The impact of seed predation by mammals on post-fire seed accumulation in the endangered shrub Grevillea caleyi (Proteaceae)

Biological Conservation 97 (2001) 377±385

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The impact of seed predation by mammals on post-®re seed accumulation in the endangered shrub Grevillea caleyi (Proteaceae) Tony D. Auld *, Andrew J. Denham NSW National Parks and Wildlife Service, PO Box 1967, Hurstville, NSW 2220, Australia Received 4 February 2000; received in revised form 14 July 2000; accepted 19 July 2000

Abstract Over several fruiting seasons, the fates of seeds placed in recently burnt habitats, and one habitat unburnt for more than 10 years, were used to examine the impact of ®re on seed predation levels in the endangered species Grevillea caleyi from southeastern Australia. Native rodents, Rattus fuscipes, and macropods, Wallabia bicolor, were responsible for seed losses after seeds fell below parent plants. Virtually all seeds (99±100%) were lost to these mammals for the ®rst two fruiting seasons after a wild®re. Such losses usually exceeded pre-®re loss estimates or estimates from a site unburnt for more than 10 years. There was no signi®cant di€erence in seed losses to mammals in three recently burnt sites over four fruiting seasons. However, there was a slight trend for some seed escape (seed losses 91±97%) and a slowing of the rate of seed loss in the fourth fruiting season after ®re. Time since the last ®re accounted for some 60% of the estimated variation in magnitude of seed losses to mammals. These results suggest that in the endangered, ®re-sensitive G. caleyi, replenishment of the soil seed bank after ®re is severely retarded by mammal seed predation. The implications are that after a ®re, G. caleyi should be protected from the risk of a future ®re well beyond three times the primary juvenile period in the species or local extinction will occur. # 2001 Elsevier Science Ltd. All rights reserved. Keywords: Seed predation; Rodents; Macropods; Australia; Seed banks; Fire; Threatened species

1. Introduction Species exhibit a range of characteristics that may lead to rarity (Rabinowitz, 1981). If rare species are subject to population declines, then they are likely to be considered threatened and be of a high priority for conservation action. The assessment of threat status of species has been developed in a number of ways, most comprehensively by the World Conservation Union (IUCN) (Mace and Lande, 1991; IUCN, 1994; Isaac and Mace, 1998). Quantitative criteria for risk assessment based on characteristics of species that are believed to re¯ect their risk of extinction have been developed (IUCN 1994, 2000), and include, rate of decline, distributional range size, population size and quantitative risk of extinction. Among species considered threatened are a number of plants characterised by restricted distributions containing few remnant populations and subject to a number of signi®cant * Corresponding author. Tel.: +61-2-9585-6497; fax: +61-2-95856606. E-mail address: [email protected] (T.D. Auld).

threatening processes (Palmer et al., 1997; Keith, 1998; Schnittler and Gunther, 1999). The degree of threat to species with restricted distributions may be exacerbated in highly fragmented landscapes subject to anthropogenic disturbance. Interactions between species and the disturbance regimes under which they evolved may have been altered through habitat loss and fragmentation. The ability of threatened plant species with restricted distributions to persist in the landscape under altered disturbance regimes, habitat fragmentation and other threats, is a key issue for conservation. In ®re-prone habitats, recruitment is frequently linked to ®re (Tyler, 1995). However, where human impacts on the environment alter the ®re regime (frequency, intensity, season and spatial extent), the ability of a species to persist at a site maybe reduced, especially for plants whose adults are killed by ®re (®re-sensitive) (Morrison et al., 1996; Ho€mann, 1999, Keeley et al., 1999; Veblen et al., 1999). For example, repeated ®res at short intervals will eliminate ®re-sensitive species that are slow to mature and replenish their seed banks (Morrison et al., 1995; Bradstock et al., 1997). There are also likely to be

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interactions between ®res and other organisms that may a€ect restricted species (e.g. predispersal seed predators; Bond, 1984; Auld and O'Connell, 1989). Seed predators may limit fecundity and consequently recruitment and adult establishment (Louda, 1989; Schupp and Fuentes, 1995). In southeastern Australia, post-dispersal seed predation impacts on plant abundance have been little studied. Recent work on Grevillea (Auld, 1995; Vaughton, 1998; Auld and Denham, 1999) suggests that within this genus, mammalian seed predation may have signi®cant impacts on future recruitment levels. For ®re-sensitive plants, seed predation may in¯uence the rate of buildup of seed banks between ®res (Keeley, 1987; Auld, 1995; Vaughton, 1998). How the magnitude of the seed bank in¯uences recruitment levels will depend on the nature and extent of available safe sites (sensu Harper, 1977) and their level of saturation with seeds, as well as the degree to which recruitment is limited by the availability of suitable microsites (Crawley, 1992). Losses of seeds to seed predators will in¯uence recruitment unless all safe sites are already occupied. In Australia, some 1071 plant species are recognised as being threatened (ANZECC, 1999), representing just under 5% of the ¯ora. A further 7% are considered to be rare and 12% poorly known, and hence potentially rare or threatened (Briggs and Leigh, 1996). The genus Grevillea (Proteaceae) (represented by some 357 species; Makinson, 2000) is the third largest genus of Australian plants and is widespread across a range of habitats in Australia. In the Sydney region of southeastern Australia, some 28 Grevillea spp. are known, of which six are listed as threatened under the NSW Threatened Species Conservation Act 1995 and a further six have restricted distributions and are considered rare or poorly known (Briggs and Leigh, 1996). Most are moderately long-lived (10±50 years) perennial shrubs that occur in ®re-prone communities. Most of these threatened or restricted species are ®re-sensitive, although a few have the ability to resprout after ®re. The endangered plant G. caleyi is highly restricted and endemic to ®re-prone habitats in the interface of urban areas and bushland in northern Sydney, southeastern Australia (approx. 33 530 E, 151 130 S). Maintenance of the remaining fragments of populations of G. caleyi is dependent upon eliminating a number of threats and maintaining a ®re regime that is not detrimental to G. caleyi or other species that co-habit with it (Scott et al., 1995). G. caleyi is killed by ®re and relies on germination from a soil seed bank for establishment after a ®re (Auld and Scott, 1996). It takes 2±4 years for seedlings to mature (primary juvenile period) and seed production generally increases as plants grow, up to 8±10 years of age (Scott et al., 1995). The size of the soil seed bank is predicted to increase with time since ®re up to 10±15 years post-®re before declining as plants sensece and die (Auld, 1995).

Persistence of G. caleyi at a site is therefore dependent upon the interaction between ®re frequency and the post-®re rate of replenishment of the soil seed bank (Auld and Scott, 1996). G. caleyi is known to su€er high levels of seed losses to native mammals in areas unburnt for greater than 10 years (Auld and Denham, 1999). This pattern is re¯ected in other common and rare Grevillea species in southeastern Australia (Vaughton, 1998; Auld and Denham, 1999). This paper examines the impact of mammalian seed predators on the endangered plant G. caleyi following extensive ®res in January 1994 in the Sydney region of southeastern Australia. We asked: 1. Are mammals important seed predators of annual seed-crops after ®re? 2. Are the levels of post-®re seed predation by mammals di€erent to pre-®re levels using a comparison with the pre-®re data from Auld and Denham (1999)? 3. What is the likely impact of post-®re seed predation levels on G. caleyi and its ability to replenish its soil seed bank after ®re? 4. What are the management implications of seed losses to mammals in G. caleyi? 2. Methods 2.1. Study species G. caleyi R.Br. (Proteaceae) is a bushy shrub up to 5  5 m occurring as part of the shrubby understorey in eucalypt forests on laterite ridgetops. Some 85% of the former habitat of the species has been cleared for urbanisation (Scott et al., 1995), and the remaining remnant locations are highly fragmented and subject to a range of threats including further clearing, weed invasion and human disturbance to the habitat. Some remnant patches are subject to being burnt in major wild®res or in hazard reduction burns to protect life and property, while others, isolated from nearby large patches of remnant vegetation by urban areas, are rarely burnt. Seeds are large (average of 318±351 mg from samples of 25 seeds; Auld and Denham, 1999) and are passively released from the generally one-seeded fruit in late spring to early summer, with ¯owering predominately in autumn to winter. Some minor ¯owering and fruiting can occur sporadically throughout the year. The seeds have no obvious appendages and are not dispersed by ants, in contrast to other Grevillea species in the habitat (Auld and Denham, 1999). No dispersal agents are known. 2.2. Study sites Sites were all located within the limited distribution of G. caleyi in northern Sydney, southeastern Australia.

T.D. Auld, A.J. Denham / Biological Conservation 97 (2001) 377±385

Annual precipitation for Sydney is around 1300 mm, while the average monthly maximum/minimum temperatures are 26/18 C in summer and 16/8 C in winter. The study area has been subjected to repeated ®res. The recent ®re history of the sites studied is detailed in Table 1. Most of the large patches of bushland containing G. caleyi were burnt in extensive wild®res in Sydney in January 1994 or in hazard reduction burns in mid 1994. Estimates of mammalian seed predation were available from three sites in 1991 and 1992 (Auld and Denham, 1999): these `pre-®re' sites were subsequently burnt in January 1994. This study utilised the same sites post®re, as well as selecting an additional site that escaped the 1994 ®re. Insucient area of habitat for G. caleyi remained unburnt in 1994 for any further unburnt replicate sites to be sampled. The unburnt site sampled in this study was subsequently burnt in October 1998 and was not sampled in the 1998/99 season (see Table 1). 2.3. Estimates of mammalian seed predation Mature fruits and seeds were opportunistically collected by a mixture of hand picking of ripe, undehisced fruits o€ plants, recently dehisced seeds o€ the ground, and by bagging large green fruits until they had dehisced. Fruits were bagged just before seed ripening and it was assumed that this did not a€ect seed characteristics. Intact seeds were stored in envelopes at room temperature. At each of three recently burnt study sites (Sites 1±3), three plots (30  30 m) were established in areas containing G. caleyi, while at Site 4 (unburnt for >10 years) only one plot could be established due to the limited size of this habitat (see Table 1). In each plot, for four consecutive post-®re fruiting seasons (1995/96, 1996/97, 1997/98 and 1998/99 (Site 4 not sampled in 1998/99) the fates of cohorts of 10 seeds placed at random within the plots were followed weekly for up to 3 months. Four cohorts were established at each plot (one per week for 4 consecutive weeks). All ®eld trials were conducted at roughly the same time each year, with the timing of Table 1 Sampling regime for studya Site

Fire history (last ®re/2nd last ®re)

Fruiting seasons sampled

Number of replicate plots per fruiting season

1 2 3 4

1994/1979 1994/1979 1994/1975b 1998/1984c

95/96 96/97 97/98 98/99 95/96 96/97 97/98 98/99 95/96 96/97 97/98 98/99 95/96 96/97 97/98

3 3 3 1

a

Fire history based on ®re history records held by NSW National Parks & Wildlife Service. b Based on ®eld estimates of plant growth. c Between 1984 and 1987 based on ®eld estimates of plant growth.

379

trials coinciding with natural seed fall (November±February). The study was not controlled for variation in the Grevillea seed densities available to potential predators as seed predators could take seeds of other Grevillea species that co-occurred with G. caleyi (Auld and Denham, 1999) and potentially other taxa as well. In sites burnt in 1994, there was no seed production by G. caleyi, by other local Grevillea species known to have seed eaten by mammals (Auld and Denham, 1999), or by most other local plant species in late 1994/early 1995. No estimates of seed predation were made in this season. In the following fruiting season (late 1995/early 1996), seed rain was close to zero, as most G. caleyi plants were immature, with only a few individuals (16% of a sample of 189 plants, Scott and Auld unpubl.) maturing fruits during the course of these trials. No other Grevillea species occurring at the sites were mature. This was the ®rst year these trials were run (see Table 1). In the second, third and fourth fruiting seasons after the January 1994 wild®res, many more individuals of G. caleyi matured fruit (64, 86 and 77%, respectively, from a sample of 185, 182 and 177 plants; Scott and Auld, unpubl.) as well as other Grevillea species and other taxa at the sites. Levels of fecundity increased from 1995/96 to 1998/99 as G. caleyi plants became larger (G. caleyi fruit production estimated to be 1.1, 5.2, 6.2 and 6.4 seeds per plant, respectively, for 1995/96, 1996/ 97, 1997/98 and 1998/99; Scott and Auld, unpubl.). Data from Auld and Denham (1999) collected prior to 1994, utilising comparable techniques to this study, were used for pre-®re estimates of seed predation at Sites 1±3. In all trials, locations of seeds were recorded in a grid layout in the plot at each site and each seed was also marked nearby with a numbered, small metal stake. In 1995/96, at Site 1 only, a comparison of marked and unmarked seeds was made to test the impact of marking seeds for ease of relocation of seeds. Seeds were marked with a small white dot of typewriter correction ¯uid. Marking, however, may also provide a scent cue for mammals to ®nd seeds. This trial involved the establishment of three additional replicate plots at Site 1 for the marked seeds, with cohorts of 10 seeds placed weekly for 4 weeks. Hence, in 1995/96 at Site 1, there were six plots (three replicates with marked seeds and three with unmarked seeds). A two-factor ANOVA was used to compare the proportion of seeds eaten by predators over the duration of the trials across all sites (Sites 1±4) for 1995/96, 1996/97 and 1997/98. No data were available for the unburnt Site 4 in 1998/99 so this year was excluded from the analysis. Plots in Sites 1±3 were pooled as only one plot was available for Site 4. A nested three-factor ANOVA comparison was also made of the proportion of seeds eaten by predators over the duration of the trials for all recently burnt sites (Sites 1±3) across all four sampling years (1995/96±1998/99), incorporating nested plot

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e€ects. The e€ect of seed marking in the recently burnt Site 1 in 1995/96 was examined by comparing the proportion of seeds eaten by predators over the duration of the trial using a nested two-factor ANOVA (with nested plot e€ects). For all analyses, Cochran's test was used to test for homogeneity of variances. Where heterogeneous variances were detected, the data were arcsine transformed (Underwood, 1981). For the comparison of Sites 1±4 from 1995/96 to 1997/98, the data were heterogeneous even after arcsine transformations and the ANOVA was performed on the raw data with a conservative approach to rejecting the null hypothesis in order to avoid Type 1 errors (i.e. the null hypothesis was not rejected unless the probability of the F-ratio in the ANOVA was <0.01). Where F ratios in the analyses were signi®cant, individual means were compared using Student±Newman±Keuls tests (Zar, 1974). The relationship between the total estimated seed loss to predators and the time since the last ®re was examined in a simple linear regression. Data on the proportion of seeds removed by predators was pooled across all available cohort and plot data [including the pre-®re data from Sites 1, 2 and 3 from Auld and Denham (1999)]. Rates of seed loss were compared using a multivariate comparison of proportional seed removal by pooling all available cohort and plot data [including the pre-®re data from Sites 1, 2 and 3 from Auld and Denham (1999)] using a Gower Metric matrix of association and non-metric multi-dimensional scaling (Belbin, 1993). Data were standardised across sites and years by only considering loss of seeds over the ®rst 8 weeks. Clustering analysis (FUSE and DEND in PATN; Belbin, 1993) was used to identify major grouping of sites and years of sampling. This allowed examination of the patterns both between sites, and over times since ®re. A principal axis correlation (Belbin, 1993) was then used to examine how well three variables (time since last ®re, site, year of sampling) ®tted in the ordination space. As sites have no linear relationship, the analysis was run for all possible numerical ordering of sites to examine any possible site in¯uence. 3. Results Seed losses were of two types: (a) seeds eaten in situ or within a 15 cm radius of the seed location (attributed to losses by native bush rats, Rattus fuscipes; cf. Auld and Denham, 1999), although a very small percentage of seeds were lost to unknown invertebrates. In these cases, seed testa remains were present; or (b) seeds wholly removed (attributed to swamp wallabies, Wallabia bicolor). Experimental work on identifying agents removing Grevillea seeds (Auld and Denham, 1999) indicated that seeds removed were eaten by swamp wallabies. Some

seed removal attributed to swamp wallabies may have been moved by rats and then consumed but the seeds remains not found. Hence, it is possible that seed losses to swamp wallabies may be overestimated and losses to bush rats underestimated. It is also possible that rats may not consume all seeds that they move, although there is no evidence of seed hoarding by these rats in Australia. There was no detectable e€ect of marking seeds on the level of seed predation (F1,18=1.0, P=0.33) as virtually all seeds were eaten, nor any nested plot e€ect (F4,18=1.0, P=0.43). All sites and plots showed high levels of mammalian seed predation throughout the study (Fig. 1). Levels of seed losses were consistently very high (99±100%) in 1995/96, i.e. within 2 years after the ®re. High levels of seed loss were maintained in the subsequent seasons (1996/97, 1997/98) with a slight decline in the 1998/99 fruiting season (Table 2). No signi®cant di€erences were found between the replicate burnt sites (Sites 1±3) over 1995/96 to 1998/99, although there were signi®cant plot e€ects (Table 3), indicating variation at small spatial scales. There was a signi®cant site by year of sampling interaction in the comparison of all sites over 1995/96 to 1997/98 (Table 3). The unburnt Site 4 had signi®cantly less seed loss to predators in 1995/96 and 1996/97 than all three burnt sites (Sites 1±3), whilst in 1997/98 losses at Site 4 were comparable to Sites 2 and 3, but signi®cantly more than Site 1. The three burnt sites were similar (as per plot e€ect analysis over four fruiting seasons) except that in 1997/ 98, Site 1 had the lowest seed predation (signi®cantly less than for Site 2). However, the site di€erences in 1997/98 were very minor (97.5±100% of seeds lost; Table 2). Pattern analysis (Fig. 2) revealed a clustering of sites with rapid and mostly total seed loss (recently burnt sites in 1995/96 and 1996/97; see Fig. 1). A second group of sites consisted of a mixture of the pre-®re (1992/93) data available from Sites 1±3, the long unburnt Site 4 and data from burnt sites (Sites 1±3) in 1997/98 and 1998/99 (Fig. 2). This group essentially re¯ected a slower rate of seed loss than the ®rst group, as illustrated by Site 3 in 1998/99 (Fig. 1). One site (Site 3, 1997/98) was ungrouped and three sites (Site 1, 1992/ 93, Site 1, 1998/99 and Site 4, 1996/97) broadly grouped. These sites had slowest initial seed loss rates (e.g. see Site 1, 1998/99 in Fig. 1). There was a reasonable correlation (0.6) of the ordination with time since the last ®re (Fig. 2), while site (0.13±0.46, depending on ordering) and year of sampling (0.02) (Fig. 2) were weakly or poorly correlated with the ordination. This suggests that time since ®re may in¯uence predation levels, but that year of sampling or site sampled had little impact. Time since the last ®re was a reasonable (R2=0.6) predictor of overall percentage seed loss based on a linear regression (Fig. 3).

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Fig. 1. Rates of seed losses to mammalian seed predators in G. caleyi in Site 1 (a), 2 (b), 3 (c) (all burnt in 1994 ®re) and Site 4 (d) burnt in 1984. Data pooled across plots and cohorts. Vertical lines represent standard errors. Di€erent symbols and lines for each site represent di€erent sampling years: Ð*Ð, 1995/96; Ð~Ð, 1996/97; Ð&Ð, 1997/98; Ð^Ð, 1998/99. Note ®nal data points in this ®gure re¯ect last sampling week where all cohorts were sampled and so points may vary slightly from overall removal rates in Table 2.

4. Discussion Most seeds of the endangered shrub G. caleyi released onto the soil surface were consumed by seed predators (rodents and macropods) in both a site unburnt for more than 10 years and also in three recently burnt sites. Seed losses were not a€ected by marking of seeds with a white dot in the one site and year this trial was performed. The marking certainly assisted with the ability to ®nd seeds in the ®eld but as virtually 100% of seeds were lost in both the marked and unmarked seed trial, there was no evidence of an in¯uence of the scent from the material used to mark seeds on the ability of rodents to detect seeds. The estimated proportion of seeds that were eaten in situ was also comparable between marked and unmarked seeds (Table 2). In general, throughout the study, estimates of losses to rats (35±68%) and to wallabies (31±65%) were comparable (Table 2) suggesting

that both agents were responsible for seed losses across all sites and years. Given the levels of seed loss recorded in this study at sites that were recently burnt (91±100%), virtually the entire annual seedcrop can be lost post-®re in this species. Predation by mammals represents a major reduction in the magnitude of annual seed inputs to the persistent soil seed bank. While there was no signi®cant variation between sites, there was a signi®cant plot e€ect (Table 3), indicating that within a site there is spatial variation of overall seed loss to mammals. Similar patterns of small scale variation has been documented for rodent seed loss (Hulme, 1994). The cause of such variation has at least partially been attributed to the distribution of small mammals (Hulme, 1994) and variation in the amount of leaf litter (Clark et al., 1991). In the estimates of mammal seed predation before the 1994 ®re (Auld and Denham, 1999) and in the one

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Table 2 Seed fates in Grevillea caleyi over several post-®re seasonsa Site/fruiting season sampled

Years since last ®re

Sites 2±5 years after a ®re 1/1995/96 2 1b/1995/96 2 1/1996/97 3 1/1997/98 4 1/1998/99 5 2/1995/96 2 2/1996/97 3 2/1997/98 4 2/1998/99 5 3/1995/96 2 3/1996/97 3 3/1997/98 4 3/1998/99 5 Sites unburnt for >10 years 1c/1992/93 13 2c/1992/93 13 17 3c/1992/93 4/1995/96 13 4/1996/97 14 4/1997/98 15

Eaten in situ

Removed

Total

49.6 48.1 35.2 45.7 55.4 53.3 42.5 50.8 43.3 42.5 57.5 67.5 50.5

(3.4) (7.7) (5.0) (6.5) (5.3) (1.9) (4.6) (5.3) (3.1) (4.8) (5.8) (4.3) (4.1)

49.6 51.9 64.8 51.8 35.5 46.7 57.5 49.2 53.3 56.7 42.5 30.8 45.4

(2.6) (7.7) (5.0) (6.5) (4.8) (1.9) (4.6) (5.3) (2.8) (4.7) (5.8) (4.0) (3.8)

99.2 (0.8) 100 (0) 100 (0) 97.5 (1.3) 90.8 (2.9) 100 (0) 100 (0) 100 (0) 96.7 (1.9) 99.2 (0.8) 100 (0) 98.3 (1.1) 95.8 (1.9)

32.0 70.0 46.0 35.0 47.5 59.3

(8.6) (7.1) (8.6) (6.5) (6.3) (8.2)

50.0 22.0 38.0 52.5 35.0 40.7

(5.5) (8.8) (8.6) (4.8) (6.5) (8.2)

82.0 (6.6) 92.0 (3.7) 84.0 (5.1) 87.5 (6.3) 82.5 (2.5) 100 (0)

a Data are means ( S.E.) of percentage of seeds lost as a result of post-dispersal seed predators. Data pooled across plots for burnt Sites 1, 2 and 3. b Marked seeds in burnt plots (see text). c Data from Auld and Denham (1999).

Table 3 Analysis of Variance comparisons of total seed removal levels across Sites 1 to 4 and years of sampling Source

DF

Mean square

F-ratio

Probability

a. Comparisons of seed losses at Sites 1±4 over three consecutive fruiting seasons (1995/96 to 1997/98), excluding marked seeds from Site 1 in 1995/96 Site Year of sampling Site  year Residual

3 2 6 108

0.301 0.010 0.013 0.001

23.38 7.729 9.762

<0.001 <0.001 <0.001

b. Comparison of seed losses at three recently burnt sites (Sites 1±3) over 1995/96 to 1998/99 Site Year of sampling Plot (site) Site  year Year  Plot (site) Residual

2 3 6 6 18 108

0.010 0.022 0.068 0.047 0.002 0.002

1.54 4.64 3.61 2.03 1.24

0.288 0.053 0.003 0.115 0.246

unburnt site used in this study, the level of seed predation by mammals (over 8±9 weeks after seed release) was also high (82±100%). For such sites unburnt for more than 10 years, in 5/6 of sampled sites/years, there was some small amount of seed escape from mammals.

As some of these seeds could be relocated in the litter one year after a trial was established (e.g. seeds from the 1997/98 trial relocated in 1998/99) we suggest that not all seeds are eventually consumed by mammals, although there may be some additional seed losses over time. Auld (1995) postulated that the impact of high seed predation levels recorded in a number of Grevillea species would be reduced if in recently burnt areas there was some signi®cant seed escape from predators. A possible mechanism for such seed escape (Auld, 1995) was that the mammalian seed predators would have their abundance (and hence impact) reduced by the ®re and would take a number of years to recover, based on some work on Rattus fuscipes abundance in relation to ®re (Fox and McKay, 1981). Rodent abundance is known to ¯uctuate in relation to ®re (Catling, 1991; Friend, 1993; Haim and Izhaki, 1994; Sutherland and Dickman 1999). Evidence from this study suggests that this hypothesis is untenable at least in the urban/bushland interface around Sydney. The work of Vaughton (1998) on the rare Grevillea barklyana in southeastern Australia also revealed a pattern of very high (100%) seed losses to mammals shortly (2 years) after ®re. She found lower seed losses (78±98%) in sites unburnt for 17±26 years, again suggesting that highest rates of seed losses to mammals occur in the ®rst few years post-®re, although her studies were only based on seed losses over 1 week. In 1995/96 and 1996/97, very high post-®re seed losses occurred at a time when very few Grevillea seeds were produced locally (1995/96) or when seed production levels were still moderate (1996/97). This was >15 (1995/96) or > 27 (1996/97) months after the release of seeds from serotinous species following the 1994 ®re. In subsequent years, other plant species (including other Grevillea species) initiated seed production and a greater seed resource should have been available to seed predators. Although we did not sample mammal abundance after the ®re, this study and the work of Vaughton (1998) suggests that the impact of mammals was increased immediately after ®re. Possible explanations for this increase in the impact of mammals include the following: a. Interactions between the spatial extent of the ®re and the survival of mammals. Small scale burns may leave much unburnt habitat and hence, result in little decline in mammal densities (Auld, 1995; Vaughton, 1998). In this study, the 1994 wild®res were extensive and little vegetated habitat remained unburnt (although there was spatial variation in the intensity of the ®re). However, the habitat in many of the study sites is highly fragmented and lies adjacent to urban and semi-rural areas. These areas may o€er short-term refugia from the lethal e€ects of a passing ®re. This may

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imply that the dynamics of endangered plant and seed predators have been altered by urbanisation. If seed predators have an increased ability to survive ®re following urbanisation, then this will have a detrimental impact on the persistence of G. caleyi populations. b. A low availability of seeds in the plant community generally in the ®rst few years post-®re as plants recover from the ®re (either via vegetative regrowth or from seed), excluding the immediate post-®re release of seeds by serotinous species. Species with pyrogenic ¯owering would be an exception, e.g. in the habitat of the present study Angophora hispida, Telopea speciosissima and Xanthorrhoea spp. (Keith, 1996). This low seed availability may e€ectively increase mammalian predation impacts on the seeds that are available even if mammal numbers are greatly reduced, but not eliminated by ®re. With increasing time since ®re there may be a reduction in the rate of seed loss and overall seed losses to mammals via predator satiation (cf. Janzen, 1971) and an increase in litter cover (Clark et al., 1991). One possible trend discernible with time since ®re was a slowing of the rate of seed loss, even though overall losses remained high (Figs. 2 and 3). This would assume

Fig. 2. Multidimensional scaling ordination plot of proportion of G. caleyi seeds remaining per week of sampling (up to a maximum of 8 weeks) for each site and year sampled. Data pooled for plots and cohorts. Site and year codes as follows: 1st digit, site number; 2nd and 3rd digits, initial sampling year, e.g. 397 represents Site 3 in 1997/98. Di€erent lines represent three explanatory variables in ordination space (time since ®re, number of years since the last ®re; site, site sampled; year, year of sampling). Length of lines is in proportion to correlation strength of each variable. The site correlation presented is the mean of all possible combinations. Groupings are based on results of clustering analysis (see text).

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that all seeds surviving at the end of our trials survived to be incorporated into the soil seed bank. There was some evidence of long-term survival of seeds in our plots, but because of the high levels of seed loss recorded and the variation in seed loss levels across longer unburnt sites (> 10 years post-®re), there is also the likelihood of further seed losses for those seeds that survived the length of our trials (up to 13 weeks after seed release). The time since the last ®re in years accounted for some 60% of the variation in total seed losses. There were slight, although not signi®cant, di€erences between the ®rst three fruiting seasons post ®re (1995/96, 1996/97, 1997/98), and the next one (1998/99). In two out of three fruiting seasons at a long unburnt site there were signi®cantly less seed losses than in the three recently burnt sites. The one year of pre-®re data (Auld and Denham, 1999) for our burnt study sites also suggests a possible trend for lower seed losses in sites unburnt for greater than 10 years. Lower seed losses at sites may re¯ect impacts of an increased food resource and an increased diculty in ®nding seeds with time since ®re. In contrast, both year of sampling and site were not strong explanatory variables for the pattern of seed losses observed (Fig. 2). For G. caleyi, mammalian seed predators will act to reduce the rate of build-up and the size of a soil seed bank after ®re and hence, in¯uence the resilience of these species to frequent ®re. In many ®re-prone habitats, ®re is the major disturbance event promoting recruitment (Tyler, 1995). Fires eliminate above-ground

Fig. 3. Overall seed losses in G. caleyi as a function of time in years since the last ®re. Linear regression is y=1.01ÿ0.01x. Data are total seed losses at a site in any sampled year. Data for Sites 1, 2, and 3 for 13, 13 and 17 years, respectively, post-®re are from Auld and Denham (1999). Time since the last ®re for each site is given in Table 1 (Site 1 *, Site 2 ~, Site 3, , Site 4 &).

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plants in ®re-sensitive species such as G. caleyi studied here, and the level of recovery depends largely on the magnitude of the soil seed bank. The length of the ®re interval will in¯uence the time seedlings have to mature and replenish the seed bank. Seed losses to mammals in the endangered plant G. caleyi were very high (91± 100%), from 2 to 5 years after a ®re. As seed production is also lower per plant in younger plants, the re-establishment of a soil seed bank is likely to be severely retarded after a ®re (i.e. low seed production and very high seed predation). Under such a scenario, seed accumulation in a soil seed bank would not occur for at least 4±6 years after ®re in G. caleyi. Seed accumulation after ®re will occur only when seed predation falls below the extreme levels of seed losses in the ®rst few fruiting seasons after ®re and becomes more comparable with the pre®re rates and there is a corresponding increase in the magnitude of plant fecundity as plants grow and age. Even in 1998/99, when some seeds were not eaten at Sites 1±3, germination occurred in 36% of 22 remaining intact seeds following heavy local rains, and these seeds would not then form a part of the persistent soil seed bank. This implies that G. caleyi has been very slow at replenishing soil seed reserves after the 1994 ®res and hence, the species is susceptible to declines or even local extinctions after frequent ®re (declines of 50±70% have been recorded after two ®res within 2±3 years; Auld, unpubl.). We estimate that a minimum ®re-free interval beyond 3 times the primary juvenile period in G. caleyi (i.e. some 8±12 years) would be required to allow accumulation of seed in the soil after the 1994 ®res. G. caleyi seeds are by far the largest of any Grevillea species in the habitat (6±10 times the seed size of other conspeci®cs) which may make this species more prone to high seed predation levels. In addition, other cohabiting Grevillea species such as G. buxfolia, G. linearifolia, G. sericea and G. speciosa, have elaiosomes that may allow increased seed escape from mammalian seed predation through seed removal by ants (Auld and Denham, 1999). G. caleyi is likely to be the slowest species in the community to replenish its seed bank and this maybe one reason for the rarity of the species. The signi®cant loss of seeds to mammals and the slow predicted replenishment of the soil seed bank after ®re are both elements that place G. caleyi at increased risk of local extinction in ®re-prone habitats, especially where the risk of frequent ®re is high and other threatening processes are operating. The implications for ®re management resulting from this study apply directly to the sites studied. However, G. caleyi is also found in some tiny remnants surrounded by urban areas where swamp wallabies are unlikely to exist, although Rattus fucipes or even the introduced R. rattus may be present. The dynamic interaction between soil seed accumulation in this endangered plant and seed predators in such tiny remnant sites is unknown.

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