an experimental test using egg predation by small mammals in new zealand

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Safety in Numbers for Secondary Prey Populations: An Experimental Test Using Egg Predation by Small Mammals in New Zealand Author(s): Christopher Jones Source: Oikos, Vol. 102, No. 1 (Jul., 2003), pp. 57-66Published by: on behalf of Wiley Nordic Society OikosStable URL: http://www.jstor.org/stable/3547858Accessed: 13-09-2015 04:37 UTC

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OIKOS 102: 57-66, 2003

Safety in numbers for secondary prey populations: an experimental test using egg predation by small mammals in New Zealand

Christopher Jones

Jones, C. 2003. Safety in numbers for secondary prey populations: an experimental test using egg predation by small mammals in New Zealand. - Oikos 102: 57-66.

New Zealand's native avifauna is threatened by introduced mammalian predators. Native species are often not the primary prey of these predators, which depend on introduced mice and rabbits as their primary food source. Theoretical models predict that predation risk for a subsidiary, or "secondary" prey species is inversely proportional to its population size. This prediction was tested by a quasi-natural experiment in which four different sized prey "colonies" were constructed at four existing sooty shearwater breeding sites. Domestic hens' eggs were placed in shearwater burrows immediately following the shearwater breeding season and egg predation rates monitored at five, ten and fifteen days. Treatments were switched between sites and the experiment run for a second time after a two-week stand-down period. The net effect of increasing colony size was to lower individual risk of predation. The larger number of individuals present served to effectively "buffer," or dilute, per-capita predation risk from predators whose numbers are fixed by extraneous factors: chiefly the abundance of their primary prey. Although eggs were removed more slowly from smaller colonies than from larger ones, each loss had a greater per-capita effect on individual mortality risk. The inverse density dependent relationship found between colony size and predation risk implies that predator population dynamics are largely independent of secondary prey numbers. Abundant introduced predators can therefore easily drive a small secondary prey population to extinction. Control of primary prey populations may be an important management tool in these circumstances.

C. Jones, Dept of Zoology, Univ. of Otago, P.O. Box 56, Dunedin, New Zealand. Present address: Landcare Research, P.O. Box 282, Alexandra, New Zealand [email protected] o.nz).

Introduced predators pose a particular set of ecological threats to species that have evolved in their absence. Australasian ecological communities have suffered from the impacts of introduced house cats (Felis catus L.), mustelids (Mustela spp.), rats (Rattus spp.) and red foxes (Vulpes vulpes L.), amongst others (Moors and Atkinson 1984, Burbidge and McKenzie 1989, Innes and Hay 1991). Control of these pest species can often lead to marked increases in endemic species populations (O'Donnell et al. 1996), but direct management inter- vention does not always have the intended result (C6t& and Sutherland 1997).

For conservation management to be most effective, research must be directed towards an understanding of

Accepted 30 January 2003 Copyright ?) OIKOS 2003 ISSN 0030-1299

how the predator-prey systems operate: different patterns of threat may be predicted depending on whether the prey species is the maintenance, or "primary" prey or the "secondary" (subsidiary) food resource of the local predator guild. If predation reduces primary prey abundance, the dependent predators will suffer reduced survival and reproductive rates and subsequently decline as a result. This will, in turn, release the primary prey from predation pressure and allow it to persist. In contrast, both empirical and theoretical evidence suggests that a prey population that is not the main food resource of its predators may be at a greater risk because a decline in the prey will not trigger a commen- surate reduction in predator abundance. Extinction of

OIKOS 102:1 (2003) 57



the secondary prey may result if the predators responsi- ble are maintained by an abundant primary prey population.

Native fauna are often the secondary prey of introduced predators that depend on other introduced mammals as their principal food source. Predation models predict that for secondary prey populations predation will be inverse density-dependent at all prey densities (Pech et al. 1995, Sinclair and Pech 1996). The total predation impact on a secondary prey population will also be determined by the number of predators which is in turn dependent on the abundance of primary prey (Pech et al. 1995).

Theoretical models predict that this relationship can result in stable secondary prey populations at high densities, but unstable dynamics below some critical low-density threshold. This lower threshold occurs because total predation impact exceeds the rate of growth of the secondary prey population. Below this threshold, secondary prey will decline to extinction (Sinclair et al. 1998).

In New Zealand, rabbits (Oryctolagus cuniculus L.) and mice (Mus musculus L.) constitute the primary prey of feral ferrets (Mustela furo L.), stoats (M. erminea L.) and cats (Murphy and Dowding 1994, Alterio and Moller 1997, Ragg 1998). New Zealand's native birds represent the secondary prey of these introduced carni- vores. In a recent study of predation levels at mainland sooty shearwater (Puffinus griseus Gmelin) breeding colonies, which are threatened by introduced mammalian predators, Lyver et al. (2000) noted that individual predation risk appeared to be inversely related to colony size and suggested a "safety in numbers" dilution effect. Although their findings must be interpreted carefully due to unreplicated and non-independent data points, this may have been an example of the predicted predator-secondary prey relationship.

This study uses a quasi-natural experiment to test the theoretical predictions of an inverse density-dependent relationship between predation risk and the abundance of a secondary prey. The null hypothesis is that individual predation risk is independent of colony size, whereas theory predicts that predation risk will decline with increasing colony size. Whilst existing sooty shearwater breeding areas are used as study sites, the objec- tives of the study are to experimentally test the predicted relationship and not to estimate natural predation rates.

Methods

Experimental design

Different sized "breeding colonies" were constructed at four sites on the Otago coast, South Island, New Zealand by placing domestic fowl (Gallus gallus L.)

eggs in existing sooty shearwater burrows. Existing burrows were used to mimic natural densities and to avoid many of the problems of constructing completely artificial nests (Major and Kendal 1996, Ortega et al. 1998). The treatment variable was colony size which was set at n = 30, 60, 90 and 120 eggs. Few large sooty shearwater breeding colonies remain on mainland New Zealand (Hamilton et al. 1997, Wilson 1999, Jones 2000). Because of this the n = 120 treatment was able to be assigned to only two of the sites. This largest treatment was therefore initially allocated between the two suitable sites by a coin toss; the other three treatments were assigned randomly.

For each treatment, the number of eggs lost at five-day intervals up to 15 days after the nests were first baited was recorded. To allow for site-specific effects, treatments were switched between sites and ran the experiment for a second time, two weeks after the first. This period was a compromise between the need to maintain temporal independence of treatments and the need to keep other factors, especially predator density as similar as possible for subsequent comparisons.

Study sites

All sites were sooty shearwater breeding colonies at which predation had recently been recorded (Hamilton et al. 1997, Jones 2000, Lyver et al. 2000; N.Z. Depart- ment of Conservation, unpubl.). The sites were:

i) Bushy Beach [BB] (47 07.55S; 170 58.79E), a small coastal forest remnant, managed as a reserve and surrounded by farmland;

ii) Taiaroa Head [TH] (45 49.80S: 170 43.20E), pri- vate land, dominated by rank exotic grasses and woody shrubs lying between two privately managed conservation areas;

iii) Sandfly Bay [S] (45 54.25S; 170 39.OOE), reserve land, dominated by woody shrubs, native flax (Phormium tenax) and rank exotic grasses;

iv) Nugget Point [N] (46 27.OOS; 169 48.30E), reserve land, rank exotic grasses and native woody shrubs.

Each artificial colony covered an area of approximately 100 m x 40 m, the linear shape being a function of their coastal outlook. Treatment allocations were (experimental colony size in parentheses): BBl (30); BB2 (90); THl (60); TH2 (120); Sl(60); S2 (90); Nl (120); N2 (30).

Predator and primary prey indices

Prior to running the experiment, the presence and relative abundances of predator species, mice and lagomorphs, were recorded using index methods at all sites. A modified version of the ink-print tracking tunnel

58 OIKOS 102:1 (2003)



described by King and Edgar (1977) was used to measure relative abundances of mice, rats and mustelids. Each tunnel consisted of a wooden base, a metal cover and a metal tray that was divided into three equal sections of 195 x 95 mm. The centre section contained a foam pad soaked in a blue food dye/water solution and the two outer sections each held a piece of plain brown paper. Animals treading on the ink-pad leave a permanent record of their presence on the brown paper. Twenty tunnels were used at each site at a spacing of 100 m and were put in place 3-4 weeks prior to baiting to overcome neophobia in target species. They were baited, in late April/early May 2000, with rabbit meat and a peanut butter/oat mixture to attract both carni- vores and rodents. The papers were collected after three nights and prints were identified using the key devel- oped by Ratz (1997). Proportions of tunnels tracked at each site were used as indices of relative abundance for tracked species. Confidence intervals were assigned following Zar (1999, p. 527). Recent trapping histories were made available by site managers. Monitoring changes in feral cat populations is much more difficult because cats typically exist in very low density in mainland habitats and are notoriously difficult to recapture (Fitzgerald and Karl 1986, Norbury and Heyward 1996). Accordingly, only presence/absence measures were possible for this species.

Lagomorph relative abundances were indexed immediately prior to the experiment using the 'Gibb' score (Gibb et al. 1969). This is an index with which monitored areas are assigned a score of from 0 to 10 based on observed faecal pellet density. Significant correla- tions between pellet counts and rabbit density have been demonstrated by Gibb et al. (1969) and Wood (1988). A Gibb score was assigned to ten 100 m long by 2 m wide transects at each site. Each transect was divided into four 25 m sections and a score assigned to each section. A grand mean was estimated for each site. As climate is very similar at all four sites, the pellet breakdown rates were assumed to be approximately the same at all sites.

Any direct observations of mammal species or their sign throughout the fieldwork were also recorded.

Experimental protocols

The first set of treatments ran from late May to early June 2000. The starting date was determined by the time of fledging and subsequent departure from breeding colonies of that season's young sooty shearwaters. The second set of treatments ran from late June to early July 2000. All burrows were mapped and numbered at the study sites prior to placing the eggs in them. When there were more available burrows than required, adja- cent burrows were used in order to maintain an approx-

imation of natural nest density rather than distributing the eggs throughout a larger area and thus introducing density as another variable. The eggs were placed approximately 20 cm down inside burrows and the use of very steep or fragile, unstable burrows was avoided so that eggs could not be lost without some direct animal interference. Each egg was anointed with a single drop of sooty shearwater "oil" (proventricular lipid regurgi- tate obtained in studies of the birds' diet) to provide an olfactory cue to the eggs' presence. Egg loss was monitored after 5, 10 and 15 nights and any eggs remaining after this period were removed. Rubber surgical gloves were worn throughout the fieldwork to minimise hu- man scent traces.

Analyses

In addition to deriving simple predation rates as proportions of eggs taken and as daily removal rates, survival analysis methods were used (Kleinbaum 1996, Klein and Moeschberger 1997) to facilitate formal comparisons between treatments. These techniques estimate survival functions, i.e. the probability of an individual surviving beyond a specified time. The standard method is the 'Kaplan-Meier product limit estimator' (Kaplan and Meier 1958) which calculates conditional survival probabilities and is able to take into account those individuals surviving beyond the end of the experiment (right-censored data). The survival functions for each treatment were then compared using the log-rank test (Breslow 1975).

Cox proportional hazards models were used (Cox 1972) to examine the effects of initial colony size and a range of site-specific variables on predation rates. This is a distribution-free regression method which predicts relative risk based on one or more predictor variables and produces an output similar to standard regression models. The estimated regression coefficient corresponding to a particular covariate gives the change in the logarithm of the hazard function (the instantaneous death rate function) produced by unit change in the predictor variable, assuming all other variables remain constant (Everitt and Pickles 1999, pp. 209-229). A positive variable coefficient indicates that larger values of the variable are associated with greater mortality and vice versa. The site-specific factors tested were: site, initial burrow occupancy rate (no. burrows with eggs/ total available burrows), number of empty burrows, relative abundances of mice, lagomorphs and mustelid species. In constructing the models, factors that were not logically independent of each other, e.g. occupancy rate and number of empty burrows or initial colony size were not included together. Sites were compared with respect to primary prey relative abundances using standard ANOVA and contingency table methods.

OIKOS 102:1 (2003) 59



Results

Mammal species at study sites

Examination of tracking tunnel prints and other direct evidence (Table 1 and 2) shows that stoats were present at all sites, although no prints were recorded at Taiaroa Hd. All sites were visited by cats during the study period. Neither possums (Trichosurus vulpecula Kerr) nor hedgehogs (Erinaceus europaeus occidentalis Bar- rett-Hamilton) were recorded at Sandfly Bay, but they were present elsewhere. Lagomorph relative abundance was noticeably higher at Taiaroa Hd than at the other sites, although this pattern was not significant (F = 2.50, d.f. = 3, p = 0.08). Mouse abundance varied significantly between sites (X2 = 17.25, d.f. = 3, p < 0.01) with all tunnels at Sandfly Bay and 95% of those at Nugget Pt being tracked.

Predation of eggs Predation of eggs was recorded at all sites, although only one egg was lost throughout the entire experiment at Taiaroa Hd. The saturation of the response variable (i.e. all eggs taken) during treatment N2 by the 10-day check means that simple comparisons of removal rate after this time (10-15 days) are invalid, although data can still be analysed using survival analysis methods. Proportion of eggs taken declined with increasing colony size at two of the sites (N and S) for which non-trivial results were obtained but did not differ significantly at the third (BB; Fig. 1). Average daily egg loss rates for each replicate at 10 days (Fig. 2) increased with initial colony size (R2 = 0.67, F = 8.31, d.f. = 5, p = 0.047).

Comparison of the six treatments where non-trivial levels of egg loss were recorded using Kaplan-Meier

Table 1. Predator species present at each study site.

Species/site Bushy Beach Taiaroa Head Sandfly Bay Nugget Point

Felis catus F F F F Mustela furo T P T P M. erminea T 0 T T Rattus sp. T 0 Trichosurus vulpecula F F F Erinaceus europaeus occidentalis T T T

Key: T = tracking tunnel print; P = other print; 0 = direct observation; F = faeces.

Table 2. Indices of relative abundances of mammal species at experimental sites.

Species/site Bushy Beach Taiaroa Head Sandfly Bay Nugget Point

Lagomorph (mean Gibb score; 95% C.I.) 0.275 (0.332) 1.025 (0.666) 0.525 (0.473) 0.400 (0.329) Mice (% tunnels tracked; 95% C.I.) 50 (27.2; 72.8) 65 (40.8; 84.6) 100 (83.2; 100.0) 95 (74.9; 99.9) Stoat (% tunnels tracked; 95% C.I.) 5 (0.1, 25.1) 0 10 (1.2; 32.4) 10 (1.2; 32.4) Ferret (% tunnels tracked; 95% C.I.) 10 (1.2; 32.4) 0 0 5 (0.1, 25.1)

100 n=60 30

90 1190

70-

60 60

50 Fig. 1. Proportion of eggs -12 taken after 1r0 days at

T 40 experimental sites: Bushy Beach (BB), Taiaroa Head

30 - n-- 30 ~~~~~~~~~~~~~~~~(TH), Sandfiy Bay (S) and 20 -Nugget Point (N). The

number 1 or 2 refers to the 10 10first or second series of

n-- 60 ~~~~~~~~~~~~~~treatments; n = original 0 ~~~~~~~~~~~~~~~~~~~~~~~~~~~~~~~number of eggs present. Error

081 1112 THIl T12 Si S2 Ni N2 bars are 95% confidence Treatment intervals.

60 OIKOS 102:1 (2003)



Fig. 2. Average daily rates of 9 n= 120 egg loss after 10 days at 8 _ experimental sites: Bushy n90 Beach (BB), Taiaroa Head 7- _ _ (TH), Sandfly Bay (S) and 6 6 Nugget Point (N). The _ number 1 or 2 refers to the 5 first or second series of w 4 n=90 treatments; n = original n _ =30 number of eggs present. 53

2 -2

1 - n=30 n=60 n 120 0

BB1 BB2 THi TH2 Sl S2 Nl N2

Treatment

methods shows that survival probabilities varied significantly between treatments (log-rank test: Mantel- Haentzel X2 = 127.41; d.f. = 5; p < 0.01). Survival was highest in treatments Bl and B2 and lowest in S2 and N2 (Table 3).

The results from the first set of Cox proportional hazards models, using data from sites BB, S and N only are shown in Table 4. Both site (categorical variable) and initial colony size showed significant effects. Colony size had a weak inverse density-dependent effect on predation risk (Fig. 3). To investigate which characteristics of the sites determined this relationship "site" was substituted as a variable with the factors: mouse, stoat, ferret and lagomorph relative abundance. Only initial colony size had a consistently significant effect. To test for a "dilution of search" effect, i.e. by taking into account the number of empty burrows present at each treatment, initial occupancy was substituted rate for colony size, but this was not significant.

A second set of models were run which included data from all four sites including the data from Taiaroa Hd (Table 5). The variables site and initial colony size were again significant. Of the site variables, stoat relative abundance had a strong positive effect on predation. Mouse relative abundance and initial colony size both had weaker, but significant negative effects. Neither lagomorph relative abundance nor occupancy rate were significant.

Table 3. Survival functions S(t) for experimental treatments at which non-trivial egg loss was recorded after 15 days. Survival functions represent the probability of an individual surviving beyond a specified time.

Treatment Initial colony size S(t)

BB1 30 0.73 BB2 90 0.53 Si 90 0.21 S2 60 0.00 NI 120 0.10 N2 30 0.00

Discussion

Safety in numbers

The weak negative relationship between colony size and individual predation risk described by the Cox proportional hazards models and by the per-capita removal rates allows rejection of the null hypothesis that predation risk is independent of colony size for this range of breeding colony sizes. Egg losses represented the response of the local predator population, but, because the experiment ran for a short period outside of predator breeding season, it is unlikely that predator populations increased during this period. The response measured is therefore likely to represent the type of functional response of predators (Sinclair et al. 1998). A similar response may be obtained if primary prey, and thus predator, densities increase systematically and coincidentally with secondary prey abundance. Spatial replication, in the form of treatment switching, elimi- nated this potential problem.

The results also lend support to the empirical model of predation effects on sooty shearwater breeding colonies of Lyver et al. (2000). Their logistic regression model described a shallow positive relationship between colony size and both breeding success and chick survival for small colonies. Further evidence of safety in numbers comes from Cuthbert (2002) who combined data on sooty and Hutton's shearwater (P. huttoni Mathews) predation and again found an inverse density dependent relationship. Norbury (2001) described a similar pattern of predation on native New Zealand skinks (Oligosoma spp.) in a ferret/cat and rabbit- dominated system.

Sinclair et al. (1998) applied density theory to data on predator-prey relationships for a number of native Australian small mammal species threatened by introduced predators. They described inverse density- dependent predation for some of these populations typical of the interactions predicted when predators depend on another species as their primary prey. Under these conditions, if predators are abundant they can drive a secondary prey population to extinction without

OIKOS 102:1 (2003) 61



Table 4. Cox proportional hazards model output for experimental sites (Taiaroa Hd excluded). The estimated regression coefficient corresponding to a particular covariate gives the change in the logarithm of the hazard function produced by unit change in the variable, conditional on other covariates remaining constant. A more positive coefficient indicates a greater mortality risk associated with that variable.

Parameter Coefficient 95% C.I.s S.E. t-ratio p-value

Model 1 Site (category) -0.510 -0.663; -0.357 0.078 -6.528 <0.001 Initial size -0.006 -0.009; -0.002 0.002 -2.995 0.003

Model 2 Initial size -0.004 -0.009; 0.000 0.002 -2.122 0.034 Mouse n.s. Stoat n.s. Lagomorph n.s.

Model 3 Occupancy rate n.s. Mouse n.s. Stoat n.s. Lagomorph n.s.

n.s. indicates a non-significant result.

0.9

0.7 - m 0.6 - e 0.5 [ Fig. 3. Estimated effect of

O 0.4 b colony size on relative 0.3 - predation risk. Curves

G 0.3 - represent Cox proportional g 0.2 hazards model coefficients

0.1 with initial colony size, ________________________________________________________ m ouse, stoat an d lagom orp h 0 I I I I I relative abundance as factors

0 20 40 60 80 100 120 140 using data from: (a) only those sites at which egg loss

Colony size was recorded; (b) all sites.

Table 5. Cox proportional hazards model output - all sites. The estimated regression coefficient corresponding to a particular covariate gives the change in the logarithm of the hazard function produced by unit change in the variable, conditional on other covariates remaining constant. A more positive coefficient indicates a greater mortality risk associated with that variable.

Parameter Coefficient 95% C.I.s S.E. t-ratio p-value

Model 1 Site (category) -0.881 -1.000; -0.761 0.061 -14.445 <0.001 Initial size -0.009 -0.012; -0.006 0.002 -5.421 <0.001

Model 2 Initial size -0.006 -0.009; -0.002 0.002 -3.200 0.001 Mouse -3.722 -5.877; -1.567 1.100 -3.385 0.001 Stoat 61.220 42.016; 80.423 9.798 6.248 <0.001 Lagomorph n.s.

Model 3 Occupancy rate n.s. Mouse -3.646 -5.589; -1.702 0.992 -3.676 <0.001 Stoat 58.486 41.728; 75.244 8.550 6.840 <0.001 Lagomorph n.s.

n.s. indicates a non-significant result.

risking their own decline (Sinclair and Pech 1996). A similar relationship was reported by Vickery et al. (1992) wherein opportunistic or "incidental" predation on grassland birds' nests which, although of secondary importance to the predators (striped skunks, Mephitis mephitis Schreber), was potentially disastrous to the rare prey.

Larger secondary prey populations may be able to withstand depredation and remain at stable densities as inverse density dependent predation becomes less effec-

tive with increasing population size. The critical prey density below which extinction becomes likely is determined by the interaction between predation and recruit- ment rates (Pech et al. 1995).

Larger colonies may be more attractive

Whilst the net effect of colony size on individual predation risk was inverse density dependent, this appears to have been moderated by a density dependent response

62 OIKOS 102:1 (2003)



in terms of daily removal rates. This apparently para- doxical situation may reflect the clumped spatial distribution of the burrows in which eggs were placed. Investigations of the relationship between nest distribution patterns and predation frequently show a density dependent relationship, both in artificial and natural situations (Goransson et al. 1975, Hoi and Winkler 1994, Hogstad 1995). The greater numbers of eggs at my larger colonies may have been sufficient to induce an area-restricted search (ARS) behaviour in predators (Tinbergen et al. 1967). Increased predation rates have been ascribed to this behavioural response in recent experiments involving artificial nests (Andersson and Wiklund 1978, Larivi&re and Messier 1998). The latter authors suggested that opportunist nest predators may switch to ARS behaviour following a chance encounter with a locally abundant prey resource. This would allow generalist predators to take advantage of local, ephemeral peaks in secondary prey abundance.

The attractive effect of locally dense aggregations was described by Niemuth and Boyce (1995) who found that daily egg loss rates from simulated nests were greater at high density than at low density sites, but that there was no significant difference in proportional egg loss overall. The larger colonies in this investigation may also have presented a stronger olfactory cue to predators thereby increasing the "radius of detection" of the colony (Whelan et al. 1994). Predation rate may also have been influenced by the rate at which predators encountered burrows containing eggs. There was no significant effect of initial burrow occupancy rate in either set of models which suggests that this was not the case. This should be further tested by repeating this type of experiment with constant numbers of prey at varying densities.

Effects of site-specific factors

The results also suggest that the effects on a secondary prey population are likely to depend the local ecological conditions within a community at the time. For those treatments where significant levels of predation were recorded, the study site had a significant effect. Never- theless, individual characteristics of the sites, when analysed separately, did not predict predation. This may be a true representation, but could also be a statistical artefact resulting from testing a limited range for each factor and from minimal replication. The lower predation rates at the Bushy Beach site, irrespec- tive of colony size, may have contributed to this result. A review of nest predation studies by Clark and Nudds (1991) found that 79% described an inverse density- dependent relationship, but numerous factors (nest con- cealment, use of artificial nests, predator taxa and foraging efficiency) may have influenced these patterns and no clear-cut relationship could be discerned.

The Taiaroa Head site differed from the others in a number of ways: no predator tracks, except for those of hedgehogs, were recorded, it had a large number of unused burrows and suffered negligible egg loss. When data from this site were included in the models the effect of stoat relative abundance on predation risk became significant. Whilst this provides an explanation for the pattern of site-specific effects, caution must be exercised in interpreting a result where the regression curve is made significant by one highly influential zero- zero data point. There is a general trend in the data where sites showing higher stoat relative abundances suffer higher predation. Stoats have been implicated as possibly the greatest risk to breeding sooty shearwaters at the sites used (Hamilton 1998, Lyver 2000) and are likely to persist throughout the year because their primary prey, mice and rabbits, are also present. Most of the eggs lost during the experiment were completely removed, leaving no trace of shell. This is generally considered to be characteristic of mustelid predation (Flack and Lloyd 1978, Moors 1978, King 1990). Other potential egg predators (possums, hedgehogs and rats) leave abundant shell remains (Moors 1983, Brown et al. 1996). Stoats are also known to remove food to be cached for later use and have been observed rolling eggs away from nests (King 1989).

Mouse relative abundance was negatively associated with predation risk when data from Taiaroa Hd were included in models. Whilst the same statistical caveat applies to this as to the effect of stoat abundance as a predictor of risk, it is also quite possible that stoats are less likely to switch to egg predation when mice are abundant. Nest predation by mustelids and other small generalist predators has been shown to decline in response to increases in the availability of alternative foods (Dunn 1977, Angelstam et al. 1985, Schmidt and Whelan 1999) and may also show varying relationships to focal prey density. Nest predation has been shown to change from density dependent to density independent or inverse density dependent as alternative prey becomes available (Hogstad 1995, Schmidt and Whelan 1999). Diet switching by stoats in New Zealand fol- lowed a poisoning operation which reduced the abundance of their primary prey, ship rats (Rattus rattus), and led to increased predation on native birds (Murphy et al. 2001). This raises the need for further research on primary prey thresholds at which prey switching by predators occurs.

Reliability of results

The most important assumption of any experiment is that treatments are independent. In this experiment the study sites were well separated spatially, but the ques- tion of temporal independence must also be addressed. Higher predation rates recorded during the second set

OIKOS 102:1 (2003) 63



Elijah

Highlight

of treatments may be indicative of some type of learned response by predators. Such a response would suggest that temporal dependence between the first and second runs of the experiment had occurred. Predation rates have been shown to increase in some experiments with subsequent trials in the same sites (Goransson et al. 1975, Yahner and Wright 1985). An alternative explanation is that this apparent time-effect arose by chance from the order of allocation of treatments and the effective absence of useful data from one site. Compari- son of daily egg removal rates (Fig. 2) indicates that the latter is likely to have been the cause: at two of the three sites daily egg loss rates declined between the first and second set of treatments. This suggests that no learning effect occurred and that temporal pseudoreplication (Hurlbert 1984) was avoided.

Other assumptions in design were that eggs were equally attractive to all predators, egg loss is due to predation and that natural localised variations in burrow density do not influence predation rate.

Whilst the quasi-natural experimental design used here was intended to investigate patterns of predation and not as a measure of natural rates, it is of value to note that rates of egg loss were considerably higher than those recorded for real nests at two of the sites used in this study for which data on natural predation rates are available (Table 6). A number of studies have recorded higher predation rates during artificial nest experiments compared to the natural systems that they attempt to simulate (Storaas 1988, Reitsma et al. 1990, Wilson et al. 1998). The responses of predators to artificial nests may be quite different from those to natural nests, where such factors as researcher activity and variable ecological conditions, including the presence and behaviour of parent birds, may affect quanti- tative results in various ways (Major and Kendal 1996, Ortega et al. 1998, Zanette 2002). In this study these differences may simply be a result of the different prevailing ecological conditions (such as different predator or primary prey abundances) between spring, when sooty shearwater eggs are present, and late au- tumn when this experiment took place. The differences may also reflect the design of the experiment. For example, eggs were placed approximately 20 cm inside burrows which is likely to make them easier for preda-

tors to detect and remove than in natural nests, where nests may be up to 2 m from the burrow entrance (pers. obs.). The presence of a parent bird may also act as a deterrent to egg predation.

Synthesis and management implications

Whilst larger colonies may attract more attention from predators or induce ARS type behaviour, the net effect of increasing colony size was to lower individual risk of predation. The larger number of individuals present served to effectively "buffer," or dilute, per-capita predation risk from predators whose numbers are fixed by extraneous factors: chiefly the abundance of their primary prey. Although eggs were removed more slowly from smaller colonies, each loss had a greater per- capita effect on individual mortality risk. The two effects described here are not necessarily mutually ex- clusive as real threats to prey populations are likely to depend on a number of possibly conflicting factors. This experiment should be repeated using less densely packed prey aggregations to remove the density dependent effects of clumped prey distribution on predation risk. It may be predicted that an inverse density dependent relationship would result and that this would be stronger than that found in this study.

This study gives provisional support to the hypothesis that predation on secondary prey is inverse density- dependent at low densities. Predator dynamics are therefore not directly dependent on the abundance of these prey. This situation exists in Australia and New Zealand where introduced predators depend on other introduced mammal species as primary prey. Under these circumstances predators will respond in a density dependent manner to their primary prey. Control of primary prey populations may therefore be as important as predator control as a management tool. More work is required on the relationship between predator: primary prey ratios, thresholds for prey switching and subsequent effects on valuable secondary prey populations. Under these circumstances control of primary prey must be carefully timed so as not to stimulate prey-switching at times of the year when threatened populations are at their most vulnerable such as early in the breeding season.

Table 6. Comparison between experimental and real daily loss rates of eggs at Nugget Point and Sandymount sooty shearwater colonies (based on data in Lyver et al. (2000) and the author's unpublished data). "Season" refers to breeding season. For real egg loss rates data cover the period from just after laying (early Dec.) to soon after hatching (late Jan.) and thus may include some effect of early chick survival.

Colony Nugget Point Sandymount

Season/treatment 1994-95 1995-96 1997-98 Ni N2 1997-98 S1 S2

Initial number 86 93 8 120 30 19 90 60 Days 68 70 55 10 10 20 10 10 Daily loss rate 0.72 1.00 0.05 8.5 3.0 0.95 7.1 5.9

64 OIKOS 102:1 (2003)



Temporarily abundant eggs and chicks may not represent a primary resource for long-lived mammalian or avian predator guilds. In such situations where small breeding populations are under threat, even from naturally occurring incidental predation, use of density- dependent predation models may be of conservation value.

Acknowledgements - I would like to thank Harald Steen and Henrik Moller for their guidance throughout. Grant Norbury also made valuable comments on an earlier draft of this manuscript. Chris Jacobson, Fiona Kemp, Karin Ludwig, Chris O'Kane and Ilka Sdhle helped set up the field sites This work could not have been carried out without the financial support of the University of Otago Department of Zoology.

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