Long-term monitoring of the endemic Rana latastei: suggestions for after-LIFE management
L UCA C ANOVA and A LESSANDRO B ALESTRIERI
Abstract We monitored egg clutch numbers of a popula- loss (Houlahan & Findlay, ; Cushman, ), pollution tion of the endemic Italian agile frog Rana latastei in a (Bridges & Semlitsch, ), disease epidemics and climate Site of Community Interest in northern Italy (SCI IT change (Kiesecker et al., ; Ficetola & Maiorano, ). ) during – with the aim of assessing the As for many other taxa (Menzel et al., ; Thackeray long-term variation in its abundance. We walked along et al., ; Chen et al., ), a shift to earlier breeding as the banks of canals and small ponds (n = ) – times per a result of global warming has been reported for several week between early February and mid-April each year to anuran species (Terhivuo, ; Reading, ; Corn, ; detect egg clutches. The relationships between the start of Tryjanovski et al., ). Shifts are stronger for anurans than the breeding season, yearly egg mass counts, rate of yearly those reported for trees, birds and butterflies (Parmesan, change in the number of recorded egg masses and climat- ), but the consequences of earlier breeding for popula- ic and environmental variables were assessed by multiple re- tion dynamics are still unknown. gression. The first deposition of eggs occurred progressively Neither phenological shifts (Blaustein et al., ), nor later in the year throughout the study period and mean air population decline (Blaustein et al., ; Richter et al., temperature during the breeding season decreased over this ; Stuart et al., ) affect all amphibian populations. period. Agile frogs showed high deposition site-fidelity. The reasons for these variations are still being debated Despite large variations in the number of egg clutches and identifying them requires information on breeding detected from year to year, the population size remained ecology and population trends, which is often difficult to ob- stable in the long term. Peaks in the number of egg clutches tain, particularly for rare or declining species (Richter et al., occurred years after the dredging of canals, carried out ). every – years to improve water availability, starting in In amphibians clutch size (the number of egg masses de- as part of a LIFE Nature Project. This was the only posited) is an important life history trait that varies between predictor of the number of egg clutches deposited, suggest- taxonomic groups, populations, and individuals within the ing that periodical management is needed to support the same population (Wells, ; Cadeddu & Castellano, ). agile frog population. Our results reinforce the need for At population-level, variation in clutch size depends on food multi-year monitoring to determine both the long-term availability and environmental conditions, mainly tempera- success of habitat restoration projects and the status of ture (Reading, ), rainfall (Jensen et al., ) and hydro- residual populations. period (Semlitsch et al., ). Climatic conditions in spring may affect the length of the breeding period (Jørgensen, Keywords Clutch size, conservation, habitat restoration, ; Reading & Clarke, ), resulting in variations in Italian agile frog, LIFE projects, long-term monitoring, clutch sizes (Morrison & Hero, ). population trend, Rana latastei Egg clutch counts have been widely used for monitoring amphibian populations (Crouch & Paton, ; Bernini et al., ; Loman & Andersson, ) and are considered Introduction a valid indicator of population trends (Meyer et al., ; Houlahan et al., ). Because the number of egg masses mphibian populations worldwide are declining at an deposited can vary significantly between years, collecting Aalarming rate (McCallum, ; Hayes et al., ), data for . years may be necessary to assess the trend with % of amphibian species threatened; i.e. categorized of an amphibian population with sufficient precision as Vulnerable, Endangered or Critically Endangered on (Scherer & Tracey, ). the IUCN Red List (Stuart et al., ). Several anthropo- In addition to providing descriptions of population genic factors contribute to their decline, including habitat dynamics, long-term data are needed to identify changes driven by anthropogenic stressors (Magurran et al., ) and the causes of declining amphibian populations (Stuart LUCA CANOVA Department of Chemistry, University of Pavia, Pavia, Italy et al., ). Long-term data improve ecosystem models ALESSANDRO BALESTRIERI (Corresponding author) Department of Biosciences, and forecasts, supporting effective management actions University of Milan, Via Celoria 26, I-20133 Milan, Italy E-mail [email protected] (Giron-Nava et al., ). Received August . Revision requested October . Despite its importance for conservation management, Accepted December . long-term monitoring and collection of basic data on
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fecundity and population trends are often hampered by low (Bernini et al., ). The Action Plan has highlighted the funding and unstable political conditions (Elzinga et al., need for long-term (. years) studies (Edgar & Bird, ; Estrada, ). Only a few egg clutch time series span- ) to account for large annual fluctuations of population ning . years are available, including – years for Rana size. We monitored egg clutch sizes over a -year period temporaria (Switzerland; Meyer et al., ), years for (–) in a small protected area in the Lombardy re- Lithobates sylvaticus (New England; Raithel et al., ), gion with the aim of determining long-term variation in and years for Rana dalmatina (Italy; Bernini et al., ). agile frog abundance. Because the area was the subject of a Although Palearctic amphibians are less threatened than -year LIFE Nature Project (LIFE NAT/IT/)to tropical species, northern Italy is among the Eurasian areas increase habitat suitability for amphibians and Ardeidae hosting the highest number of endemic and threatened spe- during –, we also aimed to assess the Project’s cies: out of (%) are endemic and are categorized as long-term impact on R. latastei. threatened ( Endangered and Vulnerable) on the IUCN Red List (Stuart et al., ; Rondinini et al., ). The Mediterranean region is considered a hotspot for conserva- Study area tion investment (Myers et al., ; Brooks et al., ). The Italian agile frog Rana latastei is a monotypical, en- The study area is located at the Site of Community Interest demic species of northern Italy, the Swiss canton Ticino ‘Riserva di Monticchie’ (SCI IT ; N, (Grossenbacher, ) and the Istria peninsula (Burlin & E). The Site covers c. ha on the left bank of the River Dolce, ), and also occurs locally in lowland hygrophil- Po, of which . ha are hygrophilous forest and . ha ous woods below m in Slovenia and Croatia (Barbieri & are agricultural land. Residual forested areas consist of allu- Mazzotti, ). Females lay their eggs in February–April in vial woods with alder Alnus glutinosa, white willow Salix single clutches (one per year), which are usually deposited alba and common ash Fraxinus excelsior, and deciduous ri- within cm of the water surface of river pools, ponds, parian woods with oak Quercus robur and elms Ulmus spp. springs and canals in wooded areas. Deposition sites are R. latastei has been recorded in the area since the early typically rich in aquatic vegetation or provide submerged s (Ferri, ). In – the LIFE Nature Project branches and leaves (Barbieri & Mazzotti, ). R. latastei ‘Ardeides and Amphibians: habitat conservation in the is an explosive breeder, with most ovipositions occurring Monticchie Natural Reserve’ (LIFE NAT/IT/) within – days, eggs hatching – days after deposition, aimed to increase the cover of alluvial forests through select- and tadpoles completing their metamorphosis in c. ive cutting of allochthonous species, planting of , indi- months (Sindaco et al., ). Less than breeding sites genous trees and shrubs over a ha area, and restoration of are known (Grossenbacher, ), most populations are water quality and availability in canals and springs by im- fragmented and genetic diversity decreases from east to proving the existing canal network and the circulation of west and in peripheral populations (Garner et al., ). ground water arising from the foot of a fluvial terrace The species is included in Annexes II and IV of the (Fig. ). Since , canals have been periodically dredged Habitat Directive of the European Union (EC /) to remove sediments and improve water availability. and categorized as Vulnerable on the IUCN Red List. Reasons for concern are water pollution, increasing urban- ization and widespread intensive agriculture, which threat- Methods en the residual humid deciduous forests of the Po-Venetian plain, one of the most densely populated areas in Italy From to all waterbodies (n = ) of the site were (Lassini et al., ; Sindaco et al., ). Additional threats surveyed – times per week from early February until are invasive predatory fishes and crayfish, which have a c. mid April (depending on rainfall and frog breeding activ- negative impact on amphibian communities (Ficetola ity) and deposited egg masses were counted. Clutches were et al., a) and may have caused the extinction of R. la- detected by walking along the banks of canals (n = , total tastei from part of its range (Ficetola et al., b). length = , m, mean length = . ± SD . m; mean Considering the Italian agile frog one of the most threa- width = . ± SD . m) and small ponds – cm deep tened amphibians in Europe, the Standing Committee of the (n = , width = – m). Surveys were usually carried out in Bern Convention commissioned an Action Plan for its con- the morning, by a main observer and a helper who recorded servation (Edgar & Bird, ) and the species has been re- the main observer’s count and any sightings of additional introduced in five protected areas of the Lombardy region in egg masses. Both observers wore polarized sunglasses to northern Italy (Scali et al., ; Bernini & Razzetti, ). reduce the glare of the sun on the water. To help with Despite the increasing interest in its conservation, until now the identification of newly-laid clutches, all egg masses only short-term population surveys have been carried out were photographed and their location marked on a map for this species, with the exception of a -year census of the site with landmarks such as trees and stones.
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FIG. 1 Aerial view of the study area in . Wooded areas that have been improved during or after the LIFE project (–) and the canal network are highlighted. The location of the study area in Italy is shown on the inset map.
Because the agile frog R. dalmatina, whose egg clutches All climatic and environmental variables that were not are similar to those of R. latastei (Bernini et al., ), has correlated with any of the dependent variables (P . .) never been recorded in the study area despite several surveys were discarded from subsequent analyses. The influence of (e.g. Ferri, , ; Canova & Marchesi, ) and the remaining variables on reproductive activity was then hydrophone recordings (G. Pavan, unpubl. data), all egg analysed using multiple regression. Before the analyses, all masses could be assigned unequivocally to the target species. variables were tested for normality by Kolmogorov– The rate of yearly change in egg mass number was mea- Smirnov’s test. When necessary, data were transformed to sured using the ΔN method (Houlahan et al., ): achieve normality and homoscedasticity by Box-Cox’s Δ − N = log (N + )t log (N + )t−, where N represents the method ( ). To avoid multicollinearity, which can inflate population size (number of the egg masses) at time t. the standard errors of the estimates of the model coefficients The relationship between the start of the breeding season and produce unreliable results (Hosmer & Lemeshow, ; (the ordinal date when the first egg mass was recorded), Quinn & Keough, ), correlations between the predictors yearly egg mass counts, and rate of yearly change in egg were measured by Pearson’s coefficient. Variables to be en- mass number and climatic and environmental variables tered in the model were then selected to omit those clearly was first explored by Spearman’s correlation coefficient. representing redundant information; when two variables The following independent variables were used: () year, were correlated, the one to be rejected was chosen according () total precipitation (mm) in February in the years when to the strength of its correlation with the dependent variable. egg masses were counted, () total precipitation during the The model was then fitted with the predictors in decreasing previous year (rainfall affects adult survival; Berven, ), order, according to the strength of correlation between the (–) mean maximum temperature in January (pre- dependent variable and each predictor, and following back- reproductive period), February (start of breeding activity) ward elimination of the non-significant predictors (sequen- and February–March (overall reproductive period), (–) tial regression method). mean minimum temperature and (–) overall mean tem- Trends through time of climatic variables recorded in perature in the same three periods, () air humidity in February were estimated by regression of each variable on February, () water availability, and () mean water depth. year. Statistical analyses were run in SPSS . (IBM, Rainfall (mm), air humidity (%) and mean temperatures Armonk, USA) and PAST .c (Hammer et al., ). (°C) were calculated from daily values obtained from the historical archives of the weather stations of Piacenza and ’ Sant Angelo Lodigiano (Regional Agency for Environmental Results Protection), which are c. and km from Monticchie, respectively. Water availability was expressed as the per The number of egg clutches recorded in a single breeding season cent length of canals with water depth $ cm; each year, ranged from in to in (mean = . ± SD .; water depth was measured at deposition sites when egg Fig. ). Peaks in the number of eggs deposited by R. latastei oc- clutches were recorded. curred years after dredging (Fig. ). The overall trend in the rate
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FIG. 2 Yearly variation in the number of egg clutches deposited by Rana latastei at the Site of Community Interest ‘Riserva di Monticchie’ in northern Italy. Arrows indicate the years when the canal network was dredged to increase water availability.
of yearly change in egg mass number was slightly positive over The first egg clutch was detected at a mean of . ± SD the study period (ΔN = . ± SD .; Fig. ). . days, with the ordinal date of first deposition increasing − Throughout the study period, agile frogs most frequently significantly throughout the study period (b = · ± SD − selected the same group of canals in the centre of the site .· ,P=.; Fig. ). The analysis of year-to-year for egg deposition, with % of all egg clutches deposited variation in climatic variables showed that the mean daily there. These canals were used in –% of reproductive maximum temperature in February decreased and air hu- seasons, whereas out of the monitored canals were midity increased (Table ; Fig. ). Breeding date and max- used # times, mainly during reproductive peaks. imum temperature in February were inversely related, The number of egg clutches increased with water availabil- although not significantly (r = −.,P=.). ity (r = .,P, .) and depth (r = .,P=.), and was inversely related to maximum air temperature in February Discussion (r = .,P=.)(Fig. ). Water availability was the only predictor included in the regression model for the number Egg counts are typically incomplete and represent only a of egg clutches deposited (b = . ± SD .,P, .). proportion of the actual female population (Campbell When running multiple regressions with only the climatic Grantetal.,). Although we did not account for detect- variables, the final model included the mean maximum tem- ability, we surveyed each waterbody several times per perature in February (b = −. ± SD .,P=.). breeding season, ensuring that our count of egg masses
FIG. 3 Rate of yearly change (ΔN)inR. latastei egg clutch numbers at the Site of Community Interest ‘Riserva di Monticchie’ in northern Italy. The dashed line shows the slightly positive overall trend.
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FIG. 4 The effect of (a) water availability, (b) water depth and (c) maximum water temperature on the number of egg clutches deposited by R. latastei in the study area during –. Regression lines are shown for each graphic.
was as complete as possible. Because the same surveys temperature in February on the number of egg clutches de- methods were used every year, we expected inter-year posited is difficult to explain, although frogs breeding in comparisons to reflect fluctuations in breeding population closed canopy ponds may be less tolerant of high tempera- size accurately. tures than those from open areas (Skelly & Freidenburg, Italian agile frogs were consistently found to breed in the ). Because males call underwater (Farronato et al., monitored area throughout the study period. However, as ) and water temperature remained constant, variations reported for several other anuran species (Richter et al., in air temperature might not affect breeding activity. ; Hartel, ; Scherer & Tracey, ) the number of Rainfall, which has been shown to affect breeding popula- egg clutches deposited varied significantly between years. tion size in other amphibians (Semlitsch et al., ), did Despite this variation in reproductive output, monitoring not seem to affect population fluctuations of R. latastei. over decades revealed no clear trend, suggesting an overall Similar results have been found for three populations of R. stable breeding population. temporaria (Meyer et al., ). This result contrasts with the conclusions of the final re- For anurans that deposit their eggs in standing water port of the LIFE Nature Project (Marzatico, ) carried (% of anuran families; Duellman & Trueb, ), water out in –, which stated ‘a large increase [...]in availability is a major determinant of both distribution the amount of eggs deposited’. Although the sudden in- (Banks et al., ; Rodriguez et al., ) and reproductive crease in clutch number recorded during the intervention success (Rowe & Dunson, , ). The relationship be- supported the actions undertaken by project managers, tween clutch size and water availability (per cent length and our results reinforce the need for multi-year monitoring depth of active canals) recorded in our study confirms the to determine the long-term success of species-specific importance of the availability of suitable oviposition sites habitat restoration projects (Silva et al., ). The risk of during the breeding period. The importance of water avail- drawing erroneous conclusions about population trends ability was also indicated by the clutch size peaks following from the analysis of short-term data has also been high- dredging actions, which started in during the LIFE lighted in previous analyses of -year long time-series project and aimed to improve water circulation in the (Meyer et al., ; Pechmann et al., ). canal network. The -year delay between dredging and Variation in clutch numbers depends on weather condi- clutch size peaks may be explained by the time required tions such as daily fluctuations in temperature and humidity for the renewal of aquatic vegetation and deposition of during the breeding season, rainfall in the previous seasons, leaf litter and wood debris, which agile frogs require for habitat changes and demographic patterns (i.e. the survival breeding (Barbieri & Bernini, ). Another factor may rate of adults in the pre-reproductive period) (Berven, ; have been that dredging was carried out in November, po- Reading & Clarke, ; Harper & Semlitsch, ; Wells, tentially disturbing hibernating frogs. Canals used regularly ). In the study area, climatic conditions in both the pre- for oviposition were located in the inner, less disturbed and reproductive and breeding periods played a negligible role in more forested part of the study area. These canals showed determining year-to-year variation in the number of egg lower variation in water availability throughout the study clutches deposited. The negative effect of maximum air period compared to peripheral water bodies and have
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TABLE 1 Tests for potential trends in climatic variables at Piacenza and Sant’Angelo Lodigiano in February –, with mean values and coefficients (b) and their standard errors (SE) from re- gressions of the variables against year. Significant trends (t-tests P , .) are shown in italics.
Mean B SE P Mean temperature (°C) 4.77 −0.700 0.703 0.332 Minimum temperature (°C) −0.04 0.489 0.607 0.430 Maximum temperature (°C) 8.76 −1.574 0.527 0.008 Dew point (°C) 1.37 1.057 0.423 0.022 Air humidity (%) 76.73 0.354 0.105 0.003 Wind speed (km/h) 6.69 1.279 0.677 0.074 Rainfall (mm) 63.73 0.047 0.023 0.054
with the global trend, corresponds with the recorded de- crease in the daily maximum temperatures in February, al- though mean temperatures did not vary accordingly. Other studies have also found that some anuran species do not tend to breed earlier or even show a tendency to breed later (Blaustein et al., ; Gibbs & Breisch, ), probably as a consequence of local variation in climatic conditions. Yearly monitoring allowed us to record the actual trend of the local agile frog population, relating large fluctuations in clutch size to water availability and management actions and assessing the long-term success of the LIFE Nature Project. Although pre-metamorphic survival is mainly determined by density dependent factors (Berven, ), anecdotal evidence suggests that water availability also may be important for agile frog reproductive success during the developmental period. During –, most canals occasionally dried up before tadpoles underwent metamor- phosis (Ferri, ), threatening tadpole survival and their
FIG. 5 Variation in (a) date of first deposition, (b) maximum air recruitment into the breeding population in subsequent temperature and (c) humidity in February during –. years. Given that rainfall increased only slightly during the Regression lines are shown for each graphic. study period, drying up was probably caused by either the occlusion of groundwater springs by sediments or water usage for agricultural purposes. been used by frogs since the s (Ferri & Agapito The periodical dredging (every years) of the existing Ludovici, ), suggesting high site-fidelity. The larger canal network is an important management action to ensure number of canals used during reproductive peaks reflects the availability of suitable breeding sites and support the the higher water availability following dredging and suggests conservation of this agile frog population. The results of that in dry springs intraspecific competition for oviposition our long-term monitoring suggest that in small wooded sites may be more intense. areas in an agricultural landscape, water availability can be In temperate regions the beginning of breeding activity in highly variable because of its exploitation for watering sur- explosive-breeding anurans is determined by rising tem- rounding crops, and can become a limiting factor for am- peratures at the end of winter (Wells, ; Sofianidou & phibians. In such cases, we recommend the following Kyriakopoulou-Sklavounou, ) and mean air tempera- management measures: () dredging should be carried out ture in February can affect the breeding dates of Rana regularly to prevent the silting up of canals and ensure a spp. (Terhivuo, ; Hartel, ). In the -year period water depth suitable for oviposition and tadpole dev- of monitoring, a period long enough to detect shifts in the elopment (– cm), () dredging activities should be car- onset of breeding caused by climate change (Reading, ; ried out at the end of summer, before the species enters Beebee, ; Forchhammer et al., ), agile frogs tended hibernation, and () long-term monitoring (. years) of to breed progressively later. This finding, which contrasts the size of the targeted population beginning at the start
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of a project is required for a full assessment of the success Nazionale della Societas Herpetologica Italica (eds O. Picariello, of conservation interventions. Site-fidelity implies that G. Odierna, F.M. Guarino & D. Capolongo), pp. –. Università habitat restoration and reintroduction or reinforcing degli Studi di Napoli Federico II, Napoli, Italy. BERNINI, F., GENTILLI, A., MERLI,E.&RAZZETTI,E.() Rana plans need to take into account the historical distribution dalmatina and R. latastei: Habitat selection, fluctuation in egg clutch of the species in the intervention area, and that many deposition and response to exceptional floods in northern Italy. years may pass before agile frogs colonize a new area Italian Journal of Zoology, , Suppl. , –. permanently. BERVEN, K.A. () Factors affecting population fluctuations in larval – Efforts to recreate aquatic and terrestrial habitats to sup- and adult stages of the wood frog (Rana sylvatica). Ecology, , . port the long-term viability of agile frog populations have BLAUSTEIN, A.R., WAKE, D.B. & SOUSA,W.P.() Amphibian been limited to date (Edgar & Bird, ). Since , the declines: judging stability, persistence, and susceptibility of populations reserve authorities have managed to increase water availabil- to local and global extinctions. Conservation Biology, , –. ity and stabilize water levels at the study site. The first inter- BLAUSTEIN, A.R., BELDEN, L.K., OLSON, D.H., GREEN, D.M., ROOT,T. vention was the construction of an artificial pond, L. & KIESECKER, J.M. ( ) Amphibian breeding and climate change. Conservation Biology, , –. connected to the water table, to which egg clutches can be BOX, G.E.P. & COX, D.R. () An analysis of transformations. moved when canals dry up. Authorities are currently plan- Journal of the Royal Statistical Society Series B, , –. ning to construct shallow ponds and marshy areas, covering BRIDGES, C.M. & SEMLITSCH, R.D. () Variation in pesticide c. ha, to provide further suitable deposition sites. An add- tolerance of tadpoles among and within species of Ranidae and – itional step may be the creation of a buffer zone to avoid pol- patterns of amphibian decline. Conservation Biology, , . BROOKS, T.M., MITTERMEIER, R.A., MITTERMEIER, C.G., DA lution of the inner area during chemical treatment of FONSECA, G.A.B., RYLANDS, A.B., KONSTANT, W.R. et al. () neighbouring croplands. Our results have also been consid- Habitat loss and extinction in the hotspots of biodiversity. ered for preparing a Regional Action Plan for the conserva- Conservation Biology, , –. tion of threatened aquatic species. BURLIN,M.&DOLCE,S.() Osservazioni faunistiche sull’erpetofauna dell’Istria. Atti Museo Civico di Storia Naturale di Trieste, , –. Acknowledgements We thank the administration of Monticchie CADEDDU,G.&CASTELLANO,S.() Factors affecting variation in Natural Reserve and Assessorato Ambiente, Regione Lombardia for the reproductive investment of female treefrogs (Hyla intermedia). funding [GC-32-17042009; GC-99-28122011], permissions and Zoology, , –. logistic support, P. Mazzoleni for permission to visit his farms, CAMPBELL GRANT, E.H., JUNG, R.E., NICHOLS, J.D. & HINES, J.E. and A. Mascherpa, A. Cremonesi, A. Lucchini, S. Ghidotti and () Double-observer approach to estimating egg mass S. Uccellini for their help with fieldwork. G. Pavan recorded and ana- abundance of pool-breeding Amphibians. Wetlands Ecology and lysed male calls by hydrophone and S.J. Lovejoy provided language Management, , –. editing. CANOVA,L.&MARCHESI,M.() Amphibian and reptile communities in eleven Sites of Community Importance (SCI): Author contributions Research conception and clutch size relations between SCI area, heterogeneity and richness. Acta monitoring: LC; data analysis: AB; writing of the manuscript: LC Herpetologica, , –. and AB. CHEN, I.-C., HILL, J.K., OHLEMÜLLER, R., ROY, D.B. & THOMAS, C.D. () Rapid range shifts of species associated with high levels of Ethical standards The research was non-intrusive and had the climate warming. Science, , –. necessary approval and permits from the administrations of CORN, P.S. () Amphibian breeding and climate change: the Monticchie Natural Reserve and Lombardy Region. importance of snow in the mountains. Conservation Biology, , –. Conflicts of interest None. CROUCH, W.B. & PATON, P.W.C. () Using egg mass counts to monitor wood frog populations. Wildlife Society Bulletin, , –. References CUSHMAN, S.A. 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