)). Five samplings undertaken in December 1994, March 1995, July 1995, March 1996 and June 1996 (2708 collected snails) provided a baseline record of the gastropod and trematode communities before the drought (in summer 1996). From September 1996 to May 1997, 5067 snails were collected; populations were sampled at the end of each month by which time the recolonization of the pond by the gastropods was successful (establishment of a new cohort composed of numerous juveniles born from colonizers). Water temperature and depth were measured at each sampling. Mean values of temperature varied from 5.5 ◦ C in December–January to 16.5 ◦ C in May, and the maximum water depth was reached in April with 65 cm. Samplings were made always by the same person, using a pond-net (nylon mesh: 1 mm, square aperture: 0.5×0.5 m) over a period of 20–30 min.
863
Jul-95
Jun-96
57.1 0.8 0.2 10.3 38.1 15.5
5.4
10.7 0.2 14.7
5.8 4.3 43.5
0.5 5.1 22.7 1.0 7.2 3.1
1.2
472
Mar-96
4.3 0.2 0.1 5.8
21.7 20.3 1.5
0.1 2.1
0.2
2.9
99
1175
60
The pond-net contents were examined in the laboratory. The presence of egg masses was recorded and all the collected snails were systematically identified, measured to 0.1 mm with calipers: height for conic shells, diameter for discoïd shells, then dissected under a stereoscopic microscope to record infection. The parasites (sporocysts or rediae, and cercariae) were observed alive and drawn with the help of a microscope equipped with a camera lucida. In September and October 1996, because of the impoverishment of the littoral area due to the summer drought (no vegetation and no organic debris capable of being used as habitat and food by the snails), the only place where vegetation was present (Nymphea alba) was also sampled; situated at 6–8 m from the shore, this area, named ‘waterlily zone’, measured about 400 m2 and was 30 cm deep.
Results Conditions before the drought: from December 1994 to June 1996 Samplings undertaken before the drought (Tables 1,
11 Table 2. Trematode community in Combourg lake before drought (Presence: 1 / absence:0) Dec-94 Mar-95 Jul-95 Mar-96 Jun-96 cercariaeum 1 xiphidiocercariae 1 1 xiphidiocercariae 2 1 xiphidiocercariae 3 1 echinostome 1 furcocercariae 1 1 furcocercariae 2 1 furcocercariae 3 1 notocotyle 1 lophocercariae 0
1 1 1 1 1 1 1 1 1 0
1 1 1 1 1 1 1 1 1 0
1 1 1 0 1 0 1 1 1 1
1 1 0 0 1 0 1 1 1 0
2 and 3) confirmed the overall stability of the gastropod and trematode communities, characterized by great species richness and abundance: 15 species of gastropods (3 Prosobranchia and 12 Pulmonata) (Table 1) and 10 species of trematodes (1 cercariaeum, 3 xiphidiocercariae, 1 echinostome, 3 furcocercariae, 1 notocotyle, 1 lophocercous) (Table 2). Eleven species of gastropods belonging to Planorbidae, Lymnaeidae and Valvatidae were found harbouring larval trematodes (Table 3). Despite the typical variability in species frequencies of freshwater gastropods, planorbids were always dominant in the gastropod community, followed by valvatids and lymnaeids (Table 1). During each of the 5 samplings undertaken before the drought, between 6 and 9 species of trematodes out of the 10 described in the lake were found (Table 2). The overall prevalence was 5.13% corresponding to 139 infected out of 2708 snails: 87 planorbids, 35 lymnaeids and 17 valvatids (Table 3). Conditions after the drought: from September 1996 to May 1997 Results obtained from September 1996 to May 1997 are presented in Tables 4 and 5 and in Figures 1 and 2. Determination of the drought stress imposed on the populations In September 1996, water level enormously decreased and the quantity of mud greatly increased (maximum water and mud depth = 10 cm and 90 cm, respectively); by October 1996, the situation had not improved greatly (maximum water and mud depth = 10 cm and 50 cm). Molluscs were practically absent
from the littoral area (Table 4): 4 Valvata piscinalis (Müller) (Prosobranchia) in September 1996, 0 in October 1996. The ‘waterlily zone’ harboured 27V. piscinalis and 2 Lymnaea peregra (Müller) (Pulmonata) in September, 22 V. piscinalis and 3 L. peregra in October. The valvatids represented all age classes of juveniles and adults (size 1.75–5.75 mm), whereas the few lymneids were solely juveniles (size 2.4–5.8 mm) (Fig. 1). None of these molluscs was infected by larval trematodes. Beginning of recolonization In November 1996, the water level increased considerably following rain (maximum water and mud depth = 26 cm and 15 cm, respectively). Twenty-six individuals were collected (Table 4), of which 6 only were truly aquatic: 5 L. peregra and 1 Gyraulus albus (Müller), the 20 others were amphibious or hygrophilic: 15 Lymnaea truncatula (Müller), 1 Zonitoides nitidus (Müller), 1 Succinea sp. and 3 Arionidae. V. piscinalis was absent. Of all the snails collected, a single individual, L. truncatula, was parasitized by trematodes, the cercariaeum type (Tables 4 and 5). Recovery of an aquatic snail community During December 1996, January and February 1997 (mean water depth of 41 cm), the hygrophilic species were progressively replaced by aquatic species (Table 4): L. truncatula was still present in December, but L. peregra had become dominant. Other species of lymnaeids appeared: Lymnaea palustris (Müller), Lymnaea stagnalis (Linné) and Lymnaea auricularia (Linné); the Planorbidae (G. albus, Planorbis planorbis (Linné)) were rare. From February to March 1997, the abundance diminished even though the species richness increased (Table 4). In March, snails were mainly reproducers as shown by their large size and the presence of 18 egg masses (15 of lymnaeids, 3 of planorbids). In April 1997, the number of egg masses greatly increased (45) and 216 gastropods were collected (Table 4), mainly very young snails. Among the 149 lymneids, 8 were adults and 141 were juveniles (mean size <2. The dynamics of lymneids (Fig. 1) demonstrated 2 successive cohorts: that of colonizing snails appeared in November 1996, reproduced from February to March 1997 and died in April 1997 giving birth to a new cohort. The total prevalence recorded from December 1996 to April 1997 was extremely small (Table 5): 0.76% (4 gastropods infected of 527 collected in 5
12 Table 3. Host community in Combourg lake before drought. Number of infected snails and prevalence of trematodes (%) Host species Planorbis planorbis Planorbarius corneus Gyraulus albus Segmentina nitida Lymnaea peregra Lymnaea auricularia Lymnaea stagnalis Lymnaea palustris Valvata cristata Valvata pulchella Valvata piscinalis infected snails total of snails overall prevalence
Dec-94 23 2 5 0 4 0 4 0 2 2 2 44 863 5.01
Mar-95 2 1 11 0 0 0 0 0 0 0 1 15 502 2.99
months). All the 4 infected snails were lymnaeids: 2 L. peregra, 1 L. palustris and 1 L. auricularia; only 2 types of trematodes were identified out of the 3 observed: rediae from the cercariaea group (observed twice) and rediae from immature echinostomes (observed once), the 3rd type corresponded to a prepatent infection with immature sporocysts that didn’t produce cercariae (necessary for identification). In March and April, none of the snails was found infected.
Demographic explosion in the gastropod community In May 1997, 4456 snails (vs 216 in April) belonging to 11 different species were sampled, not only lymneids (Fig. 1b), but also planorbids that became dominant in the community (Fig. 2). The collected snails were very young and the mean sizes of the 3 most abundant species were 4.65±0.10 mm, 2.80±0.03 mm and 4.41±0.10 mm, respectively, for P. planorbis (from 1.8 to 12.7 mm), G. albus (from 1.0 to 5.5 mm), and L. peregra (from 1.5 to 13.8 mm). Thirteen snails: 12 P. planorbis (mean size = 7.58±2.42 mm) and 1 L. auricularia (19.10 mm) were found infected by 3 species of trematodes (Table 5): cercariaea (observed in 10 P. planorbis), immature sporocysts (observed in 1 L. auricularia) and xiphidiocercariae (observed in 2 P. planorbis and described for the first time after the drought).
Jul-95 1 5 3 0 10 0 2 0 0 0 0 21 99 21.21
Mar-96 7 0 17 3 4 0 0 4 9 1 0 45 1175 3.83
Jun-96
Total
0 0 7 0 2 5 0 0 0 0 0 14 69 20.29
139 2708 5.13
Discussion The summer drought on Combourg lake resulted in increased temperature, decreased water level, dryness, silting, absence of littoral vegetation. The littoral area of the pool, formerly inhabited by gastropods, dried out and the snail populations suffered severe mortality with repercussions on trematodes. According to Dudgeon (1982), the relative abundance of gastropods is controlled by the interaction of water level fluctuations and breeding biology. He suggested that the increase in predator pressure and interspecific competition related to the restricted size of habitat during the dry period leads to the elimination of some species and to a reduction of diversity. From the investigations of Pointier & Combes (1976) in Guadeloupe, the whole malacological fauna declines during the dry season and new generations appear only after the water level rises again. The behaviour of freshwater gastropods during a drying stress has been well studied, and 2 main survival strategies are evident: (i) snails may migrate to more favourable areas of the pool, (ii) snails may bury in the substratum to estivate and reduce desiccation. Seasonal migrations are generally considered as responses to temperature variations (Cheatum, 1934; Horst & Costa, 1975), whereas the escape mechanism of estivation is more often interpreted as an adaptation to temporary water bodies, particularly for tropical species (Pointier et al., 1977; Hanifa, 1978). The estivation ability of
Succinidae: Zonitoidae: Arionidae:
Acroloxidae Physidae:
Total of snails Species richness Prevalence of parasitization (%) Number of infected species
Stylommatophora
Planorbidae:
PULMONATA Basommatophora
Lymnaeidae:
Valvatidae:
PROSOBRANCHIA
Succinea sp. Zonitoides nitidus -
Planorbis planorbis Gyraulus albus Gyraulus laevis Armiger crista Segmentina nitida Lymnaea peregra Lymnaea auricularia Lymnaea stagnalis Lymnaea palustris Lymnaea truncatula Acroloxus lacustris Physella acuta
Valvata cristata Valvata piscinalis
4+29 2 0 0
0+2
4+27
Sep-96
0+25 2 0 0
0+3
0+22
Oct-96
15
26 6 3.85 1
100 7 1.00 1
3
2 38 26
1 1 3
62
2 2
3
Dec-96
5
1
Nov-96
106 5 1.89 2
1
2 13
58
7
Jan-97
76 9 1.32 1
1
2
41 12 4 2
1 1
1
Fev-97
29 6 0 0
5
15 6
1 3
2
Mar-97
216 9 0 0
1 4
22
39 2 11 69 2 121 23
20
Apr-97
4456 11 0.29 2
114
924 226
1721 1361
4 2
May-97
Table 4. Number of gastropods sampled in the Combourg lake from September 1996 to May 1997 (numbers are underlined when species are parasitized, numbers in September and October 1996 correspond to the snails of sampling area plus that of waterlily zone)
13
14 Table 5. Host (H)/parasite (P) associations and prevalences recorded from September 1996 to May 1997 (Ltr = L. truncatula, Lpe = L. peregra, Lpa = L. palustris, Lau = L. auricularia, Pp = P. planorbis, Cer = Cercariaea, Ech = Echinostome immature, Xip = Xiphidiocercariae, Spo = Sporocyst prepatent) Sep-96
Oct-96
Nov-96
Dec-96
Jan-97
Fev-97
Mar-97
Apr-97
May-97
H/P associations Prevalence (%)
–
–
Ltr/Cer 6.7
Lpe/Cer 1.6
Lpe/Ech 1.7 Lpa/Cer 2.6
Lau/Spo 8.3
–
–
Lau/Spo 0.44 Pp/Cer 0.58 Pp/Xip 0.12
Number of infected snails Overall prevalence (%)
0 0
0 0
1 3.85
1 1.00
2 1.89
1 1.32
0 0
0 0
13 0.29
lymneids and planorbids, the gastropods dominant in Combourg lake, have been demontrated by some authors (Richards, 1963; Storey, 1972; Brown, 1979). The proportion of survivors at the end of estivation depends directly on the drought duration and varies according to the species and the strain. The period of drought must not exceed a week for some populations of L. peregra (Lambert, 1990), but may last up to several months for Biomphalaria glabrata, a very resistant species (Richards, 1963; Sturrock, 1970; Pointier et al., 1977). According to Sturrock (1970), drought both reduces snail populations and alters the age structure of the survivors. In the gastropod community of Combourg lake, the prosobranch V. piscinalis didn’t estivate and seemed to tolerate the harsh environmental conditions. Although a rare species before the desiccation stress, this drought-resistant snail became largely dominant and constituted 91.4% of collected gastropods in September and October. According to Russel-Hunter (1961), success of freshwater mollusc populations subjected to severe environmental constraints depends on their ability to tolerate considerable physiological variations. However, in the case of V. piscinalis, its presence during drought could be due to the fact that, at that time, the lake margins changed to resemble their characteristic habitat, probably very different from that of the other species observed before and after disturbance. The only other species present at the same period is L. peregra, a very ubiquitous species. As soon as favourable environmental conditions were restored, the progressive recolonization of the littoral area by the snails could have taken place by classical processes of recruitment (immigration and
natality). The pioneer community was not constituted only by surviving estivating snails, but also by dispersal of immigrants from the persisting waters of the lake or by phoresia: transport of egg masses by birds (Okland, 1990), and, to a lesser extent, by insects, fishes, amphibians and humans. The first recolonizers (November, December) were hygrophilic (stylommatophorans: succineids, zonitoids and arionid slugs) and amphibious (L. truncatula) species not recorded in samples prior to drought, whose presence was directly linked to the progressive rising of water in the littoral area. These species were then progressively replaced during winter (December–January) by fully aquatic species: L. peregra initially, a good colonizer species whose success reflected its ubiquitous nature, then, other basommatophorans and some prosobranchs (Valvatidae), in decreasing order of colonization ability. The gastropod community of the pool in the following spring was dominated until April by Lymnaeidae whose colonizing capacities were highest (Fig. 3). The proportion of Planorbidae, the dominant family before disturbance, increased progressively and became again dominant only in May reaching 71.0% of the whole gastropod community. The family of Valvatidae was not really present, except in April (9.26%), and was represented mainly by Valvata cristata (Müller), one of the more frequent species before dryness. The 2 species absent after desiccation were rare species: Valvata pulchella (Steenbuch) and Planorbarius corneus (Linné). It can be considered that the gastropod community was restored after 9 months post-disturbance, resembling that observed before dryness (Fig. 2).
15
Figure 1a. Figure 1. Histograms of the size distribution of Lymnaeidae in Combourg lake. (a) from September 1996 to April 1997, (b) in May 1997.
Overall, the drought seriously affected the community of trematodes in Combourg lake. Only 4 species of trematodes were recorded after the drought compared to 10 before, and very few snails were infected: 0.36% vs 5.13% before drought. The number of host species was strongly reduced after the drought (5 vs 11) among lymneids and planorbids; valvatids were not found harbouring trematodes. The rate of parasitization fluctuates in relation to abiotic and biotic factors including the characteristics of the environment, the densities of intermediate and definitive hosts
and the development cycle. In general, aquatic snails in Europe present 2 peaks of parasitization (Erasmus, 1972; Crews & Esch, 1986), at the end of spring (May–June) and summer (September–October). The absence of the peak of end summer is directly linked to the dryness of the lake and to the great mortality of the snail hosts. Consequently, the amplification phase of the trematode cycle within the molluscs which compensates the massive mortality in dispersion phases (cercariae), did not take place. The heavy mortality in parasites will have repercussions to the develop-
16
Figure 1b
ment cycle affecting future prevalence. The recolonization of the parasite would be likely to take place after restoration of the snail community in the pool (truly favourable conditions), mainly from vertebrate hosts harbouring adult trematodes (sexual reproduction), and, to a lesser extent, with some infected snails that survived desiccation. The four types of trematodes recorded (cercariaeum, echinostome, xiphidiocercaria, immature sporocyst) were among the 10 types recorded before disturbance (Table 2); among them, the cercariaeum type, a non-specific trematode with rediae using pulmonates and prosobranchs as intermediate
hosts (Gérard, 1997, 1998), was the most frequent (72.2% of infected snails). Five parasitized lymneids were collected during the coldest period of the year when prevalence is usually low. The low prevalence in winter could therefore be unrelated to the disturbance of the biotope. However, Badger & Oyerinde (1996) demonstrated cercarial development delayed by prolonged desiccation of the estivating infected snails. The cercariae produced in winter could have originated from post-summer infections of molluscs that survived the desiccation period. In the absence of disturbance, these cercariae probably would be released during the late summer peak of prevalence. In March and April, the rate of parasitism was nil, contrasting with the situation in normal conditions where the number of infected snails increases until the spring peak. These results may be interpreted in different ways. In March, the snail community was composed of old reproducers of the colonizing cohort. The absence of parasites in these old snails was mainly related to the absence of a summer parasitization peak, but can be explained also by the reduced survival rate of infected snails in the majority of trematode-snail associations (Woolhouse, 1989; De Kock, 1993). In April 1997, the snail community was composed of numerous neonates and juveniles. The probability of infection increases with age (Minchella et al., 1985; Goater et al., 1989; Manga-Gonzalez et al., 1994), so the probability of a neonate being exposed to a miracidium approximates zero. This implies that there will be a delay before parasitization of the new cohort is manifested. In the months after the birth of this second cohort, there will be a re-appearance of larval trematodes with a progressive increase of prevalence, as demonstrated by the presence of 13 infected snails in May 1997.
Conclusion This study demonstrates the difficulty which trematodes face in preserving an equilibrium of trematodesnail associations in freshwater ecosystems. The compromise established between the host and parasite communities is destroyed when a major environmental disturbance occurs. Is it, therefore, possible that, in the field, parasites can play a role in the regulation of host populations? This may be the case in a few snailtrematode associations, but only when populations are well established in their biotope. In cases of ‘disequi-
17
Figure 2 Comparison of the families in the gastropod community of Combourg lake before the drought (mean values from December 1995 to June 1996) and after the drought (in April and May 1997).
librium’ induced by environmental stress, trematodes have no regulatory action on the host populations. The freshwater environment represents a multifactorial system where the effect of one factor or parameter is often modified by other factors or conditions. Diversity and abundance of snail and trematode faunas and the nature of their interactions are related to various environmental parameters of such a complex system. Taking into account the time necessary for the re-establishment of communities in a freshwater habitat after disturbance, a long term study on the level of individuals, populations and communities is necessary to have a better understanding of the functioning of trematode-mollusc systems in the field.
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