A comparative analysis of parasite species richness of Iberian rodents

453

A comparative analysis of parasite speCIes richness of Iberian rodents C. FELIUl, F. REN.A.UD 2 , F. CATZEFLIS 3 , J.-P. HUGOT 4 , P. DURAND 5 and S. MORAND 5 * Labo1"atori de Pa1'asitologia, Facultat de Farmacia. Universitat de Barcelona, Avda. Diagonal, 08028 Barcelona, Spain Laboratoire de Parasitologie Comparee (UMR 5555 CNRS) , Universite Montpellier II, place E. Bataillon, 34095 1Vlontpellie1' Cedex 05, France 3 Institut des Sciences de l'Evolution (Ul\IJR 5554 CNRS) , Universite Montpellier II, 34095 Montpellie1' Cedex OS, France 4111useum National d'Histoil'e lVa tU1"elle, Labo1"atoire de Biologie parasitaire (URA 114b CNRS) , 75231 Paris Cedex OS, France ;) Centre de Biologie et d' Ecologie tropicale et med£te1'raneenne (Ul\IJR 5555 CNRS) , Universite de Perpignan, 66860 Perpignan-Cedex, France 1

2

(Rece£ved 16 January 1997,. revised 3 .l'vlarch and 28 1Ylarch 1997,. accepted 28 1\Ilarch 1997)

SUMlVIARY

Data on parasites of rodents, collected over an 18-year perioq. on the Iberian peninsula, were used to find the determinants of parasite species richness ..A. total of 77 species of helminth parasites (nematodes, cestodes and digeneans) was identified among 16 species of rodents. Parasites were classified into groups according to their specificity towards their host and their life-cycle. 1\ working phylogeny of the rodents was proposed on the basis of molecular and paleontological data and for each host the following parameters were recorded: sample size, weight, geographical range, longevity, and life-style. Two comparative methods were used, the independent comparisons method of Pagel (1992) and the distance matrix method of Legendre, Lapointe & Casgrain (1995). The second method has the advantage of measuring the relative contribution of phylogeny. Both methods gave similar results. Overall parasite species richness correlated only with host sample size. Host body size does not correlate with any subset of parasite species richness. However, host phylogeny is a good predicator of specific parasites and the species richness of digeneans correlates with host geographical range. A phylogenetic reconstruction of host relations was performed using the parasites belonging to subgroups in which richness is correlated with host phylogeny. These parasite species were treated as Dollo characters, i.e. we made the assumption that the loss of a parasite species is irreversible. The consensus tree obtained reflects the major phylogenetic divisions of the host group. Finally, this study illustrates the relative importance of processes acting at different temporal and spatial scales (evolutionary time and actual geographical range of hosts) in determining the structure of helminth parasite fauna. Key 'words: parasite species richness, independent comparisons, specificity, biogeographical range, Iberian peninsula.

It is of great interest to discern the causal factors that explain species richness and diversity. Dealing with parasites allows one to investigate some of these factors because hosts are well-defined habitats characterized by size, weight, population density, geographical range, longevity, life-style and history (phylogeny). These characteristics allow one to search for correlates of parasite species richness. Studies on parasit'e species richness tested several determinants of parasite species richness: host geographical range (Dritschilo et al. 1975; Price & Clancy, 1983; Gregory, 1990), host body size (Guegan et al. 1992; Guegan & Hugueny, 1994); immunity (John, 1995); complexity and/or physiology of host alimentary canal (Kennedy, Bush &

* Corresponding author: Centre de Biologie et d'Ecologie tropicale et nH~diterraneenne (UlVIH. 5555 CNRS), L"'" niversite de Perpignan, 66860 Perpignan-Cedex, France. Tel: 33 (0)468662187. Fax: 33 (0)468 66 22 81. E-mail: n10rand(~univ-perp.fr. Parasitology (1997), 115, 453-466.

Printed in the United Kingdom

Aha, 1986); host ecology and ethology (Kennedy et al. 1986; Keymer et al. 1991) and evolutionary time (Brooks, 1980, 1988; Bush, Aho & Kennedy, 1990; Guegan & Kennedy, 1993) among others. Two hypotheses have been considered to explain the observed patterns: island biogeography theory (Strong, 1974; Kuris & Blaustein, 1977; Tallamy, 1983) and the colonization time hypothesis, i.e. the time since the host arrived in a new locality and was subsequently colonized by parasites (Rohde, 1989). However, Guegan & Kennedy (1993) showed that the colonization time hypothesis is related to the island biogeographical theory because of the crosscorrelation between time since the host arrived and host geographical range. Price & Clancy (1983) found a strong relationship correlation between fish host range and heln1.inth species richness but 2 later studies (Gregory, 1990; Guegan & Kennedy, 1993) question their findings: the former by shovving the bias induced by sampling © 1997 Cambridge lJniversity Press

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effort and the later by supporting a colonization time hypothesis. As Gregory (1990) pointed out, investigations on parasite species richness must take into account differential sampling effort. Differential sampling effort is a consequence of .both the researcher's salnpling procedure and of thegeographical range of the hosts? and both may affect host-researcher encount~rs, and thus directly influence the observed number of parasite species. Historical components could also be of great importance not only because they may affect the correlation bet,\\reen traits measured in related species (Pagel & Harvey, 1988) but also because of the fact that parasite richness could be. the result of accumulation of parasites among hosts over time (Price, 1990; Guegan & Kennedy, 1993; Kennedy & Guegan, 1994). 1\1ore recentl"y, Poulin (1995) and \Valther et al. (1995) eluphasized both the importance of salnple bias and phylogenetic effects in comparative studies of parasite species richness an10ng host taxa.

In this paper we investigate factors that may explain the species richness of helminths of Iberian rodents taking into account host phylogeny and sampling effo'rt. \1\1 e use 2 different comparative methods: the independent comparisons method (I C) of Pagel (1992) and the Inatrix distance method (MD) of Legendre et ai. (1995). Both methods give relative contribution of sampling effort but the MD method of Legendre et al. (1995) measures the relative contribution of phylogeny. We have limited our investigation to heln1inth parasites. A total of 77 species was morphologically identified belonging to 3 groups of helminths: Nematoda, Cestoda and Digenea. \7\Te tested 6 kinds of explanatory factors, namely host traits (body size, longevity and life-style), host geographical range, salupling effort and phylogeny. Parasite species richness is exalnined separately for each group of helminths as \vell for all groups together, \7\1 e also exalnined parasite species richness according to their host specificity.

Parasite species richness of Iberian rodents

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Time of divergence (MY) Fig. 2. Working phylogeny of rodents: evolutionary divergences. A: JVlus, Apodemus/ Rattus: 10-12 MY (fossil record; J eager et aZ. 1986); 10 MY (molecular data; Catzeflis et aZ. 1987). B: Mus / Apodemus: > 8 MY (fossil record; Aguilar & Michaux, 1987); > 8· 5 MY (fossil record; Jacob & Downs, ~ 994); 8· 5-9'5 MY (molecular data; Catzeflis et ai. 1987); 8·5 MY (molecular data; She et ai. 1990). C: Rattus rattus/Rattus norvegicus-: 2·1 MY (Molecular data; Catzeflis et ai. 1993). D: Mus nzuscuZus/ lV/us spretus: (molecular data;' She et af. 1990); 1·6 MY (molecular data; Catzefiis et aZ. 1987). E: Clethrionomys/Microtini: 3'5-4·5 (fossil record; Chaline & Graf, 1988); 4·6 MY (molecular data; Catzefiis et al. 1987); 3,7 MY (biochemical data; Graf, 1982); 4·2 MY (biochemical data, Mezhezherin& Serbenyuk 1992. F: ArvicoZa/lVlicrotus (included Pitymys, Chionomys): 2·4 MY (fossil record; Chaline & Graf, 1988); 3'5 MY (fossil record; Chaline, 1987); 3·8 MY (molecular data; Catzefiis et af. 1987); 3·2 MY (biochemical data; Mezhezherin et aZ. 1993). G: Microtus/Chionomys nivaZis: 0,6-1,0 MY (fossil record; Chaline & Graf, 1988); 2·4 MY (molecular data; Chaline, 1987; Chaline & Graf, 1988). H: Microtus / Pitymys: 1·5 MY (fossil record; Fejfar & Heinrich, 1981); 2 MY (biochemical data; Chaline & Graf, 1988). I: Arvicola terrestris I Arvicola sapidus: O' 5 MY (fossil record; Chaline & Graf, 1988); 1 MY (biochemical data ; Chaline & Graf, 1988). J: Arvicolinae/Murinae: > 20 MY (fossil record; Jaeger et al. 1985); 25-30 MY (fossil record; Lindsay, 1978); > 17 MY (molecular data; Catzefiis et aZ. 1993); 20-25 MY (immunological data; Nikoletopoulos et ai. 1992). K: Gliridae/Muroidea: > 35 MY, 40 MY (fossil record; Vianey-Liaud, 1994).

MATERIALS AND METHODS

Rattus norveg£cus (Berkenhout, 1769): AB, B, BU,

CR, GE, GU, LE, L, MA, SO, T, TO, V.

Data on hosts

Sixteen species of rodents vvere trapped over an 18year period (November 1973 to August 1991). The numbers of individuals of each species are given in Table 1. Most of the Spanish part of the Iberian peninsula was prospected for the collection of rodents. The geographical origins of each sample of each species of rodent are as follows (see Fig. 1 for geographical locations and codes). Muridae. (Linna~us, 1758): B, L, T, GE, ZA, TE, HU, GR, ], MA. .1\IIus 1nusculus Linnaeus, 1766: B, L, GE, LE, MA,], M,T. .1\!1us spretus Lataste, 1883: B, L, rID, TE, J, 1\1..-\, B.\, T. Rattus rattus (Linnaeus, 1758): B, BU, C.L~, GR, ], rvI./\, 5, T, V.

Apodemus sylvaticus

Arvicolidae (Pitymys) duodecimcostatus (De SelysLongchamps, 1839): i\, AB, B, CA, GE, GR, HU,], L, M, MA, lVIU, T, TE, TO, V. Microtus (Pitymys)lusitanicus (Gerbe, 1879): i\V, BI, BU, HU, LE, LO, LU, lVi, OR, 0, P, PO,S, SG, SO, TE, VI. Microtus (Pitymys) pyrena£cus (De SelysLongchamps, 1847): BI, NA. Microtus agrestis (Linnaeus, 1761): B, BI, BU, GE, HU, L, La, LU, NA, OR, 0, P, PO,S, SO. Microtus arvalis(Pallas, 1778): i\.B, BI, BU, CR, GE, HU, LE, L, LO, M, P, SG, S0, TE . Microtus cabrerae (Thomas, 1906): ee, CD, IV!. 1Ylicrotus (Ch£oTlolnys) 'n£valis (lvIartins, 1842): .J;."\l, B, ELl, GE, GR, HU, L, LE, LlJ, 1\1, 0, OR, S, SIG, SO, ZA. Arrvicola sapidus l\IIiller, 1908: i\\/, B, BU, CC, CA, Microtus

C. Peliu and others

456

l\1orozov-Leonov, 1993; Catzeflis et al. 1993; Jacob & Do\vns, 1994; Vianey-Liaud, 1994) to provide a working phylogenetic tree (Fig. 2).

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Parasites were removed from viscera, liver, and digestive tract. Collection methods are described in previous works (see list below). The list of parasite species is given in Appendix 1 and summarized in Table 2. A total of 77 species of helminths belonging to Nematoda, Cestoda and Digenea was identified on the basis of lTIorphological characters . Voucher specimens of each species were preserved in alcohol and deposited in the Laboratory of Parasitology (Faculty of Pharmacy, University of Barcelona). Original data and other references can be found in Mas-Coma & Feliu (1977), Feliu (1980, 1987), Feliu et ai. (1980, 1983, 1984a, b, 1985 a, b, 1987 a, b, 1991, 1993). Lije-histo1l'Y of parasites

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Fig. 3. Relationships between host geographical range and (A) euryxenous parasites, (B) digenean species richness vvhen all variables are controlled for host sample size.

CU, GE, GR, HU, LE, L, LO, LU, lVI, NA, 0, P, PO, SO, T, TE. Arvicola tel'rest7~is (Linnaeus, 1758): BI, BU, L, LE, LV, P, S. Cleth1~ionon1Ys glareolus (Schreber, 1780): LU, LO, S, BI, HU, L, BU, GE, B, P, \11. Gliridae Eli01nys quercinus (Linnaeus, 1766): AV, B, BU, CU, GE, HU, L, 1\1, 1\1A , S, TE, TO,Zl\.

ee,

\1oucher specimens of rodents are deposited in the Laboratory of Parasitology (Faculty of Pharmacy, University of Barcelona). N umber of hosts sampled and other characteristics of hosts are given in Table 1. Data on life-history traits were taken from Gosalbez (1987), Niethammer (1982a, b), Corbet & Harris (1991), l\lacdonald & Barrett (1993) and Hausser (1995). The phylogeny of rodents is not fully resolved. \7\1 e used se\,reral studies (Lindsay, 1978; Fejfar & Heinrich, 1981; Graf, 1982; Jaeger et al. 1985; Jaeger, Tong & Dennis, 1986; ..A..guilar & IVlichaux 1987; Catzeflis et aZ. 1987; Chaline, 1987; Chaline &, Graf, 1988; She et al. 1990; l\1ezhezherin & Serbenyuk, 1992; l~ikoletopoulos, Chondropoulos 8: Fraguedakis- Tsolis, 1992; l\1ezhezherin,Zykov &

Digeneans and cestodes have a life-cycle involving at least 2 hosts, a definitive and 1 or 2 intermediate ones. Rodents can be either definitive or intermediate hosts of cestode species. The first intermediate host of digeneans is always a terrestrial or a freshwater mollusc. Nematode species have either a direct life-cycle involving 1 definitive host or an indirect life-cycle involving 1 definitive host and 1 intermediate host. Parasites can also be described by their specificity towards their host. Four kinds of specificity are defined according to Euzet & Combes (1980): oioxenous parasite: highly specific to a host species; stenoxenous parasite: specific at the level of host genus; oligoxenous parasite: specific at the level of a host family; euryxenous parasite: infests a broad range of non-related hosts. In our analysis, stenoxenous and oioxenous parasites are combined because of the few parasite species belonging to the oioxenous type. Comparative anaZ.ysis

In general, closely related species of parasites are more likely to exhibit similar development than distantly-related species (Pagel & Harvey, 1988)...~ number of comparative methods have recently been proposed to control for the effects of phylogeny in order to study the correlation among traits (Felsenstein, 1985; Garland, Harvey & Ives, 1992; Pagel, 1992; but see Harvey & Pagel, 1991). l\ ne\;\/ approach to the problen1 V\Till be used in this paper. I t is an adaptation of the 111ultiple regression on distance matrices, proposed by Legendre et al. (1995) to explain nlatrices representing either plain distances, dendrogralTls or cladogran1s, using other

457

Parah'ite species richness of Iberian rodents

Table 1. Host names of the rodents vvith code, sampling effort (number of individuals), geographical range and SOlne life-traits

Host species Muridae Apodemus sylvaticus (Linnaeus, 1758) ~Mus musculus Linnaeus, 1766 Mus spretus Lataste, 1883 Rattus rattus (Linnaeus, 1758) Rattus norvegicus (Berkenhout, 1769) Arvicolidae Pitymys duodecimcostatus (De Selys-Longchamps, 1839) Pitynlys lusitanicus (Gerbe, 1879) PitynlYs pyrenaicus (De Selys-Longchamps, 1847) Microtus agrestis (Linnaeus, 1761) lVlicrotus arvalis (Pallas, 1778) lVlicrotus cabrerae (Thomas, 1906) Chiononzys nivalis (lVlartins, 1842) Arvicola sapidus Miller, 1908 Arvicola terrestris (Linnaeus, 1758) Clethrionomys glareolus (Schreber, 1780) Gliridae Elio-mys quercinus (Linnaeus, 1766)

Code

Sampling effort (no. of trapped hosts)

ASY

1213

19-33

18

505000

Terrestrial

MlVIU

758

12'5-29

18

505000

Terrestrial

MSP RRA

333 116

8,5-17,5 135-240

12 12

505000 505000

Terrestrial Terrestrial

RNO

654

180-415

12

505000

Terrestrial

PDU

130

19-32

12

490000

Fossorial

PLU

172

14-23

12

210150

PPY

5

18-24

12

32690

lVIAG

171

21-41

12

189135

Semiunderground Semi underground Terrestrial

lVIAR

311

17-41

12

135430

MCl\.

70

17-64

12

74720

CNI

190

21-70

12

74720

ASA

139

155-300

24

505000

ATE

257

100-180

18

74720

Underground

CGL

509

19'5-30

18

98070

Terrestrial

ELI

109

505000

Terrestrial

matrices also representing plain distances, dendrograms or cladograms. The coefficient of determination of the multiple regression, as well as the partial regression coefficients, are tested for significance through permutation methods. This method is used to overcome the problem of controlling for the effect of a phylogeny in studying the correlation among traits. (1) The dependent variable, parasite species richness, is transformed into a distance matrix Y by computing the' distance' among values (absolute value of the difference, vvhich is also equal to the Euclidean distance among values). (2) Similarly, host vveight, number of hosts sampled, biogeographical range and other variables are turned into 'distance' matrices X2, X3, ... , Xn. (3) The host phylogeny is represented in the analysis by a matrix Xl of patristic distances among species. .L1. multiple regression is computed vvith Y as the dependent variable. ftegression coefficients are

Weight (g)

60-120

Longevity (month)

Host geographical range (km 2 )

\'\1 ay of life

48-60

Semiunderground Semiunderground Terrestrial Amphibious

obtained for Xl, X2, X3, ... , Xn and tested for significance using the method for simple dependent distance matrices of Legendre et al. (1995). Multiple regression coefficients are actually partial regression coefficients (Sakal & Rohlf, 1981). Probabilities were computed after 999 random permutations of the distance Inatrix; as a consequence, the lowest attainable probability value is 0·001. The values in both distance matrices were standardized before computing the regression, so that there is no intercept and the regression coefficients become standard regression coefficients (Manly, 1991 ; Legendre et al. 1995). The backward elimination procedure for selecting an optimal subset of explanatory matrix variables is used. The result of the selection procedure is given. vVe used the Permute!2 package of Casgrain (1 994) . The second method is the rflethod of independent comparisons (Ie) (Burt, 1989; Pagel, 1992). This

458

C. Fel£u and others

Table 2. Number of parasites in each species of rodents (see i\ppendix 1 for a detailed list) Parasites are defined according to their specificity to\vards their host: stenoxenous, oioxenous, oligoxenous or euryxenous (codes of rodent species are given in Table 1, see Materials and l\1ethods section for definition of terms.)

Host species

Muridae A. sylvaticus (ASY) M. musculus (MMU) M. spretus (MSP) R. rattus (RRA) R. norvegicus (RNO) Arvicolidae P. duodecimcostatus (PD U) P. lusitanicus (PLU) P. pY1~enaicus (PPY) M. agrestis (MAG) M. a1~valis (MAR)

M. C.

A. A. C.

cab1~e1'ae

(MCA) nivalis (eNI) sapidus (ASA) ten~estris (ATE) glareolus (CGL)

Gliridae E. que1'cinus (ELY)

Stenoxenous Total and Nematodes Digeneans Cestodes Oioxenous -Oligoxenous Euryxenous parasites

15

5

9

7

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6

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13

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6

5

4

6

5

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5

6

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6

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9 9

5

3

14 12

4 12

0 4

4 17

10

3

13

4

1 2

14

5

3 8 6 4 "6 6 4 10

7

method is now largely used in cOll1parative analysis, and readers are invited to refer to the original references for further details on methods (Garland et aZ. 1992; Purvis & Rambaut, 1995). We used the CAlC package of Purvis & Rambaut (1994, 1995). Data on host body size, number of hosts sampled and host biogeographical range \vere previously Ln transformed; data on parasite species richness were Ln (x + 1) transformed.

RESULTS

Parasite spec£es richness

In the Iberian peninsula, murid rodents harbour a higher nUll1ber of parasite species (mean = 18'4) than arvicolid rodents (mean = 12'7) (Table 2). Nematodes are dominant among the helminth fauna and digeneans are less common.

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6

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7

2

9

9

17 10 20

7

0

4

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(P = 0·001). Sampling effort is also the only variable explaining total parasite species richness using the IC method (P = 0'026).

Pal'asite species richness and parasite g1'OUPS

Host sampling effort appears to be the main factor explaining the species richness of nematodes, whatever the ll1ethod used (Tables 3 and 4). Both methods found no significant correlation between any variables and the species richness of cestodes except that the DM method revealed significant influence of host phylogeny (Table 3, P = 0'028). Host range is significantly correlated \\rith digenean species richness (Table 3, P = 0·003 for DM; Table 4, P = 0·001 for IC). The IC method gives a second explanatof".Y variable \\rhich IS sampling effort (Fig. 3; Table 4, P < 0'001). Parasite species richness and parasite specificity

Parasite species richness and sampling effort

A significant correlation bet\\Teen host sample size and total parasite species richness was found using both comparative methods (Tables 3 and 4). Six independent matrix variables (host sampling effort, host biogeographical range, host phylogeny, host longevity, host \\7eight and host's life-style) \\7ere tested for their correlations \\Tith the dependent 111atrix-variable (total parasite species richness). N one of thein except san1pling effort significantly correlates \\Tith the total nU111ber of parasite species

Highly specific or oioxenous parasites correlate ",rith host phylogeny (Table 3, P = 0·003; DM method) or \\!ith no factors (Table 4, IC method) while the species richness of less specific or oligoxenous parasites correlate \\rith host phylogeny (Table 3, P = 0'024; Dl\1 method). Both methods yield comparable results for the species richness of non-specific or euryxenous parasites. Salnpling effort and host range correlate \vith the species richness of this type of parasite (Fig. 3) .

r

I

459

Parasite species richness of Iberian rodents

Table 3. Results of the backward elimination procedure of the distance matrix method for selecting an optimal subset of explanatory matrix-variables for each matrix-dependent variable (Std. b is the standard partial regression coefficient. All probabilities (P, onetailed), are computed after 999 random matrix permutations of the dependent matrix-variable. At each step, the variable with the largest probability is eliminated if its probability is larger than the Bonferroni-corrected significance level (a = 0'05/number of variables in the model at the given step) (see Materials and Methods section) Dependent matrix-variable (species richness)

Independent matrixvariable

Std. b

R2

(P)

(P)

0·676 (0'001) 0·504 Oioxenous and stenoxenous parasites Host phylogeny (0-003) 0-573 Host phylogeny Oligoxenous parasites (0-024) 0-616 Host sampling effort Euryxenous parasites (0-001 ) Host geographical range 0-393 (0-001 ) 0-666 Host sampling effort Nematodes (0-001 ) Host geographical range 0-477 Digeneans (0'003) 0-455 Host phylogeny Cestodes (0-028) Host sampling effort

Total parasites

0-456 (0-001) 0-254 (0-003) 0-329 (0-024)

0-703 (0-001 ) 0-443 (0-001 ) 0-228 (0-003) 0-207 (0'028)

Table 4_ Summary of the linear regression models (ordinary least square regression without intercept) using independent contrasts on some aspects of the parasite species richness and host traits Dependent variable (species richness)

Independent variable

(P)

Slope±s.D.

Total parasites

Host sampling effort

0·23 ± 0·09 (0'0260)

0-405 (0-0260)

None Oioxenous and stenoxenous parasites Oligoxenous parasites None Euryxenous parasites Sampling effort

Nematodes Digeneans

Cestodes

0'24±0-O6 (0'0034) Host geographical range 0'46±0'07 (0'.0001 ) Host sampling effort 0'32±0'04 (0'0001 ) Host· geographical range 1·28 ±O-12 (0-0001 ) Host sampling effort 0-41 ± 0·11 (0-0048) None

The use of parasitological data to provide a tree of hosts

Results of both comparative methods are similar, an advantage of the' distance method is that the model provides an estimate of the contribution of the phylogeny. vVe used the parasite species belonging to parasite subgroups \vhich are correlated with the host

0·896 (0-0001) 0·881 (0-0001)

0·927 (0'0001 )

phylogeny to build new host trees. Firstly, we used all parasite species as unordered characters. The data on parasite species are transformed into a matrix of presence/absence of each parasite species for each host species. vVe used thePi\UP package (Swofford, 1991 ). According to the results of Table 3, oioxenous and oligoxenous parasite species and all the cestodes were used and coded as Dollo characters. P. pyrena£cus "vas removed because of its small sample

c. Fel£u

and others

460

]

A. sylvat/cus

59 80

71

~

M. musculus R.rBttus R. norvegicus M. spretus

s:

C

:D

6

» m

P. duodecimcostatus

> :%J < 0

P. lusitanicus

53

M. agrestis M. arvalis

0 r-

M. CIIbrerae C. nivalis

80

C > m

A. sapidus A. terrestris

c.

glBreolus

Eliomys

GllRIDAE

Fig. 4. Relationship betV\Teen rodents using parasites as characters in a parsimonious construction tree. Subsets of parasite species are coded as Dollo characters (see text for the choice of parasite species) (values of boostrap analysis are given on the figure, 100 replicates). Note that major phylogenetic relationships are found and the correct position of Cleth,"ionomys gla,"eolus as a sister-group of the other Arvicolidae. Pitymys pyraneicus was removed from the analysis because of the small sample size.

size (5 individuals, Table 1). The bootstrap tree (Fig. 4) reflects the major divisions of the host group. However, the position of 1\1. spretus within the Muridae is not congruent with the working phylogeny .. However, C. glareolus is the sister-group of all other arvicolids as in the working phylogeny.

DISCUSSION

Rodents have been the subject of several investigations on the population dynamics of parasites in Europe (Kisielewska, 1970; Haukisalmi, Henttone & Tenora, 1988; l\10ntgomery & l\10ntgomery, 1988) but surprisingly no work has been done on the determinants of their parasite species richness. Most of the studies on parasite species richness have been conducted by using data from literature (Price & Clancy, 1983 ; Gregory , 1990; Keymer et ale 1991 ; Guegan & Kennedy, 1993). The present study is an exception as it uses data obtained by the same investigator using standard procedures, which make them more appropriate for comparative analyses than data gathered in the literature. Poulin (1995), Walther et ale (1995) and Gregory, Keymer & Harvey (1996) emphasized that both sampling effort and phylogeny must be controlled for \vhen investigating the parasite species richness. Hence, a \iVorking phylogeny of rodents has been provided and tV\ 0 comparative methods Vlere used, both taking into account san1pling effort. 7

S0111.pl£ng e.ffort and parasite species richness In our study, salnpling effort is the only correlate ,\Then considering all parasite species (Gregory,

1990; Gregory et al. 1996; \Valther et aZ. 1995). For example, host body size and/or host geographical range have been shoV\Tn to correlate V\Tith helminth richness in fishes (Price & Clancy, 1983), but further studies that take into account sampling effort reveal no significant influence of both factors on parasite richness (Gregory, 1990; Guegan & Kennedy, 1993). V\Te may suggest that the total parasite species richness has not reached its upper limit. Hence for other cases like non-specific parasites (euryxenous parasites) an asymptote of species richness seen1S to be reached suggesting that sampling effort is a bias more or less important depending on the slope of the relation between richness and sampling effort.

Pa1"asite species richness and geographical range

Controlling for both sampling effort and host phylogeny, the species richness of euryxenous parasites and digenean parasites is correlated \vith host range. The increase of host range presumably allows the host to encounter more parasite species (Price & Clancy, 1983; Gregory, 1990). This pattern is clearly found for non-specific parasite species and particularly for digeneans having terrestrial invertebrate intermediate hosts.

Pa1r asite species 1'ichness and host life-traits

Host body size does not seem to play a role in the parasite species richness of rodents, in contrast with studies on parasites of fish, birds and mammals (Bush et ale 1990; Gregory, Keymer & Harvey, 1991; Gregory, 1990; Gregory et ale 1996). For example, Bell & Burt (1991) and Guegan et ale (1992) showed a significant increase of the parasite species richness with the increase of host size. HOV\Tever, using the independent comparison method, Poulin (1995) failed to find any relationship between host body size (bird, mammal and fish) and parasite species richness. We also failed to find any significant relationships bet\veen parasite species richness and the host life-style (terrestrial, an1phibious, underground, sen1i-underground).

Pa1 asite spec£es 1 ichness and host phylogeny r

r

The third explanation of parasite species richness is linked to host phylogeny. The DM method shoV\7 s that richness of some types of parasites is directly linked V\Tith the phylogeny of their host. This pattern is clearly illustrated when using parasite species as characters for a tree reconstruction of host relationship. The relatively host-specific parasites have the salne property as Dollo characters: yvhen a parasite is lost during evolution it is not able to return. Thus, synapon1orphies reflect con1n1on losses of characters \?\There a loss is either a true loss, the

Paras£te species richness of Iberian rodents

host escaping the parasite or caused by speciation yielding a nevv parasite species. However, there is no indication of any parasite being lost through evolution (Bush & Kennedy, 1994). The major divisions of the phylogeny of the rodents are recognized: Muridae, Arvicolidae and Gliridae. Some changes are noted within groups. Mus spretus typically has the helminth fauna of the murids but this species is not infected by other helminths thus explaining its position in the tree as a sister-group of all other murids. However, M. spretus is not a rodent commensal of man and its arrival in the Iberian peninsula from North Africa is more recent. Apodemus sylvaticus is infected by a great number of helminth species and is widely distributed on the Iberian peninsula. This species is frequently associated with other rodents and is in a middle position within the Muridae. The helminth fauna of Rattus rattus is poor compared to other murids possibly because its range is restricted by the presence of the competitively superior Rattus norvegicus. Clethrionomys glareolus is the sister group of the other Arvicolidae. The whole Arvicolidae is isolated from the Muridae and from the Gliridae. Pa1~asite

species richness and equilibrium

Brooks (1980), Price (1 987) and Rohde (1 989) all have suggested that parasite communities are noninteractive for different reasons. For example, Brooks (1980) argued that historical factors are the main explanations. Price (1987) hypothesized the role played by stochasticity, which induced a turnover of the parasite fauna, and proposed an asymptotic equilibrium model. Rohde (1989) claimed that parasite species accumulate in host species without saturation. For example, a non-asymptotic relation-

461

ship has been proposed by Strong (1 974) for the case of insects on trees. The absence of any relationship vvith host body size strongly suggests that niches are vacant within hosts. However, vve do sho,,, that non-specific parasites could accumulate when host geographical range increases. In addition, our study clearly demonstrates that host phylogeny and thus evolutionary time plays a significant role in the accumulation of parasite species within Iberian rodents. The Iberian peninsula is like an island separated from Europe by the Pyrenean mountains and from Africa by the Gibraltar channel. Overall, rodents inhabiting the Iberian peninsula have fewer parasites than their European congeners (Feliu, 1980) although, Pitymys lusitanicus, an endemic rodent of the peninsula, does not show a decrease in its helminth richness. Nevertheless, Microtus cabrerae, another endemic rodent, harbours a lesser number of parasite species. Finally, the invasion of the Iberian peninsula by the miomorph rodents (Muridae and Arvicolidae) occurred at different periods. The Muridae appeared in the Upper Miocene (9'5 MY) whereas the Arvicolidae have been recorded in the Pliocene (3-4 MY) (Gosalbez, 1987). Hence, the Muridae seem to be more heavily parasitized than the Arvicolidae. We are grateful to Roderick Page, Dale Clayton, Pierre Legendre, Yannis Michalakis, and ,Richard Gregory for their comments on earlier drafts of this paper. We thank Robert Poulin and an anonymous referee for their valuable comments which greatly improved this manuscript. Many thanks to .A.ndy Purvis for providing CAlC and Philip~e Casgrain for providing Permute! and for helpful discussions. Special thanks for Bruno Walther and Dan Haydon for discussions and help. This work was supported by the PICASSO initiative and theCNRS.

1. List of the helminth parasites of Iberian rodents (the codes of rodent species are given in Table 1) with some of their life-style traits. rrhe presence of each parasite species in a given rodent is marked by a x. Codes of parasite life-style are: DLC, direct life-cycle nematode; ILC, indirect life-cycle nelnatode; 1.1, larval cestode; A, adult cestode; T, trematode with terrestrial first intermediate host; Aq, trematode vvith aquatic first intermediate host.

APPENDIX

Parasite species

Life-style

ASY MMU MSP RRA RNO PDU PLU PPY MAG MAR MCA CNI ASA ATE CGL ELI

~

~

~.

e

~ ~

;:;-..

~ v;

Nematodes 1'r£churis 111uris (Schrank, 1788) l'richuris sp. AOllchotlzeco 01l11ulosa (Dujardin, 1843) A. 111uris-sylvatici (Diesing, 1851) A. 111yoxi-nitellae (Diesing, 1881) /-l. wioletti (I{llchljadeva, 1950) E'ucoleus gastriCl_is (Baylis, 1926) E. bacillatus (Eberth, 1863) Calodili171 hepaticu111 (Bancroft, 1893) l'richoso111oides c1~assicauda (Bellingham, 1840) C'apilla1"ia sp. Gallegostrollgylus ibicellsis Mas-coma, 1977 Angiostrollgylus dujardini Drodz et Doby, 1970 Ii eterakis Spll11l0Sa Schneider, 1866 1\1astophorus 11lllris (Gmelin, 1790) Rictularia proni Seurat, 1915 Pterygodennatites hispallica Quentin, 1973 1'richostrongylus retortaefor111is (Zeder, 1800) flehg1110so111o£des polygyrus (Oujardin, 1845) HeHgl1loso1110ides laevis (Oujardin, 1845) H elig1110so111zon costellatunl (Dujardin, 1845) [-{elig111oso111oides glareoli Baylis, 1928 Nippostrongylus brasiliensis (Travassos, 1914) l\1o!£neus patens (Dujardin, 1845) (~arolinensis 111inulus (Dujardin, 1845) "Strongyloides raui Sandground, 1925 Syphac£a frederici Roman, 1945 S. I1l1l1'is (Yamagllti, 1935) S. lligeriana (Baylis, 1928) S. obvelata (Rudolphi, 1802) S. petfllSe'lviczi Bernard, 1966 S. stro111a (Linstow, 1884) Aspiculuris tetrapte1'a (Nitsch, 1821) Aspiculuris sp.

0

OLC OLC DLC? DLC? DL,C? DLC? OLC? Ol.lC? DLC OLC

x

x

x

x

x x

x

x

x

x

x

x

x

x

x x

x

x x x x

x x

x

x

x

x x

x

x

x

x

x

x

ILC 11.JC OLC ILC ILC IIJC OLC Ol.lC OLC DLC OLC DLC DLC OLC DLC DLC DLC OLC DLC OLC DLC DLC OLC

x

x

x

x

x

x x x

x

x

x

x

X

x x

x x

x

x

x

x

x

x x x

x

x x

x x

x x

x x x

x x

x

x x

x

x

x x x

x

x

x

x

x

x x

x

x x

x

x

x

x

x

x

x

x x x

x

x x

x

x x

x

x

Cestodes Taenia taelliaefonnis (Batsch, 1786) Taenia tenuicollis Rudolphi, 1819 1'. 11lartis (Zeder, 1803) T. par"l)o Baer, 1926

L L

1.1 L

x

x

x

x

x

x

x x x

x

x x

x

x x

x

x

x

x ~

0"

lv

~ l::l

1'. crassiceps (Zeder, 1800) l'./>o(vacanlha (Leuckart, 1856) C:/adotaenia globlfera (Batsch, 1786) C'afenolaenia pllsilla (Goeze, 1782) ('. aSl~atica l'enora et Murai, 1975 ('. cricetOrlal1 (I{irschenblat, 1949) [Jseudocatenotaenia 111atovi (Genov, 1971) ~Skljabinotaenia lobata (Baer, 1925) -I.4noplocephaloides dentata (Galli-Valerio, 1905) Paranoplocephala 1nas-c01nai Murai et aI. 1980 P. oJJ1phalodes (lIermann, 1783) P. gracilis Tenora et Murai, 1980 CJallegoides arfaai (Mobedi et Ghadirian, 1977) 1\1esocestoides sp. liY1l1ellolepis dinzinuta (Rudophi, 1819) Ii. fraterna (Stiles, 1906) Fl. ,",franlinea (Goeze, 1782) H. asyn1Jnetrica Janicki, 1904 H. horr£da (Linstovv, 1901) ll.lJ1yoxi Rudolphi, 1809 HYl1zcnolepis sp.

Trennatodes Brachylailna sp. Plagiorchis talassel1sis 1'okobaev et Erkulov,

L

2

x

1.1 L

~.

X

~

x

A A A A A A A A A A L A A A A A A A

x

l' Aq

x x

Aq T

x

x

~ ~ ("")

x

~.

x

V)

tS

x

x x

~

~

x

x

x

x

x

x

x

x

x x

x

x

x x

x

x

x

x

x x

x

x

X

~ ~

c:;-.. ~

"'i

5·

x

x

;:!

a

x x x

x x

x

x

x

x x

x

~-

x

~

x x

V)

x x

x

x x

x

x

x x x

x

x

x

x

x

x

x

x

x

x

x

x x

1966 Plagiorclzis sp. (-;orrigia 'villa (Dujardin, 1845) DicrocoeliulJl sp. B rachy/eeit/nan elio1nydis Jourane et Mas-

x

x x

x

T T?

x x

x x

COlna, 1977 E'chinostol1za echinatu111 (Zeder, 1803) Echilloparyphiurn recurvatlun (von l..Jinstow,

Aq Aq

x

x x

1873) HypoderaeUJ11 c01loideU111 (Block, 1782) Postorchigenes gY11111esiclis l\1as-Colua et aI. 1981 l\daritrelna sp. C'ollyrieloides 111assanae Vaucher, 1969 Notocotylus neyrai Gonzalez Castro, 1945 lV. gOJ1zalezi Simon Vicente et al. 1985 lVlediogoni111lls jOllrdanei Mas-Coma et

Aq Aq Aq ~r ? Aq Aq Aq

x x

x x x

x

x x

x

x

x

x x

x

x

H.ocan1ora, 1978 Psilotrenlll spiculiger1l11l (Muhling, 1898) 1\1acyella apodenli Jourdane et Triquell, 1973 Nephrotre1ua truncatlll11 (Leuckart, 1842)

Aq Aq Aq

x x x -+-

Q\

w

464

C. Feliu and others

c. (1980). Contribucion al conocimientot de la helmintofauna de microlnamiferos ibericos. Hehnintos de Gliridae y Muridae (Rodentia). Tesis Doct. Universitat Barcelona, 556 pp. FELIU, c. (1987). Efecto de 1a dispersion geografica de una especie hospedadora sobre su parasitofauna: El caso de los helintos de las poblaciones ibericas de Glis glis (Linnaeus, 1766) (Rodentia: Gliridae) y Cleth1~ionomys glareolus (Schreber, 1780) (Rodentia: Arvicolidae). Revista Ibe1'ica de Pa7'asitologia 47, FELIU,

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