Biodiversity and Conservation 10: 511–525, 2001. © 2001 Kluwer Academic Publishers. Printed in the Netherlands.
Local and regional influences on patterns of parasite species richness of central European fishes ANDREA SIMKOVÁ1,2, SERGE MORAND3 , IVETA MATEJUSOVÁ2 , PAVEL JURAJDA4 and MILAN GELNAR2 1 Faculty of Natural Scienes, Comenius University, Mlynská dolina B-1, 84215 Bratislava, Slovak Republic; 2 Faculty of Science, Masaryk University, Kotlárská 2, 61137 Brno, Czech Republic; 3 Centre de Biologie et d’Ecologie Tropicale et Mediterranéenne, UMR 5555 CNRS, Université de Perpignan, Avenue de Villeneuve, 66860 Perpignan Cedex, France; 4 Institute of Vertebrate Biology, Academy of Sciences of the Czech Republic, Kvetná 8, 603 65 Brno, Czech Republic; ∗ Author for correspondence (e-mail:
[email protected]; fax: +33-4-68662281)
Received 17 January 2000; accepted in revised form 1 May 2000
Abstract. Local, regional and global influences on the patterns of parasite species richness of 39 freshwater fish species from Central Europe were investigated. Host local abundance and host occurrence were considered respectively as local and regional factors, while host geographical range in longitude and latitude was considered as a global factor. Influences of size, ecology and behavior of hosts were also included in a comparative analysis using the independent contrasts method. We considered host habitat, host diet, host shoaling behavior and mobility. We found a positive relationship between local occurrence of fish and global range of their distribution. We confirmed previous findings showing the importance of host behavior and ecology on the variability of parasite species richness. Second, we showed how a global pattern, such as host geographical range, may affect the variability in parasite species richness through its effects on local abundance and distribution of hosts. A negative relationship between endoparasite species richness and host longitudinal range was found. This suggests that fish with eastern distribution live in the boundary of their distribution in Central Europe far from their center of distribution, which should also be characterized by a higher diversity of parasites. Key words: comparative analysis, fish behavior, fish distribution, freshwater fish, independent contrasts, local and regional influences, parasites
Introduction Numerous studies have recognized parasitism as significant factor that may affect host natural population dynamics (Scott 1988; Hudson and Dobson 1989; Begon et al. 1992). Parasites are known to potentially decrease the survival or the reproduction of host populations (Minchella and Scott 1991), and parasitism is now largely taken into account in studies of biodiversity (Viggers et al. 1993; Sasal et al. 2000). As parasites may have negative effects on their hosts, it is thus of great importance to characterize the determinants of parasite species diversity (Poulin and Morand 2000). Current studies on parasite diversity try to determine which factors, host or environmental, are the best determinants of parasite species richness (Poulin and Morand
512 2000). Several recent studies have investigated the determinants of parasite species richness of freshwater and marine fishes (Bell and Burt 1991; Guégan and Kennedy 1993; Poulin 1995; Poulin and Rohde 1997; Sasal et al. 1997; Morand et al. 2000). Historical, biogeographical, environmental and ecological variables were found to be major determinants of parasite species richness (Poulin and Rohde 1997; Sasal et al. 1997; Poulin 1998). The respective roles of local, regional and global influences on the patterns of parasite species richness have rarely been taken into account. Hence, several studies have either emphasized the importance of local influences, such as local host abundance or density (Morand et al. 2000), or have focused on the importance of regional and global influences, i.e. geographical ranges (Aho and Bush 1993). Host abundance was found as a local factor influencing parasite species richness of fish hosts (Polyanski 1961; Sasal et al. 1997). Parasite species richness can be positively correlated with host local abundance because more abundant hosts will more readily sustain populations of parasites (Bell and Burt 1991; Poulin and Morand 1999; Morand et al. 2000). Host local occurrence (i.e. the number of sites in which a host occurs within its regional distribution) can also be positively correlated with parasite species richness because more widely distributed hosts in their local sites will encounter more parasite species. But to our knowledge the influences of host local occurrence on patterns of parasite species richness have never been tested. Host biogeographical range was repeatedly found positively correlated with parasite species richness (Aho and Bush 1993). Wider host distribution will make it possible to harbor more parasite species (Rohde 1978; Price and Clancy 1983; Gregory 1990; Bell and Burt 1991; Rohde 1993; Guégan and Kennedy 1996; Feliu et al. 1997). Here, we investigated the determinants of parasite species richness of central European fishes. Our aims are to disentangle the respective roles of local (i.e. host local abundance), regional (i.e. host occurrence), and global (i.e. host geographical range) influences. We also take into account the influences of several other factors linked to host ecology and behavior, such as: host body size, host diet, host shoaling behavior, host mobility and host habitat. We conducted a comparative analysis, controlling possible host sample bias, using the independent contrasts method (Felsentein 1985).
Materials and methods Data on parasite species richness were obtained from published studies from four rivers of the Czech Republic (Gelnar et al. 1990, 1994; Moravec et al. 1997) and unpublished data were also used for this study. The analysis was performed on a total of 1073 fish individuals representing a total of 39 fish species (belonging to 10 fish families). The total number of macroparasite species, the number of ectoparasite species (monogeneans and crustaceans) and endoparasite species (digeneans, cestodes,
513 acanthocephaleans and nematodes) were recorded for each host species in the four Czech rivers. We obtained the following information for each fish species (Table 1). Host sample size Host sample size is considered to be an important parameter for estimating parasite species richness. In the absence of parasitological data on individual hosts, host sampling bias can be controlled by using residual values derived from regressions of parasite species richness versus host sampling size (Gregory 1990; Guégan and Kennedy 1996). Several studies showed that the estimation of parasite species richness depends on the number of individual hosts examined and/or number of localities studied (Gregory 1990; Walther et al. 1995; Gregory et al. 1996; Guégan and Kennedy 1996). Host sample size (number of host individuals examined) was obtained from published papers (Gelnar et al. 1990, 1994; Moravec et al. 1997) and unpublished data from fish dissections were also used. Host body size Host size was found to be the major determinant of parasite species richness in fish species (Bell and Burt 1991; Guégan et al. 1992; Guégan and Hugeny 1994; Guégan and Morand 1996; Sasal et al. 1997; Sasal and Morand 1998), although some studies did not support this relationship (Poulin 1995; Poulin and Rohde 1997). Maximal host body length (in cm) and maximal host weight (in kg) were obtained (Barus and Oliva 1995; Blahák 1996). Relative local abundance and occurrence of hosts Relative host local abundance was calculated as the mean of relative abundance, i.e. the relative ratio of individuals belonging to a given fish species to the total number of all fish in a given sample. Host occurrence is the number of sites occupied by a given host species within the rivers of the Czech Republic. All sampling were done using the same method (electrofishing). Both relative local abundance and host occurrence were obtained from Lucky (1955), Hochman and Jirasek (1958), Kubecka (1990), Gelnar et al. (1990, 1994), Moravec et al. (1997) and unpublished data. Host geographical range Host geographical range (in latitude and longitude), middle geographical latitude and longitude were assigned using data from Muus and Dahlström (1968) and references therein. Introduced host species were not scored for this variable.
Abramis brama 159 Abramis sapa 9 Alburnus alburnus 81 Alburnoides 4 bipunctatus Anguilla anguilla 9 Aspius aspius 11 Barbus barbus 8 Barbatula barbatula 12 Blicca bjoerkna 25 Carassius auratus 14 Carassius carassius 4 Chondrostoma nasus 7 Cobitis taenia 3 Cottus gobio 26 Cyprinus carpio 15 Esox lucius 21 Gobio albipinatus 7
Fish species 12 11 15 0 5 8 5 5 13 5 2 1 1 3 3 7 2
13 6 19 1
0 7 7 3 10 9 3 5 1 0 9 6 2
EctoEndoHost parasite parasite sample species species size richness richness
0 4 6 2 9 8 2 4 1 0 8 2 2
10 5 16 1 140 100 100 16 54.5 52 53 56.5 11.8 15 120 138 12
75 30 20 15 6 14 15 0.08 1 3 3.4 1 0.005 0.08 30 10 0.008
4 0.8 0.08 0.06
Monogenean Host Host species Length weight richness (cm) (kg)
0.46 0.63 1.2 0.25 1.05 0.5 0.83 4.03 0.05 3.75 3.95 1.38 1
12.49 0.1 7.09 1.25
Local abundance (%)
4 4 5 4 7 6 4 2 1 1 5 11 2
9 1 11 1 51 49.5 47 55 54 ? 53.5 51 45.5 54 53.5 44 ?
55 53 54 53 12.5 37.5 15 65 21.5 ? 55 22 65.5 22.5 55 85 ?
30 42 25 32.5
Local Occurrence Lati- Lon(number tude gitude of sites) range range
42 21 10 30 24 ? 33 28 19 28 33 32 ?
30 22 26 24 95 65 40 150 49 ? 130 50 145 55 130 190 ?
80 56 60 75
4 5 3 3 4 4 2 1 3 3 4 5 3
3 3 2 3
0 1 0 0 0 0 1 0 1 1 0 1 ?
0 0 0 0
0 0 0 1 1 1 1 0 1 1 1 1 1
0 0 1 1
3 1 3 3 3 3 3 3 3 3 2 2 3
3 3 1 1
1 1 1 1 3 2 3 1 1 1 3 3 1
3 1 3 1
MidMidrange Host Host range longiSocial- Mobil- hab- hablatitude tude Diet ity ity itat 1 itat 2
Table 1. List of freshwater fishes investigated with data on parasite species richness (endoparasites, ectoparasites and monogeneans), length, weight, local distribution (abundance and occurrence), global distribution (range and midrange of latitude and longitude), host diet, host sociality, host mobility and host habitat (habitat 1 = benthic versus pelagic; habitat 2 = calm water versus running water).
514
Gobio gobio 64 Gymnocephalus 8 cernuus Gymnocephalus 1 schraetser Leuciscus cephalus 108 Leuciscus idus 6 Leuciscus leuciscus 39 Lota lota 1 Oncorhynchus 14 mykiss Pelecus cultratus 3 Perca fluviatilis 172 Pseudorasbora par- 12 va Rhodeus sericeus 32 Rutilus rutilus 98 Salmo trutta 27 Salvelinus fontinalis 3 Scardinius erythro- 13 phthalmus Silurus glanis 3 Stizostedion luciop- 15 erca Thymallus thymallus 12 Tinca tinca 22 Vimba vimba 4 Zingel zingel 1
7 1 3 21 4 10 1 8 0 13 1 2 9 12 7 3 3 8 5 6 2 1
9 0
0
23 7 7 0 1
3 9 1
4 20 2 1 5
1 5
3 5 4 0
2 3 4 0
1 3
3 18 2 1 3
3 4 0
8 1 2 0 1
0
6 0
60 68 51 50
315 100
7.5 52 82 54 45
60 61 9
78 62 35 79 89
30
14 30
1.5 6 1.5 0.5
30 6
0.007 1 3.1 1 1
2 0.5 0.017
5 4 1 2 7
0.25
0.01 0.25
3.13 0.28 0.05 0.03
0.13 1.08
3.75 16.23 31.25 0.25 0.24
0.03 13.08 0.5
13.2 0.05 1.68 0.25 1.25
0.03
12.39 0.13
5 9 2 1
2 6
11 16 4 1 6
1 20 4
17 2 7 1 2
1
16 2
60 52 46 46
49.5 53.5
48.5 52.5 45 ? 52.5
51 52.5 ?
49.5 52 55 55 ?
53.5
47.5 53.5
?
?
?
30 50 29.5 21
35 36
30
70 55 22.5
39.5 65
23.5 62.5 65 90
7.5
65 80
24 26 12 8
27 27
23 35 30 ? 29
18 35 ?
27 30 30 30 ?
33
21 33
70 120 45 18
60 58
105 130 65 ? 80
51 150 ?
67 115 150 180 ?
35
150 180
3 3 3 3
5 5
1 2 5 5 1
2 5 3
4 4 3 5 3
3
3 3
0 1 0 ?
0 1
0 0 1 1 0
0 0 0
1 0 0 1 1
0
0 0
0 1 0 1
1 0
0 1 0 0 1
0 1 1
1 0 1 1 1
0
1 1
1 3 3 3
3 3
2 1 1 1 1
1 2 3
1 1 3 3 1
3
3 3
1 3 1 1
3 3
3 3 1 1 3
1 3 ?
1 3 1 1 1
1
1 3
515
516 Host diet Host diet (trophic category) seems to be important for parasite species with complex life cycles because of the existence of intermediate hosts that serve as prey to fish as definitive hosts (Price and Clancy 1983; Bell and Burt 1991; Guégan and Kennedy 1993; Sasal et al. 1997). Two hypotheses have been proposed to explain relationships between host diet and parasite species richness: (1) top predators (carnivores) would harbor rich parasite communities because of parasite species accumulation through predator–prey relationships (Bell and Burt 1991) and (2) benthic feeders seem to harbor more parasite species than pelagic-feeding host species (Holmes 1990). Host diet (trophic category) was coded from 1 to 5 as follows: (1) herbivorous, (2) planktivorous, (3) bentophagous, (4) omnivorous, (5) carnivorous using data from Barus and Oliva (1995). Host behavior Host shoaling behavior (gregarious versus solitary) could influence parasite diversity. Parasite species richness is supposed to increase with host gregariousness (Esch et al. 1990; Poulin 1991; Ranta 1992; Sasal et al. 1997; Sasal and Morand 1998). Host shoaling behavior was coded as (0) gregarious and (1) solitary (Barus and Oliva 1995). Host mobility was found as a determinant of parasite species richness (Polyanski 1961). This factor may be related to host gregariousness as gregarious fish are often migratory fish. Host mobility was coded as (0) migrant and (1) non-migrant according to Barus and Oliva (1995). Host habitat Host habitat is described by a fish’s preferred position in the water column and/or by current velocity in the part of rivers in which fish species live. On one hand, benthic fish may harbor more directly transmitted parasite species than pelagic fishes. On the other hand, fish living in calm water (limnophilous fish) should harbor more directly transmitted parasite species than fish living in running water (rheophilous fish). Host habitat regarding the fish position in water column was coded as (1) pelagic (2) indifferent and (3) benthic (Barus and Oliva 1995). Host habitat regarding current velocity was coded as (1) rheophilous (fishes that prefer to live in running water) (2) indifferent (3) limnophilous (fishes that prefer to live in calm water) (Schiemer and Waidbacher 1992). Comparative analysis Several studies on determinants of parasite species richness have emphasized the importance of phylogenetic effects (Poulin 1995, 1998; Morand 1997; Morand and
517 Poulin 1998; Sasal and Morand 1998). Hence, the search for the determinants of parasite species richness should be investigated after controlling for confounding phylogenetic effects (Poulin 1995; Gregory et al. 1996; Morand 1997). A non-phylogenetic approach may lead to false conclusions, i.e. spurious correlations due to pseudo-replication. The phylogenetic independent contrasts method has been developed to resolve the problem of non-independence of studied traits (Felsenstein 1985; Garland et al. 1992). In the present study, the phylogeny of fish species was obtained from Lecointre (1994) and completed by phylogenetic information on Cyprinidae obtained from Gilles et al. (1998) (Figure 1). The phylogenetic independent contrasts method was used (Felsenstein 1985) by the CAIC program for Macintosh (Purvis and Rambault 1995). Continuous variables were log-transformed before analysis. A total of 27 independent contrasts were obtained. We tested the respective importance of each factor in determining total parasite species richness, endoparasite species richness and ectoparasite species richness by performing a stepwise regression forced through the origin (Garland et al. 1992) on all independent variables.
Results Total parasite species richness correlated with host sample size (R 2 = 0.611, P < 0.0001; Figure 2A). Positive relationships between host sample size and both local host abundance (R 2 = 0.551, P < 0.0001; Figure 2B) and host occurrence (R 2 = 0.685, P < 0.0001; Figure 2C) were found. A positive relationship was found between fish occurrence and fish geographical range (Figure 3). We controlled parasite species richness, local host abundance and host occurrence for host sample size in all analyses. Determinants of total parasite species richness were investigated and the results of stepwise regressions performed on independent contrasts are given in Table 2. We found that total parasite species richness correlated positively with host weight and fish occurrence but negatively with geographical range in longitude and host habitat regarding current velocity (Table 2). We noticed that there was a positive covariation between the endoparasite species richness and the ectoparasite species richness using independent contrasts (Figure 4). Endoparasite species richness was positively correlated with host diet and host occurrence and negatively with geographical range in longitude and host habitat regarding current velocity. As diet is a categorical variable, we examined the influence of diet on estimated parasite species richness in relation to changes in diet state (i.e., from 1 to 2, 2 to 3, 3 to 4 and 4 to 5) using the program CAIC. There were 17 changes in diet state. In 16
518
Figure 1. Phylogenetic relationships of the investigated fishes.
of the diet state changes, an increase in carnivory was associated with an increase in parasite species richness (Binomial test, P = 0.00014). Ectoparasite species richness was positively correlated with host weight, host occurrence and host habitat regarding both criteria: pelagic versus benthic and limnophilous versus rheophilous.
519
Figure 2. (A) Relationship between total observed parasite species richness and host sample size. (B) Relationship between relative host local abundance and host sample size. (C) Relationship between host occurrence and host sample size.
520
Figure 3. Relationship between contrasts in fish occurrence and contrasts in fish geographical area.
Discussion Two main conclusions can be drawn from our study. First, we confirm previous findings showing the importance of certain aspects of host behavior and ecology on the variability of parasite species richness. Second, we show how a global pattern, such as host geographical range, may affect the variability in parasite species richness through its effects on local abundance and distribution of hosts.
Table 2. Relationships between parasite species richness (controlled for host sample size) and subsets of determinants obtained by stepwise regression performed on independent contrasts. Dependent variable
Independent variables
Slope
F
R 2∗
Total parasite species richness
Host weight Range longitude Host occurrence Host habitat (current velocity)
0.121 −0.001 0.045 −0.098
17.27 5.09 28.50 12.81
0.73
Endoparasite species richness
Host diet Range longitude Host occurrence Host habitat (current velocity)
0.102 −0.001 0.026 −0.081
14.45 5.27 6.67 7.4
0.61
Ectoparasite species richness
Host weight Host occurrence Host habitat (pelagic/benthic) Host habitat (current velocity)
0.09 0.053 0.083 0.063
10.35 36.4 5.63 5.25
0.71
∗ P < 0.0001.
521
Figure 4. Covariation between contrasts in endoparasite species richness and contrasts in ectoparasite species richness (both variables were controlled for host sampling size).
Host size, ecology and behavior of hosts as determinants of parasite species diversity Our study confirms previous findings on the determinants of parasite species richness. Our study also emphasises the need to take into account the type of parasites, i.e. ectoparasites versus endoparasites, which corresponds also to their transmission, respectively direct or complex, in the search of determinants of species richness. We found a positive relationship between host weight and ectoparasite species richness. Several other studies showed host body size as the main determinant of ectoparasite species richness of fish species (Bell and Burt 1991; Guégan et al. 1992; Guégan and Morand 1996; Sasal et al. 1997; Sasal and Morand 1998). For example, host size has been found as the major factor of monogenean infracommunity structure of West African cyprinids (Guégan and Hugueny 1994), where maximal host length explained 86% of the variation in monogenean species richness. All those findings can be explained in the light of island biogeography theory (Kuris et al. 1980) where larger hosts offer larger habitats for parasite colonization than smaller ones (Esch et al. 1990). Our results confirmed several studies, which failed to find any relationship between endoparasite species richness and fish body size (Poulin and Rohde 1997; Sasal et al. 1997; Morand et al. 2000). Host feeding preferences were considered to be important for endoparasite species richness (Price and Clancy 1983; Bell and Burt 1991) because of their complex life cycle. Following Bell and Burt (1991), a carnivorous diet represents a large number and a taxonomically diverse range of potential intermediate hosts, which may favor
522 an accumulation of parasite species. We confirmed this hypothesis by showing an increase of endoparasite species richness from herbivorous to carnivorous diet. Host shoaling behavior could increase the number of parasite species with direct transmission, i.e. ectoparasite species (Côté and Poulin 1995; Poulin and Rohde 1997; Sasal and Morand 1998). However, our results confirmed Poulin (1991) and Ranta (1992), who also did not find any relationship between fish shoaling behavior (gregarious versus solitary) and parasite species richness. Host habitat may mainly affect the variability in ectoparasite species richness. Parasites with direct transmission are obviously favored in calm water. Indeed, we found that fishes living in calm water (limnophilous) and/or at the bottom of rivers (benthic fish) harbor more ectoparasite species than fishes living in running water or pelagic fishes. Global and local influences on parasite species richness We found a positive relationship between geographical range and local occurrence of fish. This finding highlights the indirect effect of host global distribution on local patterns of parasite species richness. The intricate influences of co-varying factors such as sample size, host abundance and/or host geographical range on parasite species richness have been emphasized by Guégan and Kennedy (1996). For example, a positive relationship between host geographical range and parasite species richness may arise because of a lack of control for sample size or because of a three way relationship: parasite species richness correlates with area, which correlates with sampling effort. However, we failed to find a relationship between host geographical range and host sample size. A positive effect of host occurrence in determining both endo- and ectoparasite species richness was found, whereas there was no relationship between host abundance and parasite species richness. This finding supports the view that it is the level of host population fragmentation rather than the abundance of hosts, which plays an important role. Hosts with less fragmented populations seem to sustain more easily parasite populations as emphasized by Bell and Burt (1991). The diversity of parasites may increase with a decrease in latitudinal distribution. For example, Rohde (1978, 1989, 1993) showed that the number of monogenean species (a group of ectoparasites) increases from temperate waters to tropical waters. We did not find any relationship between geographical range in latitude and parasite species richness, which may be due to the small range of latitudinal distribution for European fishes. Parasite species richness can be positively correlated with host geographical range (Aho and Bush 1993; see also Gregory 1990; Feliu et al. 1997). Price and Clancy (1983) found a positive relationship between host geographical range and parasite species richness of British freshwater fish species. However, they did not separate indigenous from introduced fish species and they did not take into account
523 sample size and host phylogenetic effects. An alternative explanation was expressed in terms of the colonization time hypothesis (Guégan and Kennedy 1993), i.e. parasite species richness is related to the time since a given fish species arrived to a given biogeographical region. Guégan and Kennedy (1993) found no significant relationship between host geographical range and parasite species richness, although using a non-phylogenetic approach. We found no relationship between host geographical range and ectoparasite species richness. However, we found a negative relationship between total parasite species richness and endoparasite species richness and the geographical range in longitude of fish. This finding suggests that fish with eastern distribution, harbor fewer parasite species than fish with western distribution. This new finding may highlight a possible relationship between invasions of eastern fish species with poor parasite species communities. It may also suggest that these fishes live in the boundary of their distribution in Central Europe far from their center of distribution, which should also be characterized by a higher diversity of parasites. This hypothesis remains to be critically investigated.
Acknowledgements This study was supported by the programme ‘Origine, Distribution et Dynamique de la Biodiversité’ of the French CNRS and by the Grant Agency of the Czech Republic, project number: 524/98/0940, and by the Research Project of the Masaryk University, Brno, project number: J07/98:143100010. Andrea Simková was supported by a grant from the French Embassy in Slovak Republic.
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