ECOGRAPHV 21: 4S4-494. Copenhagen 1998

Breeding habitat selection and larval performance of two anuransin freshwater rock-pools

Anssi Laurila

Laiirila, A. 1998. Breeding habitat selection and larval performance of two anuransin freshwater rock-pools. - Ecography 21: 484 494.

I studied breeding habitat choice of common toad Bufo bufo and common frog Ranatemporaria in 221 freshwater rock-pools on 15 small islands in the southwestern coastof Finland. I monitored tadpole growth rate in a number of rock-pools differing insize, competitors and predator regime. Furthermore, I carried out a short-term fieldexperiment to investigate the efTeets of different predators on larval survival. Ranabred in pools of virtually all sizes, although ihe very smallest ones were usuallyavoided. A logistic regression analysis showed that the amount of aquaticmacrophyte vegetation and pool surface area were the most important pool charac-ters for Rana. Bufo preferred the largest pools, and pool surface area was by far themost important habitat variable. Rana avoided pools with the lowest pH. but wasmore common than expected at pools with pH around 6. In Bufo such an effect wasnot found, but this may he due to relatively low numher of pools occupied hy Bufo.In Rana there was a positive correlation between pool area and tadpole body lengthin early June, but two weeks later this relationship was not significant. In Bufotadpole body size was not significantly affected by pool area. Presence of predatorsor presence of the other tadpole species did not affect growth or tadpole body size ineither Rana or Bufo. A short-term experiment in wading pools indicated that bothspeeies suffered heavy mortality in the presence of a diving heeile larva. In thepresence of predatory fish, mortality of Bufo did not differ from controls, whereasmortality was high among Rana tadpoles. It appears that although predators preyheavily on Runa tadpoles, they do not exclude Rana from larger rock-pools.However, it is not evident from this study why Bufo avoids smaller pools.

A. Laurila (anssi.laurila@helsinki.fi), Depl of Ecology and Systematics. Div. oj Papula-lion Biology. P.O. Bo.x 17. FfN-00014 Unii. of Helsinki, Finland.

Hydroperiod atid predation have been acknowledged as ability (Woodvt'ard 1983. Wellborn et al. 1996). How-major structuring forces of aquatic communities ever, high activity levels increase predation risk (Sih{Collins and Wilbur 1979, Wiggins et al. 1980, Skelly and Moore 1990, Skelly 1994), and species living in1995a, 1996, Schneider and Frost 1996, Wellborn et al. predator-rich permanent ponds are predicted to have1996, Corti et al. 1997). Small temporary ponds contain lower activity levels (Woodward 1983, Wellborn et al.less predators but run a risk of desiccation. Large 1996).

ponds and lakes do not desiccate but harbour a rich Amphibians breed in a wide variety of freshwaterpredator fauna. Because natural selection favours dif- habitats. To maximize its fitness a breeding amphibianferent behavioural and life history traits in different should reproduce in a habitat that maximizes larvalhabitats, desiccation-predation risk gradient has pro- survival and quality. Amphibian tadpoles respond tonounced impact on the structure of animal communities variation in environmental conditions with remarkable(Wellborn et al. 1996). Developmental rate is of crucial phenotypic plasticity in larval life history traits (Wilburimportance in temporary ponds and, consequently, and Collins 1973. Newman 1992). Also presence ofthese habitats favour high activity level and competitive predators and competitors may affect larval perfor-

Accepted 5 March 1998

Copyright © ECOGRAPHY 1998ISSN 0906-7590Printed in Ireland - all rights reserved

484 ECOGRAPHY 21:5 (1998)

mance (Skelly 1992. 1995a, Werner and Anholt 1996).Time of and size at metamorphosis are largely depen-dent on larval growth rate (Wilbur and Collins 1973).Size differences at metamorphosis persist through laterhfe, and because reproductive success is size-dependentin amphibians, eariy metamorphosis at large size mayincrease reproductive success as a breeding adult(Berven and Gill 1983, Smith 1987, Semlitseh et al.1988). Because between-habitat differences in growthrate may be reflected as differences in fitness of adultindividuals, measurement of larval growth rate in dif-ferent ponds may provide information on performancenot only in larval habitat but also as adults.

It has been postulated that tadpoles living alonghydroperiod-predation gradient should differ in theicbehaviour from species living in more temporary poolsby being more active and susceptible to predation(Woodward 1983, Werner and McPeek 1994, Skelly1995a, 1996. Wellborn et al. 1996). Common frog Ranatemporaria, hereafter Rana and common toad Bufobufo, hereafter Bufo tadpoles differ markedly in theirability to cope with different predators. Rana is takenby all predators large enough to capture them, but Bufois unpalatable to most vertebrate predators (e.g., Lard-ner and Loman 1995). However, insect predators preyreadily on Bu.fo (Lardner and Loman 1995, Laurila etal. 1997). The species also differ in their antipredatorbehaviour: Bufo is more active and responds to preda-tors mainly by shoaling whereas Rana lowers its aetivitylevel and avoids predators spatially (Laurila et al. 1997,1998, Watts et al. 1997).

In this study I describe breeding habitat selection ofthese two species in an archipelago of roeky islands andskerries in the northern Baltic. This area provides agood opportunity to study breeding habitat selection,because the anurans breed in freshwater rock-pools thatdiffer widely in their biotic and abiotic characters (e.g.Ranta 1982). I examined whether habitat selection ofthese species is in accordance with the habitat gradienthypothesis. Specifically, as a species palatable to widerange of predators, Rana should be constrained tosmall pools without predators whereas Bufo should befound more often in large pools with predators. Toinvestigate whether pool size affects tadpole perfor-mance, I monitored growth rate of the tadpoles indifferent-sized pools. Because obtaining comparablesurvival data from different-sized pools is very difficult(e.g. Wilbur 1984), I carried out a short-term experi-ment in wading pools to compare the vulnerabihty oftadpoles to different predators in a structurally simpleenvironment resembhng small rock-pools.

Methods

Rana lemporaria and Bufo bufo are the most wide-spread and common anurans in northern Europe. Both

species are 'explosive" breeders (Wells 1977) and in mystudy area breeding occurs in late April-early May.The peak spawning in Bufo usually occurs about aweek later than in Rana (unpubl.). Besides smooth newtTriiurus vulgaris., no other amphibians occur in thestudy area. Moor frog Rana arvalis breeds on severallocations in the nearby mainland (the nearest sites are< 2 km from the study area), but during several yearsof intensive study I have never found it on any of mystudy islands.

The study area lies in the vicinity of TvarminneZoological Station, Hanko, southwestern Finland. Itconsists of a number of small rocky islands and sker-ries. On larger islands there are pine forests, but smallerskerries and islands further away from the mainlandlack forests and vegetation consists mainly of grassesand junipers. A considerable proportion of eaeh islandis bare bedrock. For further information on islandvegetation, see Pokki (1981).

In the study area the anurans breed in rock-pools,depressions in the bedrock filled with water. The rock-pools lie near ( < 50 m) the shoreline in areas of openterrain with bare bedrock and low grass-dominatedvegetation. Pools very close to shoreline get some oftheir water from the sea but those further off the shoreget their water exclusively by precipitation. Most largerpools support aquatic macrophyte vegetation, butsmaller pools usually lack vegetation, and a thin layerof sediment and scattered stones are the only elementsof structural complexity. For further information onthe rock-pool system, see Ranta (1982) and referencestherein.

Census methods

Each Rana female lays only one clump of eggs perseason (Savage 1961). As the egg clumps are distinctand easy to count I was able to estimate the number offemales reproducing in each rock-pool. Occurrence ofBufo reproduction was assessed by the presence of eggstrings or tadpoles. However, when several females laytheir eggs in a restricted area (as is the case in manyrock-pools), counting the egg strings (breeding females)afterwards is impossible. I was therefore not able toestimate the number of breeding Bufo females in therock-pools.

I recorded breeding habitat choice of Rana and Bufoin 221 rock-pools on 15 islands during 1993-1995.Characters of the study islands are presented in Table1. Fourteen of the islands had breeding Rana in 1993-1995 and the remaining one (Isskar, Table 1) hadbreeding population in 1994-1995. The pool occupancypattern was recorded during all the three years. In BufoI used pool occupancy data only from years 1993 and1995 as the survey of tadpole period was incomplete in1994. A potential factor that may affect the distribution

ECOGRAPHY 31.5 (1998) 485

of Bufo in this study is that the islands were selected onthe basis of occurrence oi' Rana. and Bufo simply couldnot have colonized some of the islands. Hovi'ever. this isa realistic possibility only in the island oi Spikarna(Table 1) which is separated from the nearest Bufopopulation by I km of open sea. From other islands thedistance to the nearest occupied island varies between50 and 600 m (average distance 204 m). Furthermore,results of an analysis performed with data consistingonly of islands occupied by Bufo did not differ qualita-tively from the whole data set.

The anurans reproduce extremely seldom in poolsvery close to sea probably because of high salinity inthose pools. Pools with marine algae (e.g. Entero-morpha sp.) were therefore not included in the analysis.Also the very smallest and most ephemeral pools (depth< 5 cm) were not included, mostly because they hadvery little water in May after relatively snowless wintersin 1993 and 1995.

The habitat variables were scored in May after bothspecies had spawned. The described pool charactersincluded maximum pool area, maximum pool depthand percentic coverage of aquatic vegetation on poolbottom. Pool pH was always measured from at least 30cm from pool shore or macrophyte vegetation by indi-cator paper. Presence of predators (smooth newt, fishes,large predatory insects) was assessed by visual inspec-tion in smaller pools but in larger pools and in poolswith vegetation sweep net samples were taken. 1 con-centrated on physical and biolic characters, becauseprevious studies had indicated that water chemistrydoes not have much effect on habitat choice in thesespecies (Strijbosch 1979. Aston et al. 1987).

The presence of the anurans in relation to habitatvariables was analysed by logistic regression analysis.In the analyses, a rock-pool was considered occupiedby the species if spawn or tadpoles were found in one ofthe study years. Similarly, the occurrence of predators

was analysed with logistic regression. After an initialscreening of the variables, pH was omitted from theanalyses, both because of low significance it achievedand since it was unlikely (hat the effect would bedetected by an average-related method (pools with lowand high pH are both likely to be avoided). Because pHhas been shown to affect breeding habitat choice (Strij-bosch 1979) and larval performance (Cummins 1989,Beattie and Tyler-Jones 1992), I analysed the effects ofpH on breeding habitat selection of the anurans inde-pendently of other habitat characters.

Tadpole growth in rock-pools

At two-week intervals in May-June 1995 I monitoredthe growth of Rana and Bufo tadpoles in a number ofrock-pools. The pools were selected in such a mannerthat the whole size range of pools used by both specieswas included. Pool pH varied between 5 and 7. In 1995none of these pools dried up until late July. Initially, Imeasured growth of Rana in 25 and growth of Bu.fo in14 pools (in total 32 pools). However, in June I wasonly able to obtain samples from 21 Rana pools and 11Bufo pools (in total 27 pools) because of high naturalmortality of tadpoles in some of the pools. In mostcases not a single tadpole was found in early (in thecase of Rana) or mid-June {Bufo) although tadpoleshad been present two weeks earlier. Most of these poolssupported high densities of predators and predation isthe most likely reason for the disappearance of thetadpoles.

A sample of tadpoles was caught with a sweep-net.The tadpoles were then transferred to a plastic boxfilled with 2-3 mm of pool water, photographed andreleased back in their natal pool. The snout-vent bodylength (from the tip of the snout to the base of the tail)of the tadpoles was measured from the photographs

Table I. Characters of the study islands. Pool size refers to pool surface area. Number of Rana spawn clumps refers to averagevalue in each island during 1993 1995. Occurrence of predators: A = absent, P = present.

Island

BrannskiirFuruskarSkallotholmenL^ngskarL^ngskar StorgrundetMeilanskarLillhamnVindskarIsskarSpikarnaYastra HamnskarOstra HamnskarPorskarNorra PorskarVargskar

Islandarea (ha)

13.012.67.9

22.01.4

12.03.2

15.62.22.85.62.4

22.41,83,4

Total numberof pools

2521

2361213

117

113141039

710

Median poolsize (m-)

67.5

168

1010

12008

500202012.5166

Largestpool (m-)

354818

15003650

1200104500

506420

375220

50

Pools <3CCU-

pied byRana

1482

25561

1114

124

27

5

Bufo

0103001I1000

II01

Rana spawnclumps

16.311.75.7

93.713.74.0

15.052.04.0

11.336.0

7.7131.313.735.0

Newt

APPPAAAPPAPAPAP

Fish

APAPAAPAAPAAPAA

Insect

APAPAAPPPAAAPAA

486 ECOGRAPHY 21:5 (I99R)

Table 2. Habitat characters used for describing the presence of a) liana and Bufo and b) newt, iish and insect predators inrock-pools.

a)

Character

RanaPresent Absent

BufoPresenl Absent

n mean + SE n mean + SE n mean + SE n mean + SE

Area 128 41.25 + 12.22 93 30.73 + 16.50 21 243.76 93,7Max. depth (m) 128 0,38 ± 0,02 93 0.37 ± 0.03 21 0,69±0,!l

128 -0,01 ±0,02 93 0.02 ± 0.02 21 0,07±0.065,9

±0.04+ 0,21

Res, depthAq. veget. ("/>)Rana dens.pH% occupied byBufo I RanaNewtFishInsects

12812899

23.5 ±2,80.20 ± 0.036,15+0,11

939359

8.9 ±2.50.0 ± 0.0

5.18 + 0.20

212120

25.70.156.24

IS22

6

14.117.24.7

17,2

3.21.14.32.2

18103

12

200200200200300138

110137

12

15.10± 1.420.35 ±0,01

-0.01 ±0,0116.5 ±2.10.11 ±0.026.15 ±0.11

55.06,53,56,0

b)

Character

NewtPresent Absent

FishPresent Absent

InsectsPresent Absent

n mean+SE n mean + SE n mean-I-SE n mean ± SE n mean + SE n mean + SE

Area (m-) 23 1]3.9±43,48 198 27,9 ± 9.7 10 294.9±177,7 211Max, depth (m) 23 0,58±0,07 198 0.36±0.02 10 0,74±0,15 211Res, Depth 23 0.05 ± 0.05 198 -0,01 ±0.01 10 0,]7±0,04 211Aq, veget, (%) 23 32,7 ± 5,20 198 15.60 ± 2.10 10 19,10 ± 8,60 211pH 22 5,83 ± 0,18 138 6,20 ± 0,11 10 6,83 ± 0.39 150Rana dcus. 23 0,24 + 0,04 198 0.10±0.02IO 0,16±0,07 211

24.6 ± 5,3 24 218.8 ± 82.9 197 14.7 ± 1,40.36 ±0.02 24 0,66 ±0,09 197 0.34 ± 0.01

-0.01 ±0.01 24 0,07±0,05 197 -0.01 ±0,0117,30 ±2.0 24 34,20 ±5,30 197 15.3 ±2.106,H)±0.10 22 5,89±O.I6 138 6.19±0.110,11 +0.02 24 0,22 + 0,04 197 0.10 + 0.02

with the aid of digitizing equipmetit. 1 measured at least10 individuals from each pool. However, this was notalways possible due to heavy mortality in some of thepools. The measurements used in this study were taken31 May-2 June and 14 -21 June.

For eaeh pool T calculated specific growth rate (SGR)of the tadpoles by using the formula

S G R = 100 X [(In Y . - l n Y | ) / T . - T | ]

where Y2 is the pool-specific average snout-vent lengthduring the second measurement time, Yj is the averagelength at the first measurement time and T; — T, is thetime interval between the measurements. The otherresponse variables analysed were average tadpole bodylength on I and 15 June. Since I was not able to samplethe tadpoles in all the pools during a single day, thevalues were transformed to correspond to these particu-lar dates with the help of specific growth rate. The firstmetamorphs of Rana were observed 15 June. However,in most of the pools metamorphosis started later andthere were plenty oi' Rana tadpoles in 14 of the pools inthe beginning of July. Metamorphosis of Bufo occurredin late June in most of the pools.

In both species Pearson correlations were establishedto examine the relationship between rock-pool surfacearea and tadpole growth and size parameters. Pool area

was log-transformed before the analyses. The data werealso analysed with multivariate analysis of variance(MANOVA) in respect to presence of predators and theother tadpole species. In three of the Rana pools 1 hadintroduced a threespine stickleback Gasterosteus aculeu-tus population for the purpose of another study {Lau-rila and Aho 1997). In other Rana pools predatorsincluded the smooth newt and large predatory insects(odonates. Dytiscus. Notoneeta). Tn Bufo only poolswith insect predators were included in the 'predatorspresent" category.

Predation experiment

Small ponds are difficult to sample quantitatively(Wilbur 1984). and I was not able to produce rehableestitnates of tadpoie survival in the field. Therefore, toinvestigate the vulnerability of the tadpole species todifferent predators I carried out a short-term experi-ment in opaque wading pools (diameter 160 cm, height25 cm). The wading pools were arranged in three blockson the shore cliffs of the island of Langskar, The poolswere filled with 15 cm water from a near large rock-pool, and 20 g of rabbit pellets were added as food forthe tadpoles. No refuge was available for the tadpoles,and the setting thus resembled small rock-pools withoutany structural complexity. The pools were stocked with

ECOCiR.APHY 21:5 487

either 100 Rana tadpoles [mean weight 0.086 + 0.026(SE) g. developtnental stages 26-29 (Gosner I960),n - 2 0 ] or 100 Bufo tadpoles (mean weight 0.090 ±0.029 g, developmental stages 25-28. n = 20). Thetadpoles, originating from four egg masses in bothspecies, had been collected from natural rock-pools aseggs and raised in the laboratory. I let the tadpolesget accustomed to the wading pools for eight hoursbefore introducing the predators. Each pool either re-ceived one perch Perca fiuuiarilis [mean length214.5 + 8.4 (SE) mm. n = 6], one late-instar larva ofthe diving beetle Dytiscus marginali.s [mean length53.5 + 2.2 mm. n ^ 6], or served as a predator-freecontrol. These species are representative top predatorsin invertebarte- (D. marginalis) or fish-dominated(perch) aquatic communities. Perch docs not occur inthe study pools, but it is the most important fishspecies in small forest lakes in Scandinavia (e.g.Sviirdson 1976) and Rana tadpoles avoid it be-haviourally (unpubi.). The perch used in the experi-ment had been caught from the Baltic Sea with gillnets. Dylixcu.s margiualis is on^ of the most commoninsect predators in the study area and the larvae usedin the experiment originated from rock-pools in thenearby archipelago. Two days after the beginning ofthe experiment, I removed the predators and countedthe number oi' surviving tadpoles.

The experiment was a 2 x 3 factorial design withtadpole and predator species as treatments and threereplicates resulting in eighteen experimental units. Inone of the Rana-con\Yo\ pools I found several late-in-star damselfiy (Cocnagrionidae) larvae that apparentlyhad reduced the survival of tadpoles. This unit wasexcluded from the analysis. The survival values werearc-sine transformed before the analysis.

Results

Breeding habitat use

Over half of the investigated rock-pools (57.9%) wereoccupied by Rana (Table 2). Logistic regressionshowed that the most important habitat variable forRana was the amount of aquatic macrophyte vegeta-tion (Table 3). Pools with vegetation had breedingRana with a higher probability than pools withoutvegetation (Table 3, Fig. 1). However, Rana also bredcommonly in pools without vegetation (Fig. I). In-creasing pool surface area had a positive effect on theoccurrence of Rana (Table 3, Fig. 1). There was alsoa trend towards positive association between occur-rence of Rana and newts. The other variables did nothave significant effects (Table 3).

By contrast, only 9.5%> of the pools were inhabitedby Bufo. Bufo clearly preferred rock-pools with thelargest surface area (Tables 2, 3, Fig. 2) and surfacearea was the only significant habitat variable in thelogistic regression analysis (Table 3). There was anonsignifcant positive relationship between Ranaspawn clump density and occurrence of Bufo (Tables2, 3, Fig. 2).

All predator types preferred large pools (Table 2).However, logistic regression analyses revealed that inboth newt and insect predators the most importanthabitat variable was the presence of the other preda-tor type indicating a strong positive association in theoccurrence of the two predator types (Table A). Afterthe other predator type had been removed from themodel, pool area became the most important habitatvariable for both insects and newts. Interestingly, theoccurrence of both newts and insect was positivelyaffected by Rana density (Table 4). Pool depth was

Table 3. Results of logistic regression analyses for effects of rock-pool characters on pool oecupancy by a) Runa and b) Bufo.

a)Predictor variiiblo

Pool areaMax. depthAq. veget.BufoFishNewlInsect

b)Pool areaMax. depthAq. veget.Raua densityFishNewtInsect

CoelTicient

0.839-0.870

0.9400.647

-0.7502.1440.348

2.7611.221

-0.6851.942

-1.0940.4171.121

P

0.0420.2710.0140.3770.4010.0690,717

0.0040.4640.4220.1850.4020.6660.250

Odds ratio

2.320.422.561.9!0.478.531.42

15.813.390.506.970.331.523.07

95"/! Confidence intervalLower

1.030.091,2!0.460.080.850.36

2.440.130.090.390.030.230.45

limitsUpper

5.191.985.428.012.72

85.709.32

102.4889.31 •2.68

123.204.32

10.1320.71

488 liCXXiRAPllY 31:5 (I'WK)

a)

95H0)CTI

IbCC

£

o

o o0 o o

oO O Qj o

66 <Q>o

oCD

cP

o o

- 1 0 1 2 3Log pool surface area

1 2 3 4Log pool surface area

Fig, I. Percentage coverage of aquatic macrophyle vegetation(jittered values) in relation to log-transformed pool surfacearea, a) Pools with Rana, b) pools without Rana.

the only significant habitat variable affecting occur-rence of fish, deeper pools having fish with greaterprobability (Tables 2, 4).

Higher proportion of the pools inhabited by Bufohad newts (47.6 vs 17.2%, x^ = 9.91, DF = 1, p - 0.002,Table 2) or insect predators (57.1 vs 17.2%: x^ = 16.35,DF = 1, p < 0.001, Table 2) than the pools inhabited byRana. This reflects Rana\ tendency to occur in smallerpools than Bufo and could be taken as evidence foravoidance of pools with predators. However, occur-rence of newts and insects was positively associatedwith Rana density (Table 4). Thus, although Rana andpredators coexisted in relatively few pools, there weremore reproducing Rana females per unit area in thosepools. Only ten pools were inhabited by fish and bothanurans were found in some of those pools (Table 2).There was a trend towards fewer pools with fish beingoccupied by Rana than Bufo (x~ = 2.93, DF = 1, p =

0.087, Table 2). Another feature related to pool sizewas that 85.7'Mi of the pools with Bufo supported alsoRana, whereas only 17.2% of the pools occupied byRana were also inhabited by Bufo (Table 2).

Pool pH affected occupation pattern in Rana (Table5, j^2= 14.54, DF=-5, p = 0.013). Rana avoided poolswith lowest pH, and an excess of pools was occupied atpH 6 (Table 5). In Bu.fo pH had no effeel on pooloccupancy (Table 5, X--7.04, DF = 5, NS). However,relatively low number of the pools were inhabited byBu.fo. Pool area and pH were not correlated (r =-0.045, n - 160, NS).

Tadpole growth and survival

Specific growth rate of the tadpoles was not affected byrock-pool surface area in either species {Rana: T =-0.189, D F = 1 9 . Bufo: r = 0.277, DF = 9, both NS).Body length of Rana was positively associated withpool area in early June (Fig. 3, r — 0.447, D F = 1 9 ,p < 0.05) but in mid-June this relationship was nolonger significant, although still positive (Fig. 3, r =0.272. NS). In Bu.fo body size was not significantlyassociated with pool area (Fig. 4, early June: r =-0.067. mid-June: r = 0.279, DF - 9, NS in bothcases). Neither occurrence of predators or the othertadpole species affected growth nor body size of theRana or Bufo tadpoles. However, variation betweenpools was substantial (Figs 5 and 6, Table 6).

In the wading pool experiment both tadpole species(Fi.9 = 58.556, p < 0.001) and predator treatments(F2,9= 100.328, p < 0.001) had a significant effect ontadpole survival (Fig. 7). Rana tadpoles suffered somemortality also in the control pools whereas the survivalof Bufo was excellent in those pools. Survival of Bufo

0.95

0.7

cn

I 0.45p

0.2-

-0.05

o o

- 1 0 1 2 3 4Log pool surface area

Fig. 2. Occurrence of Bufo m relation to pool surface area(log-transformed data) aud Rana density (number of eggclumps m " - pool surface area, jittered values). Open symbols:pools without Bufo, closed symbols: pools with Bufo.

ECOGRAPHY 1\:5 (1998) 489

Table 4. Results of logistic regression analyses for effects of rock-pool characters on pool occupancy by a) smooth newt, b) fishand c) insect predators.

a)Predictor variable Coefficient Odds ratio 95'^ Confidence interval limits

Lower Upper

Pool areaMax. depthAq. veget.BufoRana densityFishInsect

b)Pool areaMax. depthAq. veget.Bu/oRana densityNewtInsect

c)Pool areaMax. depthAq. veget.BufoRana densityFishNewt

1.3540.2760.4730.0062.162

-1.2923.773

0.0346-0600,171

-0.5211.634

-0.0700.519

1.6364.0001.1101.1412.612

-0.7643.628

0,1690.8900.5770.9950.0290.351

< 0,001

0.9720.0080.8570.6700.1770.9520.701

0.1350.1700.2070.2440.0420.595

< 0-001

3,871,321,601,018,690,27

43,52

1,03428,29

\.\90,595,120,931,68

5,1422,19

3,033,13

13.630,47

37,64

0.560.030-300.151,250,029.24

0,164,970,180,050,480,100,12

0,6(10,260,540,46i , i n0,038,49

26.6565.81

8,466.79

60,524,15

204.98

6,6436872.82

7,616,53

54.879,07

23.82

43,991864,80

17,0521,39

169,087,80

166,99

tadpoles were not affected by perch, but survival ofRana tadpoles was ca 1/8 of that in the control treat-ment. However, both tadpole species stiffered high mor-tality by larval D. marginalis (Fig. 7), This difference invulnerability resulted in significant species x predatorinteraction (F.y-18,534, p-O.OOl).

Discussion

The most striking difference in breeding habitat choicebetween the two anurans is that in pool size, Ranabreeds in pools of almost all sizes whereas Bufo clearlyprefers the largest pools (Figs 1. 2). A larger proportionoi" pools occupied by Bufo also supported predators incomparison to pools occupied by Rana. In addition, inthe wading pool experiment the survival of Rana wasvery low in the presence of both predator types,whereas Bufo was preyed only by insect predators (Fig.7). As the more vulnerable species Rana reproducesmore often in smaller rock-pools and as larger poolsare more often inhabited by predators, habitat gradientseems to some extent affect habitat selection of theanurans. However, Rana was abundant also in largerpools. Partly this may be due to the relatively lownumber of very large pools in the pool sample: fewpools had fish which have been considered as the mostefficient predators of temporary pond atnphibians (e.g,Collins and Wilbur 1979, Woodward 1983, Wellborn etal. 1996),

That predators can effectively reduce the numbers ofRana tadpoles is evident also from the tadpole perfor-mance study in natural rock-pools: in all four caseswhere tadpoles disappeared the pools had rich predatorpopulations. Additional field observations indicate thatmortality was not exceptionally severe in 1995. butRana reproduces in these pools each year with relativelyhigh density (on average 0.413 egg clumps m"^ poolarea in 1993-1995), Thus, despite high tadpole mortal-ity breeding Rana females do not avoid rock-pools withpredators (see also Laurila and Aho 1997). Similarly,spawn clump density was positively related to the oc-currence of newt and insect predators indicating thatRana commonly co-occurs with these predators. How-ever, survival seems to be better in smaller pools with-out predators and it is possible that migration fromthose pools is necessary to maintain the breeding popu-lations in predator-rich pools (see also Gill 1978, Ire-land 1989, Semlitsch et al. 1996),

Aquatic vegetation was the most important habitatvariable that affected habitat choice by Rana. Twoexplanations may account for this pattern. First, vege-tation provides cover against predators (e.g,, Werner etal, 1983. Folsom and Collins 1984, Babbitt and Jordan1996, but sec Denton and Beebee 1997). However,although vegetation may sometimes increase the proba-bility of survival within a pool, at between-pool level itmay increase the incidence of predators (Demon andBeebee 1997). Second, aquatic macrophyte vegetation isnot able to persist in ephemeral pools and therefore its

490 ECCXiRAPHY 2!:5

Table 5. Rock-pool occupancy by the anurans at different pH levels.

pH range

3.5-4.494.5-5.495.5-6.496.5-7.497.5-8.498.5-10.5

Total no of pools

935523421

9

Ranapresent

2224023104

"/,

22.262.876.967.647.644.0

Bufopresent

02

10440

0.05.7

19.2n.819.00.0

presetice itidicates low risk of desiccation. Pools withlow desiccation risk should be preferable, though Ranaalso breeds in smaller pools where prolonged dry spellsin early summer cause high mortality among the tad-poles (unpubl.).

Bufo strongly preferred large pools. Since largerpools support more predators, unpalatability of Bufotadpoles may allow them to exist in predator-richpools. However, in two of the three cases where Bufotadpoles disappeared, the pools supported dense popu-lations of larval D. marginalis. This suggests that insectpredators sometimes reduce markedly survival of Bufo.Pools rich in aquatic vegetation support insect preda-tors at higher densities which may thus increase mortal-ity of Bufo tadpoles (Denton and Beebee 1997). On theother hand, fish may enhance their survival as theyreduce the numbers of invertebrates but do not prey onBufo tadpoles (Werner and McPeek 1994. Denton andBeebee 1997).

Body size of Rana tadpoles was positively correlatedwith pool size in early June. In mid-June this relation-ship was still positive but no longer significant. Inamphibians large metamorphs have increased fitness(Berven and Gill 1983, Smith 1987, Semlitsch et a!.1988) and tadpoles originating from larger pools maytherefore survive better and have higher reproductivesuccess. Also in Bufo correlation was positive, althoughnot significant, in mid-June suggesting that also Bufotadpoles may fare slightly better in larger pools.

Tn this study occurrence of predators or the otheranuran species did not affect tadpole growth rate orbody size. It has to be kept in mind that it may bedifficult to detect such effects from non-experimentalfield survey data where factors like resource availabihtyand hatching date inevitably remain uncontrolled andexperimentation is needed to solve their importance inthis rock-pool system. The importance ol" predation andcompetition on tadpole performance has recently beenaddressed in several field or artificial pond experimentswhere differences in pond or resource quality have beencontrolled for (e.g. Skelly 1992, 1995a. b. Smith andVan Buskirk 1995. Werner and Anholt 1996). Theyhave usually emphasized the role of predation andrevealed only weak effects of interspecific competi-tion on tadpole performance {Skelly 1995a, b, Smithand Van Buskirk 1995. but see Werner and Anholt1996).

As Bufo tadpoles are generally more active thanRana (Laurila et al. 1997) they may be better competi-tors as well (Woodward 1983). Competition seemstherefore an unlikely explanation for why Bu^fo avoidsthe smaller pools. Bufo tadpoles could be sensible tocatastrophic mortahty by desiccation and thereforeavoid breeding in small pools. However, there is not

a)20 n

EE

10-

oCO

b)20-1

10-<1)

oc

CO

I r0.5 1 1.5

1 I

2 2.5

0.5 1 1.5Log pool area

2.5

Fig. 3. Snout venl-length of Rana uidpoles in relation torock-pool surface area in early a) and mid-June b).

ECOGRAPHY 21:5 491

a)20 n

Z 10-

oc

b)20 n

EE

>ZJ

oCO

10-

0 1 2 3 4Log pool area

Fig. 4. Snoul vent-lenglh of Bujo tadpoles in relation lorock-pool surface area in early a) and mid-June b).

much difference between the species in length of larvalperiod in laboratory conditions (Laurila et al, 1998).Also in this study metamorphosis was quite syn-chronous in the two species. Clearly, an experimentalapproach is needed to settle why Bufo avoids smallpools.

In the initial analyses pH did not affect breedinghabitat choice of the anurans. However, when theeffects of pH were analysed separately Runa seemed toavoid rock-pools with low pH. This was expected,because pH below 4.5 has been found to increasemortality of Rana embryos and affect larval growthand development negatively (Cummins 1989, Beatticand Tyler-Jones 1992). Interestingly, there seems to be

variation between Rana populations in this respect.Strijbosch (1979) reported that Rana avoided reproduc-tion in ponds with low pH whereas Aston et al. (1987)found no such evidence. Breeding habitat choice in apopulation may be affected by environmental quahty

>

o

b)

(D

O)

O

CO

c)

CD

D)

oc

CO

4n

3

2

1

12-

8-

4-

.- 16-

12-

8-

4-

0

Absent Present

10 11 16 5

1^ 11

TT

T

T

T

Predators BufoFig. 5. Average specific growth rate a) and body size b, c) ofRana tadpoles in rock-pools with or without predators andwith or without Bufo. Error bars denote upper 95% confidencelimit. Number of pools in each category are given in a).

492 ECOGRAPHY 21:5 (1998)

a)10n

15 8H(U

0) 6 -o

s? 4 -

o6b)

CD

0)

(U

O

c

C)

CDLO

D)

O

2-

12n

8-

4 -

16n

12-

— ft-

>• ^ 4

0

Absent Present

3 8 3 8

1 1

TT

T

T

Predators RanaFig. 6. Average specific growth rate a) and body size b, c) ofBufo tadpoles in rock-pools with or without predators andwith or without Rana. Brror bars denote upper 95% confi-dence limit. Number of pools in each category are given in a).

and available alternative breeding habitats. For in-stance, in Bufo calamila the relative importance ofchemical, physical and biotic factors in breeding habitatchoice differs in different environments and betweenpopulations (Banks and Beebee 1987). There is also

Table 6. MANOVA tables for effects o'i presence of predatorsand the other tadpole species on growth of Rana a) and Bufob) tadpoles.

Source DF Wilk's /. F

PredatorBufoPredator x Bufv

3.153,153.15

0.8490.7930.842

0.8891.3020.936

0.4690.3100.448

PredatorRanaPredator x Rana

3,53,53,5

0.7240.3890.696

0.6342.6191.160

0.6250.1630.411

0 8-

0 6 -

0.2-

0

D Rana 0 Bufo

Predator: None Perch Beetle larva

Fig. 7. Effects of predators on average survival of Rana andBufo tadpoles. Error bars denote I SE.

some evidence for genetic differences between popula-tions in tolerance for low pH {Beattie and Tyler-Jones1992. Pierce and Wooten 1992). Whether the mecha-nism for avoidance of low pH pools is active choice bybreeding adults or repeated failure of recruitment ispresently not known. However, in my study area thelarge number of available pools in most islands maypromote behavioral avoidance oi low pH pools.

Acknowledgements - Tvarminne Zoological Stcitlon kindlyprovided access to part of the study area and the transportdevices. J. Kujasalo helped with the predation experiment andH. Rita gave advice on statistics. Earlier drafts of themanuscript benefitted by comments of T. Aho, P. Eklov. P.Edenhamn, H, Hirvonen, N. Peuhkuri and E. Ranta. Thisstudy has received financial supporl from the Univ. of Helsinkiand the Acadetny of Finland.

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