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Factors influencing the timing of spring migration incommon toads (Bufo bufo)H. Arnfield1, R. Grant2, C. Monk3 & T. Uller1

1 Edward Grey Institute, Department of Zoology, University of Oxford, Oxford, UK2 Department of Life Sciences, Anglia Ruskin University, Cambridge, UK3 Hilburn, Chapel Lane, Middleton, Matlock, Derbyshire, UK

Keywords

phenology; amphibian; temperature;breeding.

Correspondence

Tobias Uller, Edward Grey Institute,Department of Zoology, University ofOxford, Oxford OX1 3PS, UK.Email: [email protected]

Editor: Mark-Oliver Rödel

Received 4 December 2011; revised 19April 2012; accepted 24 April 2012

doi:10.1111/j.1469-7998.2012.00933.x

AbstractWe analysed 12 years of data on the spring migration of the common toad Bufobufo L. to breeding ponds across 25 locations in Derbyshire, UK, to determinefactors influencing the number of toads active per night. We also tested whetherthe timing of spring migration is predicted by annual variation in temperatureor precipitation. More toads migrate in warmer temperatures and as the moonwaxes, whereas precipitation did not have a significant effect on toad activity.Across years, spring migration begins earlier in warmer years, but the mainmigration of toads was not predicted by air temperatures before the onset of thebreeding season. Contrary to the majority of studies of amphibian breeding phe-nology, there has been a temporal shift towards later timing of breeding over thepast 12 years. Overall, comparison of our results with that of previous studiessuggests that it can be difficult to generalize about the factors that influencebreeding phenology, even within species. However, as more studies accumulate, itshould be possible to address whether variation in breeding phenology is consist-ently linked to geographic variation in abiotic conditions or species biology, whichwill help to evaluate its consequences under climate change.

Introduction

The timing of breeding is a characteristic with potentiallyimportant implications for individual fitness and populationdynamics. Breeding phenology is expected to show substantialvariation within and between populations and years as a resultof variation in environmental conditions. This is particu-larly true for amphibians, whose activity patterns should bestrongly dictated by climatic variables such as temperature andrainfall. Indeed, several studies have found a significant rela-tionship between rainfall and the timing of amphibian breed-ing (Byrne, 2002; Vaira, 2005; Hartel, 2008; Scott, Pithart &Adamson, 2008), although some studies have failed to find asignificant relationship (e.g. Gittins, Parker & Slater, 1980;Reading, 1998). The potential effect of daily (or nightly) vari-ation in temperature on amphibian breeding activity seems tohave been little explored (but see Byrne, 2002). However, thetemperature preceding the breeding season has been shown toinfluence the timing of breeding, with a number of studiesdocumenting earlier breeding in warmer years (Terhivuo,1988; Beebee, 1995; Blaustein et al., 2001; Reading, 2003; Try-janowski, Rybacki & Sparks, 2003; Sparks et al., 2007;Kusano & Inoue, 2008; Scott et al., 2008; Carroll, Collinson &Beebee, 2009; Neveu, 2009; Phillimore et al., 2010). Indeed,amphibians seem to respond strongly to ongoing climatechange (Beebee, 1995; Parmesan & Yohe, 2003; Root et al.,2003), with average advancement of spring breeding date per

decade being between two and seven times larger for amphib-ians than for other animals and plants for which comparabledata are available (Parmesan, 2007). However, changes inbreeding phenology over time also seem to be unusually vari-able in amphibians (Parmesan, 2007), suggesting that addi-tional factors such as precipitation (Oseen & Wassersug, 2002;Vaira, 2005) and celestial cues (Grant, Chadwick & Halliday,2009) may play important roles.

Here, we use data on toad migration to breeding pondscollected from 25 sites across Derbyshire, UK, to addresswhich factors predict variation in toad activity within andbetween years. In particular, we were interested in whetherdaily variation in temperature and rainfall and the lunar cycleinfluence toad migration. Furthermore, we wanted to testwhether temperatures preceding the breeding season influenceannual variation in the timing of migration and if this hasresulted in consistent changes in breeding phenology acrossyears.

Materials and methodsThe common toad Bufo bufo is widely distributed in Europeand Northern Eurasia (Gasc, 1997). It is highly adaptable andcan be found in both disturbed and undisturbed habitats. Ithibernates in burrows; often quite far from the closest body ofwater. In England, the migration to spawning sites, typically

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still bodies of water, usually occurs after dusk in early spring(Beebee & Griffiths, 2000).

Migration data on the common toad, B. bufo, from 25 sitesacross Derbyshire were obtained from the records of the Der-byshire Amphibian and Reptile Group. The study sites aresituated along roads in a rural landscape, with bodies of waternearby in which common toads are known to breed. Data areheld from 1998 to 2010, except for 2001 when the monitoringwas prevented by an outbreak of foot and mouth disease inthe county, although the number of years of data availablevaries between sites (see Supporting Information Table S1).Members of the public volunteered to patrol back and forthalong the sides of roads which migrating toads were known tocross, from dusk onwards, for a length of time, which, to someextent, varied between nights. Patrols were performed mostlyat night during the common toad migration period, there beingon average 52 days between the first and last patrol, start-ing before the beginning of migration and continuing untilnumbers gathered per night had dwindled to zero, indicatingthe migration was over. Toads were identified by torchlight,collected in buckets and deposited at the breeding pond, inorder to reduce road mortality. Numbers of live and deadtoads were recorded separately, but these are summed to givea total number migrating per night in this paper. Includingdead toads is justified, as fatalities that have been counted areremoved from the road to ensure they are not counted again,which means that any dead toads encountered would havebeen active in the last 24 h. Toads returning back from thebreeding pond late in the migration period are sometimesfound by the volunteers, details of these are noted but notincluded in the total numbers of toads recorded migrating tothe pond. For each location, data are held on the total numberof toads collected each night volunteers went out; the totalnumber of toads recorded across all sites is 110 210. From this,we calculated two estimates of breeding activity for each loca-tion. ‘Onset of migration’ was estimated at each location as thedate at which 5% of the total number of toads recorded hadmigrated. ‘Main migration’ was estimated in a similar way, butusing 50% of the total number of toads recorded at eachlocation as the cut-off. For some sites and years, we also haddata on the number of volunteers searching for toads per siteand night and the time spent searching, which was combinedinto an estimate of ‘search hours’ per night.

Rainfall and maximum/minimum daily temperatures wereobtained from four weather stations across Derbyshire, andthe toad collecting sites were grouped around their neareststation (referred to as ‘region’; see Supporting InformationTable S1). Average temperatures in January and Februarywere calculated from maximum and minimum daily tempera-tures in these months. It was predicted that the average tem-perature in the months preceding migration would influencewhen migration occurred, such that warmer temperaturesearly in the year precipitate the start and peak of breeding, asshown by Beebee (1995), Blaustein et al. (2001), Carroll et al.(2009) and Neveu (2009). As B. bufo migrates to the breedingponds mainly in March and April, with movement sometimesbeginning in February, the average temperatures acrossJanuary and February were used. We also confirmed the

results using the average temperature in February as anexplanatory variable for the timing of breeding activity, assome other studies had used only the month before rather thanthe previous 2 or 3 months (Terhivuo, 1988; Kusano & Inoue,2008); however, as the results stay the same, we only report theresults from the first set of analyses.

Data were analysed using SAS STAT 9.2 (SAS InstituteInc., Cary, NC, USA). The effect of daily temperature andrainfall on the number of toads observed on a given day wastested on log-transformed data [i.e. log(1 + number of toadsobserved per night)]. The data were averaged so that there wasa single data point per day for each of the four weather stationregions, and we included region and year as random effects inall models. All continuously distributed variables were stand-ardized to a mean of 0 and a standard deviation of 1. Becausedaily temperatures naturally increase with date in our sample(r = 0.15, P < 0.001, n = 764), we confirmed our results usinga date-corrected temperature (residual from a regression oftemperature on the number of days since 1 January). As theresults remained qualitatively the same, we only report thedetails from the analyses including daily temperature.

As circular random variables such as moon phase cannot beanalysed using simple linear regression, because of the delimi-tation of the circumference by a closed space and undefinedorigin, periodic regression (also called circular-linear regres-sion) should ideally be used to avoid the adjacent values of0 and 360° being treated as outliers (Hussin, 2007). Periodicregression also results in increased statistical power comparedwith categorical tests (DeBruyn & Meeuwig, 2001). This isrelatively simple to achieve by converting the number of dayssince the last full moon to an angular measurement (f) by theformula f = 2p(t/T), where t is the days of the lunar cycle andT is the period (which in this case is the length of the lunarcycle, i.e. 29.53 days; however, to avoid the problem of having0.53 of a day, the value of 30 was used here). Once convertedto an angular measurement, both the sine and the cosine of theangle can be used in linear regression (along with other pre-dictors if required) to test the effect of moon phase on thedependent variable (SenGupta & Ugwuowo, 2006), which is,in our case, the log of the number of toad arrivals. To furthertest whether lunar phase affected the frequency of migrationpeaks (i.e. the date with the majority of toads migrating foreach site), the lunar days on which the peaks occurred wereconverted to angles as explained earlier. These were plotted ona circular histogram and tested using the Rayleigh test, whichis a circular goodness-of-fit test, where the null hypothesisstates that values are distributed uniformly around the circu-lar space. The software used was Oriana 3.0 (Kovach Com-puting Services, Anglesey, UK).

In the analyses of daily variation in toad migration (PROCMIXED in SAS 9.2.2), we excluded data from 1998 and 2000because it was only available for one of the geographic regions.Estimates were calculated for each location and then averagedacross locations within regions. Because the time spent search-ing for toads showed substantial missing data, we conductedanalyses both with and without including the time spentsearching per night as a factor in our models. We usedmaximum likelihood estimation and ranked models based

Timing of spring migration in toads H. Arnfield et al.

2 Journal of Zoology •• (2012) ••–•• © 2012 The Authors. Journal of Zoology © 2012 The Zoological Society of London

on the second-order corrected Akaike information criterion(AICc) (Burnham & Anderson, 2002).

Analyses of the average date at which 5 and 50% of the totalnumber of toads had migrated were performed using a generallinear mixed model (PROC MIXED) with year and averageJanuary/February temperature and rainfall as fixed effectsand region as a random effect. Because we were interested intrends over time, we included year as a continuous variable inthis model. We confirmed that the results were not biased bysites with a single record by removing them, recalculatingaverages for each region and repeating the statistical analyses.However, here we only provide details from statistical modelsincluding all sites.

Results

Predictors of toad activity during migration

The model with the lowest AICc included (in addition to therandom effects group and year) temperature and the sine ofthe angle of the lunar cycle (Table 1). More toads migrate onwarmer days and from day 7 to day 21 of the lunar cycle. The

parameter estimates for fixed effects indicate that temperaturehas a stronger effect than lunar phase (Table 1). Year andregion each explained only a small proportion of the variance(Table 1). Although the AICc for models including additionalfixed effects (rainfall and cosine of the angle of lunar cycle)were similar to that of the top-scoring model, the parameterestimates for those factors were substantially lower than fortemperature and lunar phase, and their inclusion resulted inonly minor reduction in residual model variance (SupportingInformation Table S2).

Analysis of migration peaks indicated that peak movementsof toads are non-random with respect to moon phase and tendto occur in the waxing part of the lunar cycle, the mean vectorbeing 218, which corresponds to 10 days prior to next fullmoon (Rayleigh test: n = 90, Z = 9.65, P < 0.001; Fig. 1). Fewpeak arrivals occurred in the moon’s waning gibbous phase(between 0 and 7 days after last full moon; Fig. 1).

Long-term trends

The onset of migration occurred significantly earlier in warmeryears (Table 3; Fig. 2). However, there was no effect of thetemperature or rainfall during the preceding months on thetiming of the main migration (Table 3; Fig. 2). Althoughthe January and February temperature did not signifi-cantly influence the timing of the main migration to breedingponds per se, it could, to some extent, contribute to the trendstowards later breeding as the average temperature in January/February showed a significant decrease across the study periodwhen the four regions were combined (r = -0.6105, n = 12, P =0.035). However, separate regressions on data averaged acrossall regions suggested that year explains more variation in thedate at which 50% of toads had migrated than does the averageJanuary/February temperature (average air temperature:-0.28 � 0.303, t = 0.96, P = 0.37; n = 12; R2 = 0.08; year: 0.56 �0.261, t = 2.16, P = 0.05, n = 12; R2 = 0.32).

DiscussionThe results of this study suggest that common toad migrationto breeding ponds in spring is positively influenced by daily

Table 1 Top scoring linear mixed models for the number of toads foundmigrating per day (log-transformed)

Model Deviance AICc

(A) 1 + 2 2215.7 2223.8(B) 1 + 2 + 3 + 4 2040.8 2052.9(C) 1 + 2 + 3 + 4 + 5 2040.3 2054.4(D) 1 + 2 + 3 + 4 + 5 + 6 2039.8 2055.9(E) 1 + 2 + 3 2065.3 2075.4

Variables are coded as follows: (1) Year (random); (2) Region (random);(3) daily average temperature; (4) sine of the angle of the lunar cycle; (5)daily average rainfall; (6) cosine of the angle of the lunar cycle. The firstmodel includes only random effects, the following are ordered fromlowest to highest AICc. For details on the model with lowest AICc(model B), see Table 2. For details on all models, see Supporting Infor-mation Table S2.AICc, corrected Akaike information criterion.

Table 2 Output for the (a) top scoring model in Table 1 (model intercept: -0.060 � 0.0929); (b) the same model including the time spent searchingper night (model intercept: 0.00 � 0.111)

Random effects

(a) (b)

Estimate c2 P Estimate c2 P

Year 0.015 � 0.0131 3.8 0.05 0.066 � 0.0381 20.7 <0.001Region 0.021 � 0.0204 6.1 0.01 0.011 � 0.0138 3.0 0.08Residual 0.834 � 0.0431 0.708 � 0.0448

Fixed effects Estimate � SE ddf F P Estimate � SE ddf F P

Temperature 0.37 � 0.035 745 109.6 <0.001 0.39 � 0.041 465 87.8 <0.001Sine angle -0.16 � 0.034 739 22.8 <0.001 -0.15 � 0.039 513 14.7 <0.001Search time 0.36 � 0.040 484 83.4 <0.001

ddf, denominator degrees of freedom; SE, standard error.

H. Arnfield et al. Timing of spring migration in toads


temperature (independent of time of year), with the lunar cycleshowing a weaker effect. In contrast, we found no evidencethat toad activity peaked on particularly wet days. Acrossyears, the temperature preceding spring predicted the onset ofmigration, but did not affect the time at which 50% of thepopulation had migrated. Instead, there has been a shifttowards later spring migration over the past 12 years, theopposite result to that found by the majority of studies ofamphibian phenology.

Rainfall is an important cue for species breeding in tempo-rary ponds, but it could also be important during migration asamphibians have permeable skin and therefore could be indanger of dehydration in dry conditions. Indeed, rainfall hasbeen found to influence amphibian breeding activity in severalspecies (e.g. Byrne, 2002; Vaira, 2005; Hartel, 2008). In con-trast, our results confirm the lack of effect of rainfall on breed-ing activity in common toads reported by two previous studies(Gittins et al., 1980; Reading, 1998). Species differences in theeffect of rainfall on amphibian breeding phenology probablyreflect differences in species’ breeding patterns and local cli-matic conditions. Specifically, it may not be vital for amphib-

Table 3 Output from linear mixed models with region as a random effect and year, average January and February air temperature and rainfall as fixedeffects

Random effects

(a) 5% of total number of toads migrated (b) 50% of total number of toads migrated

Estimate c2 P Estimate c2 P

Region 0.33 � 0.333(0.09 � 0.153)

6.3(0.7)

0.01(0.40)

0.18 � 0.206(0.01 � 0.131)

3.1(0)

0.08(.)

Residual 0.58 � 0.149(0.62 � 0.169)

0.66 � 0.171(0.74 � 0.207)

Fixed effects Estimate � SE ddf F P Estimate � SE ddf F P

Year 0.17 � 0.166 28.4 1.03 0.32 0.43 � 0.145 31.2 8.99 <0.010.37 � 0.189 29.0 3.77 0.06

Temperature -0.36 � 0.187 23.9 3.70 0.07 -0.16 � 0.196 19.6 0.68 0.42-0.44 � 0.158 30.5 7.82 <0.01

Rainfall 0.01 � 0.201 9.05 0.00 0.95 0.29 � 0.201 3.66 2.03 0.23

Values in bold refer to model output after backward elimination of non-significant fixed factors, which in (a) resulted in a model including onlytemperature and in (b) in a model including only year. Model intercepts: (a) -0.10 � 0.190 (-0.09 � 0.206); (b) 0.00 � 0.254 (-0.05 � 0.170).ddf, denominator degrees of freedom; SE, standard error.

0

90

180

270 16 16

16

16

9 9

9

9

4 4

4

4

1 1

1

1

Figure 1 Toad migration peaks occurred non-randomly with respect tomoon phase, with most peaks being in the moon’s waxing phases, witha low frequency of peak migrations in the moon’s first quarter. Meanvector = 218°.

Year

1998 1999 2000 2002 2003 2004 2005 2006 2007 2008 2009 2010

Day

s si

nce

Janu

ary

1

60

65

70

75

80

85

90

95

100

Peak migrationFirst migration

Figure 2 Average timing of the onset of migration (5% of the totalpopulation having migrated; open circles) and the main migration (50%of the total population having migrated; filled circles) of common toadsin Derbyshire, UK. Data points represent average timing of migration �

SE for four different regions (note that in years 1998 and 2000, data areonly available from one region).



ians in the UK to migrate during wet weather, as the air in theearly spring is unlikely to be warm and desiccating enough toprove an immediate danger. Indeed, common toads are moretolerant of desiccation than most frogs and newts (Heatwoleet al., 1969), which should increase flexibility in activity pat-terns. Furthermore, toads breed in permanent bodies of waterso rainfall is not required to create the breeding habitat, incontrast to many other amphibians (e.g. Vaira, 2005).

The phase of the moon had a small, but statistically signi-ficant, effect on the number of arriving toads, with toadnumbers increasing as the sine angle decreased (i.e. in thesecond and third lunar quarters, from day 7 to day 21 after lastfull moon). Migration peaks occurred more frequently in thewaxing part of the cycle. A recent study (Grant et al., 2009)reported that at Marston Pond, Oxford, UK (which is at a moresoutherly latitude than the present study), large arrival eventsover a 10-year period in B. bufo occurred primarily from day 24of the lunar cycle until just after the full moon, and spawningoccurred from just before the full moon into the first lunarquarter. The present study has no data on spawning, but itappears that migrations also occur during the waxing part ofthe cycle although earlier in the lunar cycle than those atMarston Pond. Church (1960a, 1961) also found that the lunarcycle affected reproductive timing in the Javanese toad Bufomelanostictus, with more animals found in amplexus when themoon was waxing and more female toads with mature ovariesaround the full moon. Byrne & Roberts (2004) and Grant et al.(2009) proposed that the lunar cycle could be used by somespecies of amphibians to synchronize reproduction for thepurpose of maximizing reproductive success, but this hasnot been tested. Changes in behaviour or reproductive timingaccording to moon phase can also be an antipredator responsein a variety of species (e.g. Fitzgerald & Bider, 1974; Bouskila,1995). Although it is often assumed that prey animals will avoidthe full moon, the increased light levels around the full mooncan be advantageous to animals hunted by predators that relyon olfactory, vibrational or auditory cues (Grant, Halliday &Chadwick, 2012). Particularly for spring breeders in the tem-perate Northern Hemisphere, the effects of moon phase onmigrations and spawning are likely to be constrained byclimate, especially minimum temperatures (Fitzgerald & Bider,1974; Grant et al., 2009). This could explain the rather weakeffects of the lunar cycle noticed in our study.

Naturally, one of the most important abiotic factors thatinfluence activity patterns in ectotherms is temperature. Spe-cifically, in spring when temperatures consistently are belowoptimal, toads should be more active on warmer nights, whichshould result in higher numbers of migrants. Indeed, we founda positive correlation between daily temperature and the totalnumber of toads collected. The effect of daily temperature ontoad activity does not seem to have received much attention inthe literature, making it difficult to compare these results withother studies (but see Byrne, 2002). Perhaps, the effect of dailytemperature has been examined little previously because it isprimarily relevant to studies recording migratory activity,whereas most studies use spawning dates. As water tempera-tures are likely to be more constant than air temperatures,the effect of ambient temperature may be more important

during migration to the breeding pond rather than for breed-ing activity per se.

The timing of amphibian breeding activity is also expectedto be affected by temperatures earlier in the year, both becausehigher temperatures are associated with an earlier onset ofspring (Walther et al., 2002; Parmesan, 2006) and becausetemperature directly influences maturation of gametes [inmany temperature species, including B. bufo, vitellogenesisand spermatogenesis occurs during spring and summer (e.g.Jorgensen, Larsen & Lofts, 1979) but final gamete maturationupon arrival to the breeding pond is temperature-dependent;Reading & Clarke 1993]. The effect of average temperatureover the preceding months on amphibian breeding has beensubject to a number of studies. The majority have found sig-nificant negative relationships between temperature beforebreeding commences and the timing of breeding phenology.For example, the average temperature over the preceding40 days predicted the timing of the main arrival of commontoads at the breeding pond (Reading, 2003) and the averageJanuary–March temperature predicted the timing of peakroad mortality (and thereby peak migratory activity) and firstspawning, respectively, in two other populations in westernPoland and in Cambridge, UK (Tryjanowski et al., 2003;Sparks et al., 2007). In addition, Beebee (1995) found strongcorrelations between breeding activity and average minimumtemperatures in March and April in Bufo calamita. Our resultsfrom B. bufo suggest that the onset of migration occurs earlierin warmer years across several sites in Derbyshire. However,we did not find any support for a direct effect of air tempera-ture in January and February on the timing of the main springmigration. Although our study period (12 years) is somewhatshort compared to some other studies, this suggests that thelink between temperature early in the year and the timing ofbreeding activities should not be taken for granted even inspecies living at relatively high latitudes. Furthermore, it sug-gests that results may depend on the estimates used (e.g. onsetof migration versus peak migration, migration versus breed-ing) and we suggest that there may also be substantial varia-tion arising from highly local effects (e.g. Savage, 1961;Heusser & Ott, 1968; Oseen & Wassersug, 2002), such as thelocation of hibernation sites and the distance to breedingponds, which can confound large-scale patterns.

As a result of this temperature dependence, breeding phe-nology has become progressively advanced in warmer years inthe majority of amphibians (Parmesan, 2007). In contrast, thetiming of main migration of common toads in Derbyshireseems to have shifted towards later dates over the last decade.Although the significance of this result is compromised by therelatively short period of study, investigations into whetheramphibian breeding phenology is showing advancement have,in fact, produced a variety of findings, both between and withinspecies. For example, Blaustein et al. (2001) found no signifi-cant change in the timing of breeding in three species of Ameri-can anuran (Bufo boreas, Rana cascadae and Bufo fowleri) buta trend towards later breeding in Pseudacris crucifer, whileTodd et al. (2011) found no significant trend for five species ofwinter and spring breeding anurans in the US (Pseudacriscrucifer, Rana sphenocephala, Bombus terrestris, Gastrophryne



carolinensis and Scaphiopus holbrookii) but a significantadvance in Pseudacris ornata.

In the case of much-studied amphibian species such asB. bufo and Rana temporaria, results also differ betweenpopulations. Rana temporaria has been found to be breedingearlier in more recent years in the UK (Scott et al., 2008),France (Neveu, 2009), Poland (Tryjanowski et al., 2003) andFinland (Terhivuo, 1988). However, studies by Beebee (1995)and Sparks et al. (2007), both in the UK, found no signifi-cant trend over time. Similarly, a variety of patterns regard-ing the timing of breeding activity have been found inB. bufo. Sparks et al. (2007) found a significant trend towardsearlier breeding in Cambridge, UK, as did Tryjanowski et al.in Poland (2003), but Reading (1998, 2003) found no signifi-cant trend over time in south Dorset, UK. Our study addscomplexity to the overall picture, as populations of toads inDerbyshire, central England, actually tend to migrate later inmore recent years. Although the effects probably are partlyexplained by a weak decrease in temperature over the studyperiod, our analyses strongly suggest that there are additionalfactors contributing to later migration in more recent years.Nevertheless, we emphasize that there may be additionalvariation driven by highly local climatic effects, the cause ofwhich may be very difficult to establish with the typicallylimited data on, for example, hibernation sites and small-scale temperature fluctuations.

In addition to lack of data on potential confounders,perhaps the largest limitation of studies like this is that theobservational data can be subject to various kinds of bias. Thesurvey of toad migration that contributed to this dataset relieson volunteers that follow a given set of instructions (and fill ina standardized form), which may lead to variation in searcheffort. However, the fact that the earliest records for each yeartypically did not include any sightings suggest that samplingbias is unlikely to explain annual variation in the onset oftoad breeding phenology. Likewise, although search effortundoubtedly would influence the number of toads sighted ona given night, controlling for the time spent searching did notinfluence our conclusions regarding predictors of daily varia-tion in toad activity, which also suggests that the estimate ofthe main period of activity is reasonably accurate. If carefullyused, long-term data from monitoring schemes may proveuseful to establish long-term trends in animal populations.

In summary, more toads migrated to breeding ponds onwarmer days, whereas rainfall had no effect. The phase of themoon also seems to have some effect on the timing of toadmigrations. The average temperature in January and Februarysignificantly predicted the onset of migration, but not thetiming of the main migration of populations. In contrast tomost other studies of amphibian breeding phenology, commontoads in central England exhibit a weak, but statistically sig-nificant, shift towards later migration to breeding ponds inmore recent years.

AcknowledgementsWe would like to thank all members of the DerbyshireAmphibian and Reptile Group for their efforts in collecting

these data, Professor Ashis SenGupta for the advice oncircular statistics and two reviewers for very constructivecomments on a previous draft.

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Supporting informationAdditional Supporting Information may be found in theonline version of this paper:

Table S1 Summary of toad crossing sites used in thisstudy.

Table S2 Output for (a) the model in Table 1 includingonly random effects and (b–e) the four top scoring models inTable 1. Model intercepts: (a) 0.00 � 0.094; (b) -0.06 � 0.093;(c) -0.06 � 0.094; (d) -0.06 � 0.094; (e) -0.05 � 0.095. Thesecond-order Akaike information criterion (AICc) and theproportional change in residual variance (PCV) relative tomodel A is provided for each model.

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