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Persistence and stability of the component helminth community of the foothill yellow-legged frog, Rana boylii (Ranidae), from Humboldt County, California, 1964-1965, versus 2004-2007.

INTRODUCTION

The foothill yellow-legged frog, Rana boylii Baird, 1854, occurs in parts of Oregon, California and perhaps Baja California although it has suffered a great reduction in its range (Stebbins, 2003). Parasite community structure is hierarchical: a parasite infrapopulation includes all members of a single species of parasite within an individual host; a parasite infracommunity includes all infrapopulations within an individual host; a component parasite community represents all infracommunites within a given host population; and a supercommunity represents all helminth species within all host species in a defined locality (Bush et al., 1997). Much of the work on anuran helminths has concentrated on faunistic surveys based upon collections taken during a single season. A general conclusion drawn from these studies is that helminth communities of anurans are depauperate and isolationist (Barton, 1997). However, two measures of helminth community structure developed by Meffe and Minckley (1987) are not addressed by single season collections: persistence, a measure of presence or absence of a species over time, and stability, a qualitative measure based upon the relative constancy of species abundances over time. These measures can only be addressed with long-term studies and to our knowledge there are few such studies: in Poland, Grossman and Sandner (1953), in Russia, Markov and Rogoza (1949, 1953) and in England, Lees (1962) published data on seasonal variation in the prevalence of helminths of R. temporaria. Also in Poland, Kuc and Sulgostowska (1988) published data collected from R. ridibunda over a period of 4 y. In the United States (California), Goldberg and Bursey (2001a) examined specimens of Hyla regilla (currently Pseudacris regilla) collected 1943-1998. The purpose of this paper is to examine persistence and stability of the component helminth community of R. boylii from northern California.

MATERIALS AND METHODS

One hundred fifty Rana boylii (mean snout-vent length [SVL] not determined) and 100 R. boylii (SVL, 45.2 mm [+ or -] 9.5 mm SD; range, 19-70 mm) collected in Humboldt County, California 1964-1965 and 2004-2007, respectively, were utilized in this study. Collection localities and number of frogs collected at each locality are presented in Figure 1. The frogs of the 1964-1965 collection were from Walker (1965), examined within 48 h of collection; double-pithed then the body cavity was opened by an incision from vent to throat and the lungs, liver, gall bladder, heart, stomach, intestine, rectum, kidneys and urinary bladder removed and examined individually for helminths. The mouth and coelomic cavity were also examined. Cestodes and trematodes were killed with hot formal-acetic acid alcohol (FAA), stained in hematoxylin and examined as whole mounts; nematodes were killed in hot FAA and mounted in lactophenol for examination. Frogs of the 2004-2007 collection were captured at localities previously sampled (Fig. 1), pithed on site, fixed in 10% neutral buffered formalin and preserved in 70% isopropanol. At necropsy, the body cavity was opened by an incision as before. The abdominal cavity, stomach, intestine, lungs, urinary bladder were examined separately for helminths using a dissecting microscope. These helminths, fixed in situ, were removed to vials of 70% ethanol. Nematodes and acanthocephalans were identified from temporary lactophenol wet mounts; cestodes and trematodes were regressively stained in Delafield's hematoxylin, mounted in Canada balsam and identified from the whole-mounts. Where possible, chi square ([x.sup.2]) statistic was used to compare infection rates between the two samples. Voucher helminths from the 2004-2007 collection were deposited in the United States National Parasite Collection, USNPC, Beltsville, Maryland: Distoichometra bufonis (USNPC 100930); Glypthelmins quieta (USNPC 100931); Gorgoderina multilobata (USNPC 100932); Haematoloechus kernensis (USNPC 100933); Megalodiscus microphagus (USNPC 100934); Digenean metacercariae (USNPC 100938); Cosmocerca variabilis (USNPC 100935); Rhabdias ranae (USNPC 100936); Acanthocephalan cystacanth (USNPC 100937). Frogs were deposited in the herpetology collection of the University of Michigan (UMMZ), Ann Arbor, Michigan.

[FIGURE 1 OMITTED]

RESULTS AND DISCUSSION

Thirteen helminth species were found; one species of Cestoda (Distoichometra bufonis); six species of Digenea (Deropegus aspina, Glypthelmins quieta, Gorgoderina multilobata, Haematoloechus kernensis, Megalodiscus microphagus, an unidentified species represented by Echinostome metacercariae); four species of Nematoda (Cosmocercoides variabilis, Rhabdias ranae, Hedruris sp., a unidentified species belonging to the Physalopteridae [third stage larvae only]; and two unidentified species of Acanthocephala (Centrorhynchid and Oligacanthorhynchid cystacanths). A total of 1585 individuals was tallied for the 1964-1965 sample and 357 individuals were listed for the 9004-2007 sample. A compilation of helminth species from the two collections of Rana boylii is presented in Table 1.

Distoichometra bufonis, Glypthelmins quieta, Gorgoderina multilobata, Haematoloechus kernensis, Megalodiscus microphagus, Cosmocercoides variabilis and Rhabdias ranae are common parasites of anurans; reported Californian hosts are listed in Table 2. The remaining helminth species found in this study are typically associated with non-anuran hosts. Deropegus aspina is commonly found in fresh-water salmonid fishes of western Oregon, but has been reported in the salmon Oncorhynchus kisutch collected in Humboldt County, California (McCauley and Pratt, 1961) and Rana boyli collected in Butte County, California (Ingles, 1936). Echinostomatid digeneans are parasites of reptiles, birds and mammals; however, cercariae may encyst on or in anurans (Prudhoe and Bray, 1982). However, to our knowledge, there are no reports of echinostome cysts in California anuran hosts. Species of Hedruris are generally associated with salamanders (Baker, 1987) and in the northwest United States have been reported in Taricha torosa and T. granulosa (Chandler, 1919; Lehmann, 1954, 1956). To our knowledge, there are no reports of a species of Hedruris from California; but Hedruris sp. has been reported in Bufo boreas, Bufo woodhouse, Hyla regilla, Rana aurora and Rana catesbeiana from the northwest United States (Lehmann, 1965). Species of Physaloptera are commonly found in the stomachs of reptiles, birds and mammals (Morgan, 1941); but, because physalopterans require an insect intermediate host any insectivore might harbor third stage larvae. Goldberg et al. (1993) provided a list of North American anurans in which third stage larvae but no adults had been reported. Insects are the usual intermediate hosts for acanthocephalans (Nickol, 1985); thus, their occurrence in insectivores could be anticipated. However, when inappropriate hosts are encountered, acanthocephalans remain as juvenile forms (Nickol, 1985).

Sorenson's quotient of similarity (Q/S) (Magurran, 2004) is based on species presence in a community and for this study equals 76.2 (Q/S ranges from 0, no species in common, to 100, all species in common). The difference between the two samples results form the absence in the 2004-2007 collection of four species, Deropegus aspina, Hedruris sp., physalopteran larvae and Centrorhynchid cystacanths. It should be noted that these three species were found in 3, 1, 1, 4 hosts, respectively, in the 1964-1965 sample. In that sample, D. aspina was found at two sites, Hedruris at one site, physalopteran larvae at one site and Centrorhynchid cystacanths at two sites (Table 3); there were comparable host collections for the two samples at the sites yielding D. aspina, Hedruris sp. and physalopteran larvae, but in the 2004-2007 collection no hosts were collected at the sites previously yielding C. cystacanths (Fig. 1). Whether the absence in 2004-2007 is due to small sample size or represents actual loss to the community cannot be determined.

Morisita's index considers number of species, number of individuals and proportion of the total represented by each species and for this study equals 0.31 (Morisita's index ranges from 0, no similarity, to 1, identical). The difference between the two samples is primarily due to fewer helminths collected in the 2004-2007 sample, approximately one fifth of the number in the 1964-1965 sample. With the exception of Glypthelmins quieta, Haematoloechus kernensis and Oligacanathorhynchid cystacanths, prevalence for each species was greater in the 1964-1965 collection (Table 1). Where there was sufficient data, infection rates between the two samples were evaluated by [x.sup.2]. Infection rates for Distoichometra bufonis and Glypthelmins quieta were not significantly different between the two samples ([x.sup.2] = 3.46 and 1.36, respectively, 1 df, P > 0.05); infection rates of Gorgoderina multilobata, Haematoloechus kernensis and Rhabdias ranaewere significantly different between the two samples ([x.sup.2] = 5.66, 1 df, P < 0.05; [x.sup.2] =19.02 and 20.03, 1 df, P < 0.001, respectively). The conclusion we draw from the two samples is that 8 of 13 helminth species were persistent and two species were stable, but the community as a whole was not stable in that prevalence of infection for an individual species (with the exceptions noted above, D. bufonis and G. quieta) was highly variable between the two samples (Table 1). The results reported here are not dissimilar from those of Goldberg and Bursey (2001a) in that for the component helminth community of Pseudacris regilla (= Hyla regilla), six helminth species were found (two digenean species, one species of cestode, and three species of nematode) of which only one nematode species was found to be persistent, but not stable.

The helminths found in this study as well as those in the Goldberg and Bursey (2001a) study are generalists in that they infect several host species (Table 2; see also Goldberg and Bursey, 2002). Presence of these helminths in Rana boylii is, no doubt, a result of patchy distribution of a particular helminth species (Table 3). Thus, it is possible that a particular host is unimportant to the helminth community; infection in a particular host species may fluctuate from year to year as seen here; but the helminth population may maintain an overall stable presence in the helminth supercommunity. Obviously, examination of sympatric anuran hosts for these helminths will be necessary before the question of stability can be properly addressed.

Acknowledgments.--We thank Sarah Goldsberry, Sean Kark and Tenzing Doleck for assistance with dissections. Rana boylii were collected under authority of Scientific Collecting Permit 801190-05 issued by the State of California, Department of Fish and Game to JBB.

LITERATURE CITED

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BARTON, D. P. 1997. Why are amphibian helminth communities depauperate? Mem Mus. Vict., 56:581-586.

BUSH, A. O., K. D. LAFFERTY, J. M. LOTZ AND A. W. SHOSTAK. 1997. Parasitology meets ecology on its own terms: Margolis et al. revisited. J. Parasitol., 83:575-583.

CHANDLER, A. C. 1919. On a species of Hedruris occurring commonly in the western newt, Notophthalmus torosus. J. Parasitol., 5:116-122.

CORT, W. W. 1919. A new distome from Rana aurora. Univ. Calif. Pub. Zool., 19:283-298.

GOLDBERG, S. R. AND C. R. BURSEY. 2001a. Persistence of the Nematode, Oswaldocruzia pipiens (Molineidae), in the Pacific treefrog, Hyla regilla (Hylidae), from California. Bull. Southern Calif. Acad. Sci., 100:44-50.

-- AND --. 2001b. Helminths of the California treefrog, Hyla cadaverina (Hylidae) from Southern California. Bull. Southern Calif. Acad. Sci., 100:117-122.

-- AND --. 2002. Helminths of the bullfrog, Rana catesbeiana (Ranidae), in California with revisions to the California anuran helminth list. Bull. Southern Calif. Acad. Sci., 101:118-130.

-- AND S. HERNANDEZ. 1999. Helminths of the western toad, Bufo boreas (Bufonidae) from southern California. Bull. Southern Calif. Acad. Sci., 98:39-44.

--, N. NIETO AND J. BETTASO. 2004. Rana aurora aurora (Northern red-legged frog). Endoparasites. Herpetol. Rev., 35:161-162.

-- AND R. TAWIL. 1993. Gastrointestinal helminths of the western bush lizard, Urosaurus graciosus graciosus (Phrynosomatidae). Bull. Southern Calif. Acad. Sci., 92:43-51.

GROSSMAN, T. AND H. SANDNER. 1953. Helmintofauna plazow Bialowieskiego Parku Narodowego. Acta Parasitol. Polonica, 1:345-352.

INGLES, L. G. 1936. Worm parasites of California Amphibia. Trans. Amer. Micro. Soc., 55:75-92.

-- AND C. I. LANGSTON. 1933. A new species of bladder fluke from California frogs. Trans. Amer. Micro. Soc., 52:243-246.

KOLLER, R. L. AND A. J. GAUDIN. 1977. An analysis of helminth infections in Bufo boreas (Amphibia: Bufonidae) and Hyla regilla (Amphibia; Hylidae) in southern California. Southwest Nat., 21:503-509.

KUC, I. AND T. SULGOSTOWSKA. 1988. Helminth fauna of Rana ridibuna Pallas, 1771 from Goclawski Canal in Warszawa (Poland). Acta Parasitol. Polonica, 33:101-105.

LEES, E. 1962. The incidence of helminth parasites in a particular frog population. Parasitology, 52:95-102.

LEHMANN, D. L. 1954. Some helminths of West Coast urodeles. J. Parasitol., 40:231.

--. 1956. Some helminths of Oregon urodeles. J. Parasitol., 42:25.

--. 1960. Some parasites of Central California amphibians. J. Parasitol., 46:10.

--. 1965. Intestinal parasites of northwestern amphibians. Yearbook Amer. Phil. Soc., 1965:284-285.

MAGURRAN, A. E. 2004. Measuring Biological Diversity. Blackwell Publishing, Malden, Massachusetts. MARKOV, G. S. AND M. L. ROGOZA. 1949. [Parasitic fauna of male and female grass frogs.] C. R. Acad. Sci. U.R.S.S., 65:317-420.

--AND --. 1953. [Seasonal and microzonal differences in the parasitic fauna of grass frogs.] C. R. Acad. Sci. U.R.S.S., 91:169-172.

MCCAULEY J. AND I. PRATT. 1961. A new genus Deropegus with a redescription of D. aspina (Ingles, 1936) nov. comb. Trans. Amer. Micro. Soc., 80:373-377.

MEFFE, G. K. AND W. L. MINCKLEY. 1987. Persistence and stability offish and invertebrate assemblages in a repeatedly disturbed Sonoran Desert stream Am. Midl. Nat., 117:177-191.

MORGAN, B. B. 1941. A summary of the Physalopterinae (Nematoda) of North America. Proc. Helminthol. Soc. Wash., 8:28-30.

N1CKOL, B. B. 1985. Epizootiology, p. 307-346. In: D. W. T. Crompton and B. B. Nickol (eds.). Biology of the Acanthocephala. Cambridge University Press, Cambridge, United Kingdom.

PRUDHOE, S. AND R. A. BRAY. 1982. Platyhelminth parasites of the Amphibia. British Museum (Natural History) and Oxford University Press, Oxford, United Kingdom.

STEBBINS, R. C. 2003. A field guide to western reptiles and amphibians. 3rd Edn. Houghton Mifflin Company, Boston, Massachusetts.

WALKER, M. E. 1965. A survey of the helminth parasites of Rana boylei from Humboldt, California. Master's thesis, Humboldt State College, Arcata, California. 33 p.

CHARLES R. BURSEY, (1) Department of Biology, Pennsylvania State University, Shenango Campus, Sharon 16146; and STEPHEN R. GOLDBERG, Department of Biology, Whittier College, Whittier, California 90608 and JAMIE B. BETTASO, U.S. Fish & Wildlife Service, Arcata FWO, Arcata, California 95521. Submitted 4 September 2008; accepted 15 June 2009.

(1) Corresponding author: e-mail: cxb13@psu.edu
TABLE 1.--Prevalence and mean intensity of helminth species in
Rana boylii, Humboldt County, California (1964-1965; 2004-2007)

                              1964-1965 collection (Walker, 1965)

                                                    Mean intensity
                              n       Prevalence       (range)
Cestoda
  Distoichometra bufonis        32    7%   11/150   3.0       ?

Digeneana
  Deropegus aspina               7    2%   3/150    2.3    (1-3)
  Glypthelmins quieta           16    6%   9/150    1.8    (1-5)
  Gorgoderina multilobata       82   11%   17/150   7.4   (1-50)
  Haematoloechus kernensis     121   10%   15/150   8.1   (1-33)
  Megalodiscus
    microphagus                 16    5%   8/150    2.0    (1-5)
  Echinostome
    metacercariae             1000   39%   59/150   --       --

Nematoda
  Cosmocercoides variabilis     13    6%   9/150    1.4    (1-5)
  Hedruri.s sp.
    (unidentified adults)       10    1%   1/150     10      --
  Rhabdias ranae               255   47%   70/150   3.6   (1-16)
  Physalopteridae (third
    stage larvae)                2    1%   1/150      2      --

Acanthocephala
  Centrorhynchid
    cystacanths                 31    3%   4/150    7.8   (1-27)
  Oligacarrathorhynchid
    cystacanth                   0   --       --    --       --

                                      2004-2007 collection

                                                   Mean intensity
                              n     Prevalence       (range)
Cestoda
  Distoichometra bufonis        4    2%   2/100    2.0    (1-3)

Digeneana
  Deropegus aspina              0   --       --    --       --
  Glypthelmins quieta          35   10%   10/100   3.5    (1-7)
  Gorgoderina multilobata       4    3%   3/100    1.3    (1-2)
  Haematoloechus kernensis    228   32%   32/100   7.1   (1-35)
  Megalodiscus
    microphagus                 2    1%   1/100      2      --
  Echinostome
    metacercariae              35    1%   1/100     35      --

Nematoda
  Cosmocercoides variabilis     1    1%   1/100      1      --
  Hedruri.s sp.
    (unidentified adults)       0   --       --    --       --
  Rhabdias ranae               47   19%   19/100   2.5    (1-8)
  Physalopteridae (third
    stage larvae)               0   --       --    --       --

Acanthocephala
  Centrorhynchid
    cystacanths                       0      --    --       --
  Oligacarrathorhynchid
    cystacanth                  1    1%   1/100    --       --

TABLE 2.--Californian hosts of common anuran helminths collected
during this study

Helminth                  Host                    Reference

Distoichometra    Bufo boreal             Koller and Gaudin, 1977
  bufonis                                 Goldberg et al., 1999
                  Hyla cadavenna          Goldberg and Bursey, 2001b
                  Hyla regilla            Goldberg and Bursey, 2001a
Glypthelmins      Rana aurora             Cort, 1919
  quieta                                  Ingles, 1936
                  Rana boylii             Ingles, 1936
                                          Lehmann, 1960
Gorgoderina       Rana aurora             Ingles and Langston, 1933
  multilobata                             Ingles, 1936
                  Rana boylii             Ingles and Langston, 1933
                                          Ingles, 1936
                  Rana pretiosa           Ingles, 1936
Haematoloechus    Bufo boxeas             Goldberg et al., 1999
  kernensis       Rana aurora             Ingles, 1936
Megalodiscus      Bufo boxeas             Ingles, 1936
  microphagus     Rana aurora             Goldberg et al., 2004
Cosmocercoides    Aneides favipunctatus   Lehmann, 1960
  variabilis      Aneides lugubdris       Lehmann, 1960
                  Bu/b boxeas             Ingles, 1936
                                          Koller and Gaudin, 1977
                                          Goldberg et al., 1999
                  Hyla regilla            Koller and Gaudin, 1977
                  Rana aurora             Ingles, 1936
                  Rana cateseiana         Ingles, 1936
Rhabdias ranae    Hyla cadaverina         Goldberg and Bursey, 2001b
                  Hyla regilla            Goldberg and Bursey, 2001a
                  Rana catesbeiana        Lehmann, 1965

TABLE 3.--Helminth distribution by location

Collecting site (Fig. 1):      1     2     3 *  4     5      6    7 *
       Helmith                      Data arrangement 64-65; 04-07

Cestoda
  Distoichometra bufonis      -;x   x;-   -;   x;-   x;-    x;-   -;

Digeneana
  Deropqacs aspina            -;-   -;-   -;   x;-   -;-    x;-   -;
  Glyjpthelmins quieta        x;-   -;-   -;   -;x   -;-    x;x   -;
  Gorgodezna multilobata      -;-   -;-   x;   -;-   -;-    -;-   x;
  Haemaloloechus kerraensis   -;-   -;-   -;   -;-   -;x    x;-   -;
  Megalodisrus mirrophagus    -;-   -;-   x;   -;-                x;
  Echinostome
    metacercariac             -;-   -;-   -;   x;-   -;-    x;-   x;

Nematoda
  Cosmocercoides variabilis   -;-   -;-   -;   -;-   x;-    x;-   x;
  Hedruris sp. (unidentified
    adults)                   -;-   -;-   -;   -;-   -;-    -;-   -;
  Rhabdias ranae              x;-   x;x   -;   x;x   x;-    x;x   x;
  Physalopteridae (third
    stage larvae)             -;-   -;-   -;   -;-   -;-    -;-   -;

Acanthocephala
  Centrorhynchid
    cystacanths               -;-   -;-   -;   -;-   -;-    -;-   x;
  Oligacanathorhynchid
    cystacanth                -;-   -;-   -;   -;x   -;-    -;-   -;

Collecting site (Fig. 1):     8     9 *   10    11   12   13   14
     Helmith                                x = present; - = absent

Cestoda
  Distoichometra bufonis      x;-   x;    x;x   -;-  -;-  x;-  x;-

Digeneana
  Deropqacs aspina            -;-   -;    -;-   -;-  -;-  -;-  -;-
  Glyjpthelmins quieta        -;-   -;    -;x   -;-  -;-  x;x  x;-
  Gorgodezna multilobata      -;-   x;    -;-   x;x  x;-  x;x  x;-
  Haemaloloechus kerraensis   -;-   -;    -;x   -;x  x;x  x;x  x;x
  Megalodisrus mirrophagus    x;-   -;    -;-   -;-  -;-  -;x  -;-
  Echinostome
    metacercariac             x;-   x;    x;x   x;-  x;-  x;-  x;-

Nematoda
  Cosmocercoides variabilis   -;x   x;    -;-   -;-  -;-  x;-  -;-
  Hedruris sp. (unidentified
    adults)                   -;-   -;    -;-   x;-  -;-  -;-  -;-
  Rhabdias ranae              x;-   x;    x;x   x;x  x;-  x;-  x;-
  Physalopteridae (third
    stage larvae)             -;-   -;    -;-   -;-  x;-  -;-  -;-

Acanthocephala
  Centrorhynchid
    cystacanths               -;-   -;    x;-   -;-  -;-  -;-  -;-
  Oligacanathorhynchid
    cystacanth                -;-   -;    -;-   -;-  -;-  -;-  -;-

Collecting site (Fig. 1):      15 *
     Helmith                x = present;
                            - = absent

Cestoda
  Distoichometra bufonis       x;

Digeneana
  Deropqacs aspina             -;
  Glyjpthelmins quieta         -;
  Gorgodezna multilobata       x;
  Haemaloloechus kerraensis    x;
  Megalodisrus mirrophagus     -;
  Echinostome
    metacercariac              x;

Nematoda
  Cosmocercoides variabilis    x;
  Hedruris sp. (unidentified
    adults)                    -;
  Rhabdias ranae               x;
  Physalopteridae (third
    stage larvae)              -;

Acanthocephala
  Centrorhynchid
    cystacanths                -;
  Oligacanathorhynchid
    cystacanth                 -;
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Title Annotation:Notes and Discussion
Author:Bursey, Charles R.; Goldberg, Stephen R.; Bettaso, Jamie B.
Publication:The American Midland Naturalist
Article Type:Report
Geographic Code:1USA
Date:Apr 1, 2010
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