critical times of the year for myotis myotis, a temperate zone bat: roles of climate and food...

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Critical times of the year for Myotis myotis a temperate zonebat roles of climate and food resourcesAuthor(s) Andreas Zahn Luiacutesa Rodrigues Ana Rainho and Jorge MPalmeirimSource Acta Chiropterologica 9(1)115-125 2007Published By Museum and Institute of Zoology Polish Academy of SciencesDOI httpdxdoiorg1031611733-5329(2007)9[115CTOTYF]20CO2URL httpwwwbiooneorgdoifull1031611733-53292820072995B1153ACTOTYF5D20CO3B2

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INTRODUCTION

The dynamics of a population may notbe just a function of the average environ-mental conditions but of those occurring atlsquocriticalrsquo times of the year when due to spe-cific constraints the animal cannot fulfil itsenergy requirements (Racey 1982 Barclay1991) The identification of such bottle-necks and of their determinants is importantnot only to understand abundance and dis-tribution of species but also to direct con-servation action in order to halt and reverse

population declines (Payne and Wilson1999 Primack 2002) This is particularlyrelevant in bats because the populations ofmany species have been declining and sev-eral of these are now threatened (Mickle-burgh et al 2002)

Temperate zone bats have a well-definedannual cycle largely determined by cli-mate Climate may influence their energybalance in multiple ways It may imposeconstraints on energy intake by influencingthe availability of food and limiting the for-aging activity In fact climate is known to

Acta Chiropterologica 9(1) 115ndash125 2007PL ISSN 1508-1109 copy Museum and Institute of Zoology PAS

Critical times of the year for Myotis myotis a temperate zone bat roles of climate and food resources

ANDREAS ZAHN1 LUIacuteSA RODRIGUES2 ANA RAINHO2 and JORGE M PALMEIRIM3

1Ludwig-Maximilians-Universaumlt Muumlnchen Groszlighaderner Str 2 D-82152 Planegg - Martinsried GermanyE-mail AndreasZahniivde

2Instituto da Conservaccedilno da Natureza e da Biodiversidade Rua de Santa Marta 55 1150-294 Lisboa Portugal 3Departamento de Biologia Animal and Centro de Biologia Ambiental Faculdade de CiLncias

Universidade de Lisboa 1749-016 Lisboa Portugal

In highly seasonal temperate zones climate may cause fluctuations in the accessibility of prey for insectivorousbats The main objective of this project was to evaluate if these fluctuations can result in resource bottlenecksthat affect the body condition of a temperate zone bat mdash Myotis myotis Seasonal changes in body conditionfollowed different patterns in Portugal and Germany which have different climates In Germany bats usethermally better hibernacula which allow them to minimize energy expenditure but because of the longerwinters they emerge from hibernation in poorer condition Except during the hibernation period food wasalways abundant in Germany but the condition of the animals was poor when bad weather constrained foragingparticularly in early spring In Portugal food was limiting during the long dry summer and this affected thecondition of the animals for several months The conclusion that food resources can act as a limiting factor isrelevant for conservation because like other bat species M myotis forages mostly in agricultural and forestryhabitats and can be affected by practices that accentuate resource bottlenecks Where necessary themanagement of agroecosystems near colonies of M myotis and of other threatened bats should aim atminimizing seasonal food bottlenecks

Key words Myotis myotis diet prey availability resource bottlenecks body condition Portugal Germany

be a determinant factor in the abundance ofinsect prey (Racey 1982) and rough weath-er conditions can restrict the ability of batsto forage (Lewis 1992) Climate also deter-mines the temperature of hibernation roostslimiting the capacity of bats to optimisebody temperature (Neuweiler 2000) andthe length of hibernation both of whichmay increase mortality (Thomas 1995)

It is well known that the body mass ofbats shows seasonal fluctuations throughoutthe year this may be explained by endo-genous mechanisms (Beasley et al 1984)andor by seasonal variations in access toresources Endogenous mechanisms shouldprogram bats to avoid a great accumulationof fat at times when it is not needed be-cause this may be costly during flight(Ransome 1990) Under optimal environ-mental conditions one would expect thebody mass changes to be fully determinedby the endogenous mechanisms Howeverif resources are limited the observed bodycondition of the bats will be a result of boththe endogenous mechanisms and the envi-ronmentally-induced energetic constraintsIn order to determine if there are seasonalresource bottlenecks that weaken body condition it is necessary to ascertain if the seasonal body mass variations are notsolely explained by endogenous mecha-nisms

We separated the effect of the two fac-tors by comparing the patterns of seasonalfluctuation of body mass of the same batspecies in regions with different climates Ifendogenous mechanisms alone determinethe seasonal variations in body mass thenwe predicted that they would follow verysimilar patterns in the two regions If how-ever climatically controlled resources arelimiting patterns of body condition shouldbe different Using Myotis myotis (Bork-hausen 1797) as a model we tested thesepredictions to determine if there are criti-cal times of the year for temperate zone

bats In addition we studied the rolesplayed by climate and food resources in thegeneration and timing of these potential bot-tlenecks

MATERIALS AND METHODS

Myotis myotis is a medium-size insectivorous batthat ranges from the Mediterranean to the Baltic andis thus exposed to a variety of temperate climates(Guumlttinger et al 2001) This study compares the pop-ulations of two European regions with very differentclimatic conditions Portugal has a Mediterranean tosub-Mediterranean climate with cool and rainy win-ters and dry hot summers (Fig 1) Upper Bavaria inGermany has longer and colder winters and it rainsthroughout the year In Germany samples were takenin 14 nursery colonies and 30 attics with male roostslocated in the southern part of Upper Bavaria(47deg36rsquondash48deg15rsquoN) In Portugal these data were col-lected in five nurseries and four caves with maleroosts in the south-central part of the country(37deg40rsquondash39deg40rsquoN)

We studied seasonal variations in the body condi-tions of the bats using a ratio (gmm) between thebody mass (g) and the forearm length (mm) meas-ured in 1950 animals in Germany and 2100 inPortugal [captured between 1987 and 2002 samplesizes per month 68ndash493 bats except December inPortugal (23) and November in Germany (20)] Thisindex was used instead of the mass because Por-tuguese bats are slightly larger than German bats(forearm means mdash Portugal XX 629 plusmn 19 YY607 plusmn 14 Germany XX 619 plusmn 16 YY 595 plusmn 15)Because the samples were taken in the afternoon andevening the influence of recent food consumption on the condition could be neglected Body mass was measured with a spring balance rounded to the nearest 025 grams and forearm length with a caliper rounded to the nearest 001 mm Our month-ly condition values are the average of the monthlymeans of each year Adult animals were recognizedby tooth wear the ossification of the carpal joints andthe absence of the dark spot usually present at the tipof the lower lip of the juveniles (Rodrigues et al2003) Since the spot is very faint in some indi-viduals a few may have been mistakenly classified as adults Bats were caught by hand inside the day-time roosts or with harptraps (Palmeirim and Ro-drigues 1993) during the emergence under permitsby Instituto da Conservaccedilno da Natureza e da Bio-diversidade and Regierung von Oberbayern To avoidcritical disturbances in Germany no bats were meas-ured during hibernation

116 A Zahn L Rodrigues A Rainho and J M Palmeirim

To study the diet of M myotis in Portugal we col-lected 15 faecal pellets per month in March JulyAugust September and November 1997 in the roostwhere most measurements were obtained (an aban-doned mine near Montemor-o-Novo) The pelletswere collected from a cloth placed for about 24 hourson the ground under the colony They were thensoaked in ethanol and dissected under a binocular mi-croscope Prey remnants were identified using a localinsect collection and information in the literature(Whitaker 1989 McAney 1991 Wolz 1993 Ar-lettaz 1995) We used frequency of occurrence of a prey type in pellets to measure its importance in thediet These results were compared to those obtained inthe German colonies by the same methods in 1993(Rudolph et al 2004 Zahn et al 2006)

Myotis myotis is a ground gleaning bat that usual-ly forages in sites with short ground vegetation(Arlettaz 1995 Guumlttinger 1997) Consequently todetermine seasonal variations in food resourcesaround the referred Portuguese roost we sampled theground insect fauna at sites with short ground vegeta-tion in the most abundant landcover types of the re-gion We used 63 pitfall traps (105 times 17 cm 10 cmdeep) set in equal numbers in each landcover type in areas where radio tracking revealed that M myotisforages (Rainho pers com) The traps were open for six consecutive nights in February March JuneJuly September and November 1997 Taxa of thecollected arthropods were determined to family levelWe did not measure food abundance in Germany be-cause data collected in the Bavarian study area by the

same method were available in the literature (Audet1992)

RESULTS

Seasonal Variation in Body Condition

The timing of the various phases of theannual cycle of females is quite different inthe two sites (Fig 2a) Changes betweenwinter- and summer roosts and increase offoraging activity marking the end of hi-bernation began later in Germany (MarchApril) than in Portugal (February) and thisresulted in delay in the peak of body masscorresponding to late pregnancy After giv-ing birth females in Germany remained ingood condition whereas in Portugal theircondition deteriorated and remained verypoor in the post weaning period untilAugust Only in September and October didPortuguese females gain body mass and inGermany they reached hibernation in bettercondition than their southern counterpartsOverall body mass loss during winter was more accentuated in German than inPortuguese females and the former ended

Critical times of the year for Myotis myotis 117

FIG 1 Average monthly variation of rainfall and temperature in Portugal (Instituto de Meteorologia) and Germany (Schoumlnwiese 1994) Bars and lines represent monthly rainfall and monthly mean ambient

temperature respectively

0

20

40

60

80

100

120

140

160rain Portrain Germtemp Porttemp Germ

Months

Rai

nfal

l (m

m)

Tem

pera

ture

(degC

)

30

25

20

15

10

5

0

-5Jan Feb Mar Apr May Jun Jul Aug Sep Oct Nov Dec


FIG 2 Monthly variation of body condition of adult females (a) and males (b) in Portugal and Germany In the representation of the seasonal cycle lsquoNursingrsquo includes both pregnancy and lactation Vertical lines represent

standard error

Months

winter in worse condition In Germanybody mass loss appears to continue duringthe first weeks of activity after hibernationin MarchApril In contrast Portuguese fe-males start to accumulate fat reserves assoon as they emerge from hibernation

The differences between German andPortuguese males (Fig 2b) were very simi-lar to those observed for the femalesGerman males arose from hibernation laterthan Portuguese males As in females thebody mass loss of males during hibernation

was more accentuated in Germany than inPortugal resulting in a poorer condition atthe end of hibernation Finally the condi-tion of Portuguese males during the summerwas also worse than that of German malesThe decline in condition observed at bothsites in September although more pro-nounced in Germany corresponds to themating season

In Portugal fledging occurs betweenMay and June and in Germany betweenJuly and early August After fledging body

Con

ditio

nC

ondi

tion

Jan Feb Mar Apr May Jun Jul Aug Sep Oct Nov Dec


PortugalGermany

PortugalGermany

053

048

043

038

053

048

043

038

Females

Males

condition of juveniles improved steadily until just before hibernation although inPortuguese bats (n = 340) much more slow-ly than in German juveniles (n = 886) Thebody mass of the latter increased about 31in just three months (JulyndashOctober) where-as it took five months (MayndashOctober) forthe body mass of Portuguese juveniles to increase by 22 However the longerwarm season allowed Portuguese juvenilesto continue gaining mass between Octoberand November (+20) thus reaching a sig-nificantly better body condition than theGermans before hibernation mdash 053 versus045 (P lt 001 in males and females)

Diet and Seasonal Variation in PreyAvailability

As in Germany M myotis in the mainPortuguese study colony was heavily de-pendent on ground dwelling prey especially

Carabidae and other Coleoptera (Fig 3)However its diet was more diverse and in-cluded a large proportion of Gryllidae notconsumed in Germany The seasonal varia-tion in the availability of the most con-sumed prey in Portugal indicated a fall inprey abundance during the summer (Fig 4)The data from foraging areas in the Germanstudy region demonstrated that the key foodresources are several times more abundantthere than in Portugal although they alsodeclined greatly from spring to summer(Fig 5)

DISCUSSION

We predicted that if seasonal variationsin body mass are determined by endogen-ous mechanisms alone the patterns wouldbe very similar in the two study areas Infact there were parallels that are certain-ly the result of the action of endogenous


FIG 3 Diet composition in Germany and Portugal Lines represent 95 confidence intervals

0 20 40 60 80 100

Coleoptera

Coleopt larvae

Carabidae

Scarabaeidae

Acrididae

Tettigonidae

Gryllidae

Ggryllotalpa

Diptera

Hymenoptera

Lepidoptera

Arachnida

Chilopoda

Frequency ()

PortugalGermany

Frequency ()

G gryllotalpa

mechanisms common to other bats (Beas-ley et al 1984) However we observedseveral important differences at variousstages of the annual cycle which demon-strates that environmental constraints playan important role in the definition of thebody condition of M myotis The observeddifferences can be parsimoniously ex-plained by contrasting the situation of thetwo sites at the level of food availabilityweather constraints to foraging activity andlength of the winter

Seasonal Food Resource Bottlenecks

In Germany while the availability of the main prey declines through the summer(Audet 1992) the body condition of the batsimproved (Fig 2) This suggests that foodresources are not limiting for this centralEuropean population which is to be expect-ed since even at the end of the summer foodis more abundant than any time in PortugalThe decline in body condition observed inboth Portuguese and German males inSeptember is probably due to their invest-ment in mating activities which takes placeat the same time in the two regions (Ro-drigues et al 2003)

In Portugal food resources declined sev-eral fold between the wet spring and thevery hot and dry summer (Fig 4) Such a decline was also observed in a differentyear in another region of southern Portugal(Pereira et al 2002) However a reductionof food resources does not necessarily im-ply a resource bottleneck To ascertain thisit is necessary to demonstrate that the rela-tive scarcity of food results in a worse bodycondition Three observations in this studysupport the assertion that summer food re-sources are limiting to Portuguese bats (i)In spring the condition of both males andfemales is better in Portugal than in Ger-many However when food resources getscarcer in the summer the condition of Portuguese animals of both sexes drops andbecomes substantially lower than in Ger-many (Fig 2) (ii) After weaning the con-dition of the females in Germany progres-sively improves whereas in Portugal it doesnot (Fig 2a) Finally (iii) after weaning thecondition of the juveniles in Portugal im-proves more slowly than in Germany Theliterature also suggests that during the sum-mer M myotis in Mediterranean Portugal isforced to consume large numbers of spidersdue to the scarcity of their preferred prey


FIG 4 Seasonal changes of prey availability in Portugal Vertical lines represent 95 confidence intervals for the total number of prey

Mea

n nu

mbe

r per

trap

per

nig

ht

10

08

06

04

02

00

MonthsFeb Mar Jun Jul Sep Nov

GryllidaeOther ColeopteraCarabidae

which are beetles and crickets (Pereira etal 2002) our data show that this alterna-tive diet does not allow them to maintain a good condition During periods of lowabundance of preferred prey foraging effi-ciency may drop to critical levels Bats areparticularly sensitive to such situations be-cause their high metabolic rate requiresthem to sustain a high foraging efficiency(Neuweiler 2000) It has been suggestedthat scarce food resources can also be re-sponsible for a seasonally low body condi-tion of nectarivorous bats (Ceballos et al1997) and is a key factor for the timing ofbirth (Arlettaz et al 2001)

Although it seems clear that a scarcity offood resources affects the summer conditionof Portuguese animals we do not have datato ascertain directly if it becomes lowenough to increase mortality The averagecondition of Portuguese animals at this timeis very low but still higher than the lowestobserved value (spring) in Germany How-ever the period in which animals remain inpoor condition in the Portuguese summer isparticularly long (about 45 months) To-gether with a scarcity of food resources thisduration increases the probability of the oc-currence of stochastic events that may drivesome individuals to fatal levels of body con-dition Populations of species with low

breeding rates like bats are particularlysusceptible to stochasticity (Payne and Wil-son 1999)

Constraints on Foraging Activity AffectCondition

It has been demonstrated that severeweather can constrain the foraging activitiesof temperate zone bats (Zahn and Kruumlger-Barvels 1996 Guumlttinger et al 2001) Inthis study we attempted to determine if suchconstraints can substantially affect the bodycondition of M myotis We observed that inPortugal bats start gaining body mass assoon as they end hibernation in Febru-ary (Fig 2) In contrast the condition ofGerman females (we do not have equiva-lent data for males) remains poor one monthafter ending hibernation even though foodis abundant during that period This may bedue to the greater harshness of the Ger-man spring in which cold rainy nights are common and bats are forced to foregoforaging (A Zahn personal observation)Consequently we conclude that foragingconstraints due to severe weather may contribute to poor body conditions even when food resources are abundant In factthe effects of Germanyrsquos bad weather in early spring on bats already weakened by


FIG 5 Seasonal changes of the availability of Coleoptera in the German study area where diet is dominated byColeoptera Data from Audet (1992) but the values have been halved to compensate for the fact that the traps

used in that study were twice the size of ours Vertical lines represent 95 confidence intervals

0

5

10

15

May Jun Jul AugMonths

Mea

n nu

mbe

r of C

olle

opte

rape

r tra

p pe

r nig

ht

hibernation resulted in the weakest animalsobserved in our study Bouts of bad weath-er are also responsible for unusually highmortality of both pre- and post-weaning juveniles (Zahn 1999 Rudolph et al2004)

Another constraint on foraging activitythat seems to have a substantial effect on thebody condition of males is mating Our datashow a marked decline in batsrsquo condition atthe peak of the mating season in Septem-ber both in Germany and in Portugal Dur-ing this period males reduce their foragingtime substantially to wait for females attheir mating territory (Zahn and Dippel1997) This loss of condition is less mark-ed in Portugal either because mating isspread over a longer period (Rodrigues etal 2003) or because Portuguese bats reachthe mating season in such poor conditionthat they cannot limit foraging activity asmuch

Winter Duration Can Impose SeriousConstraints

It is known that energy loss during hi-bernation may cause mortality in bats(Horaacutecek 1985) because they may exhausttheir energy reserves before the end of thewinter It is reasonable to expect that hiber-nation is a greater challenge in colder cli-mates because winters are longer but this isnot necessarily true In fact colder hiber-nacula allow bats to make a more efficientreduction of the metabolic rate (Neuweiler2000) Furthermore in some species mostof the winter energy reserves are spent inarousals from hibernation (Thomas 1995)and arousals may be more frequent inwarmer hibernacula (Ransome 1971) Thebalance of these climatically related factorswill determine the energy expenditure dur-ing hibernation

We used our data to check if longer cold-er winters are in fact more challenging for

M myotis than shorter warmer winters Ourresults demonstrated that German bats lostmore body mass during hibernation thanPortuguese bats and consequently theircondition on arousal was worse The loss ofbody mass reported for other central Euro-pean populations was similar to what weobserved in Germany (Krzanowski 1961Prucha and Hanzal 1989) The typical tem-perature of hibernacula in the German studyarea is 4degC and in Portugal about 9degC(Rodrigues et al 2003) The latter temper-ature is well above the optimal temperaturefor hibernating temperate zone bats (Webbet al 1996 Arlettaz et al 2000) so batsare likely to spend more energy per unit of time than their German counterpartsHowever we can conclude that the shorterhibernation period more than compensatesfor the disadvantages of warmer hiberna-cula

It has been suggested that long wintersmay also affect bats by limiting the timeavailable for the juveniles to prepare for hi-bernation (Ransome 1990 Thomas 1995)and this was confirmed by our comparisonFood resources are far more abundant forGerman than for Portuguese juveniles andso after weaning they accumulate fat re-serves faster However the period betweenweaning and hibernation is so much shorterin Germany that its juveniles simply do nothave time to reach a body condition compa-rable to that of their Portuguese counter-parts Their condition is also lower than thatof German adults Such low reserves for hi-bernation are likely to result in a high mor-tality during the first winter In fact we ob-served that some of the lighter German ju-veniles do not even switch to hibernationroosts and remain at nursing sites wherethey end up dying (Guumlttinger et al 2001)High juvenile winter mortality has been observed for M myotis (Horaacuteegraveek 1985) and other species of Myotis (Tuttle 1976Thomas 1995)


Conclusions and Implications forConservation

We observed periods of critically lowbody condition in both Portuguese andGerman populations of M myotis althoughthe environmental challenges that they faceare different In Portugal the most chal-lenging time of the year for this bat seems tobe the long dry summer during which thescarcity of prey keeps their body conditionat low levels for a prolonged period InGermany prey are abundant throughout thenon-hibernation season but the bats experi-ence other difficulties In spite of using thermally more suitable hibernacula thantheir Portuguese counterparts German batsemerge from the longer winter in muchpoorer condition The effect of the longwinter is then compounded by bouts of badspring weather during which bats cannotforage efficiently which makes this themost difficult period to survive for GermanM myotis Mating activity is apparently re-sponsible for periods of very low body con-dition for males in both Portugal andGermany

Agriculture and forestry have broughtabout drastic changes in landcover through-out the world While this has resulted in anoverall decline of the quality of habitats forbats many species are now dependent onthese man-made ecosystems (Russo et al2002) This is very clear in Europe whereM myotis and other bats forage mostly inagricultural or forestry areas (Guumlttinger1997 Zahn et al 2005)

We have demonstrated that some batspecies foraging in agroecosystems are sub-jected to seasonal food resource bottle-necks Any changes in agricultural or for-estry practices that accentuate bottlenecksin areas used for foraging by bats are like-ly to negatively impact their status Con-versely proper habitat management inagroecosystems can favour bats by targeting

the availability of food during recognizedbottlenecks In fact it has been proven thatdifferent agricultural and forestry practiceshave a substantial effect on the availabilityof insect prey (eg Wickramasinghe et al2003 Bus de Warnaffe and Lebrun 2004)The recently created Natura 2000 Networkprotected a large proportion of the Europeancolonies of threatened bat species includingthose of M myotis The Habitats Directiverequires that the areas in the Network aremanaged to maintain or improve the situa-tion of protected species Farming and envi-ronmental subsidies for this managementare becoming available and knowledge ofresource bottlenecks is critical to planningit This especially important in southernEurope where climatic change is supposedto cause longer and dryer summers (Miran-da et al 2002) which may increase the crit-ical period for M myotis

ACKNOWLEDGEMENTS

We are indebted to M J Pereira and H Rebeloand other colleagues who helped us during fieldworkA Rottenwallner determined prey items in the drop-pings Part of this study was funded by a grant fromDAAD Referees and Luka Clarke made useful com-ments on an earlier version of the manuscript

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ARLETTAZ R P CHRISTE A LUGON N PERRIN andP VOGEL 2001 Food availability dictates the tim-ing of parturition in insectivorous mouse-earedbats Oikos 95 105ndash111

AUDET D 1992 Roost quality foraging and youngproduction in the mouse eared bat Myotis myotisa test of the ESS model of group size selectionPhD Thesis York University York 128 pp


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BEASLEY L J K M PELZ and I ZUCKER 1984 Cir-cannual rhythms of body weight in pallid batsAmerican Physiological Society 246 955ndash958

CEBALLOS G T H FLEMING C CHAacuteVEZ and JNASSAR 1997 Population dynamics of Lepto-nycteris curasoae (Chiroptera Phyllostomidae)in Jalisco Mexico Journal of Mammalogy 781220ndash1250

DU BUS DE WARNAFFE G and P LEBRUN 2004 Ef-fects of forest management on carabid beetles inBelgium implications for biodiversity conserva-tion Biological Conservation 118 219ndash234

GUumlTTINGER R 1997 Jagdhabitate des Groszligen Maus-ohrs (Myotis myotis) in der modernen Kul-turlandschaft Buwal-Schriftenreihe Umwelt 288

GUumlTTINGER R A ZAHN F KRAPP and W SCHOBER2001 Myotis myotis mdash Groszliges Mausohr Pp123ndash207 in Handbuch der Saumlugetiere EuropaBd 4 Fledertiere Teil 1 Chiroptera 1 (F KRAPPed) Aula Verlag Wiebelsheim 602 pp

HORAacuteEgraveEK I 1985 Population ecology of Myotis myotis in central Bohemia (Mammalia Chiro-ptera) Acta Universitatis Carolinae Biologica 8161ndash267

KRZANOWSKI A 1961 Weight dynamics of bats win-tering in the cave at Pulawy (Poland) Acta The-riologica 4 249ndash263

LEWIS S E 1992 Effect of climatic variation on re-production by pallid bats (Antrozous pallidus)Canadian Journal of Zoology 71 1429ndash1433

MCANEY K 1991 The analyses of bat droppingsOccasional Publications of the Mammal SocietyLondon 14 pp

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MIRANDA P F E S COELHO A R TOMEacute M AVALENTE A CARVALHO C PIRES H O PIRES VC PIRES and C RAMALHO 2002 20th centuryPortuguese climate and climate scenarios Pp23ndash83 in Climate change in Portugal Scenariosimpacts and adaptation measures mdash SIAM project (F D SANTOS K FORBES and R MOITAeds) Gradiva Lisbon 454 pp

NEUWEILER G 2000 The biology of bats UniversityPress New York 310 pp

PALMEIRIM J M and L RODRIGUES 1993 The 2-minute harp trap for bats Bat Research News34 60ndash64

PAYNE R J H and J D WILSON 1999 Resource

limitation in seasonal environments Oikos 87303ndash314

PEREIRA M J R H REBELO A RAINHO and J MPALMEIRIM 2002 Prey selection by Myotis my-otis (Vespertilionidae) in a Mediterranean regionActa Chiropterologica 4 183ndash193

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RACEY P A 1982 Ecology of bat reproduction Pp57ndash68 in Ecology of bats (T H KUNZ ed) Ple-num Press New York 425 pp

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RANSOME R D 1990 The natural history of hiber-nating bats Christopher Helm London 235 pp

RODRIGUES L A ZAHN A RAINHO and J M PAL-MEIRIM 2003 Contrasting the roosting behaviourand phenology of an insectivorous bat (Myotismyotis) in its southern and northern distributionranges Mammalia 67 321ndash335

RUDOLPH B U A ZAHN and A LIEGL 2004 Gro-szliges Mausohr (Myotis myotis) Pp 203ndash231 inFledermaumluse in Bayern (Bayerisches Landes-amt fuumlr Umweltschutz ed) Verlag Eugen UlmerStuttgart 411 pp

RUSSO D G JONES and A MIGLIOZZ 2002 Habitatselection by the Mediterranean horseshoe batRhinolophus euryale (Chiroptera Rhinolophidae)in a rural area of southern Italy and implicationsfor conservation Biological Conservation 10771ndash81

SCHOumlNWIESE C D 1994 Klimatologie EugenUlmer Stuttgart 436 pp

THOMAS D W 1995 Physiological ecology of hiber-nation in vespertilionid bats Pp 233ndash244 inEcology evolution and behaviour of bats (P ARACEY and S M SWIFT eds) Symposia of theZoological Society of London 67 1ndash421

TUTTLE M D 1976 Population ecology of the graybat (Myotis grisescens) factors influencinggrowth and survival of newly volant youngEcology 57 587ndash595

WEBB P I J R SPEAKMAN and P A RACEY 1996How hot is a hibernaculum A review of the temperatures at which bats hibernate CanadianJournal of Zoology 74 761ndash765



WHITAKER J O 1989 Food habits analyses of insec-tivorous bats Pp 171ndash189 in Ecological and be-havioural methods for the study of bats (T HKUNZ ed) Smithsonian Institution Press Wash-ington DC 533 pp

WICKRAMASINGHE L P S HARRIS G JONES and NVAUGHAN 2003 Bat activity and species richnesson organic and conventional farms impact ofagricultural intensification Journal of AppliedEcology 40 984ndash993

WOLZ I 1993 Untersuchungen zur Nachweisbarkeitvon Beutetierfragmenten im Kot von Myotisbechsteini (Kuhl 1818) Myotis 31 5ndash25

ZAHN A 1999 Reproductive success colony sizeand roost temperature in attic-dwelling bat My-otis myotis Journal of Zoology (London) 247275ndash280

ZAHN A and B DIPPEL 1997 Male roosting habitsmating system and mating behaviour of My-otis myotis Journal of Zoology (London) 243659ndash674

ZAHN A and K KRUumlGER-BARVELS 1996 Waumllder alsJagdhabitate von Fledermaumlusen Zeitschrift fuumlrOumlkologie und Naturschutz 5 77ndash85

ZAHN A H HASELBACH and R GUumlTTINGER 2005Foraging activity of central European Myotis my-otis in a landscape dominated by spruce monocul-tures Mammalian Biology 70 265ndash270

ZAHN A A ROTTENWALLNER and R GUumlTTINGER2006 Population density of the greater mouse-eared bat (Myotis myotis) local diet compositionand availability of foraging habitats Journal ofZoology (London) 269 486ndash493

Received 18 December 2006 accepted 25 March 2007

INTRODUCTION

The dynamics of a population may notbe just a function of the average environ-mental conditions but of those occurring atlsquocriticalrsquo times of the year when due to spe-cific constraints the animal cannot fulfil itsenergy requirements (Racey 1982 Barclay1991) The identification of such bottle-necks and of their determinants is importantnot only to understand abundance and dis-tribution of species but also to direct con-servation action in order to halt and reverse

population declines (Payne and Wilson1999 Primack 2002) This is particularlyrelevant in bats because the populations ofmany species have been declining and sev-eral of these are now threatened (Mickle-burgh et al 2002)

Temperate zone bats have a well-definedannual cycle largely determined by cli-mate Climate may influence their energybalance in multiple ways It may imposeconstraints on energy intake by influencingthe availability of food and limiting the for-aging activity In fact climate is known to

Acta Chiropterologica 9(1) 115ndash125 2007PL ISSN 1508-1109 copy Museum and Institute of Zoology PAS

Critical times of the year for Myotis myotis a temperate zone bat roles of climate and food resources

ANDREAS ZAHN1 LUIacuteSA RODRIGUES2 ANA RAINHO2 and JORGE M PALMEIRIM3

1Ludwig-Maximilians-Universaumlt Muumlnchen Groszlighaderner Str 2 D-82152 Planegg - Martinsried GermanyE-mail AndreasZahniivde

2Instituto da Conservaccedilno da Natureza e da Biodiversidade Rua de Santa Marta 55 1150-294 Lisboa Portugal 3Departamento de Biologia Animal and Centro de Biologia Ambiental Faculdade de CiLncias

Universidade de Lisboa 1749-016 Lisboa Portugal

In highly seasonal temperate zones climate may cause fluctuations in the accessibility of prey for insectivorousbats The main objective of this project was to evaluate if these fluctuations can result in resource bottlenecksthat affect the body condition of a temperate zone bat mdash Myotis myotis Seasonal changes in body conditionfollowed different patterns in Portugal and Germany which have different climates In Germany bats usethermally better hibernacula which allow them to minimize energy expenditure but because of the longerwinters they emerge from hibernation in poorer condition Except during the hibernation period food wasalways abundant in Germany but the condition of the animals was poor when bad weather constrained foragingparticularly in early spring In Portugal food was limiting during the long dry summer and this affected thecondition of the animals for several months The conclusion that food resources can act as a limiting factor isrelevant for conservation because like other bat species M myotis forages mostly in agricultural and forestryhabitats and can be affected by practices that accentuate resource bottlenecks Where necessary themanagement of agroecosystems near colonies of M myotis and of other threatened bats should aim atminimizing seasonal food bottlenecks

Key words Myotis myotis diet prey availability resource bottlenecks body condition Portugal Germany












RESULTS






0

20

40

60

80

100

120

140


Months

Rai

nfal

l (m

m)

Tem

pera

ture

(degC

)

30

25

20

15

10

5

0




standard error

Months





Con

ditio

nC

ondi

tion



PortugalGermany

PortugalGermany

053

048

043

038

053

048

043

038

Females

Males





DISCUSSION




0 20 40 60 80 100

Coleoptera

Coleopt larvae

Carabidae

Scarabaeidae

Acrididae

Tettigonidae

Gryllidae

Ggryllotalpa

Diptera

Hymenoptera

Lepidoptera

Arachnida

Chilopoda

Frequency ()

PortugalGermany

Frequency ()

G gryllotalpa







Mea

n nu

mbe

r per

trap

per

nig

ht

10

08

06

04

02

00











0

5

10

15


Mea

n nu

mbe

r of C

olle

opte

rape

r tra

p pe

r nig

ht














ACKNOWLEDGEMENTS


LITERATURE CITED

























































RESULTS






0

20

40

60

80

100

120

140


Months

Rai

nfal

l (m

m)

Tem

pera

ture

(degC

)

30

25

20

15

10

5

0




standard error

Months





Con

ditio

nC

ondi

tion



PortugalGermany

PortugalGermany

053

048

043

038

053

048

043

038

Females

Males





DISCUSSION




0 20 40 60 80 100

Coleoptera

Coleopt larvae

Carabidae

Scarabaeidae

Acrididae

Tettigonidae

Gryllidae

Ggryllotalpa

Diptera

Hymenoptera

Lepidoptera

Arachnida

Chilopoda

Frequency ()

PortugalGermany

Frequency ()

G gryllotalpa







Mea

n nu

mbe

r per

trap

per

nig

ht

10

08

06

04

02

00











0

5

10

15


Mea

n nu

mbe

r of C

olle

opte

rape

r tra

p pe

r nig

ht














ACKNOWLEDGEMENTS


LITERATURE CITED
















































standard error

Months





Con

ditio

nC

ondi

tion



PortugalGermany

PortugalGermany

053

048

043

038

053

048

043

038

Females

Males





DISCUSSION




0 20 40 60 80 100

Coleoptera

Coleopt larvae

Carabidae

Scarabaeidae

Acrididae

Tettigonidae

Gryllidae

Ggryllotalpa

Diptera

Hymenoptera

Lepidoptera

Arachnida

Chilopoda

Frequency ()

PortugalGermany

Frequency ()

G gryllotalpa







Mea

n nu

mbe

r per

trap

per

nig

ht

10

08

06

04

02

00











0

5

10

15


Mea

n nu

mbe

r of C

olle

opte

rape

r tra

p pe

r nig

ht














ACKNOWLEDGEMENTS


LITERATURE CITED


















































DISCUSSION




0 20 40 60 80 100

Coleoptera

Coleopt larvae

Carabidae

Scarabaeidae

Acrididae

Tettigonidae

Gryllidae

Ggryllotalpa

Diptera

Hymenoptera

Lepidoptera

Arachnida

Chilopoda

Frequency ()

PortugalGermany

Frequency ()

G gryllotalpa







Mea

n nu

mbe

r per

trap

per

nig

ht

10

08

06

04

02

00











0

5

10

15


Mea

n nu

mbe

r of C

olle

opte

rape

r tra

p pe

r nig

ht














ACKNOWLEDGEMENTS


LITERATURE CITED




















































Mea

n nu

mbe

r per

trap

per

nig

ht

10

08

06

04

02

00











0

5

10

15


Mea

n nu

mbe

r of C

olle

opte

rape

r tra

p pe

r nig

ht














ACKNOWLEDGEMENTS


LITERATURE CITED






















































0

5

10

15


Mea

n nu

mbe

r of C

olle

opte

rape

r tra

p pe

r nig

ht














ACKNOWLEDGEMENTS


LITERATURE CITED



























































ACKNOWLEDGEMENTS


LITERATURE CITED














































critical times of the year for myotis myotis, a temperate zone bat: roles of climate and food...

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