Loranthaceae) on the Cactus Echinopsis Chilensis

Home , Loranthaceae, Tristerix, Tristerix aphyllus

Revista Chilena de Historia Natural 73: 525-531, 2000

Factors affecting the circular distribution of the leafless mistletoe Tristerix aphyllus (Loranthaceae) on the cactus Echinopsis chilensis

Factores que afectan la distribuci6n circular del muerdago sin hojas Tristerix aphyllus (Loranthaceae) sobre el cacto Echinopsis chilensis

CAREZZA BOTTO-MAHAN', RODRIGO MEDEL', ROSANNA GINOCCHI02 & GLORIA MONTENEGR03

'Departamento de Ciencias Ecologicas, Facultad de Ciencias, Universidad de Chile, Casilla 653, Santiago, Chile, e-mai I: rmedel@ abello.dic. uchile.cl 2Departamento de Ecologfa, Facultad de Ciencias Biologicas, Pontificia Universidad Catolica de Chile, Casilla 114-D, Santiago, Chile. 3Departamento de Ciencias Vegetales, Facultad de Agronomfa y de Ingenierfa Forestal, Pontificia Universidad Catolica de Chile, Casilla 306, Santiago, Chile

ABSTRACT

We describe the pattern of emergence of the holoparasitic mistletoe Tristerix aphyllus from its cactus host Echinopsis chilensis in a semiarid Chilean ecosystem. The observed circular distribution of the parasite inflorescence differed significantly from a uniform distribution based on a random process. We quantified the circular distribution of the seeds defecated on the cactus surface by Mimus thenca, the only bird responsible of seed dispersal. Our data did not support the idea of a directional seed deposition by the bird. To test the hypothesis that the observed circular distribution can be attributable to a differential seed survival due to microsite temperature variation, we infected cacti with seeds ofT. aphyllus every 30°and quantified the temperature associated to each angle. Our results revealed that even though seeds located in angles with higher sun exposure had the lowest haustoria! disk formation, this variation in mortality is not sufficient to explain the angular polarity observed in this species. Inspection of inflorescences of T. aphyllus that emerged 17 months after the experimental infection, revealed mean angular values indistinguishable from the natural circular distribution. Assessment of the anatomical structure at two opposing angles of the cactus revealed striking differences in epidermal constitution, such as a four-fold thicker epidermis in north than in south facing samples due to formation of highly lignified bark. We suggest that bark formation is likely the most important factor determining the biased circular distribution ofT. aphyllus.

Key words: parasitic plant, inflorescence, seed deposition, bark formation, circular statistics.

RESUMEN

Describimos el patron de emergencia del muerdago holoparasito Tristerix aphyllus desde su cacto hospedador Echinopsis chilensis en un ecosistema semiarido de Chile. La distribucion circular de !as inflorescencias del parasito difirio significativamente de una distribucion uniforme basada en un proceso aleatorio. Cuantificamos la distribucion circular de !as semillas defecadas sobre la superficie del cacto por el mfmido Mimus the ne a, ei único ave responsable de la dispersion del muerdago. Nuestros datos no sostuvieron la idea de una deposicion de semillas direccional por parte del ave. Para someter a prueba la hipotesis que la distribucion circular observada es atribuible a una sobrevivencia diferencial de !as semillas debido a variacion termica entre micrositios, infectamos cactos con semillas de T. aphyllus cada 30° y evaluamos la temperatura asociada a cada angulo. Aun cuando !as semillas ubicadas en angulos con mayor exposicion solar presentaron la menor formacion de disco haustoria!, esta variacion en mortalidad no fue suficiente para dar cuenta de la polaridad angular observada. No obstante, !as inflorescencias de T. aphyllus que emergieron 17 meses despues de la infeccion experimental, revelaron estadfgrafos circulares indistinguibles de aquellos observados en la situacion natural. La inspeccion de la estructura anatomica en dos angulos opuestos de la cactacea revelo diferencias en la constitucion de la epidermis, observandose un espesor en promedio cuatro veces mayor en !as muestras orientadas hacia el norte que en !as orientadas hacia el sur debido a la formacion de corteza altamente lignificada. Sugerimos que la formacion de corteza es probablemente el factor másimportante en determinar la distribucion circular sesgada de T. aphyllus.

Palabras clave: planta parasita, inflorescencia, deposicion de semillas, formacion de corteza, estadfstica circular.

(Received March 22, 2000; accepted June 14, 2000; managed by P. Marquet) 526 BOTTO-MAHAN ET AL.

INTRODUCTION abiotic factors as the putative cause for the observed pattern. More specifically, we address the follow- Establishment in suitable microhabitats is a criti- ing questions: i) Does the emergence of the mistle- cal step in determinig the prevalence and abun- toe inflorescences occur randomly from the cactus dance of parasites in host populations (see re- surface or exhibit an angular bias ? ii) What is the views in Esch et al. 1990, Poulin 1998). In para- importance of environmental temperature for the sitic plants, establishment involves two steps: i) attachment process ? iii) Can the circular distribu- attachment, defined as the adhesion of the hausto- tion of inflorescences be explained by thermal dif- rium to the host plant surface, and ii) penetration, ferences between microhabitats ? iv) What is the defined as the process following attachment, importance of cactus morphology in explaining the where the periferal cells of the radicle ingress to angular distribution of the mistletoe? the host tissues (phloem or xylem) through the host cortex (Riopel & Timko 1995). Establish- ment is perhaps the most sensitive step from the METHODS parasitic life-cycle perspective (Norton & Car- penter 1998). It is known that variation in tem- Field procedure perature, moisture, and light availability can dra- matically reduce mistletoe seed survival (e.g., The field study was conducted in the Reserva Lamont 1983, Salle 1983, Boone et al. 1995), Nacional Las Chinchillas, Auc6 (31 °30'S, which in turn restrict the establishment of para- 71°06 'W), approximately 300 km north Santiago. sitic plants to a restricted set of within-host mi- We measured the circular distribution of seeds crohabitats (e.g., Norton et al. 1997, Yan & Reid and inflorescences from September to October 1995, Powell & Norton 1994). In this paper we 1997, using a mirror compass, and always setting assess the importance of the thermal environment the magnetic north to 0°. Because the mistletoe for seed attachment and subsequent development inflorescences are best represented by an arc on in a holoparasitic mistletoe endemic to the arid the perimeter of cacti, we recorded the minimum, zones of Chile. bisecting, and maximum angle covered by the Tristerix aphyllus (Loranthaceae) is a parasite in 118 cacti. Selected cacti averaged 1.85 holoparasitic Chilean mistletoe that parasitizes only m height (range: 0.23- 2.55 m) and most mistle- species of Cactaceae (Kuijt 1969, 1988). This un- toes where located in the upper half of the cactus usual species has leaves reduced to minute scales columns ( 1.28 m on the average, range: 0.11 - and its red inflorescence emerges from the cactus 2.26 m). Contrasts between the circular distribu- surface. The only species responsible of consum- tion of inflorescences and seed shadow were per- ing and dispersing the mistletoe seeds at the study formed according to circular statistics procedures site is the Chilean mockingbird Mimus thenca (Batschelet 1981, Fisher 1993). (Martinez del Rfo et al. 1995, Medel 2000). Once defecated by the bird, a reddish radicle emerges from a viscid seed, which often contacts and presses Temperature analysis against the epidermis of cacti to form an haustoria! disk. Once attached, narrow hairlike filaments pass To explore in more detail the factors involved in through the stomata and the penetration of the the circular pattern of the mistletoe, we quanti- cactus is effected (Mauseth et al. 1984, Mauseth et fied the angular variation in the daily temperature al. 1985). Attachment of the haustorium is not at the surface of one individual of E. chilensis 1.5 restricted to cacti but also occurs on a broad range m above the ground. We measured simultaneously ofliving and non-living substrates (Mauseth 1985). the temperature every 30° by setting thermo- Within the cactus tissues, T. aphyllus constitutes couples type T (± 0.1 %accuracy) connected to a an extensive system of endophytic strands leading 12-channel scanning thermometer Digi-Sense. in all directions (Kuijt 1969, Mauseth et al. 1984, Temperature was recorded at the end of the seed Mauseth et al. 1985). The rest of the seedling dispersal period ofT. aphyllus (December 1997), remains on the outside of the cactus and dies after every 10 min from 7:00 to 21:00 h during three host penetration. consecutive days. In this contribution we describe a striking To evaluate experimentally the role of tempera- microdistributional pattern of the inflorescences ture on the circular distribution of the mistletoe, of T. aphyllus along the radial surface of the in August 1998 we set 12 seeds per cactus at 1.5 cactus Echinopsis chilensis (Colla) Friedr. et m above ground. We placed one seed each 30° in Rowl. (=Trichocereus chilensis B. et R.). At the 10 not parasitized host plants. Only seeds def- same time, we evaluate the importance of biotic and ecated by M. thenca and showing a radicle not CIRCULAR DISTRIBUTION IN Tristerix aphyllus 527

exceeding 3 mm long were selected for artificial mm) and stained with safranin and fast-green for infection. All seeds were oriented to ensure effec- histological analysis at OM. SEM samples were tive contact between the seed viscin and the host dehydrated in an increasingly graded acetone se-

cuticle. We assessed seed survival and haustoria! ries and dried from 100% acetone via C02 in a disk formation four months after manual infec- Polaron E3,000 critical point drying apparatus. tions. Both the subsequent emergence and the Finally, they were coated with a gold layer 100 A circular distribution of the 120 experimental in- thick and viewed in the SEM Jeol JSM-25-SII. fections were quantified in January 2000, 17 Measurements of surface thickness consisted on months after the initiation of experiment. the linear distance from the outermost cell of the epidermis to the base of the hypodermis, adyacent to the chlorenchyma. Anatomical analysis

To assess the importance of morphological barri- RESULTS AND DISCUSSION ers of cacti to the penetration or emergence of the mistletoe, we analyzed tissue samples of approxi- Inflorescences described an arc of 132.6° ± 49.9° mately 20 x 20 mm taken from five not parasitized on the surface of E. chilensis (mean vector ± individuals in a locality near Santiago. Tissue circular SD, range: 36.0°- 267.0°, N = 118), and samples were taken l. 7 5 m above ground from the circular distribution of the bisecting angles north (0°) and south (180°) exposition. The depth differed significantly from a uniform distribution of tissue sampling was approximately 10 mm. (mean vector± circular SD, 118.1 o ± 42.0°, range: After each tissue sample was removed they were 50.7°- 186.3°, Rayleigh test for uniformity, P < fixed immediately in F.A.A. (formalin-alcohol- 0.00 l ). This pattern implies a conspicuous polar- acetic acid). Samples were analysed through Op- ity in the circular distribution ofT. aphyllus in-the tical Microscope (OM) and Scanning Electron direction SE that can not be explained by a ran- Microscopy (SEM). Samples were embedded in dom process (Fig. 1). We assessed the seed shadow Paraplast, sliced in thin transversal sections (15 of the mistletoe on cacti as a potential factor a b Inflorescence Seed deposition

o· o•

180° IBO• Fig. I. Circular distribution of the bisecting angle of inflorescences of Tristerix aphyllus on Echinopsis chilensis (a), and circular distribution of the seed deposition made by Mimus the nea on cacti (b). The mean vector and circular deviation in the inflorescence data are indicated. Distribuci6n circular del angulo bisectriz de !as inflorescencias de Tristerix aphyllus sobre Echinopsis chilensis (a), y distribuci6n circular de la deposici6n de semillas efectuada por Mimus thenca sabre Ios cactos. (b) Se indica el vector promedio y la desviaci6n circular en Ios datos de inflorescencia. 528 BOTTO-MAHAN ET AL.

responsible for the angular polarity of inflores- 50 cences. Because seeds remain adhered to cacti 45 once defecated by M. thenca, it was possible to estimate the circular distribution of the seed u 40 shadow by recording the exact angle at which 1:.- 35 every seed was observed on the host (mean vector ~ 30 of the seed shadow± circular SD, 197.6° ± 104.2°). ~Q) c. The inflorescence distribution was more concen- 25 Q)E trated than the seed shadow (2.49 and 0.39, re- ..... 20 spectively), and comparison of the mean vectors 15 revealed significant differences between the two distributions (Watson F-test for two circular 10 means, F = 59.76, df = 337, P < 0.001, Fig. 1). 0 30 60 90 120 150 180 210 240 270 300 330 This result indicates that the seed shadow does Azimuth not necessarily translate into the observed emer- Fig. 2. Descriptors of the maximum (e), mean (•), gence of the inflorescences, and consequently and minimum(+) temperature for 12 can not be considered as responsible for the po- thermocuples set up at intervals of 30° on the larity in the circular distribution of the mistletoe. surface of Echinopsis chilensis. Like non-parasitic plants, germination and de- Descriptores de la temperatura maxima (e), media C• ), y velopment of mistletoes require permissive tem- minima(+) para 12 termocuplas ubicadas a intervalos de peratures (Boone et al. 1995) and the optimum 30" sobre la superficie de Echinopsis chilensis. temperature for germination and radicle elonga- tion varies depending on the environment (Lamont Results from the experimental infection revealed 1983 ). In the study site, the mean temperature that seeds located between 270- 330° had a lower around the cactus ranged from 25.9- 29.5 oc (~T probability of successful infection as shown by = 4.6 °C), and the highest value was observed at haustoria! disk formation (Fig. 3). Overall, 69.2 270° (Fig. 2). The maximum temperature ranged % of the 120 experimental seeds survived to form from 36.6-47.9 °C (~T= 11.3 "C), and the highest haustoria! disk (t-test for dependent samples, t = value also occurred at 270°. The minimum tem- 4.27, df = 11, P = 0.001). However, disk forma- perature ranged from 12.4- 14.0 oc (~T= 1.6 oc). tion was not always followed by a subsequent Because the greatest temperature variation was emergence of the mistletoe from the cactus cu- observed in maximum temperatures, it is reason- ticle. Only 15.8 % of the infected cacti showed able to consider this as one of the likely con- inflorescence emergence 17 months after experi- straining factors for mistletoe seed survival. mental infection (Fig. 3), a relatively low fraction

0.8 :::>- :.0 0.6 m ..0 0 0.4 a.'- 0.2

0 0 30 60 90 120 150 180 210 240 270 300 330 Azimuth Fig. 3. Probability of haustoria! disk formation (grey bars) and subsequent emergence of inflorescences (black bars) of Tristerix aphyllus from the experimental infection on Echinopsis chilensis. Probabilidad de formaci6n de disco haustoria! (barras grises) y subsecuente emergencia de inflorescencias (barras negras) de Tristerix aphyllus a partir de !as infecciones experimentales sobre Echinopsis chilensis. CIRCULAR DISTRIBUTION IN Tristerix aphyllus 529 in comparison to the total seeds that developed haustoria! disk (19 out of 83 · seeds)(t-test for a b dependent samples, t = 7.09, df = 11, P < 0.001). Emergence of new inflorescences occurred in the range 60° - 180° (Fig. 3), which fits well to the natural circular distribution of emergence (range: 50.7° - 186.3°). Comparisons of the minimum, mean and maximum angles of the natural inflorescences with those emerged from experimental infected cacti did not reveal significant differences (Table 1). Overall, these results indicate that temperature, although important for seed survival and haustoria! disk formation, is not sufficient to explain the emergence of new inflorescences and thus the angular polarity of T. aphyllus observed at this level. Our results indicate that seed deposition and temperature can not unequivocally be identified as responsible for the angular pattern of the inflorescences. Even though temperature seems to be an important abiotic factor influencing the emergence ofT. aphyllus from the cactus tissue, other factors need to be assessed for a better under- standing of the angular polarity of this species. For instance, anatomical analysis revealed striking differences in the surface thickness of cactus depending from the azimuth (see also Evans et al. 1994c ). South facing samples (180°) consist on a smooth thin epidermis that cover a thick hypodermis made of six to eight layers of cells with Fig. 4. SEM microphotographies showing trans- extremely thick walls (Fig. 4a). Above the epi- verse sections of stems at the level of the surface dermis there is a profusion of epicuticular waxes of Echinopsis chilensis. a) South facing sample that originate in the epidermic cells, leaving sto- showing an epidermis of two or three layers mata deeply sunken under the surface. Although covered with a great profusion of epicuticular stomata are located at the surface, cuticularized waxes with sunken stomata. Under the epidermis stomatal canals pass from the stomata through the there is a pluristratified hypodermis of very thick hypodermis to the assimilatory tissues beneath. walls, interrupted by long sub-stomatic chambers Interestingly, north facing samples (0°) consist which end in the chlorenchyma, x 50. b) North on several layers of highly lignified periderm, facing sample showing a barking surface with which originates from cellular divisions in the several overlaped layers of periderm obstructing epidermal cells (Fig. 4b). Sequential analysis of stomata (shown by an arrow), x 50. (e: epidermis, transversal thin sections of tissue samples indi- w: epicuticular waxes, h: hypodermis, eh: chloren- cated that, unlike samples from the south orienta- chyma, cc: cork cambium, ph: phellem, pc: tion, several overlapping layers of periderm parenchymatic cells). clearly obstruct stomata located in the epidermis, Microfotograffas de microscopfa electr6nica indicando inhibiting their function in gas exchange between secciones transversales de la superficie de E. chilensis. a) inside and outside of the stem. Comparison of the Muestra de exposici6n sur mostrando una epidermis de dos - tres capas cubiertas con ceras epicuticulares con estomas stem thickness between samples revealed a four- hundidos. Bajo la epidermis hay una hipodermis fold higher thickness in north than in south samples pluriestratificada de paredes muy gruesas, las cuales son (mean (mm)± SD, north: 1539.0 ± 508.7; south: interrumpidas por largas camaras sub-estomaticas que 374.9 ± 80.0, n = 5, paired t-test, t = 5.05, P < terminan en el clorenquima, x 50. b) Muestra de exposici6n 0.001 ). Because infection occurs when hairlike norte mostrando una superficie de corteza con varias capas filaments ofT. aphyllus pass through the stomata sobrepuestas de peridermis que obstruyen Ios estomas (indicado por flecha), x 50. (e: epidermis, w: ceras of cacti (Mauseth 1985, Mauseth et al. 1984, epicuticulares, h: hipodermis, eh: clorenquima, cc: 1985), the asymmetrical formation of peridermis fel6geno, ph: peridermis, pc: celulas parenquimaticas). seems to be the most important factor responsible of the bias in the circular distribution of T. 530 BOTTO-MAHAN ET AL.

TABLE I

Results from contrasts of the mean vectors (SD) of inflorescences of Tristerix aphyllus in natural and field experimental conditions (df = 125 for all comparisons)

Resultados de contrastes de Ios vectores promedios (SD) de !as inflorescencias de Tristerix aphyllus en condiciones naturales y experimentales de terreno (gl = 125 para todas !as comparaciones)

Minimum angle Bisecting angle Maximum angle

Natural 50.73° (52.64°) 118.05° (41.97°) 186.28° (44.20°) 0 Experimental 44.80° (30.92°) 105.83° (26.53°) 167.93° (32.1] ) F 0.11 0.73 1.42 p 0.74 0.39 0.24 aphyllus. There is evidence that establishment and haustoria! connections in some hemiparasitic LITERATURE CITED mistletoes infecting tree species tend to relate inversely with host bark thickness (e.g., Sargent BA TSCHELET E (1981) Circular statistics in biology. 1995, Norton & Ladley 1998). We hypothesize Academic Press, London. 371 pp. & that uneven bark formation in the surface of E. BOONE LS, G FATE, M CHANG DG LYNN (1995) Seed germination. In: Press MC & JD Graves (eds), chilensis represents a critical physical barrier for Parasitic plants: 14-38. Chapman & Hall, London. the conductivity of the haustorium ofT. aphyllus. ESCH GW, AO BUSCH & JM AHO (1990) Parasite com- However, bark formation in the north facing epi- munities: patterns and processes. Chapman & Hall, dermis is not restricted to E. chilensis as revealed London. 335 pp. by detailed studies done in several cactus species EVANS LS, VA CANTARELLA, KW STOLTE & KH from the northern and southern hemispheres (see THOMPSON ( 1994a) Epidermal browning of saguaro Evans et al. 1994a, b, c). These authors suggested cacti (Carnegia gigantea): surface and internal char- that the causal agent of barking relates with sun acteristics associated with browning. Environmental and Experimental Botany 34: 9-17. exposure and UV irradiance. The extent to which EV ANS LS, V A CANT ARELLA, L KASZCZAK, SM bark formation in E. chilensis is adaptive to pre- KREMPASKY & KH Thompson (1994b) Epidermal vent parasitism or represent an incidental effect browning of saguaro cacti ( Carnegia gigantea): physi- to environmental conditions with no implication ological effects, rates of browning and relation to for the host-parasite coevolution remains to be sun/shade condition. Environmental and Experimen- tested in future studies. tal Botany 34: 107-115. EV ANS LS, C MCKENNA, R GINOCCHIO, G MONTENEGRO & R KIESLING (1994c) Surficial injuries of several cacti of South America. Environ- ACKNOWLEDGMENTS mental and Experimental Botany 34: 285-292. FISHER NI (1993) Statistical analysis of circular data. We thank J orge Arroyo, Claudia Ortiz, and Eric Cambridge University Press, Cambridge. 277 pp. Rivera for their help during part of the field work. KUIJT J (1969) The biology of parasitic flowering plants. Logistic support for temperature field measure- University of California Press, Berkeley. 246 pp. ments was provided by Marfa Victoria Lopez and KUIJT J (1988) Revision of Tristerix (Loranthaceae). Manuel Contreras (the good one). CONAF IV Systematic Botany Monographs 19: 1-61. Region authorized this study in the National Re- LA MONT B (1983) Germination of mistletoes. In: Calder & serve and provided logistic support. David Norton M P Bernhardt (eds) The biology of mistletoes: 129-143. Academic Press, Sidney. and an anonymous reviewer made important sug- MARTINEZ DEL RIO C, M HOURDEQUIN, A SILVA & gestions that improved the clarity of the manu- R MEDEL (1995) The influence of cactus size and script. CB was supported by a CONICYT fellow- previous infection on bird deposition of mistletoe ship for graduate studies. This work was funded seeds. Australian Journal of Ecology 20: 571-576. by FONDECYT 1970497 to RM, FONDECYT MAUSETH JD (1985) Relation between Trichocereus 1980967 and NSF USDA 2U01 TW00316-07 to chilensis and the holoparasite Tristerix aphyllus. GM, and FONDECYT 1000750 to RG. This study Medio Ambiente 7: 39-44. & is part of the activities of the Center for Advanced MAUSETH JD, G MONTENEGRO AM W ALCKOWIAK (1984) Studies of the holoparasite Studies in Ecology and Research on Biodiversity Tristerix aphyllus (Loranthaceae) infecting funded by Milenio P99-103-F ICM. Additional Trichocereus chilensis. Canadian Journal of Botany support was provided by an endowed Presidential 62: 847-857. Science Chair to Mary T. Kalin-Arroyo. CIRCULAR DISTRIBUTION IN Tristerix aphyllus 531

MAUSETH JD, G MONTENEGRO & AM POWELL GR & DA NORTON (1994) Contrasts in crown W ALCKOWIAK (1985) Host infection and flower development of the mistletoes Alepis flavida (Hook. formation by the parasite Tristerix aphyllus f.) Tiegh. and Peraxilla tetrapetala (L. f.) Tiegh. (Loranthaceae). Canadian Journal of Botany 63:567- (Loranthaceae) parasitic on Nothofagus solandri 581. (Hook. f.) Oerst., Craigieburn Ecological District, MED EL R (2000) Assessment of parasite-mediated selec- New Zealand. New Zealand Journal of Botany 32: tion in a host-parasite system in plants. Ecology 81: 497-508. 1554-1564. RIOPEL JL & MP TIMKO (1995) Haustoria! initiation NORTON DA & MA CARPENTER (1998) Mistletoes as and differentiation. In: Press MC & JD Graves (eds) parasites: host specificity and speciation. Trends in Parasitic plants: 39-79. Chapman and Hall, London. Ecology and Evolution 13: 101-105. SALLE G (I 983) Germination and establishment of Viscum NOR TON DA & 11 LADLEY (I 998) Establishment and album L. In: Calder M & P Bernhardt (eds) The early growth of Alepisflavida in relation to Nothofagus biology of mistletoes: 145-159. Academic Press, solandri branch size. New Zealand Journal of Botany Sidney. 36:213-217. SARGENT S (1995) Seed fate in a tropical mistletoe: the NORTON DA, 11 LADLEY & HJ OWEN (1997) Distribu- importance of host twig size. Functional Ecology 9: tion and population structure of the loranthaceous 197-204. mistletoeAlepisflavida, Peraxilla colensoi, Peraxilla Y AN Z & N REID (1995) Mistletoe (Amyema miquelii and tetrapetala within two New Zealand Nothofagus for- A. pendulum) seedling establishment on eucalypt hosts ests. New Zealand Journal of Botany 35: 323-336. in eastern Australia. Journal of Applied Ecology 32: POULIN R ( 1998) Evolutionary ecology of parasites: 778-784. from individuals to communities. Chapman & Hall, London. 2 I 2 pp.