Voitto Haukisalmi

The impact of climatic factors and host density on the long-term population dynamics of vole helminths

SummaryThe seasonal and long-term population dynamics of helminths parasitizing voles suggested that density-dependent factors might be important in the population dynamics of common species, whereas density-independent factors predominate in the regulation of the rare species. To test this, we used single and multiple regression to analyse the effects of climatic factors and host density on populations of six species of vole helminths over 12 years. The data do support the idea of a difference between common and rare species of helminths, but they clearly do not support the above hypothesis. The common helminths Heligmosomum mixtum (Nematoda) and Catenotaenia sp. (Cestoda) responded to changes in temperature sum (>5° C days) and precipitation during summer. The combined effect of climatic factors and host density explained most of the variation in the long-term dynamics of these common species. By contrast, the long-term dynamics of the rare helminths Paranoplocephala kalelai (Cestoda), Mastophorus muris, Capillaria sp. and Syphacia petrusewiczi (Nematoda) were explained less well by weather and host density than those of the common ones. Furthermore, the common and rare helminths differed in some ways in their responses to climatic factors.

Systematic relationships of hymenolepidid cestodes of rodents and shrews inferred from sequences of 28S ribosomal RNA

Haukisalmi, V., Hardman, L. M., Foronda, P., Feliu, C., Laakkonen, J., Niemimaa, J., Lehtonen, J. T. & Henttonen, H. (2010). Systematic relationships of hymenolepidid cestodes of rodents and shrews inferred from sequences of 28S ribosomal RNA. —Zoologica Scripta, 39, 631–641.

Analysing interspecific associations in parasites: alternative methods and effects of sampling heterogeneity

Abstract The purpose of the present study was (1) to test the ability of six alternative methods to detect random and non-random patterns of overall association in artificial presence/absence data sets, and (2) to analyse overall associations and effects of sampling heterogeneity in four empirical presence/absence data sets of helminths of the common shrew Sorex araneus. In the null model, the expected distribution was created by means of a randomisation procedure. Application of methods on artificial data sets indicated a generally low probability of type I statistical error. All methods were more likely to detect positive non-randomness than negative non-randomness of comparable strength, which may partly explain the predominance of positive overall associations in empirical data sets. The analyses based on artificial data sets indicated slight differences between methods in their ability to detect non-randomness of known strength (type II error). However, some of the methods failed to detect strong overall association when the artificial assemblages consisted of roughly equal numbers of positive and negative pairwise interactions. The structure of the artificial data sets always disappeared when the expected distribution was constrained to account for “sampling heterogeneity”, i.e. varying prevalence of species among subsamples. The patterns of overall association in real helminth communities were variable, depending on the locality and association method used, but not usually on the simulation constraint used. Of the four empirical data sets analysed, one showed an unequivocal positive structure, in one the structure depended on the method used, and two data sets from the same locality were unequivocally unstructured (random). We discuss the applicability of various association measures, and the possible causes of positive overall associations in parasites.

Coexistence in Helminths of the Bank Vole Clethrionomys glareolus. II. Intestinal Distribution and Interspecific Interactions

1. We studied the intestinal distribution of helminths (cestodes and nematodes) in the bank vole Clethrionomys glareolus, and changes in distribution due to the presence and varying abundance of other species. The material was obtained from two localities in Finland: Pallasjarvi in western Lapland and Lammi in southern Finland. 2. The intestinal distribution of the common species Heligmosomum mixtum (Nematoda) was affected by the rare species Capillaria sp. (Nematoda) and Paranolocephala gracilis (Cestoda). The common species showed inconsistent negative interactions with other common species. 3. The data indicate that interactions between the intestinal helminths of the bank vole are most likely to occur between species with large intestinal overlap, but not necessarily feeding overlap

Variability of sex ratio, mating probability and egg production in an intestinal nematode in its fluctuating host population

In dioecious parasites, the chances of co-occurring with the opposite sex depend on the sex ratio, abundance and distribution pattern of parasites within the host population. Theory suggests that if the abundance and degree of aggregation are very low, mating probability may decrease so much that the parasite population is vulnerable to extinction. Our aim is to determine the factors affecting the mating probability and egg production in Heligmosomum mixtum (Heligmosomidae), an intestinal nematode of the bank vole, Clethrionomys glareolus, at Pallasjärvi, Finnish Lapland. We also search for factors responsible for the persistence of H. mixtum in its fluctuating host population. The results showed that during high parasite abundance practically all nematode females co-occurred with males, but during a phase of very low abundance only 15% of females had a chance to mate. Comparison of observed mating probabilities and those predicted by a theoretical model (May & Woolhouse, 1993) showed that deviation from the assumption of complete aggregation between males and females results in underestimation of the mating probability. Sex ratio and the degree of aggregation showed a minor effect on mating probability. The sex ratio (proportion of females) of H. mixtum, which was female-biased (0.58), showed a negative correlation with the mean intensity of infection in the monthly samples (decreasing female-bias at high mean intensity), but no significant relation to the intensity of infection (number of worms in a host individual). The long-term persistence of H. mixtum in its strongly varying host population seems to be due to the high transmission efficiency and long life-span of the parasite.

Biogeography of helminth parasitism in Lemmus Link (Arvicolinae), with the description of Paranoplocephala fellmani n. sp. (Cestoda: Anoplocephalidae) from the Norwegian lemming L. lemmus (Linnaeus).

We describe the gastrointestinal helminth fauna of true lemmings (Lemmus spp., Arvicolinae) based on published and original material throughout the Holarctic range of these hosts. According to the existing data, the helminth fauna of true lemmings consists of three widespread and/or locally common taxa: Hymenolepis horrida (sensu lato) (Hymenolepididae), Anoplocephaloides lemmi (Anoplocephalidae) and Heligmosomoides spp. (Heligmosomidae). Despite the taxonomic boundaries and ancient phylogenetic splits in the hosts, there are no major faunistic differences for parasites within western (Siberian) L. sibiricus and L. bungei, and eastern (North American) L. trimucronatus throughout their distribution range. In contrast, the Norwegian lemming L. lemmus, which is a Fennoscandian endemic and closely related to the western populations of L. sibiricus, has only a single host-specific helminth, the cestode Paranoplocephala fellmani n. sp. (Anoplocephalidae). We describe the new species and show that it differs consistently from related species by its long and slender cirrus-sac. However, there are also a number of other significant differences, e.g., P. fellmani n. sp. and Andrya primordialis in Tamiasciurus hudsonicus (Sciuridae) evidently have a unique (sub)type of uterine development among Andrya/Paranoplocephala spp. Because P. fellmani n. sp. was also found to occur in Alaska (host L. trimucronatus), this species seems to follow the same biogeographical pattern as the other specialist helminths of Lemmus. We suggest alternative explanations for the absence of three major helminth taxa in the Norwegian lemming in Fennoscandia.

PARASITISM BY HELMINTHS IN THE GREY-SIDED VOLE (CLETHRIONOMYS RUFOCANUS) IN NORTHERN FINLAND: INFLUENCE OF DENSITY, HABITAT AND SEX OF THE HOST

We have studied helminths from 532 grey-sided voles (Clethrionomys rufocanus) in two localities in northern Finland, representing different biogeographic zones, during 1978–1983. The helminth communities in the two study areas were similar, characterized by a small number of species (eight) compared to eastern Siberia and Japan, and by the dominance of a single anoplocephalid cestode Andrya kalelai. The prevalence of this helminth varied significantly among habitats, possibly because of differences in the distribution and abundance of the intermediate hosts, oribatid mites. Vole density did not explain the habitat differences in A. kalelai, nor did the prevalence of A. kalelai increase between 2 yr of sustained high density in the host population. A between-year increase in the prevalence of the larval cestode Taenia tenuicollis at Kilpisjärvi was probably due to a simultaneous increase in the abundance of its definitive hosts, mustelids. The prevalence of A. kalelai was always higher in males; no sexual differences were detected in the larval T. tenuicollis.

Molecular systematics and morphometrics of Anoplocephaloides dentata (Cestoda, Anoplocephalidae) and related species in voles and lemmings

This study presents extensive molecular phylogenetic and morphometric data for Anoplocephaloides dentata (Galli‐Valerio, 1905)‐like cestodes (Anoplocephalidae) and related species parasitizing arvicoline rodents (voles and lemmings) in the Holarctic region. The molecular phylogeny is based on nucleotide sequences of cytochrome oxidase I (mtDNA) and 28S ribosomal RNA. Anoplocephaloides dentata‐like cestodes included three main clades, two in western Eurasia and one in the Holarctic region (excluding western Eurasia). Three well‐supported sublineages were included in the southern European clade, one of which represents the true A. dentata from Chionomys nivalis and sympatric Microtus arvalis and Dinaromys bogdanovi. These clades generally had non‐overlapping distributions and showed a preference for certain host species. Multivariate analysis of morphometric data failed to discriminate unambiguously the various A. dentata‐like lineages recovered in the molecular phylogeny, although two to three of the (sub)lineages were morphologically divergent. The overall evidence suggests, however, that instead of a single host‐generalist species there are at least five more or less host‐specific species of A. dentata‐like cestodes. Colonization of new host lineages seems to have been the predominant mode of diversification, suggested by the considerable incongruence between host and parasite phylogenies at multiple taxonomic levels. Based on the results of the molecular survey, a redescription and neotype designation are provided for A. dentata.

Description and morphometric variability of Paranoplocephala serrata n. sp. (Cestoda: Anoplocephalidae) in collared lemmings (Dicrostonyx spp., Arvicolinae) from Arctic Siberia and North America.

We describe Paranoplocephala serrata n. sp. (Cestoda, Anoplocephalidae) from collared lemmings Dicrostonyx torquatus and D.xa0groenlandicus (Arvicolinae, Rodentia) in Arctic Siberia and North America. The new species was recorded from the Yamal Peninsula (type-locality), Yana Delta, Kolyma Delta, Wrangel Island, Alaska and Victoria Island/Kent Peninsula (Northwest Territories). P.xa0serrata n. sp. is characterised by a long, ribbon-like strobila, distinctly serrated segments, a small scolex, unilateral or infrequently alternating genital pores and testes confined to the antiporal part of the segment. It differs from the related species (Andrya bairdi, Parandrya feodorovi and Paranoplocephala maseri) by several morphological features, including the distribution of testes (several testes antiporal to ventral longitudinal osmoregulatory canal), structure of the cirrus-sac and vagina, and large eggs (0.053–0.068xa0mm in the type-material). The material of P.xa0serrata n. sp. from North America differs from the Siberian material by the shorter cirrus-sac, smaller dimensions of the female reproductive organs, larger seminal receptacle and larger eggs. However, the statistical differences in the dimensions of reproductive organs mainly reflect the larger size of mature segments in Siberian specimens compared with North American specimens. The main diagnostic features, i.e. the size and form of scolex and suckers, number and distribution of testes, position of female glands, vagina/cirrus-sac ratio and morphology of reproductive organs, do not differ markedly between the Palaearctic and Nearctic specimens. According to the structure of the early-stage uterus, A.xa0bairdi Schad, 1954 belongs to the genus Paranoplocephala. Parandrya Gulyaev & Chechulin, 1996 is probably a synonym of Paranoplocephala. A redescription is provided for Paranoplocephala bairdi n. comb.

Distribution patterns and microhabitat segregation in gastrointestinal helminths of Sorex shrews

We studied the distribution patterns and microhabitat use in gastrointestinal helminths of the shrews Sorex araneus and S. caecutiens in Finland. The distribution of species prevalences was bimodal, and in S. araneus the abundance (mean intensity) was positively associated with commonness (prevalence), as assumed by the core-satellite species hypothesis (Hanski 1982). However, the positive correlation between prevalence and intensity was observed only when the effects of helminth body size and taxonomic group (cestodes vs nematodes) on intensity were controlled for. The nematodes of the genus Longistriata occurred predictably as core species, whereas the identity of the core cestodes was more variable between host species and regions. Helminth body size and taxonomic group were not related to the degree of aggregation in shrew populations, but helminth body size seemed to explain the differences in the distribution patterns of helminths between shrews and voles. The core species did not show more segregation in microhabitat use than randomly selected species. In fact, the two core nematodes showed largely overlapping intestinal distributions. We conclude that linear intestinal space is not a key resource for shrew nematodes, but it may be for shrew cestodes.