INTRODUCTION
The ability of a parasite to persist within a host population is largely dependent on its transmission potential or basic reproductive ratio (R0). The R0 of directly transmitted parasites with free-living stages is frequently limited by environmental conditions that negatively affect development and survival rates (Hudson et al. Reference Hudson, Cattadori, Boag and Dobson2006). One family of parasitic nematodes, the Trichostrongylidae, has evolved a strategy that may increase transmission potential by inhibiting larval development once ingested by the host, thus limiting exposure of free-living stages to adverse conditions and concentrating egg production during periods of suitable conditions. Larval inhibition is characterized by a non-reversible cessation of growth at a precise point in the parasite's life cycle and postponing development to the adult stage, often by several months (Armour and Duncan, Reference Armour and Duncan1987; Eysker, Reference Eysker1993; Sommerville and Davey, Reference Sommerville and Davey2002). Generally, only a portion of the larval population will enter into inhibition while the remaining individuals develop immediately into adults (Borgsteede and Eysker, Reference Borgsteede and Eysker1987) and the propensity for inhibition is highly variable both within and between species (Eysker, Reference Eysker1993). Although the exact mechanisms of inhibition are not well understood, the time of year, environmental conditions experienced by the free-living stages, the age and immune status of the host, and behavioural characteristics of the host may all influence whether and what proportion of larvae enter inhibition (Eysker, Reference Eysker1993, Reference Eysker1997; Sommerville and Davey, Reference Sommerville and Davey2002).
Larval inhibition allows parasites to persist in oscillating environments and is more prevalent in areas where there are distinct seasons or extreme environmental conditions (Chiejina et al. Reference Chiejina, Fakae and Eze1988; Giangaspero et al. Reference Giangaspero, Bahhady, Orita and Gruner1992; Almeria et al. Reference Almeria, Llorente and Uriarte1996). Temporal and spatial overlap of hosts and parasites is necessary for directly transmitted parasites and, in some systems, larval inhibition synchronizes the presence of infective stages with the presence of susceptible hosts (Cattadori et al. Reference Cattadori, Boag, Bjornstad, Cornell and Hudson2005). Larval inhibition increases the flexibility of a parasite's life cycle and allows for alternate transmission strategies. Wildlife generally live in a matrix of environments, many of which are not suitable for parasite development, survival, and/or transmission. By synchronizing the infective stages of the parasite with the host in both time and space, larval inhibition can maintain parasites in host populations when transmission is not favoured across all seasons or the entire range of the host. Despite its potential importance, few studies have described inhibited development in wildlife host-parasite systems (Shaw, Reference Shaw1988; Belem et al. Reference Belem, Couvillon, Siefker and Griffin1993; Delahay and Moss, Reference Delahay and Moss1996).
Ostertagia gruehneri is a parasitic nematode in the family Trichostrongylidae and has a direct life cycle. It is the most common gastrointestinal parasite of caribou and reindeer (Rangifer tarandus ssp.) and can cause decreased food intake, weight loss, and reduced pregnancy rates (Arneberg et al. Reference Arneberg, Folstad and Karter1996; Arneberg and Folstad, Reference Arneberg and Folstad1999; Stien et al. Reference Stien, Irvine, Ropstad, Halvorsen, Langvatn and Albon2002). The life cycle and pre-patent period of O. gruehneri have not previously been determined; however, based on the conservativeness of the trichostrongylid life cycle they are presumed to be similar to related species parasitic in domestic animals. Adult O. gruehneri are found in the abomasum of infected hosts. Eggs are shed in the lumen of the gastrointestinal tract and passed to the external environment in the feces of the host. Previous studies have indicated a cessation of egg production throughout the winter months (Irvine et al. Reference Irvine, Stien, Halvorsen, Langvatn and Albon2000). Once in the environment, L1 hatch from the eggs and undergo development to the infected L3. Third-stage larvae are passively ingested by hosts during grazing. Larvae then migrate into the abomasal mucosa and develop to L4, prior to development to the adult stage. Similar to other trichostrongylids, O. gruehneri L4 may undergo larval inhibition while in the mucosa and delay the completion of the life cycle. The development and survival rates for the free-living stages of trichostrongylids are dependent on temperature (Stromberg, Reference Stromberg1997; O'Connor et al. Reference O'Connor, Walkden-Brown and Kahn2006), therefore, larval inhibition is likely to be prominent in systems with highly seasonal climatic conditions (Eysker, Reference Eysker1993; Sommerville and Davey, Reference Sommerville and Davey2002). Previous research has focused on the effects of adult O. gruehneri on the host whereas the transmission patterns in free-ranging Rangifer are not well understood.
To investigate larval inhibition in O. gruehneri we experimentally infected captive reindeer. We hypothesized that the propensity for larvae to inhibit would be affected by the date of infection, the age and infection history of the host, and environmental conditions experienced by larvae prior to entering the host (i.e. storage of larvae at different temperatures). Based on previous larval inhibition studies for related trichostrongylids in domestic animals, we expected that: (1) larvae would be more likely to inhibit in late summer than early summer because larval inhibition occurs during the winter in the northern hemisphere (Chiejina et al. Reference Chiejina, Fakae and Eze1988; Eysker, Reference Eysker1993; Almeria et al. Reference Almeria, Llorente and Uriarte1996); (2) larvae would be less likely to inhibit in naïve hosts compared to those with previous exposure to gastrointestinal nematode infections because of differences in the immune response to infection (Miller, Reference Miller1984); and (3) larvae exposed to cold conditions prior to infection would be more likely to inhibit because of environmental cues received by the L3 (Chiejina et al. Reference Chiejina, Fakae and Eze1988; Eysker, Reference Eysker1993; Almeria et al. Reference Almeria, Llorente and Uriarte1996).
MATERIALS AND METHODS
All captive animals used in this study were housed at the Wildlife Research Station (WRS), University of Calgary, Calgary, Alberta. Reindeer were housed on a newly fenced pasture that was not grazed by livestock for at least 5 years but was grazed by small numbers of periurban cervids (white-tailed deer and moose) prior to fencing. The experimental herd was initiated in 2006 with 2 reindeer from a herd south of Calgary. Four calves from a farm in Stettler, Alberta were added to the herd in 2008, followed by 7 more adult reindeer from the farm south of Calgary. All reindeer were quarantined and intensively treated with anthelmintics upon arrival at WRS. Repeated fecal samples were analysed using the Wisconsin double centrifugation technique (Egwang and Slocombe, Reference Egwang and Slocombe1982; Hoar et al. Reference Hoar, Oakley, Farnell and Kutz2009) and animals were not released to pasture until consecutive samples were negative for trichostrongylid eggs. A muskox from the University of Saskatoon was housed on an adjacent pasture at WRS and was also quarantined and treated with anthelmintics before release on to pasture. The animals were then kept on pasture and supplemented with commercial zoo ruminant pellets and locally produced hay.
Fecal samples containing O. gruehneri eggs were obtained from wild migratory tundra caribou or from previously infected animals housed at WRS. Ostertagia gruehneri is the predominant trichostrongylid species recovered from migratory tundra herds used as the initial source of parasites for all infected reindeer. Teladorsagia boreoarcticus is the only other species found in these herds with morphologically similar eggs and it occurs at very low intensities (Kutz et al. Reference Kutz, Ducrocq, Verocai, Hoar, Colwell, Beckmen, Polley, Elkin and Hoberg2012). Strongyle eggs morphologically consistent with O. gruehneri were isolated from the fecal samples by thoroughly mixing pellets with tap water to obtain an homogenous slurry and washing through a 75 μm sieve. The filtrate was centrifuged at 264 g for 10 min, the supernatant decanted, and the remaining pellet thoroughly mixed with a saturated salt solution before centrifuging again at 264 g for 10 min (technique modified from Hubert and Kerboeuf, Reference Hubert and Kerboeuf1984). The supernatant was then washed through a FlukeFinder© (Soda Springs, Idaho, USA). Recovered eggs were washed into Petri dishes (maximum 2000 eggs per dish) to develop and 1 ml of larval food (Hubert and Kerboeuf, Reference Hubert and Kerboeuf1984) was added once the majority of eggs had hatched.
2007–2008 infections
Between July 2007 and November 2008 4 reindeer and a muskox, all with previous exposure to trichostrongylid infections, were treated with anthelmintics and then experimentally infected with O. gruehneri. The purpose of these infections was to develop a reliable and local monoculture of O. gruehneri eggs for further experimental studies, not to study larval inhibition. For initial infections, larvae were grown from eggs collected from the Bathurst caribou herd in Northwest Territories and Nunavut, Canada and were cultured in Petri dishes in the laboratory at room temperature. Two adult female reindeer were infected once on 31 July and again on 3 August 2007 (eggs isolated within 2–3 weeks of infection) with 3500 F0 O. gruehneri L3 each time. These reindeer were used as the source of eggs for the infection study in 2009. An adult male muskox was infected on 4 January 2008 with 7000 F0 L3 from the original batch that had been refrigerated since the August 2007 infections. Two yearling male reindeer (born in spring 2008) were infected on 20 November 2008 (eggs isolated on 27 October) with 850 and 1700 F1 L3 grown from eggs collected from the muskox feces. Weekly fecal samples were collected from all 5 animals starting 1 week post-infection and analysed using the Wisconsin double centrifugation technique (Egwang and Slocombe, Reference Egwang and Slocombe1982; Hoar et al. Reference Hoar, Oakley, Farnell and Kutz2009).
2009 infection study
Twelve reindeer (identified by ear tags) were infected in June and July of 2009 with a mix of F1 and F2 L3 from the originally infected female reindeer. The reindeer infected for this study included 5 adult females, 2 adult males, 1 yearling male, and 4 calves of the year (Table 1). Adult and yearling reindeer were treated subcutaneously with 200 μg/kg Ivomec® (Merial, Australia) on 12 May 2009 and dosed orally with 15 mg/kg 4Farmers Fenbendazole® (4Farmers, Australia) for 3 days starting on either 26 or 27 May. Calves were treated with 10 mg/kg 4Farmers Fenbendazole® orally for 3 days starting on 26 or 27 May. Reindeer infected on 16 July were additionally treated subcutaneously with 200 μg/kg Dectomax® (Pfizer, New York, USA) on 4 June. All reindeer were kept on a parasite-free pasture for the duration of the study and individual fecal samples were collected weekly and analysed using the Wisconsin double centrifugation technique (Egwang and Slocombe, Reference Egwang and Slocombe1982; Hoar et al. Reference Hoar, Oakley, Farnell and Kutz2009) to ensure absence of trichostrongylid eggs. For the purposes of pasture management, 1 of the calves infected on 17 June was housed on a contaminated pasture because its mother was already infected with O. gruehneri (see 2007–2008 infections). Sample sizes per treatment were limited by the availability of animals. Likewise, serial necropsies were not used in this project because of the limited number of animals available.
Summary of the 2009 reindeer infection study including, sex and age of host, larval treatment prior to infection, dates of infection and patency, and maximum epg from March to April 2010
Fecal samples from previously infected reindeer were collected during the first and second week of May as the source of parasites for the June infections and the first week of June for the July infections. Following isolation, O. gruehneri eggs were placed in an incubator at 20°C under a 24-h light regime to develop L3. Once larvae developed to L3, half of the larvae were kept at 20 °C and 24-h light and half were kept at 5°C and no light for a period of 4 weeks. Larvae stored at 5°C were gradually warmed to 20°C over a period of 3 days.
The reindeer were equally divided into 2 groups (Table 1). Half of the reindeer were infected on 17 June 2009 (prior to the summer solstice) and the other half was infected on 16 July 2009 (after the solstice). The solstice was chosen as a seasonal marker to delineate early and late summer based on regimes of increasing and decreasing photoperiod to which the reindeer are exposed. One adult female and 1 male in each group were infected with the larvae stored under cold conditions at 5°C; all other reindeer were infected with larvae stored at a constant 20°C.
Each reindeer received a single dose of approximately 1200 L3. Reindeer were manually restrained during the infection process. Larvae were administered into the back of the mouth of the reindeer using a 60 ml dosing syringe containing the larvae in 30 ml of water. The syringe was rinsed 3 times with 30 ml of water, which was administered orally to the reindeer.
Fecal samples were collected weekly from all animals starting 1 week post-infection. Fecal collections were reduced to every 2 weeks from October 2009 to 17 March 2010 because egg production ceased over the winter. Fecal collections were stopped at the beginning of calving (14 April 2010) to reduce handling stress on the animals.
Larval species identification
Trichostrongylid eggs were isolated from the feces of infected animals and larvae were cultured. Species identification was confirmed by PCR amplification and genetic sequencing. Larvae from all animals infected during the 2007–2008 infections were collected and sent to the University of Saskatchewan, Saskatoon, Saskatchewan for identification (Sim et al. Reference Sim, Hoar, Kutz and Chilton2010).
PCR amplification for the purpose of identifying larvae for the 2009 infection study was completed at the University of Calgary. Eight larvae from each reindeer infected in 2007 were individually lysed and the second internal transcribed spacer region (ITS-2) was sequenced from both sides to identify the species and to ensure validity of this technique for identification of O. gruehneri. Eight larvae from each reindeer infected in 2009 (88 larvae plus 8 internal negatives) were identified as follows. Nematodes were lysed and prepared for PCR analysis as described by Eberhardt et al. (Reference Eberhardt, Mayer and Streit2007) with the following modifications. Individual larvae were each transferred into 4 μl of lysis buffer (50 mM KCl, 10 mM Tris–HCl, pH 8·3, 2·5 mM MgCl2, 0·45% (v/v) Nonidet p-40, 0·45% (v/v) Tween-20, 0·01% gelatin and 120 mg/ml proteinase K), frozen at −80°C for 10 min, and incubated at 60°C for 60 min, 65°C for 60 min, followed by a 15 min incubation at 95°C to inactivate the proteinase K. Six μl of water were added and 2 μl of this lysate were used as a template for PCR amplification. The ITS-2 sequence was amplified by PCR using the primers NC1 (5′-ACGTCTGGTTC AGGGTTGTT-3′) and NC2 (5′-TTAGTTTCTT TTCCTCCGCT-3′) (Sim et al. Reference Sim, Hoar, Kutz and Chilton2010). The PCR reaction volume was 25 μl, containing 1×PCR buffer, 0·5 units Taq DNA polymerase, 200 μM dNTPs, 0·5 μM of each primer and 2 μl (0·2 worm equivalent) of DNA lysate. The program used for PCR amplification was: 94°C/4 min, [94°C/30 s, 56°C/30 s, 72 °C/45 s] 35 cycles, 72°C/5 min. The resulting products were single fragments of expected lengths (ca. 328 bp) and sent to Eurofins MWG Operon (Huntsville, Alabama) for sequencing with primer NC1. The chromatograms were analysed and compared using the Lasergene software (DNASTAR).
RESULTS
2007–2008 infections
The 2 female reindeer infected with O. gruehneri in the summer of 2007 first shed eggs on 24 March 2008, almost 8 months post-infection. They continued to shed eggs until October 2008 and then ceased egg production until the last week of March 2009 (Fig. 1A). The 2 male reindeer infected on 20 November 2008 did not shed eggs until 7 April and 20 May 2009. Consistent egg shedding began on 20 May 2009 for both yearling reindeer, 6 months post-infection. Egg production continued until October 2009 and ceased over the winter until the last week of March 2010 (Fig. 1B).
Ostertagia gruehneri epg from fecal samples collected regularly from reindeer infected in 2007 and 2008. Samples were collected from January 2008 to April 2010. (A) Epg from 2 adult female reindeer infected 31 July 2007 and (B) epg from 2 yearling male reindeer infected 20 November 2008. Pregnancy status of the female reindeer differed with the year: open symbols, calved (1) in June 2009; closed symbols, calved (1) in May 2010.
2009 infection study
Reindeer did not shed eggs until between 17 March and 31 March 2010, i.e. 8 to 9 months post-infection (Table 1). One of the adult female reindeer infected on 17 June 2009 died in August 2009 from unrelated causes. At the time of death, no trichostrongylid eggs had been recovered from her feces and no nematodes were recovered from her abomasum (technique modified from Irvine et al. Reference Irvine, Stien, Halvorsen, Langvatn and Albon2000). There was extensive tissue damage that, together with the low infection dose, may have prevented recovery of larvae. Post-mortems were not carried out on any other animals.
Results of sequencing
All larvae that produced a PCR product (7–8 larvae per reindeer) were positively identified as O. gruehneri (Accession number AJ400716). Both ITS-2 variants (differing by the presence of A/G mixed base pairs at the position 108) described from reindeer by Dallas et al. (Reference Dallas, Irvine and Halvorsen2000a ,Reference Dallas, Irvine, Halvorsen and Albon b ) were detected in this study. All internal negative controls were negative.
DISCUSSION
Our results suggest 100% larval inhibition in reindeer exposed to larvae at different times of year and under different conditions. In total, 16 reindeer were experimentally infected with O. gruehneri from late spring to early winter; the age of the animals ranged from 2 months to 10 years and the larvae were cultured under different conditions. None of the reindeer shed eggs until the following spring, 6–9 months post-infection. We had expected a significantly higher propensity for larval inhibition in hosts infected after the summer solstice, hosts with previous exposure to trichostrongylid infections, and for larvae exposed to the cold treatment. We did not anticipate 100% inhibition under any scenario, let alone under all treatments.
Adult parasite intensities at different times post-infection were not evaluated in this study as this would have required euthanasia of the animals and the number of animals available for the study was limited. It is possible that larvae could have developed to the adult stage within the same year as infection and either did not produce eggs or produced eggs at a rate below the sensitivity of the Wisconsin double centrifugation technique used to quantify epg. Since no eggs were detected until the following spring, this system is functionally equivalent to 100% inhibition. Further studies involving larger sample sizes and serial necropsies are required to confirm obligate inhibition. However, our results suggest that larval inhibition is likely to be a major component of the transmission strategy in the O. gruehneri/migratory tundra caribou system in the Canadian Arctic.
The resumption of egg production of O. gruehneri was highly synchronized in the spring for all but 2 yearling reindeer infected in late November. In the yearling reindeer, consistent egg production did not begin until late May, 6 months post-infection, despite the fact that the other reindeer had begun shedding eggs by late March. Winter infection with O. gruehneri is highly unlikely in migratory populations, so the November infections did not reflect natural conditions. Nevertheless, the delay in the onset of egg production in these winter-infected reindeer suggests that there may be a minimum time required for larvae to remain inhibited, which roughly corresponds to the length of winter in the Arctic. The synchronized resumption of egg production further supports the importance of larval inhibition within this system.
Larval inhibition of O. gruehneri in reindeer in Finland has been reported (Hrabok et al. Reference Hrabok, Oksanen, Nieminen and Waller2006a , Reference Hrabok, Oksanen, Nieminen and Waller2007) but it was not obligate. In 2002–2004 the prevalence and intensity of O. gruehneri in winter-slaughtered (October to January) reindeer was determined for both adults and calves (Hrabok et al. Reference Hrabok, Oksanen, Nieminen and Waller2007). Adult O. gruehneri were recovered from all calves (n=53) but were heavily outnumbered by early L4 (EL4) (69–94% of total worm burden), suggesting a high propensity for larval inhibition. Further studies using parasite-free tracer calves on naturally infected pastures found that the proportion of EL4 increased significantly over time until a peak in mid-winter (Hrabok et al. Reference Hrabok, Oksanen, Nieminen and Waller2006a ). This peak was followed by a subsequent decline in EL4 numbers throughout late winter and early spring, corresponding to an increase in adult numbers. These results demonstrate that larval inhibition is a prominent feature of the O. gruehneri life cycle but is not obligate across populations.
Studies of O. gruehneri infections in other herds and locations suggest further differences in larval inhibition. On the high Arctic archipelago of Svalbard, Norway, adult nematodes are not common in reindeer calves of the year. Four calves collected in October 1979 had no adult O. gruehneri (Bye and Halvorsen, Reference Bye and Halvorsen1983). Subsequent studies in the mid-1990s recovered low numbers of adult nematodes from reindeer calves sampled in October (n=39, 44% prevalence, mean of 15 nematodes per calf) (Irvine et al. Reference Irvine, Stien, Halvorsen, Langvatn and Albon2000). In contrast, reindeer calves on the sub-Antarctic island of South Georgia have high fecal egg counts in their first summer, suggesting that many larvae develop into adults in the first year and that larval inhibition may be less important in this system (Leader-Williams, Reference Leader-Williams1980). The exact propensity for larval inhibition in the above studies could not be determined because abomasal larvae were not quantified in any of the studies and necropsies were not done in South Georgia.
Obligate inhibition has not been confirmed in any other trichostrongylid. Several studies report a high propensity of larval inhibition in Haemonchus contortus populations in the fall and at the northern extent of its range (Connan, Reference Connan1971; Waller and Thomas, Reference Waller and Thomas1975; Ogunsusi and Eysker, Reference Ogunsusi and Eysker1979; Waller et al. Reference Waller, Rudby-Martin, Ljungstrom and Rydzik2004). However, inhibition was not as prominent earlier in the summer and experimental studies failed to achieve rates of inhibition greater than 36% (Capitini et al. Reference Capitini, McClure and Herd1990).
While 100% inhibition may be an effective strategy for parasite populations in migratory caribou under highly seasonal and continental Arctic conditions, it may not be an effective strategy across all populations or geographical regions. Seasonal migration of tundra caribou in northern Canada may reduce transmission risk throughout much of the growing season by spatially separating the host from the infective stages. However, transmission risk likely increases substantially during periods of higher host densities and reduced movement (i.e. calving grounds). In addition, egg production of O. gruehneri is limited to the growing season (Fig. 1: Irvine et al. Reference Irvine, Stien, Halvorsen, Langvatn and Albon2000) and the few eggs shed outside of the growing season do not survive freezing (De Bruyn, Reference De Bruyn2010 and unpublished data). Larval inhibition in migratory caribou concentrates egg production during a time when eggs can survive, development to L3 is possible, and re-infection may occur prior to migration. Such a strategy may not be as important in regions where the period for larval development is extended and/or the hosts are more sedentary. For example, in much of Scandinavia and on South Georgia Island the climate is characterized by a strong maritime influence, resulting in longer summers and moderate winter temperatures. Additionally, these host populations do not migrate great distances from their summer ranges and exposure to infective larvae may be more consistent throughout the growing season. Further factors influencing the propensity for larval inhibition include the higher densities of semi-domesticated reindeer, anthelmintic treatment, and other husbandry practices. Both host ecology and geographically distinct climatic conditions influence the propensity for larval inhibition of O. gruehneri across populations. Levels of inhibition appear to be highest in migratory host populations inhabiting harsh environments (migratory tundra caribou); moderate in semi-migratory host populations in mild climates (reindeer in Finland); and minimal in relatively sedentary host populations inhabiting mild environments (reindeer on South Georgia).
Larval inhibition is not typically an all-or-nothing strategy, even when larvae are exposed to identical conditions in the external environment and in the host (Sommerville and Davey, Reference Sommerville and Davey2002). By producing offspring with a distribution of strategies, or bet hedging, parasites are better able to reproduce during favourable conditions and increase the survival rate of offspring under suboptimal conditions (Fenton and Hudson, Reference Fenton and Hudson2002), further increasing the flexibility of the parasite's life cycle. Plasticity of inhibition may increase the ability of parasites to adapt to wide-scale climate and other environmental changes. Many trichostrongylid nematodes undergo inhibition and the pattern and propensity is highly flexible and adaptive to local environmental conditions (reviewed by Sommerville and Davey, Reference Sommerville and Davey2002). Distinct ecotypes have been identified on the basis of larval inhibition for H. contortus, O. ostertagi, and Teladorsagia circumcincta; however, the propensity for inhibition can change within only a few generations when these ecotypes are moved to different regions (reviewed by Eysker, Reference Eysker1993).
The different propensities for larval inhibition in migratory tundra caribou in Canada compared to reindeer in Finland and South Georgia Island indicate that there are distinct ecotypes of O. gruehneri. Preliminary data from field collections of the Bathurst caribou herd in northern Canada demonstrate that, even in this system, a small proportion of the parasite population develops to adults by the fall in calves of the year. Small numbers of adult nematodes (mean intensity of 10 nematodes per calf) were recovered from 4 of the 16 calves (25%) sampled in the fall, whereas adult nematodes were recovered from 9 out of 10 calves (90%) sampled in the spring with intensity ranging from 10 to 510 nematodes per calf. These findings suggest that some larvae, however few, do not inhibit and this minimal amount of variation may allow O. gruehneri to adapt to changing climatic conditions, complete its life cycle in a single season, and produce more than 1 generation per year. Our study was done at temperate latitudes under a significantly warmer climate than the Arctic tundra and with F0-F2 generation O. gruehneri. Under such conditions, and over additional parasite generations, it is expected that the propensity for larval inhibition in this population of O. gruehneri would eventually decrease. Because of obligate inhibition in the migratory tundra caribou/O. gruehneri system may negatively impact the ability of this parasite to adapt to a changing environment and compete with invasive trichostrongylid species. Currently, the annual recruitment of O. gruehneri in migratory tundra caribou appears effectively limited to 1 generation of adults per year. In contrast, temperate species of Trichostrongylidae, many for which reindeer are suitable hosts (Hrabok et al. Reference Hrabok, Oksanen, Nieminen, Rydzik, Uggla and Waller2006b ), can produce multiple generations each year. Dobson and Roberts (Reference Dobson and Roberts1994) demonstrated that fecundity and transmission potential are reliable factors in dividing a parasite community into ‘core’ and ‘satellite’ species. If O. gruehneri retains its obligate inhibition under warming climatic conditions and cannot compensate for this longer generation time with increased reproductive and transmission success, then it may be outcompeted by invasive species.
Inhibited development is an integral part of the transmission strategy for many parasitic nematodes. Apparent obligate inhibition of a population of O. gruehneri in migratory tundra caribou underscores the importance of this phenomenon for the transmission dynamics in at least 1 wild host-parasite system. While larval inhibition has been reported in other Rangifer populations, it may have increased importance in the O. gruehneri/migratory tundra caribou system because of Arctic climatic conditions and the long-distance migrations that separate host and parasite in time and space. The occurrence of larval inhibition has long-term ecological and evolutionary consequences for both the host and the parasite and may become increasingly important as climate change alters interactions between hosts, parasites, and the environment.
ACKNOWLEDGEMENTS
We thank Patricia Kelly, Pat Curry, Jayninn Yue, Marianne Jorgenson, Dean Brown, Jesse Invik, Lynn Klassen, and Greg Muench for their assistance throughout this project. We thank Kathreen Ruckstuhl for her assistance in editing the manuscript.
FINANCIAL SUPPORT
This work was financially supported by Alberta Innovates (B.H., 200800734), NSERC (S.K., 312178–2007), and International Polar Year Canada.
