Helminth communities in small mammals in southeastern new south wales

HELMINTH

COMMUNITIES IN SMALL MAMMALS NEW SOUTH WALES

IN SOUTHEASTERN

D.M. SPRATT Division of Wildlife & Rangelands P.O. Box 84, Lyneham, A.C.T.

Research, CSIRO, 2602 Australia.

INTRODUCTION Our research group is concerned with derivation of the ecological principles governing the dynamics of animal communities in fluctuating environments. Community patterns may be influenced by chance events which generate temporal or spatial changes in the environment, by competition, by mutualism, by predators or by parasites, and in general by the complicated interplay of all of these factors. Each may affect selective fitness of individual species, which in turn affects community patterns. Holmes (1979) and Price (1980) have stressed that the structure of the host community (species diversity, population size) has the potential to affect the population dynamics of individual species or complexes of parasites. On the other hand, parasites may have significant effects on the structure of the host community by affecting interspecific competition, predator-prey relationships and by effecting selective mortality of heavily infected hosts. The following is a preliminary and general overview of the fluctuations of populations of small marsupial and eutherian mammals, and of populations of their helminth parasites, in eucalypt forest and heathland habitats at Nadgee and Timbillica State Forests south of Eden, New South Wales from September 1977 to September 1985. In the study region there is a high probability of “wildfire” occurring every 3-7 years (Walker, 1981). Fire is an important component of the Australian ecosystem. The pervasive nature of adaptations to a fire regime (burning frequency, fire intensity and seasonal occurrence) in plant species and the requirement for a particular seral stage for survival of some indigenous marsupial and eutherian mammal species highlight the long history of exposure of Australian flora and fauna to fire. Populations of most vertebrate species survive low to moderate intensity fires (Christensen, Reacher & Hoare, 1981) but extensive, high intensity wildfires, such as the 1972 fire in the Nadgee Nature Reserve, may have a more severe effect on vertebrate populations. Although vertebrates may survive fires there is generally a population decline during the weeks following wildfire, attributed to shortage of food and to increased predation (Newsome, McIlroy & Catling, 1975). Recolonisation and repopulation of burnt areas is dependent upon distance from unburnt refuge areas and upon the pattern of recovery of the plant community, the latter influenced markedly by rainfall and season. Consequently, a change occurs, frequently in the composition and invariably in the abundance of animal species following wildfire (Newsome et al., 1975; Christensen, Reched & Hoare, 1981; Catling, Newsome & Dudzinski, 1982). On 18 November, 1980, with temperatures exceeding 42”C, humidity falling below 15% and northwesterly winds gusting to 70 km/h wildfire burnt an area of 47,000 ha in Nadgee and Timbillica State Forests and in the adjoining Nadgee Nature Reserve. MATERIALS AND METHODS Animals were collected using Elliott small mammal live-traps. Pre-fire trapping was conducted randomly and all animals trapped were examined. Post-fire trapping was conducted systematically on 6 grids selected on the basis of their productivity (high trapping success) and small mammal diversity pre-fire. Grids were trapped on two successive nights. All animals caught on the first night were marked and released to obtain data on host population sizes. All odd numbered animals (e.g. lst, 3rd, 5th etc.) of each species caught on the second night were collected for examination, to a maximum of 6 representatives per host species per 100 trap sites. Trapping was conducted at least 4 times annually at intervals of not more than 3 months. 197

D.M. Sprati

198

Post mortem examination of the tissues and organs of all animals was conducted under a stereomicroscope. Total counts of all helminth species were made, with the exception of species of Mursupostrongylus in Antechinus spp., Cercopithifilaria johnstoni in R. fuscipes and Capillaria gastrica in Rattus spp. Representative specimens of all helminth species collected are accessioned in the Helminth Collection of the Division of Wildlife & Rangelands Research, CSIRO. The prevalence of infection of individual parasite species in each host taxon was calculated, and the intensity of infection determined according to Margolis, Esch, Holmes, Kuris & Schad (1982). The diversity of the helminth communities in each host taxon pre- and post-wildfire was calculated using Simpson’s Index (Simpson, 1949) as employed by Holmes & Podesta (1968) and expressed as l/S (Leong & Holmes, 1981). The overall similarity of helminth communities in all of the host taxa pre- and post-wildfire was determined using Sorenson’s Index of Similarity (Greig-Smith, 1964).

1 12' ll-

lo-

9-

a-

21OI

-3

I

-2

I

-1

I

I

1

2

Time post-fire

1

1

3

4

5

(years)

Fig. 1. Trends, expressed as % trapping success, in populations of small marsupial and eutherian mammals pre- and post- wildfire in southeastern coastal New South Wales, 1977-1985.

RESULTS Five species of small marsupials and two species antechinus, Antechinus stuartii (lo-38 g); the dusky white-footed dunnart, Sminthopsis leucopus (9-28 (550-1320 g); the southern brown bandicoot, Isoodon (20-169 g) and the swamp rat, Rattus lutreolus (36-170 Mus musculus (6-33 g), were trapped post-fire. Trends in population abundance of small mammal

of native rodents were trapped pre-fire: the brown antechinus, Antechinus swainsonii (30-138 g); the g); the long-nosed bandicoot, Perameles nasuta obesulus (260-1570 g); the bush rat, Rattus fuscipes g). These species plus the introduced house mouse, taxa pre- and post-wildfire

are presented

in Fig. 1.

Helminth communities in mammals

199

These are expressed as percent trapping success, i.e. the number of different individuals of a species caught per trapping effort multiplied by 100. R. fuscipes decreased in abundance and R. lutreolus disappeared in the year following the fire. R. fuscipes increased in abundance during the second to fourth years post-fire, R. lutreolus during the third to fifth years post-fire. The bandicoots, P. nasuta and 1. obesulus were trapped in small numbers and the former was slow to recolonise post-fire. Abundance of the brown antechinus, A. stuartii, remained low for 2 years post-fire but increased markedly during the third to fifth years after the wildfire. The dusky antechinus, A. swainsonii, was slow to recolonise post-fire. The dunnart, S. leucopus was trapped once pre-fire but a population increase occurred post-fire. The house mouse, M. musculus was not trapped pre-fire but populations increased dramatically post-fire. A total of 1I trematode, 16 cestode, 60 nematode and 2 acanthocephalan species were found in the hosts examined. Overall, the helminth communities in A. stuartii and A. swainsonii were characterised by dicrocoeliid, diplostomid and brachylaimid trematodes, hymenolepid cestodes, and trichinelloid, rhabditoid, trichostrongyloid and metastrongyloid nematodes. The community in S. leucopus was characterised by diplostomid trematodes, a hymenolepid cestode and trichinelloid, trichostrongyloid and seuratoid nematodes. Overall, the helminth communities in P. nusuta and 1. obesulus were characterised by dilepidid and hymenolepid cestodes, and trichinelloid, trichostrongyloid, seuratoid and physalopteroid nematodes. The communities in R. fuscipes and R. lutreolus were characterised by diplostomid and brachylaimid trematodes, anoplocephalid and davaineid cestodes, and trichinelloid, rhabditoid, trichostrongyloid, heterakoid and physalopteroid nematodes. That in the introduced M. musculus was characterised by trichostrongyloid and oxyuroid nematodes. The helminth communities in all host taxa were dominated by nematodes. The intestinal helminth fauna of each host taxon was dominated (prevalence, intensity and diversity) by trichostrongyloid nematodes. Herpetostrongylid trichostrongyles predominated in the dasyurid marsupials, mackerrastrongylids in the peramelid marsupials and heligmosomatids in the rodents. Trematodes were not found in P. nasuta, R. lutrelous and M. musculus; adult acanthocephala were found only in A. swainsonii and larval acanthocephala only in A. stuartii and S. leucopus. Helminth species richness in each taxon pre- and post-wildfire, including the number of helminth species known from the 5 marsupial and 3 eutherian hosts over their geographic ranges in Australia (Mackerras, 1958; Spratt, Beveridge & Walter, in preparation) are presented in Table 1. Helminth species diversity was highest in A. swainsonii post- and pre-fire and lowest in S. leucopus pre-fire and in M. musculus, which occurred only post-fire (Table 1). Overall similarity between helminth communities was highest in the native rats, R. fuscipes and R. lutreolus post- and pre-fire, in the marsupial antechinuses, A. stuartii and A. swainsonii post- and pre-fire, in the dasyurid marsupials A. stuartii, A. swainsonii and S. leucopus post-fire and in the marsupial bandicoots, P. nasuta and I. obesulus post-fire (Table 2). Helminth communities in S. leucopus were completely dissimilar to those in I. obesulus and in R. lutreolus pre-fire; communities in the 3 rodent taxa were completely dissimilar to those in the bandicoots. TABLE 1. HELMINTH SPECIES RICHNESS EXPRESSEDAS NUMBER OF SPECIES AND HELMINTH SPECIES DIVERSITY EXPRESSED USING THE RECIPROCAL OF SIMPSON’S INDEX (l/S) IN SMALL MARSUPIAL AND EUTHERIAN MAMMALS PRE- AND POST-WILDLIFEIN SOUTHEASTERNCOASTAL NEW SOUTH WALES.

Species richness (no.)

Australia

Antechinus stuartii Antechinus swainsonii Sminthopsis leucopus Perameles nasuta Isoodon obesulus Rat&s fuscipes Rattus lutreolus MIASmusculus

Species diversity (l/S)

Coastal N.S.W.

Total*

Total

pre-

post-

41 36 20 35 28 55 28 22

32 28 16 19

24 24 2 17

28 22 16 9

29 20 12

22 14 -

23 19 12

11

9

* after Mackerras, 1958; Spratt, Beveridge & Walter, in preparation. t present pre-, absent post-; absent pre-, present post-.

6

appp+

pre-

post-

4 6 0

8 4 14

14.5 2.0

11.0

10.8

6

7 6

ppap:

10 5

-

1

2 2

-

10.4 8.0

6.5 5.8 -

14.7 7.7 9.0 6.0

5.6 5.2 3.0

D.M. Spratt

200 TABLE 2. OVERALL

SIMILARITIES(%)• FHELMINTHCOMMIJNITIESIN PRE-AND POST-WILDFIRE,EXPRESSEDUSING

A. Stuart. pre- post(preA. swainsonii

/pre-

nasuta

obesulus

54.6

(pre-

lutreolus

10.8

10.5 6.5

16.0 0

12.1

15.4

1

5.9 17.4

53.3

9.1

7.1

10.3

16.7

8.7

6.5

1

(pre-

13.3

15.7

0

15.4 0

10.5

10.5

0 8.7

6.5

61.1

i

(post-

M.

47.4 14.6

12.1

[post-

R.

7.7

19.5

1

[prefuscipes

R. lutreo. pre- post-

64.0 15.4

(post-

R.

R. fusci. pre- post-

54.2

(post-

1.

1. obesu. pre- post-

1

(post(preP.

P. nasuta pre- post-

MAMMALS

1

(post-

S.leucopus

A. s\ssain. S. leuco. pre- postpre- post-

SMALLMARSUPIALANDEUTHERIAN SORENSON’S INDEX.

(pre-

i (post-

12.8

11.4

14.6

0

10.0

11.8

0

66.7

-

-

-

14.3

0

0

28.6

32.3

DISCUSSION The small mammal fauna of Australian forests and heathlands is neither as abundant nor as diverse as its counterpart in North America. Changes in the abundance of small mammal species following the wildfire of November, 1980 were similar to those reported after the wildfire in Nadgee Nature Reserve in 1972 (Newsome et al., 1975; Christensen et al., 1981; Catling et al., 1982), however species composition was more diverse in the present study, both pre- and post-wildfire. Many of the helminths recorded from the 7 native mammal species in this study have been described or redescribed during the past decade. Nevertheless, considerable taxonomic work is required, particularly in the Trematoda. All host taxa harboured a diverse helminth fauna dominated by nematodes. Helminth species found in A. stuartii, A. swuinsonii, S. leucopus and R. htreolus at Nadgee and Timbillica State Forests represented more than 70% of the total helminth faunas known to occur in these hosts throughout their geographic ranges in Australia; those found in P. nusutu, R. fuscipes and M. musculus represented more than 50% and those found in I. obesulus represented less than 40% of the total faunas known from these hosts (Mackerras, 1958; Spratt, Beveridge & Walter, in preparation). Several species reported in previous studies of helminth communities in small mammals in Australia were notable by their absence from hosts at Nadgee and Timbillica State Forests. Beveridge & Barker (1976) recorded the spirurid nematodes Stummerinemu su$odiux (19% prevalence) and Synhimuntus uustruliensis (29%), the trematode Plugiorchis sp. (1%) and the cestode Chounotueniu rutticolu in a population of A. stuurtii at Powelltown, Victoria. Obendorf (1979) recorded the nematodes Nippostrongylus brusiliensis (2.1%), Longistriata sp. (10.6%), Odiliu muckerrusue (2.1%), Capillariupraeputiulis (31.9%), Physulopteru troughtoni (25.5%), S. suffodiux (6.4%), Gongylonemu beveridgei (2.1%) and Contrucuecum sp. (larvae) (2.1%) in populations of R. fuscipes in southeastern Victoria. He also observed the cestode C. ratticola and the nematodes 0. muckerrusue and S. suffodiax in R. lutreolus (Obendorf, 10~. cit.). Singleton (1985) recorded the oxyurid nematode Aspiculuris tetrupteru (6.2%) in M. musculus in the mallee wheatlands of western Victoria. Of the helminth species found in these same 4 hosts at Nadgee and Timbillica State Forests, 22 species from A. stuartii, 17 species from R. fuscipes, 16 species from R. lutreolus and 4 species from M. musculus were not encountered in the Victoria studies. Helminth species richness increased markedly in S. leucopus and decreased markedly in P. nasuta post-fire. Species diversity in S. leucopus exhibited a corresponding increase but that in P. nasuta did not decrease correspondingly post-fire. These results reflect the dearth of (n=l), and the low helminth species

H&ninth communities in mammals

201

richness in (n’2) S. leucopus pre-fire and the moderate species richness (n=9) in P. nasuta despite slow recolonisation post-fire (n’l). S. leucopus appears to be a fire-enhanced species able to exploit the mid- to late-seral stages of succession following wildfire. Species richness in R. lutreolus was enhanced considerably post-fire but species diversity decreased, indicating that although more helminth species were present, many occurred at a low prevalence in the host population. The decreased species diversity in A. stuartii and R. fuscipes post-fire despite increased species richness reflect reduced prevalences of the different helminth species in these host populations. Conversely, increased species diversity in A. swainsonii post-fire despite decreased species richness reflects increased prevalences of the various helminth species in this host population. Several helminth species exhibited a catholic host range. Cupillaria sp. 11 was recorded from dasyurid marsupials, a peramelid marsupial, native rodents and the introduced house mouse. The trichostrongyloid nematode Tetrubothriostrongylus mackerrasae occurred in some dasyurid and peramelid marsupials and in the bush rat; another trichostrongyloid, Peramelistrongylus skedastos was recorded in dasyurid and peramelid marsupials but not in rodents. Larval stages of physalopterid nematodes were found in the 3 dasyurid and the 3 rodent species but not in the peramelid marsupials. These larvae are believed to be species of Abbreviata which occur as adults in snakes and lizards, the small marsupials and the rodents presumably serving as intermediate hosts of the parasites and components of the diet of the definitive hosts. Larval stages of Ophidascaris robertsi, an ascaridoid nematode of the carpet python, Moreliu spilota varieguta, were found in A. stuartii, A. swainsonii, P. nasuta and R. fuscipes, highlighting another food chain involving small marsupial and eutherian mammals. The broad host ranges of larval nematodes, reflecting food chains, contrast with the narrow host ranges of adult trichostrongyloid nematodes, the dominant intestinal fauna of all hosts. The predominance of herpetostrongyloids in the dasyurid marsupials, mackerrastrongylids in the peramelid marsupials and heligmosomatids in the rodents clearly reflect host phylogenetic relationships. Three distinct helminth communities and a fourth less distinct community are apparent; one in the dasyurid marsupials A. stuartii, A. swainsonii and S. leucopus; a second in the peramelid marsupials P. nasuta and I. obesulus; a third in the native rodents R. fuscipes and R. lutreolus, and a fourth in the introduced house mouse, M. musculus. The latter host, a species characteristic of perturbed habitat, underwent rapid colonisation of forest and heathland after the wildfire, and exhibited greatest similarity of helminth community with the native rodents, R. lutreolus and R. fuscipes. M. musculus shared only 2 helminth species with the dasyurid marsupials and no helminth species with the bandicoots. This preliminary overview of fluctuations of small mammal populations and of their helminth parasite populations following perturbation by wildfire provides baseline information on host and parasite community structures. Our more detailed analyses of (a) demographic changes in host populations, (b) the effects of host sex, host age, season and habitat upon parasite populations and (c) the pathogenesis of parasite species and correlation with host population fluctuations shall place us in a better position to address and to test the hypotheses of Holmes (1979) and Price (1980) concerning the interactions responsible for host and parasite community structures. SUMMARY 1. Changes in the composition and abundance of 5 marsupial and 3 eutherian mammal species, and of their helminth communities pre- and post-perturbation by wildfire at Nadgee and Timbillica State Forests in southeastern coastal New South Wales during the period September 1977 to September 1985 are reported. 2. Dasyurid marsupials (Antechinus stuartii, Antechinus swainsonii and Sminthopsis leucopus), peramelid marsupials (Perumeles nasuta and Isoodon obesulus) and native eutherian rodents (Rattus fuscipes and Rattus lutreolus) occurred pre-fire. These species and the introduced house mouse (Mus musculus) occurred post-fire. 3. All host taxa harboured a diverse helminth fauna dominated by nematodes. The helminth communities in A. stuartii, A. swainsonii, S. leucopus and R. lutreolus represented more than 70%, those in P. nusuta, R. fuscipes and M. musculus represented more than 50% and that in I. obesulus represented less than 40% of the total helminth faunas known to occur in these hosts throughout their geographic ranges in Australia. 4. Adult nematodes of Cupillaria sp. 11 and Tetrabothriostrongylus mackerrasae occurred in all host groups, those of Perumelistrongylus skedastos occurred in both marsupial groups but not in rodents, larval stages of the ascaridoid nematode Ophidascaris robertsi occurred in all host groups and physalopterid nematode larvae believed to be Abbreviuta spp. occurred in dasyurid marsupials and in rodents but not in peramelid marsupials.

D. M. Spmtt

202

5. Four helminth communities were recognised: one in the dasyurid marsupials, a second in the peramelid marsupials, a third in the native rodents and a fourth in the introduced house mouse. 6. Differences in the helminth communities in host taxa pre- and post-wildfire were associated with the ecological strategies of the hosts and their roles as opportunistic invaders (M. musculus), fire-enhanced species (S. leucopus) or slow recolonisers (I? nasuta) post-perturbation by wildfire.

Acknowledgements-l am grateful to Peter Haycock and Elizabeth Walter whose conscientious and expert technical assistance in the field and in the laboratory constitutes the foundation of this research project, to Drs I. Beveridge, J. Calaby and G.R. Singleton for constructive comments on an earlier draft of the manuscript and to Mrs J. Rudd for typing the manuscript. The collaboration and co-operation of the following helminth taxonomists is gratefully acknowledged: Drs I. Beveridge, 0. Bain, A.G. Chabaud, M. Cl. Durette-Desset, L.M. Gibbons, I. Humphery-Smith. J.C. Pearson and C. Vaucher. The work was conducted under permits issued annually by the New South Wales National Parks and Wildlife Service and the Forestry Commission of New South Wales.

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and

sex-related

CATLING P.C., NEWSOME, A.E. & DUDZINSKIG. 1982. Small mammals, habitat components and fire in southeastern Australia. Proceedings of the Symposium on Dynamics and Manugement of Mediterruneun-Type Ecosystems pp. 199-206 San Diego, California. CHRISTENSENP., &HER H. & HOAREJ. 1981. Responses of open forests (dry sclerophyll forests) to fire regimes. In: Fire and the Australian Biota Ch. 15. vv 367-393 (Edited bv Gill A.M.. Groves R.H. & Noble I.R.) Australian Academy of Science, Canberra. ._ GREIG-SMITHP. 1964. Quantitative Plant Ecology. Butterworth & Co., London. HOLMESJ.C. 1979. Parasite populations and host community structure. In: Host-Parasite Interfaces pp 2746 (Edited by B.B. Nickel) Academic Press, N.Y. HOLMESJ.C. & PODES~AR. 1968. The helminths of wolves and covotes from the forested region of Alberta. Cunudiun Joournul ofZoology 46: 1193-1204. LEONG T.S. & HOLMES J.C. 1981. Communities of metazoan parasites in open water fishes of Cold Lake, Alberta. Journal of Fish Biology 18: 693-713. MACKERRASM.J. 1958. Catalogue of Australian mammals and their recorded internal parasites. Part I. Monotremes and marsupials. Part II. Eutheria. Proceedings of the Linnueun Society of New South Wales 83: 101-143. MARGOLISL.G., ESCH G.W., HOLMES, J.C., KURIS A.M. & SCHAD G.A. 1982. The use of ecological terms in parasitology. Journal ofPurusito/ogy 68: 131-133. NEWSOME, A.E., MCILROYJ. & CATLINGP. 1975. The effects of an extensive wildfire on populations of twenty ground vertebrates in south-east Australia. Proceedings of the Ecological Society of Australia 9: 107-123. OBENDORFD.L. 1979. The helminth parasites of Ruttus fuscipes (Waterhouse) from Victoria, including description of two new nematode species. Australian Journal of Zoology 27: 867-879. PRICE P.W. 1980. Evolutionary Biology of Purasites. Monographs in Population Biology. 15. Princeton University Press, Princeton N.J. SIMPSONE.H. 1949. Measurement of diversity. Nuture London 163: 688. SINGLETONG.R. 1985. The population dynamics of Mus musculus and its parasites in mallee wheatlands in Victoria during and after drought. Australian Wildlife Research 12: 437-445. WALKERJ. 1981. Fuel dynamics in Australian vegetation. In: Fire and the Australian Biotu Ch. 5, pp 101-127 (Edited by Gill A.M., Groves R.H. & Noble I.R.) Australian Academy of Science, Canberra.