Factors influencing the timing of spring migration in common toads (Bufo bufo)

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<ul><li><p>Factors influencing the timing of spring migration incommon toads (Bufo bufo)H. Arnfield1, R. Grant2, C. Monk3 &amp; T. Uller1</p><p>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</p><p>Keywordsphenology; amphibian; temperature;breeding.</p><p>CorrespondenceTobias Uller, Edward Grey Institute,Department of Zoology, University ofOxford, Oxford OX1 3PS, UK.Email: tobias.uller@zoo.ox.ac.uk</p><p>Editor: Mark-Oliver Rdel</p><p>Received 4 December 2011; revised 19April 2012; accepted 24 April 2012</p><p>doi:10.1111/j.1469-7998.2012.00933.x</p><p>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.</p><p>Introduction</p><p>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 &amp;Adamson, 2008), although some studies have failed to find asignificant relationship (e.g. Gittins, Parker &amp; 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 &amp; Sparks, 2003; Sparks et al., 2007;Kusano &amp; Inoue, 2008; Scott et al., 2008; Carroll, Collinson &amp;Beebee, 2009; Neveu, 2009; Phillimore et al., 2010). Indeed,amphibians seem to respond strongly to ongoing climatechange (Beebee, 1995; Parmesan &amp; Yohe, 2003; Root et al.,2003), with average advancement of spring breeding date per</p><p>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 &amp;Wassersug, 2002;Vaira, 2005) and celestial cues (Grant, Chadwick &amp; Halliday,2009) may play important roles.</p><p>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.</p><p>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</p><p>bs_bs_bannerJournal of ZoologyJournal of Zoology. Print ISSN 0952-8369</p><p>Journal of Zoology (2012) 2012 The Authors. Journal of Zoology 2012 The Zoological Society of London 1</p></li><li><p>still bodies of water, usually occurs after dusk in early spring(Beebee &amp; Griffiths, 2000).</p><p>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 toadmigration 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. Mainmigration 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.</p><p>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</p><p>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 &amp; Inoue,2008); however, as the results stay the same, we only report theresults from the first set of analyses.</p><p>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 &lt; 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.</p><p>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 &amp; 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 &amp; 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).</p><p>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</p><p>Timing of spring migration in toads H. Arnfield et al.</p><p>2 Journal of Zoology (2012) 2012 The Authors. Journal of Zoology 2012 The Zoological Society of London</p></li><li><p>on the second-order corrected Akaike information criterion(AICc) (Burnham &amp; Anderson, 2002).</p><p>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.</p><p>Results</p><p>Predictors of toad activity during migration</p><p>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</p><p>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).</p><p>Analysis of migration peaks indicated that peakmovementsof 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 &lt; 0.001; Fig. 1). Fewpeak arrivals occurred in the moons waning gibbous phase(between 0 and 7 days after last full moon; Fig. 1).</p><p>Long-term trends</p><p>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 hadmigrated 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: 0.560.261, t = 2.16, P = 0.05, n = 12; R2 = 0.32).</p><p>DiscussionThe results of this study suggest that common toad migrationto breeding ponds in spring is positively influenced by daily</p><p>Table 1 Top scoring linear mixed models for the number of toads foun...</p></li></ul>


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