1

Local climate aridity inuences the distribution of thelastomatoid nematodes of the Australian giant burrowing cockroach
A. R. JEX 1*, M. A. SCHNEIDER 2, H. A. ROSE 3 and T. H. CRIBB 1
1 2

School of Molecular and Microbial Sciences, The University of Queensland, St Lucia, Queensland, Australia School of Integrative Biology, The University of Queensland, St Lucia, Queensland, Australia 3 School of Land, Water and Crop Sciences, The University of Sydney, Camperdown, New South Wales, Australia
(Received 23 January 2007; revised 25 February 2007; accepted 25 February 2007)
SUMMARY

In this study, we examined the eects of local climate aridity on the richness and composition of the thelastomatoid (Nematoda : Oxyurida) guild parasitizing the Australian giant burrowing cockroach, Macropanesthia rhinoceros (Blattodea : Geoscapheinae). In total, 9 thelastomatoid species parasitized this cockroach in north-eastern Australia (Queensland). Local observed richness ranged from 3 species (in Cooktown, Magnetic Island, Maiden Springs and Whitsunday Island) to 7 species (in Rochford Scrub). The lowest richness occurred in both relatively wet and dry climates, and the highest richness was in moderate climates. Three species, Cordonicola gibsoni, Leidynemella fusiformis and Travassosinema jaidenae, were found at all 13 collection sites. One species, Geoscaphenema megaovum, was found exclusively in dry to moderate climates. The remaining species, Blattophila sphaerolaima, Coronostoma australiae, Desmicola ornata, Hammerschmidtiella hochi and Jaidenema rhinoceratum, were found in moderate climates only. We hypothesize that the egg is the stage in the thelastomatoid life-cycle most vulnerable to the eects of adverse climate and that the geographical distribution for each species is, in part, bound by environments that are too dry, resulting in egg desiccation, and by environments that are too wet, resulting in decreased oxygen uptake across the egg-shell and in osmotic lysing. Key words: Nematoda, Thelastomatidae, guild, distribution, species-richness, climate.

INTRODUCTION

For as long as parasite systems have been studied, parasitologists have sought to explain variation in the assemblage of species parasitizing dierent individuals within and among host species. Variation in parasitic guild structure among host species is surely inuenced by a range of factors, such as host specicity and host ecology. Within a species, however, discerning patterns beyond random variation among individuals has been as fascinating as it has been perplexing. Overarching patterns governing faunal variation are rare and universal laws dicult to determine (Gue gan et al. 2005). Perhaps the most consistent patterns, when patterns exist, governing a host individuals parasite fauna have been linked to the distance decay hypothesis (Poulin and Morand, 1999 ; Morand and Gue gan, 2000 ; Poulin, 2003) and the latitudinal gradient hypothesis (Rohde, 1993 ; Poulin, 1998 b). The distance decay hypothesis, in relation to parasite systems, predicts that the similarity in the make-up of the parasite fauna of conspecic host populations will decrease with an increase in the geographical distance between them

* Corresponding author : Department of Veterinary Science, The University of Melbourne, Werribee, Victoria, Australia. E-mail : ajex@unimelb.edu.au
Parasitology, Page 1 of 8. f 2007 Cambridge University Press doi:10.1017/S0031182007002727 Printed in the United Kingdom

(Poulin and Morand, 1999). The latitudinal gradient hypothesis is directed more specically at overall species richness of the assemblage parasitizing a given host and is based on the observation, both in parasite and non-parasite systems, that species richness is higher in ecosystems closer to the equator than in those closer to the poles (Hawkins et al. 2003). However, these patterns do not necessarily apply to all systems (Kennedy et al. 1991 ; Brown, 1995 ; Rosenzweig, 1995) and, although they have been used successfully in some systems occurring over large geographical areas, the utility of distance decay and latitudinal gradients across smaller geographical ranges or, in the case of the latitudinal gradient hypothesis, longitudinally broad rather than latitudinally long ranges, is perhaps somewhat limited. A major obstacle in dening non-random patterns in parasite systems is the remarkable array of parasitic behaviours and life-cycles. Perhaps a more targeted approach of searching for non-random patterns in more specic systems in which there are fewer confounding obstacles, such as intermediate hosts, will provide a simpler system for investigations leading to additional discernment of useful patterns in the variation of parasite assemblages. For any parasite, one of the most dangerous periods of its life-cycle is the time during which it must exist outside of its host. Multi-host life-cycles,

A. R. Jex and others

such as those found in many platyhelminths and protists, represent a common adaptation which helps overcome this danger by allowing life-cycle stages to shelter in intermediate hosts. Many parasites, such as the oxyurid nematodes ( pinworms ), do not have intermediate hosts, and thus have direct modes of transmission. In pinworm systems, females produce eggs which are shed in the hosts faeces and must survive in the external environment long enough to be ingested by a new host (Adamson, 1984). Numerous studies have suggested that oxyurid eggs are sensitive to environmental conditions, particularly moisture (Geller, 1944 ; Anya, 1966 ; Adamson, 1989 ; Grice and Prociv, 1993). Geller (1944) showed that eggs of the human pinworm, Enterobius vermicularis, required humidity levels of y100 % to develop. Similar requirements were observed by Skrjabin et al. (1960) for the horse pinworm, Oxyuris equi. Grice and Prociv (1993) demonstrated that eggs of the rat pinworm, Syphacia obvelata, collapsed if exposed to conditions that were too dry and ruptured or opened prematurely in excessive moisture. However, these responses are not universal ; levels of susceptibility vary among species (McSorley, 2003), suggesting that some species are more or less suited than others to the external environment across a range of climates. From these ndings, it can be predicted that the pinworm fauna of widely distributed hosts varies in response to dierent local climatic conditions. There is presently little information available to test this hypothesis. Macropanesthia rhinoceros (Blattodea : Geoscapheinae) has an unusually wide geographical distribution relative to the other burrowing cockroaches (Roth, 1977 ; Walker et al. 1994). Jex et al. (2006) reported the thelastomatoid fauna of this species from a number of localities across Queensland, Australia. Here, we extend this previous study and examine in detail the relationship between local climate and the observed and estimated richness and overall composition of the thelastomatoid guilds parasitizing this host species. We test for patterns in thelastomatoid distribution both at the individual species and the guild levels. Additionally, we examine ecological and physiological characteristics which may explain these distribution patterns.

immediately anterior to the origin of the Malpighian tubules. The excised hindgut was dissected, and all nematodes found were extracted and preserved in fresh 70 % ethanol. Preserved nematodes were placed in a (v/v) solution of 100 % glycerol in 100 % ethanol to a nal concentration of 5 % glycerol and 95 % ethanol. These were left uncovered for 48 h to allow the ethanol to evaporate, thereby leaving the specimens in 100 % glycerol. This was done to limit any damage to the worms caused by rapid transfer to pure glycerol. The nematodes were mounted in glycerol using the wax-ring method described by Hunt (2002). All nematodes were identied using a morphological character database compiled from the literature as described by Jex et al. (2005).

Climate comparisons Relative aridity was calculated using Budykos Aridity Index (h) (Budyko, 1974). We used the equation as dened by Arora (2002): h=P/PE, where P is annual precipitation and PE is annual potential evapotranspiration. We employed areal potential evapotranspiration, which is dened as the evapotranspiration that would take place, if there is unlimited water supply, from an area large enough such that the eects of any upwind boundary transitions are negligible, and local variations are integrated to an areal average . This was done to limit the impact of micro-climate variation at individual localities. All climate and potential evapotranspiration data were provided by the Bureau of Meteorology, Victoria, Australia (webclim@bom.gov.au).

Estimation of species richness and non-linear regression analysis Species richness estimates were calculated using the software package EstimateS v.7.0 (available at http://viceroy.eeb.uconn.edu/estimates). Although this software package provides many species richness estimators, only Bootstrap (Smith and van Belle, 1984), Chao2 (Chao, 1987) and Jack1 (Burnham and Overton, 1978, 1979 ; Heltshe and Forrester, 1983 ; Smith and van Belle, 1984) were used, as recommended by Walther and Morand (1998) and Poulin (1998 a). Richness estimation values were calculated over 1000 runs, using a randomized dataset for each run. Trend analysis was performed using the software package Statistica Kernel release 5.1 (available at www.statsoft.com). Trend lines were tted using the least squares method.

MATERIALS AND METHODS

Data collection Specimens of Macropanesthia rhinoceros (n=114) were collected from 13 localities across Queensland, Australia, over y20 years. All cockroach specimens were preserved in 70 % ethanol, where they remained until recent dissection. A transverse incision was made along the posterior end of the abdomen. The hindgut was then teased out and severed at the point

Egg morphometrics The eggs were measured (at 400r magnication) using an ocular micrometre employing an Olympus BH-2 light compound microscope. Egg length

Climate aridity eects on thelastomatoid nematode distribution

3 4 5 11 7 10 2 12 9 8 13

Fig. 1. Map of the sampling sites for Macropanesthia rhinoceros in Queensland, Australia. Alpha (1), Boonderoo (2), Coen (3), Cooktown (4), Dimbulah (5), Duaringa (6), Gumlu (7), Granite Gorge (8), Magnetic Island (9), Maiden Springs (10), Mt Garnet (11), Rochford Scrub (12), Whitsunday Island (13).

species at Cooktown, Magnetic Island, Maiden Springs and Whitsunday Islands, to 8, 12 and 10 at Rochford Scrub for the estimators Bootstrap, Chao2 and Jack1, respectively. All 9 species were never found at a single locality. Localities were ranked by Budykos aridity index (Table 2). The aridity index ranged from 0.29 for Maiden Springs (driest locality) to 0.94 for Cooktown (wettest locality). Trend analysis using the least squares tting method suggested a strong curvilinear relationship between species richness and climate aridity (Fig. 2). Only the comparison between observed richness and aridity is shown. However, comparisons between estimated richness and aridity revealed a similar trend, regardless of the estimation method used. Overall fecundity, as measured by number of eggs in utero, ranged from a mean of 90 per female for Hammerschmidtiella hochi to just 1 per female for Geoscaphenema megaovum (Table 3). Egg volume ranged from 0.19 pl (L. fusiformis) to 2.23 pl (G. megaovum). Egg surface area ranged from 6 nm2 (T. jaidenae) to 24 nm2 (G. megaovum). Egg shell thickness ranged from 0.95 mm (B. sphaerolaima) to 4.37 mm (G. megaovum). We compared the climate range, as indicated by Budykos aridity index, for each thelastomatoid species with these 3 parameters (Fig. 3) ; the ndings of which are discussed in detail in the following section on egg morphology.

and width were measured from the longest and widest portion of each egg. Egg volume was estimated by calculating the volume of an ellipsoid of the same dimensions (=4/3p * polar radius * equatorial radius2 ; where polar radius is one half of the total egg length, and equatorial radius is one half of the total egg width). Egg surface area was estimated as the surface area of an ellipsoid of the same dimensions (=2p * equatorial radius2 * (1+(polar radius/equatorial radius) * arcsin(e)/e), where e= eccentricity and is calculated as e=(1x(polar radius2/equatorial radius2))1/2).
RESULTS

DISCUSSION

Species richness For all localities examined, except Rochford Scrub and Mount Garnet, estimated richness was within 2 species of observed richness, suggesting that a high proportion of the thelastomatoid species infecting M. rhinoceros at these localities have been found. Rochford Scrub and Mount Garnet had observed species richness levels of 6 and 7, respectively (Bootstrap=8 and 7, Chao2=11 and 12, and Jack1=10 and 10, respectively). These localities were highly species rich and all included several species found in only a single cockroach individual ; C. australiae, G. megaovum and J. rhinoceratum at Rochford Scrub and L. fusiformis, C. australiae, G. megaovum and D. ornata at Mt. Garnet. It is rare species (particularly singletons or doubletons) which relate to estimated richness levels that are greater than observed species richness. This eect is exacerbated for smaller sample sizes. Walther and Morand (1998) indicated that the Chao2 and Jack1 estimation methods performed best and should be used in studies of parasite species richness . The present data appear to agree with this observation. In most localities for which estimated richness diered from the observed richness, the Bootstrap based richness estimates were consistently lower than those

We examined 114 adult M. rhinoceros from 13 localities in Queensland, Australia (Fig. 1). These localities represent the known distribution for M. rhinoceros (see Roth, 1977 and Walker et al. 1994). We identied 9 species of Thelastomatoidea. The prevalences of infection for the species at each site ranged from 9 to 100 %, with the lower gure representing a single infection (Table 1). Abundance and intensity values were not considered here. Observed species richness ranged from 3 species, at Cooktown, Magnetic Island, Maiden Springs and Whitsunday Islands, to 7 species at Rochford Scrub (Table 2). Estimated species richness ranged from 3

A. R. Jex and others

Table 1. Prevalence of infection for each thelastomatoid species parasitizing Macropanesthia rhinoceros in Queensland, Australia
(Localities ranked by decreasing aridity. Cordonicola gibsoni (Cg), Leidynemella fusiformis (Lf), Travassosinema jaidenae (Tj), Geoscaphenema megaovum (Gm), Coronostoma australiae (Ca), Jaidenema rhinoceratum (Jr), Desmicola ornata (Do), Blattophila sphaerolaima (Bs) and Hammerschmidtiella hochi (Hh).) Locality Maiden Springs Boonderoo Alpha Dimbulah Coen Rochford Scrub Mt. Garnet Duaringa Granite Gorge Gumlu Magnetic Island Whitsunday Island Cooktown n 7 9 8 10 6 11 10 6 10 6 10 10 11 Cg 86 56 100 100 67 100 90 100 90 83 100 100 73 Lf 43 33 75 80 100 73 10 33 30 83 30 60 64 Tj 57 11 63 50 33 64 20 100 90 50 100 70 55 Gm 11 50 10 83 9 10 Ca 17 9 10 17 10 Jr 10 9 17 Do 27 10 Bs 10 Hh 17

Table 2. Observed and estimated thelastomatoid species richness, climate variables, Budykos aridity index by locality for Macropanesthia rhinoceros in Queensland, Australia
(Precipitation (Prec), average areal potential evapotranspiration (AAPE), Budykos aridity (BA), observed species richness (Obs), bootstrap based richness estimation (Boot), Chao2 based richness estimation (Chao2) and Jack1 based richness estimation (Jack1).) Prec (mm) 475 491 498 723 900 825 900 820 860 1058 1169 1776 1809 AAPE (mm) 1635 1617 1549 1694 1906 1715 1758 1500 1500 1835 1800 1988 1919

Locality Maiden Springs Boonderoo Alpha Dimbulah Coen Rochford Mount Garnet Duaringa Granite Gorge Gumlu Magnetic Island Whitsunday Island Cooktown

BA 0.29 0.31 0.32 0.43 0.47 0.48 0.51 0.55 0.57 0.58 0.65 0.89 0.94

Obs 3 4 4 5 6 7 6 4 5 4 3 3 3

Boot 3 5 4 6 7 8 7 4 6 4 3 3 3

Chao2 3 6 4 7 7 12 11 4 7 5 3 3 3

Jack1 3 6 4 7 8 10 10 4 7 5 3 3 3

predicted by Chao2 or Jack1, with the exception of the dataset for the locality Duaringa, where Bootstrap was slightly higher than Chao2 (4.42 vs. 4.33). In addition, in most of these localities, the dierences between Chao2- and Jack1-based richness estimates were less than the dierences between the values calculated via either of these estimators as well as those calculated using the Bootstrap method. The exceptions to this apparent trend were Rochford Scrub and Mount Garnet, the 2 localities with the highest richness levels or, perhaps more importantly, the greatest number of singletons. It may be that in systems with a high number of singletons, the Chao2 method overestimates richness levels. We take the view here that there may be

species that we have not detected in some localities and, therefore, all subsequent analyses of the data were repeated for observed richness and the 3 richness estimators. In either case, Coen, Mt. Garnet and Rochford Scrub are clearly the most species-rich of the sites surveyed ; any uncertainty about their true richness is unlikely to have a negative impact/eect on the subsequent analysis. Distribution of thelastomatoids by local climate Macropanesthia rhinoceros is found in some of the driest to some of the wettest areas of Australia. There appears to be a clear relationship between thelastomatoid guild richness and local climate

Climate aridity eects on thelastomatoid nematode distribution

75 Observed species richness 65 55 45 35
MS RS

Co MG

Di

GG

BoAI

Du Gu

MI

WI CK

25 02

03

04

05

06

07

08

09

10

Budyko's aridity

Fig. 2. Non-linear regression analysis of observed species richness versus relative aridity for Macropanesthia rhinoceros by locality in Queensland, Australia. Locality (2) ; Alpha (Al), Boonderoo (Bo), Coen (Co), Cooktown (Ck), Dimbulah (Di), Duaringa (Du), Granite Gorge (GG), Gumlu (Gu), Magnetic Island (MI), Maiden Springs (MS), Mount Garnet (MG), Rochford Scrub (RS), Whitsunday Island (WI). (Note : Although not included here, analysis using estimated richness, regardless of the estimation method used, produces a similar trend.)

aridity. Wet localities, such as Cooktown (observed species : 3), Whitsunday Island (3) and Magnetic Island (3) and dry localities, such as Alpha (4), Boonderoo (4) and Maiden Springs (3) have lower species richnesses than mid-range localities, such as Coen (6), Mt. Garnet (6) and Rochford Scrub (7). Importantly, the relationships between guild richness and climate aridity correspond to real species not just numerical variations in richness statistics. Three species of thelastomatoid, C. gibsoni, L. fusiformis and T. jaidenae, were found at all localities. Geoscaphenema megaovum was found in all localities with a dry climate, except Maiden Springs, and was not found in the 6 wettest sites. The other 5 species were all found only in mid-range aridity sites ; none was found in any of the 3 wettest or the 3 driest sites. Egg morphology The survival of any parasite species depends upon its ability to successfully infect new hosts. Successful infection is certainly improved by maximizing the number of host encounters. In parasites with direct life-cycles, the number of encounters can be increased by increasing egg longevity, maximizing the time over which an encounter may occur or, by increasing fecundity, allowing greater frequency of host encounters by weight of numbers. Clearly, climate may have an eect on egg longevity when eggs are shed into the environment. Conversely, it seems unlikely that climate directly impacts fecundity. Certainly, any impact that climate may have on fecundity will be indirect and exceedingly dicult to predict.

We propose that egg longevity varies from site to site, largely due to the climatic conditions encountered. Based on previous studies (Geller, 1944 ; Anya, 1966 ; Adamson, 1989 ; Grice and Prociv, 1993), we predict that in dry climates desiccation is the greatest threat to egg longevity and that in wet climates it is threatened by osmotic lysing and egg suocation in water-logged soils. We hypothesize that, under these circumstances, the most likely indicators of egg longevity in response to environmental stress will be egg surface-area to volume ratios and egg-shell thickness. Presumably, eggs with lower surface area to volume ratios (i.e. large eggs) will be less susceptible to desiccation. Also, we predict that eggs with thick shells will be less susceptible to desiccation and, hence, more successful in dry environments. A comparison of the egg characteristics from the 9 species examined suggests that there is some correlation with the climate-related distributions of these species. Three species, Cordonicola gibsoni, Leidynemella fusiformis and Travassosinema jaidenae, were reported from all localities surveyed and had by far the broadest climate ranges. An examination of the egg characteristics of these 3 species relative to all others showed that they were in the mid-range in most respects. The mean numbers of eggs in utero for these species were 8 (L. fusiformis), 11 (C. gibsoni) and 13 (T. jaidenae). Two species, G. megaovum (1 egg) and J. rhinoceratum (5), had fewer eggs in utero, and the other 4 species, D. ornata (15), C. australiae (24), B. sphaerolaima (40) and H. hochi (90) had more. Egg surface area to volume ratios were 14.2 nm2/pl for C. gibsoni, 16.7 nm2/pl for T. jaidenae and 55.1 nm2/pl for L. fusiformis. With the exception of L. fusiformis, these had also mid-range levels. Three species, G. megaovum (10.8 nm2/pl), Jaidenema rhinoceratum (11.8 nm2/pl) and C. australiae (12.5 nm2/pl), had lower surface area to volume ratios and 3 other species, Desmicola ornata (17.4 nm2/pl), B. sphaerolaima (33.4 nm2/pl) and H. hochi (37.2 nm2/pl) had higher ratios. All 3 common species had an approximately mid-range shell thickness ; 1.56 mm, 1.78 mm and 2.62 mm thick for C. gibsoni, L. fusiformis and T. jaidenae eggs, respectively. Two species, H. hochi (1.25 mm) and B. sphaerolaima (0.95 mm), had thinner shells, 1 species, J. rhinoceratum (1.64 mm) had similar shell thickness and 3 species, D. ornata (2.76 mm), C. australiae (3.10 mm) and G. megaovum (4.37 mm), had thicker shells. Overall, the eggs of the 3 dominant species are unremarkable in comparison with the other 6 species examined here. We suspect that the unremarkable morphology and morphometrics of the eggs for these dominant species is precisely what permits them to be so widespread. By producing eggs of moderate size (with the exception of L. fusiformis), shell thickness and number, the 3 dominant species

A. R. Jex and others

Table 3. Mean number of eggs in utero and egg morphometrics for each thelastomatoid species parasitizing Macropanesthia rhinoceros
Eggs in utero 11 8 13 1 24 5 15 40 90 Egg length ( mm) 82 71 57 115 100 84 83 91 67 Egg width ( mm) 50 25 38 68 59 55 46 36 29 Shell thickness ( mm) 1.56 1.78 2.62 4.37 3.1 1.64 2.76 0.95 1.25 Surface area ( nm2) 12 10 6 24 18 13 13 16 9 Volume ( pl) 0.86 0.19 0.34 2.23 1.46 1.06 0.74 0.49 0.24 Surface area: Volume 14 200 55 100 16 700 10 800 12 500 11 800 17 400 33 400 37 200

Parasite species Cordonicola gibsoni Leidynemella fusiformis Travassosinema jaidenae Geoscaphenema megaovum Coronostoma australiae Jaidenema rhinoceratum Desmicola ornata Blattophila sphaerolaima Hammerschmidtiella hochi

A 90 80 70 60 50 40 30 20 10 0 0.2 0.4 0.6 0.8 1 Budyko's aridity B Egg surface area to volume 54500 49500 44500 39500 34500 29500 24500 19500 14500 9500 0.2 C. gibsoni L. fusiformis T. jaidenae G. megaovum C. australiae J. rhinocerata D. ornata B. sphaerolaima H. hochi

C. gibsoni L. fusiformis T. jaidenae G. megaovum C. australiae J. rhinocerata D. ornata B. sphaerolaima H. hochi 0.4 0.6 0.8 1

Budyko's aridity C 4.5 Egg shell thickness 4.0 3.5 3.0 2.5 2.0 1.5 1.0 0.5 0.2 0.4 0.6 0.8 1 Budyko's aridity

C. gibsoni L. fusiformis T. jaidenae G. megaovum C. australiae J. rhinocerata D. ornata B. sphaerolaima H. hochi

Fig. 3. Comparison of climate range with egg characteristics for each Thelastomatoidea species parasitizing Macropanesthia rhinoceros across Queensland, Australia ; eggs in utero. (A) Egg surface area to volume ratio ; (B) egg-shell thickness (C).

may represent a generalist compromise that allows them to survive in a broad range of climatic conditions. Eggs of Geoscaphenema megaovum are the largest and have the thickest shells of any of the thelastomatoids reported here. In addition, this species never had more than 1 egg in utero. This species was found in all of the dry localities, except Maiden Springs. Conversely, it was not found in any of the wet localities. In fact, although we found a number of cockroach species harbouring this parasite across large geographical areas within Australia, we have yet to nd it in a wet locality (Jex et al. 2007). These distributional data and the combination of large egg size and thick shell for this species suggest that G. megaovum is an arid climate specialist. Coronostoma australiae and J. rhinoceratum also have large, thick-shelled eggs and broad distributions across most arid localities and no wet localities for M. rhinoceros. Jaidenema rhinoceratum may also be an arid climate specialist as it has also been found in many cockroach species in Australia but not in wet localities (Jex et al. 2007). However, although not found in any wet climates in this study, C. australiae has been reported previously from another cockroach species, Panesthia tryoni tryoni, from a particularly wet locality, Lamington National Park, Queensland (Jex et al. 2005). Therefore, we cannot consider this species to be an arid specialist, although it is apparently more successful in arid regions. None of the species reported here could be considered a wet climate specialist based on the present data. Overall, we showed that the thelastomatoid fauna of M. rhinoceros, across its entire range, is heterogeneous. The variation in the fauna appears to be correlated to local climate aridity and some of this variation appears to be ascribable to egg morphology. However, inconsistencies between egg surface area to volume ratio, thickness of egg-shell and width of climate range presented by the 3 dominant thelastomatoids, C. gibsoni, L. fusiformis and T. jaidenae,

Eggs in utero

Climate aridity eects on thelastomatoid nematode distribution

7 Chao, A. (1987). Estimating the population size for capture-recapture data with unequal catchability. Biometrics 43, 783791. Geller, E. R. (1944). [Epidemiology of enterobiasis] in Russian. Meditsinskaia Parasitologia i Parazitarnye Bolezni 5, 1623. Grice, R. L. and Prociv, P. (1993). In vitro embryonation of Syphacia obvelata eggs. International Journal for Parasitology 23, 257260. gan, J.-F., Morand, S. and Poulin, R. (2005). Are Gue there general laws in parasite community ecology ? The emergence of spatial parasitology and epidemiology. In Parasitism and Ecosystems (ed. Thomas, F., Renaud, F. and Gue gan, J.-F.), pp. 2242. Oxford University Press, Oxford. Hawkins, B. A., Field, R., Cornell, H. V., Currie, D. J., gan, J.-F., Kaufman, D. M., Kerr, J. T., Gue Mittlebach, G. C., Oberdor, T., OBrien, E. M., Porter, E. E. and Turner, J. R. G. (2003). Energy, water, and broad-scale geographic patterns of species richness. Ecology 84, 31053117. Heltshe, J. and Forrester, N. E. (1983). Estimating species richness using the jackknife procedure. Biometrics 39, 111. Hunt, D. J. (2002). The African Rhigonematoidea (Nematoda : Rhigonematida). 2. Six new species of Rhigonema Cobb, 1989 (Rhigonematidae). Nematology 4, 803827. Jex, A. R., Schneider, M. A., Rose, H. A. and Cribb, T. H. (2005). The Thelastomatoidea (Nematoda : Oxyurida) of two sympatric Panesthiinae (Blattodea) from south-eastern Queensland, Australia : taxonomy, species richness and host specicity. Nematology 7, 543575. Jex, A. R., Schneider, M. A., Rose, H. A. and Cribb, T. H. (2006). Thelastomatoidea (Nematoda : Oxyurida) of the Australian giant burrowing cockroach, Macropanesthia rhinoceros (Blattodea : Geoscapheinae). Nematology 8, 347357. Jex, A. R., Schneider, M. A., Rose, H. A. and Cribb, T. H. (2007). A comprehensive analysis of the biogeography of the thelastomatoid pinworms from Australian burrowing cockroaches (Blaberidae : Geoscapheinae, Panesthiinae) : no evidence of coevolution. Parasitology (this issue). Kennedy, C. R., Hartvigsen, R. A. and Halvorsen, O. (1991). The importance of sh stocking in the dissemination of parasites throughout a group of reservoirs. Journal of Fish Biology 38, 541552. McSorley, R. (2003). Adaptations of nematodes to environmental stress. Florida Entomologist 86, 138142. gan, J.-F. (2000). Distribution and Morand, S. and Gue abundance of parasite nematodes : ecological specialisation, phylogenetic constraint or simply epidemiology ? Oikos 88, 563573. Poulin, R. (1998 a). Comparison of three estimators of species richness in parasite component communities. Journal of Parasitology 84, 485490. Poulin, R. (1998 b). Evolutionary Ecology of Parasites : from Individuals to Communities, Chapman and Hall, London, New York. Poulin, R. (2003). The decay of similarity with geographical distance in parasite communities of vertebrate hosts. Journal of Biogeography 30, 16091615.

demonstrate that egg morphology is not the only important factor. Local climate may be a signicant component in shaping non-random variation in parasite fauna of a host species existing across a broad climate range. This, of course, depends largely on the extent to which stages of the parasites life-cycle are exposed to the external environment and undoubtedly will be more pronounced in, if not conned to, terrestrial systems and those parasites utilizing a simple lifecycle with a directly infective stage that is shed into the external environment. Clearly, variation in the parasite fauna among individuals is the result of highly complex interactions and, undoubtedly, much of the variation, particularly at a local level, will be the result of chance. The extent to which the observations presented here occur in other systems or can be developed into any predictive model remains to be tested. Despite potential limitations, such patterns may oer useful insights into additional parasite systems.
This study was supported by the Queen Elizabeth II Centennial Scholarship (Government of British Columbia, Canada), the University of Queensland International Postgraduate Research Scholarship, the International Postgraduate Research Scholarship (Government of Australia), and the Australian Biological Research Study. The authors thank Leslie Rohland, the Australian Bureau of Meteorology, for the provision of precipitation and evapotranspiration data and Dr David Marcogliese and Professor Ian Beveridge for comments, advice and suggestions.

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