Lifetime reproductive success, weather and fitness in dragonflies

6 Pages·1997·0.51 MB·English

by  Thompson, D J

Odonatologica26(1): 89-94 March I. 1997
Lifetimereproductivesuccess,
weatherand fitness in dragonflies*
D.J.Thompson
PopulationBiologyResearch Group,SchoolofBiologicalSciences,
University ofLiverpool,P.O. Box 147,Liverpool,L69 3BX, United Kingdom
Received June 18, 1996/Reviewed andAcceptedAugust 14, 1996
There aremorestudiesofmatingorreproductivesuccessofdragonfliesthanofany
other insects; their size andabilitytobe marked and watched renders them particu-
larlysuitable forsuch studies. - Laboratorystudies onfeedingand developmentrates
oflarvae indicate thatwell-fed larvaemoultintolargeranimalsanddososoonerthan
poorlyfed individuals. - This trend is reflected in adecline in size at emergence
throughthe seasonandin those adultsarriving ataparticularrendezvous tobreed.-
For many earlyemergingspecies the best weatherforreproductiveactivity isat the
end oftheirflyingperiod,atimelikely tobe encounteredby smaller adults. Weather
isknown tohave amajorinfluenceonlifetimereproductive successofdragonflies.-
Itseemsthatthe “best” larvae, those that emerge first,sufferreduced reproductive
activity because later emergers experience better weather and consequently obtain
more matings.- The present paperexplores this apparent paradox and attemptsto
resolve it.
INTRODUCTION
Therehavebeenmorestudiesoflifetimematingorreproductive success in drag-
onflies than any other insect order (e.g. FINCKE, 1982, 1986; BANKS &
THOMPSON, 1985, 1987; HAFERNIK & GARRISON, 1986; KOENIG &
ALBANO, 1987;McVEY, 1988).Studies oflifetimemating success are usually
accomplished by marking as many individualsofa population as possible, and
noting through thewholebreeding season, whichanimalsmate together. Because
they arerelatively big, easy tomark and watch atdiscrete breeding sites, and in
temperateregions atleasttheyarerelatively short-lived, dragonfliesanddamselflies
are particularly suitablesubjects for thestudy oflifetimemating success.
* Paperpresentedatthe 12th International Symposium ofOdonatology,Osaka, Japan;August 1-11,
1993
90 D.J. Thompson
Estimatesoflifetimematingorreproductive success are importantfromthepoint
ofviewofanevolutionary biologistbecausethey enablesomething rathercloseto
fitness (the “Holy Grail” ofevolutionary biology) to beestimated.This is not the
casewiththemoreusual short-termmeasures ofmating success (e.g.THOMPSON
&BANKS, 1989).InCoenagrion puella,BANKS &THOMPSON(1985a) showed
thatsmallmalesachievedahigher dailymatingratethanlarge males,butthatlarge
males live longer than small males, and living longer compensates for reduced
daily matingrates.Anyone simply studying short-termmating success inthisspe-
cies wouldhaveconcluded,wrongly, that smallmalesdidbetterthanlargemales.
FINCKE (1982)andTHOMPSON (1989)haveintimatedthat theremay bestabi-
lizing selection on male size and FINCKE (1988) showed that to be true for
Enallagma hageni.
Dragonfly biologists have beenparticularly successful inobtaining estimatesof
lifetimemating or reproductive success. Theseestimates haveexposed deficien-
cies in short-term measures ofreproductive success andhave been obtainedina
few weeks, whereas comparable datafor birds andmammals may take years to
gather. Thus dragonflies are apparently ideal animalsin which tostudy lifetime
reproductive success.
However,thereare problems forentomologists, ingeneral, andodonatologists,
inparticular, inestimating anything betweenreproductive success andfitness.The
mainoneisthatitis not possible totrackthefatesoftheoffspring. Thisiscertainly
thecase forinsects with aquatic larval stagesand alarge numberofinstars, like
dragonflies. The aim ofthispaperis toexplore some oftheconsequencesofthis
problem, andin particular aparadox thatexists forsomenorthernEuropean spe-
cies.
LARVALFEEDING,DEVELOPMENTAND EMERGENCE
Laboratory studieson feeding and development rates ofdamselfly larvaeindi-
catethatthereareanumberofresponses to variationsinpreyconsumedduringan
instar(LAWTON, etal„ 1981;PICKUP& THOMPSON, 1984, 1990).The most
obvious is that well-fed larvaecomplete any given instarfaster than poorly-fed
larvae.Inaddition,well-fedlarvaeshowagreaterpercentageincreaseinheadwidth
atthemoultthan poorly-fed larvae.
So we might thinkof“good” larvaedeveloping quicker and moulting intopro-
gressively relatively bigger larvae than “poor” larvae. Poorlarvaeare poorfora
numberofreasons, butoneis likely tobethatthey arenot abletoestablishthem-
selves inareas ofhigh prey density.
Thistrend is continuedas far as emergenceand beyond. A numberofstudies
havedemonstratedthatlargeranimalsemergesoonerthan small animalsand that
consequently larger adults arrive at thebreeding site before smalleradults (e.g.
BANKS& THOMPSON, 1985b;GRIBBIN& THOMPSON, 1991a, 1991b).
Lifetimereproductive successin dragonflies 91
WEATHER
TableIshows the28-yearmeantemperature(1953-1980)fromBidstonObserva-
tory, Wirral, northernEngland. Although the weather in England is notoriously
unpredictable, on average there are higher temperatures
andmore sunny days in July than June.This means that
Table 1
theadultsthatemergefrom“good” larvaeexperience worse 28-yearmeantemperatures
weatherconditionsthanthose from“poor” larvae. from BidstonObservatory,
Weatherisknownto influencelifetimemating success Wirral, northern England
in damselflies in at least 2 ways. THOMPSON (1990) (1953-1980)
showedthateach 1°Crise intemperaturewithintherange
June 17.35°C
experienced addedabout 12eggsto a clutch ofeggsof July 18.35-C
Coenagrion puella. Aclutchproduced atanaveragetem- August 18.25°C
perature of 10°C contains 71% ofthe eggs produced at September 16.36°C
15°C (around 200 eggs). As well as temperature,the
numberofsunny days experienced inadult lifeplays a majorpart in determining
eggproduction, becausereproductive activity only takesplace onsunny days.
THOMPSON(1990)simulatedtheeffectsofweatheronlifetimeeggproduction
using fieldestimatedparameters for C. puella. Using thebest fieldestimatesof
daily survival fa- Coenagrion of0.85, it was possible to look at the effects of
differentweatherconditions,specificallyproportion ofsunny days,on lifetimeegg
production.Theresults werethatingood monthslifetimeeggproduction wasaround
750eggsbutinbadmonthsitwas under350.Thebadmonthsare morelikely tobe
Junesthan Julys.Thusthe “poor” larvae,those that did not feedwell and devel-
oped slowly andemergedlater, produced onaveragerathermoreoffspring thanthe
better fed,faster developers.
THEPARADOX
So the question we might ask then is,“Does it pay to be a poor larva, ifthis
meansemerging laterintheseasonandexperiencing weatherconditionsmoresuit-
ableforreproductive activity?”
One oftheproblems withworking with insects forthose whowould study life-
timereproductive success is thatitis not possible tomark the larvaeand follow
themthroughthelifecycle. But, wecan guessatthefatesofthelarvaeofearly and
lateemerging adultsfromtheresults oflaboratory experiments.
LARVALCOMPETITION
GRIBBIN & THOMPSON (1990) compared the development rates and head
widthincreases at themoultof two larval instarsofIschnuraelegans, (F-l) and
(F-3),thetwo instars thatearly andlatelarvaemightbeexpected to reach by au-
92 DJ. Thompson
tumn whengrowth stops.Larvae were maintainedwithasuperabundance offood
andeitherlarvaefrom thesameorthelarger/smaller instar.Theexperiments were
performed insmallcontainerswitheitheroneor fourperches, thatiseither“low”
or “high” perch availability. The mean development times, and percentage head
width increases atthe moult, of small larvaein4treatments: (1) isolation, (2) in
combinationwith othersmalllarvae, (3) withsmall andlarge larvae,and(4) with
largelarvae,were measured.Smalllarvaesufferedincreaseddevelopment timesin
the presenceoflarge larvae, but not when inthe presenceofother small larvae.
Development timesoflarge larvaewere not affectedby thepresenceofsmalllar-
vae. There was a significant reduction in percentage head width increase when
small larvaewere maintainedwith three large larvae. Theseinterferenceeffects
werebothreduced when therewere more perches available so the mechanismof
competition is likely tobethatlarge larvaeforcesmallerlarvaeintoinferiorfishing
sites.
Theseexperiments describeasymmetric intraspecific competition whenthereis
an abundanceoffoodavailable.They reflect what we might think ofas one end,
themore subtleend,ofthespectrum ofintraspecific effects. Theotherendofthe
spectrum,andthemost extremeintraspecificeffect, iscannibalism,whichhasbeen
reported in odonate populations in the fieldfrom analysis offaecal pellets. Al-
though not as terminalas cannibalism, asecond phenomenon that canbefalllate
larvaeis thatthey missthewindow ofemergencealtogether and haveto spend a
secondwinteras larvae.Thesurvivalprospectsofthelaterpartofasplit cohortare
unlikely to be high.
CONCLUSION
It is likely that theincreased lifetimemating success ofadults oflateemerging
larvaeis morethancounterbalancedby a combinationfourthings:
(1) cannibalism- someoffspring are likely to becannibalised,
(2) small larvae being forced frompreferred (safe) fishing sites, and following
fromthat,
(3) thegeneral high probability ofbeingeaten bysomething, beitotherodonates
orfish, is higher themoretimeis spentinlarvallife.
(4) Onemore directwayin whichlateadultsmaysufferagainst early adultsis in
choiceofoviposition substrate. Atthe end ofthe season many oviposition
substratesaresimply saturatedwitheggssothatlateadultsareforcedtolay in
sub-optimal locations (A. Martenspers.comm.;FINCKE, 1985, 1988). Itis
not clearhow widespread thisphenomenon is.
The resolutionof the paradox is that success as a larva is more important in
fitness terms than increased lifetimemating success as an adult. It may be that
dragonflybehaviouralecologists willhaveto graspthenettleandlearnsomeDNA
fingerprinting techniques tofindwhoselarvaedevelop rapidly toemergenceinthe
Lifetime reproductive successin dragonflies 93
field.It is likely that RAPD fingerprinting results willsoon be available for the
tree-holebreeding species Megaloprepus coerulatus, in which FINCKE (1992)
has already demonstratedthat many ‘successful’ males, in terms of mating suc-
cess, getzero fitness, intermsofoffspring produced, fromthe tree holes they de-
fend(O.M.Fincke, pers. comm.).
ACKNOWLEDGEMENTS
DAVID ATKINSONcontributed the weather data and DEBORAH POPE& IAN HARVEY and
threereferees made helpfulsuggestionswhich improved the manuscript.
REFERENCES
BANKS, M.J.& D.J. THOMPSON, 1985a. Lifetime matingsuccessinthe damselfly Coenagrion
puella.Anim. Behav. 33: 1175-1183.
BANKS, M.J. & D.J. THOMPSON, 1985b. Emergence,longevity and breeding area fidelityin
Coenagrionpuella(L.)(Zygoptera: Coenagrionidae).Odonatologica14:279-285.
BANKS,M.J.& D.J.THOMPSON, 1987, Lifetime reproductivesuccessin females ofthe damselfly
Coenagrionpuella(L,).J.Anim.Ecol. 56: 815-822.
FINCKE, O.M., 1982, Lifetimemating successina natural populationofthe damselflyEnallagma
hageni(Walsh)(Odonata: Coenagrionidae).Behav. Ecol. Sociobiol. 10:293-302.
F1NCKE, O.M., 1985. Alternative mate-finding tactics in a non-territorial damselfly(Odonata:
Coenagrionidae).Anim.Behav. 33: 1124-1137.
FINCKE, O.M., 1986.Lifetimereproductivesuccessandtheopportunityforselection inashort-lived
damselfly(Odonata: Coenagrionidae).Evolution 40: 791-803.
FINCKE,O.M.,1988. Sourcesofvariationinlifetimereproductivesuccessinanon-territorialdamselfly
(Odonata: Coenagrionidae).In:T.H. Clutton-Brock, [Ed], Reproductivesuccess, pp. 24-43,
Univ. ChicagoPress.
FINCKE, O.M., 1992. Consequencesoflarval ecologyforterritorialityandreproductivesuccessina
neotropical damselfly.Ecology73: 449-462.
GR1BB1N, S.D. & D.J. THOMPSON, 1990. Asymmetricintraspecificcompetitionamong larvae of
the damselflyIschnura elegans(Zygoptera:Coenagrionidae).Ecol. Em. 15:37-42.
GRIBBIN, S.D. & D.J, THOMPSON, 1991a. Emergence ofthe damselfly Pyrrhosomanymphula
(Sulzer)fromadjacentpondsinnorthern England(Zygoptera:Coenagrionidae).Hydrobiologia
209: 123-131.
GRIBBIN, S.D.& D.J.THOMPSON, 1991b. Theeffects ofsizeandresidence onterritorial disputes
and short-term mating success in the damselfly Pyrrhosoma nymphula (Zygoptera:
Coenagrionidae).Anim. Behav. 41;689-695.
HAFERN1K, J.R,& R.W. GARRISON, 1986. Matingsuccess and survival ratein apopulationof
damselflies: results at variancewith theory?Am. Nat. 128: 353-365.
KOENIG,W.D.& S.S.ALBANO, 1987. Lifetime reproductivesuccessandtheopportunityforselec-
tion inthe white-tailed skimmer Plathemis lydia(Odonata:Libellulidae).Evolution 41: 22-
-36.
LAWTON, J.H., B.A.THOMPSON& D.J.THOMPSON, 1980. Theeffectsofprey density onsur-
vival and growthofdamselflylarvae. Ecol. Enl. 5: 39-51.
McVEY, M.E., 1988. The opportunity for sexual selection in a territorial dragonfly,Erythemis
simplicicollis.In:T.H.Clutton-Brock,[Ed.],Reproductivesuccess, pp. 44-58, Univ. Chicago
Press.
94 D.J. Thompson
PICKUP,J.& D.J. THOMPSON,1984. Theeffectsofprey densityandtemperature ondevelopment
oflarvae ofthe damselflyLestes sponsa (Hans.) (Zygoptera:Lestidae). Adv. Odonatol. 2:
169-176.
PICKUP, J.&D.J. THOMPSON, 1990. The effectsoftemperature and prey densityonthe develop-
mentrates and growthofdamselflylarvae (Odonata;Zygoptera).Ecol.Ent. 15: 187-200,
THOMPSON,D.J, 1989. Sexual sizedimorphisminCoenagrionpuella(L.)(Zygoptera:Coenagrioni-
dae).Adv. Odonatol. 4: 123-131.
THOMPSON, D.J., 1990. Theeffectsofsurvival and weather onlifetimeeggproductioninamodel
damselfly.Ecol. Ent. 15:455-462.
THOMPSON,D.J.& M.J.BANKS. 1989. Short-term matingsuccessin maleCoenagrionpuella(L.)
(Zygoptera:Coenagrionidae),Odonatologica 18: 65-73.